Integrated Pest Management: (Cabi Publishing) - PDF Free Download (2024)

00Integrated pest prelim.QXD 14/4/04 2:23 pm Page i

Integrated Pest Management

Potential, Constraints and Challenges

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page ii

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page iii

Integrated Pest Management Potential, Constraints and Challenges

Edited by

Opender Koul Insect Biopesticide Research Centre Jalandhar, India

G.S. Dhaliwal Department of Entomology Punjab Agricultural University Ludhiana, India and

G.W. Cuperus Department of Entomology and Plant Pathology Oklahoma State University, Stillwater, Oklahoma, USA

CABI Publishing

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page iv

CABI Publishing is a division of CAB International CABI Publishing CAB International Wallingford Oxfordshire OX10 8DE UK Tel: +44 (0)1491 832111 Fax: +44 (0)1491 833508 E-mail: [emailprotected] Website:

CABI Publishing 875 Massachusetts Avenue 7th Floor Cambridge, MA 02139 USA Tel: +1 617 395 4056 Fax: +1 617 354 6875 E-mail: [emailprotected]

© CAB International 2004. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners.

A catalogue record for this book is available from the British Library, London, UK.

Library of Congress Cataloging-in-Publication Data Integrated pest management: potential, constraints, and challenges/ edited by Opender Koul, G.S. Dhaliwal, G.W. Cuperus. p. cm. Includes bibliograpical references and index. ISBN 0-85199-686-8 (alk. paper) 1. Pests--Integrated control. I. Koul, Opender. II. Dhaliwal, G.S. III Cuperus, Gerrit W. IV. Title. SB950.I4577 2004 632’.9--dc22


ISBN 0 85199 686 8

Typeset by Columns Design Ltd, Reading Printed and bound in the UK by Biddles, King’s Lynn

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page v


About the Editors






1. Integrated Pest Management: Retrospect and Prospect G.S. Dhaliwal, Opender Koul and Ramesh Arora


2. Cultural Practices: Springboard to IPM Waheed I. Bajwa and Marcos Kogan


3. The Relevance of Modelling in Successful Implementation of IPM David E. Legg


4. Manipulation of Tritrophic Interactions for IPM Robert H.J. Verkerk


5. Behaviour-modifying Chemicals: Prospects and Constraints in IPM Larry J. Gut , Lukasz L. Stelinski, Donald R. Thomson and James R. Miller


6. Transgenic Insecticidal Cultivars in IPM: Challenges and Opportunities Julio S. Bernal, Jarrad Prasifka, M. Sétamou and K.M. Heinz


7. Plant Resistance Against Pests: Issues and Strategies C. Michael Smith


8. The Pesticide Paradox in IPM: Risk–Benefit Analysis Paul Guillebeau


9. Manipulation of Host Finding and Acceptance Behaviours in Insects: Importance to IPM Richard S. Cowles


10. IPM in Forestry: Potential and Challenges Imre S. Otvos



00Integrated pest prelim.QXD 14/4/04 2:24 pm Page vi



11. Consumer Response to IPM: Potential and Challenges Craig S. Hollingsworth and William M. Coli


12. The Essential Role of IPM in Promoting Sustainability of Agricultural Production Systems for Future Generations G.W. Cuperus, R.C. Berberet and R.T. Noyes


13. Opportunities and Challenges for IPM in Developing Countries David Bergvinson




00Integrated pest prelim.QXD 14/4/04 2:24 pm Page vii

About the Editors

Opender Koul, Fellow of the National Academy of Agricultural Sciences and the Indian Academy of Entomology, is an insect toxicologist/physiologist/chemical ecologist and currently the Director of the Insect Biopesticide Research Centre, Jalandhar, India. After obtaining his PhD in 1975 he joined the Regional Research Laboratory (CSIR), Jammu and then became Senior Group Leader of Entomology at Malti-Chem Research Centre, Vadodara, India (1980–1988). He has been a visiting scientist at the University of Kanazawa, Japan (1985–1986), the University of British Columbia, Canada (1988–1992), and the Institute of Plant Protection, Poznan, Poland (2001). His extensive research experience concerns insect–plant interactions, spanning toxicological, physiological and agricultural aspects. Honoured with an Indian National Science Academy (INSA) medal and the Kothari Scientific Research Institute award, he has authored over 140 research papers and articles and is the author/editor of the books Insecticides of Natural Origin, Phytochemical Biopesticides, Microbial Biopesticides and Predators and Parasitoids. He has also been an informal consultant to the Board of Science and Technology for International Development (BOSTID), the National Research Council (NRC) of the USA and at the International Centre for Insect Physiology and Ecology (ICIPE), Nairobi. G.S. Dhaliwal, a Fellow of the National Environmental Science Academy (NESA), Society of Plant Protection Sciences and Society of Pesticide Sciences, India, is Professor of Ecology in the Department of Entomology at the Punjab Agricultural University, Ludhiana, India. Having completed his PhD in Entomology at the Indian Agricultural Research Institute (IARI), New Delhi, in 1972, he was awarded the Gurprasad Pradhan Gold Medal and became a postdoctoral fellow at the International Rice Research Institute, Manila, for 2 years. He has authored/edited more than 30 books on different aspects of pest management and the environment. Honoured with the Best Scientist Award of NESA, he is the founding President of the Indian Society for the Advancement of Insect Science and the Society of Biopesticide Sciences, India, and President of the Indian Ecological Society as well as Vice-President of the Indian Society of Allelopathy and the Society of Pesticide Science, India. He is a member of the World Food Prize Nominating Academy, The World Food Prize Foundation, Des Moines, Iowa. Gerrit W. Cuperus, was a Regent’s Professor and Integrated Pest Management Coordinator at Oklahoma State University for over 20 years. Dr Cuperus obtained his PhD in 1982, joined vii

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page viii


About the Editors

the Department of Entomology at Oklahoma State University and has since been involved in national IPM programmes of the USA aiming at an interdisciplinary focus to solve management issues. Dr Cuperus has chaired and served in different capacities in various national committees on food safety and pest management. He has made specific contributions in extension/research and has won distinguished service awards from the US Department of Agriculture (USDA). His research efforts, focused on stored-product pest management, have helped to build the Stored Product Research and Education Center (SPREC) at Oklahoma State University. He has authored over 60 research papers and articles and is an editor of Successful Implementation of IPM for Agriculture Crops (1992) and Stored Product Management (1995).

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page ix


Ramesh Arora, Department of Entomology, Punjab Agricultural University, Ludhiana 141 004, India Waheed I. Bajwa, Department of Entomology and Integrated Plant Protection Center, Oregon State University, Corvallis, OR 97331, USA R.C. Berberet, Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA David Bergvinson, International Maize and Wheat Improvement Center (CIMMYT), El Batán, Mexico CP 56130, Mexico Julio S. Bernal, Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843–2475, USA William M. Coli, Department of Entomology, University of Massachusetts, Amherst, MA 01003, USA Richard S. Cowles, Connecticut Agricultural Experiment Station, Valley Laboratory, PO Box 248, Windsor, CT 06095, USA G.W. Cuperus, Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078, USA G.S. Dhaliwal, Department of Entomology, Punjab Agricultural University, Ludhiana 141 004, India Paul Guillebeau, Department of Entomology, University of Georgia Cooperative Extension Service, Athens, GA 30602, USA Larry J. Gut, Department of Entomology, Michigan State University, East Lansing, MI 48824, USA K.M. Heinz, Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843–2475, USA Craig S. Hollingsworth, Department of Entomology, University of Massachusetts, Amherst, MA 01003, USA Marcos Kogan, Department of Entomology and Integrated Plant Protection Center, Oregon State University, Corvallis, OR 97331, USA Opender Koul, Insect Biopesticide Research Centre, 30 Parkash Nagar, Jalandhar 144 003, India David E. Legg, Department of Renewable Resources, University of Wyoming, Laramie, WY 82071, USA James R. Miller, Department of Entomology, Michigan State University, East Lansing, MI 48824, USA ix

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page x



R.T. Noyes, Department of Biosystems and Agricultural Engineering, Oklahoma State University, Stillwater, OK 74078, USA Imre S. Otvos, Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, 506 West Burnside Road, Victoria, BC, V8Z 1M5, Canada Jarrad Prasifka, Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843–2475, USA M. Sétamou, Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843–2475, USA C. Michael Smith, Department of Entomology, Kansas State University, Manhattan, KS 66506–4004, USA Lukasz L. Stelinski, Department of Entomology, Michigan State University, East Lansing, MI 48824, USA Donald R. Thomson, DJS Consulting Services, LLC, 3015 SW 109 Street, Seattle, WA 98146, USA Robert H.J. Verkerk, Department of Biological Sciences, Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY, UK

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page xi


The concept of integrated pest management (IPM) excelled during the mid-1970s when environmental, health and production problems associated with dependence on large-scale use of synthetic organic pesticides came into the limelight. Following some large-scale successes with IPM based on biological control systems, improved profitability and pesticide reduction IPM has moved from a peripheral to the central stage of pest suppression. Today it is considered to be the springboard to sustainable crop management. Over the years more than 70 definitions of IPM (including related terms) have been proposed. Although some new terms such as ‘biointensive IPM’ and ‘ecologically based pest management’ have been suggested, the essence of all the definitions is the promotion of compatibility of management tactics to ensure economic and ecological sustainability. There have been many success stories, particularly in the developed world, and many bottlenecks, more so in developing countries. The availability of modern tools and transgenic crop-protection technology has opened new opportunities and challenges. All these issues form the focus of the book, where they have been discussed by world authorities in their respective areas of specialization. With the growing interest in IPM, opportunities and challenges have come to the fore and it is necessary to understand the potential in such programmes. To begin with, the book outlines the historical perspective of IPM in the first chapter and sets the stage for the discussion on potential, constraints and challenges involved in IPM. It covers the era of traditional approaches, from ancient times to 1938, the era of pesticides, from 1939 to 1975 and the current era of IPM, from 1976 onward. The significance of the ‘farmer first’ concept in IPM development and implementation is stressed. The potential of different management tactics in future IPM programmes has been discussed in various chapters, such as cultural practices, the relevance of modelling in the successful implementation of IPM, the manipulation of tritrophic interactions for the systems and the role of behaviour-modifying chemicals. There are several challenges and opportunities for transgenic insecticidal cultivars, which have been discussed in Chapter 6, and the role of Bacillus thuringiensis (Bt) insect-resistant transgenes, molecular markers, cloning and sequencing plant resistance genes in host-plant resistance to pests has been highlighted in Chapter 7. The risk–benefit analysis of different groups of pesticides (i.e. insecticides, fungicides and weedicides) with respect to biological controls is an important component of IPM implementation. An effort has been made to make pesticides more compatible with IPM by improving pesticide selectivity via manipulating various spray parameters such as placement, timing and formulations, or through official policies and regulations and these are comprehensively discussed. xi

00Integrated pest prelim.QXD 14/4/04 2:24 pm Page xii



Chapter 9 focuses on the manipulation of host finding and acceptance behaviours to shift highly mobile and discriminating insect populations to plants or traps outside the valued crops. Potential tools for implementing the ‘push–pull strategy’ have been explained and several models have been proposed to demonstrate the application of behavioural manipulation in trap crops. The consumer response to IPM has been discussed in Chapter 11 and the various constraints and bottlenecks have been highlighted. The forest ecosystem is much more complex, resilient and longer term than that of agriculture, and the threshold level of damage caused by insects or pathogens is much higher in forestry than what most consumers are willing to accept on or in their fruits or vegetables. Therefore, IPM has an important role to play in silviculture pest management and this has been discussed comprehensively in Chapter 10. The role of IPM in sustaining productivity in future has been discussed in Chapter 12. The contribution of IPM in meeting economic, environmental and social mandates has been elaborated. The role of diagnostic tools, weather forecasting, transgenic plants, biological control and chemical pesticides in future IPM programmes has been highlighted and the strategies to meet the challenges of pest adaptation have been outlined. The need for improved information transfer among all groups involved in the development, implementation and application of IPM has been stressed. Finally, it is essential to know the status of IPM in developed versus developing countries. Therefore, the potentials and the constraints between the two worlds have been compared extensively in the last chapter of this book. We received a tremendous response and support from all the authors for preparing their chapters in tune with the theme of the book, for which we express our gratitude to them. We are also thankful to Tim Hardwick at CABI Publishing for his cooperation and help at various stages in the preparation of this volume. Through this IPM book we also want to pay homage to Prof. Bill Brown, who could not complete his chapter for this volume due to his untimely demise in January 2003. Prof. Brown, worked in Nigeria, Thailand, South Korea and Bolivia after becoming a Professor of Plant Pathology and Cooperative Extension IPM Coordinator at Colorado State University. He had a passion for teaching plant pathology and the philosophy of IPM. We hope the book will prove useful to all those interested in promoting the cause of IPM in formal and informal applications in both developed and developing countries, so that sustainability in the agricultural system and environmental protection for future generations is achieved. Opender Koul G.S. Dhaliwal Gerrit W. Cuperus

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 1


Integrated Pest Management: Retrospect and Prospect G.S. Dhaliwal,1 Opender Koul2 and Ramesh Arora1


of Entomology, Punjab Agricultural University, Ludhiana 141 004, India; Biopesticide Research Centre, Jalandhar 144 003, India E-mail: [emailprotected]; [emailprotected]


Introduction In the history of the world, no century can match the population growth of the one that has just come to a close. We entered the 20th century with fewer than 2 billion people and left it with more than 6 billion. At the current pace, when the population increases by about 78 million per year, the global population is projected to rise to over 8 billion by 2025 (Hinrichsen and Robey, 2000). Thus, the population may grow even more in the 21st century, but in a very different way. The new century’s growth will occur almost exclusively in the developing countries – among people with limited financial resources. The developed countries, which almost doubled their population in the 20th century, will grow slowly or not at all. Over half of the world population growth will occur in Asia and one-third will be in Africa. The world farmers will thus need to produce enough food for the expanding population (Dhaliwal and Arora, 2001). The future of world food supply is closely linked with the pattern of population growth. In many countries over the past two decades, growth in food supply has lagged behind population growth. Worldwide, the grain harvest increased by 1% annually between 1990 and 1997, a rate of growth sub-

stantially slower than the average population growth rate of 1.6% in the developing world (Hinrichsen and Robey, 2000). Since humans started practising agriculture about 10,000 years ago, the increased need for food that resulted from increasing population or rising living standards was met by bringing a greater area of land under cultivation. However, during the last century, larger needs for food were mostly met by increasing productivity per unit of land. This trend is likely to continue as the populations increase and the land is required for purposes other than agriculture (FAO, 2001). Food production per unit of land is limited by many factors, including fertilizer, water, genetic potential of the crop and the organisms that feed on or compete with food plants. These organisms that interfere significantly with the productivity or quality of plants considered useful for humans are called pests. Broadly speaking, a pest is any organism that is in competition with humans for some resource. In agriculture, pests occur in many groups of organisms, including plants, arthropods (insects, mites), fungi, bacteria, nematodes, viruses, viroids, mycoplasma-like organisms, rodents, birds and other vertebrates. Food plants of the world are damaged by 10,000 species of insects, 30,000 species of weeds, 100,000 dis-

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


01IntpestManCh1.QXD 14/4/04 2:24 pm Page 2


G.S. Dhaliwal et al.

eases (caused by fungi, viruses, bacteria and other microorganisms) and 1000 species of nematodes (Hall, 1995). The global losses due to various categories of pests vary with the crop, the geographical location and the weather. Total yield losses from different pests of all crops have been estimated to be US$500 billion worldwide. Despite the plant-protection measures adopted to protect the principal crops, 42.1% of attainable production is lost as result of attack by pests. However, if no control measures were used to protect crops, the figure would be 69.8%. Animal pests account for 15.6% loss of production, pathogens 13.3% and weeds 13.2% (Oerke et al., 1994).

Evolution of Management Tactics During ancient times, humans had to live with and tolerate the ravages of crop pests, but they gradually learned to improve their condition through trial-and-error experiences. Over the centuries, farmers developed a number of mechanical, cultural, physical and biological control measures to minimize the damage caused by phytophagous insects. Synthetic organic insecticides developed during the mid-20th century provided spectacular control of these pests and resulted in the abandonment of traditional pest-control practices. Thus, the evolution of the concept of pest management spans a period of more than a century (Table 1.1). Many components of pest management were developed in the late 19th and early 20th centuries. Rapidly developing technologies and changing societal values had their impact on pest-control tactics also. The history of agricultural pest control thus has three distinct phases, namely, the era of traditional approaches, the era of pesticides and the era of integrated pest management (IPM) (Metcalf, 1980; Dhaliwal et al., 1998).

Era of traditional approaches (ancient–1938) Cultural and mechanical practices, such as crop rotation, field sanitation, deep ploughing, flooding, collection and destruction of

damaging insects/insect-infested plants, etc., developed by farmers through experience were among the oldest methods developed by humans to minimize the damage caused by insect pests (Smith et al., 1976). These were followed by the use of plant products from neem, chrysanthemum, rotenone, tobacco and several other lesser-known plants in different parts of the world. The Chinese were probably the pioneers in the use of botanical pesticides as well as biological control methods for the management of insect pests of stored grains and field crops (Dhaliwal and Arora, 1994a). However, systematized work on many important tactics of pest control, including the use of resistant varieties, biological control agents and botanical and inorganic insecticides, was done in the USA from the end of the 18th to the end of the 19th century. Remarkable success was achieved in the management of grape phylloxera, caused by Viteus vitifoliae (Fitch), by the grafting of European grapevine scions to resistant North American rootstocks during the 1880s. At around the same time, cottony cushion scale, Icerya purchasi Maskell, which was causing havoc in the citrus industry in California, USA, was successfully controlled by release of the vedalia beetle, Rodolia cardinalis (Mulsant), imported from Australia (DeBach, 1964). A number of synthetic inorganic insecticides containing arsenic, mercury, tin and copper were also developed towards the end of the 19th and the beginning of the 20th century. With the development of these insecticides, the focus of research in pest control slowly shifted from ecological and cultural control to chemical control, even before the development of synthetic organic insecticides (Perkins, 1980).

Era of pesticides (1939–1975) The synthetic inorganic insecticides were broad-spectrum biocides and were highly toxic to all living organisms. These were followed in due course by the synthetic organic insecticides, such as alkyl thiocyanates, lethane, etc. The era of pesticides, however, began with the discovery of the insecticidal

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 3

IPM: Retrospect and Prospect


Table 1.1. Landmarks in the history of agricultural pest management (modified after Dhaliwal et al., 1998). Period



The Chinese used wood-ash for the control of insect pests in enclosed spaces and botanical insecticides for seed treatment. They also used ants for biological control of stored grain as well as foliage-feeding insects. In India, neem leaves were placed in grain bins to keep away troublesome pests. In the Middle and Near East, powder of chrysanthemum flowers was used as an insecticide The myna (a bird) from India was imported for the control of locusts in Mauritius ‘Underhill’ variety of wheat reported resistant to Hessian fly in the USA ‘Winter Majetin’ variety of apple reported resistant to woolly apple in the USA A. Fitch reported the role of ladybird beetles, green lacewings and other predacious insects in the control of insect pests of crops Pyrethrum first used for insect control in the USA Biological control of cottony cushion scale on citrus in the USA by use of the vedalia beetle imported from Australia Control of grape phylloxera in Europe by grafting of European grapevine scions to resistant North American rootstocks Multiple-component suppression techniques involving the use of resistant varieties, sanitation practices and need-based application of insecticides developed for the control of boll-weevil in the USA ● Insecticidal properties of DDT reported by Paul Muller in Switzerland ● Bacillus thuringiensis Berliner first used as a microbial insecticide Insecticidal activity of hexachlorocyclohexane (HCH) discovered in France Parathion, the first organophosphatic insecticide developed ‘Doom’ based on Bacillus popilliae Dutky and Baciilus lentimorbus registered in the USA for the control of Japanese beetle larvae on turf ● R.H. Painter published his classic book Insect Resistance in Crop Plants ● Introduction of first carbamate insecticide, isolan ● Concept of integrated control involving integration of chemical and biological control introduced ● Concept of economic injury level and economic threshold developed by V.M. Stern and co-workers Publication of the book Silent Spring, by Rachel Carson, which dramatized the impact of the misuse and overuse of pesticides on the environment Publication of the book Biological Control of Insect Pests and Weeds, by Paul DeBach, which established biological control as a separate discipline in entomology ● Elcar (Helicoverpa nucleopolyhedrovirus (NPV)) registered for the control of boll-worm and tobacco budworm on cotton ● First insect growth regulator (Methoprene) registered for commercial use in USA ● Publication of the book Introduction to Insect Pest Management by R.L. Metcalf and W.H. Luckmann, which was the first comprehensive treatise on IPM and established the concept on a firm footing The interest in botanical pesticides revived and the First International Conference on Neem was held at Rottach-Egern, Germany Development of first transgenic plant, reported by M. Vaeck and co-workers of Belgian biotechnology company, Plant Genetic System, by transferring B. thuringiensis -endotoxin gene to tobacco for the control of Manduca sexta (Johannsen) An IPM Task Force was established to garner international support for the development and implementation of IPM programmes. A team of consultants appointed by the Task Force reviewed the status of IPM and made recommendations. The Task Force was later reconstituted as the Integrated Pest Management Working Group (IPWG) in 1990 ● Concept of environmental economic injury levels proposed by L.P. Pedigo and L.G. Higley ● Dr Edward F. Knipling and Dr Raymond C. Bushland were awarded the World Food Prize for developing sterile-insect technique Continued

1762 1782 1831 1855 1858 1889 1890 1923

1939 1941 1946 1948 1951 1959

1962 1964 1975

1980 1987



01IntpestManCh1.QXD 14/4/04 2:24 pm Page 4


G.S. Dhaliwal et al.

Table 1.1. Continued. Period

1994 1995

1996 1997 2002

Landmark(s) ● United Nations Conference on Environment and Development (Rio de Janeiro, Argentina) assigned a pivotal role to IPM in the agricultural programmes and policies envisaged as part of its Agenda 21 A Task Force consisting of FAO, the World Bank, UNDP and UNEP co-sponsored the establishment of the Global IPM Facility with the Secretariat located at FAO, Rome Dr Hans R. Herren was awarded the World Food Prize for developing and implementing the world’s largest biological control project for cassava mealy bug, which had almost destroyed the entire cassava crop of Africa Insect-resistant transgenic (Bt) cotton, maize and potato were commercialized in the USA Dr Ray F. Smith and Dr Perry L. Adkisson were awarded the World Food Prize for their pioneering work in the development and implementation of the IPM concept Bt cotton approved for commercialization in India

DDT, dichlorodiphenyltrichloroethane; FAO, Food and Agriculture Organization; UNDP, United Nations Development Programme; UNEP, United Nations Environment Programme; Bt, Bacillus thuringiensis.

properties of 2,2-bis(p-chlorophenyl)-1,1, 1-trichloroethane (DDT) by Paul Muller in 1939. The impact of DDT on pest control is perhaps unmatched by any other synthetic substance and Muller was awarded a Nobel Prize for this work in 1948. DDT was soon followed by a number of other insecticides, such as hexachlorocyclohexane (HCH), chlordane, aldrin, dieldrin, heptachlor (organochlorine group), parathion, toxaphene, schradan, O-ethyl O-4(nitrophenyl) phenyl phosphonothionate (EPN) (organophosphorus group) and allethrin (synthetic pyrethroid), during the 1950s and a large number of other popularly used organophosphates and carbamates in the ensuing decade. Due to their efficacy, convenience, flexibility and economy, these pesticides played a major role in increasing crop production. The success of high-yielding varieties of wheat and rice, which ushered in the ‘green revolution’, was partially due to the protective umbrella of pesticides (Pradhan, 1983). The spectacular success of these pesticides masked their limitations. The intensive and extensive use, misuse and abuse of pesticides during the ensuing decades caused widespread damage to the environment. The most serious effects of pesticides are those on human health and life. It has been reported that at least 3 million, and perhaps as many as 25 million, agricultural workers are poisoned each year by pesticides, and some 20,000 deaths can be directly attributed to

agrochemical use (Meerman et al., 1997). Nearly three-quarters of the documented deaths take place in the Third World, even though it consumes only 15% of the global pesticide output. In addition, long-term teratogenic, carcinogenic and mutagenic effects of pesticides are well documented. In a landmark report, the National Resource Defence Council (NDRC) of the USA reported that one out of every 3400 children between 1 and 5 years of age could one day get cancer because of the pesticides they consumed as young children (NDRC, 1989). Only a small amount (< 1%) of the pesticide applied to a crop reaches target pests and the remaining (> 99%) enters different components of the environment to contaminate soil, water, air, food, feed, forage and other commodities. Nearly 100% of the human population has been found to contain some residues of pesticides, such as DDT and HCH (Dhaliwal and Arora, 2001). In developing countries, such as India, a large proportion of market samples of nearly all types of food commodities have been found to contain pesticide residues above the legal maximum residue limits (MRLs). In addition to human beings, the whole range of living organisms, including natural enemies, pollinators, domestic and wild animals, birds, fish and other aquatic organisms and even soil fauna are affected by the use of insecticides in agriculture (Dhaliwal and Singh, 2000). In addition, pest problems in some crops increased following the continuous

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 5

IPM: Retrospect and Prospect

application of pesticides. This, in turn, further increased the consumption of pesticides, resulting in the phenomenon of the pesticide treadmill (Altieri, 1995). The combined impact of all these problems, together with the rising cost of pesticides, provided the necessary feedback for limiting the use of the chemical control strategy and led to the development of the IPM concept.

Era of IPM (1976 onwards) Although many IPM programmes were initiated in the late 1960s and early 1970s in several parts of the world, it was only in the late 1970s that IPM gained momentum. The first major IPM project in the USA, commonly called the Huffaker project, spanned 1972–1978 and covered six crops, i.e. lucerne, citrus, cotton, pines, pome and stone fruits, and soybean. This was followed by another large-scale IPM project called the Consortium for Integrated Pest Management (CIPM) (1979–1985), which focused on lucerne, apple, cotton and soybean. The average adoption of IPM for four crops was claimed to be about 66% over 5.76 million ha (Frisbie and Adkisson, 1985a,b). In 1993, the US government set up the National IPM Initiative and submitted that implementing IPM practices on 75% of the nation’s crop area by 2000 was a national goal (Sorenson, 1994). In a recent accounting of the progress by the US Department of Agriculture (USDA) in achieving this goal, it has been estimated that some level of IPM has been implemented on about 70% of the US crop acreage (Baron, 2002). National IPM programmes were launched in the late 1980s and early 1990s in several developing countries. The most outstanding success has been the Food and Agriculture Organization (FAO) IPM programme for rice in South-east Asia. By the end of 1995, 35,000 trainers and 1.2 million farmers had been exposed to IPM through this programme (FAO, 1995). A recent development at FAO in support of IPM is the establishment of the Global IPM Facility, co-sponsored by the United Nations Development Programme (UNDP), the United Nations Environment Programme (UNEP) and the World Bank. The concept is in response to the United Nations Conference on


Environment and Development, held in Rio de Janeiro, Brazil, in 1992, which assigned a central role for IPM in agriculture as part of Agenda 21. The Facility will serve as a coordination, consulting, advising and promoting agency for the advancement of IPM worldwide (Kogan, 1998). Major efforts in implementing IPM in irrigated rice have been carried out in Asia by the FAO through the Inter-Country Programme for the Development and Application of Integrated Pest Control in Rice in South-east Asia. This programme remains one of the best examples of IPM implementation in the tropical region. It involves purposeful, direct efforts to change farmers’ practices, in contrast to some more indirect routes of IPM technology diffusion in many industrialized, temperate environments. The programme itself has evolved into its present transnational form from a relatively small project supported by Australia in the late 1970s, following the large-scale pest outbreaks in several South-east Asian countries (NRI, 1992). The first phase of the FAO programme (1980–1986) focused on developing and testing the technical aspects of the IPM concept in its seven participating countries, namely, Bangladesh, India, Malaysia, the Philippines, Sri Lanka and Thailand. More recently, the project has been directed towards enhancing farmers’ adoption of IPM. Australia, The Netherlands and the Arab Gulf fund have supported the programme. One significant accomplishment of the programme has been to cause policy changes within several governments, in the form of official support of IPM as the means for national plant protection in the Philippines, Indonesia, India, Sri Lanka and Malaysia (NRI, 1992). A case study of the National IPM Programme in Indonesia as a part of the regional programme during 1989–1991 provides an interesting scenario. Following research findings showing the relation between brown planthopper outbreaks and high pesticide use, the Indonesian government banned the use of 57 broad-spectrum pesticides and declared IPM as the national pest-control strategy. These measures, together with the gradual abolition of the high subsidies on pesticides, created a favourable climate for the large-scale implementation of IPM (Fig. 1.1).

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 6


G.S. Dhaliwal et al.


50 28

85% 40 75%


30 55% 22


20 Rice Pesticides

Pesticide subsidy 0%

10 1984




Milled rice production (millions of tonnes)

Pesticide production (× 1000 tonnes)



Fig. 1.1. Impact of pesticide subsidy on rice production in Indonesia (after FAO, 1990).

To assess the impact of IPM on pest control and yield, the latter were compared with those of non-IPM farmers (van de Fliert, 1993). IPM farmers really decreased their frequency of pesticide sprays during and after the training to a level consistently lower than that of non-IPM farmers (Table 1.2). Consequently, IPM farmers’ expenditure on insect chemical control decreased. The number of farmers not applying pesticides was also significantly higher among IPM farmers.

In spite of this, IPM farmers obtained higher yields than non-IPM farmers, which, in addition to lower pest-control expenditure, resulted in higher returns from the crop. Additionally, there were fewer variations in fields among IPM farmers than among nonIPM farmers, indicating less risky farm management under the IPM regime. Timeliness and adequacy of various cultivation and pest-control practices, resulting from better monitoring and decision-making skills, seem to be most important in this respect (van de Fliert, 1998). During the second phase of the National IPM Programme (1994/95), 310,550 farmers participated in rice IPM field schools. IPM farmers applied pesticides, on average, 1.25 times while non-IPM farmers made an average of 3.62 applications during the season. Similarly, IPM farmers used fewer formulations (co*cktails) per spray event, with an average of 2.6 for IPM farmers versus 7.2 for non-IPM farmers. China, which has been experimenting with IPM for the control of rice pests since the early 1980s, was also invited to join the FAO project in 1989. During 1989/90 alone, nearly 160,000 farmers from over 2000 villages received IPM training. Compared with untrained farmers, IPM-trained farmers saved roughly a third of the pesticides in rice cultivation and still obtained a 7% higher yield. It was estimated that the investment in IPM training generated a return of more than

Table 1.2. Insect pest-control practices, expenditures and yields of IPM and non-IPM farmers in two villages in Central Java, before, during and after IPM training (from van de Fliert, 1993). Before training Parameter


Frequency of spray 1.4 applications (no./season) Frequency of granular 0.4 applications (no./season) Farmers not using 26 pesticides (%) Average insect control 32 cost (Rs 1000/ha) Average yield (t/ha) 5.38

During training

After two seasons

After one season





































IPMF, IPM farmers; NIPMF, non-IPM farmers.







01IntpestManCh1.QXD 14/4/04 2:24 pm Page 7

IPM: Retrospect and Prospect

400%. Encouraged by these results, the Ministry of Agriculture has set up a National Steering Committee for the comprehensive prevention and control of diseases and insect pests to protect the nation’s rice crop and increase profits. The Committee conducts IPM tests, gives demonstrations and makes appraisals (Quinghua, 1995). In the Philippines, a National IPM Programme was launched in 1993 and a total of 40,024 farmers were trained during 1993–1995, among whom 36,024 are rice farmers. Of 1632 farmers’ field schools (FFSs), 1470 were devoted to rice farmers. The increase in rice yield obtained by IPM farmers varied from 4.7 to 62%. The expenditure on pesticide use (15% of total cost) was almost eliminated in the case of IPM farmers (Kenmore, 1997). In Vietnam, during 1992–1995, 5941 FFSs were organized in 3095 villages (out of 9274 villages in the country), with a total of 173,650 farmers trained. The number of insecticide applications by IPM farmers was reduced by 80–90% and, in some agroecological regions, there was almost no use of insecticides. IPM fields produced 150–460 kg/ha more rice than non-IPM fields. One study of over 1300 villages in Vietnam showed a 4% yield increase in rice and over 20% increase in profits (Kenmore, 1997). In Bangladesh, the Cooperative for American Relief to Everywhere (CARE)Bangladesh began introducing IPM activities into an ongoing rice irrigation project in the late 1980s. Most of the farmers that CARE worked with were very small, owning less than half an acre of land. The farmers were trained in rice–fish culture and IPM. A survey among the farmers trained in rice–fish culture and IPM revealed that, during 1992/93, virtually all of them stopped using


pesticides and satisfactory control of insect pests was being provided by fish and naturally occurring parasitoids and predators (Table 1.3). Farmers cultivating fish in their rice fields totally eliminated the use of pesticides even without training in IPM. However, only 20% of the farmers could cultivate fish, mainly due to lack of adequate water, the poor water-holding capacity of the soil and the risk of flooding. Those farmers who could not cultivate fish still reduced their pesticide use by 76% with IPM training. By harvest time, some farmers were able to harvest quantities of fish worth as much as their rice. These results underline the need for undertaking an IPM programme as part of overall rural development programmes (Kamp et al., 1993). During 1995, farmers at IPM schools applied an average of 0.19 spray/season as compared with 1.65 sprays/season during the pretraining period. The average yield increased by 17% from 3.76 t/ha during the pretraining period to 4.4 t/ha after IPM training. The average number of pests per ten rice hills decreased from 20 to 11 and the number of natural enemies increased from 18 to 31. In India, FFSs were organized at locations covering all the major rice growing areas of the country during 1994/95. Pesticide use in IPM fields decreased by 50–100% as compared with non-IPM areas. There was an increase in yield between 6.2 to 42.1% in IPM fields as compared with non-IPM areas (Rajak et al., 1997). The success of the rice programme persuaded FAO to launch similar IPM Intercountry Programmes for vegetables (1996) and cotton (1999). Moreover, in the

Table 1.3. Effect of training in rice–fish culture and IPM on pesticide use by rice growers during 1992/93, Rangpur, Bangladesh (from Kamp et al., 1993). Parameter Number of farmers Type of training

Reduction in pesticide use (%) Increase in rice yield (%)

Group I 121 Rice–fish culture only 100 6

Group II

Group III

Group IV

58 Rice–fish culture and IPM 100 13

972 IPM only

60 Nil

76 10

– –

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 8


G.S. Dhaliwal et al.

individual countries, FFS activities were started in a range of other crops, sometimes with external donor support, sometimes without. The Asian model of FFS IPM training has been applied in other continents as well, albeit with adjustments for different cropping and socio-economic conditions (Eveleens, 2002).

integrated control was first conceived by Hoskins et al. (1939) when they said:

Origin of IPM Concept

The credit for using the term ‘integrated control’ for the first time goes to Michelbacher and Bacon (1952), who, while working on the control of codling moth, Cydia pomonella (Linnaeus), stressed ‘the importance of considering the entire, entomological picture in developing a treatment for any particular pest … All effort was directed towards developing an effective integrated control program of the important pests of walnut.’ Subsequently, Smith and Allen (1954) stated that ‘integrated control … will utilize all the resources of ecology and give us the most permanent, satisfactory and economical insect control that is possible’. Following this was a series of papers that established integrated control as a new trend in entomology (Kogan, 1998). Stern et al. (1959) were the first to define integrated control as ‘applied pest control, which combines and integrates biological and chemical control’. This definition remained in place through the late 1950s and early 1960s, but began to change soon in the early 1960s as the concept of pest management gained acceptance among crop protection specialists.

The basic tactics of IPM were proposed and used to protect crop plants against the ravages of pests long before the term was coined. Most discussions of IPM include the concept of economic threshold, implying that whatever cost one applies to the pest control techniques should be returned from the production of the crop (McNeal, 1988). Another concept is that of team effort, where IPM strives to bring together as many disciplines and areas of interest as possible. The concern over pesticides as a main source of pest control is that it makes one totally reliant on such technology and, if that technology starts to fail, the only way out is a new replacement that promises an improvement over the old one, even if the transfer may also cause difficulties. Thus, in the absence of modern synthetic pesticides, crop protection specialists during the late 19th and early 20th centuries relied on pest biology and cultural practices to propose multitactical approaches, which could be considered as precursors of modern IPM systems. To be precise, the concept of technology packages assembled in IPM can help us to avoid some of the pitfalls inherent in reliance on a single technology (McNeal, 1988).

Integrated control According to McNeal (1988), one of the activities most responsible for the genesis of IPM was the work done in cotton entomology in Arkansas in the 1920s. This research was overshadowed in the late 1940s as pesticides came along, but the work continued into the 1950s with the cotton scouting programme in Arkansas. However, apparently the idea of

Biological and chemical control are considered as supplementing to one another or as the two edges of the same sword … nature’s own balance provides the major part of the protection that is required for the successful pursuit of agriculture … insecticides should be used so as to interfere with natural control of pests as little as possible.

Pest management The idea of managing insect-pest populations was proposed by Geier and Clark (1961), who called this concept ‘protective population management’, which was later shortened to ‘pest management’ (Geier, 1966). By the mid-1970s, integrated control and pest management coexisted essentially as synonyms. However, a synthesis of the two expressions had already become available when Smith and van den Bosch (1967) wrote: ‘The determination of insect numbers is broadly under the influence of the total

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 9

IPM: Retrospect and Prospect

agroecosystem and a background role of the principal elements is essential to integrated pest population management’.

Integrated pest management It was, however, in 1972 that the term ‘integrated pest management’ was accepted by the scientific community, after the publication of a report under the above title by the Council on Environmental Quality (CEQ, 1972). In creating this synthesis between integrated control and pest management, no obvious attempts seemed to have been made to advance a new paradigm. Much of the debate had already taken place during the 1960s and by then there was substantial agreement on the following issues (Kogan, 1998):


pest management’ (EBPM), emphasizing that it was: ● safe for farmers and consumers; ● cost-effective and easy to adopt and integrate with other crop protection practices; ● durable and without adverse environmental and safety consequences; and ● used with ecosystems as the ecological focus.

● ‘Integration’ means the harmonious use of multiple methods to control single pests as well as the impacts of multiple pests. ● ‘Pests’ are any organisms detrimental to humans, including invertebrate and vertebrate animals, pathogens and weeds. ● ‘Management’ refers to a set of decision rules based on ecological principles and economic and social considerations. The backbone for the management of pests in an agricultural system is the concept of economic injury level (EIL). ● ‘IPM’ is a multidisciplinary endeavour.

All these goals have been well taken care of by the concept of IPM. Thus IPM is here to stay and to provide suitable solutions to future pest problems. Recently, Benbrook (2002) proposed a new term: the IPM continuum. According to the author, IPM systems exist in almost limitless variety along an IPM continuum. It includes four major zones/levels: no, low, medium and high or biointensive IPM. Farmers in the ‘non-IPM’ zone manage pests with routine pesticide applications. Low-end IPM depends on basic field sanitation, scouting and pesticide applications linked to thresholds. Medium-level IPM shifts a portion of the control burden to largely preventive measures and requires farmers to bypass most applications of pesticides because of the greater degree of reliance on beneficial organisms. High-level IPM systems manage pests largely through multitactic preventionbased interventions. Biointensive IPM (or Bio IPM) lessens pest pressure through management of ecological and biological processes and interactions.

Alternative paradigms

Defining IPM

Although the success of IPM has been accepted worldwide, some new terms have been proposed to lay emphasis on particular strategies. Frisbie and Smith (1991) proposed ‘biologically intensive IPM’ or ‘biointensive IPM’, which would rely on host-plant resistance, biological control and cultural control. In fact, the utilization of biological control and other non-chemical methods has been amply stressed in all IPM programmes. Recently, a special committee of the National Research Council’s Board of Agriculture (NRC, 1996) proposed ‘ecologically based

Since the first definition of integrated control (Stern et al., 1959), more than 65 definitions of integrated control, pest management or IPM have been proposed. A broader definition was adopted by FAO Panel of Experts (FAO, 1967): Integrated pest control is a pest management system that, in the context of associated environment and population dynamics of the pest species, utilizes all suitable techniques and methods in as compatible a manner as possible and maintains pest populations at levels below those causing economic injury.

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 10


G.S. Dhaliwal et al.

It is not simply the juxtaposition or superimposition of two control techniques but the integration of all suitable management techniques with the natural regulating and limiting elements of the environment. According to the National Academy of Sciences, IPM refers to an ecological approach in pest management in which all available necessary techniques are consolidated in a unified programme, so that pest populations can be managed in such a manner that economic damage is avoided and adverse side effects are minimized (NAS, 1969). Most other contemporary definitions perpetuate the perception of an entomological bias in IPM because of the emphasis on pest populations and EIs, of which the former is not always applicable to plant pathogens and the latter is usually attached to the notion of an action threshold that is often incompatible with pathogen epidemiology or many weedmanagement systems. Smith (1978) defined IPM as a multidisciplinary ecological approach to the management of pest populations, which utilizes a variety of control tactics compatibly in a single coordinated pest-management system. In its operation, integrated pest control is a multitactical approach that encourages the fullest use of natural mortality factors, complemented, when necessary, by artificial means of pest management. In other words, IPM seeks to integrate multidisciplinary methodologies to develop pest-management strategies that are practical, effective, economical and protective of both public health and the environment (Smith et al., 1976). IPM has also been defined as a pest population management system that utilizes all suitable techniques in a compatible manner to reduce pest populations and maintain them at levels below those causing economic injury (Frisbie and Adkisson, 1985a,b). Dr Ray F. Smith and Dr Perry Adkisson were awarded the 1997 World Food Prize for their pioneering work in the development and implementation of the IPM concept. However, in 1998, USDA came up with a definition that IPM is a sustainable approach that combines the use of prevention, avoidance, monitoring and suppression strategies in a way that minimizes economic, health and environmental risks (

IPM is systematic approach to crop protection that uses increased information and improved decision-making paradigms to reduce purchased inputs and improve economic, social and environment conditions on the farm and in society (Allen and Rajotte, 1990). IPM is a comprehensive approach to pest control that uses combined means to reduce the status of pests to tolerable levels while maintaining a quality environment (Pedigo, 1991). IPM is also defined as the intelligent selection and use of pest-control tactics that will ensure favourable economic, ecological and sociological consequences (Luckman and Metcalf, 1994). IPM is a dynamic and constantly evolving approach to crop protection in which all the suitable management tactics and available surveillance and forecasting information are utilized to develop a holistic management programme as part of a sustainable crop production technology (Dhaliwal and Arora, 2001). Here it needs to be emphasized that the aim of future IPM programmes should not be restricted merely to the efficient use of pesticides and product substitution (biorationals and botanicals in place of conventional insecticides) within an agricultural system that remains essentially unchanged (Table 1.4). Rather, these programmes should aim at fundamental structural changes through a better understanding of ecological processes and synergy between crops (van Veldhuizen and Hiemstra, 1993). Kogan (1998) carried out numerical analyses of various definitions spanning the last 35 years and found that most of the authors depended on the following issues to capture the essence of the IPM concept: ● The appropriate selection of pest-control methods, used singly or in combination. ● The economic benefits to growers and to society. ● The decision rules that guide the selection of the control action. ● The need to consider impacts of multiple pests. Taking into consideration all the above points and the current thought, Kogan (1998) put forward his definition:

Reduce losses due to pests


Diversity Ecosystem stability Spatial scale

Time scale


Criteria for intervention

Principal method

Research goal

Extension technique

Effect on environmental Usually negligible quality


2 3 4








Nil due to absence of organized effort Nil

Cultural and mechanical measures

Past experience

Single pest or closely related groups of pests

Long term

High Uncertain Single farm


No. Parameter

Resistant varieties, cultural practices, monitoring, product substitution, insecticide resistance management and multiple interventions More kinds of interventions

Several pests around a crop and their natural enemies Economic threshold

Low or medium Unstable Single farm or small region defined by pests Single season

Reduce costs of production

Present IPM

Transfer of technology TOT (TOT) Highly detrimental Moderately detrimental

Improved pesticides

Calendar date or presence of pest Pesticides

Single pest


Eliminate or reduce pest species Low Highly unstable Single farm


Pest management system

Table 1.4. Approaches to insect pest management: retrospect and prospect (from Dhaliwal and Arora, 1994b).

Complementarity between TOT and farmer-first (FF) mode Negligible

Minimize need for intervention

Agroecosystem design to minimize pest outbreaks and mixed strategies, including group action on an area-wide basis to complement pest controls aimed at individual fields

Multiple criteria

Long-term steady-state oscillatory dynamics Fauna and flora of a cultivated area and linkages with non-cultivated ecosystem

High Striving towards stability and equilibrium Biogeographical regions

Multiple-ecological, economic and social

IPM in sustainable agriculture

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 11

IPM: Retrospect and Prospect 11

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 12


G.S. Dhaliwal et al.

IPM is a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/benefit analyses that take into account the interests of and impacts on producers, society and the environment.

Decision Making Systems Pest management is a combination of processes that include decision making, taking action against a pest and obtaining the information to be used in reaching these decisions (Ruesink and Onstad, 1994). In assessing, evaluating and choosing a particular pest-control option, farmers are likely to take three major factors into account (Fig. 1.2): ● Farmers’ perception of the problem and of potential solutions is the most important factor. Here, the farmer’s ability to identify pests, his/her assessment of likely and potential pest losses and his/her opinion regarding the efficacy of different control options will affect the decision process. ● The way in which control options are assessed will depend on the farmers’ objectives. Subsistence farmers may opt for a guaranteed food supply, while commercial farmers are more concerned with profit. ● The number of options that a farmer can feasibly use will depend on the constraints set by the resources available. Various alternative pest-control options could be evaluated for their cost-effectiveness (Reichelderfer et al., 1984): ● Determine from experimental results both the per hectare cost and a measure of effect of each alternative practice. If effectiveness can be measured in terms of output (yield and/or crop quality), use partial budgeting or other analytical techniques to evaluate alternatives. If effectiveness cannot be measured in these terms, proceed with determination of cost-effectiveness. ● Using the same units in which effectiveness is measured (e.g. reduction in pest

numbers or damage), specify an effectiveness target that is appropriate, given the experimental data and information at hand (e.g. a 50% reduction in pest population). ● Multiply the cost of each practice times the effectiveness target and then divide that product by the actual level of effectiveness achieved by the practice. This gives a set of relative cost-effectiveness figures. ● Compare the cost-effectiveness of alternative practices. The practice that has associated with it the lowest cost to achieve the effectiveness target is the most costeffective practice.

Implementation Although IPM has been accepted in principle as the most attractive option for the protection of agricultural crops from the ravages of insect and non-insect pests, implementation at the farmers’ level has as yet been rather limited. Some of the important constraints to wider adoption of IPM and suggested measures to overcome them are discussed in this section.

Constraints in IPM implementation The Consultant Group of the IPM Task Force has conducted an in-depth study of the constraints on the implementation of IPM in developing countries, which can be categorized into the following five main groups (NRI, 1992; Alam, 2000). Institutional constraints IPM requires an interdisciplinary, multifunctional approach to solving pest problems. Fragmentation between disciplines, between research, extension and implementation and between institutes leads to a lack of institutional integration. Secondly, both the national programmes of developing countries and the donor agencies have lacked a policy commitment to IPM in the context of national economic planning and

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 13

IPM: Retrospect and Prospect

Farmer’s resources

Farmer’s perception of pest problem and its control

Farmer’s needs and objectives


Assessment of options, feasibility and appropriateness

Pest-control options

Evaluation and comparison among appropriate options

Action arising from choice of option

Outcome of action Fig. 1.2. The process of decision making in IPM (after Reichelderfer et al., 1984).

agricultural development. This has resulted in a low priority for IPM from national programmes and donors alike. Thirdly, the traditional top-down research in many cases does not address the real needs of farmers, who eventually are the end-users and who elect to adopt or reject the technology based on its appropriateness. Institutional barriers to research scientists in national programmes conducting on-farm research in developing countries are real and need to be addressed.

individual control techniques are well known, little knowledge is available on using them in an integrated fashion under farm conditions. The lack of training materials, curricula and experienced teachers on the principles and practice of IPM is another major constraint. In many cases, the field level extension workers are not sufficiently trained in IPM to instil confidence in the farmers. Sociological constraints

Informational constraints The lack of IPM information that could be used by farmers and extension workers is a major constraint in implementation. In a recent study regarding the implementation of IPM in Haryana, India, it was found that more than three-quarters of the farmers were not even aware of the concept of IPM. Even those who were aware of the concept reported that they lacked the skills necessary to practise IPM (Alam, 2000). While the

The conditioning of most farmers and farmlevel extension workers by the pesticide industry has created a situation where chemicals are presented as highly effective and simple to apply. This acts as a major constraint in IPM implementation. There appears to be a direct conflict between the industry’s objective of more sales and the IPM message of rational pesticide use in the eyes of farmers. There is a need for private industry and public-sector extension agencies to work in a

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 14


G.S. Dhaliwal et al.

more complementary manner. A majority of the farmers in a recent study in Haryana, India, expressed their lack of faith in IPM. They considered IPM practices to be risky as compared with the use of chemical pesticides (Alam, 2000). Economic constraints A major constraint, even if IPM is adopted in principle, is the funding for research, extension and farmer training needed for an accelerated programme. IPM must be viewed as an investment and, as with other forms of investment, requires an outlay. Starting with the Huffaker project, the US Environmental Protection Agency (USEPA) and USDA have financed a number of IPM programmes, resulting in substantial progress in the development and implementation of IPM. In the long run, IPM programmes may become selfgenerating due to savings on resource inputs for production. A majority of the farmers purchase pesticides on credit and depend on shopkeepers and pesticide dealers for information about pest-control methods. Political constraints The relatively low status of plant-protection workers in the administrative hierarchy is a constraint to general improvement in plant protection. Associated with the above is the moral and financial standing of these workers. The continuance of pesticide subsidies by the government for political reasons and their tie-up with the government-provided credit for crop production act as a major constraint to farmers’ acceptance of IPM. Various vested interests associated with the pesticide trade also act as a political constraint on the implementation of IPM (Jiggins, 1996).

Strategies for IPM implementation Acceleration of IPM implementation in developing countries requires farmers’ participation, increased government support, an improved institutional infrastructure and a favourable environment.

Farmers’ participation It would not be an exaggeration to say that the dawn of civilization started with farmer innovation. Ever since that day, farmers have improved ways of growing crops through successive innovations. Prior to the emergence of crop-protection sciences and even before the broad outlines of the biology of pests were understood, farmers evolved many cultural, mechanical and physical control practices for the protection of their crops from insects and non-insect pests (Smith et al., 1976). Farmers’ innovations were the only source of improvements in crop production and protection technology until formal research by on-station scientists started complementing it during the late 18th and 19th centuries (Haverskort et al., 1991). Unfortunately, with the advent of modern high-tech agriculture, comprising of highyielding varieties (HYVs), fertilizers and pesticides, farmers have been completely displaced from the research and development process. Instead, this role has been usurped by private industry and government agencies. The technology generated by farm scientists is being transferred through extension agencies to farmers. The new technology package has created a number of ecological and environmental problems. The alternative path of sustainable agriculture requires farmers’ participation at every step of the research and development process in order to draw on their understanding of the local conditions and constraints, their innovativeness and their skills at making the best possible use of limited resources. Placing the farmer at the centre of the development process is wholly consistent with the IPM goal of making the farmer a confident manager and decision maker, free from dependence on a constant stream of pest-control instructions from outside. The role of researchers, extension workers and non-governmental organizations (NGOs) is to act as consultants, facilitators and collaborators, stimulating and empowering the farmers to analyse their own situation, to experiment and to make constructive choices. A number of terms have been proposed for the new approach. These include:

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 15

IPM: Retrospect and Prospect

‘farmer first and last’, ‘farmer participatory research’, ‘farmer first’, ‘approach development’, ‘people-centred technology development’ (PCTD) and ‘participatory technology development’ (PTD) as well as the old term ‘sustainable agriculture’ (Chambers et al., 1991; Haverskort et al., 1991). PTD serves to improve the experimental capacity of farmers and helps in the development of locally adapted improved technologies. The approach has been used for implementation of IPM programmes in Indonesia (Matteson et al., 1994). In this method, farmers are divided into small groups to monitor the crop and then each group analyses the field situation by identifying the key factors. Group members then decide whether any action is required. At a combined meeting, each group presents and defends its summary to the other trainees. The trainer facilitates by asking leading questions or adding technical information if necessary. This process allows farmers to integrate and practise their skills and knowledge and gives trainers an opportunity to evaluate the trainees’ ability. Thousands of farmers have been trained utilizing this approach and it is being tried on a pilot scale. A survey among these farmers during the first post-training season revealed that they really decreased their frequency of pesticide sprays to a level consistently lower than that of non-IPM farmers. The percentage of farmers not applying pesticides was also significantly higher among the trained farmers. In spite of lower pest-control expenditures, these farmers obtained higher yields than the non-IPM farmers. This programme has been extended to several other Asian countries and the evident advantages of the approach are a marked reduction in the use of pesticides, with measurable benefits to the environment (APO, 1996; Heinrichs, 1998; Ooi, 2000). Government support Both the national programmes of developing countries and the donor agencies must have a policy commitment to IPM in the context of national economic planning and agricultural development. The costs to developing countries of not bringing their policies in line


with the objectives of IPM are relatively greater than the costs to developed countries. National policies to promote IPM require close regulation at all stages related to the importation and/or manufacture, distribution, use and disposal of pesticides. In the case of pesticides that do not meet prescribed standards for safety, persistence, etc., import and manufacturing bans should be enacted. At a minimum, the conditions laid out by the FAO Code of Conduct on the Regulation, Distribution and Use of Pesticides should be adopted. Pesticide subsidies need to be eliminated in order to make IPM an attractive alternative. The funds thus saved may be utilized for the implementation of IPM. Funds may also be diverted from some of the current research programmes to IPMoriented plant-protection programmes. Additional monetary resources may be generated through cooperation with bilateral/ multilateral agencies willing to support such programmes (NRI, 1992). Legislative measures IPM is an information system and its adoption reduces pest-control costs. The alternative to IPM is the indiscriminate use of broad-spectrum synthetic organic pesticides. Unfortunately, while pesticide manufacturers and users (farmers) derive the full benefits from the use of these chemicals, they pass on the environmental and ecological costs of their use to the society as a whole. If they are made to bear the full cost of the use of these toxicants, they may find IPM a more economical and attractive alternative. This could be achieved by enforcing suitable legislative measures. Secondly, the success of an IPM programme in any geographical region depends upon its implementation by all the farmers in the area. Ideally, farmers may voluntarily adopt an IPM programme but some farmers may hold out. Such farmers, called ‘spoiler holdouts’, may impair the success of a programme by failing to adopt a necessary practice, thus causing damage to adjacent areas. This is especially important in the case of mobile pests. In addition, some farmers may free-ride and thus shift the costs of imple-

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 16


G.S. Dhaliwal et al.

menting and managing a programme to a group of participating farmers. To overcome ‘spoiler holdouts’ and ‘free riders’, it may be necessary to impose a programme upon an unwilling minority through suitable legislative measures (Tarlock, 1980). Improved institutional infrastructure IPM cannot be implemented unless there is a basic infrastructure for plant protection in a country. There is a need to develop and support national programme capabilities for onfarm testing and technology extrapolation. At the international level, the establishment of an IPM working group to coordinate and monitor the funding of IPM projects is bound to provide an impetus to the implementation of IPM. IPM is predominantly a knowledge technology, the use of which requires training of the many groups involved. There is currently little training material for most of these groups, including farmers, extension personnel and researchers. If IPM is to become the major approach for pest management in the developing world, this deficiency must be remedied urgently (NRI, 1992). Another aspect requiring greater attention is coordination of effort within and between countries (which is especially important with mobile insect species, such as the brown planthopper), between national research, training and implementation institutes/programmes, and among international development agencies. Lack of a reliable database has also hampered the progress of IPM programmes. A reliable source of accurate information on the status of crops and pests in farmers’ fields is necessary for many IPM activities. Most of the successful IPM programmes in both developed and developing countries have a reasonably accurate system of monitoring and evaluating various biological and environmental parameters in the agroecosystem. A reliable database on crop yield and pest losses is required for planning and resource allocation at the national and international level. Systems analysis has been used as a problem-diagnosis tool for IPM in developed-country cropping systems and may be used in developing countries as well.

Improved awareness Increased education and awareness regarding the objectives, techniques and impact of IPM programmes are required at all levels including policy makers, planners, farmers, consumers and the general public. The importance and benefits of pesticides are being overemphasized by a multibilliondollar industry utilizing the services of not only their salesmen but also agricultural scientists, administrators and planners. There is not yet a strong market in IPM information. Policy makers and planners need to be convinced that without IPM current agricultural production systems are not sustainable. Similarly, much important information that might induce a farmer to adopt IPM is not immediately observable and is therefore not sought by the farmer. A manufacturer has no incentive to recommend a programme that uses less pesticide or even selective pesticides that kill a limited range of pests (Tarlock, 1980). Consumer groups and the general public may also be able to support the implementation of IPM programmes by demanding residue-free commodities. There is now a distinct market for organically produced food and other products. For example, there is a major programme at Cornell University, USA, for pesticide-reduced produce. NGOs and consumer groups need to be strengthened in developing countries, so that there is a public-oriented movement for implementation of IPM.

Future Outlook Initially, IPM programmes evolved as a result of the pest problems caused by repeated and excessive use of pesticides and increasing cases of pest resistance to these chemicals. It is only during the past few years that the economic and social aspects of IPM have also received increasing attention (Fig. 1.3). It is now being increasingly recognized that modern agriculture cannot sustain the present productivity levels with the exclusive use of pesticides. Increasing pest problems and disruptions in agroecosystems can only be cor-

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 17

IPM: Retrospect and Prospect

Natural control

Ecological sustainability

Economic sustainability


Farmers’ practices

Social stability

Modern approaches

Fig. 1.3. Role of IPM in ecosystem stability (after Dhaliwal and Heinrichs,1998)

rected by use the of holistic pest-management programmes. If the environmental and social costs of pesticide use are taken into account, IPM appears to be a more attractive alternative with lower economic costs. The IPM programmes do not endanger non-target organisms, nor do they pollute the soil, water and air. IPM builds upon indigenous farming knowledge, treating traditional cultivation practices as components of location-specific IPM practices. This is especially important for farmers in developing countries, where traditional agricultural systems are based on indigenous farming practices. The incorporation of IPM into these practices helps the farmers to modernize while maintaining their cultural roots.


There needs to be a paradigm shift in the pest-management approach from managing components or individual organisms to an approach that examines processes, flows and interactions between populations of plants and populations of pest, beneficial and innocuous organisms (Dent, 1995; Hall, 1995; NRC, 1996; Kogan, 1998). There is a need for a better understanding of factors that affect ecosystem stability, the population dynamics of pests and the ability of populations to recover from stress. Technologies generated for the control of one group of pests, such as insects, diseases, weeds or nematodes, must be integrated in a crop-production system. There is a need to integrate the traditional practices of farmers with the advanced biological technologies now available in order to develop a profitable, safe and sustainable approach to pest management. It must be remembered that the success of any IPM programme will depend upon the effective transfer of technology to farmers. Therefore, the quick transfer, synthesis and simplification of information among farmers, suppliers of agricultural inputs and public agencies would speed up the successful development and implementation of IPM. Finally, the challenge to develop new technology, new management skills and new concepts of integration for pest management must be met so that we may protect our environment and provide a continuous supply of safe and nutritious food for the rapidly expanding world population.

References Alam, G. (2000) A Study of Biopesticides and Biofertilizers in Haryana, India. Gatekeeper Series No. 93, International Institute of Environment and Development, London. Allen, W.A. and Rajotte, E.G. (1990) The changing role of extension entomology in the IPM era. Annual Review of Entomology 25, 379–397. Altieri, M.A. (1995) Escaping the treadmill. Ceres 27, 15–23. APO (1996) Integrated Pest Management in Asia and the Pacific. Asian Productivity Organization, Tokyo, 170 pp. Baron, J.J. (2002) The role of reduced risk crop protection chemicals on the success of IPM in the US. In: International IPM Conference Exploring New Frontiers in Integrated Pest Management, 24–26 March, 2002, Toronto, Ontario, Canada, pp. 60–62. Benbrook, C.M. (2002) Measuring IPM adoption and the IPM continuum. In: International IPM Conference Exploring New Frontiers in Integrated Pest Management, 24–26 March, 2002, Toronto, Ontario, Canada, pp. 48–50. CEQ (1972) Integrated Pest Management. Council on Environmental Quality, Washington, DC, 41 pp.

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 18


G.S. Dhaliwal et al.

Chambers, R., Pacey, A. and Thrupp, L.A. (eds) (1991) Farmer First: Farmer Innovation and Agricultural Research. Intermediate Technology Publications, London. DeBach, P. (1964) Biological Control of Insect Pests and Weeds. Chapman & Hall, London. Dent, D. (1995) Integrated Pest Management. Chapman & Hall, London, 356 pp. Dhaliwal, G.S. and Arora, R. (eds) (1994a) Trends in Agricultural Insect Pest Management. Commonwealth Publishers, New Delhi, 547 pp. Dhaliwal, G.S. and Arora, R. (1994b) Components of insect pest management: a critique. In: Dhaliwal, G.S. and Arora, R. (eds) Trends in Agricultural Insect Pest Management. Commonwealth Publishers, New Delhi, pp. 1–55. Dhaliwal, G.S. and Arora, R. (2001) Integrated Pest Management: Concepts and Approaches. Kalyani Publishers, New Delhi, 427 pp. Dhaliwal, G.S. and Heinrichs, E.A. (eds) (1998) Critical Issues in Insect Pest Management. Commonwealth Publishers, New Delhi, 287 pp. Dhaliwal, G.S. and Singh, B. (2000) Pesticides and Environment. Commonwealth Publishers, New Delhi, 439 pp. Dhaliwal, G.S., Arora, R. and Heinrichs, E.A. (1998) Insect pest management: from traditional to sustainable approach. In: Dhaliwal, G.S. and Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management. Commonwealth Publishers, New Delhi, pp. 1–25. Eveleens, K.G. (2002) International IPM implementation and adoption: the Asian experience. In: International IPM Conference Exploring New Frontiers in integrated Pest Management, 24–26 March, 2002, Toronto, Canada, pp. 75–77. FAO (1967) Report of the First Session of the FAO Panel of Experts on Integrated Pest Control. Food and Agriculture Organization of the United Nations, Rome. FAO (1990) Mid-term Review of FAO Intercountry Program for the Development and Application of Integrated Pest Control in Rice in South and South-East Asia. Mission Report, Food and Agriculture Organization, Rome. FAO (1995) Intercountry Programme for the Development and Application of Integrated Pest Control in Rice in South and South-East Asia. FAO Plant Protection Service, Rome, Italy. FAO (2001) World Review of the State of Food and Agriculture. Food and Agriculture Organization of the United Nations, Rome, Italy, 295 pp. Frisbie, R.E. and Adkisson, P.C. (1985a) Integrated Pest Management on Major Agricultural Systems. Texas A&M University, College Station, Texas. Frisbie, R.E. and Adkisson, P.L. (1985b) IPM: definitions and current status in US agriculture. In: Hoy, M.A. and Herzog, D.C. (eds) Biological Control in Agricultural IPM Systems. Academic Press, Orlando, Florida, pp. 41–51. Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In: Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological Society of America, Lanham, Maryland, pp. 151–164. Geier, P.W. (1966) Management of insect pests. Annual Review of Entomology 11, 471–490. Geier, P.W. and Clark, L.R. (1961) An ecological approach to pest control. In: Proceedings of the Eighth Technical Meeting, 1960, Warsaw, Poland. International Union for Conservation of Nature and Natural Resources, Warsaw, pp. 10–18. Hall, R. (1995) Challenges and prospects of integrated pest management. In: Reuveni, R. (ed.) Novel Approaches to Integrated Pest Management. Lewis Publishers, Boca Raton, Florida, pp. 1–19. Haverskort, B., van der Kamp, J. and Waters-Bayer, A. (1991) Joining Farmers Experiments – Experiences in Participatory Technology Development. Intermediate Technology Publications, London. Heinrichs, E.A. (1998) IPM in the 21st century: challenges and opportunities. In: Dhaliwal, G.S. and Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management. Commonwealth Publishers, New Delhi, pp. 267–276. Hinrichsen, D. and Robey, B. (2000) Population and the Environment: the Global Challenge. Population Reports, Series M, No. 5, Johns Hopkins University School of Public Health, Baltimore, Maryland, 31 pp. Hoskins, W.M., Borden, A.D. and Michellbacher, A.E. (1939) Recommendations for a more discriminating use of insecticides. In: Proceedings of the 6th Pacific Science Congress, Vol. 5, pp. 119–123. Jiggins, J. (1996) Women and the re-making of civil society. Forest Trees and People Newsletter 30, 18–22. Kamp, K., Gregory, R. and Chowhan, G. (1993) Fish cutting pesticide use. LEISA 9, 22–23. Kenmore, P. (1997) A perspective on IPM. LEISA 13, 8–9.

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 19

IPM: Retrospect and Prospect


Kogan, M. (1998) Integrated pest management: historical perspectives and contemporary developments. Annual Review of Entomology 43, 243–270. Luckman, W.H. and Metcalf, R.L. (1994) The pest management concept. In: Metcalf, R.L. and Luckman, W.H. (eds) Introduction to Insect Pest Management. John Wiley & Sons, New York, pp. 1–34. McNeal, C.D. Jr (1988) Integrated pest management. In: Pesticides: Risks, Management, Alternatives. Virginia Water Resources Research Center, Blacksburg, Virginia, pp. 9–12. Matteson, P.C., Gallagher, K.D. and Kenmore, P.E. (1994) Extension of integrated pest management for planthoppers in Asian irrigated rice: empowering the user. In: Denno, R.F. and Perfect, T.J. (eds) Planthoppers: Their Ecology and Management. Chapman & Hall, London, pp. 656–685. Meerman, F., Bruinsma, W., Vanhuis, A. and Terweel, P. (1997) Integrated pest management: smallholders fight back with IPM. LEISA 13, 4–5. Metcalf, R.L. (1980) Changing role of insecticides in crop protection. Annual Review of Entomology 25, 215–226. Michelbacher, A.E. and Bacon, O.G. (1952) Walnut insect and spider mite control in Northern California. Journal of Economic Entomology 45, 1020–1027. NAS (1969) Principles of Plant and Animal Pest Control, Vol. 3. Insect Management and Control. National Academy of Sciences, Washington, DC. NDRC (1989) Intolerable Risk: Pesticides in Our Children’s Food. Natural Resource Defense Council, Washington, DC. NRC (1996) Ecologically Based Pest Management: New Solutions for a New Century. National Academy Press, Washington, DC, 144 pp. NRI (1992) Integrated Pest Management in Developing Countries: Experience and Prospects. National Resources Institute, Chatham, UK. Oerke, E.-C., Dehne, H.-W., Schonbeack, F. and Weber, A. (1994) Crop Production and Crop Protection. Elsevier Science, Amsterdam, 808 pp. Ooi, P.A.C. (2000) Present status of IPM in the Asian region. In: Farmer-led Integrated Pest Management. Asian Productivity Organization, Tokyo, pp. 21–29. Pedigo, L.P. (1991) Entomology and Pest Management. Macmillan, New York. Perkins, J.H. (1980) The quest for innovation in agricultural entomology. In: Pimentel, D. and Perkins, J.H. (eds) Pest Control: Cultural and Environmental Aspects. AAAS Selected Symposium 43, Westview Press, Boulder, Colorado, pp. 23–80. Pradhan, S. (1983) Agricultural Entomology and Pest Control. Indian Council of Agricultural Research, New Delhi. Quinghua, Z. (1995) Careful control: IPM in China. Ceres 27, 12–13. Rajak, R.L., Diurakar, M.C. and Mishra, M.P. (1997) National IPM programme in India. Pesticides Information 23, 23–26. Reichelderfer, K.H., Carlson, G.A. and Norton, G.A. (1984) Economic Guidelines for Crop Pest Control. FAO Plant Production and Protection Paper 58, Food and Agriculture Organization of the United Nations, Rome. Ruesink, W.G. and Onstad, D.W. (1994) Systems analysis and modelling in pest management. In: Metcalf, R.L. and Luckman, W.H. (eds) Introduction to Insect Pest Management. John Wiley & Sons, New York, pp. 393–420. Smith, R.F. (1978) History and complexity of integrated pest management. In: Smith, E.H. and Pimetel, D. (eds) Pest Control Strategies. Academic Press, New York, pp. 41–53. Smith, R.F. and Allen, W.W. (1954) Insect control and the balance of nature. Scientific American 190, 38–92. Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Kilgore, W.W. and Doutt, R.L. (eds) Pest Control: Biological, Physical and Selected Chemical Methods. Academic Press, New York, pp. 295–340. Smith, R.F., Apple, J.L. and Bottrell, D.G. (1976) The origins of integrated pest management concepts for agricultural crops. In: Apple, J.L. and Smith, R.F. (eds) Integrated Pest Management. Plenum Press, New York, pp. 1–16. Sorenson, A.A. (1994) Proceedings Integrated Pest Management Forum, Arlington, Virginia. American Farmland Trust, Dekalb, Illinois. Stern, V.M., Smith, R.F., van den Bosch, R. and Hagen, K.S. (1959) The integration of chemical and biological control of the spotted lucerne aphid. 1. The integrated control concept. Hilgardia 29, 81–101. Tarlock, A.D. (1980) Legal aspects of integrated pest management. In: Pimentel, D. and Perkins, J.H. (eds) Pest Control: Cultural and Environmental Aspects. AAAS Selected Symposium 43, Westview Press, Boulder, Colorado, pp. 217–236.

01IntpestManCh1.QXD 14/4/04 2:24 pm Page 20


G.S. Dhaliwal et al.

Van de Fliert, E. (1993) Integrated Pest Mangement: Farmers’ Field Schools Generate Sustainable Practices. Wageningen Agricultural University, Wageningen, The Netherlands. Van de Fliert, E. (1998) Integrated pest management: springboard to sustainable agriculture. In: Dhaliwal, G.S. and Heinrichs, E.A. (eds) Critical Issues in Insect Pest Management. Commonwealth Publishers, New Delhi, pp. 250–266. Van Veldhuizen, L. and Hiemstra, W. (1993) Cutting back: cure or prevent. ILEIA Newsletter 9, 3–4.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 21


Cultural Practices: Springboard to IPM

Waheed I. Bajwa and Marcos Kogan Department of Entomology and Integrated Plant Protection Center, Oregon State University, Corvallis, OR 97331, USA E-mail: [emailprotected]; [emailprotected]

Introduction Each agricultural region of the world grows a set of crops, the basic elements of agroecosystems, and uses unique technological procedures that in combination constitute the typical cropping system of the region. Cropping systems evolved under the pressure of the region’s prevalent agroecological conditions and the sociocultural and economic characteristics of its human population. Cropping systems range from extremely monotonous, such as the huge small-grain monocropping systems in the traditional bread baskets of the world, to the highly diversified mixed or intercropping systems that prevail in many subsistence agricultural production systems in the less developed countries of Central and South America, Africa and Asia. In the hierarchy of environmental forces that shape a regional cropping system, climate and soil must be at the top. Soil fertility and texture have shaped the nature of cropping systems throughout history, but current knowledge and availability of adequate amendments have allowed farmers to correct soil deficiencies in many parts of the world. Climate, however, is not amenable to large-scale correction; therefore, crop mixes available for local production systems are usually limited by climatic factors. For instance, apples, pears, cherries and other temperate-zone fruits cannot be

economically grown under tropical or subtropical conditions, and the reverse is true for tropical tree crops, such as citrus, coffee, pawpaw, cocoa and coconuts. Average annual temperatures and photoperiods are the key climatic factors. Where irrigation is not feasible, precipitation is another climatic determinant of cropping-systems evolution. Not far behind the climatic and edaphic conditions in shaping the nature of regional cropping systems are the pest complexes that attack the otherwise regionally adapted crops. Throughout the evolution of cropping systems, the presence of weeds, plant pathogens and arthropod pests has led to the adoption of procedures that in the aggregate are defined as cultural controls. Cultural controls, therefore, represent a fundamental integrated pest management (IPM) tactic even if the adoption of the practices, as driven by biotic factors of the environment, may remain unrecognized by growers. One of the dilemmas in maximizing the efficiency of cultural controls in IPM, however, is that seldom, if ever, are cropping systems optimized to cope with pest problems. Usually economic determinants take absolute precedence over all other factors. For a long time, maize-growers in the Midwestern USA knew that they could reduce the impact of rootworm, Diabrotica spp., attacks if they rotated maize with soybean. Continuous planting of maize, however, was more profitable for a

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


02IntpestManCh2.QXD 14/4/04 2:24 pm Page 22


W.I. Bajwa and M. Kogan

large segment of the grower population that raised pigs or dairy cattle. The economic consideration often prevailed over the IPM consideration. The main focus of cultural controls in IPM is to explore and enhance synergies of ecological processes that limit pest invasion and population growth in an agroecosystem. IPM systems are generally developed and implemented in a stepwise manner and the first step requires the full understanding of the cropping system that is targeted for management. Cultural-control approaches that best fit the nature of the cropping system form the foundation upon which the other IPM tactics will be implemented. Use of cultural practices for pest control is one of the oldest and most effective pest-management tactics. Cultural-control tactics are agronomic practices primarily aimed at the prevention and reduction of pest outbreaks by increasing pest mortality or reducing its rates of increase, dispersal and overall damage potential. At present, most successful IPM programmes for major annual and perennial crops are based on a combination of cultural control and biological control, coupled with moderate use of chemical pesticides. Under the label ‘cultural control’ are included cropping-systems practices related to the crop ecology with an impact on crop/ pest interactions and practices that have a physical or mechanical nature. Practices related to crop ecology include crop rotations, row spacing (for row crops), planting dates (for annual crops), inter- and mixed cropping, strip cropping and cover cropping, among others. Practices that have an effect on the pests because of direct physical or mechanical impact include ploughing, discharrowing, cultivating, burning, flooding and pruning, among others. So cultural controls operate either through physical forces that suppress or limit pest-population growth or by promoting conditions within the agroecosystem that are detrimental to the pest but favourable to its natural enemies. Therefore, conserving pests’ natural enemies and promoting their effectiveness are essential parts of cultural-control programmes. The appropriate use of cultural-control practices can reduce the damage potential to crops of

essentially all pests. Cultural control, when well planned and integrated into an IPM system, can provide economic control of many insect pests, plant pathogens and weeds and greatly reduce reliance on pesticides. The ecology of the crop, including the surrounding vegetation, determines the potential for the proliferation of pests and the complement of the pests’ natural enemies. In an optimal cropping system, producers strive to provide the best conditions for crop plants to express their yield potential and to create adverse conditions for the potential pests and the most favourable conditions for the pest’s natural enemies to flourish. Many stages in crop husbandry may provide such enhancements, and each of these stages should be considered in designing and implementing an IPM programme. It is possible often to identify underlying weaknesses in the ecosystem and in the prevailing agronomic practices that have allowed organisms to reach pest status. Identification of these weaknesses requires a thorough knowledge of the bionomics, behaviour and ecology of the pest in relation to the crop and its surroundings. Such knowledge is essential for developing alternative cultural practices that limit the potential of an organism to reach pest status. If these practices are cost-effective and can be integrated easily with other production practices, they are usually readily adopted by growers. In many parts of the world, good cultural-control methods have become stable farming practices that serve multiple purposes and help maintain agroecosystem sustainability. Agronomic practices may have a positive, negative or neutral impact on a pest and its natural enemies. Analysis of these impacts provides a basis for the development of cultural-control programmes. Cultural-control practices fall into three main categories: prevention, avoidance and suppression (Table 2.1). Individually or together, these practices improve the ability of a crop to withstand pest attack, make the crop less suitable for the pest or make it more suitable for natural enemies. Some of the practices involve many aspects of crop management, such as the use of pest-free seed, good sanitation and the

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 23

Cultural Practices


Table 2.1. Use of various cultural control practices for different categories of pests. Cultural control strategy/tactics
























Prevention/avoidance Clean seed and planting material Selection of well-adapted cultivars (including pest-resistant cultivars) Optimal crop nutrition Optimal water management (timing and proper amount of irrigation) General sanitation of farm equipment (cleaning of cultivating and harvesting equipment) Soil tillage Crop rotation Selection of planting and harvesting dates Trap crops Suppression Adjustment of seeding rates and optimal row spacing (optimal plant density and fast canopy closure) Cultivation or hand hoeing (mainly for weed suppression) Habitat management for natural-enemy enhancement (hedgerows, alternative crops, cover crops, mulches) Crop diversification/mixed cropping Soil tillage (reduction of seasonal carry-over) Destruction of alternative hosts and volunteer-crop plants

destruction of plant residue to limit the spread of pests; provision of optimum growing conditions to minimize stress on the crop; tillage practices that disrupt the insect’s life cycle and destroy crop residue; early or late planting and harvest dates to promote phenological asynchronies between the crop and the pests; and crop rotations that include non-susceptible crops. In addition, several specific practices fall under the concept of habitat management, where practices are implemented to render the crop environment less favourable for the pests or more favourable for the pests’ natural enemies. Intercropping, mixed cropping, hedge-vegetation management, trap cropping, cover cropping and certain other methods help divert pests from the main crop and promote the activities of beneficials (Landis et al., 2000). These practices are generally compatible among themselves and with other pestcontrol tactics within a comprehensive IPM







strategy and thus are highly desirable for the management of all pests. Variety selection is a key cultural practice and selection of resistant varieties is a major IPM tactic. Most texts on IPM, however, deal with host-plant resistance as a separate tactic, not under cultural controls.

Characteristics of Cultural-control Practices The following features characterize culturalcontrol practices within an IPM context: ● Cultural-control methods are simple modifications or adaptations of regular farm operations. The added cost of their incorporation into pest-management systems is minimal in most cases. They are often the only control measures economically feasible for low-value crops.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 24


W.I. Bajwa and M. Kogan

● Cultural-control practices generally produce no, or negligible, undesirable ecological consequences. ● Cultural control is primarily aimed at the prevention and reduction of pest outbreaks. Its effectiveness is dependent on long-term, careful planning. The objective is either to reduce pest numbers below economic injury levels or to keep pests at a level that allows natural or biological control to take effect. ● Results of cultural practices as applied to arthropods are often difficult to quantify, primarily because ecological relationships within crop systems are poorly understood and because baseline data on pest abundance in the absence of cultural controls are not available. The effects of physical methods for weed control and crop rotations for disease control are often dramatic and very well documented. ● Cultural-control tactics are an effective means of pest control. They do not result in total elimination of the pest, thus allowing for conservation of beneficial insects. In the USA biological control of musk thistle is an excellent example (Kok, 2001). ● Most cultural practices indirectly affect arthropod pests. They are relatively slow acting and thus cannot resolve a pest outbreak. They are important, however, in minimizing pest damage by preventing pest build-up, rather than relieving an already existing pest problem. ● Cultural-control methods make cropping systems less friendly to the establishment and proliferation of pest populations. While they are designed to have positive effects on farm ecology and pest management, negative impacts may also result due to variations in weather, changes in crop management or perturbations in agroecosystems. ● Timing is critical to the success of many cultural controls; accordingly, the implementation of cultural-control tactics requires thorough knowledge of pest ecology and its interaction with the cropping system. In designing cultural control, special attention is given to recognizing the ‘weak link’ in the pest’s

life cycle, pest–crop interactions or the ‘flaws’ in agronomic practice that have allowed organisms to reach pest status. ● An area-wide deployment of culturalcontrol practices is essential for the effectiveness of the practice in IPM. If deployed in only a small area, a mobile arthropod pest would merely move from surrounding areas; effective use of some of these practices requires cooperation among farmers within communities. ● Cultural-control methods are often pest-, crop- and region-specific. Care should be exercised in transferring tactics to a region with markedly different agroecological conditions.

Cultural Practices and Sustainable IPM Systems Optimizing plant health and the biological diversity of the farm system is the foundation of effective cultural controls. Healthy and vigorous crops are inherently tolerant of pests or their effects. Decreased biodiversity tends to result in unstable agroecosystems prone to recurrent pest outbreaks, reduced soil health and gradually declining productivity. Systems high in biodiversity tend to be more dynamically stable. Such systems provide more checks and balances to component species, thus helping prevent any given species from overwhelming the system. Most cultural-control tactics lower pest numbers in an ecosystem, and some may affect the carrying capacity of the ecosystem. These impacts tend to accumulate over time to produce sustained suppression of pest populations, keeping them below economic injury levels (Fig. 2.1). Cultural-control practices, therefore, must be a continuous component of an IPM programme so as to have a positive impact on all other practices by reducing overall levels of pest populations (MacHardy, 2000). Cultural controls tend to favour natural biological control directly by providing shelter and nectar for predators and parasitoids or indirectly by reducing insecticide use. It is the level and integration of both cultural and biological control that determine the

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 25

Cultural Practices

Pest population

Effect of cultural-practice changes on EIL


Time Fig. 2.1. Hypothetical effect of a change in cultural practices that lowers the general equilibrium position of a pest population, thus maintaining the population below the economic injury level (EIL).

nature and amount of other control actions to be taken at the farm level.


Cultural-control Practices Table 2.1 lists the major cultural practices most commonly recommended for the control of weeds, plant pathogens and arthropods. These are discussed in some detail in the following sections. Comprehensive reviews of the major cultural-control methods are available in the literature. Variety selection and preference for adapted cultivars that incorporate resistance to arthropods and diseases are key components of the decision-making process in crop management. Host-plant resistance, however, is such an important component of IPM systems that it deserves special treatment in most texts. Detailed discussions of both traditional and genetically engineered plant resistance are offered in Chapters 6 and 7.


Cultural-control Practices and Contemporary Production Systems The introduction of the concept of IPM in the late 1960s shifted the emphasis in pest control from a single-tactic, chemically based to a multitactic, ecologically based or biointensive system (Frisbie and Smith, 1991). Since the early days of IPM, cultural controls have been considered a first line of defence in many pest-management systems. Cultural practices alone may not give completely satisfactory pest control but, within an IPM system, they provide the matrix upon which other IPM tactics are deployed and often help reduce dependency on chemical pesticides (MacHardy, 2000). Ecologically based production systems, including organic farming (Brumfield and Ogier, 2000), total-habitat management (Prokopy, 1994; Kogan and Bajwa, 2001) and integrated fruit and crop production (Sansavini, 1997), take maximum advantage of farming practices that promote plant health and pests’ natural controls and allow crops to escape or tolerate pest injury. Cultural control is a cornerstone for most biointensive IPM programmes, where each component complements and often augments the effects of others (ecological synergism) (Fig. 2.2).

Sanitation involves removing and destroying overwintering sites, breeding refuges of arthropod pests and substrates for pathogen inoculum. Sanitation also prevents new pests from becoming established on the farm. This cultural-control method has been particularly useful for horticultural and tree-fruit crops. Fruit, twig and branch as well as rootcrop pests can be affected by carefully conceived sanitation procedures. The most common means of field sanitation is destruction of crop residues by shredding and ploughing, separately or in combination. This process not only kills some pests directly but also speeds up natural rotting of the residues thus removing them as food or shelter source. Removing crop residues can reduce the carry-over of pests from one season to the next. After harvest, destroying the stubble of cotton, maize and sugarcane is an important measure in the control of cotton bollworm, boll-weevil and pink bollworm in cotton, various corn borers and sugarcane borers (All, 1999). The practice of grazing by livestock of cotton fields after last picking is effective in reducing hibernating loads of pink bollworm and American bollworm in many regions (Bajwa, 1988). In the USA,

02IntpestManCh2.QXD 5/5/04 2:30 pm Page 26

W.I. Bajwa and M. Kogan

Control tactics

Chemointensive crop protection


Chemical control (nonselective)




Biological/ natural control


Cultural control/ plant resistance

Negative environmental impacts







Biointensive crop protection (IPM) Fig. 2.2. Graphic representation of two opposing strategies of pest control. Triangle at left: biointensive pest control system (= IPM). These systems are integrative, stable and environmentally benign, with little reliance on broad-spectrum pesticides. The contribution of each control tactic to the stability of the system is represented as a proportion of the area of the triangle sector (or trapezoid) corresponding to that tactic. The various tactics complement and often potentiate each other (ecological synergism). Triangle at the right: chemointensive pest-control systems, on the other hand, are unstable (the ecological base is weak); control methods other than pesticides are not emphasized or their effects are masked by the antagonistic effects of chemical pesticides.

sheep grazing wheat stubble during the autumn and autumn/spring gave an effective control of wheat-stem sawfly, Cephus cinctus Norton (Hatfield et al., 1999). In rice, destroying stubble and off-season sprouts reduces populations of the leafhopper, Nephotettix impicticeps Ishihara, and the whitebacked planthopper, Sogatella furcifera (Horvath) (Bajwa, 1988). In sugarcane and maize, destruction of cane trash and maize stalks in the winter significantly reduces the hibernating loads of several stem borers (Capinera, 2001). Removal of fallen fruit from orchards and destruction of tree prunings are useful in reducing insect pests and plant-disease agents that overwinter in these materials. Destruction of prunings can control the

peach borer, Synanthedon exitiosa (Say), and the lesser peach borer, Synanthedon pictipes (Grote and Robinson) (Cox and Atkins, 1964). Collecting and using dropped fruit or else destroying them reduces the populations of some important direct pests, such as plum curculio, Conotrachelus nenuphar (Herbst) (All, 1999), the codling moth, Cydia pomonella (Linnaeus) (Prokopy, 2001), the false codling moth, Cryptophlebia leucotreta (Meyrick), and many species of fruit flies (Bajwa, 1989; Stoll, 2000). Other sanitation techniques include using pest-free seeds or transplants and decontaminating equipment, animals and other sources of food and shelter. Insects in cuttings or roots used in the vegetative propagation of crops can initiate infestations.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 27

Cultural Practices

Seeding equipment should be clean and free of pests. Ideally, all farm machines should be cleaned before going from one field to another. Such procedures are essential to prevent the spread of soil-inhabiting pests, such as the grape phylloxera in vineyards of California and Oregon, in the USA (Hellman and Watson, 2000). In the tropics, the use of clean planting material reduces banana weevil, Cosmopolites sordidus (Germar), infestation by up to 80% (Stoll, 2000).

Soil tillage While tillage may be a part of field sanitation, it can be an effective direct means of pest control by itself. Tilling the soil destroys life-cycle stages that occur in the soil or in crop residues. It destroys pests by mechanical action, starvation through debris destruction, desiccation and exposure to predators or adverse environmental conditions. Tillage may modify the soil microclimate, which will influence pest behaviour and plant growth. Often tillage timing and depth are the major considerations for the management of soil-inhabiting animal pests and critical factors in weed management. Timing is usually determined when pests are in an immobile stage (pupation or dormancy), and depth is recommended by the location of this stage in soil. Generally, tillage may be conducted in the autumn or early winter and in the spring before planting. Soil-inhabiting pests such as rootworms, white grubs, wireworms and the overwintering larvae and pupae of Lepidoptera and Coleoptera may be exposed to desiccation or bird predation by ploughing. The pests that feed on stubble after harvest may starve if the ground is tilled (Speight et al., 1999). Deep ploughing after harvest buries infested plant parts and stubble and destroys the larvae of pests such as army worm, Pseudaletia unipunctata (Harworth) (Capinera, 2001); wheat-stem sawfly, C. cinctus; maize earworm, Helicoverpa zea (Boddie); European corn borer, Ostrinia nubilalis (Hübner); soybean stem borer, Dectes texanus LeConte; grape berry moth, Endopiza viteana Clemens (Herzog and Funderburk, 1986); rice stem


borers, Tryporyza incertulas (Walker) and Chilo suppressalis (Walker); and cotton bollworms, Pectinophora gossypiella (Saunders) and Earias insulana (Boisduval) (Bajwa, 1988). In the case of the European corn borer, the ploughing of stubble may result in a 90% reduction of hibernating larvae (Horn, 1988). Shallow autumn tillage may provide up to 90% sawfly control (Steffey et al., 1992). If only spring tillage operations are performed, approximately 25% of larvae may be destroyed, depending upon the tillage implements used (Steffey et al., 1992). Reduced- or conservation-tillage practices may increase soil surface residues. These residues may have an impact on populations of certain pests. The presence of such residues repels the colonizing of a field by greenbugs, Schizaphis graminum (Rondani) in wheat and sorghum (Burton et al., 1987), but attracts black cutworms in maize (Steffey et al., 1992). Greenbugs prefer fields with more bare ground visible, while black cutworm prefers crop residue for oviposition. Reducedtillage systems may have higher soil moisture and be slower to warm up in the spring, thus reducing crop growth. This may add to damage from soil pests (wireworms, white grubs and other seed and seedling pests) by increasing their feeding time on young plants (Steffey et al., 1992). Biological control agents are often affected by tillage practices. Discing or harrowing has fewer negative impacts on the parasitoid population than does ploughing (Herzog and Funderburk, 1986). Parasitoids of the cereal leaf beetle, Oulema melanopus (Linnaeus), can be severely affected by tillage operations, which has little effect on the pest (Pedigo, 2002). Reduced-tillage systems may increase populations of various predatory arthropods by increasing populations of their prey, such as other insects, mites and organisms that feed on decaying organic matter. Increased levels of predatory insects and predation on black cutworms, Agrotis ipsilon (Hufnagel), and maize earworm, H. zea, have been observed in reduced-tillage systems (Stinner and House, 1990). Tillage is not always advantageous and can actually aggravate some pest problems.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 28


W.I. Bajwa and M. Kogan

For example, in some areas the soil surface tends to form a crust; keeping this crust intact can inhibit weed germination and/or prevent the penetration of soil-inhabiting pests (Norris et al., 2003). Serious side effects of tillage are loss of organic matter, especially in warm soils, and accelerated loss of soil to wind and water erosion if the soil is left bare for an extended period.

(Lidell and Schuster, 1990); potato tuberworm, Phthorimaea operculella (Zeller); potato aphid, Macrosiphum euphorbiae (Thomas) (Capinera, 2001); cutworms, Agrotis spp. (van den Berg et al., 1998); and the wheat curl mite, Eriophyes tosichella (Keifer) (Buntin et al., 1991).

Maintaining and improving plant health Management of alternative hosts Eliminating plants that can serve as alternative hosts when the crop is not present can suppress overwintering populations and reduce the growth rate of many pest populations. Vegetation serving as the alternative host may occur within the crop field and/or in surrounding areas. Whiteflies use many broad-leaved weeds as alternative hosts when suitable crops are not present (Norris et al., 2003). Johnson grass is an excellent host of sorghum midge (Pedigo, 2002). Significant reductions of these pests have been reported where weed destruction by burning and other means was used. Many vegetable pests, such as squash- and stinkbugs, overwinter in crop debris and plant cover at the edge of plantings. Elimination of these hibernating habitats can significantly reduce infestations in squash, beans, cabbage and other vegetables (Capinera, 2001). Destruction of alternative hosts may also require careful scrutiny as it may eliminate an important habitat for beneficial insects. Volunteer plants of a crop that remain in parts of a field after harvest may be a potential source of pest carry-over. These plants may harbour a large number of insect pests at times when pest presence would otherwise be impossible. The destruction of these volunteer plants is particularly important when crop rotation is practised to eliminate pests. For example, volunteer maize in soybean fields should be removed to prevent maize rootworm adults, Diabrotica spp., from laying eggs and producing larvae that would colonize maize the following season (Goodwin, 1985). Destruction of volunteer plants is also recommended for the suppression of other pests, such as Hessian fly

The primary goal of agricultural production is to maximize the yield of high-quality produce. Healthy plants are essential for optimal agricultural production. Stressed plants, including those with nutritionally induced low vigour, are often more susceptible to pest attack (Stoll, 1988). Vigorous plants are better able to tolerate pests, as well as producing high yields. In most crops, yield losses to a given degree of pest injury vary considerably depending on the vigour of the plants. However, there are documented instances of modern fertilizers and irrigation increasing vulnerability to certain pests (discussed below). Excessive nutrients (particularly nitrogen) and relative nutrient balance (ratios of nutrients) in soils affect the pest response to plants. Imbalances in the soil can make a plant more attractive to insect pests, less able to recover from pest damage or more susceptible to secondary infections by plant pathogens (Daane et al., 1995; Phelan, 1997). Cultural practices, such as proper irrigation and drainage, fertilization, row spacing and weed control, significantly influence the vigour of the crop and consequently the amount of pest damage. Undernourished plants, because of their pale or yellowish appearance, are often more attractive to colonizing aphids (Ferro, 1996). In some instances, however, the vigorous growth of plants may attract or enhance the development of many pest species. For example, leafhoppers and Spodoptera littoralis (Boisduval) have been most abundant on rice fertilized with high rates of nitrogen (Stoll, 2000). Excessive nitrogen may increase the incidence of Tetranychus mites (Stoll, 2000), fungal diseases and sucking insects (Flint and Gouveia, 2001) on an array of crops.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 29

Cultural Practices

Succulent cotton growth attracts higher populations of the cotton aphid, Aphis gossypii (Glover), cotton fleahopper, Pseudatamoscelis seriatus (Reuter), and cotton bollworm, H. zea (Herzog and Funderburk, 1986). Increasing levels of soil fertility delay crop maturity in cotton, thereby reducing the potential for escape from pest injury (Anon., 1996). Increases in soil fertility of wheat result in increased wheat-stem sawfly injury due to the preference of ovipositing females for large succulent wheat plants (Morrill and Kushnak, 1996). Good soils can improve yields and produce robust crops that are less vulnerable to pests. Soils used for years of continuous farming often require heavy fertilizer application to produce high yields. Soil quality can be maintained and enhanced in many ways, including incorporation of animal waste (manure), living plants or plant debris (compost). The addition of organic matter to soil is known to result in the suppression of a wide range of soil-borne plant pathogens (Cook and Baker, 1983). Application of manure to maize fields increases the predatory efficiency of mesostigmatid mites on maize rootworm larvae (Allee and Davis, 1996). Water management can be used to grow more vigorous plants and thereby reduce losses. Excessive irrigation or frequent irrigations may favour the spread and development of many diseases and should be avoided. Cotton is severely stressed by inadequate irrigation, but excessive water may result in overly lush plants with higher insect densities and increased vulnerability to pest damage (Horn, 1988). Winter irrigation may reduce populations of overwintering pink bollworms by up to 50–70% (Bariola, 1983; Beasley, 1992). Cotton bollworms are attracted to succulent, rank-growing cotton plants; therefore, keeping water, fertilizer and plant density at recommended levels is important in order to avoid rank growth (Anon., 1999). Sprinkler irrigation has been effective in suppressing certain foliage-feeding insects by a washing and drowning action. The diamondback moth, Plutella xylostella (Linnaeus), and codling moth, C. pomonella, are effectively sup-


pressed by frequent overhead irrigation of potatoes, head cabbage (McHugh and Foster, 1995) and apple trees (Knight, 1998), respectively. In California, sprinkler irrigation has been observed to suppress spider mites (Flint and Gouveia, 2001). Flooding is frequently used to reduce populations of sugarcane (Cherry, 1987; Deren et al., 1993) and vegetable pests (Capinera, 2001). Paddy rice in the Orient has a complex biota (Kiritani, 2000). The biological impact of flooding in the rice paddy is a critical factor in the economic production of rice in vast regions of the world. Nevertheless, effective use of this technique depends on factors such as flood susceptibility and the stage of the pest species, the duration of flooding, water temperature and, perhaps more importantly, the availability and cost of water.

Timing of planting and harvest (disrupting crop–pest phenological synchrony) Plant phenology can be manipulated to disrupt synchronization with the phenology of the major pests. It is sometimes possible to alter the timing of crop development by modifying regular cultural practices and thus to effect a substantial reduction in damage. This can be achieved by modifying planting time, by either delaying or advancing planting dates. In some cases, earlyplanted crops are less likely to suffer from pest outbreaks as they become well established before pests appear. They are either less palatable to herbivores or tolerant of higher pest densities without suffering much effect on yield. Early harvest often produces phenological asynchronies capable of disrupting a pest’s life cycle, allowing harvest of the crop before the damaging state occurs. Planting early-maturing varieties often allows fields to escape infestations by lateseason pests. Early-planted maize is far less susceptible to maize earworm and stem borer, Diatraea grandiosella Dyar, damage than late-planted crops. The female D. grandiosella tends to lay fewer eggs on more mature plants and the plants have already passed their critical growth stage before significant numbers of

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 30


W.I. Bajwa and M. Kogan

larvae begin to feed (Herzog and Funderburk, 1986). In addition, earlyplanted maize can be harvested before many fully grown pre-diapause larvae have girdled the mature plants and caused yield losses through lodging of the plants (Roth et al., 1995). The early planting of maize in East Africa is known to reduce problems with both maize leafhopper, Cicadulina mbila (Naude), and stalk borer, Papaipema nebris (Guenee) (Bajwa and Schaefers, 1998). The practice is so effective that no additional control measures are generally needed. Earlierplanted tomatoes in the western USA are far less likely to be infested by the tomato fruitworm, H. zea, than those planted later in the season (Anon., 1998). Early-season varieties of cotton avoid most boll-weevil and bollworm populations, and early-maturing soybean cultivars sufficiently evade bean-leaf beetles compared with standard varieties (Horn, 1988). Early-planted groundnuts avoid aphid damage in tropical Africa (Bajwa and Schaefers, 1998). Early planting of rice reduces or eliminates many insectrelated problems (Speight et al., 1999). This effect may not be a general rule for all pests and ecological situations. Early rice transplanting in South Korea may increase populations of striped rice borer, C. suppressalis (Ma and Lee, 1996). Late planting of soybean interferes with the colonization patterns of the soybean thrips that are vectors of the bud-blight virus (Kogan et al., 1999). Late planting of wheat has been used for a long time to manage Hessian flies. Adult Hessian flies have a very short lifespan (3–4 days) and oviposition occurs over a limited span of time during early autumn. If planting is delayed so that most of the flies have died before the wheat emerges, damaging infestations may be avoided. In regions where Hessian flies are a problem, fly-free dates have been established to guide autumn planting of wheat, based on the seasonal occurrence of the adults (Dufour, 2001). In situations in which migrant rather than resident populations are the major source of infestation, crop planting should be delayed until any major pest migration is over. Damage to sugarbeets by curly-top virus can be avoided or reduced by

planting the crop after the spring migration of the beet leafhopper, a vector for the disease (Norris et al., 2003). Sometimes, it is possible to reduce pest populations or their damage by adjusting harvest time. As a general rule, crops should be harvested at the earliest possible date. Early harvesting of sorghum removes a large proportion of stem-borer populations; therefore, the crop should generally be harvested immediately after it attains physiological maturity (Omolo and Reddy, 1983). In lucerne, damage from the potato leafhopper, Empoasca fabae (Harris) and lucerne weevil, Hypera postica (Gyllenhal), can be minimized by early clipping at the early bloom or late bud stage (Steffy et al., 1994). The lack of food, and hot, dry conditions after harvest can cause considerable mortality to the leafhopper and weevil larvae. Early planting reduces the loss of yield from maize ears that drop early because of European corn-borer tunnelling. However, early-harvested maize usually has a higher moisture content and must be dried before it is stored. Early sweet potato planting and harvesting is useful in white-fringed beetle, Naupactus spp., management programmes. These pests cause damage to roots late in the season, therefore, harvesting the crop before larvae reach sufficient size to cause serious feeding damage reduces the proportion of damaged and unmarketable roots at harvest (Zehnder et al., 1998).

Crop rotation (increasing and maintaining temporal diversity) Crop rotation means growing different crops in succession in the same field. It is especially effective against host-specific pests. Crop rotation drastically changes the environment, both above and below ground, usually to the disadvantage of pests of the previous crop. The same crop grown year after year on the same field will inevitably build up populations of organisms that feed on that plant or have a life cycle similar to that of the crop. It is important that the crops in a rotation system are genetically distant (belonging to different plant families) so that

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 31

Cultural Practices

they do not have common pests. The focus is on either selecting rotations detrimental to certain pest species or avoiding rotations known to favour the pests. Crop rotation works by disrupting normal life cycles of pests by placing them in a non-host habitat (crop). It reduces pest pressure on all crops in the rotation by breaking the pest reproductive cycles. This practice seldom has any economic or ecological disadvantage; therefore, it is widely used even when crop damage is anticipated to be minimal (Herzog and Funderburk, 1986). Crop rotation is generally compatible with biological controls and forms the basis for IPM systems for many crops. Most common rotations include grass, legume and root crops. A leguminous crop in rotation generally replenishes plant nutrients, particularly nitrogen, thereby reducing the rates of needed chemical fertilizers. Also, rotation reduces the chance of pesticide build-up in the environment, thus decreasing the threat of pest resistance to pesticides (Reeves, 1994). Rotations that increase organic matter improve the environment for biological activity, which will increase the breakdown of pesticides. Crop rotation is one of the oldest and most important measures for the control of pests that overwinter in the soil as eggs or partially grown larvae. It has been successfully used against many soil pests, including arthropods, plant-parasitic nematodes, fungal pathogens and bacterial pathogens. It is most effective against arthropod pests with a restricted plant-host range, long generation cycle (1 year or longer) and limited dispersal capability. Host selectivity may occur through either ovipositional or feeding behaviour. Numerous species of major soil pests are successfully controlled by crop rotation. For example, the white-fringed weevil complex has limited dispersal capacity as the adult is unable to fly (Zehnder, 1997). These species are highly prolific on legumes; however, grasses, including maize, are in some way nutritionally deficient for supporting their feeding (Ferro, 1996). These pests cause no or low damage to grasses, but leguminous crops, soybean and groundnuts may suffer heavy losses. A soybean/maize rotation can


therefore provide an excellent control, both effective and economical. Rotating potatoes with lucerne reduces wireworm damage, and rotating oats and maize reduces maize rootworm damage. Maize rootworms, Diabrotica longicornis Say and Diabrotica virgifera Le Conte, in the Midwestern USA have been effectively controlled by a 2-year rotation of maize with soybeans. Unfortunately, this tactic has been compromised in some areas where the rootworms have developed strains that can diapause for more than 1 year (Levine and Oloumi-Sadeghi, 1991). Crop rotation may impose some limitations. Some crops used in rotation are of such low value that they contribute little to farm income. Also, an incorrect choice of crop sequence in a rotation can result in an elevated insect problem. For example, wireworms are more severe in potatoes following red clover or sweet clover (Norris et al., 2003).

Interplanting or multiple cropping systems (maintaining and improving spatial diversity) Multiple cropping or polyculture is typical of traditional farming systems in most developing countries. At present, there is insufficient experimental evidence that multiple cropping has a positive effect for pest management, although Altieri (1987, 1991, 1994), Wratten and van Emden (1995), Landis et al. (2000) and others provide abundant observational evidence that the inherent increase in biodiversity of multiple cropping systems increases the quality and quantity of the natural enemy fauna. The advantage of multiple cropping systems for IPM is postulated on the principle of habitat diversification. Monocultures inherently lack biodiversity as they are simplified and unstable agroecosystems, frequently prone to recurrent pest outbreaks that demand constant human intervention. Systems high in biodiversity tend to be more ‘dynamically stable’ because the variety of organisms provides more checks and balances on each other, thus helping prevent one species (i.e. pest species) from overwhelming the system. In IPM, biodiversity may create stability (but not

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 32


W.I. Bajwa and M. Kogan

always) within a crop season if employed as an area-wide approach. When applied to single fields, the approach may fail due to movement of pest organisms from adjacent fields. Monocultures open the way to pest infestations by providing concentrated resources and uniform physical conditions that promote pest invasions (Altieri, 1987). In these environments, the abundance and effectiveness of natural enemies are reduced because of inadequate alternative sources of food, shelter, breeding sites and other environmental factors. Increasing crop diversity, on the other hand, may be used to augment predator and parasitoid populations or to impair herbivores’ ability to find and utilize their host plants. In multiple cropping systems certain plants may deter pests and reduce food supply for pests, while attracting and increasing an abundance of natural enemies. Pest levels are thus expected to be lower in polycultures. Spatial arrangements used in multiple cropping are variations of row intercropping and strip cropping. Row intercropping is a system in which two or more crops are simultaneously planted in rows across a single field. The use of this practice as a strategy for weed control should be approached carefully. Intercropping may result in reduced yields of the main crop if competition for water or nutrients occurs. On the positive side, infestations of armyworm, Spodoptera frugipereda (J.E. Smith), in maize and Empoasca spp. (leafhoppers) and Diabrotica spp. (leaf beetles) in beans can be greatly reduced by interplanting the two crops (Altieri, 1987). Intercropping of soybean and maize increases the rate of parasitism by Trichogramma spp. (Altieri et al., 1981). In Africa, intercropping of cereal crops (mainly maize and sorghum) with the non-host molasses grass, Melinis minutiflora (Beauv.), reduces infestation by stem borers, Busseola fusca Fuller and Chilo partellus (Swinhoe), in the main crop and also increases larval parasitism by Cotesia sesamiae (Cameron) (Khan et al., 1997). Strip cropping is the practice of growing two or more crops in different strips (usually four or more rows per strip) across a field wide enough for independent cultivation.

For example, a scheme of alternating six-row blocks of soybean and maize or alternating strips of lucerne and cotton or lucerne and maize may reduce pest problems. Strip cropping may result in a more balanced insect population with an increase in beneficial insects. An example is interplanting strips of lucerne in cotton for the control of lygus bugs, which prefer and will concentrate in the strips of uncut lucerne, leaving the cotton undamaged (Godfrey and Leigh, 1994). The lucerne may be harvested later as a forage crop. In mixed-crop stands, it may be more difficult for pests to locate their host by either physical (visual clues) or chemical means (plant odours from non-host plants confuse feeding stimuli) (Bajwa and Shaefers, 1998). For example, thrips and whiteflies are attracted to green plants with a brown (soil) background, avoiding areas with full vegetation cover, such as a main crop and a cover crop between rows (Sullivan, 2001). Some intercrops have a spatial arrangement that produces the full vegetation cover that would be unfavourable for thrips and whiteflies. Other insects recognize their host plant by smell. Onions planted with carrots mask the smell of carrots from carrot flies (Sullivan, 2001). Besides the potential IPM benefits, multiple cropping may also protect farmers against the risks of crop failure; if one crop within the system fails, the other may survive and compensate in yield to some extent, allowing the farmer an acceptable harvest. Despite all its potential benefits, much more research is needed on the complex interactions between various paired crops and their pest/predator complexes before the method will be widely accepted to replace large-scale monocultures. A major drawback of multiple cropping is the difficulty in mechanized planting, cultivating and harvesting.

Trap crops Trap cropping is the practice of attracting pests to small plantings in or around a main crop or to an early planting of a crop on a

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 33

Cultural Practices

small area. Trap crops are generally more favourable hosts for the target pest than the main crop. If a trap crop is maintained in a vigorous state, the pest may never leave the trap crop. If the pest population builds up and begins to leave, the trap crop can be mowed or sprayed to prevent damage to the main crop. This action does not affect the activities of beneficial species in the main crop. In many instances, trap crops can also serve as refugia or additional reservoirs for beneficial predators and parasitoids in the event that the adjacent crop field is treated. Trap crops or trap plants have been in use against many insect pests, nematodes and plant pathogens. In beans, trap cropping can considerably reduce damage to Mexican bean beetle, Epilachna varivestis (Mulsant), and the bean leaf beetle, Cerotoma trifurcata (Forster). Early-maturing varieties can be planted 2 weeks prior to the main soybean crop. The adult beetles are attracted to these early-maturing trap crops and are then destroyed by cultivation or sprayed with an insecticide (Newsom and Herzog, 1977). Early-planted potatoes may act as a trap crop for Colorado potato beetles emerging in the spring (Hokkanen, 1991). Since the early potatoes are the only food source available, the beetles will assemble on these plants, where they can be controlled more easily. In Finland, mixed stands of trap plants (Chinese cabbage, oilseed and turnip rape, sunflower and marigold) near the main cauliflower plantings have been used for trapping the rape-blossom beetle, Meligethes viridescens (Fabricius). This beetle often ravages up to one-third of the whole harvest. As the beetle is highly mobile, several strips of trap plants are grown in the anticipated direction of infestation. Appropriately timed insecticide applications for trap cropping control the beetle and prevent its spread to the cauliflower plants. The technique has proved to increase by approximately 20% the marketable yield of the crop (Hokkanen, 1991). While some of these techniques still rely on insecticidal control, the area treated is greatly reduced (Hokkanen, 1991). A possible limitation of trap cropping is the expense of producing and destroying a crop that brings no income. Nevertheless, in


the southern USA and Hawaii, melon fields with small plantings of squash on the perimeter typically do not require insecticides. The practice reduces production costs for the main crop, conserves natural enemies and decreases the risk of secondary pest outbreaks. In this case, the squash trap crop enhances sustainability for the producer as a value-added crop. Sales of squash offset costs of the seed and pesticide and still provide additional income (Suszkiw, 1997).

Non-crop vegetation manipulation Vegetation manipulation in agroecosystems and their surroundings is an important practice used to enhance beneficial arthropods in agricultural crops. For example, an orchard ground cover, if properly maintained, promotes the build-up of natural enemies of certain pests (USDA, 1998). Recently, several studies have demonstrated the potential for establishing flowering plants in or around farm fields to attract natural enemies and enhance biological control in the adjacent field (Altieri and Nicholls, 2000). In Europe, windbreaks and hedgerows have been used to encourage the build-up of natural enemies. Flowering strips on uncultivated field margins can encourage the build-up of syrphid fly and parasitoid populations, but plant age and composition appear to be important (Altieri and Nicholls, 2000). Unfortunately, the effectiveness of this practice is generally limited to areas of the crop close to the flowering strips (Alford, 2000). Modifying the wild vegetation surrounding crop fields and orchards may favour a natural balance between pest arthropods and their enemies (Rieux et al., 1999). The technique is still in its early stages of development, but research in progress should help ascertain the role of the local flora and promising new plant introductions in and around agricultural fields. This research should help to clarify both the potential of the non-crop vegetation benefit as sources of natural enemies and the risk of harbouring phytophagous arthropods shared with the crops. Cover crops are non-crop plant species grown either concurrently with the host crop

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 34


W.I. Bajwa and M. Kogan

(usually perennial plants) or in rotation with annual crops; they are generally not harvested. Examples include the establishment of pure or mixed stands of legumes and cereals to protect the soil against erosion. This technique ameliorates soil structure, enhances soil fertility and may help suppress certain weeds, arthropod pests and pathogens. Cover crops affect the ecology of orchards and vineyards by improving soil biology and fertility and by increasing biological control of insect pests by harbouring predators and parasitoids (Altieri and Nicholls, 2000). Cover crops attract and provide a nectar source for beneficial insects, spiders and mites.

Miscellaneous cultural-control practices Increased plant density may sometimes be useful, but can add to production costs. Damage to seedlings by soil pests, such as cutworms, can sometimes be compensated for by higher seeding rates. Reducing row spacing causes the canopy to close early and improves conditions for predator colonization in many crops. Narrow row spacing in soybean decreases ovipositional preference of maize earworm moths as they prefer to oviposit in open-canopy fields. In contrast, damage to maize by larvae of the Diabrotica undecimpunctata Mannerheim borer decreases as plant density increases or when broad-leaved weeds are present rather than bare soil (Speight et al., 1999). Planting of wheat at high densities and in narrow rows decreases moisture in stems, stem diameter and plant height. The wheat sawfly, C. cinctus, prefers larger, more succulent plants for oviposition, and damage to wheat decreases as seeding density increases and row spacing decreases (Herzog and Funderburk, 1986). Mulches – natural or synthetic soil coverings – are useful for the suppression of weeds, insect pests and some plant diseases. A mulch can reduce the spread of soil-borne plant pathogens by preventing their transmission through soil splash. Winged aphids are repelled by reflective mulches (silver- or aluminium-coloured). Hay and straw mulches are more habitable than bare ground to some

spider species and can reduce considerable damage to vegetable crops by insect pests (Reichert and Bishop, 1990). Living mulches of various clovers reduce insect-pest damage to vegetables and orchard crops (Bugg et al., 1990) by providing essential resources for natural enemies. In some cases, mulching may provide a favourable environment for slugs and snails, which can be particularly damaging at the seedling stage.

Conclusions Pest managers, in general, must learn to adjust the use of cultural controls to the features and properties of extant cropping systems. Powerful ecological, economic, cultural and social pressures have shaped the predominant cropping systems in most parts of the world. For example, as a consequence of the 1973 oil crisis, Brazil launched a vigorous campaign to promote the use of sugarcanederived ethanol as a petrol substitute. Government subsidies and other incentives led growers in the state of São Paulo to replace a diverse agriculture that included some of the staples for low-income populations, such as rice and beans, with sugarcane plantations. In some areas, huge new monocrops became established almost overnight, covering millions of hectares. As expected, pest problems were aggravated and treated with an array of broad-spectrum pesticides. Industry and government gave little or no consideration to the resulting pest impacts of this shift of cropping systems until after the fact. Thus, pest pressure is but one of the ecological forces that have influenced the evolution of cropping systems as they exist at present. Among the agricultural pests, weeds, more than either arthropod pests or pathogens, have influenced the development of cropping systems. Row spacing is adjusted for ease of cultivation. Vegetation management to enhance the natural enemies of arthropod pests and the use of cover crops are often disregarded by growers for fear that these techniques may make weed control more difficult. Certain rotations and better selection of regional crops could

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 35

Cultural Practices

potentially improve overall regional crop health, but economic and cultural constraints often take these options away from the pest manager. As a result, successful use of cultural-control methods must take into account the nature of the dominant cropping system. Experiments conducted in isolated soybean fields in Louisiana showed that early planting of a border row of soybean, prior to planting of the bulk of the field, could be beneficial for the control of the bean-leaf beetle. A strip of about 10% of the total field area was planted. It attracted the colonizing beetles in large numbers. The strip was sprayed with an insecticide, thus eliminating most of the colonizing population. When the rest of the field was planted, it remained uninfested for most of the remainder of the season. The technique resulted in a 90% reduction in insecticide use. Despite the positive result of this trapcropping experiment, the technique was not adopted by growers, who objected to moving twice to the same field the huge planters used in the industry. In addition, growers within a region tend to plant at different


times; thus the early-planted fields in a region already acted as trap crops (Newsom et al., 1980). We do not presume to have offered an exhaustive discussion of cultural pest-control practices in this chapter. There is a vast literature on the subject (Herzog and Funderburk, 1986; Speight et al., 1999; Landis et al., 2000; Norris et al., 2003) and the cropspecific literature offers the pest manager the best key to the prevalent practices in each region. This literature should be the first to be studied if one is to develop an IPM system with a strong foundation on culturalcontrol tactics. The effectiveness of cultural controls often rests on the complex interrelationships among many of these practices and with other IPM tactics, particularly biological control. Nearly every operation carried out in the field will have some effect, either good or bad, on current or potential pest problems. Understanding these relationships and acting to promote the positive ones are essential steps in the success of IPM programmes that aim at optimizing the role of cultural-control methods.

References Alford, D.V. (2000) Pest and Disease Management Handbook. Blackwell Science, Oxford, 615 pp. All, J.N. (1999) Cultural approaches to management arthropod pests. In: Ruberson, J.R. (ed.) Handbook of Pest Management. Marcel Dekker, New York, pp. 395–416. Allee, L.L. and Davis, P.M. (1996) Effect of manure and corn hybrid on survival of western corn rootworm (Coleoptera: Chrysomelidae). Environmental Entomology 25, 801–809. Altieri, M.A. (1987) Agroecology: the Scientific Basis of Alternative Agriculture. Westview Press, Boulder, Colorado, 227 pp. Altieri, M.A. (1991) How best can we use biodiversity in agroecosystems. Outlook on Agriculture 20, 15–23. Altieri, M.A. (1994) Biodiversity and Pest Management in Agroecosystems. Food Products Press, New York, 185 pp. Altieri, M. and Nicholls, C.I. (2000) Applying agroecological concepts to the development of ecologically based pest management strategies. In: National Research Council (ed.) Professional Societies and Ecologically Based Pest Management. National Academy Press, Washington, DC, pp. 14–19. Altieri, M.A., Lewis, W.J., Nordlund, D.A., Gueldner, R.C. and Todd, J.W. (1981) Chemical interactions between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259–263. Anon. (1996) Integrated Pest Management for Cotton in the Western Region of the United States. Publication 3305, University of California, Oakland, California, 164 pp. Anon. (1998) Integrated Pest Management for Tomatoes, 4th edn. Publication 3274, University of California, Oakland, California, 118 pp. Anon. (1999) Integrated Pest Management for Apples and Pears. Publication 3340, University of California, Oakland, California, 232 pp. Bajwa, W.I. (1988) Pest Management of Major Field Crops. Agricultural Development Bank Pakistan, Islamabad, 60 pp.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 36


W.I. Bajwa and M. Kogan

Bajwa, W.I. (1989) Citrus Pest Management. Agricultural Development Bank Pakistan, Islamabad, 10 pp. Bajwa, W.I. and Schaefers, G. (1998) Indigenous Crop Protection Practices in Sub-Saharan East Africa, their Status and Significance Relative to Small Farmer IPM Programs in Developing Countries. Available at: Bariola, L.A. (1983) Survival and emergence of overwintered pink bollworm moths (Lepidoptera: Gelechiidae). Environmental Entomology 12, 1877–1881. Beasley, C.A. (1992) Winter irrigation reduces spring emergence of pink bollworm moths. In: Proceedings Beltwide Cotton Production Research Conference, Vol. 2. National Cotton Council of America, Memphis, Tennessee, pp. 943–944. Brumfield, R.G. and Ogier, J.P. (2000) A review of organic horticulture and agriculture in the US. In: Proceedings of the XIVth International Symposium on Horticultural Economics. Acta Horticulturae, No. 536, St Peter Port, Guernsey, UK, pp. 21–28. Bugg, R.L., Phatak, S.C. and Dutcher, J.D. (1990) Insects associated with cool-season cover crops in southern Georgia: implications for pest control in truck-farm and pecan agroecosystems. Biological Agriculture and Horticulture 7, 17–45. Buntin, G.D., Cunfer, B.M. and Bridges, D.C. (1991) Impact of volunteer wheat on wheat insects in a wheat soybean double crop system. Journal of Entomological Science 26, 401–407. Burton, R.L., Jones, O.R., Burd, J.D., Wicks, G.A. and Krenzer, E.G. Jr (1987) Damage by greenbug (hom*optera: Aphididae) to grain sorghum as affected by tillage, surface residues, and canopy. Journal of Economic Entomology 80, 792–798. Capinera, J.L. (2001) Handbook of Vegetable Pests. Academic Press, New York, 728 pp. Cherry, R.H. (1987) The effect of flooding on insect populations. Bulletin of Agricultural Experiment Stations (University of Florida) 870, 27–34. Cook, R.J. and Baker, K.F. (1983) The Nature of Practice of Biological Control of Plant Pathogens. American Phytopathological Society, St Paul, Minnesota, 539 pp. Cox, G.W. and Atkins, M.D. (1964) Agricultural Ecology: an Analysis of World Food Production Systems. W.H. Freeman, San Francisco, California, 721 pp. Daane, K.M., Dlott, J.W., Johnson, R.S., Ramirez, H.T., Michailides, T.J., Yokota, G.Y., Crisosto, C.H. and Morgan, D.P. (1995) Excess nitrogen raises nectarine susceptibility to diseases and insects. California Agriculture 49, 13–18. Deren, C.W., Cherry, R.H. and Snyder, G.H. (1993) Effect of flooding on selected sugarcane clones and soil insect pests. Journal American Society of Sugar Cane Technologists 13, 22–27. Dufour, R. (2001) Biointensive Integrated Pest Management. Appropriate Technology Transfer for Rural Areas (ATTRA), Fayetteville, Arkansas, 52 pp. Ferro, D.N. (1996) Cultural control. In: Radcliffe, E.B. and Hutchison, W.D. (eds) Radcliffe’s IPM World Textbook. University of Minnesota, St Paul, Minnesota. Available at: Flint, M.L. and Gouveia, P. (2001) IPM in Practice – Principles and Methods of Integrated Pest Management. Publication 3418, University of California, Oakland, California, 296 pp. Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In: Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological Society of America, Lanham, Maryland, pp. 151–164. Godfrey, L.D. and Leigh, T.F. (1994) Alfalfa harvest strategy effect on lygus bug (Hemiptera: Miridae) and insect predator population density: implications for use as trap crop in cotton. Environmental Entomology 23, 1106–1118. Goodwin, D. (1985) The ecology of two species of corn rootworm (Coleoptera: Chrysomelidae) on volunteer corn in soybean fields in northern Illinois. Bulletin of the Ecological Society of America 66, 179–183. Hatfield, P.G., Blodgett, S.L., Johnson, G.D., Denke, P.M., Kott, R.W. and Carroll, M.W. (1999) Sheep grazing to control wheat stem sawfly, a preliminary study. Sheep and Goat Research Journal 15, 159–160. Hellman, E. and Watson, B. (2000) Reducing the risk of Phylloxera infestation. Northwest Berry and Grape Information Network. Electronic publication. Available at: fruitgrowing/grapes/phylrisk.htm Herzog, D.C. and Funderburk, J.E. (1986) Ecological bases for habitat management and pest cultural control. In: Kogan, M. (ed.) Ecological Theory and Integrated Pest Management Practice. John Wiley & Sons, New York, pp. 217–250. Hokkanen, H.M.T. (1991) Trap cropping in pest management. Annual Review of Entomology 36, 119–138. Horn, D.J. (1988) Ecological Approach to Pest Management. Guilford Press, New York, 285 pp.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 37

Cultural Practices


Khan, Z.R., Ampong-Nyarko, K., Chiliswa, P., Hassanali, A., Kimani, S., Lwande, W. and Overholt, C.M. (1997) Intercropping increases parasitism of pests. Nature 388, 631–632. Kiritani, K. (2000) Integrated biodiversity management in paddy fields: shift of paradigm from IPM toward IBP. IPM Reviews 5, 175–183. Knight, A.L. (1998) Management of codling moth (Lepidoptera: Tortricidae) in apple with overhead watering. Journal of Economic Entomology 91, 209–216. Kogan, M. and Bajwa, W.I. (2001) IPM in the next century: how might things change? Proceedings of Oregon Horticultural Society 92, 51–70. Kogan, M., Croft, B.A. and Sutherst, R.F. (1999) Applications of ecology for integrated pest management. In: Huffaker, C.B. and Gutierrez, A.P. (eds) Ecological Entomology. John Wiley & Sons, New York, pp. 681–736. Kok, L.T. (2001) Classical biological control of nodding and plumeless thistles. Biological Control: Theory and Applications in Pest Management 21, 206–213. Landis, D.A., Wratten, S.D. and Gurr, G.M. (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology 45, 175–201. Levine, E. and Oloumi-Sadeghi, H. (1991) Management of diabroticite rootworms in corn. Annual Review of Entomology 36, 229–255. Lidell, M.C. and Schuster, M.F. (1990) Distribution of the Hessian fly and its control in Texas. Southwestern Entomologist 15, 133–145. Ma, K.C. and Lee, S.C. (1996) Occurrence of major rice insect pests at different transplanting times and fertilizer levels in paddy field. Korean Journal of Applied Entomology 35, 132–136. MacHardy, W.E. (2000) Current status of IPM in apple orchards. Crop Protection 19, 801–806. McHugh, J.J. Jr and Foster, R.E. (1995) Reduction of diamondback moth (Lepidoptera: Plutellidae) infestation in head cabbage by overhead irrigation. Journal of Economic Entomology 88, 162–168. Morrill, W.L. and Kushnak, G.D. (1996) Wheat stem sawfly (Hymenoptera: Cephidae) adaptation to winter wheat. Environmental Entomology 25, 1128–1132. Newsom, L.D. and Herzog, D.C. (1977) Trap crops for control of soybean pests. Louisiana Agriculture 20, 14–15. Newsom, L.D., Kogan, M., Miner, F.D., Rabb, R.L., Tunnipseed, S.G. and Whitecomb, W.H. (1980) General accomplishments toward better pest control in soybean. In: Huffaker, C.B. (ed.) New Technology of Pest Control. Wiley, New York, pp. 51–98. Norris, R.F., Caswell-Chen, E.P. and Kogan, M. (2003) Concepts in Integrated Pest Management. Prentice Hall, Upper Saddle River, New Jersey, 586 pp. Omolo, E.O. and Reddy, S. (1983) An overview of cultural component of an integrated pest management systems in sorghum. In: Africa: Seminar on the Use and Handling of Agricultural and Other Pest Control Chemicals. Environment Liaison Centre in support of African NGO’s Environment Network/Pesticide Action Network, Duduville, Nairobi, Kenya, pp. 100–103. Pedigo, L.P. (2002) Entomology and Pest Management. Prentice Hall, Upper Saddle River, New Jersey, 742 pp. Phelan, L. (1997) Soil management history and the role of plant mineral balance as a determinant of maize susceptibility to the European corn borer. Biological Agriculture and Horticulture 15, 25–34. Prokopy, R. (1994) Integration in orchard pest and habitat management: a review. Agriculture, Ecosystems and Environment 50, 1–10. Prokopy, R. (2001) Twenty years of apple production under an ecological approach to pest management. Fruit Notes 66, 3–10. Reeves, D.W. (1994) Cover crops and rotations. In: Hatfield, J.L. and Stewart, B.A. (eds) Crops Residue Management. Lewis Publishers, Ann Arbor, Michigan, pp. 127–172. Reichert, S.E. and Bishop, L. (1990) Prey control by an assemblage of generalist predators: spiders in garden test systems. Ecology 71, 1441–1450. Rieux, R., Simon, S. and Defrance, H. (1999) Role of hedgerows and ground cover management on arthropod populations in pear orchards. Agriculture, Ecosystems and Environment 73, 119–127. Roth, G.W., Calvin, D.D. and Lueloff, S.M. (1995) Tillage, nitrogen timing, and planting date effects on western corn rootworm injury to corn. Journal of Agronomy 87, 189–193. Sansavini, S. (1997) Integrated fruit production in Europe: research and strategies for a sustainable industry. Scientia Horticulturae 68, 25–36. Speight, M.R., Hunter, M.D. and Watt, A.D. (1999) Ecology of Insects – Concepts and Applications. Blackwell Science, London, 350 pp.

02IntpestManCh2.QXD 14/4/04 2:24 pm Page 38


W.I. Bajwa and M. Kogan

Steffey, K., Gray, M. and Weinzierl, R. (1992) Insect management. In: Conservation Tillage Systems and Management. Midwest Plan Services, Iowa State University, Ames, Iowa, pp. 67–74. Steffey, K.L., Armbrust, E.J. and Onstad, D.W. (1994) Management of insects in lucerne. In: Metcalf, R.L. and Luckmann, W.H. (eds) Introduction to Insect Pest Management, 3rd edn. John Wiley & Sons, New York, pp. 469–506. Stinner, B.R. and House, G.J. (1990) Arthropods and other invertebrates in conservation-tillage agriculture. Annual Review of Entomology 35, 299–318. Stoll, G. (1988) Principles of preventive crop protection. In: Stoll, G. (ed.) Natural Crop Protection in the Tropics. Margraf Verlag, Weikersheim, pp. 14–23. Stoll, G. (2000) Natural Crop Protection in the Tropics. Margraf Verlag, Weikersheim, 376 pp. Sullivan, P. (2001) Intercropping Principles and Practices: Agronomy Systems Guide. Appropriate Technology Transfer for Rural Areas (ATTRA), Fayetteville, Arkansas, 16 pp. Suszkiw, J. (1997) Melon growers’ next battle cry against insect pests could be squash ’em. Agricultural Research 45, 16–17. USDA (1998) Managing Cover Crops Profitably. Publication SX1005, Sustainable Agriculture Network, Washington, DC, 212 pp. van den Berg, J., Nur, A.F. and Polaszek, A. (1998) Cultural control. In: Polaszek, A. (ed.) African Cereal Stem Borers: Economic Importance, Taxonomy, Natural Enemies and Control. CAB International, Wallingford, UK, pp. 333–347. Wratten, S.D. and van Emden, H.F. (1995) Habitat management for enhanced activity of natural enemies of insect pests. In: Glen, D.M., Greaves, M.P. and Anderson, H.M. (eds) Proceedings of the 13th Long Ashton International Symposium on Arable Ecosystems for the 21st Century. Bristol, UK, p. 329. Zehnder, G.W. (1997) Population dynamics of whitefringed beetle (Coleoptera: Chrysomelidae) in sweet potato in Alabama. Environmental Entomology 26, 727–735. Zehnder, G.W., Briggs, T.H. and Pittsi, J.A. (1998) Management of whitefringed beetle (Coleoptera: Curculionidae) grub damage to sweet potato with adulticide treatments. Journal of Economic Entomology 91, 708–714.

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 39


The Relevance of Modelling in Successful Implementation of IPM

David E. Legg Department of Renewable Resources, University of Wyoming Laramie, WY 82071, USA E-mail: [emailprotected]

Introduction Integrated pest management (IPM) has evolved from its beginning as a concept of integrated control (Stern et al., 1959) to a complex study of the agroecosystem. This change was both natural and necessary because conventional agroecosystems are typically dominated by one crop or animal species (host) and thus are not diverse. Ecosystems with limited diversity are vulnerable to the rapid colonization of the host by some biological organisms, and sometimes it can result in host depredation. Consequently, the task of many IPM practitioners is to increase the diversity of an agroecosystem as well as to increase the diversity of the pest-management tools that are used in that system; this will make them more stable and less dependent on pesticide usage. To this end, IPM very much encompasses and makes use of the cultural-control tactics and practices that were identified in Chapter 2. It also embraces the practice of using biopesticides. Host-plant resistance has always been a key element in many IPM programmes and transgenic techniques present many exciting opportunities for increasing the diversity of the agroecosystem. Biological control, particularly when viewed from a perspective of tritrophic interactions,

is also an important part of the agroecosystem (see Chapter 4, this volume). Behaviourmodifying chemicals, as well as non-behaviour-modifying pesticides, have also played important roles in IPM. In addition, the behaviours of some pests can sometimes be used against them in a carefully crafted IPM programme. Finally, we must never forget that humans are an integral part of the agroecosystem, and it can be argued that the ‘consumer’ is a powerful, driving force in determining the composition of IPM programmes (see Chapter 11, this volume). It goes without saying that humans both craft agroecosystems and study the interactions between pests, their hosts, their natural enemies and the environment. From such studies, IPM specialists obtain the information upon which agroecosystem changes are based. Also from these studies, ‘tools’ are developed to describe, analyse and even mimic parts of those systems. When those tools have been developed to a sufficient degree, they may then be used to predict what will happen in the future; predictions of the future are referred to as forecasts. The tools I am referring to are models. For decades, models have been an integral part of IPM. For instance, the use of models has helped pest managers decide how the agroecosystem should be changed to favour

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


03IntpestManCh3.QXD 14/4/04 2:24 pm Page 40


D.E. Legg

economy and conservation and not to favour pests. Moreover, the use of models has allowed scientists to conduct simulated experiments when the conduct of those experiments would not have been possible. Further, models have been used whenever scientists wanted to explore as well as understand the complexities of agroecosystems. In this chapter, I will define and discuss two basic terms: models and systems. I will then discuss the systems approach to modelling, which will be followed by discussions on various classification schemes of systems, the modelling process, the implementation of models and the identification of some commonly used models in IPM. Then I will discuss the teaching of some aspects of modelling to students in the classroom and to IPM practioners in the field. Finally, I will address the future of modelling in IPM.

Two Basic Terms There are two basic terms that need to be understood; the ‘models’ and the ‘systems’. In some circ*mstances, a ‘model’ represents an idealized situation or person. For example, the clothing and garment industry has the fashion model, who demonstrates the most beautiful way in which clothing may be worn. Estate agents have the model home, which represents a well-designed and richly decorated dwelling. Society has the model citizen, who is a person that everyone should strive to emulate. Then there is the model athlete, who is a person that excels beyond all others at his/her sport while also being a good person. Happily, not all usage of the term model is of this sort. Architects and engineers often construct likenesses of whatever they are trying to build, and these constructs are called models. In addition, we can purchase miniature pieces of cars, aeroplanes, ships and the like and then assemble them; these too are called models. If the dimensions of such models are proportionally smaller versions of what is to be constructed, then they are said to be models of scale (e.g. 1 mm = 1 m). Models of scale have been used for centuries, particularly when constructing buildings and bridges.

What differentiates the former use of the word model from the latter? In the former, the focus is on an idealized representation of reality. In the latter, the focus is on an actual representation of reality. In IPM, we use models as actual representations of reality. Models represent or mimic reality in several ways and, accordingly, there are several definitions as to what constitutes a model. Smith (1974) indicates that a model is a description of general ideas that include as little detail as possible. Jeffers (1978) defines a model as any formal expression of the relationships between defined symbols. Teng (1981, 1987) defines a model as any representation of a system in some form other than the original. Manetsch and Park (1982) define a model as an abstract representation of a real-world system that behaves like the real-world system in certain respects. Further, these authors indicate that a ‘good’ model represents the important aspects of the system for problem solving and minimizes ‘behaviour’ that is insignificant to the problem. Clearly, most definitions of models indicate that they represent something called systems and depend, therefore, on the definition of those systems. A ‘system’, as defined by Miller and Miller (1984), is something that has a set of characteristics common to all systems and lacking in things that are not systems. Further, these authors indicate that a system has parts called units or components, which are interdependent and interact with one another. Focusing on living organisms, Teng (1987) indicates that a system cannot be properly understood or managed based on knowledge of some of its components. He also states that the components of a system interact with each other and are influenced in that interaction by external factors. Further, Teng (1987) indicates that the whole of the system is more than the sum of its parts. Manetsch and Park (1982) define a system as a set of interconnected elements organized towards a goal or set of goals separate from the environment, and are determined by factors completely independent of or external to the system. Teng (1987) correctly points out that the systems approach to problem solving differs from systems analysis, which is the analysis

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 41

Modelling in Successful Implementation of IPM

of system structure and behaviour, as well as from system control, which is the manipulation of input, system design, which is either the structuring of non-existing systems or the restructuring of existing systems, and system synthesis, which is a major rebuilding of systems through modelling. From these definitions, it can be deduced that any specified system is composed of components, which are relevant and necessary to the system’s function. Components of a system necessarily depend on one another, and together they function to achieve the goal of the system. One example of a system would be a wheat (Triticum aestivum L.) production system, which has the following components: crop, pests, soil, economics, environment, humans and pest and soil management. Each component of a system can be subdivided. For example, the crop component of the aforementioned system could be divided into low-, mid- and high-latitude varieties. Moreover, varieties within a latitude could be divided into plants, with each plant being divided into leaves, roots, stems and flowers. Each leaf, for example, could then be divided into cells, and each cell could be divided into molecules. Each molecule could be divided into atoms, and each atom could be divided into subatomic particles. These are examples of how a system could be specified at any number of increasing levels of resolution and decreasing levels of scale. However, I could also have specified that system at any number of decreasing levels of resolution and increasing scale, by mimicking the relations between fields within farms, farms within regions, regions within continents or continents within the planet. Clearly, then, the specification of a system is a matter of resolution. As was mentioned earlier, models are developed to mimic systems. However, models can also be developed to mimic system subcomponents. These are often referred to as submodels (e.g. Gelovani, 1984). Here, I simply note that the use of the terms model and submodel is somewhat subjective as a model that mimics one system may be a submodel in another system. For example, if a model represented or ‘mimicked’ the relations between plants in a field, that model could also be a submodel of a more inclusive


model that would mimic the relations between fields within a farm. So where does a system begin and where does it end, and how can it be specified? The use of something called the systems approach to modelling may facilitate the answering of these questions.

The Systems Approach to Modelling The systems approach, as defined by Teng (1987), is actually a problem-solving philosophy and methodology that are useful for guiding the generation of knowledge to support pest management and for synthesizing information into useful forms for delivery. The systems approach occurs in steps. As outlined by Jeffers (1978, 1984), these begin with recognizing the ‘problem’. Then the problem is rigorously defined. Next, the goals and objectives of the problem-solving effort are explicitly stated. Then two or more potential solutions are generated to solve the problem. These are then employed in the modelling process (more on that later). After modelling, the outcomes are carefully evaluated, with potential courses of action being assessed. Finally, the course of action that shows the greatest promise for achieving the stated goals is taken (taking action). Placed into the context of a wheat production system, let us use the example of the pest Diuraphis noxia (Mordvilko) being accidentally introduced into the western wheatgrowing areas of the USA. For many years after its introduction, this pest caused hundreds of millions of dollars (US) of damage (Legg and Archer, 1998). Initially, there were few alternatives to the use of insecticides, so insecticides were relied upon to keep D. noxia from causing significant economic losses (Legg and Archer, 1998). Therefore, one problem of immediate concern was that D. noxia was destroying a significant portion of the US wheat crop and insecticides were being heavily used for its control. A step towards solving this problem was to develop methods whereby the severity of D. noxia infestations could be gauged, relative to the cost of insecticide application, so that producers could assess whether such applica-

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 42


D.E. Legg

tions would be economically viable. Accomplishing this goal would reduce much of the uncertainty surrounding D. noxia infestations and, in doing so, would reduce the number of insecticide applications. To satisfy this goal, three objectives were identified: (i) to establish the relationship between wheat yield and level of D. noxia infestation; (ii) to establish a method whereby the population dynamics of D. noxia could be mimicked; and (iii) to establish methods whereby D. noxia infestations could be quickly and reliably estimated. For the sake of simplicity, I will refer to these as the wheat response–D. noxia infestation system, the D. noxia population-dynamics system and the D. noxia population-estimation system. Once these were identified, experiments were designed and conducted to provide the necessary data for creating the models that mimicked each system. These models were then evaluated, courses of action were formulated and those that provided the best promise for satisfying the stated goals were implemented (Legg et al., 1993; Legg and Archer, 1998). To summarize the generalized concepts of models and systems, it is sufficient to say that models represent systems, whereas systems are composed of objects that are united by their interactions to perform identifiable functions (Teng, 1987).

Classification Schemes for Systems Some scientists, it seems, cannot resist the temptation to group different kinds of systems into categories. This is natural and serves to qualitatively describe systems of interest. In the literature, three such classification schemes are documented and will be referred to as the Miller and Miller (1984), Bawden et al. (1984), and Teng (1987) schemes. The Miller and Miller classification scheme identifies three classes of systems. These are the concrete, the abstracted and the conceptual systems. Concrete systems represent non-random accumulation of matter and energy in a region in physical spacetime, organized into interacting, interrelated subsystems and components. In other words,

concrete systems are ‘phenomena’ of the physical world. Concrete systems can be subdivided into subsystems; Miller and Miller give 19, four of which are the nonliving, living, ecological and earth subsystems. Abstracted systems are actions that are abstracted from the behaviour of organisms. Conceptual systems, on the other hand, are systems of ideas that are expressed in symbolic form. The Bawden et al. classification scheme distinguishes the ‘soft’ from the ‘hard’ systems. Soft systems are those for which the goals are not clearly recognizable and the outcomes are ambiguous and uncertain. However, hard systems are those that have clear goals and for which their outcomes are predictable. Finally, the Teng classification system is even more fundamental than the Bawden et al. system in that Teng divides the world into systems and non-systems.

Classification Schemes for Models Up to now, I have avoided using terms that serve to classify models. This was deliberate, as there are many such classification schemes being used. One scheme, put forward by Richardson (1984), identifies 12 generalized types of models. Other classification schemes can be found in Jeffers (1978) and elsewhere (Manetsch and Park, 1982; Logan, 1994; Hess, 1996; Gutierrez, 2002). An important addition to these was put forward by Peck (2000), when he distinguished statistical from process models, the former being used to give a ‘probabilistic interpretation of the data’ without describing the underlying processes that drive the system, while the latter attempt to describe the permanent underlying biological processes that drive the system. Yet another classification scheme, which originated with Smith (1974), distinguished the practical (tactical) from the theoretical (strategic) models. These serve to identify just two of the many purposes for which modelling is undertaken (Hess, 1996). Other such purposes include crop growth, pest-population dynamics, sampling and sequential sampling. Also, models that describe or predict the change of something

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 43

Modelling in Successful Implementation of IPM

over space may be referred to as landscape or spatial models. Finally, some models are simply referred to by the name of the person or persons who either developed or popularized them. Two examples are the Nachman (Nachman, 1981) and Taylor’s power law models (Taylor, 1961). Here, I briefly describe the Richardson and Jeffers schemes for classifying models, as they include most model types identified in the other schemes that are currently in use.

Richardson classification system The Richardson system of model classification includes the sample, symbolism, simplification, analogy, scale forecast, paradigm perfection, life, caricature, computer, holism and design models. Modelling by sample involves selecting a representative number of ‘individuals’ from a specified population, assessing those individuals and inferring that assessment to the population at large; modelling by sample is an essential part of statistics. Modelling by symbolism involves the use of symbols to express and represent the relations and states of variables in a system; this type of modelling is primarily found in mathematics, studies in logic and decision making. Modelling by simplification involves the development of schemas of systems that are difficult or impossible to otherwise envision; it serves to simplify systems to the extent that just the basics are modelled. Modelling by analogy is a tangible representation of something that can be seen. Modelling by analogy requires (and provides) more detail than does modelling by simplification. An example of modelling by analogy is a map of roads or streets. Modelling by scale is producing a representative of some real-world entity, which resembles that entity in detail such that each part of the model is proportionally the correct size in relation to every other part of the model; as mentioned before, architects and engineers have used these models. Forecasting models will predict events that happen in the future. Examples include the times of sun- and moonrise (and set), the high and low temperatures for future dates,


and the longevity of one’s life. Modelling by perfecting the paradigm mimics systems through the use of rules; such models are essential to many knowledge-based systems (Stone et al., 1986; Plant and Stone, 1991). Life models are a collection of methods whose commonality resides in the fact that they mimic human life processes; life models are necessary because it would be unethical, immoral and illegal to conduct certain experiments on humans. Caricature models are models that represent systems through the use of metaphors, similes, effigies and the like. Computer models mimic systems through the incorporation of rules and mathematical equations that express relationships between variables within systems. Computer models greatly facilitate the conduct of repetitive, complicated tasks. Also, they swiftly locate pieces of information that may be ‘buried’ in a great deal of literature. Modelling by holism represents a ‘turning away’ from the standard, reduction-driven systems approach to modelling and making use of philosophies and methods that have heretofore not been used (more on that later). Modelling by design ensures that the processes and schemas are constructed so that they will serve their intended purpose (i.e. will address the stated goals and objectives of the problem-solving venture).

Jeffers classification systems Jeffers (1978) actually put forward three systems for classifying models. The first is based on a dichotomy of simulation and analytic models. Simulation models are those that can be specified by a routine of arithmetic operations (Jeffers, 1978), while simulation modelling involves the operation over time of a mathematical model that represents the structure and dynamics of a system. Simulation modelling is often conducted for the purpose of observing the system’s behaviour under controlled or experimental conditions (Berryman and Pienaar, 1974). Simulation models perform many tasks, some of which are to solve differential equations, repeatedly apply transition matrices or repeatedly use random or pseudorandom

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 44


D.E. Legg

number algorithms (Jeffers, 1978). Simulation models are very important in that they are used to conduct ‘experiments’ under conditions for which experiments could otherwise not be done. To simulate experiments, however, modellers must make assumptions about how the system works because not all components are included in the model and therefore the model is incomplete. As simulations often involve the repetitive solution of mathematical equations, as well as the handling of many individuals in specified populations, a computer is often needed to conduct them (e.g. Dowd et al., 1984; Nachapong et al., 1989; Culin et al., 1990; Berry et al., 1991; Follett et al., 1993; Flinn and Hagstrum, 1995; Legg, 2000; Legg et al., 2000, 2002; Arthur et al., 2001). There are, however, some tasks that can be simulated without a computer (e.g. Penman and Chapman, 1982). Analytic models are those for which explicit formulae are derived for predicted values or distributions (Jeffers, 1978). Also, analytic models allow modellers to conduct in-depth explorations of model ‘behaviour’ (Peck, 2000). Analytic models tend to be less complex than are simulation models, though not all are necessarily simple. Typical analytic models are those used to describe gravity (Peck, 2000) or those used in analysis of variance (ANOVA), regression and multivariate analyses, as well as those that make use of the theoretical probability distributions of statistical applications (Jeffers, 1978). The second of Jeffers’ systems for classifying models is based on a fundamental dichotomy between word models and mathematical models. Word models are purely verbal descriptions of events, processes and relations. Often they are used to define the scope and depth of a problem. If systems are extremely simple, word models will perform well in mimicking them. However, if systems are not very simple, word models fail to mimic them. This is so because it requires a great number of words to describe the complex relationships that occur in some systems, as well as their feedbacks. In addition, it is unfortunate that some words have more than one meaning; such ambiguity, when it occurs, makes word models untenable (Jeffers, 1978). Mathematical models, on

the other hand, are models that mimic systems through the use of symbolic logic. Such models are capable of expressing ideas and relations of great complexity while simultaneously retaining simplicity (Jeffers, 1978). Also, mathematical models are unambiguous. However, mathematical models must continually be checked for the presence of contradictions (Jacobsen, 1984). Mathematical models are often divided into two groups: deterministic and stochastic (Jeffers, 1978; Peck, 2000). Deterministic models make use of the branch of mathematics that was developed when mathematics were first applied to physical problems and then to engineering problems (Jeffers, 1978; Logan, 1994). Sometimes deterministic models are composed of differential and difference equations (Jeffers, 1978); however, deterministic models can be represented by almost any kind of equation (Peck, 2000). For example, if a 22% infestation of D. noxia occurred on winter wheat in Wyoming, USA, then application of the deterministic model: Yield loss = EY × (0.5 × per cent infestation/100)


would determine the yield to be reduced by 47.08 l/ha (prediction), where Yield loss is the predicted yield loss (expressed in the same units as EY), EY is the expected yield that would occur if D. noxia were not infesting that field (say, 428 l/ha), and per cent infestation is the per cent of wheat tillers that are infested with at least 1.0 D. noxia (Legg et al., 1993). A graphical representation of this model may be seen in Fig. 3.1. It has long been known that many measurements taken by scientists do not represent the actual or true values of, say, population means. Rather, they come from distributions of measures that are taken on each of those populations (Salsburg, 2001). For these measures, deterministic models cannot exactly determine or predict the true values because the predictions will deviate from the true values by random amounts. In such cases, the application of stochastic models may be more appropriate in the modelling process. Stochastic models resemble deterministic models to an extent, but

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 45

Modelling in Successful Implementation of IPM


250 Yield loss = EY × (0.5 × per cent infestation/100)

Yield loss (l/ha)





0 0

20 40 60 80 Per cent Diuraphis noxia infestation


Fig. 3.1. Graphical representation of a deterministic model, which provides the exact yield losses that will occur at given levels of Diuraphis noxia infestation on winter wheat.

they also contain symbols, terms or algorithms that represent the deviations of predicted from measured values. Moreover, the behaviour of these deviations can be explained, to an extent, through probability distributions. For example, one stochastic model that is used when testing for equality of ‘treatments’ in a one-way ANOVA is as follows: Yij = µ + τi + ξij


where Yij is a measure of the ith treatment and jth replicate, µ is the grand average of the experiment, τi is the ith treatment effect (i.e. the ith treatment average minus the grand average), and ξij is the departure of each measured Yij from its predicted value (i.e. µ + τi). These types of models are referred to as linear statistical models (Cochran and Cox, 1957). Another stochastic model that is used when testing for relations between one dependent variable (Y) and one independent variable (X) is as follows: Yi = β0 + β1Xi + ξi


where β0 and β1 are the true y intercept and slope (Weisberg, 1980). These are sometimes referred to as regression models. Regression models can have more than one independent variable, as well as more than one slope, and

these are referred to as multiple linear regression models. The errors (ξij) of linear statistical models and the errors (ξi) of regression models are known to have a mean of 0.0 and are used to calculate variance (σ2), which describes the ‘spread’ of the errors about the mean. Also, the ξij and ξi are assumed to conform to a specific probability distribution – in this case, the normal distribution (Snedecor and Cochran, 1967). Use of stochastic models in the form of linear statistical models and regression models have been very important in the successful implementation of IPM as their use has helped researchers to analyse the results of experiments (e.g. Legg et al., 1987), describe ecological relationships (e.g. Legg and Chiang, 1984) and make predictions in IPM settings (Plant and Stone, 1991). Stochastic functions can be added to almost any deterministic model. For example, if I wished to represent equation 1 as a stochastic model, I would first research which distribution describes the pattern of ξ (errors) about the predicted values, and then establish whether that distribution holds true for all values of expected yield in the absence of D. noxia (i.e. EY), as well as for all values of per cent infestation that would be encountered. Next I would establish whether

03IntpestManCh3.QXD 5/5/04 2:06 pm Page 46


D.E. Legg

Probability of departures occurring


0.008 Predicted 0.006



0.000 –150 –100 –50 0 50 100 150 Departures of measured losses from predicted (l/ha) Fig. 3.2. Simulated probability distribution for the departures of measured yield losses (winter wheat) from predicted yield losses due to infestation of the insect Diuraphis noxia.

both the spread of the errors and the value for s2 were constant over all combinations of EY and per cent infestation that would be encountered. Once those steps were completed, I would then construct a stochastic representation of Equation 1: Yield lossi = EY ¥ (0.5 ¥ per cent infestation/100) + xi


where the ‘spread’ of the xi is described by a specific distribution with a constant value for s2. If the spread of xi is described by the normal distribution and the value for s2 is constant at, say, 1849, then, for any value of per cent infestation, the probabilities of obtaining certain values for yield losses would be as shown in Fig. 3.2. Note that the probabilities of yield losses are greatest for values of per cent infestation that are at or near the ‘predicted value’ and decline in a predictable manner as departures of measured yield losses (abscissa) increase (Fig. 3.2). The stochastic model, as represented by Equation 4, could be used for all kinds of purposes, one of which is to simulate a graphical representation of that model. This was done by calculating the predicted yield losses for each per cent infestation, beginning with 0.0 and ending with 100, in increments of 1.0, and then adding a random xi,

taken from a normal distribution with a mean of 0.0 and a s2 of 1849, to each predicted value (Press et al., 1986). Using these simulated measures, I was then able to generate a graphical representation of model 4, where the predicted values (i.e. the ‘line’ from Equation 1) fails to equal each and every observed measure (dots) by some random amount (Fig. 3.3). As stochastic models are most useful when inadequate information exists for determining the outcome of each and every measure, the outcome of the modelling effort should be expressed as the chance of being within stated ‘low’ and ‘high’ values. For example, it is 90% certain that yield loss will be from 93 to 121 l/ha when per cent infestation is 50. The third of Jeffers’ systems for classifying models involves what he terms ‘families of models.’ These include the dynamic models, matrix models, multivariate models and optimization models. As pointed out by Jeffers (1978), these are not mutually exclusive as, for example, a dynamic model may also be a matrix model. The dynamic models are those that emphasize change in the variables of a system with respect to one another. They have the advantage of being very flexible and can make use of many mathematical equations to describe the change in specific

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 47

Modelling in Successful Implementation of IPM


300 Yield loss = EY × (0.5 × per cent infestation/100)

Yield loss (l/ha)






0 0

20 40 60 80 Per cent Diuraphis noxia infestation


Fig. 3.3. Simulated distribution of observed yield losses (dots) about predicted levels of yield losses (line) due to infestation of the insect Diuraphis noxia on winter wheat.

parts of the system, relative to its other parts, at any point in time. The disadvantage of dynamic models is that they do not usually contain equations for all system components, as the description of most systems is incomplete. Dynamic models must therefore operate on the condition of making several assumptions. After a dynamic model is developed it can then be used to explore the system either for further understanding or for simulation. Examples of dynamic models include testing the effectiveness of pesticides (Schaalje, 1990), the growth of winter wheat in the Western Great Plains of the USA (McMaster and Smika, 1988) and the population dynamics of the Douglas-fir tussock moth, Oryzia pseudotsugata (McDunnough) (Berryman, 1991). Matrix models use a mathematical technique that is often referred to as linear algebra. The use of matrix models involves the manipulation of values that are expressed in table-like entities, referred to as matrices, and row- and column-like entities referred to as vectors. These can be subjected to all sorts of mathematical operations and manipulations, and they most often mimic the population dynamics of biological organisms. The advantages of using matrix models lie in the fact that they are elegant in how they sum-

marize information, they simplify procedures for solving complex problems and they can be placed into computer programs that conduct repetitive and sometimes complex mathematical procedures. One disadvantage of using matrix models is that they make use of a special notation commonly used with linear algebra, so they can be confusing to non-mathematically oriented IPM practitioners. Another disadvantage to the use of matrix models is that some computer programming skill may be needed to construct and maintain them. One type of matrix model is that of Lewis (1942) and Leslie (1945). Another is that of the Markov chain, which has been used to predict the probability of grasshopper outbreaks in Wyoming (Zimmerman, 1999). Multivariate models describe the pattern of relationships between several variables at the same time. These may be most useful for investigating ecological relationships in IPM. Some timehonoured multivariate techniques that have been used are principal component analysis, cluster analysis, discriminant analysis and canonical analysis. Optimization models are often used in operations research to search for a mathematical maximum or minimum, whichever is optimal. For IPM, practitioners often wish to maximize the return on a pest-

03IntpestManCh3.QXD 15/4/04 2:23 pm Page 48


D.E. Legg

management investment, so the application of optimization models may be found in the calculation of some economic thresholds. This is by no means a trivial task, as many variables are often used, with many different values being tried for each, to find the ‘optimum’. Obviously, intensive computer programming is involved with the use of optimization models. One example of using an optimization model in IPM involved soybean pest management (Hutchins et al., 1986). Another involved rangeland IPM with respect to grasshopper infestations (Davis et al., 1992).

The Modelling Process Modelling can be thought of as involving two phases. Phase I is the conception of the model, the construction of the model and the validation and verification of the model. Phase II is the implementation of the model.

Phase I The first phase often progresses in a stepwise manner. To that end, both Jeffers (1978) and Teng (1987) have identified some of the steps in the process, which include: (i) defining and bounding the system that is to be modelled; (ii) evaluating the historical and current knowledge about the system; (iii) developing an initial conceptual (system) model; (iv) collecting data and constructing equations to describe the system; (v) structuring a detailed system model for computer modelling; (vi) translating the model into a selected language for computer performance; (vii) sensitivity analyses with verification and validation of the model; and (viii) model experimentation. Defining and bounding the system to be modelled is extremely important and, arguably, may be the most important step in the process. The objectives of this step should include the identification of how resolute the modelling process should be in order to address the stated problem, as well as the breadth of scale that should be considered for developing and applying the model. In other words,

how complex or how simple does the model need to be to satisfy its stated purpose? After these questions are answered, it is always good to conduct a thorough review of the literature and find out, from a historical perspective, what is known about the system of interest. Next, capture your ideas on how the model should be structured in a conceptual diagram. For this, I typically use flow charts, as I am comfortable with writing computer programs. However, just about any system of ‘boxes’ and arrows will be sufficient to show the variables and their relations to one another. After constructing a conceptual diagram, collect some data through either a series of designed experiments or observational studies, or both; then use these data to construct the ‘equations’ that mimic the system. Note that this step ‘assumes’ that mathematical models are to be constructed to mimic the system. This is not necessarily so, as for some problems, constructing an elegant word model or perhaps a knowledgebased system may prove satisfactory. Next, a detailed system is constructed for computer modelling. Here again, it is assumed that the identified system is sufficiently complicated for detailed analyses, as well as simulations, to be needed. Next, the constructed model is translated into a computer language for its use. Again, it is assumed that the model is mathematical in nature, is very complex, or both, and should be embedded in a computer program for ease of use. However, if the model is not of a mathematical nature, it may be represented by a knowledge-based system. Further, if the model is non-mathematical and is simple in its depth or breadth, a decision table or decision tree may be sufficient. Sensitivity analyses are then conducted on the model by varying the values for certain parameters in the equations, as well as the values for certain variables, to see if small changes in those parameters or variables induce small or large changes in the model’s performance. In a parallel effort, the model must be tested in the ‘real world’ to see if it will perform at an acceptable level on independent sets of data. Finally, once the model has been so analysed, ‘verified’, and ‘validated’, it can be used to perform experiments to see how the system will behave under new sets of conditions.

03IntpestManCh3.QXD 15/4/04 2:23 pm Page 49

Modelling in Successful Implementation of IPM

This first phase to modelling, as challenging as it may seem, can be conducted if you have some training in and experience with modelling and if you possess a measure of ‘modelling intuition.’ In addition, having an open mind (as to which types of models to use), as well as using some creativity, can also help in the modelling process (Jeffers, 1978). However, it is the second phase of modelling that has turned out to be somewhat of a challenge.

Phase II Model implementation involves three general steps: (i) introduction; (ii) adaptation; and (iii) incorporation by a specific agency, company or groups of individuals (user) (Kraemer, 1984). To date, much more attention has been given to the process of model development than has been given to the process of model implementation. As stated by Kraemer (1984), ‘Some posit that this misplaced attention has resulted in a generally low level of model use and model success’. Model introduction refers to a period during which the model is considered for adoption. During this step, some early initial testing may be conducted and the results, along with the introductory information that was presented with the model, are used to make the decision on model adoption. Model adaptation refers to the period after model introduction during which broader support for the model is developed and plans are made for instructing and training practitioners on its use as well as the interpretation of its output. During model adaptation, the model begins to be widely used. Model incorporation is the step at which the model is no longer a new entity but, rather, becomes a routine part of the user’s operation. Research has shown that the successful implementation of a model is influenced by at least three factors: (i) the inherent technical characteristics of the model itself; (ii) the social setting in which the model is used; and (iii) the uses and impacts of the model as experienced by the user (Kraemer, 1984). Interestingly, it has been hypothesized that a


‘user’ will not implement a model unless the model also serves some political interests (Kraemer, 1984).

Some Commonly Used Models in IPM As was mentioned earlier, some of the most commonly used models in IPM are the linear statistical models of ANOVA as well as the regression models. Other commonly used models include crop-growth and croploss models, economic-threshold and injurylevel models, sampling models and phenology models. Crop-growth and croploss models are commonly used in IPM. Many crop-growth models are process models that attempt to function on the physiological level (Pace and MacKenzie, 1987; Gutierrez, 2002). Most mimic plant growth by dividing the plant into its fundamental components, such as leaf, stem and root biomass accumulation, as well as photosynthesis and respiration. Some crop-growth models can be used for crop-loss assessment, through simulation. However, most crop-loss assessment is conducted through the use of regression models (e.g. Sah and MacKenzie, 1987; Shane and Teng, 1987; Walker, 1987; Mesbah et al., 1994). Economic-threshold models are deterministic in nature and either contain or are linked to population-dynamics models (Chiang, 1979, 1983; Pedigo et al., 1986); economic injury-level models are also deterministic in nature but do not contain the population-dynamics link. Economic-threshold models can also take the form of optimization models. Many examples exist in the literature of using the deterministic form of economic-threshold and economic injurylevel models in IPM (e.g. Legg et al., 1993). Examples also exist for using optimization models when calculating economic thresholds in IPM (e.g. Davis et al., 1992). Sampling models are particularly well used in IPM. The acts of sampling and sample inspection for assessing the abundance and presence of pests can take several forms (Legg and Archer, 1998). However, the sampling models serve to assist researchers and IPM practitioners in either the efficient estimation of pest-population abundance or in

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 50


D.E. Legg

the rapid classification of a pest population relative to an economic (or action) threshold. The former are often referred to as precisionbased sequential sampling models, as they serve to guide researchers (mostly) in determining how many samples are needed to estimate a population average with a certain predetermined level of precision (Hutchison, 1994); precision is a measure of the consistency of the estimates of the average (Legg and Moon, 1994). The latter are often referred to as classification-based sequential sampling models, as they serve to quickly classify infestations as being ‘high’ or ‘low’ relative to a threshold value, thus requiring less sampling effort to make a pest-management decision (Binns, 1994). Finally, phenology models serve to predict, mostly in real time, the phenological development of pest populations. These are most useful for predicting the dates of first or peak emergence or the emergence of a second generation of a pest. Almost all phenology models are driven by ambient temperature, as plant-pathogenic organisms, weeds and pestiferous insects are poikilotherms (Legg et al., 2002). However, some phenology models are driven by both temperature and moisture (e.g. Legg and Brewer, 1995). Phenology models can be developed either in the laboratory or in the field (Legg et al., 1998b). If they are developed in the laboratory, the parameters may be meaningful in a biological sense. However, care must be taken to ensure that the model output, when used for IPM purposes, reflects pest development in the field. If they are developed in the field, however, the parameters may not be biologically meaningful but they may provide acceptable predictions (Legg et al., 1998a).

Education and Modelling: Some Lessons Learned Teaching people how to develop and use models is important for producing the next generation of modellers and ensuring that models will be used by IPM practitioners. Here, I distinguish between teaching students in the classroom and educating IPM

practitioners outside the classroom. I will refer to the former as ‘teaching’ and the latter as ‘extension’ or ‘outreach’. First, I will address teaching. Teaching students about modelling actually has two perspectives: developing models and using models. Regarding the former, courses must be offered so that some students will learn how to develop models. In these courses, students learn how to use the modelling process and how to apply some modelling techniques. It has been my experience that most students who enrol in these courses are agriculturalists, biologists or natural resource scientists who also have some quantitative skills. Consequently, the teaching of ‘modelling’ must be done from a conceptual perspective using each of the following techniques: verbal, visual, activityoriented and mathematically oriented methods. The use of verbal methods requires that I, as the instructor, use words to describe what is being done, why it is done and how it is done. For me, this requires careful thought and effort as such verbal descriptions are far longer and, in some cases, less elegant than using mathematical descriptions of the same. Nevertheless, verbal descriptions must be incorporated into each of the lectures as some students are very good listeners and learn primarily through verbal descriptions. Visual methods are extremely useful for some students as they are ‘visually oriented’ and will understand the concept or process only when a chart, graph or some other visual is used. Activityoriented students are usually befuddled by either the verbal descriptions or the visual depictions I provide until I either work through an example or assign them a special project to be completed outside class (homework). Finally, there are some mathematically oriented students who are comfortable with and learn through the symbolic language of mathematics. For these, I provide explanations of processes and techniques using such tools as manipulated equations (all kinds), integrals and algebra. Teaching students how to use models is necessarily different from teaching students how to develop models. This is so because these students are agriculturalists, biologists

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 51

Modelling in Successful Implementation of IPM

or natural resource scientists who have few quantitative skills. Instead, I teach these students a little about developing models but a lot about using models. Also, these students need to be taught to interpret the results or ‘output’ from models, as well as to ‘experiment’ with them by posing ‘what if ’ scenarios and rerunning the models for each scenario. Finally, extending models to IPM practitioners necessarily differs from teaching, as practitioners do not enrol in courses and therefore cannot be forced to use models for the conduct of pest management. Instead, I have learned that the development and implementation phases of modelling must be conducted with regular input from the people who will use those models. These people include representatives from producer groups, some university personnel and, perhaps, some government officials. Also, the administrator from the modeller’s unit may be important as that individual provides resources for maintaining the models. Anyway, these individuals must work with the modellers because they have an interest in developing and maintaining the models as well as the computer programs in which they reside. This kind of ‘partnership’ is essential for developing products that are useful to and will be used by IPM practitioners.

The Future of Modelling in IPM Given the importance of modelling and systems analysis in IPM, both should play important future roles. However, the types of models that may be used and the approach to designing and implementing those models may be different from the types of models that are currently being used and the approaches that are currently being employed by modellers. Plant and Stone (1991) have pointed out that traditional systems-level problems have been solved using systems analysis, along with mathematical models, which were central to the IPM projects of the 1970s and 1980s. More recently, however, some emphasis has been placed on the use of qualitative methods (or models) to


solve agricultural problems because much of the present understanding of these systems is qualitative and is based on experience (Plant and Stone, 1991). Such knowledge is not easily quantifiable, which makes it difficult to construct mathematical models. In his 1994 article, Logan eloquently expressed how the ‘infatuation’ that IPM researchers and practitioners had with complex, mathematical simulation models waned during the 1980s, due in part to the unrealistic expectations that were put forward by the proponents of those models, the lack of the models’ ‘predictive power’ and the environment in which some models were put together. In the general modelling literature, Richardson (1984) has summarized the essence of some papers by calling for a more inclusive approach to systems definitions and analysis, one that he termed ‘holism’. Further, Richardson (1984) articulated the perception that dynamic models (and modellers) are in the process of a ‘shift of paradigm’ away from the classic application of reductionism, or Cartesian disassembly of systems, to a more inclusive approach to modelling those systems. In the IPM literature, this shift appears to be headed towards something called a ‘whole-system’, within which agriculture is viewed as an ecosystem that involves habitat management, crop attributes and multitrophic interactions as some of the principles that will guide decision making and promote agricultural sustainability (Rains et al., 2002). Modelling changes in the landscape, using the science of geographical information systems, also appear likely. Access to models and the weather data that are needed to run the models will be increasingly made available on the Worldwide Web (e.g. (Brock et al., 1995). Finally, there are the knowledge-based systems. These are computer programs that solve complex problems within some defined area of knowledge (knowledge domain). Knowledge-based systems differ from traditional mathematical models in that they are designed to mimic the human reasoning processes, which rely on logic, beliefs, generalized rules, opinion, and experience; these are typically not quantifiable (Plant

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 52


D.E. Legg

and Stone, 1991). Relatively new in their development, knowledge-based systems are extremely flexible and inexpensive to construct. They do, however, require constant

attention by teams of experts, programmers, and ‘knowledge engineers’ to keep them current and valid.

References Arthur, F.H., Throne, J.E., Maier, D.E. and Montross, M.D. (2001) Impact of aeration on maize weevil (Coleoptera: Curculionidae) populations in corn stored in the northern United States: simulation studies. American Entomologist 47, 104–110. Bawden, R.J., Macadam, R.D., Packham, R.J. and Valentine, I. (1984) Systems thinking and practices in the education of agriculturalists. Agricultural Systems 13, 205–225. Berry, J.S., Holtzer, T.O. and Norman, J.M. (1991) Experiments using a simulation model of the banks grass mite (Acari: Tetranychidae) and the predatory mite Neoseiulus fallacies (Acari: Phytoseiidae) in a corn microenvironment. Environmental Entomology 20, 1074–1078. Berryman, A.A. (1991) Population theory: an essential ingredient in pest prediction, management, and policy-making. American Entomologist 37, 138–142. Berryman, A.A. and Pienaar, L.V. (1974) Simulation: a powerful method of investigating the dynamics and management of insect populations. Environmental Entomology 3, 199–207. Binns, M.R. (1994) Sequential sampling for classifying pest status. In: Pedigo, L.P. and Buntin, G.D. (eds) Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton, Florida, pp. 137–174. Brock, F.V., Crawford, K.C., Elliott, R.L., Cuperus, G.W., Stadler, S.J., Johnson, H.L. and Eilts, M.D. (1995) The Oklahoma mesonet: a technical overview. Journal of Atmospheric and Oceanic Technology 12, 5–19. Chiang, H.C. (1979) A general model of the economic threshold level of pest populations. Food and Agricultural Organization of the United Nations Plant Protection Bulletin 27, 71–73. Chiang, H.C. (1983) Factors to be considered in refining a general model of economic threshold. Entomophaga 27, 99–103. Cochran, W.G. and Cox, G.M. (1957) Experimental Designs, 2nd edn. John Wiley Press, New York, 611 pp. Culin, J., Brown, S., Rogers, J., Scarborough, D., Swift, A., Cotterill, B. and Kovach, J. (1990) A simulation model examining boll weevil dispersal: historical and current situations. Environmental Entomology 19, 195–208. Davis, R.M., Skold, M.D., Berry, J.S. and Kemp, W.P. (1992) The economic threshold for grasshopper control on public rangelands. Journal of Agricultural and Resource Economics 17, 56–65. Dowd, P.F., Sparks, T.C. and Mitchell, F.L. (1984) A microcomputer simulation program for demonstrating the development of insecticide resistance. American Entomologist 30, 37–41. Flinn, P.W. and Hagstrum, D.W. (1995) Simulation model of Cephalonomia waterstoni (Hymenoptera: Bethylidae) parasitizing the rusty grain beetle (Coleoptera: Cucujidae). Environmental Entomology 24, 1608–1615. Follett, P.A., Kennedy, G.A. and Gould, F. (1993) REPO: a simulation model that explores the Colorado potato beetle (Coleoptera: Chrysomelidae) adaptation to insecticides. Environmental Entomology 22, 283–296. Gelovani, V.A. (1984) An interactive modelling system as a tool for analyzing complex socio-economic problems. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 75–86. Gutierrez, A.P. (2002) Modeling pest management. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 500–503. Hess, G.R. (1996) To analyse or to simulate, is that the question? American Entomologist 42, 14–16. Hutchins, S.H., Higley, L.G., Pedigo, L.P. and Calkins, P.H. (1986) Linear programming model to optimize management decisions with multiple pests: an integrated soybean pest management example. Bulletin of the Entomological Society of America 32, 96–102. Hutchison, W.D. (1994) Sequential sampling to determine population density. In: Pedigo, L.P. and Buntin, G.D. (eds) Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton, Florida, pp. 207–243. Jacobsen, E. (1984) On logic, axioms, theorems, paradoxes and proofs. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 71–73.

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 53

Modelling in Successful Implementation of IPM


Jeffers, J.N.R. (1978) An Introduction to Systems Analysis, with Ecological Applications. Edward Arnold Press, London, 198 pp. Jeffers, J.N.R. (1984) The development of models in urban and regional planning. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 87–99. Kraemer, K.L. (1984) The politics of model implementation. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 131–160. Legg, D.E. (2000) Tables of computer-simulated errors for binomial sequential sampling plans. In: Pandalai, S.G. (ed.) Recent Research Developments in Entomology, Vol IV. Research Signpost Press, Trivandrum, pp. 95–106. Legg, D.E. and Archer, T.L. (1998) Sampling methods, economic injury levels, and economic thresholds for the Russian wheat aphid (hom*optera: Aphididae). In: Quisenberry, S.S. and Peairs, F.B. (eds) Response Model for an Introduced Pest – the Russian Wheat Aphid. Thomas Say Publications in Entomology, Proceedings, Entomological Society of America, Lanham, Maryland, pp. 313–336. Legg, D.E. and Brewer, M.J. (1995) Relating within-season Russian wheat aphid (hom*optera: Aphididae) population growth in dryland winter wheat to heat units and rainfall. Journal of the Kansas Entomological Society 68, 149–158. Legg, D.E. and Chiang, H.C. (1984) European corn borer (Lepidoptera: Pyralidae) infestations: predicting second generation egg masses from blacklight trap captures and relating their abundance to several corn crop characters. Journal of Economic Entomology 77, 1432–1438. Legg, D.E. and Moon, R.D. (1994) Bias and variability in statistical estimates. In: Pedigo, L.P. and Buntin, G.D. (eds) Handbook of Sampling Methods for Arthropods in Agriculture. CRC Press, Boca Raton, Florida, pp. 55–69. Legg, D.E., Barney, R.J., Tipping, P.W. and Rodriguez, J.G. (1987) Preferred grain quantity and insect density for maize weevil (Coleoptera: Curculionidae) interaction studies. Journal of Economic Entomology, 80, 388–393. Legg, D.E., Wangberg, J.K. and Kumar, R. (1993) Decision support software for implementation of Russian wheat aphid economic injury levels and thresholds. Journal of Agricultural Entomology 10, 205–213. Legg, D.E., Van Vleet, S.M., Lloyd, J.E. and Zimmerman, K.M. (1998a) Calculating lower developmental thresholds of insects from field studies. Recent Research Developments in Entomology 2, 163–172. Legg, D.E., Struttmann, J.M., Van Vleet, S.M. and Lloyd, J.E. (1998b) Bias and variability in lower developmental thresholds estimated from field studies. Journal of Economic Entomology 91, 891–898. Legg, D.E., Van Vleet, S.M. and Lloyd, J.E. (2000) Simulated predictions of insect phenological events made by using mean and median functional lower developmental thresholds. Journal of Economic Entomology 93, 658–661. Legg, D.E., Van Vleet, S.M., Ragsdale, D.W., Hansen, R.W., Chen, B.M., Skinner, L. and Lloyd, J.E. (2002) Required number of location-years for estimating functional lower developmental thresholds and required thermal summations of insects: first emergence of adult Aphthona nigriscutis Foudras as an example. International Journal of Pest Management 48, 147–154. Leslie, P.H. (1945) On the use of matrices in certain population mathematics. Biometrika 33, 183–212. Lewis, E.G. (1942) On the generation and growth of a population. Sankhya 6, 93–96. Logan, J.A. (1994) In defence of big ugly models. American Entomologist 40, 202–207. McMaster, G.S. and Smika, D.E. (1988) Estimation and evaluation of winter wheat phenology in the central great plains. Agricultural and Forest Meteorology 43, 1–18. Manetsch, T.J. and Park, G.L. (1982) System Analysis and Simulation with Application to Economic and Social Systems, Vol. I, 4th edn. Engineering Library, Michigan State University, East Lansing, Michigan, 52 pp. Mesbah, A., Miller, S.D., Fornstrom, K.G. and Legg, D.E. (1994) Kochia (Kochia scoparia) and green foxtail (Setaria viridis) interference in sugarbeets. Weed Technology 8, 754–759. Miller, G.G. and Miller, J.L. (1984) The earth as a system. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 19–49. Nachapong, M., Legg, D.E., Kittiboonya, S. and Wangboonkong, S. (1989) Validation of computer-simulated presence-absence sequential sampling plans for the cotton bollworm (Heliothis armigera) (Hübner) in cotton. Thai Journal of Agricultural Science 22, 293–302. Nachman, G. (1981) A mathematical model of the functional relationship between density and spatial distribution of a population. Journal of Animal Ecology 50, 453–460.

03IntpestManCh3.QXD 14/4/04 2:24 pm Page 54


D.E. Legg

Pace, M.E. and MacKenzie, D.R. (1987) Modeling of crop growth and yield for loss assessment. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 30–36. Peck, S.L. (2000) A tutorial for understanding ecological modelling papers for the nonmodeler. American Entomologist 46, 40–49. Pedigo, L.P., Hutchins, S.H. and Higley, L.G. (1986) Economic injury levels in theory and practice. Annual Review of Entomology 31, 341–368. Penman, D.R. and Chapman, R.B. (1982) Design of a field-sampling simulator. Bulletin of the Entomological Society of America 28, 143–145. Plant, R.E. and Stone, N.D. (1991) Knowledge-based Systems in Agriculture. McGraw-Hill Press, New York, 364 pp. Press, W.H., Flannery, B.P., Teukolsky, S.A. and Vetterling, W.T. (1986) Numerical Recipes. Cambridge University Press, New York, 203 pp. Rains, G.C., Olson, D.M., Lewis, J.W. and Tumlinson, J.H. (2002) Systems management. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 826–828. Richardson, J.G. (1984) A primer of model systems. In: Richardson, J. (ed.) Models of Reality Shaping Thought and Action. Lomond Press, Mt Airy, Maryland, pp. 3–18. Sah, D.N. and MacKenzie, D.R. (1987) Methods of generating different levels of disease epidemics in loss experiments. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 90–96. Salsburg, D. (2001) The Lady Tasting Tea. Freeman Press, New York, 24 pp. Schaalje, G.B. (1990) Dynamic models of pesticide effectiveness. Environmental Entomology 19, 440–447. Shane, W.W. and Teng, P.S. (1987) Generating the database for disease-loss modelling. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 82–89. Smith, M.J. (1974) Models in Ecology. Cambridge University Press, London, 145 pp. Snedecor, G.W. and Cochran, W.G. (1967) Statistical Methods, 6th edn. Iowa State University Press, Ames, Iowa, 593 pp. Stern, V.M., Smith, R.F., Van Den Bosch, R. and Hagen, K.S. (1959) The integrated control concept. Hilgardia 29, 81–101. Stone, N.D., Coulson, R.N., Frisbie, R.E. and Loh, D.K. (1986) Expert systems in entomology: three approaches to problem solving. American Entomologist 32, 161–166. Taylor, L.R. (1961) Aggregation, variance and the mean. Nature 189, 732–735. Teng, P.S. (1981) Validation of computer models of plant disease epidemics: a review of philosophy and methodology. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 88, 49–63. Teng, P.S. (1987) The systems approach to pest management. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp. 160–167. Walker, P.T. (1987) Quantifying the relationship between insect populations, damage, yield, and economic thresholds. In: Teng, P.S. (ed.) Crop Loss Assessment and Pest Management. American Phytopathological Society Press, St Paul, Minnesota, pp.114–125. Weisberg, S. (1980) Applied Linear Regression. John Wiley Press, New York, 283 pp. Zimmerman, K.M. (1999) A spatial model for markov chain analysis of grasshopper population dynamics in Wyoming. MS thesis, University of Wyoming, Laramie, Wyoming, 91 pp.

04IntpestManCh4.QXD 5/5/04 2:07 pm Page 55


Manipulation of Tritrophic Interactions for IPM

Robert H.J. Verkerk Department of Biological Sciences, Imperial College London, Silwood Park, Ascot, Berkshire, SL5 7PY, UK E-mail: [emailprotected]

Introduction Until recently, there has been a tendency by those involved in integrated pest management (IPM) or integrated crop management (ICM) (Meerman et al., 1996; Denyer, 2000) to be principally concerned with effects on herbivores or interactions between just two trophic levels. However, interest in the importance of interactions between the three or four trophic levels that characterize most natural systems and agroecosystems has been increasing rapidly during the last two decades. Historically, the chemical-control exponent has rarely been concerned about hostplant effects, and has been interested primarily in chemical impacts on herbivores (the second trophic level; Fig. 4.1) and sometimes side effects on natural enemies (third trophic level; Fig. 4.1). Understanding of interactions between the levels has not been prioritized (Thomas, 1999). Most hostplant resistance specialists are concerned mainly with ways in which resistance factors within or on the plant (first trophic level; Fig. 4.1) affect the development of herbivores, while the biological control specialist tends to concentrate on ways in which predators, parasitoids or pathogens (third trophic level; Fig. 4.1) are able to limit


NATURAL ENEMY Extrinsic plant resistance HERBIVORE Intrinsic plant resistance PLANT

Fourth trophic level

Third trophic level

Second trophic level

First trophic level

Fig. 4.1. Simplified multitrophic interactions in natural and agroecosystems (adapted from Price, 1986).

the abundance of and damage caused by herbivorous pests Following from this, the plant-resistance specialist has tended to have little interest in interactions between the first, second and third trophic levels, while the biological control specialist, in turn, has given only passing attention to interactions between the first and third trophic levels. In the case of some natural systems and many fewer crop-based systems, interactions between the third and fourth trophic levels have been well studied (e.g. parasitoid–hyperparasitoid interactions). It is interesting that many traditional cultural practices – one of the less-studied

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


04IntpestManCh4.QXD 14/4/04 2:24 pm Page 56


R.H.J. Verkerk

aspects of pest-management science – exert their effects through complex multitrophic interactions, but it is exactly this complexity that makes such systems difficult to assess experimentally or validate conclusively across a broad range of environments. The reality is that agroecosystems, especially perennial ones, which are not subject to intensive pesticide regimes, like natural systems, contain much more than simple tritrophic interactions. They support food-web interactions of varying complexity across multitrophic levels (Berryman et al., 1995; Janssen et al., 1998; Letourneau and Andow, 1999). Modelling approaches, using empirical data where these are available, are contributing substantially to the understanding of interactions in agroecosystems (Gutierrez, 1996). Research on tritrophic interactions relating to arthropod herbivores has expanded rapidly since the late 1970s (e.g. Bergman and Tingey, 1979; Price et al., 1980; Strong et al., 1984; Boethel and Eikenbary, 1986; Price, 1986; Duffey and Bloem, 1987; Barbosa, 1988; Gutierrez et al., 1988; Nordlund et al., 1988; Whitman, 1988; Smith, 1989; Price et al., 1990; Fritz, 1992; Hare, 1992; Vet and Dicke, 1992; Steinberg et al., 1993; Godfray, 1994; Mattiacci et al., 1994, 1995; Dicke et al., 1998; Du et al., 1998; Redman and Scriber, 2000; Walker and Jones, 2001). However, as implied above, there have been relatively few empirical studies on crop-based systems (van Emden, 1987, 1995; van Emden and Wratten, 1991; Hare, 1992; Shimoda et al., 1997) and rigorous field studies have only been conducted in the last few years (Eigenbrode et al., 1995; Camara, 1997; Fritz et al., 1997; Karban and EnglishLoeb, 1997; Nwanze et al., 1998; Hufbauer and Via, 1999; Theodoratus and Bowers, 1999; Lill and Marquis, 2001; Chen and Welter, 2002; Thaler, 2002). Studies in the tritrophic area are taking on a new significance as less pesticide-dependent, more ecologically based approaches to the management of pests are being demanded (Poppy, 1997; Bottrell et al., 1998; Verkerk et al., 1998). As knowledge of interactions across multitrophic systems both in nature and in agroecosystems expands, researchers and pest-management practitioners are beginning to find ways of manipulating interactions

across different trophic levels in order to develop more sustainable approaches to pest management. Some of the most relevant approaches are discussed in this chapter and are supported with examples. The chapter restricts itself to consideration of tritrophic aspects of arthropod pest management as arthropods have, to date been much better studied in this regard than pathogens.

Identifying Areas for Manipulation There are a number of key areas where manipulation of crop–pest–natural-enemy interactions could provide substantial benefits in pest-management systems. The significant and growing evidence from fundamental research in certain areas, e.g. allelochemically mediated interactions, hold substantial promise with regard to the development of novel IPM or ICM techniques, but practical methods have yet to be developed for wide-scale application. In other areas, techniques involving tritrophic interactions are already practised. Although these areas are considered discretely under different headings, it is important to appreciate the considerable overlap between different techniques or approaches. Some of the conflicts or paradoxes that may be inherent in certain forms of manipulation, are also outlined.

Manipulation of host-plant quality For many years, there was a widely held view that host-plant resistance should be seen as an integral component of IPM programmes, but it has been demonstrated that host-plant resistance is by no means always compatible with biological control (van Emden, 1991, 1995; Hare, 1992; Thomas and Waage, 1994). Hare (1992), for example, cited 16 studies where interactions between resistant crop varieties and natural enemies (parasitoids) were studied and the outcomes show a spectrum of interactions, ranging from synergistic, to additive, to none apparent through to disruptive or antagonistic. Negative interactions can occur because of the presence of secondary chemicals that are

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 57

Manipulation of Tritrophic Interactions

ingested or sequestered by natural enemies feeding on hosts present on resistant or partially resistant plants (Godfray, 1994). Specific toxic components in partially resistant soy bean plants can be particularly problematic in this regard (Orr and Boethel, 1985). van Emden (1995) suggests that negative interactions between potentially toxic secondary plant compounds and natural enemies are less likely in the case of natural enemies using phloem-feeding insects, such as aphids, as prey compared with chewing insects because, when present, these compounds are quite often at low concentrations or absent in the phloem (Ryan et al., 1990). van Emden (1995) cites a number of studies showing that partial plant resistance or environmental variables (e.g. reduced nitrogen fertilization of plants) can not only reduce aphid size and fecundity but may also substantially reduce (by c. 30%) the weight and fecundity of female parasitoids, Aphidius rhopalosiphi De Stefani Perez, emerging from the aphids. Also of potential concern to the biological control practitioner were the effects of plant resistance on sex ratio (10% fewer females on a partially resistant compared with a susceptible wheat variety) and parasitoid emergence success from aphid mummies (c. 20% reduction). A subsequent study has shown that linear furanocoumarins (secondary plant metabolites) in celery plants selectively and adversely affect the polyembryonic encyrtid parasitoid, Copidosoma floridanum, while not affecting its larval noctuid host, Trichoplusia ni (Hübner) (Reitz and Trumble, 1996). Negative interactions may also be caused by physical (or chemical) factors such leaf toughness, cuticle thickness, trichomes (glandular and nonglandular), galls and plant architecture (Price, 1986). In terms of positive interactions that can be manipulated, van Emden and Wearing (1965) were the first to suggest that partial plant resistance, in combination with natural enemies, may give economic levels of control for some agricultural insect pests. However, since this time, a considerable body of work has accumulated regarding mechanisms that both support and oppose this notion. Bottrell et al. (1998) provide a useful review of plant-


resistance–natural-enemy interactions. The authors emphasize that many of the interactions that occur in field systems are poorly understood and that combining natural enemies and plant resistance may slow the adaptation of some insect pests, while it may speed up adaptations of others. Feeny (1976) and others (e.g. Moran and Hamilton, 1980; Price et al., 1980; Leather, 1985) proposed that sublethal defences (e.g. ‘digestibility reducers’) in plants increase herbivore exposure to natural enemies: the slower the growth, the higher the mortality. This aside, several studies have shown that natural enemies foraging on leaf surfaces dislodge potential (aphid) prey to a greater extent on partially resistant compared with susceptible host plants. Gowling and van Emden (1994) showed this for Metopolophium dirhodum (Walker) and the parasitoid A. rhopalosiphi (on partially resistant and susceptible cultivars of wheat) in the glasshouse, as well as for Brevicoryne brassicae (Linnaeus) on Brussels sprouts in the field, where hover flies (Diptera: Syrphidae) were the main predatory group. However, field studies on galling sawflies of willow showed the opposite phenomenon, i.e. that parasitism was greater in fastergrowing larvae, implying that sublethal plant defences remain a paradox (Clancy and Price, 1987). Faster-growing larvae of the pyralid moth Omphalocerca munroei that fed on young leaves of their host plants (Asimina spp.) were also observed to be more vulnerable to predators than their slower-growing counterparts that fed on the preferred, older leaves of the same host plants (Damman, 1987). The latter studies support the view of Schultz (1983) that bigger individuals are a more profitable resource for predators. However, galling sawflies and the pyralid moth (a gregarious shelter-builder) both live in relatively protected but highly apparent environments (i.e. vulnerable to discovery by their enemies) and may not be ideal systems to test the slow growth/higher mortality hypothesis (Leather and Walsh, 1993). To examine this hypothesis, the latter authors infested ‘poor’- and ‘good’-quality hosts (Pinus contorta of two different origins) with the pine beauty moth, whose larvae are more

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 58


R.H.J. Verkerk

exposed on foliage. They found that larvae reared on the ‘good’ host, in the absence of predators, were heavier and more numerous than those reared in a similar manner on the ‘poor’ host. However, with populations suffering predation, it was found that these heavier individuals had been the ones favoured by the predators. This result suggests that the bigger and healthier the host, the greater the reward for the predator (see Schultz, 1983), and that poor nutritional status may be a liability to the plant in these circ*mstances rather than an asset. Host-plant quality may affect the influence of pathogens of insect pests. Differential susceptibility to a nuclear polyhedrosis virus (NPV) was found for two pests, beet armyworm, Spodoptera exigua (Hübner), and maize earworm, Helicoverpa zea (Boddie), fed on different host plants. Beet armyworm was most susceptible to the virus on tomato, least susceptible on cotton and intermediate on cole-wort, while maize earworm was most susceptible on maize, least on cotton and intermediate on bean (Farrar and Ridgway, 2000). The greenhouse whitefly, Trialeurodes vaporariorum (Westwood) was found to be considerably more susceptible to the fungal pathogens Beauveria bassiana and Paecilomyces fumosoroseus when reared on cucumber compared with tomato (Poprawski et al., 2000). Host-plant variation has been shown to contribute substantially to the toxicity of endotoxins of the bacterial pathogen Bacillus thuringiensis (Bt). More than fivefold differences in toxicity of Bt subsp. aizawai were found to diamondback moth, Plutella xylostella (Linnaeus), larvae when exposed to treated leaves of susceptible and partially resistant common cabbage (Brassica oleracea var. capitata) (Verkerk and Wright, 1996a), while a more than tenfold variation in toxicity of Bt subsp. kurstaki was shown to larvae of gypsy moth, Lymantria dispar (Linnaeus), when exposed on a range of different host plants (Farrar et al., 1996). There have been few studies looking at population-level effects of variable plant phenology. In one such study, the timing of egg hatch of the gypsy moth, L. dispar was manipulated in the field (Hunter and

Elkinton, 2000). When larvae fed on old leaves, i.e. larvae released long before budburst, the adult fecundity of the moth declined owing to the low quality of the host plant. However, where the leaves were old, the dispersal rate (by ‘ballooning’) was greater than from young leaves and, since dispersal reduces herbivore density, naturalenemy-induced density-dependent mortality was also lower (Hunter and Elkinton, 2000). This shows that first and third trophic-levelmediated effects may counteract each other in relation to herbivore survival or abundance. Finally, host-plant quality can have important implications for omnivores. This has been well studied in the case of western flower thrips, Frankliniella occidentalis (Pergande), which eats both animal prey (mite eggs) and host-plant foliage. According to foraging theory, omnivores balance their diet as a result of food quality, nutritional need and the availability of alternative foods. Although it has been shown that reducing plant quality can cause omnivores to shift towards relatively more predation than herbivory (Agrawal et al., 1999), it was later shown that where plant resistance has been induced by herbivory (induced plant resistance), reduced prey density and quality may antagonize this shift towards increased predation (Agrawal and Klein, 2000).

Allelochemicals Allelochemicals are those chemicals that mediate interspecific interactions and are distinguished from pheromones, which mediate intraspecific interactions. They have been shown to be among the most important factors controlling the sequence of naturalenemy host-searching and selection behaviours, and this has been particularly well studied in the case of parasitoids (Vinson, 1984; Lewis and Martin, 1990; Turlings and Tumlinson, 1991; Whitman and Eller, 1992; Tumlinson et al., 1993). The induction of plant defence through the release of allelochemicals as a response to herbivory has been amply demonstrated (e.g. Whitman and Eller, 1992; Steinberg et

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 59

Manipulation of Tritrophic Interactions

al., 1993; Takabayashi et al., 1994; Mattiacci et al., 1995; Du et al., 1996, 1998; Dicke et al., 1998; van Poecke et al., 2001). Such allelochemicals are often referred to as synomones, given that both the plant (emitter) and the natural enemy (receiver) benefit from the chemical communication. It has been shown that the allelochemicals released following herbivory not only influence specialist and/or generalist natural enemies but can also affect the behaviour of the herbivore and, through plant–plant communication, can make adjacent plants more attractive to natural enemies. The plant emissions can be herbivore-specific. De Moraes et al. (1998) showed that tobacco, cotton and maize plants each released distinct blends of volatiles when they were exposed to herbivory by two closely related Lepidoptera larvae, Heliothis virescens (Fabricius) and H. zea. In chemical/behavioural assays, these authors demonstrated that the specialist parasitoid Cardiochiles nigriceps Viereck was able to discriminate between these blends, being attracted specifically to its own host, H. virescens. Despite recent progress and an abundance of research in the area of allelochemically mediated tritrophic interactions, there have yet to be significant advances in the applied area, so there are few examples of synomones being used practically as an IPM technique. Lewis and Nordlund (1984) demonstrated the potential of synomonemediated attraction of natural enemies by applying synomone-containing extracts from maize and tomato. Parasitism by Telenomus remus Nixon of autumn armyworm, Spodoptera frugiperda (J.E. Smith) was increased twofold on plants treated with extracts, compared with the untreated plants. Limited field studies by Altieri et al. (1981) found that application of a waterbased extract from an Amaranthus sp. significantly increased parasitism of H. zea eggs by naturally occurring Trichogramma spp. in various crops, including soybean, cowpea, tomato and cotton. The prospects for manipulating predator– prey interactions via the first (plant) trophic level have yet to be fully realized. Dicke et al. (1990) provide a useful synthesis on specific


areas of allelochemical manipulation, drawing heavily on research on herbivorous and predatory mite systems. These authors cite work relating to: enhancement of searching efficiency or triggering specific search modes in natural enemies; increasing host acceptability to natural enemies in mass rearing; using the response to an allelochemical as a criterion in the selection of natural enemies in control programmes; ensuring quality control of mass-reared natural enemies; and breeding of plant cultivars that have high emission rates of natural-enemy-attracting synomones. Aphid parasitoids may be ‘conditioned’ during their larval stage to the specific hostplant variety on which the parasitoid’s host is reared (Braimah and van Emden, 1994; van Emden, 1995). This is potentially of considerable relevance to biological control since the introduction of a crop variety with resistance based on an allelochemical may actually deter parasitoids and the existence of host-plant conditioning could offset the usefulness of weed-based reservoirs of polyphagous parasitoids (van Emden, 1995). This phenomenon may also cause suboptimal parasitism following introduction of an exotic parasitoid where mass rearing has occurred on a host-plant variety different from that constituting the target crop. The rapidly growing body of work on allelochemicals demonstrates that the use of natural-enemy-attracting chemicals produced by plants may hold substantial promise for enhancement of biological control. This is most likely either through augmentation (field application of synomones) or by breeding of plants with elevated emission rates of synomones (see Genetic manipulation section below).

Crop diversification The diversification of crop and neighbouring environments is widely regarded as benefiting biological control and sustainable agriculture systems. It is based on the premise that habitats that are structurally, biologically or temporally diverse provide greater levels of habitat diversity, which in turn

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 60


R.H.J. Verkerk

diversifies the available prey, so increasing the abundance of natural enemies (Root, 1973). There are many ways in which diversification of the crop environment can be undertaken; most practical attempts rely on polycultures (multiple cropping) or the use of refugia. Despite the theoretical benefits of crop diversification, results from studies attempting to verify the benefits or otherwise of such practices have been mixed (Sheehan, 1986) and demonstrate the importance of understanding the nature of multitrophic interactions. One of the best-known practical examples of the benefits of mixed cropping was the rediversification of the cotton agroecosystem in the Cañete Valley in Peru, after massive bollworm outbreaks followed the abandonment of mixed cropping in the 1950s (Doutt and Smith, 1971). However, it should be borne in mind that some of these benefits occurred as a result of the cessation of highly intensive insecticide application regimes. Chen and Welter (2002) tested the hypothesis that herbivores are more abundant in agroecosystems compared with more diverse natural habitats, and studied the dynamics of the sunflower moth, hom*oeosoma electellum (Hulst) and its natural enemies in agricultural and native sunflower habitats. The authors showed clearly that sunflower moths were consistently more abundant in the agricultural habitats (with domesticated sunflowers) compared with the native ones (containing wild ancestors of the domesticated varieties). Additionally, parasitism rates of the herbivore were between six and ten times higher in the native compared with the agricultural habitats. One of the likely reasons for mixed results from studies investigating the effects of crop diversification on natural enemies is the presence of confounding factors (Barbosa and Wratten, 1998). Also, the results will inevitably be limited by the specific parameters measured.

tial and habitat differences, polycultures may give rise to changes in movement rate which can only be detected through season-long studies. For example, initial colonization by a eulophid parasitoid of the Mexican bean beetle, Epilachna varivestis Mulsant, was found to be greater in monoculture than in more diverse (intercropped) plots (Coll and Bottrell, 1996). But, because emigration from the monocultural plots occurred sooner, tenure time for the parasitoid in the intercropped plots was greater as the latter provided a more favourable habitat. Intercropping may increase the effects of natural enemies because one of the intercropped plants provides allelochemical attraction or a nectar source for natural enemies or because the intercrop improves conditions (e.g. moisture, shelter) for ground-dwelling predators (van Emden, 1989). Read et al. (1970) suggested that planting cole-worts near beet might enhance biological control of beet pests because cole-worts attract braconid parasitoids, e.g. Diaeretiella rapae M’Intosh, to the general area. Field studies in Mexico showed that parasitism of the pyralid Diaphania hyalinata was greater in tricultures (squash, maize, legumes) than in monocultures of squash (Letourneau, 1987), providing partial support for the ‘enemies hypothesis’ (Root, 1973), which dictates that natural enemies should be more abundant in diverse rather than in simple habitats. However, the author also found that parasitoid attack rates were elevated in maize monocultures and that predator abundance was not enhanced in the tricultures, some predator species being actually more abundant in the monocultures. The author concluded that particular vegetational associations can enhance naturalenemy activity, although the role of single-species effects can be obscured by a focus on diversity and these enhancement effects do not apply to all natural enemies (Letourneau, 1987).

Polycultures Gold et al. (1989) showed that the density of plants in a polyculture may confound the influence of plant diversity. Apart from spa-

Refugia and non-crop plants Knowledge that uncultivated land can support a diverse range of natural enemies,

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 61

Manipulation of Tritrophic Interactions

which can help to control pests on agricultural crops, has long been known. However, in many industrialized countries, the mechanization of agriculture, as well as the availability of high-yielding crop varieties and synthetic pesticides, has meant that pestmanagement programmes have often failed to emphasize the importance of naturalenemy refugia. In Britain, for example, hedgerows and uncultivated field margins were destroyed as a result of these modern technologies and only recently have there been attempts to reverse this trend in the wake of increasing awareness of the problems associated with large-scale monocultures and over-reliance on pesticides (van Emden, 1990). Within the crop, natural-enemy refugia can take the form of unsprayed crop areas, protected plant parts of the crop itself, noncrop plants that favour natural enemies or alternative hosts, which in turn encourage economically unimportant arthropods that provide an alternative food source for natural enemies. Outside the crop, uncultivated field margins, hedgerows, ‘conservation headlands’ and ‘live fences’ have all been used, at least in part, to provide refugia for natural enemies, which can subsequently move into the crop environment. The effective use of refugia generally requires a thorough knowledge of crop– pest–natural-enemy interactions. Spatial scales are particularly important (Murdoch and Briggs, 1996). It is often not sufficient simply to leave uncultivated sections within or outside the crop. The floral composition of refuges, their location and their dimensions should be carefully considered in relation to the specific crop–pest–natural-enemy situation in question. There are many examples in the literature indicating the effectiveness of natural-enemy refugia across a wide range of agroecosystems. Some examples are considered below. The planting of lucerne (Medicago sativa) strips in cotton fields in Australia has been shown to increase the abundance of important predators (Mensah, 1999). Predatory beetles, bugs and lacewings were five- to sevenfold more abundant in the lucerne strips than in the cotton crop itself and these


predators in turn migrated into the cotton and were on average twice as abundant in cotton with lucerne strips compared with cotton without the strips (Mensah, 1999). Wild brassicas (e.g. Barbarea vulgaris and Brassica kaber) planted in the vicinity of cultivated brassicas provide floral nectar reserves for parasitoids of the diamondback moth, P. xylostella, so improving the potential for biological control (Idris and Grafius, 1996). Such non-crop plants can sometimes provide a dual function in pest management, acting both as refuge sites for natural enemies and as trap crops for the pest. However, there is also the possibility that some plants known to favour natural enemies will also attract pests to the vicinity. Border-planting of Phacelia tanacetifolia (Hydrophyllaceae) as a floral (pollen) resource has also been shown to be effective in increasing the abundance of aphid-eating hover flies, the larvae of which are often key natural enemies of aphids (White et al., 1995). Adult female hover flies generally need to consume pollen before they can lay fertile eggs so it is important that such floral reserves are present close to the crop. The common farming practice of using plum trees as parasitoid refugia has been shown to improve biological control of the western grape leafhopper, Erythroneura elegantula Osborn in vineyards in the western USA (Murphy et al., 1996). Almost twice the abundance of the egg parasite Anagrus epos Girault was found in vineyards with plum tree refugia compared with those without, the trees acting both as overwintering sites and as wind-breaks, which aid parasitoid flight and dispersal (Murphy et al., 1996). Protected parts of certain crops that are relatively free from the disturbances associated with agronomic practices can also provide important refugia for natural enemies. For example, the areas beneath the plucking surface of tea plants are well known as a refuge for a range of natural enemies of important tea pests. Research has shown that domatia, which are small, sometimes elaborate pits or shelters at the junctures of veins on the lower surface of leaves of some plants, are inhabited primarily by predatory rather than herbivorous arthropods. A group

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 62


R.H.J. Verkerk

of researchers has shown that, by adding artificial domatia to cotton plants, fruit production could be increased by 30%, compared with control plants (Agrawal and Karban, 1997). This increase was caused by enhanced predation of herbivorous mites by predatory ones that were able to harbour in the artificial domatia (Agrawal and Karban, 1997). Some natural enemies overwinter within plant parts so the removal of stubble, fruits or other crop litter may be counterproductive as these plant parts act as refugia for the natural enemies. For example, in Australia, several species of predatory mite, Typhlodromus spp., have been shown to overwinter in the calyx cavities of apple fruits, so that early-season phytophagous mite control can be improved if apples are left on the ground through winter (Gurr et al., 1997).

Resource availability Population ecologists are actively debating the relative importance of bottom-up (resource-driven) and top-down (naturalenemy-driven) processes in the regulation of herbivores (Walker and Jones, 2001; Denno et al., 2002). Walker and Jones (2001) argue that the absence of empirical data and the desire by researchers to favour one of these processes to the exclusion of the other have greatly hampered the understanding of the interactions between these processes. Very little work of this type has been conducted in relation to agricultural systems, but models using limited empirical data are increasingly being used to elucidate the importance of these processes (Gutierrez, 1996). Denno et al. (2002) investigated the relative effects of bottom-up and top-down processes in both laboratory mesocosms and the field, using a non-agricultural Spartina grassland system. They found that changes in plant nutrition and structure had complex effects on natural-enemy and herbivore abundance and that these effects were not necessarily paralleled under laboratory and field conditions because of more complex interactions in the field. However, it was

shown that in some situations resource availability can override the importance of natural enemies, and this has potential applications for pest management in agriculture. The most common method of manipulating bottom-up processes in the field is by altering the fertilization regime. Differences in nutritional status of the host plant will have different effects on herbivores compared with natural enemies, and under some conditions the growth rate of natural enemy populations may not be able to ‘keep up’ with pest populations. Walde (1995) tested this hypothesis in a mite system and found that the growth rate of a phytophagous mite, Panonychus ulmi (Koch), in apple trees was non-linear in relation to increased addition of NKP fertilizer; the density increased and then decreased with the increasing N content of the leaves. Two key predatory mite species in this system were unable to compensate for the increased growth rate of the phytophagous mite, but the populations of the latter were none the less maintained beneath the economic threshold. Apart from affecting growth rates, fertilization may affect sex ratios of natural enemies. In studies of interactions between cole-worts, diamondback moth and its ichneumonid parasitoid, Diadegma insularis (Cresson), sex ratios of parasitoids emerging from hosts on plants treated with high levels of nitrogen were found to be consistently female-biased compared with those of parasitoids emerging from unfertilized plants, where sex ratios were male-biased with the implication of lower potential parasitism (Fox et al., 1990). A comprehensive study of the effects of nitrogen treatment of cole-worts greens on the vulnerability of the cabbage white butterfly, Pieris rapae (Linnaeus), to natural enemies showed that its larvae grew more slowly under low-nitrogen conditions and were more susceptible to ground-dwelling predators (Loader and Damman, 1991). This supported the slow growth/high mortality hypotheses of Feeny (1976) and Moran and Hamilton (1980) (see above). Interestingly, however, Loader and Damman (1991) found that emergence of pupal parasites, e.g.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 63

Manipulation of Tritrophic Interactions

Pteromalus spp., was greater on high-nitrogen plants, larvae on the low-nitrogen plants frequently dying as a result of stress-induced bacterial infection, so preventing complete development of the parasitoids.

Crop background Visual cues can influence host selection by both herbivores and natural enemies. Accordingly, crop background can have an influence on long-range searching. A number of insect pests and natural enemies have been shown to be differentially attracted to particular crop backgrounds. For example, cabbage aphid, B. brassicae, abundance was greater on Brussels sprout plants where they contrasted with a bare background compared with when the background consisted of a ‘carpet’ of weeds, cut regularly to avoid excessive competition with the crop (Smith, 1969). Smith (1969) and others (e.g. Kennedy et al., 1961; van Emden, 1965) showed that aphids were more strongly attracted to the crop when it contrasted with the bare background, but that relative attraction between different groups of natural enemies (Coccinelidae, Cecidomyiidae, Chrysopidae, Anthocoridae and Syrphidae) varied significantly (Smith, 1969). Smith (1969) suggested that aphid abundance could have been affected by differential attraction of natural enemies, with anthocorid predators being most strikingly enhanced in the weedy habitats. Van Emden (1989) noted that certain species of hover fly lay more eggs on aphidinfested crops when the ground is covered, but warned that other syrphid species prefer crops surrounded by bare soil.

Exogenous interactions The application of exogenous substances, such as botanical extracts, may have differential effects on pests and natural enemies that can be exploited as a biorational method in IPM. Although such substances do not necessarily affect interactions across three trophic levels, this possibility exists. The appreciation that partial host-plant resistance could


enhance parasitism of the diamondback moth, P. xylostella (Verkerk, 1995), led to the testing of low (sublethal) concentrations of neem seed kernel extract (from Azadirachta indica), on a host plant highly susceptible to P. xylostella. This botanical treatment was shown to enhance parasitism success by Diadegma semiclausum Hellen in the laboratory, although a dose fivefold greater than this parasitism-enhancing dose led to a drastically reduced rate of pupal emergence so effectively inhibiting parasitism (Verkerk and Wright, 1994). Verkerk and Wright (1994) suggested that observed increases in the rates of parasitoid pupation when hosts were maintained either on partially resistant host plants or susceptible plants treated with neem could be caused by stress-induced impairment of the host’s immune system. This phenomenon has previously been shown to occur in other host–parasitoid systems when the hosts were subjected to nutritional stress (see Godfray, 1994). Low doses of a neem extract and azadirachtin (a primary active ingredient of neem) on plants have been shown to reduce the fecundity of several aphid species (Lowery and Isman, 1994; Koul, 2003). It has also been suggested that sublethal doses of azadirachtin may make a significant contribution to the control of the peach–potato aphid, Myzus persicae (Sulzer), while having little or no adverse impact on parasitism by Aphidius matricariae Haliday (Sugden, 1994; Mordue et al., 1996). Laboratory studies showed that azadirachtin could enhance the toxicity of gypsy moth, L. dispar, NPV to its host, the combined effects of the insecticide and NPV being greater than either product applied on its own (Cook et al., 1996). In an IPM programme targeting the glasshouse whitefly, T. vaporariorum, conventional insecticides were used at one-third rates in conjunction with a mycoinsecticide (B. bassiana: Boveral®) and the encyrtid parasitoid, Encarsia formosa (Dirlbek et al., 1992). The selection of appropriate insecticides (at reduced rates), careful timing and integration of all three control methods gave optimum whitefly control on certain lines (e.g. Transvaal daisy) where one method alone was found to be inadequate.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 64


R.H.J. Verkerk

Although not tritrophic in nature, Chilcutt and Tabashnik (1997) investigated the effects of ditrophic (within-host) interactions between different phenotypes of P. xylostella, its endolarval braconid parasitoid Cotesia plutellae Kurdyumov and Bt. The outcome of the interaction was dependent on the host phenotype (Bt-resistant or Btsusceptible). In susceptible hosts the parasitoid did not affect performance of the pathogen, in moderately resistant hosts the interaction was symmetrical and competitive, while highly resistant hosts were not susceptible to the pathogen, which created a refugium from competition for the parasitoid (Chilcutt and Tabashnik, 1997). These studies demonstrate the considerable scope for integration of chemical and biological control within a multitrophic context (see also Wright and Verkerk, 1995).

Genetic manipulation To date, most of the work on genetic manipulation for pest-management purposes, through either plant breeding or genetic engineering, has involved host plants. This has been mainly through the development of transgenic crops containing endotoxins from Bt (Brar and Khush, 1993; Daly et al., 1994; Tabashnik, 1994; Metz et al., 1995). Virtually no work has been carried out on breeding programmes or genetic engineering that affects natural enemies, despite the recognized key importance of natural enemies in pest management (Groot and Dicke, 2002). Genetic manipulation of insects (pests and natural enemies) for pest management is in its infancy but it is thought that it will become increasingly important as nonpesticidal approaches gain increasing favour in IPM (DeVault et al., 1996). As transgenic crops become more widely adopted, concerns about their potential natural-enemy and non-target impacts, as well as the likelihood of their inducing resistance to toxic principles, are increasing. In a review by Groot and Dicke (2002), the possible effects of insect-resistant transgenic and non-transgenic crops on food webs are considered. Because Bt toxins maintain their tox-

icity when bound to the soil, there is a real possibility of non-target impacts, although the effects may be indirect and difficult to evaluate. Some fauna (e.g. earthworms and some non-target herbivores) are not directly affected by the toxins, but the toxins may be ingested subsequently by susceptible invertebrates (Groot and Dicke, 2002). The potential risk of insects developing resistance to toxins in such transgenic crops has been recognized by many researchers (e.g. Strong et al., 1990; Menken et al., 1992; Daly et al., 1994), while others have argued that the risk may be smaller than that of the use of the same toxic principles in sprays (e.g. Roush, 1994). Transgenic crops such as cotton have also been known to trigger secondary pest outbreaks (e.g. Heteroptera: Miridae: see Fitt et al., 1994; Hardee and Bryan, 1997), which may need to be controlled with conventional insecticide sprays. These insecticides have the potential to harm natural enemies. Strong et al. (1990) argued that transgenic techniques need to be refined so that toxins are only expressed in a subset of crucial tissues and at specific developmental stages and they should also be integrated into an ecological framework if they are to be effective and contribute to biocontrol. Van Emden and Wratten (1991) warned that modern gene-transfer techniques aimed at creating resistant crop varieties are more likely than traditional plant-breeding methods to use an allelochemical mechanism of resistance (antibiosis), which might be damaging to natural enemies and other nontarget organisms. Genetic manipulation of crop plants to enhance nutrient uptake has been considered and could be compatible with IPM/ICM systems (Johansen et al., 1995). The potential also exists for creating genetically engineered plants that emit increased amounts of natural-enemy-attracting volatiles (synomones), although such plants are yet to be available commercially.

Tritrophic Models The intrinsic complexity of multitrophic interactions in agroecosystems and the diffi-

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 65

Manipulation of Tritrophic Interactions

culty of generating meaningful empirical data from the field have meant that modelling approaches have been used to facilitate the understanding of mechanisms and processes. Simulation models of crop–pest– natural-enemy systems used to date (e.g. Gutierrez, 1996) are based on detailed field and laboratory data. The models integrate the biology and physiology of consumers, which in turn affect resource acquisition and allocation and hence population birth and death rates. Resource availability (i.e. bottom-up effects) define the underlying base dynamics of each species, while natural enemies provide the top-down or regulatory effects (Gutierrez, 1996). Simulation models have been used to assist in the tactical evaluation of various biological control and plant-resistance interactions (e.g. Gutierrez et al., 1984, 1988, 1994) and simple analytical models (e.g. Hassell, 1978) have been used to make very general population-dynamics predictions. However, there have been very few studies that have examined tritrophic interactions using biologically realistic but quantitative population-dynamics models (see Gutierrez et al., 1993). The relatively recent application of age-structured models written as a series of delay-differential equations (Nisbet and Gurney, 1983) has promoted a middle approach between tactical and strategic predictive modelling, which may lead to a better understanding of pest–natural-enemy interactions under field conditions. Such models have been termed ‘models of intermediate complexity’ (e.g. Godfray and Waage, 1991; Briggs and Godfray, 1995) and can be applied to tritrophic systems (Thomas and Waage, 1994), although to date these models have been largely concerned with second and third trophic-level interactions (Gutierrez et al., 1994). A complex, metapopulation tritrophic model of the African cassava system was developed recently by Gutierrez et al. (1999). The model is based on a single-patch agestructured population-dynamics model, taking into account key plants and animals in the system. It also accounts for movement rates of animals between patches, these being dependent on species-specific


supply–demand relations. The model demonstrates the importance of plant-level effects on higher trophic levels. Such models can be very valuable tools in understanding agroecosystems, which can in turn facilitate better management of biological- or culturalcontrol programmes in IPM.

Conclusions Improving the understanding of multitrophic systems is critical to the development of sustainable, less pesticide-dependent or pesticide-free pest-management systems (Bottrell et al., 1998). This is because control techniques, or target pests, cannot be regarded in isolation – manipulation of any single factor will tend to have knock-on effects on different trophic levels. From a commercial point of view, the areas with greatest potential are likely to be allelochemical and genetic manipulations. However, it should be recognized that at present the biological control market is estimated to be in the region of only US$75 million (Waage, 1997), compared with the US$32 billion global agricultural-chemical market (Warrior, 2000). Thomas (1999) reasons that increasing our basic understanding of how individual pestcontrol technologies act and interact will reveal new opportunities for improving pest control. There is a great need to break away from the existing singletechnology, pesticide-dominated paradigm and to adopt a more ecological approach built around a fundamental understanding of population biology at the local farm level and the true integration of renewable technologies such as host plant resistance and natural biological control, which are available to even the most resource-poor farmers.

(Thomas, 1999) As the popularity of organic agriculture increases and pesticide-related problems (e.g. residues, resistance, side effects) continue to mount, there will be an ever greater requirement for effective and reasonably predictable natural control systems (see Verkerk and Wright, 1996b). A study of 18 commercial tomato farms in California,

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 66


R.H.J. Verkerk

half certified organic production systems, half conventionally managed and using synthetic pesticides, showed clearly the viability of organic systems (Letourneau and Goldstein, 2001). Benefits of the organic systems included greater naturalenemy diversity and abundance of functional guilds. In the interest of agricultural sustainability, tritrophic manipulation, as a dis-

tinct approach to biological and/or cultural control, is likely to be prioritized increasingly by both researchers and those responsible for the development and practical implementation of pest-management programmes. This process will be facilitated as improvements in the understanding of crop–pest–natural-enemy evolution and interactions are achieved (Bottrell et al., 1998).

References Agrawal, A.A. and Karban, R. (1997) Domatia mediate plant–arthropod mutualism. Nature 387, 562–563. Agrawal, A.A. and Klein, C.N. (2000) What omnivores eat: direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. Journal of Animal Ecology 69, 525–535. Agrawal, A.A., Kobayashi, C. and Thaler, J.S. (1999) Influence of prey availability and induced host-plant resistance on omnivory by western flower thrips. Ecology 80, 518–523. Altieri, M.A., Lewis, W.J., Nordlund, D.A., Gueldner, R.C. and Todd, J.W. (1981) Chemical interactions between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecology 3, 259–263. Barbosa, P. (1988) Natural enemies and herbivore plant interactions: Influence of plant allelochemicals and host specificity. In: Barbosa, P. and Letourneau, D.K. (eds) Novel Aspects of Insect–Plant Allelochemicals and Host Specificity. John Wiley & Sons, New York, pp. 201–229. Barbosa, P. and Wratten, S.D. (1998) Influence of plants on invertebrate predators: implications to conservation biological control. In: Barbosa, P. (ed.) Conservation Biological Control. Academic Press, San Diego, California, pp. 83–100. Bergman, J.M. and Tingey, W.M. (1979) Aspects of interactions between plant genotypes and biological control. Bulletin of the Entomological Society of America 25, 275–279. Berryman, A.A., Michalski, J., Gutierrez, A.P. and Arditi, R. (1995) Logistic theory of food web dynamics. Ecology 76, 336–343. Boethel, D.J. and Eikenbary, R.D. (1986) Interactions of Plant Resistance and Parasitoids and Predators of Insects. Wiley & Sons, Chichester, UK, 224 pp. Bottrell, D.G., Barbosa, P. and Gould, F. (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annual Review of Entomology 43, 347–367. Braimah, H. and van Emden, H.F. (1994) The role of the plant in host acceptance by the parasitoid Aphidius rhopalosiphi (Hymenoptera: Braconidae). Bulletin of Entomological Research 84, 303–306. Brar, D.S. and Khush, G.S. (1993) Application of biotechnology in integrated pest management. Journal of Insect Science 6, 7–14. Briggs, C.J. and Godfray, H.C.J. (1995) The dynamics of insect–pathogen interactions in stage-structured populations. American Naturalist 145, 855–887. Camara, M.D. (1997) Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable? Journal of Chemical Ecology 23, 2093–2106. Chen, Y.H. and Welter, S.C. (2002) Abundance of a native moth hom*oeosoma electellum (Lepidoptera: Pyralidae) and activity of indigenous parasitoids in native and agricultural sunflower habitats. Environmental Entomology 31, 626–636. Chilcutt, C.F. and Tabashnik, B.E. (1997) Host-mediated competition between the pathogen Bacillus thuringiensis and the parasitoid Cotesia plutellae of the diamondback moth (Lepidoptera: Plutellidae). Environmental Entomology 26, 38–45. Clancy, K.M. and Price, P.W. (1987) Rapid herbivore growth enhances enemy attack: sublethal plant defences remain a paradox. Ecology 68, 733–737. Coll, M. and Bottrell, D.G. (1996) Movement of an insect parasitoid in simple and diverse plant assemblages. Ecological Entomology 21, 141–149.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 67

Manipulation of Tritrophic Interactions


Cook, S.P., Webb, R.E. and Thorpe, K.W. (1996) Potential enhancement of the gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus with the triterpene azadirachtin. Environmental Entomology 25, 1209–1214. Daly, J.C., Hokkanen, H.M.T. and Deacon, J. (1994) Ecology and resistance management for Bacillus thuringiensis transgenic plants. Biocontrol Science and Technology 4, 563–571. Damman, H. (1987) Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology 68, 88–97. De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. and Tumlinson, J.H. (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573. Denno, R.F., Gratton, C., Peterson, M.A., Langellotto, G.A., Finke, D.L. and Huberty, A.F. (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology 83, 1443–1458. Denyer, R. (2000) Integrated crop management: introduction. Pest Management Science 56, 945–946. DeVault, J.D., Hughes, K.J., Johnson, O.A. and Narang, S.K. (1996) Biotechnology and new integrated pest management approaches. Bio-technology 14, 46–49. Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J. and Posthumus, M.A. (1990) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16, 3091–3118. Dicke, M., Takabayashi, J., Posthumus, M.A., Schutte, C. and Krips, O.E. (1998) Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Experimental and Applied Acarology 22, 311–333. Dirlbek, J., Dirlbekova, O. and Jedlicka, M. (1992) The combined use of mycoinsecticide, parasitoid and chemical stressor in the control of greenhouse whitefly (Trialeurodes vaporariorum Westwood). Ochrana Rostlin 28, 71–77. Doutt, R.L. and Smith, R.F. (1971) The pesticide syndrome – diagnosis and suggested prophylaxis. In: Huffaker, C.B. (ed.) Biological Control. Plenum Press, New York, pp. 3–15. Du, Y.J., Poppy, G.M. and Powell, W. (1996) Relative importance of semiochemicals from first and second trophic levels in host foraging behaviour of Aphidius ervi. Journal of Chemical Ecology 22, 1591–1605. Du, Y.J., Poppy, G.M., Powell, W., Pickett, J.A., Wadhams, L.J. and Woodco*ck, C.M. (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of Chemical Ecology 24, 1355–1368. Duffey, S.S. and Bloem, K.A. (1987) Plant defence-herbivore-parasite interactions and biological control. In: Kogan, M. (ed.) Ecological Theory and Integrated Pest Management Practice. Wiley & Sons, New York, pp. 135–184. Eigenbrode, S.D., Moodie, S. and Castagnola, T. (1995) Predators mediate host plant resistance to a phytophagous pest in cabbage with glossy leaf wax. Entomologia Experimentalis et Applicata 77, 335–342. Farrar, R.R. and Ridgway, R.L. (2000) Host plant effects on the activity of selected nuclear polyhedrosis viruses against the corn earworm and beet armyworm (Lepidoptera : Noctuidae). Environmental Entomology 29, 108–119. Farrar, R.R., Martin, P.A.W. and Ridgway, R.L. (1996) Host plant effects on activity of Bacillus thuringiensis against gypsy moth (Lepidoptera: Lymantriidae) larvae. Environmental Entomology 25, 1215–1223. Feeny, P. (1976) Plant apparency and chemical defence. In: Wallace, J.W. and Mansell, R.L. (eds) Biochemical Interaction between Plants and Insects. Plenum Press, New York, pp. 1–40. Fitt, G.P., Mares, C.L. and Llewellyn, D.J. (1994) Field-evaluation and potential ecological impact of transgenic cottons (Gossypium hirsutum) in Australia. Biocontrol Science and Technology 4, 535–548. Fox, L.R., Letourneau, D.K., Eisenbach, J. and van Nouhuys, S. (1990) Parasitism rates and sex ratios of a parasitoid wasp: effects of herbivore and plant quality. Oecologia 83, 414–419. Fritz, R.S. (1992) Community structure and species interactions of phytophagous insects on resistant and susceptible host plants. In: Fritz, R.S. and Simms, E.L. (eds) Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics. University of Chicago Press, Chicago, Illinois, pp. 240–277. Fritz, R.S., McDonough, S.E. and Rhoads, A.G. (1997) Effects of plant hybridization on herbivoreparasitoid interactions. Oecologia 110, 360–367. Godfray, H.C.J. and Waage, J.K. (1991) Predictive modelling in biological control: the mango mealy bug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology 28, 434–453. Godfray, H.J.H. (1994) Parasitoids – Behavioural and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey, 473 pp. Gold, C.S., Altieri, M.A. and Bellotti, A.C. (1989) The effects of intercropping and mixed varieties of predators and parasitoids of cassava whiteflies (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 79, 115–121.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 68


R.H.J. Verkerk

Gowling, G.R. and van Emden, H.F. (1994) Falling aphids enhance impact of biological control by parasitoids on partially aphid-resistant plant varieties. Annals of Applied Biology 125, 233–242. Groot, A.T. and Dicke, M. (2002) Insect-resistant transgenic plants in a multi-trophic context. Plant Journal 31, 387–406. Gurr, G.M., Thwaite, W.G., Valentine, B.J. and Nicol, H.I. (1997) Factors affecting the presence of Typhlodromus spp. (Acarina: Phytoseiidae) in the calyx cavities of apple fruits and implications for integrated pest management. Experimental and Applied Acarology 21, 357–364. Gutierrez, A.P. (1996) Applied Population Ecology: a Supply–Demand Approach. John Wiley & Sons, New York, 300 pp. Gutierrez, A.P., Baumgaertner, J.V. and Summers, C.G. (1984) Multitrophic models of predator prey energetics. I. Age-specific energetics models – pea aphid Acrythosiphon pisum (Harris) (hom*optera: Aphidae) as an example. Canadian Entomologist 116, 924–932. Gutierrez, A.P., Wermelinger, B., Schulthess, F., Baumaertner, J.V., Herren, H.R., Elliss, C.K. and Yaninek, J.S. (1988) Analysis of biological control of cassava pests in Africa. I. Simulation of carbon, nitrogen and water dynamics in cassava. Journal of Applied Ecology 25, 901–920. Gutierrez, A.P., Neuenschwander, P. and van Alphen, J.J.M. (1993) Factors affecting biological control of cassava mealybug by exotic parasitoids: a ratio-dependent supply–demand driven model. Journal of Applied Ecology 30, 706–721. Gutierrez, A.P., Mills, N.J., Schreiber, S.J. and Ellis, C.K. (1994) A physiologically based tritrophic perspective on bottom-up–top-down regulation of populations. Ecology 75, 2227–2242. Gutierrez, A.P., Yaninek, J.S., Neuenschwander, P. and Ellis, C.K. (1999) A physiologically-based tritrophic metapopulation model of the African cassava food web. Ecological Modelling 123, 225–242. Hardee, D.D. and Bryan, W.W. (1997) Influence of Bacillus thuringiensis-transgenic and nectarless cotton on insect populations with special emphasis on the tarnished plant bug (Heteroptera: Miridae). Journal of Economic Entomology 90, 663–668. Hare, D.J. (1992) Effects of plant variation on herbivore–enemy interactions. In: Fritz, R.S. and Simms, E.L. (eds) Plant Resistance to Herbivores and Pathogens. University of Chicago Press, Chicago, Illinois, pp. 278–298. Hassell, M.P. (1978) The Dynamics of Arthropod Predator–Prey Systems. Princeton University Press, Princeton, New Jersey, 237 pp. Hufbauer, R.A. and Via, S. (1999) Evolution of an aphid–parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53, 1435–1445. Hunter, A.F. and Elkinton, J.S. (2000) Effects of synchrony with host plant on populations of a springfeeding lepidopteran. Ecology 81, 1248–1261. Idris, A.B. and Grafius, E. (1996) Effects of wild and cultivated host plants on oviposition, survival, and development of diamondback moth (Lepidoptera: Plutellidae) and its parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Environmental Entomology 25, 825–833. Janssen, A., Pallini, A., Venzon, M. and Sabelis, M.W. (1998) Behaviour and indirect interactions in food webs of plant-inhabiting arthropods. Experimental and Applied Acarology 22, 497–521. Johansen, C., Lee, K.K., Sharma, K.K., Subbarao, G.V. and Kueneman, E.A. (1995) Genetic manipulation of crop plants to enhance integrated nutrient management in cropping systems. 1. Phosphorus. In: Proceedings of an FAO–ICRISAT Expert Consultancy Workshop, Patancheru, India, 15–18 March 1994. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, India, 177 pp. Karban, R. and EnglishLoeb, G. (1997) Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78, 603–611. Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1961) Host finding by aphids in the field. III. Visual attraction. Annals of Applied Biology 49, 1. Koul, O. (2003) Variable efficacy of neem-based formulations and azadirachtin to aphids and their natural enemies. In: Koul, O., Dhaliwal, G.S., Marwaha, S.S. and Arora, J.K. (eds) Biopesticides and Pest Management, Vol. 1. Campus Books International, New Delhi, pp. 64–74. Leather, S.R. (1985) Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecological Entomology 10, 213–217. Leather, S.R. and Walsh, P.J. (1993) Sub-lethal plant defences: the paradox remains. Oecologia 93, 153–155. Letourneau, D.K. (1987) The enemies hypothesis: tritrophic interactions and vegetational diversity in tropical agroecosystems. Ecology 68, 1616–1622. Letourneau, D.K. and Andow, D.A. (1999) Natural-enemy food webs. Ecological Applications 9, 363–364.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 69

Manipulation of Tritrophic Interactions


Letourneau, D.K. and Goldstein, B. (2001) Pest damage and arthropod community structure in organic vs. conventional tomato production in California. Journal of Applied Ecology 38, 557–570. Lewis, W.J. and Martin, W.R. (1990) Semiochemicals for use with parasitoids: status and future. Journal of Chemical Ecology 16, 3067–3089. Lewis, W.J. and Nordlund, D.A. (1984) Semiochemicals influencing fall armyworm parasitoid behavior: implications for behavioral manipulation. Florida Entomologist 67, 343–349. Lill, J.T. and Marquis, R.J. (2001) The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126, 418–428. Loader, C. and Damman, H. (1991) Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 72, 1586–1590. Lowery, D.T. and Isman, M.B. (1994) Insect growth-regulating effects of a neem extract and azadirachtin on aphids. Entomologia Experimentalis et Applicata 72, 77–84. Mattiacci, L., Dicke, M. and Posthumus, M.A. (1994) Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae – role of mechanical damage and herbivore elicitor. Journal of Chemical Ecology 20, 2229–2247. Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) Beta-glucosidase – an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences of the USA 92, 2036–2040. Meerman, F., van den Ven, G.W.J., van Keulen, H. and Breman, H. (1996) Integrated crop management: an approach to sustainable agricultural development. International Journal of Pest Management 42, 13–24. Menken, S.B.J., Visser, J.H. and Harrewijn, P. (1992) Proceedings of the 8th International Symposium on Insect–Plant Relationships. Series Entomologica Vol. 49, Kluwer Academic Publishers, Dordrecht, The Netherlands, 424 pp. Mensah, R.K. (1999) Habitat diversity: implications for the conservation and use of predatory insects of Helicoverpa spp. in cotton systems in Australia. International Journal of Pest Management 45, 91–100. Metz, T.D., Roush, R.T., Tang, J.D., Shelton, A.M. and Earle, E.D. (1995) Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein – implications for pest resistance management strategies. Molecular Breeding 1, 309–317. Moran, N. and Hamilton, W.D. (1980) Low nutritive quality as defence against herbivores. Journal of Theoretical Biology 86, 247–254. Mordue, A.J., Nisbet, A.J., Nasiruddin, M. and Walker, E. (1996) Differential thresholds of azadirachtin for feeding deterrence and toxicity in locusts and an aphid. Entomologia Experimentalis et Applicata 80, 69–72. Murdoch, W.W. and Briggs, C.J. (1996) Theory for biological control: recent developments. Ecology 77, 2001–2013. Murphy, B.C., Rosenheim, J.A. and Granett, J. (1996) Habitat diversification for improving biological control: abundance of Anagrus epos (Hymenoptera: Mymaridae) in grape vineyards. Environmental Entomology 25, 495–504. Nisbet, R.M. and Gurney, W.S.C. (1983) The systematic formulation of population models for insects with dynamically varying instar duration. Theoretical Population Biology 23, 114–135. Nordlund, D.A., Lewis, W.J. and Altieri, M.A. (1988) Influences of plant produced allelochemicals on the host–prey selection behaviour of entomophagous insects. In: Barbosa, P. and Letourneau, D.K. (eds) Novel Aspects of Insect–Plant Interactions. John Wiley & Sons, New York, pp. 65–95. Nwanze, K.F., Reddy, Y.V.R., Nwilene, F.E., Kausalya, K.G. and Reddy, D.D.R. (1998) Tritrophic interactions in sorghum, midge (Stenodiplosis sorghicola) and its parasitoid (Aprostocetus spp.). Crop Protection 17, 165–169. Orr, D.B. and Boethel, D.J. (1985) Comparative development of Copidosoma truncatellum (Hymenoptera: Encyrtidae) and its host, Pseudoplusia includens (Lepidoptera: Noctuidae), on resistant and susceptible soybean genotypes. Environmental Entomology 14, 612–616. Poppy, G.M. (1997) Tritrophic interactions: improving ecological understanding and biological control? Endeavour 21, 61–65. Poprawski, T.J., Greenberg, S.M. and Ciomperlik, M.A. (2000) Effect of host plant on Beauveria bassiana and Paecilomyces fumosoroseus-induced mortality of Trialeurodes vaporariorum (hom*optera : Aleyrodidae). Environmental Entomology 29, 1048–1053. Price, P.W. (1986) Ecological aspects of host plant resistance and biological control: interactions among three trophic levels. In: Boethel, D.J. and Eikenbary, R.D. (eds) Interactions of Plant Resistance and Parasitoids and Predators of Insects. Ellis Horwood, Chichester, UK, pp. 11–30.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 70


R.H.J. Verkerk

Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N. and Weis, A.E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41–65. Price, P.W., Cobb, N., Craig, T.P, Fernandes, G.W., Tami, J.K., Mopper, S. and Preszler, R.W. (1990) Insect herbivore population dynamics on trees and shrubs: new approaches relevant to latent and eruptive species and life table development. In: Bernays, E.A. (ed.) Insect–Plant Interactions, Vol. 2. CRC Press, Boca Raton, Florida, pp. 2–38. Read, D.P., Feeny, P.P. and Root, R.B. (1970) Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Canadian Entomologist 102, 1567–1578. Redman, A.M. and Scriber, J.M. (2000) Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids. Oecologia 125, 218–228. Reitz, S.R. and Trumble, J.T. (1996) Tritrophic interactions among linear furanocoumarins, the herbivore Trichoplusia ni (Lepidoptera: Noctuidae), and the polyembryonic parasitoid Copidosoma floridanum (Hymenoptera: Enccyrtidae). Environmental Entomology 25, 1391–1397. Root, R.B. (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monographs 43, 95–124. Roush, R.T. (1994) Managing pests and their resistance to Bacillus thuringiensis – can transgenic crops be better than sprays? Biocontrol Science and Technology 4, 501–516. Ryan, J.D., Morgham, P.E., Richardson, R.C., Johnson, R.C., Mort, A.J. and Eikenbary, R.D. (1990) Greenbug and wheat: a model system for the study of phytotoxic hom*optera. In: Campbell, R.K. and Eikenbary, R.D. (eds) Aphid–Plant Genotype Interactions. Elsevier, Amsterdam, pp. 171–186 Schultz, J.C. (1983) Impact of variable plant defensive chemistry on susceptibility of insects to natural enemies. American Chemical Society Symposium Series 208, 37–54. Sheehan, W. (1986) Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environmental Entomology 15, 456–461. Shimoda, T., Takabayashi, J., Ashihara, W. and Takafuji, A. (1997) Response of predatory insect Scolothrips takahashii toward herbivore-induced plant volatiles under laboratory and field conditions. Journal of Chemical Ecology 23, 2033–2048. Smith, C.M. (1989) Plant Resistance to Insects: a Fundamental Approach. John Wiley & Sons, New York, 286 pp. Smith, J.G. (1969) Some effects of crop background on populations of aphids and their natural enemies on brussels sprouts. Annals of Applied Biology 63, 326–330. Steinberg, S., Dicke, M. and Vet, L.E.M. (1993) Relative importance of infochemicals from 1st and 2nd trophic level in long-range host location by the larval parasitoid Cotesia glomerata. Journal of Chemical Ecology 19, 47–59. Strong, D.R., Lawton, J.H. and Southwood, T.R.E. (1984) Insects on Plants. Blackwell Scientific Publications, Oxford, 313 pp. Strong, D.R., Baker, R.R. and Dunn, P.E. (1990) Interface of natural enemy and environment. UCLA Symposia on Molecular and Cellular Biology 112, 57–64. Sugden, M.R. (1994) The effects of azadirachtin on Myzus persicae and its hymenopterous parasitoid Aphidius matricariae. MSc thesis, University of Aberdeen, UK. Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39, 47–79. Takabayashi, J., Dicke, M. and Posthumus, M.A. (1994) Volatile herbivore-induced terpenoids in plant mite interactions – variation caused by biotic and abiotic factors. Journal of Chemical Ecology 20, 1329–1354. Thaler, J.S. (2002) Effect of jasmonate-induced plant responses on the natural enemies of herbivores. Journal of Animal Ecology 71, 141–150. Theodoratus, D.H. and Bowers, M.D. (1999) Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider, Lycosa carolinensis. Journal of Chemical Ecology, 25, 283–295. Thomas, M.B. (1999) Ecological approaches and the development of ‘truly integrated’ pest management. Proceedings of the National Academy of Sciences of the USA 96, 5944–5951. Thomas, M.B. and Waage, J.K. (1994) Integration of Biological Control and Host Plant Resistance Breeding. CAB International, Wallingford, UK, 139 pp. Tumlinson, J.H., Turlings, T.C.J. and Lewis, W.J. (1993) Semiochemically mediated foraging behavior in beneficial parasitic insects. Archives of Insect Biochemistry and Physiology 22, 385–391.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 71

Manipulation of Tritrophic Interactions


Turlings, T.C.J. and Tumlinson, J.H. (1991) Do parasitoids use herbivore-induced plant chemical defenses to locate hosts? Florida Entomologist 74, 42–50. van Emden, H.F. (1965) The effect of uncultivated land on the distribution of cabbage aphid (Brevicoryne brassicae) on an adjacent crop. Journal of Applied Ecology 2, 171. van Emden, H.F. (1987) Cultural methods: the plant. In: Burn, A.J., Coaker, T.H. and Jepson, P.C. (eds) Integrated Pest Management. Academic Press, London, pp. 27–68. van Emden, H.F. (1989) Pest Control, 2nd edn. Edward Arnold, London, 117 pp. van Emden, H.F. (1990) Plant diversity and natural enemy efficiency in agroecosystems. In: Mackauer, M., Ehler, L.E. and Roland J. (eds) Critical Issues in Biological Control. Intercept, Andover, UK, pp. 63–80. van Emden, H.F. (1991) The role of host plant resistance in insect pest mis-management. Bulletin of Entomological Research 81, 123–126. van Emden, H.F. (1995) Host plant–Aphidophaga interactions. Agriculture, Ecosystems and Environment 52, 3–11. van Emden, H.F. and Wearing, C.H. (1965) The role of the host plant in delaying economic damage levels in crops. Annals of Applied Biology 56, 323–324. van Emden, H.F. and Wratten, S.D. (1991) Tri-trophic interactions involving plants in the biological control of aphids. In: Peters, D.C., Webster, J.A. and Chouber, C.S. (eds) Aphid–Plant Interactions: Populations to Molecules. Agricultural Research Service, USDA Oklahoma State University, Stillwater, Oklahoma, pp. 29–43. van Poecke, R.M.P., Posthumus, M.A. and Dicke, M. (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. Journal of Chemical Ecology 27, 1911–1928. Verkerk, R.H.J. (1995) Studies on interactions between diamondback moth, host plants, endolarval parasitoids and selective toxicants. PhD thesis, University of London, UK, 244 pp. Verkerk, R.H.J. and Wright, D.J. (1994) The potential for induced extrinsic host plant resistance in IRM strategies targeting the diamondback moth. In: Proceedings – Brighton Crop Protection Conference: Pests and Diseases – 1994. British Crop Protection Council, Farnham, UK, pp. 457–462. Verkerk, R.H.J. and Wright, D.J. (1996a) The effects of host plant-selective insecticide interactions on larvae of Plutella xylostella (Lepidoptera: Yponomeutidae) in the laboratory. Pesticide Science 44, 171–181. Verkerk, R.H.J. and Wright, D.J. (1996b) Multitrophic interactions and management of the diamondback moth. Bulletin of Entomological Research 86, 205–216. Verkerk, R.H.J., Leather, S.R. and Wright, D.J. (1998) The potential for manipulating crop pest-natural enemy interactions for improved insect pest management. Bulletin of Entomological Research 88, 493–501. Vet, L.E.M. and Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141–172. Vinson, S.B. (1984) How parasitoid locate their hosts: a case of insect espionage. In: Lewis, T. (ed.) Insect Communications. Academic Press, London, pp. 325–348. Waage, J. (1997) What does biotechnology bring to integrated pest management? Biotechnology and Development Monitor 32, 19–21. Walde, S.J. (1995) How quality of host-plant affects a predator-prey interaction in biological control. Ecology 76, 1206–1219. Walker, M. and Jones, T.H. (2001) Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant-insect herbivore-natural enemy systems. Oikos 93, 177–187. Warrior, P. (2000) Living systems as natural crop-protection agents. Journal of Pest Management Science 56, 681–687. White, A.J., Wratten, S.D., Berry, N.A. and Weigmann, U. (1995) Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera: Syrphidae). Journal of Economic Entomology 88, 1171–1176. Whitman, D.W. (1988) Allelochemical interactions among plants, herbivores and predators. In: Barbosa, P. and Letourneau, D.K. (eds) Novel Aspects of Insect-Plant Interactions. John Wiley & Sons, New York, pp. 11–64. Whitman, D.W. and Eller, F.J. (1992) Orientation of Microplitis croceipes (Hymenoptera: Braconidae) to green leaf volatiles: dose–response curves. Journal of Chemical Ecology 18, 1743–1753. Wright, D.J. and Verkerk, R.H.J. (1995) Integration of chemical and biological control systems for arthropods: evaluation in a multitrophic context. Pesticide Science 44, 207–218.

04IntpestManCh4.QXD 14/4/04 2:24 pm Page 72

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 73


Behaviour-modifying Chemicals: Prospects and Constraints in IPM

Larry J. Gut,1 Lukasz L. Stelinski,1 Donald R. Thomson2 and James R. Miller1


of Entomology, Michigan State University, East Lansing, Michigan, USA; 2DJS Consulting, Seattle, Washington, USA

Introduction Many organisms rely on chemical messages to communicate with each other or to find suitable hosts. Insects and other arthropods appear to be especially dependent on chemical stimuli for survival and reproduction. Essential insect behaviours that may be stimulated or inhibited by olfactory information include mating, feeding and oviposition. Chemical messages that trigger various behavioural responses are collectively referred to as semiochemicals. The term pheromone is used to describe compounds that operate intraspecifically (Karlson and Lüscher, 1959), while allelochemical is the general term for an interspecific effector (Whittaker and Feeney, 1971). Pheromones are categorized according to function, including sex pheromones, aggregation pheromones, alarm pheromones, trail pheromones and host-marking pheromones. Allelochemicals are classified based on the advantage of the message to the receiver or sender. Alomones benefit the sender, kairomones give advantage to the receiver and synomones benefit both parties. Examples of these kinds of semiochemicals include floral compounds that are attractive to pollinators and plant-produced feeding or oviposition deterrents or stimulants.

Since the early 1970s, considerable progress in understanding insect behaviour and complementary advances in analytical chemistry have led to the identification of thousands of pheromones and other semiochemicals (Mayer and McLaughlin, 1991; Hardie and Minks, 1999). Not surprisingly, a wide array of uses for semiochemicals has been tested over the past few decades and many practical applications have become integral components in pest-management programmes (Metcalf and Metcalf, 1992; Jones, 1998; Knight and Weissling, 1999; Suckling and Karg, 2000). Applied scientists have long recognized the potential of using behaviourally active compounds to trap insects (Lanier, 1990). Monitoring the activity of insects with pheromone- or kairomone-baited traps is now a standard practice in the majority of pest-management systems. The information gathered can be used to time insecticide applications or for determining the need to treat. Trapping is also widely used to detect the presence of pests in quarantine or survey programmes. The realization that behaviours critical to insect survival were strongly influenced by semiochemicals rapidly led to proposals for using these agents as practical tools for pest suppression (Wood et al., 1970; Shorey and McKelvey, 1977). For example, some early

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


05IntpestManCh5.QXD 14/4/04 2:24 pm Page 74


L.J. Gut et al.

pioneers proposed the tactic of broadcasting insect sex-attractant pheromones for direct control through communication disruption (Gaston et al., 1967; Mitchell et al., 1974; Shorey et al., 1974). In addition to recognizing the strengths offered by semiochemicalbased controls, the early innovators also appreciated the weaknesses of behavioural controls (Knipling, 1979; Ritter, 1979; Mitchell, 1981). These inherent strengths and weaknesses are well worth reviewing. As rendered by Miller and Cowles (1990), damage to a crop can be approximated by the expression: damage ∝ D A S T, where D is the density of pest in a crop, A is the acceptability of the crop to the pest, S is the suitability of the crop to the pest and T is the time of the interaction. Generally, as more of these parameters are reduced by a control tactic, the outcome for crop damage reduction improves. For example, a great strength of insecticides lies in the dramatic reduction in pest density, crop suitability and time of the interaction. The lack of a negative effect on acceptability is actually advantageous in this case because ingestion of the toxic substance is desired. Behavioural controls often do not kill the target pest. In this case, they do not directly reduce pest density or the time of pest–crop interactions, unless the mode of action is repellence. Thus, while insecticides can prove effective during their short lifespan on the crop, behavioural controls must remain effective for longer durations, usually throughout the lifetime of the pest. Additionally, behavioural controls can sometimes lose their effect over time due to changes in physiological and behavioural thresholds resulting from, for example, increased hunger or build-up of eggs (Miller and Cowles, 1990). The effectiveness of controls involving antibiosis is generally independent of pest density. In contrast, the efficacy of behavioural controls can be density-dependent. Under such conditions, behavioural-control measures become more suited for management of pest populations that are below the outbreak threshold rather than for suppression (sensu Knipling, 1979) after an outbreak has occurred. Despite some fundamental limitations, the development and implementation of pest-management strategies and control

tactics based on semiochemicals have progressed considerably since the earliest attempts at direct control. New regulations governing the use of pesticides, increasing environmental concerns and the regular occurrence of resistance to chemical controls have provided a strong impetus for the adoption of novel technologies, including behavioural controls. In addition, growing numbers of producers have recognized that the weaknesses of behavioural controls are to some extent counterbalanced by the advantage of negligible environmental impact and increased compatibility with biological and cultural methods of control. Although the majority of successful uses of semiochemicals are for monitoring pest activity, there is an increasing number of examples of direct control with pheromones and other behaviour-modifying compounds. The various approaches in which semiochemicals are used in pest management are listed in Table 5.1. Monitoring the activity of insects using pheromone- or kairomonebaited traps is an integral part of many pestmanagement programs. Trapping is often the most efficient method of detecting the presence of a species or measuring its seaTable 5.1. Practical uses of semiochemicals in pest management (adapted from Knight and Weissling, 1999). Monitoring 1. Detect the presence of a species 2. Measure seasonal activity and provide decision support 3. Evaluate the effectiveness of mating disruption 4. Assess levels of insecticide resistance Direct control 1. Mass deployment of attractant-baited traps 2. Application of attract-and-kill formulations or devices 3. Pheromone-mediated mating disruption 4. Manipulation of natural enemies using allelochemicals 5. Pheromone-based interference with host location or acceptance 6. Plant allomone-based deterrence of feeding or oviposition 7. Application of pheromones to enhance pollination

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 75

Behaviour–modifying Chemicals

sonal activity. This kind of information is helpful in making economically sound management decisions. Attractant-baited lures also form the basis for two direct control measures: mass trapping and attract-andkill. Both strategies require a high level of attraction to the lure. Another set of direct controls using pheromones or kairomones is based on interfering with an insect’s natural behavioural response to these compounds. The most developed tactic is termed mating disruption. This approach entails releasing large amounts of synthetic sex pheromone into the atmosphere of a crop in an effort to interfere with mate-finding, thereby controlling the pest by curtailing the reproductive phase of its life cycle. Our chapter is not intended to be a comprehensive review of the possible uses of behaviour-modifying chemicals in pest management, nor will it attempt to identify all of the constraints to successful deployment of the various approaches. Several treatises covering these subjects have been published over the past 25 years (Shorey and McKelvey, 1977; Mitchell, 1981; Nordlund et al., 1981; Kydonieus and Beroza, 1982; Jutsum and Gordon, 1989; Ridgway et al., 1990; Cardé and Minks, 1995, 1997; Jones, 1998). In keeping with the intent of this book, we present an overview of the potential role of semiochemicals in pest management and provide some examples of successes. The core of the chapter, however, is a discussion of the constraints and future prospects for mating disruption. We have emphasized this approach over others largely for practical reasons. A review of the literature quickly reveals that mating disruption is the most highly developed and widely adopted semiochemical-based control tactic. In addition, over the past 5–10 years our personal efforts have focused on the practical and commercial use of various mating disruption technologies in plant protection.

Monitoring Applications of trapping systems The production of synthetic copies of numerous kinds of semiochemicals has led to the


development and widespread commercial use of attractant-baited traps for monitoring and trapping insect pests in many agricultural production systems, government detection and quarantine programmes, and consumer-protection efforts. Unlike other sampling methods that may be very time consuming and require technical expertise, semiochemical-based monitoring is efficient and easy to use. In addition, the approach is effective over a range of pest densities and often provides the most practical means of monitoring adult activity. Detect the presence of a species Semiochemical-baited traps provide a relatively simple and reliable means of detecting pest infestations. They are one of the primary tools employed in quarantine surveys to determine the presence of a species and prevent its establishment and spread (Johnson and Schall, 1989; Schwalbe and Mastro, 1990). Traps are routinely deployed around airports and harbours to detect potential introductions of exotic pests at these high-risk sites. In a similar manner, large numbers of traps are used in regional survey programmes to determine the distribution of specific pests and to provide the information needed for preventing spread to new areas (Schwalbe and Mastro, 1990). The use of attractant-baited traps to demonstrate pest-free production zones is of increasing importance. The process often requires implementing a defined monitoring programme to allow for the export of an agricultural commodity to a specific country (Riherd et al., 1994). The monitoring protocols can be quite demanding, often specifying the kind of trapping system, the density of traps and a specific treatment regimen if a single individual is detected. Measure seasonal activity and provide decision support Monitoring with attractant-baited traps is an important component of pest-management programmes. The combination of pheromone traps and degree-day models can provide a reliable method for monitoring adult activity,

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 76


L.J. Gut et al.

predicting egg hatch and timing insecticide sprays (Welch et al., 1981; Riedl et al., 1986; Knight and Croft, 1991). The precision of this method of timing sprays has been well documented for codling moth, a key pest of pome fruits throughout the world (Beers et al., 1993). The phenology model for this pest is based on accumulating degree-days (base 10°C) beginning on the day the first moth is captured in a pheromone trap, provided moths are captured on two successive trapping dates. This start of sustained moth capture is referred to as biofix. The first spray is applied at 121 degree-days (°C) post-biofix, which coincides with the start of egg hatch. In 6 of 10 years in the state of Washington, USA, this model predicted the start of egg hatch on the same day that it was first observed in the field (Table 5.2) and there was never a discrepancy of more than 2 days between the predicted and observed event. Prior to the development of the degree-day approach, the first spray for codling moth in Washington State was timed on a calendar basis. The emergence of moths from overwintering sites was anticipated at full bloom on ‘Delicious’ apples and the first treatment was applied 21 days after this event. Based on this approach, treatments were often applied before egg hatch. In 7 of 10 years the predicted start of egg hatch occurred at least 3 days prior to observed hatch in the field and, moreover, predictions were over 13 days early on three occasions (Table 5.2). The use of a degree-day model rather than a calendar approach to time insecticide applications will become increasingly crucial in the coming years because many new insecticide chemistries, such as insect growth regulators, require precise timing as they are primarily active against specific instars or life stages. Semiochemical-based monitoring systems can also be used to assess population trends and determine the need to treat. Quantitative relationships between adult captures and counts of larval stages or signs of larval feeding, such as faeces or damage, have been found for pests of tree fruits (McBrien et al., 1994; Bradley et al., 1998), annual crops (Van Steenwyk et al., 1983) and forests (Sanders, 1988; Evenden et al., 1995; Morewood et al.,

Table 5.2. Comparison of a degree-day model with a calendar approach for timing the first insecticide spray for control of hatching codlingmoth larvae (based on Beers et al., 1993). Accuracy in timing sprays (days)a Year



1979 1980 1981 1982 1983 1984 1985 1986 1987 1993

0 0 2 0 1 0 1 0 2 0

3 4 13 2 8 18 1 13 2 6

a Positive numbers indicate predicted timing was too early, negative numbers indicate predicted timing was too late.

2000). In some cases, captures in one year can be used to predict events in a subsequent year. McBrien et al. (1994) demonstrated a correlation between catches of male mullein bug, Campylomma verbasci (Herrich-Schaffer), in the autumn and the density of nymphs the following spring in apple orchards. There has been developed for the eastern spruce budworm, Choristoneura fumiferana (Clemens), an early-warning system that uses male captures in pheromone traps to predict a severe outbreak of this pest several years in advance (Sanders, 1988). Basing management decisions on adult catches rather than taking a preventive or calendarbased approach is a key step in many efforts to reduce insecticide inputs. The approach typically entails intervening with a spray only if catches exceed a predetermined level. The decision can be based on a single weekly catch, consecutive catches or cumulative catches over an extended period time, such as a generation. Sticky-coated red spheres baited with synthetic apple volatiles can be used to monitor apple maggot activity and to alert growers as to the need for a spray (Stanley et al., 1987; Agnello et al., 1990). An action threshold of eight flies per trap allowed for a 70% reduction in sprays and acceptable levels of control. Reducing the

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 77

Behaviour–modifying Chemicals

threshold to five flies per trap resulted in 0.6 fewer sprays, but the conservative threshold was more likely to be adopted by apple growers. Treatment thresholds for codling moth based on moth captures in pheromone traps have been developed for most pome fruit producing regions of the world (Riedl et al., 1986; Wall, 1989). Evaluate the effectiveness of mating disruption An increasingly important use of attractantbaited traps is to measure the efficacy of mating-disruption formulations. Capture of zero (complete shutdown) or very few moths in a pheromone-baited trap has been used to indicate successful disruption of the target pest. The rationale behind this measure of mating-disruption effectiveness is that, if male moths were incapable of finding a lure releasing synthetic pheromone, they were also unable to find a female moth releasing natural pheromone. Unfortunately, it is not uncommon to record low moth catches in traps and still have less than adequate pest control in pheromone-treated plots (refer to several chapters in Ridgway et al., 1990). In some cases, it is possible to greatly inhibit catches in pheromone traps but still detect substantial numbers of mated females (Rice and Kirsch, 1990; Atanassov et al., 2002) or actual mating (Suckling and Shaw, 1992). In the former situation where mated females are found in treated plots, it is possible that a portion of these females immigrated from adjacent plots not treated with pheromone. There have been two approaches to improving the usefulness of pheromonebaited traps as monitoring tools in pheromone-treated plots. Cardé and Elkinton (1984) suggested that a lure with an emission rate closer to the natural rate would seem to be the most suitable for measuring the efficacy of a disruption treatment. Charmillot (1990) took a different approach, opting to use lures with very high release rates as a means of following changes in adult population densities in spite of air permeation with pheromone. In a series of experiments over the course of 2 years, he showed that, for codling moth, the sensitivity of pheromone traps in pheromone-treated orchards could


be improved by increasing the amount of codlemone in the lure. Moth catch in disrupted orchards increased considerably when traps were baited with 10 or 20 mg of pheromone. Others have subsequently confirmed a significantly greater sensitivity of 10 mg- compared with 1 mg-baited traps in disrupted orchards (Barrett, 1995; Judd et al., 1996). A further increase in moth captures in orchards treated with mating-disruption dispensers can be achieved by placing traps in the upper canopy (Barrett, 1995). Although the high-load pheromone trap is a useful tool for monitoring codling-moth activity in disrupted orchards, when used alone it is not a reliable method for assessing the effectiveness of the pheromone treatment. Trapping should be used in conjunction with visual inspection of fruit for codling-moth damage. The biggest concern with using pheromone traps to measure the effectiveness of mating disruption, regardless of the lure load, is the regular occurrence of ‘false negatives’ (Knight, 1995). This refers to a situation where low or no catches are recorded and yet fruit injury occurs in the block. Assess levels of insecticide resistance A dramatic rise in resistance to insecticides over the past decade (Norris et al., 2003) has brought about an acute need to have simple and reliable methods for monitoring its severity and distribution. Pheromone-trap bioassays are one of the more widely adopted methods for assessing the susceptibility of lepidopteran pests to insecticides. The basic approach was developed by Riedl et al. (1985) to test codling-moth susceptibility to azinphosmethyl. It has since been modified and used to evaluate the tolerance of other pests to various insecticides (Suckling et al., 1985; Haynes et al., 1987; Knight and Hull, 1989; Varela et al., 1997; Shearer and Usmani, 2001). The bioassay entails collecting large numbers of males in traps and testing for expression of resistance by topical application of insecticides or through incorporation of insecticide into the glue. The major advantage of pheromonetrap bioassays over most other methods of assessing resistance is that many individuals

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 78


L.J. Gut et al.

can be tested without incurring the costs in time and money associated with rearing large numbers of larvae. The simplicity of the trap bioassay does not come without trade-offs. Dose–mortality responses may be strongly affected by a number of factors, including whether the toxicant was delivered topically or through the adhesive (Knight and Hull, 1989; Shearer and Riedl, 1994). The technique may overestimate the impact of resistance in the field because only males are captured and assayed. Sex-related differences in the tolerance to organophosphorous and carbamate insecticides have been discovered for populations of Oriental fruit moth in the USA, with females more susceptible than males (deLame et al., 2001; Shearer and Usmani, 2001). A major limitation of the approach is that it cannot be used to monitor for resistance to materials whose primary mode of action requires ingestion. Unfortunately, this includes most of the newer insecticide chemistries, such as insect growth regulators and neonicotinoids.

Performance of trapping systems The development and commercialization of pheromone- or kairomone-based monitoring systems has greatly enhanced society’s ability to monitor and manage insect pests. As a means of estimating population density or predicting crop damage, however, the strategy has proved to be of more limited utility. Morse and Kulman (1985) found no significant relationship between catches of the yellowheaded spruce sawfly, Pikonema alaskensis, and the degree of defoliation inflicted by this pest. A lack of correlation between moth catches and egg numbers has been reported for several vegetable pests; examples are Helicoverpa zea (Boddie) on tomato (Campbell et al., 1992) and field maize (Latheef et al., 1991). A trap will sample only a portion of the pest population in an area. For a trap to accurately reflect the true population density and thus the potential for crop loss, the trap’s attractiveness should remain constant, as should the proportion of the individuals from the population that are captured. The inadequacy of attractant-baited monitoring sys-

tems as quantitative decision tools is due in part to the substantial effect that trap design, attractiveness of delivery device, trap maintenance programme, and placement in the crop have on the performance of the system. Various trap designs and means of dispensing attractants have been developed for monitoring insects (Cardé and Elkinton, 1984; Wall, 1989; Jones, 1998). The majority of trap types employ a sticky surface to capture attracted insects. Other trap designs rely on a flight barrier, often combined with a knockdown insecticide or a liquid trapping medium to retain attracted insects. Attractants are commonly formulated in reservoirs made of various materials, including rubber, polyethylene, polyvinyl chloride and hollow fibres. The probability of insects finding a trap is highly dependent on the attractiveness of the lure and the placement of the trap. Traps may be placed within or outside the crop, on the edge or interior of the plot, high or low in the canopy or on different sides of a tree. The location of the trap with respect to these parameters can have a substantial impact on moth catch. For example, differences in captures due to vertical positioning of traps within the crop canopy have been documented in both annual and perennial crops. Riedl et al. (1979) demonstrated that catches of male codling moth varied substantially depending on trap placement in the tree canopy (Fig. 5.1). Higher catches were recorded in the upper compared with lower canopy positions. Very few moths were captured above or below the canopy. Simandl and Anderbrant (1995) documented a similar outcome for the sawfly, Neodiprion sertifer (Geoffroy). Pheromone traps installed in the crowns of conifers (> 9 m) caught up to 15 times as many males as did traps suspended at 2.5 m. Derrick et al. (1992) found that traps placed within maize fields at ear level (1.5 m) captured greater numbers of European corn borer, Ostrinia nubilalis (Hübner), than traps hung in the field at canopy height (3.0 m). Trap design and maintenance will influence the likelihood of capturing an insect after it finds the trap. The effectiveness of many trap designs depends on maintaining the integrity of trap shape and the quality of the adhesive surface throughout the season.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 79

Behaviour–modifying Chemicals


Proportion caught (%)

4 m canopy height 40 30 20 10 0


1.4 2.3 3.2 4.1 Trap elevation (m)

Fig. 5.1. The influence of canopy position on codling-moth captures in pheromone traps (from Riedl et al., 1979).

Traps that depend on a sticky surface to capture insects can lose their ability to retain new arrivals if the surface becomes covered with debris or target and non-target insects. The efficiency of trapping for codling moth declined as catches exceeded 20–30 moths in traps with a 185 cm2 sticky surface, while catches of 50–60 moths unacceptably reduced the performance of traps with a 360 cm2 sticky surface (Riedl et al., 1986). Under conditions of moderate or high pest pressure, traps can quickly become saturated with moths and diminish the likelihood of accurately measuring pest density by moth captures.

Future prospects Drawing range of lures A crucial problem with using pheromonebaited traps to measure pest density and predict damage is that insects may be attracted from distances well beyond the boundaries of the crop. Using the mark-and-recapture technique, Thayer (2002) demonstrated that male oblique-banded leaf-rollers could be captured in pheromone traps at distances of up to 440 m from the release point. The active space of a trap baited with 1 mg of pheromone was calculated to be 152,000 m2 or nearly 15 ha. Baker and Roelofs (1981) recognized the problems associated with a large active space and proposed modifying the dose of the attractant to optimize the draw-

ing range. Using this approach, they were able to restrict the sampling of Cydia molesta (Busck) to the immediate vicinity of the trap by lowering the dose. Faccioli et al. (1993) found that reducing the pheromone dosage in traps for the polyphagous pest Argyrotaenia ljungiana (Thunberg) enhanced the correlation of moth catch to larval infestation. The major reason for the improved precision was a decrease in the number of ‘false positives’ or cases of high catch with little or no concurring infestation. There are other possibilities for mitigating the effects of sampling large numbers of individuals from outside the crop on the usefulness of trapping information. The simplest approach for highly polyphagous pests would be to avoid placing traps close to the perimeter of a plot as a large portion of the area monitored by the trap would be outside its boundaries. However, placing traps in the interior still may not sufficiently limit the active space. A significant number of insects may move considerable distances prior to attraction, effectively increasing the area of influence of a trap (Wall and Perry, 1987). Knight and Hull (1988) found that a better correlation between pheromone-induced catches of tufted apple-bud moth, Platynota idaeusalis (Walker), and damage could be obtained if predictions were based on captures early in the flight, presumably before substantial movement by the moths, rather than over the entire flight period. Another promising approach is to bait traps with a lure that attracts both males and females.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 80


L.J. Gut et al.

Monitoring males and females The use of a food bait or specific kairomone that attracts both sexes offers some distinct advantages over a sex-pheromone lure that attracts males only. Capture of females is more directly linked to oviposition and the potential for larval damage. Because females in many species do not disperse great distances, catch of females may more accurately reflect pest densities in the block that is being monitored. The attraction to host volatiles should not be greatly impeded or suppressed by pheromone-based mating disruption, offering the possibility of a means of monitoring pest density in disrupted plots. Traps baited with a brown sugar and terpinyl acetate solution have been used to monitor Oriental fruit moth activity in pheromone-treated pome and stone-fruit orchards (Sexton and Il’ichev, 2000; Il’ichev and Sexton, 2002; Il’ichev et al., 2002). These food traps are not specific to Oriental fruit moth, but they do capture females and males of this species and provide a more reliable measure of pest pressure than pheromone-baited traps. More recently, ethyl-(2E,4Z)-2,4-decadienoate (DA), a volatile present in the odour of ripe Bartlett pears, has been identified as a compound that is attractive to both sexes of codling moth (Light et al., 2001). This pear ester is a stable compound that can be readily synthesized and loaded into a rubber septum to make a lure for monitoring both sexes of codling moth. Comparisons of DA and pheromone lures to monitor the activity of codling moth have been carried out for the past few years, most extensively in the western USA. Trials by a team of scientists (Light et al., 2001) indicated that DA lure-baited traps provided good resolution of moth flight patterns for both sexes in conventional and especially mating-disrupted orchards. A number of factors may influence the performance of traps baited with the DA lure and should be considered when using this trapping system. The crop or cultivar in which traps are placed influences moth catch in traps baited with the pear ester. Higher catches with this kairomone lure were recorded in walnut and in some late-season apples than in pear or in early-season apples

(Light et al., 2001; Alan Knight, Washington, USA, 2002, personal communication). Additional research on cultivar effects and the range of attraction is crucial to the development of a reliable pear ester-based monitoring system for codling moth. Commercial implementation of monitoring programmes Perhaps the greatest factor limiting the usefulness of attractant-baited traps is the incongruence between the monitoring programme that is developed and tested through experimentation and the system that is actually implemented in the field. Researchers focus on developing a tool and set of monitoring guidelines that are scientifically sound but often impractical. For example, treatment thresholds for codling moth in apple or pear were largely developed based on a trapping density of one trap per hectare because this was determined to be the active space of a trap. For an integrated pest management (IPM) practitioner, the economically ‘practical space’ is closer to one trap per 4 ha. A consultant is typically paid a set fee based on the size of the block monitored and must carefully consider the time involved in inspecting and maintaining traps in deciding how many to deploy. From the researcher’s perspective, a consultant or other IPM practitioner often ignores critical aspects of trap placement or maintenance. In fruit orchards in the USA, codling-moth traps are routinely placed at ‘truck-window’ height, as well as on the very edge of a block. This certainly facilitates inspecting the trap but is counterproductive because very few moths will be caught. The typical justification for placing traps in less than optimum positions is that the best monitoring system is the one that provides the most reliable estimate of the population, not necessarily the catch of the greatest number of insects. However, it is essential to have at least adequate numbers upon which to base a decision. Moreover, there is likely to be no relationship between information garnered from a poorly run trapping programme and thresholds or other information that has been generated through more carefully conducted experiments.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 81

Behaviour–modifying Chemicals

The bottom line is that the best monitoring programme will develop through an awareness and consideration of the concerns and limitations expressed by the researcher and the practitioner, especially the cost of the programme. For example, effective monitoring of codling moth can be achieved by placing traps at mid-canopy height, and at a density of one trap every 4–6 ha on farms with large uniform plantings without a history of localized infestations. A tighter spacing of traps is required on farms with small plantings or a suspected uneven distribution of codlingmoth pressure or in mating-disrupted blocks. Finally, in pheromone-treated orchards, consultants are urged to place traps high in the canopy.

Attraction–annihilation Attraction–annihilation is probably the earliest use of attractants for pest control. Many early efforts were discouraging or, when effective control was demonstrated, practical deficiencies often inhibited the commercial adoption of the control system. The principles of attraction–annihilation and the potential of mass


trapping, attract-and-kill and other practical applications of this pest-management approach have been reviewed comprehensively (Bakke and Lie, 1989; Lanier, 1990; Jones, 1998). Here we summarize the constraints, provide examples of some successes and offer some challenges for the future.

Mass trapping The aim of mass trapping is to prevent crop damage by capturing a substantial proportion of a pest population prior to mating, oviposition or feeding. Success with this method requires the combination of a very attractive lure and a highly efficient trap. Although examples of mass trapping for pest control are fairly plentiful (see Table 5.3 for examples), most efforts have not been successful from the standpoint of commercial adoption. Constraints The commercial viability of mass trapping is limited by a number of practical and biological requirements. Of foremost importance

Table 5.3. Some promising applications of attraction–annihilation for insect pest management. Approach



Mass trapping Attractants and water-based funnel traps Attractant-baited traps Sex pheromone-baited traps Attractant-baited multisurface traps Pheromone-based mass trapping Inhibitor combined with mass trapping Sex pheromone-based mass trapping

Carpophilus beetles Japanese beetle Chinese tortrix Cigarette beetle Ambrosia beetles Mountain pine beetle Beet armyworm

James et al., 1996 Wawrzynski and Ascerno, 1998 Zhang et al., 2002 Buchelos and Levinson, 1993 Borden, 1990 Lindgren and Borden, 1993 Park and Goh, 1992

Attract-and-kill Pesticide-treated spheres

Apple maggot fly

Pesticide-treated spheres

Blueberry maggot fly

Pheromone bait spray Sex-pheromone-based attracticide Sex-pheromone-based attracticide

Olive fly Codling moth Light-brown apple moth

Prokopy et al., 2000; Stelinski et al., 2001 Ayyappathe et al., 2000; Stelinski and Liburd, 2001 Jones, 1998 Charmillot et al., 2000 Suckling and Brockerhoff, 1999

Diamondback moth Japanese beetle Tobacco budworm

Furlong et al., 1995 Klein and Lacey, 1999 Jackson et al., 1992

Autodissemination Pheromone trap and fungus Attractant trap and fungus Pheromone trap and baculovirus

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 82


L.J. Gut et al.

are the costs of substantial numbers of traps and the expenses for the material and labour needed to maintain them. The technique is more useful for the control of low-density than high-density populations. Traps can quickly become saturated with insects at high densities. If the attractant is a sex pheromone, mass trapping will require many traps to be effective against high-density populations because of competition with calling females (Knipling, 1979). The kind and potency of the attractant influence the outcome of a mass trapping programme. The chances for success are improved if both males and females are attracted to the trap. If only males are trapped, it is essential that they be captured before mating. In most insect species, males can mate more than once; thus a very high proportion of individuals needs to be removed from the population to obtain the high reduction in female fecundity required for control (Roelofs et al., 1970). Therefore, optimizing the lure is critical to the success of mass trapping. Synthetic lures must compete well with natural attractive sources. The lure must be potent enough to draw in insects from a considerable distance without impeding progress once they are close to the source. Trap density is based on both economic considerations and the attractiveness of the lure. The spacing of traps should be such that competition between traps occurs, but just to a level that does not reduce the total kill (Lanier, 1990). Finally, as pointed out in the monitoring section, the ability to attract and retain very high numbers of individuals will be affected by trap design, placement and maintenance. Prospects The success of a mass-trapping programme is directly related to the desired outcome. A very high percentage of the individuals in the population must be removed if the tolerance for damage is very low. Pests that cause direct damage to a crop and have tolerances near zero are probably not the best choices for this control tactic. Better opportunities for mass trapping are in situations where there is some flexibility in the desired outcome, such as where the public is willing to tolerate

some pest damage in exchange for a perceived reduced exposure to insecticides. In parks and city plantings, 80–90% rather than 100% control may be acceptable. Male removal using sex-pheromone traps was demonstrated to be an effective means of controlling Chinese tortrix, Cydia trasias, on street-planted Chinese scholar trees (Zhang et al., 2002). Four years of mass trapping with a sex and floral lure reduced a small pocket of Japanese beetles in a city park by 97% (Wawrzynski and Ascerno, 1998). The prospects for mass trapping are enhanced if population densities are low or if the technique is carried out in an area where immigration by the pest from outside the treated area is limited. The success of the above-mentioned efforts in urban or park settings was, in part, due to the isolation of the sites and the relatively low pest densities. Attempts to control Japanese beetle in other settings or where population densities were high have proved ineffective (Klein, 1981; Gordon and Potter, 1985, 1986). Food warehouses and other enclosed situations provide a high level of isolation, which should enhance the prospects for mass trapping (Suckling and Karg, 2000). Control of Mediterranean flour moths, Ephestia kuehniella Zeller, in flour mills was achieved through the mass deployment of pheromone-baited funnel traps combined with careful cleaning of the rooms and machinery (Trematerra and Battaini, 1987). Perhaps the most successful use of this tactic has been for the control of some species of forest beetles. Semiochemicals play a major role in the process of host colonization by bark beetles. Intensive trapping of bark beetles for pest control is facilitated by their high dependence on aggregation pheromones that are attractive to both sexes as they mass attack a host. Mass trapping combined with other control measures, such as sanitation cutting, were used to control populations of the conifer bark beetle, Ips typographus (Linnaeus), in Norway and Sweden (Bakke and Lie, 1989). One of the most effective uses of mass trapping has been for control of ambrosia beetles in timber-processing facilities in British Columbia (Borden, 1990). In this case, the programme probably benefited

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 83

Behaviour–modifying Chemicals

from the trapping area being somewhat isolated from beetle populations in the forest (Schlyter and Birgersson, 1999). Control of some forest beetles may be enhanced by use of deterrents to ‘push’ the target beetles away from a host, combined with attractant-baited traps or trap trees to ‘pull’ them away (Borden, 1997). Aggregation and anti-aggregation pheromones were successfully used in this push–pull manner against the mountain pine beetle, Dendroctonus ponderosae Hopkins (Lindgren and Borden, 1993).

Attract-and-kill As a control tactic, attract-and-kill is similar to mass trapping in that an attractant-based system is used to eliminate a substantial proportion of a pest population and thereby prevent unacceptable levels of crop damage. The major difference is that the attract-andkill approach relies on a toxicant, rather than a trap, to remove individuals that respond to the synthetic attractant. In many ways this technique suffers from the same constraints as outlined for mass trapping, including population density, attractiveness of the lure and efficiency of the method of killing. A major advantage of the attract-and-kill approach is that the problem of trap saturation can be eliminated. This may improve the effectiveness of control in high-density situations. The issues of trap maintenance and the high cost of the control programme can also be mitigated to some extent, especially if the system relies on attracting the insect to a plant surface that has been treated with an insecticide rather than to some kind of target device (Jones, 1998). Attract-and-kill formulations have been developed for control of various beetles, moths and especially flies (see examples in Table 5.3). Some of the earliest and most widely tested applications of attractants in combination with insecticides have been for control of tephritid fruit flies (Jones, 1998). They have largely evolved from attempts to mass trap these insects, which often failed because of the problem of trap saturation. Jones (1998) has summarized efforts to control the olive fly, Bactrocera oleae Gmelin, in


Greece through various attract-and-kill strategies. His review illustrates well the process of developing this approach for fruitfly control. Protein/insecticide-bait sprays have been used for control of this pest in most Mediterranean olive-growing areas for a number of years. A major concern with this tactic is that the bait is highly attractive and toxic to natural enemies. To overcome the detrimental effects on natural enemies, a system was developed based on the use of target traps baited with either a food-attractant or a sex-pheromone dispenser. This target-device method of controlling B. oleae was effective at reducing fruit infestation, especially when applied on an area-wide basis. In addition, the effectiveness of the device allowed for a reduction in the use of bait sprays and an accompanying increase in natural-enemy populations. The most recent development for fruit-fly control has been a microencapsulated sprayable formulation comprised of the sex pheromone of this species, 1,7-dioxaspiro, and an insecticide (either malathion or dimethoate). Interestingly, the pheromonebait spray has provided significant reductions in fruit infestation, while attempts to use the pheromone as a mating disruptant only have failed because the approach produces substantial immigrations of male and female olive flies into the treated area. Concerted efforts to develop lure-baited trapping systems for control of Rhagoletis fruit flies are ongoing in the eastern and Mid-western USA. Some early success was achieved using sticky-coated red spheres for direct control of Rhagoletis pomonella (Walsh) (Duan and Prokopy, 1995). A major impediment to commercial adoption of this control system was the high level of maintenance required to ensure trap effectiveness. Recent efforts, therefore, have focused on developing a system that relies on a small dose of toxicant, rather than a sticky material, to kill alighting flies. Biodegradable or wooden spheres laced with a low dose of imidacloprid show promise for control of R. pomonella in apple and Rhagoletis mendax Curran in blueberry (Hu et al., 1998; Liburd et al., 1999; Ayyappathe et al., 2000; Prokopy et al., 2000; Stelinski and Liburd, 2001; Stelinski et al. 2001). Pesticide-treated spheres rely on a

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 84


L.J. Gut et al.

combination of attractants, a feeding stimulant and a toxicant to lure and kill the target pest. Sphere shape and colour and fruitvolatile or food-based lures are the major attractants. The insecticide is incorporated into the latex paint used to colour the spheres, which aids in maintaining the residual activity of the toxicant. Sucrose is used as a feeding stimulant, which coerces flies to ingest lethal doses of toxicant. Placement of biodegradable spheres baited with an attractive component of host odour, butyl hexanoate, on perimeter trees of commercial apple blocks were nearly as effective as insecticide sprays at intercepting apple maggot flies and preventing fruit injury (Prokopy et al., 2000).

Autodissemination Autodissemination is an innovative and promising control technique that combines an attractive lure with an entomopathogen. Suckling and Karg (2000) recently proposed the term ‘lure and infect’ to describe this approach and provided a good summary of its limitations and unique advantages. Individuals that arrive at the source are not killed, but rather are inoculated with the pathogen and hopefully magnify the treatment by spreading the disease to other individuals. The host specificity of the pathogens means that the method will be highly compatible with biological control. The approach has been attempted using a variety of disease organisms (Table 5.3). Shapas et al. (1977) substantially suppressed populations of a stored-product pest, Trogoderma glabrum (Herbst), using a combination of its pheromone and spores of a pathogenic protozoan, Mattesia trogodermae. Autodissemination of a baculovirus for management of tobacco bud-worm has been tested by Jackson et al. (1992). The effectiveness of a pheromone trap designed to deliver conidia of a fungal pathogen has been explored for control of the diamondback moth, Plutella xylostella (Linnaeus) (Furlong et al., 1995). A fungus is also being developed for use against Japanese beetle. A Trece Catch Can Japanese-beetle trap modified to serve as an inoculation chamber

has been tested for control of this pest, using the fungal pathogen Metarhizium anisopliae (Klein and Lacey, 1999). High levels of mortality were recorded for beetles emerging from the trapping device. In addition, it was demonstrated that contaminated beetles could pass the fungus to untreated beetles in quantities sufficient to kill a high proportion of the population. A number of deficiencies will have to be overcome to make the autodissemination approach a commercially viable option. Some innovation will be required to design effective transfer stations. For example, Vega et al. (1995) invented an autoinoculating device that induces sap beetles to pick up whatever microorganism is loaded into it. The pathogens that are placed in delivery stations should also be readily transferred between individuals. Suckling and Karg (2000) pointed out that fungi might be the best candidates as they are transferred between adults and larvae, and do not require consumption or copulation to become pathogenic. Once an appropriate pathogen is selected, a formulation must be developed that protects the organism from environmental degradation. A major constraint with these systems, as with masstrapping strategies, is likely to be the ability to make them cost-effective as many bait stations may need to be deployed for the approach to be effective. Finally, a general public concern over the production of pathogens and their release into the environment may limit the development and acceptance of this technique.

Mating Disruption The most successful approach using semiochemicals for pest control over the last few decades has been the release of large amounts of synthetic pheromone into a crop in an effort to prevent or delay mating. The potential to control insects through mating disruption was first demonstrated for Trichoplusia ni (Hübner) over 30 years ago (Gaston et al., 1967). Similar efforts with other moth species confirmed that dispensing large quantities of pheromone into a crop could

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 85

Behaviour–modifying Chemicals

disrupt mate location, thereby controlling the pest by interfering with the fertilization of eggs (Mitchell et al., 1974; Shorey et al., 1974; Taschenberg et al., 1974; Rothschild, 1975). There has been considerable progress in the application of formulated pheromone for direct pest control since the first promising trials. Through the combined efforts of researchers, private entrepreneurs, extension personnel and others, mating disruption has become an accepted control option for a number of lepidopteran pests of fruits, vegetables and forests (Ridgway et al., 1990; Cardé and Minks, 1995, 1997). A listing of commercial formulations currently registered for use in North America and the estimated total area treated in 2002 (Table 5.4) provides strong testimony to the success of this approach. A number of developments had to occur in order to make mating disruption an effective and economically viable control tactic. Continual advances in understanding the many biological characteristics, behavioural and otherwise, that influence the outcome of a mating-disruption programme were certainly instrumental in paving the way. Some advances were more technical in nature,


such as the development of new techniques for identification and synthesis of pheromones and devices for releasing the pheromone over an extended period of time. Often overlooked was the strong involvement of government agencies, both in research and in technology transfer. Companies developing mating-disruption products typically had very small research budgets, with support provided primarily as donations of product to government researchers to conduct efficacy trials. Government agencies have played a particularly important educational role in area-wide projects and deserve a great deal of the credit for providing technical expertise and demonstrating the benefits of mating disruption (Staten et al., 1997; Calkins et al., 2000; Il’ichev et al., 2002). Finally, changes in regulatory requirements were made that accelerated the registration process (Thomson et al., 1998). Although substantial inroads into commercial markets have been made since the early 1980s, disruptants and other semiochemical products continue to hold a rather small share of the total pest-control market. Jones and Casagrande (2000) placed the

Table 5.4. Commercial disruption formulations registered for use in North America and estimated area treated in 2002. Number of formulations Crop


Almond Apple

Peach-twig borer Codling moth Leaf-roller Oriental fruit moth Pink bollworm Black-headed fireworm Sparganothis fruitworm Grape berry moth Omnivorous leaf-roller Oriental fruit moth Peach-twig borer Codling moth Tomato pinworm Codling moth

Cotton Cranberry Grape Peach Pear Tomato Walnut

Reservoirtype 2 6 2 2 2 1 2 1 4 2 6 2 1


Hectares treated

Per cent of total hectares planted

1 4 1 2 2 2 1 1 1 3 1 4 2 3

200 45,000 1,600 400 8,900 200 100 300 500 17,800 600 8,000 10,000 1,200

< 0.1 18.0 0.6 0.1 0.2 1.5 0.7 0.1 0.1 26.2 0.9 28.6 5.6 1.5

Current market value ($US) 30,000 13,750,000 200,000 40,000 562,000 25,000 12,500 18,750 31,250 1,780,000 90,000 2,200,000 72,000 330,000

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 86


L.J. Gut et al.

worldwide sales of semiochemical products at about US$70–80 million or about 1% of the agrochemical market. More recently, the world pheromone market for mating-disruption products was estimated to be $80 million (K. Ogawa, Japan, 2002, personal communication). A limited understanding of what is required to achieve success, technical deficiencies and tightening profit margins in agriculture are the principal factors that have slowed the rate of adoption of mating disruption. Even some of the failures have been useful for identifying patterns that will improve our ability to select pest species, production systems and specific sites that will maximize the chance for the success of mating disruption from the outset. The discussion that follows is an attempt to identify and synthesize the patterns that have emerged since the first disruption field trials were conducted some 40 years ago. To a large extent, the potential for the success of mating disruption is determined by the following set of biological parameters: ● Biology/ecology of the target species. ● Male sensitivity to the pheromone (physiological). ● Chemical characteristics of the pheromone. ● Influence of the physical environment. It is how this suite of features plays out for a specific pest, commodity or site that determines the suitability of mating disruption for that particular situation. Once the decision is made to implement a mating-disruption programme, its commercial success depends on a set of operational parameters that provide for effective delivery of the active ingredient. Practical considerations, such as cost, ease of application and the reliability of a scouting programme will determine the extent to which users will embrace this technique.

Pest biology and ecology A number of biological and ecological attributes are likely to influence the suitability of a pest species as a candidate for control by mating disruption (Rothschild, 1981; Cardé and Minks, 1995; Sanders, 1997). The success

of mating disruption is dependent upon population density, the ecological setting of the treated area, and specific traits of the target species. Key biological traits include host specificity, dispersal capacity, number of generations and adult lifespan, fecundity, characteristics of pheromone emission by the female and other aspects of mating behaviour. Experience teaches us that the effectiveness of mating disruption is compromised in situations where mated females invade from outside the treated area. Treatment with pheromone alone provides no protection against immigrating females, which can readily deposit fertile eggs. Immigration of gravid females is believed to be a key process that contributes to the development of border infestations (Tatsuki, 1990; Il’ichev et al., 2002). It follows that a high dispersal capacity and a wide host range are lifehistory traits that tend to reduce the suitability of a species for mating disruption. Furthermore, the impact of these traits should be most pronounced where the area treated with disruptant is adjacent to untreated areas that harbour hosts for the target pest. As with other semiochemical-based control tactics, there is often a strong interaction between population density and the effectiveness of mating disruption. In many instances, high-density populations are more difficult to control with this technique than less dense populations. For example, the best disruption of codling moth has been achieved where pest pressure is low, while attempts to control high-pressure populations have been problematic at best (Trimble, 1995; Gut and Brunner, 1998; Vickers et al., 1998). In an effort to mitigate the effects of population density, growers typically apply one or more companion insecticide sprays to reduce pest pressure. It is worth noting that, for some pest species, mating disruption is equally effective over a range of population densities. Field trials to determine the effectiveness of disruption for control of peach-tree borer, Synanthedon exitosa (Say), were conducted in peach orchards in Georgia, USA, using Hercon vinyl laminated dispensers loaded

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 87

Behaviour–modifying Chemicals

with 43 mg of the main component of the pheromone for this species, (Z),(Z)-3,13octadecadienyl acetate (Snow, 1990). Excellent control was achieved under either moderate or heavy population pressure. Damage was recorded in the high-density area in the first year of the trial, but no mating was recorded on mating tables, and larval infestation was attributed to infiltration of mated females from outside the treated area. After 2 years, it was impossible to conduct further trials in these peach blocks because the population had essentially been eliminated. We will return to this apparent disparity in the effect of density on mating disruption, as we believe it is of critical importance in identifying promising targets for this technique.

Male response to pheromone The male’s response to pheromone is perhaps the most important biological characteristic determining the outcome of a mating-disruption programme. Perception The most important and specialized matedetection organs in moths are the antennae. These comb-like or hairy, rod-shaped structures are adapted to sift odorant molecules from the air, which are then perceived by specifically tuned receptor cells. These olfactory receptor neurones elicit receptor potentials in response to species-specific pheromone components which manifest in specific patterns of action potentials that convey information about both odorant quantity and quality to the moth’s brain (Kaissling, 1986). Usually, just a few receptor neurones are situated within hair-like, odourperceiving structures, called sensilla, covering the external surfaces of moth antennae. Pheromone molecules adsorb on to the surface of sensilla and diffuse into the interior sensillum through minute pores sprinkled over the exterior sensillar shaft. Once inside the sensillum lymph, the hydrophobic pheromone molecules are dissolved through the association with pheromone-binding


proteins (Klein, 1987). Finally, the binding protein complexes travel from the pores to receptors on the dendritic membranes of the odour neurons. After activation of the dendritic receptor, pheromone molecules must be rapidly removed in order for the moth to detect further stimuli. This is thought to be achieved by enzymatic degradation of the pheromone molecules (Vogt and Riddiford, 1986; Rybczynski et al., 1989). The rapid termination of the pheromone signal by degrading enzymes is required for the high quantitative and temporal resolution of the odour signal (Stengl et al., 1992). The electric potential generated across moth antennae after stimulation with their pheromone was successfully measured by Schneider (1956, 1962) using the electroantennogram (EAG) technique. An EAG measures the depolarization of receptor potentials summed across the antennal olfactory neurones over the length of the antenna. EAGs have been an effective means of identifying the sensitivity of moths to odorants, quantifying dose–response relationships and measuring adaptation effects at the peripheral level of odour detection. Other researchers began to perform extracellular recordings from single sensilla and thus demonstrated the specificity of populations of sensilla to odorants in various insect taxa (Den Otter, 1977; Dickens, 1979; Fonta and Masson, 1987; Almaas and Mustaparta, 1990). Moth pheromones are commonly comprised of complex blends of components (Tamaki, 1979; O’Connell, 1981). Although the major components of such blends often elicit some behavioural responses typical of males responding to calling females, usually the full complement and correct ratio of components are required to induce the complex sequence of male sexual behaviours (Linn et al., 1984). Such sensitivity to specific blend ratios is believed to function as a mechanism for maintaining species isolation (Linn and Roelofs, 1983). It is thought that numerous types of narrowly tuned receptor neurones are specialized for detecting each separate pheromone component; this is known as the component hypothesis (O’Connell, 1972; Den Otter, 1977; Akers and O’Connell, 1988; Almaas et al., 1991). However, there is also

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 88


L.J. Gut et al.

evidence that separate components of a multicomponent pheromone blend may interact with common receptor binding sites; the blend hypothesis (O’Connell, 1985; Christensen et al., 1989). Receptors having a very high affinity for pheromonal compounds are said to be ‘tuned’ to that odour stimulus. Such ‘tuning’ is based on molecular shape, length of the carbon chain and position of double bonds and functional groups (Todd and Baker, 1997). Orientation A female-produced pheromone plume is a filamentous structure of varying internal concentration detected by males as a series of stimulus pulses of varying duration and concentration (Murlis et al., 1992). The intensity at which pheromone molecules are detected by the antennae determines the rate of action potentials generated. This information is passed to higher processing centres in the brain that control the rate of casting and counterturning behaviour, flight speed and orientation up the pheromone plume by the moth (Baker et al., 1985). This plume-following behaviour brings males within close proximity of the calling female. At this point, the high pheromone concentration, along with visual cues, arrests flight. The male and female may then undergo courtship behaviours (Baker and Cardé, 1979) and then mate. The disruption of any or the entire above-described plume following and courtship behaviours is referred to as mating disruption or pheromone confusion. Mechanisms for disruption The most popular explanatory models for disruption of pheromone-based communication are: (i) sensory adaptation at the peripheral level affecting olfactory receptors; (ii) habituation affecting processing of and normal responsiveness to olfactory information reaching the central nervous system (CNS); (iii) camouflage of female-produced plumes; and (iv) false-trail-following of synthetic pheromone plumes by male moths (Rothschild, 1981; Bartell, 1982; Cardé, 1990).

The first two mechanisms result from prolonged exposure to high and/or constant concentrations of pheromone delivered by synthetic dispensing systems. Under the third mechanism, it is assumed that male moths are unable to distinguish between female-produced pheromone plumes and the background concentration of pheromone emanating from dispensers. Finally, the fourth model postulates that males may follow the pheromone plumes generated by point sources of synthetic dispensers. Real females are thought to be out-competed by false plumes. Different combinations of the above mechanisms may be important in practical mating-disruption programmes based on crop canopy structure, wind speed, pheromone chemistry, the pheromone delivery system and the insect species. Permeation of agricultural habitats with synthetic pheromones presumably exposes the target pest moths within those localities to unnaturally high and/or constant doses of pheromone. Given this presumption, many investigations have examined the effects of short and prolonged exposures of moths to their species-specific synthetic pheromones and geometric isomers (Bartell and Roelofs, 1973; Bartell and Lawrence, 1976a,b; Linn and Roelofs, 1981; Sanders, 1985). Bartell and Lawrence (1976a,b) differentiated between two possible effects of prolonged pheromone exposure: they called the effect operating at the peripheral level ‘adaptation’ and the effect operating at the level of the CNS ‘habituation’. Many experiments directed at establishing whether adaptation or habituation validly explains mating disruption have not adequately differentiated between these two mechanisms, effectively lumping peripheral and central effects together (Rumbo and Vickers, 1997; Sanders, 1997). Numerous basic investigations have shown that exposing male moths to their pheromone decreases subsequent stereotyped behavioural responses, such as wing fanning and rapid walking. In addition, preexposed male moths were less successful in orienting towards pheromone point sources, as measured by mark–release–recapture and wind-tunnel studies (Rumbo and Vickers, 1997; Daly and Figueredo, 2000). Such studies

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 89

Behaviour–modifying Chemicals

provide evidence that either habituation in the CNS or adaptation of the peripheral sensory apparatus had affected subsequent male behaviours. At least one study (Kuenen and Baker, 1981) demonstrated that pheromone exposure of male T. ni disrupted normal orientation responses of males with no corresponding effect on the olfactory receptor neurones as measured by EAGs. These results implicate habituation of the CNS as opposed to adaptation of the peripheral receptors on the antennae as the cause of the subsequent aberrant male behaviours. Furthermore, a later study demonstrated that male C. molesta exhibited days-long habituation after exposure to their pheromone (Figueredo and Baker, 1992). Similarly, windtunnel and field experiments on Heliothis virescens (Fabricius) implicated CNS habituation lasting up to 96 h as the major mechanism for decreasing male moth response to female pheromone and as the underlying means for pheromone-based mating disruption of this species (Daly and Figueredo, 2000). Bartell and Lawrence (1976b) suggested that male moth exposures to pulsed pheromonal stimuli would more effectively reduce normal sexual responses compared with constant stimulation, because peripheral adaptation would be circumvented, allowing for greater central habituation. Kuenen and Baker (1981) obtained data supporting this hypothesis for T. ni by showing that pulsed rather than constant pre-exposure resulted in greater disorientation of subsequent sexual responses. Also, they demonstrated decreased EAG amplitudes with concurrent exposure, indicating that receptor adaptation was occurring. Therefore, this study implicated receptor adaptation in the antennae as an impediment for CNS habituation. In other words, a pheromone-exposed antenna becomes adapted and thus fires fewer action potentials in response to later pheromonal stimulation. In this sense, an adapted antenna can be considered as a filtering mechanism of the sensory information that would otherwise flood the CNS, perhaps preventing habituation and the associated reduction of normal sexual behavioural responses.


Recent studies with vertebrate olfactory receptor neurones distinguish three different forms of adaptation based on their different onset and recovery time courses and their pharmacological properties (Zufall and Leinders-Zufall, 2000). The two short-lived variants have onset times on the order of 100 ms and 4 s and corresponding recovery times of 10 s and 1.5 min, respectively. The third type of adaptation is characterized as ‘long-lasting’; onset occurs after an exposure of 25 s and subsequent recovery takes place after 6 min. In addition, research has shown that these three types of adaptation are mediated by separate molecular mechanisms (Zufall and Leinders-Zufall, 2000). There is also evidence for a distinction between long-lasting and short-lived variants of peripheral adaptation in insects. Kuenen and Baker (1981) documented a short-lived form of pheromonal adaptation in T. ni, using EAGs. In this case full receptor-cell recovery occurred within 1 min of exposure. In contrast, Schmitz et al. (1997) recorded a longerlasting antennal adaptation in Lobesia botrana Denis and Schiffermüller, using EAGs, and observed that receptor recovery took place after 5 min. Stelinski et al. (2003a) have recently documented a ‘long-lasting’ form of peripheral adaptation in Choristoneura rosaceana (Harris), along with no such corresponding adaptation in Argyrotaenia velutinana (Walker). Exposure to high doses of pheromone for 60 min reduced sensory responsiveness of C. rosaceana by up to 60%, while identical exposure of A. velutinana yielded no long-lasting peripheral sensory adaptation (Fig. 5.2). Neither species adapted after only 5 min of exposure to pheromone. The EAG responses of C. rosaceana were lowered by 55–58% following exposure to pheromone for 15 min and made a linear recovery to 70–100% of the pre-exposure response within 12.5 min at a rate of 3–4%/min (Stelinski et al., 2003a). By performing recordings from single antennal neurones, Baker et al. (1989) showed that male Agrotis segetum (Denis and Schiffermüller) olfactory receptor neurones adapted when they were exposed to high pheromone concentrations known to cause in-flight arrestment of progress toward the source. Using





Time of measurement

Before exposure 1 min after exposure 60 min after exposure 1 min after 60 min after sham sham exposure exposure

2µg Blank


Cartridge dosage









Time of measurement

Before exposure 1 min after exposure 60 min after exposure 1 min after 60 min after sham sham exposure exposure

2µg Blank


Cartridge dosage



EAG response (mV)

Fig. 5.2. Peripheral response of Choristoneura rosaceana (left) and Argyrotaenia velutinana (right) to the main component of their pheromonal blend and traces of its geometric isomer (Z11–14Ac and E11–14Ac, respectively) as measured by EAGs following 60 min exposure to high pheromone concentrations (adapted from Stelinski et al., 2003a).

EAG response (mV)


05IntpestManCh5.QXD 14/4/04 2:24 pm Page 90

L.J. Gut et al.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 91

Behaviour–modifying Chemicals

the same technique, they also showed that antennal neurones from H. virescens failed to adapt regardless of concentration. Baker et al. (1989), proposed that, given the low emission rate of (Z)-11–16:Ald from the rubber septa employed in their study, it was unlikely that H. virescens neurones were challenged to the same degree as those of A. segetum had been by the more volatile pheromone of that species. Alternatively, we suggest that A. segetum and H. virescens may differ in their susceptibility to peripheral sensory adaptation, as was observed with C. rosaceana and A. velutinana. Given these data and the fact that chemical signalling pathways are conserved among insects and vertebrates (Fein, 1986), it is possible that different molecular mechanisms and signal-transduction pathways may be involved in different forms of insect odour adaptation; these mechanisms may differ across insect taxa.

Chemical characteristics of the pheromone Moth sex-attractant pheromones are comprised of blends of straight-chain hydrocarbons, alcohols, aldehydes and acetates, varying in chain length from c. C10 to C20 and in number and isomeric configuration of internal double bonds (Tamaki, 1979; O’Connell, 1981; Chapman, 1998). All are lipids – soluble in organic solvents rather than water. In pure form, most are oils at room temperature. Moreover, it is correctly understood that these agents of longdistance sexual communication operate as volatiles. As such, sex pheromones are invisible when they travel through air; yet their powerful effects on moth behaviours provide convincing evidence that atmospheric transfer of information is occurring. Given their many similarities in the visible liquid state, it is understandable that persons working with pheromones can get lulled into envisioning that the behaviours of all these chemicals in the environment are similar. However, as the next sections will document, such a conclusion is a risky overgeneralization. Differences in molecular weight and functional group can profoundly influence rates of evaporation, dispersion in


air and adsorption on to solid surfaces. Collectively, differences in these physicochemical properties can translate into highly disparate residence times of semiochemicals in the environment and the need for tailoring application technologies to suit the particular molecular specimen being used to manipulate a pest insect. Vapour pressures The pressure attained at equilibrium by the volume of pure vapour that builds up over a pure liquid or solid in a closed vessel is known as vapour pressure (VP). This property is expressed in pressure units, e.g. mmHg. VP is an equilibrial measure – the net value of the propensities of molecules to evaporate, as well as to condense. Compounds with high VPs evaporate rapidly, while those with low VPs evaporate slowly. Moreover, VP varies exponentially with molecular weight. Therefore, plots of molecular weights of compounds in a particular class (e.g. alcohols) against log10 of VP yield straight lines (Fig. 5.3). Several notable conclusions arise from Fig. 5.3. First, VPs vary dramatically with molecular weight. Small organic molecules with low polarity, e.g. methyl acetate (C3H6O2, MW = 74) or hexane (C6H14, MW = 86) have VPs higher than 100 mmHg. In contrast, only modestly larger molecules of similar polarity, e.g. pentyl acetate (C7H14O2, MW = 130) or decane (C10H22, MW = 142) have dramatically lower VPs, < 10 mmHg. Back-calculations from the regression equations given in Fig. 5.3 reveal a consistent threefold decrease in VP for each additional –CH2– unit added to any compound in a given molecular series. Secondly, adding a particular functional group to a straightchain hydrocarbon base may strongly influence VP while adding another may not. For example, adding an –OH moiety to the corresponding hydrocarbon decreases VP by nearly 100-fold, as derived from the difference in y intercepts of the regression equations (Fig. 5.3). Only c. 4% of this change can be explained by increasing the molecular weight by 16 (one oxygen atom), leaving some 96% of the effect attributable to altered

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 92


L.J. Gut et al.

chemical characteristics – most probably increased polarity due to the prevalent hydrogen bonding of alcohols (Morrison and Boyd, 1974). An even greater effect would be expected from organic acids. In contrast, nearly all of the effect of adding an acetate moiety to a hydrocarbon base is explained by increasing molecular weight, as evidenced by acetate data adherence to the hydrocarbon line (Fig. 5.3) when regressed against molecular weight. VP data for aldehydes fall between the lines for alcohols and acetates (Fig. 5.3), consistent with their known intermediate polarity. The evaporation rate of pheromones measured in flowing open air at field-relevant temperatures is probably a parameter of greater direct relevance to applied chemical ecologists than is VP. Under these conditions, evaporation apart from condensation would be the main effect measured. Unfortunately, such data are not readily available even for standard reference com-

Log vapour pressure (mm Hg)

4 2

borer 10:Ac

(10) (1) ethanol (0.1)



= hydrocarbons = acetates = aldehydes = alcohols

methyl acetate 1:Ac pentyl acetate 5:Ac peach-twig


pounds like those in Fig. 5.3. However, some predictions can be deduced from an understanding of physicochemical properties as to how VP measures would translate into open evaporation measures. At ordinary field temperatures, small compounds (MW < 100) have a much higher propensity to evaporate than to condense (see following section). The converse is true for large compounds (MW > 200) at similar temperatures; condensation is much more favoured than evaporation. It follows that removing condensation effects from equilibrial VP measures will raise the rate of evaporation for large compounds proportionately more than for small compounds. Thus, in a plot with the log of the evaporation rate in open air on the y axis against molecular weight on the x axis, the slope of the resultant line would be expected to be smaller than the threefold reduction for VP values seen with the addition of each –CH2– (Fig. 5.3). In other words, the effect of molecular weight would be less severe on


hexanol 6:OH

OFM 12:Ac leaf-roller moths 14:Ac

10:OH codlemone 12:OH

–4 –6

peach-tree borers 18:Ac

bombykol 16:OH tomato hornworm 16:Ald

–8 –10

20 40 60 80


20 40 60 80


20 40 60 80


20 40 60 80


Molecular weight Fig. 5.3. Vapour pressures for straight-chain hydrocarbons, acetates, aldehydes and alcohols at 25ºC as a function of molecular weight. Data points were obtained from manufacturers’ MSDS sheets via website ( Estimates of vapour pressures for the selection of moth sex pheromones shown by arrows were extrapolated using the dashed lines. For the solid lines, regression equations were: (alcohols) log VP 0.034 MW 3.31; R2 0.99. Not being statistically distinguishable, data for the hydrocarbons and acetates were combined: log VP 0.030 MW 4.50; R2 = 0.96.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 93

Behaviour–modifying Chemicals

evaporation rate in free moving air than it is for equilibrial VP. Although not originally done for this purpose, we have produced some data on the relative rates of evaporation of pheromonal compounds in open moving air as a function of molecular weight. In one situation, the rates of evaporation of several milligrams of the pheromones of Oriental fruit moth (12:Ac) and peach-tree borer (18:Ac) loaded on to filter-paper discs were compared in a wind tunnel operating at c. 30°C and a wind speed of 2 m/s. In another situation, an ethanolic solution of long-chain primary alcohols was sprayed on to apple trees under typical Michigan midsummer field conditions and the disappearance of the compounds from leaves was measured over days by gas–liquid chromatography (GLC). The resultant data are co-plotted in Fig. 5.4 as time for disappearance of half the sample of applied compound against molecular weight. Although these data should be considered preliminary, the outcome supports the above prediction of a less severe molecular weight effect for free


evaporation than for equilibrial VP. For example, the difference in evaporation rates for 12:Ac vs. 18:Ac was less than two orders of magnitude, rather than the nearly three orders of magnitude predicted for VP. The 2.4-fold decrease in evaporation rate for each additional carbon compares well to the 2.7-fold decrease in evaporation rate per additional carbon recorded by McDonough et al. (1989) for acetates evaporating from rubber septa. Clearly, molecular weight still has a dramatic effect on pheromone longevity in the open air and explains the relationship across data points of Fig. 5.4 quite well. Half of the 12:Ac and 14:OH samples disappeared in less than 7 and 3 h, respectively. Over half of the 12:OH sample had evaporated in the first hour after application. Thus, the longevity at the site of release of pheromonal compounds smaller than this is fleeting under summertime field conditions. On the other hand, the longevity of the larger moth sex pheromones was appreciable. It took 10 days for half of the sample of 18:Ac to evaporate at c. 30°C. Corresponding values for C18 and C16 alcohols were 4 days

Time for half-disappearance (days)

30 10

18:Ac 18:OH



1 0.3

12:Ac 14:OH

0.1 0.03

20 40 60 80

12:OH 20 40 60 80


20 40 60 80


20 40 60 80



Molecular weight Fig. 5.4. Relative evaporation rates of differently sized straight-chain alcohols or acetates in moving air or under Michigan summertime conditions. Comparisons within a compound type (same functional group) are reliable; comparisons across compound types should be considered preliminary, as test conditions were not identical.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 94


L.J. Gut et al.

and 1 day, respectively, measures thought (by interpolation using Fig. 5.4) likely to correspond to those for C16 and C14 acetates. These large differences in VP and evaporation rates across the spectrum of moth sexpheromonal chemicals argues that the challenges in formulating them for use in pest control will likewise vary widely. For example, formulating pheromone to successfully meter it out for 1 month above a disruption threshold should be much easier for peach-tree borers than for codling moth. For peach-tree borer pheromone, the release profile (rate over time) without additives naturally lies much closer to the desired straight-line profile (representing constant release) than is true for the pheromone of codling moth or peach-twig borer, whose release profiles are naturally severely concave. Whether or not the underlying reasons were understood, this pattern of achieving greater success in formulating large vs. small pheromones is widely experienced by those manufacturing and testing pheromone formulations used as lures for traps and especially as devices for mating disruption. Adsorption of pheromones on surfaces – condensation and partitioning Another common misconception concerning the behaviour of volatile chemicals is that, once they do evaporate, it is difficult for them to be retrieved from the vapour state – i.e. achieve condensation. However, condensation is another physicochemical property that is highly influenced by the molecular weight and the functional group of given molecules (Miller, 2004). It turns out that it is remarkably easy for pheromonal compounds larger than molecular weight 200 to adsorb on to solid surfaces at ordinary environmental temperatures. The requirements are simply: (i) a short time (probably only seconds or less) to pass after evaporation and during which large molecules in the vapour state distribute some of their atypically high energy in collisions with the small gaseous molecules comprising air; and (ii) collision with a surface sufficiently large to allow multiple sites of contact between pheromone

molecule and that surface. If the forces of cohesion to various sites along the molecule collectively exceed some energetic threshold, the molecule becomes ‘adsorbed’ and begins to skid about on the surface of the solid in two- rather than three-dimensional space, as was the case in air. The temperature of this surface establishes the probability that this ‘captured’ molecule will, by chance, at some point in time, receive a sufficient energetic boost to tear it from this surface and again thrust it into the vapour state (reevaporation). The process of molecules travelling through space, sometimes in the vapour state while at other times adsorbed on to or permeating into surfaces, is known as ‘partitioning’. Significant partitioning occurs for all moth sex-pheromone molecules at normal field temperatures, provided the pheromone molecules are released into an environment in which contacts with solid surfaces are probable. We used the technique of gas–solid chromatography to quantify the degree to which moth sex pheromones of various molecular weights and functional groups partition between air and various types of solid surfaces at 25oC. Standard gas chromatography (GC) measures and equations were used to generate partitioning coefficients (Cps), which express the ratio of the compound on a solid surface over that in the adjacent gaseous phase. For example, a Cp of 1.0 means there was one pheromone molecule on the solid for every molecule in the gas immediately over that solid. A Cp of 10 indicates ten times more pheromone molecules on the surface than in the vapour immediately over it, etc. Perhaps a more intuitive way to view this phenomenon is that Cp values equate to compound ‘stickiness’; the higher the Cp value, the more sticky is the compound when contacting a solid. Figure 5.5 reveals the Cp values for various straight-chain pheromonal compounds travelling through a 2 m long × 2 mm inside diameter (i.d.) glass tube at 25°C with a nitrogen flow rate of 20 ml/min. Hydrocarbons were the least sticky. Nevertheless, even hydrocarbons with carbon numbers of 13, 14 and 15 partitioned

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 95

Behaviour–modifying Chemicals


= hydrocarbons = acetates = epoxide o = aldehyde = alcohols


Log partitioning coefficient

4 3





peach-tree borer (18:Ac) gypsy moth (19:epx) leaf-rollers (14:Ac) (14:OH) (12:Ald)

codling-moth (12:OH) o






(20:HC) (12:Ac) Oriental fruit moth; grape-berry moth

(10:Ac) peach-twig borer (10:HC)

–2 0








Molecular weight Fig. 5.5. Partitioning coefficients of straight-chain hydrocarbons and selected pheromonal compounds when moving through a narrow-bore glass tube as influenced by functional group. All data points were measured by Miller (2004); those indicated only by an arrow are extrapolated estimates.

sufficiently to be completely resolved from one another while traversing this column; they emerged in 5, 9 and 16 min, respectively. As was true for VP, stickiness increased by a consistent threefold for every additional –CH2– added to the hydrocarbons as well as their oxygenated derivatives. The preference of the C20 hydrocarbon was nearly 300-fold higher for the glass surface than for the gas immediately over it. Moreover, hydrocarbon stickiness was stable and independent of the tube composition – glass, silylanized glass, stainless steel or Teflon. This argues that the condensation effect is driven mainly by molecular energetics and is not explained only by specialized binding sites on the solid surface. Oxygenation of the hydrocarbons further increased Cp as compared with just raising the molecular weight. Adding ester, epoxide, aldehyde and hydroxy oxygens increased Cp by 1.5-, 1.5-, 10-, and 30-fold, respectively, over the corresponding hydrocarbon for the glass-tube system (Fig. 5.5). Relative to one another, the Cps for various familiar

pheromone molecules vary immensely, as visually illustrated in Fig. 5.6. For example, the Cp of 18:Ac is 100 times larger than that of 12:Ac. If the font size for the 18:Ac were adjusted to fit on the page of Fig. 5.6, the printing for 12:Ac would be illegible. Hopefully, such contrasts drive home the conclusion that pheromones can differ greatly in their physicochemical behaviour when chain lengths vary by seemingly just a few carbons. Compared with the glass tube, Cps for the oxygenated pheromonal compounds were even higher for a stainless-steel tube but lower for a Teflon tube. It is well established that the lipid pheromones under consideration are strongly retained, even at elevated temperatures, when moving through GC columns with a thin film of wax used as the stationary phase. Thus, surfaces at normal environmental temperatures, such as plant leaves and insect cuticle, which are coated with waxes, would be expected to have a strong affinity for pheromonal compounds, leading to strong adsorption and high Cps.


Fig. 5.6. Relative magnitude of partitioning coefficients of representative moth sex pheromone molecules as depicted by font size. Data derived from Fig. 5.5.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 96

L.J. Gut et al.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 97

Behaviour–modifying Chemicals

Possible consequences of pheromone partitioning effects in the field and evidence from the literature Based on the above data, the fates of pheromones deployed in crops to achieve mating disruption can be expected to vary as a function of compound molecular weight and functional group. As covered in a previous section, pheromone evaporation rates from dispensers vary widely with molecular weight. After the given molecules have evaporated, the degree to which they partition on to foliage as they are dispersed by wind again depends on the molecular properties under discussion, as well as such factors as: temperature, wind velocity and foliage density. Substantial pheromone ‘haloes’ could build up around a dispenser of a large pheromone, such as the doubly unsaturated 18:Ac of peach-tree borers. This effect will be especially large if foliage is dense, wind velocities are low, temperatures are not excessive and compounds do not quickly degrade chemically. Relative to 18:Ac, dispensers of smaller pheromones, such as codlemone ((E),(E)-8,10-12:OH), under the same conducive environmental conditions are much less likely to build up sizeable haloes, because of much reduced stickiness once evaporated and greatly increased evaporation rates after incidents of adsorption. An additional factor hindering codlemone build-up in the crop is the instability of its conjugated diene system, which is susceptible to oxidation and polymerization when exposed to sunlight and oxygen (Millar, 1995). The picture we wish to paint here for pheromone-based disruption is that the movement of pheromones through crop foliage can be viewed as occurring roughly by a process of inefficient chromatography, where the wind is the mobile phase, the foliage is the column packing, the waxes on the leaves are the stationary phase and pheromone is constantly being injected into the system. In such a system, pheromone build-up over time will be positively correlated with the density of the packing, the molecular weight of the pheromone and its


stickiness to the stationary phase. Pheromone build-up over time will be inversely correlated with wind velocity and temperature. Hopefully, an understanding of these fundamental chemical principles and the reference data provided above will assist pest managers in making implementation decisions for pheromone disruption in the face of limited data on the expected behaviours of the particular pheromone components in the field. Evidence that pheromone partitions on to foliage under field conditions is documented in the literature. However, the range of chemical structures for which it is characterized is, as yet, severely limited. The early evidence of this partitioning phenomenon by moth sex pheromones arose from observations that foliage near calling female moths or pheromone-baited traps continued to be attractive after the calling female had departed or the trap was removed (Wall et al., 1981; Wall and Perry, 1983; Noldus et al., 1991). Upon development of the field EAG measurement technique, Karg et al. (1990), working with the European grapevine moth and its doubly unsaturated 12:Ac pheromone, demonstrated that pheromone concentration in the air of disruption plots and the structure of the pheromone cloud in treated vineyards were highly dependent on the density of vegetation in the target area. Dense foliage was found to be conducive to pheromone build-up. Two possible reasons were given for this effect. First, dense foliage reduces wind velocity, thus reducing dilution of the pheromone emanating at a roughly constant rate from the hand-applied polyethylene dispensers used in these tests. Secondly, Karg et al. (1990) concluded that pheromone was adsorbing on to the grape leaves and being re-released over time. Proposed positive effects for disruption were the wider and more hom*ogeneous dispersal of pheromone throughout the crop. Working with colleagues in New Zealand, Karg et al. (1994) found that leaves placed downwind of a rope releasing (E)-11-14:Ac became maximally loaded with the pheromone of the light-brown apple moth in just 3 min, as measured by EAG. Such leaves

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 98


L.J. Gut et al.

were then shown to release EAG-detectable levels of pheromone for at least 24 h. Moreover, leaves having ample opportunity to adsorb pheromone were slightly but significantly attractive to male moths for more than 24 h when used as lures in traps. Indeed, a halo of pheromone was found around rope dispensers that had aged in the field for some days. However, for this 14:Ac, its radius was measurable only within about 15 cm of the source. This team (Suckling et al., 1996) went on to find that shut-down of trap catches continued for a day or two after pheromone dispensers were removed from disruption plots. This disruption ‘ghost effect’ was rightly attributed to the build-up of a socalled ‘buffer’ of pheromone thought to have travelled away from the dispensers and yet remaining in the crop in concentrations that remained disruptive. This several-day ‘ghost effect’ for the C-14 acetates of Epiphyas postvittana (Walker) corresponds well with our estimate from Fig. 5.4 of approximately a 1-day interval for the half-disappearance of a 14:Ac. Important questions remain to be answered with respect to these partitioning effects. Field studies should be extended to larger pheromones, which would probably produce larger haloes, as predicted by the data in Fig. 5.5. Attention should also be directed towards whether the pheromone adsorbed on or absorbed into leaves remains there or is metabolized. The unexplained rapid disappearance of 14:Ac topically applied to apple leaves (Suckling et al., 1996) provides some contradictory evidence to the simple notion that foliage would be an inert buffer for pheromone. This outcome is consistent with the unpublished preliminary observation by J.R. Miller that more than 60% of the 30 µg of 14C-labelled (Z)-11–14:Ac released into a closed vessel was taken up by apple leaves and was no longer extractable from the leaf surface after several days. Nevertheless, multiple lines of evidence now support the reality and potential importance of this partitioning phenomenon within crops. The degree to which pheromone adsorbed some distance from a dispenser contributes to disruption of communication

remains an open question. Of course, the plume of pheromone vapour coming directly from the dispenser is thought to play a key role in the success of mating disruption, consistent with conventional interpretations (Cardé and Minks, 1995; Sanders, 1997). The build-up of haloes around dispensers would definitely enlarge plumes and increase coverage by pheromones. It would probably also expand the area within the crop where resting moths are exposed to adsorbed pheromone, as suggested by Karg et al. (1994) and Karg and Sauer (1997). The possible long-lasting effects of such prolonged exposure deserve increased attention.

Influence of the physical environment It is well understood that environmental factors have a major impact on the field stability and longevity of mating-disruption formulations (Weatherston, 1990). Exposure to ultraviolet (UV) radiation and heat can degrade pheromones through oxidative decomposition, isomerization of double bonds and other chemical processes. Mating disruption may be easier to accomplish in a full-canopied crop because the pheromone is less exposed to UV. Temperature also has a major influence on the rate of pheromone emission. High temperatures increase the pheromone release rate. This may be beneficial in the short term, but ultimately it may result in reduced longevity of a disruptant. Thus, disruption formulations may require a higher pheromone-loading rate in hot, compared with cool production regions. It is also possible that cool temperatures during critical periods can reduce pheromone emission rates below the levels needed for disruption (Howell, 1992). Rainfall can adversely affect sprayable formulations by washing off a portion of the capsules or beads (Waldstein and Gut, 2003b). The distribution of pheromone is influenced by several physical factors, including wind, field or orchard topography and shape and canopy structure (Karg et al., 1990; Färbert et al., 1997). The best opportunity for disruption is where physical conditions allow for the uniform distribution of pheromone.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 99

Behaviour–modifying Chemicals

Thus, sites that are relatively calm and flat are better candidates for mating disruption than sites that experience frequent high winds or have steep slopes (Gut and Brunner, 1996). In addition, orchards with large numbers of missing trees or uneven canopies are considered poor candidates for mating disruption.

Operational factors that determine the level of success In practice, the success of mating disruption depends on the cost-effective delivery of an appropriate blend, amount and spatial distribution of pheromone for an extended period of time. Suckling and Karg (2000) identified several operational factors that affect pheromone delivery and thus the efficacy of mating disruption. Of crucial importance is the type of formulation. To a great extent, the choice of formulation defines the other operational factors. Delivery systems vary in the rate and consistency of pheromone release. They also differ in their ability to limit the impacts of temperature and UV radiation on rates of emission and pheromone stability. The effectiveness of mating disruption further depends on application parameters, such as the timing and distribution of the pheromone treatment. Ultimately, commercial success hinges on providing economically viable matingdisruption formulations.

Types of formulations At present, pheromone-based mating disruption is largely achieved through the manual application of reservoir-type release devices (Cardé and Minks, 1995; see also Table 5.4). Pheromone is enclosed in plastic or dispersed in synthetic polymers and slowly diffuses from these reservoirs over a period of several months. Pheromone is dispensed at rates of up to several micrograms per hour, which is at least 100-fold greater than the release rate of pheromone from a calling female (Sanders, 1997). Reservoir dispensers are hand-applied at a rate of at least 250 sources per hectare.


Mainly for economical reasons, the highest recommended deployment rates are usually in the range of 500–1000 dispensers per hectare. Two kinds of formulations have been developed that allow the pheromone to be sprayed on the crop either by ground or by air. Pheromone can be formulated into plastic flakes or chopped fibres designed to release pheromone at about the same rate as a calling virgin female (Brooks, 1980; Swenson and Weatherston, 1989). Female-equivalent formulations are sprayed on to a crop using customdesigned equipment, often with a sticker added so that the particles will adhere to foliage. A similar approach is to disperse pheromone in microcapsules or beads (Balken, 1980; Hall et al., 1982). The individual particles in these formulations are small enough to be applied through conventional spray equipment, but as a consequence, pheromone is released at very low rates, below those of individual calling females (Sanders, 1997). Doane (1999) has recently provided a good overview of the current status of microencapsulated pheromone formulations. This technology has proved to be efficacious against several pests, especially the pink bollworm and tomato pinworm. A recently developed approach to formulating and releasing insect sex attractants is through the use of aerosol-emitting devices, such as ‘puffers’ (Shorey et al., 1996), ‘misters’ (Mafra-Neto and Baker, 1996) or ‘microsprayers’ (Isaacs et al., 1999). Aerosol emitters are deployed at densities of only two to five per hectare, but each unit releases several milligrams of pheromone at least every 15–30 min. These super-low density devices control the release of pheromone mechanically to provide a constant predetermined release rate and a stable environment for the large volume of pheromone prior to its release. Aerosol emitters deployed at low densities have been tested for the disruption of insect pests in field crops (Shorey et al., 1996; Baker et al., 1997), tree crops (Shorey and Gerber, 1996a,b; Shorey et al., 1996), stored products (Mafra-Neto and Baker, 1996) and cranberry bogs (Baker et al., 1997). Success has varied widely; the consistently best outcomes were obtained with larger rather than smaller MW pheromones.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 100


L.J. Gut et al.

Application parameters The success of mating disruption depends on achieving an even distribution of sufficient quantities of pheromone. The most widely used pheromone formulations, including polyethylene tubes, laminates and plastic membranes or ampullae, are typically deployed at rates of 250–1000 units per hectare. The total pheromone load varies by formulation and target species and can range from 20 to 2000 g/ha in season-long disruption programmes. The amount of pheromone delivered per unit area by sprayable formulations and aerosol devices has largely been set by successes achieved using given numbers of reservoir dispensers. Microencapsulated formulations are typically applied at rates of 20–100 g of pheromone per hectare and aim to release pheromone over a period of 3–4 weeks. Multiple applications are required to achieve season-long inhibition of mate location. Aerosol emitters may be programmed to release over 700 mg of pheromone per day and may emit this large volume of active ingredient for over 120 days. At this rate, the total pheromone load provided by five units per hectare would be over 400 g. Crop damage in pheromone-treated plantings is often greater on the borders than in the interior (Knight, 1995; Gut and Brunner, 1998). Two processes are thought to contribute to the development of border infestations. Mated females emigrate from adjacent plantings that are not treated with pheromone. In addition, pheromone concentrations may be lower on the borders than in the interior (Ogawa, 1990; Karg and Sauer, 1995; Sauer and Karg, 1998), thus increasing the likelihood of males locating females and mating on the borders. Among the tactics used to protect borders is the application of extra pheromone near the edge of the planting or the extension of the pheromone treatment into adjacent plantings, if possible. Maximizing the amount of field or orchard interior relative to edge is the best protection against border damage (Fig. 5.7). Long, narrow plots are especially poor choices for mating disruption. The best approach for limiting edge effects is area-wide treatment with pheromone. Hot spots and edge infestations of Oriental fruit moth were eliminated

after implementing an area-wide disruption programme in Australia (Il’ichev et al., 2002). Large-canopied crops present special challenges for achieving an effective distribution of pheromone. The positioning of handapplied dispensers within the canopy of tree crops can dramatically affect the efficacy of mating disruption. Weisling and Knight (1995) demonstrated that significant mating of codling moth occurred when dispensers were placed in the middle, rather than in the upper portion of apple-tree canopies; the best control of codling moth with mating disruption has been achieved when dispensers are placed in the upper third of the tree canopy. Determining the most effective pattern of pheromone distribution has been largely guided by trial and error, with two primary deployment strategies being adopted: (i) a uniform distribution; or (ii) a distribution that provides for higher concentrations along the edge rather than in the plot interior. Hand-application of reservoir dispensers in a predetermined pattern distributes the pheromone load uniformly within the treated area. The recommended application rate always specifies a minimum number of dispensers needed to achieve suppression. The conventional thinking has been that sufficient numbers of dispensers are needed to provide enough false trails to compete with females. Thus, higher application rates are needed when population pressure is higher. Alternatively, we suggest that enough dispensers are needed to ‘charge’ or impregnate the area around the dispenser with sufficiently high amounts of pheromone. In this view, applying too few dispensers increases the chances of creating areas with inadequate pheromone coverage. In principle, sprayable formulations should provide a highly uniform distribuGood choice

Best choice

Poor choice

Area-wide Fig. 5.7. Selection of appropriate plots for control with pheromones.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 101

Behaviour–modifying Chemicals

tion of pheromone. However, this assumes that capsules or fibres readily stick to plant surfaces. Waldstein and Gut (2003a) found considerable variation in the propensity of microcapsules to stick to various plant surfaces. Apple wood is a better substrate than fruit, which is superior to leaves. Sticking agents are often added to sprayable formulations to improve adhesion. Even with the addition of stickers, a high percentage of microcapsules may be lost following as little as 10 cm of rain (Waldstein and Gut, 2003b). Wind is the primary means for dispersing pheromone that is emitted from aerosol devices. Pheromone distribution is also accomplished secondarily through a process of adsorption on to plant surfaces and subsequent release back into the environment (Suckling et al., 1996; refer also to our earlier discussion of chemical characteristics of the pheromone). Each unit is required to disperse pheromone over an area of at least 0.5 ha. Whether this can be achieved is questionable. The rate and extent of dispersion may vary


considerably depending on several factors, including wind conditions, plant canopy structure and chemical properties, such as relative molecular mass, inherent to the specific pheromone released. A grid of pheromonebaited traps has been used to map the apparent distribution of pheromone in 0.8 ha apple plots treated with an aerosol device, the Microsprayer (Gut and Garcia-Salazar, 2001, unpublished data). Examples of the patterns that were observed for C. pomonella and A. velutinana after the Microsprayers had been running for 2 days are presented in Fig. 5.8. Patterns of moth captures indicated that pheromone coverage was poor or absent in the areas upwind from the unit. Interestingly, a ‘ghost’ plume (sensu Suckling et al., 1996) of pheromone was observed for several days after the units were turned off, supporting the role of secondary release of adsorbed pheromone from foliage as an important means of maintaining adequate pheromone levels throughout the treated area (Gut and Garcia-Salazar, 2001, unpublished data).

Fig. 5.8. Spatial mapping of moth captures using a grid of 30 pheromone-baited traps in 0.8-ha apple plots. Numbers are total catches per day in a single trap. Captures of Cydia promonella males in a plot not treated with pheromone (top left). Captures of Cydia pomonella males in a plot treated with a single aerosol device, the MSU Microsprayer, (rectangular symbol) emitting the major component of the pheromone of this species, (E) (E) 8, 10–12 : OH (bottom left). Captures of Argyrotaenia velutinana males in a plot treated with a single aerosol device, the MSU Microsprayer, emitting the major components of the pheromone of this species, Z11–14OAc and E11–14OAc in a 96 : 4 ratio (right panel). Arrows indicate the prevailing wind direction.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 102


L.J. Gut et al.

Comparison of delivery systems Rather than predicting that any particular formulation of pheromones will out-compete and displace all others, we envision that each may find a niche within pest control. Microencapsulated pheromones may be the most convenient and quick to apply, but each application lasts for periods considerably shorter than hand- or aerosol-applied materials last. This weakness may be circumvented through the application of very low rates of pheromone at frequent intervals. Widely spaced devices appear to be particularly effective for pests that use large pheromone compounds, which have a high propensity for sticking to foliage upon wind dispersal. Moreover, such devices provide the option of releasing a mixture of pheromones of several pests simultaneously. Hand-applied pheromone formulations offer the advantages of longevity and a greater guarantee of uniform pheromone dispersal throughout the crop. However, they are more labour-intensive to apply than other techniques. This is especially true if dispensers must be applied in the upper canopy of tall trees, which is currently the recommended application protocol for disruption of some fruit pests (Gut and Brunner, 1996). In addition, the rate of release is greatly affected by environmental conditions, particularly temperature. There may be considerable variation in emission rate and field longevity among formulations or within formulations between years or in different growing regions (Thomson et al., 1998).

Economic considerations Many growers are apprehensive about using mating-disruption products because the input costs are high compared with most alternatives. These include the cost of the product and additional expenses to apply reservoirtype dispensers and intensively monitor pest populations, as well as other indirect costs associated with using an approach that only controls specifically targeted species. In an attempt to address questions concerning the high input costs associated with

mating disruption, Epstein et al. (2002) developed a model for evaluating the economics of pheromone-based management programmes. The model factored in not only input costs, but how those inputs affected fruit quality, the quantity of fruit harvested and the price received for that fruit. An approach known as ranging analysis, in the economic literature, was used. Ranging analysis takes into account variation in yield and price, with price varying depending on whether fruit was destined for the fresh or processing market. Direct comparisons of the economics of mating-disruption-based management programmes versus insecticideonly programmes demonstrated that in many cases the pheromone programmes were as inexpensive as or cheaper than the conventional programmes. The use of sprayable pheromone to enhance control of leaf-rollers was the most economical matingdisruption program, yielding increased profits of US$20/acre when the yield was average and 75% of the fruit was of freshmarket grade. The major impetus for conducting the economic analysis was to determine whether initial input costs could lead to future profits through decreased insecticide use and a larger harvest of highquality fruit. The model demonstrated the economic benefit of eliminating some insecticide applications for secondary pests if fewer sprays were used to control primary pests. Presenting this information to growers was crucial to the recruitment process and enabled the project to expand from 500 to 8000 acres over a 3-year period. Difficulties in measuring the efficacy of mating-disruption formulations in small plots has led to an overwhelming reliance on conducting such trials in large commercial plantings. The major drawbacks of on-farm experiments have been that untreated controls are usually not available and that a high level of replication cannot be accomplished. Furthermore, plots often vary substantially relative to initial pest densities and pesticide inputs throughout the season. Obtaining meaningful results from on-farm trials is indeed challenging. One approach, however, has provided a very effective means of demonstrating the economic viability of

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 103

Behaviour–modifying Chemicals

mating-disruption programmes. The general experimental design is to overlay a pheromone treatment on a portion of a large block that is being treated with insecticides. As long as the entire block receives the same sprays, differences in fruit injury can be credited to the added benefit of the disruption treatment. Gut et al. (1999) reported a threeto sixfold reduction in leaf-roller damage when mating disruption was overlaid on an insecticide programme. The growing reliance on mating disruption for control of codling moth can be attributed, in part, to the discovery by fruit growers that substantially better levels of control can be achieved by using pheromones in conjunction with a fullseason insecticide programme than by relying on insecticides alone.

Towards increased success and adoption The fact that producers rely on the deployment of pheromones for pest control on 150,000 to 200,000 ha worldwide (D. Thomson, unpublished data) justifies continued efforts to develop and implement management programmes based on the use of these behaviour-modifying chemicals. But what can be done to accelerate the successful use of mating disruption and minimize failures? There is general agreement among scientists working with this technique that a better understanding of the mechanisms underlying disruption, coupled with a good working knowledge of the biology, behaviour and mating system of target pests, is needed to improve success. Although we agree, in principle, with the above goal, we also believe that practical solutions are needed to facilitate the successful adoption of mating disruption. Despite examples of marginal efficacy in field trials and insufficient knowledge of how to improve performance, we believe that many new products will be introduced into the market-place over the next decade. Target species selection In reviewing the status of mating disruption of moth pests, Cardé and Minks (1995) con-


cluded that not all species would prove to be susceptible to this technique. As a caveat to this statement, we would add that not all pest species susceptible to mating disruption may be equally controlled. For some species, such as peach-tree borer, red-banded leaf-roller and Oriental fruit moth, treatment with pheromone alone is often sufficient to mitigate crop damage. Other pests, such as the codling moth and certain leaf-rollers, appear to be more difficult to control using only mating disruption. Providing a framework that identifies certain pest species as more amenable to mating disruption than others should improve the likelihood of success. It would also minimize the considerable time and money spent on field trials that from the outset are unlikely to be successful – or are likely to fail. Taking a very practical approach, we have examined many of the successes and failures of mating disruption and propose that the following set of criteria can be used for rating species from easy to difficult to control using mating disruption: ● Extent to which moth captures are inhibited. ● Number of dispensers necessary area to achieve control. ● Pheromone dispensed per unit achieve control. ● Extent to which the outcome is dependent.

in traps per unit area to density-

Complete or nearly complete trap shutdown is consistently achieved for some species, while for others it occurs rarely, if at all. The leaf-rollers A. velutinana and C. rosaceana are representative of the two extremes. The effectiveness of an aerosol delivery system, the MSU Microsprayer, for controlling these two species was evaluated in replicated trials in orchards in Michigan, USA. Microsprayers were placed in 0.8 ha apple blocks at densities of five units per hectare. Each unit was programmed to release a total of 410 mg of a 96 : 4 blend of (Z)-11–14:OAc : (E)-11–14:OAc per day. Moth catches in pheromone-baited traps were recorded weekly for each species in the Microsprayer-treated plots and in nearby plots not treated with pheromone. The pheromone treatment provided a very high

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 104


L.J. Gut et al.

level of inhibition of moth captures for A. velutinana, averaging 99.7% across four replicates (Fig. 5.9, top). In contrast, an average of 85% inhibition was recorded for C. rosaceana in the same plots (Fig. 5.9, bottom). Similar reductions in moth catches for these species have been recorded following the deployment of hand-applied devices or microencapsulated sprayable formulations releasing the same quantities and blend of active ingredients. Additional examples of species that are effectively inhibited from orienting to pheromone-baited traps through the deployment of a disruptant, include the tomato pinworm (Jenkins et al., 1990), lesser peach-tree borer (Snow, 1990) and Oriental fruit moth (Rice and Kirsch, 1990). Determining the amount of pheromone needed to interfere with mate location in the field has proved difficult. There have been a few examples where pheromone concentrations required for disruption in the field have been estimated (Rothschild, 1975; Koch et al., 2002), but these have largely served as broad guidelines. The resultant limit in our understanding of the required airborne pheromone concentration needed to achieve communication disruption has led to the use of a trialand-error approach in determining effective application rates. This has typically involved direct comparisons of various rates in smalland large-plot field trials. Based on this empirical approach, application rates ranging from 250 to 1000 dispensers per hectare have been established for polyethylene tubes, ampullae and other hand-applied dispensers. The number of devices deployed depends on the target species and may also vary in accordance with anticipated levels of pest pressure. The pheromone loading rate in the dispensers is often tuned to the requirements for communication disruption of a particular species. Other considerations include the cost of the active ingredient and the length of time a formulation must release pheromone. For example, a higher loading rate is required for season-long disruption of multiple-generation pests with extended periods of activity. The peach-tree borer, Synanthedon exitosa (Say), is an example of a species that is ‘easy’ to disrupt using pheromone. A low applica-

tion rate of c. 250 dispensers per hectare (one per tree), with each device releasing c. 0.3 mg of pheromone per day, provides levels of inhibition of moth catches in traps usually in excess of 97%. In addition, the level of disorientation to traps and decrease in larval densities appears to be independent of pest pressure (Snow, 1990). Similar levels of disorientation to traps and population suppression are readily achieved for the Oriental fruit moth, C. molesta (Rice and Kirsch, 1990; Vickers, 1990). In contrast, the obliquebanded leaf-roller, C. rosaceana, exemplifies a species that is ‘difficult’ to control using this technique. An application rate of 1000 dispensers per hectare, with each device loaded with 80–160 g of pheromone, provides levels of trap inhibition in the range of 85–92%. Doubling or tripling the rate of deployment does not significantly improve the level of inhibition of moth captures (Lawson et al., 1996). Also, the level of disorientation to traps and suppression of the larval population appears to be highly related to population density, with commercially acceptable impacts only observed under low pest pressure (Novak et al., 1978; Reissig et al., 1978; Roelofs and Novak, 1981; Deland et al., 1994; Agnello et al., 1996; Lawson et al., 1996; Knight, 1997). The codling moth, C. pomonella, is another example of a pest that appears to be relatively difficult to control through communication disruption. Deployment of 500 dispensers per hectare is only sufficient if pest densities are low. At higher densities, application rates up to 1000 devices per hectare and companion insecticide sprays are needed to achieve commercially acceptable control. If indeed some species are highly amenable to disruption and others are not, then what are the factors that allow the more resilient species to operate in environments permeated with synthetic pheromone? We have documented in a previous section (Male response to pheromone) that there are fundamental differences in the capacities of species to become adapted and/or habituated when exposed to high doses of synthetic pheromone. In addition, we know that species differ in their dispersal and reproductive capabilities. Finally, we have provided evidence in an earlier section

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 105

Behaviour–modifying Chemicals

an advantage to moth species such as C. rosaceana relative to species such as A. velutinana, which do not appear to exhibit a physiological capacity for a long-lasting form of adaptation (Stelinski et al., 2003a). For example, perhaps moths under long-lasting adaptation might sufficiently subdue their overt sexual responses so as to preclude exhaustion and cause them to depart from extraordinarily high-concentration pheromone sites where the likelihood of mate-finding is low. If they then happen to arrive in a location of low or no pheromone, disadaptation would occur within a short interval (10–15 min) and their ability to discriminate and orient to a natural pheromone plume would be restored, provided the possible effects of CNS habituation were shielded (Bartell and Lawrence, 1976b; Kuenen and Baker, 1981). Evenden et al. (2000) subjected male C.

Mean moths per trap per week ± SE

(Chemical characteristics of the pheromone) that pheromones vary considerably with respect to rates of evaporation, dispersion in air and adsorption on to solid surfaces. Collectively, differences in these physicochemical properties can have profound effects on the longevity and movement of pheromones in the environment. It is these basic differences in the properties of moths and their pheromones that make some species highly susceptible to mating disruption, while others are capable of averting the effects of this control technique (Fig. 5.9). Certain lepidopteran species appear to be good ‘adapters’ in that they are physiologically capable of decreasing their sensitivity to pheromone for an extended period of time following pheromone exposure. We speculate that, under pheromone mating-disruption regimes, long-lasting adaptation may confer 35 30 25

Pheromone Control

20 15 10 5 0 Jun

Mean moths per trap per week ± SE





4.5 4.0


3.5 3.0


2.5 2.0 1.5 1.0 0.5 0.0 Jun




Fig. 5.9. Inhibition of Argyrotaenia velutinana (upper) and Choristoneura rosaceana (lower) male catches in pheromone-baited traps following deployment of a disruption treatment. An aerosol delivery system, the MSU Microsprayer, was placed in 0.8-ha apple plots at densities of five units per hectare. Each unit was programmed to release a total of 400 mg of a 96 : 4 blend of the main component of their pheromonal blend and traces of its geometric isomer (Z-11–14Ac and E11–14Ac). SE, standard error.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 106


L.J. Gut et al.

rosaceana to 1 h of constant pheromone exposure and then tested their behavioural response to a pheromone source in a windtunnel 10–30 min after the exposure treatments. Constant pre-exposure did not alter the proportion of males orienting upwind to pheromone plumes in the wind-tunnel. The conclusion was that habituation probably plays a minor role as a mechanism of mating disruption in this species. Evenden et al. (2000) chose to assay their pheromoneexposed C. rosaceana 10–30 min after treatment in order to avoid the effects of antennal adaptation. Our results showed that olfactory receptor neurones of C. rosaceana disadapt within 12.5 min after constant pre-exposure to pheromone. Therefore, the combined results of our study and that of Evenden et al. (2000) suggest that ‘long-lasting’ adaptation may shield C. rosaceana from CNS habituation, explaining why this species could successfully orient to pheromone point sources shortly after constant exposure to pheromone. Alternatively, both adaptation and habituation might occur, but recovery from both might be rapid. Currently, hand-applied rope dispensers are the dominant method of dispensing pheromone for mating disruption of moth pests in orchards (Nagata, 1989; Agnello et al., 1996; Knight et al., 1998; Knight and Turner, 1999). The release rate for ropes marketed for leaf-roller moths averages c. 11 ng/s (Knight et al., 1998; Knight and Turner, 1999). Moths within the treated crop could perceive the applied pheromone in several ways, including: (i) as a ‘cloud’ of pheromone resulting from a coalescence of plumes emanating from the many dispensers; (ii) as a localized plume downwind of a nearly dispenser; or (iii) a moth could even be attracted on to a dispenser. In our field tests, C. rosaceana did exhibit longlasting adaptation upon exposure to pheromone ropes, but only when held within a few centimetres of the dispenser (Stelinski et al., 2003b). Nevertheless, these results demonstrate that this phenomenon can occur under field conditions. Use of lowdensity, high-release dispensers, such as puffers (Shorey and Gerber, 1996a,b) or microsprayers (Isaacs et al., 1999), offers an

even greater opportunity for target moths to be exposed to extraordinarily high concentrations of pheromone as the pheromone solution emitted in an aerosol spray falls on to foliage and droplets of pure pheromone accumulate over time on the source tree. Moreover, large and highly concentrated plumes are thought to waft great distances downwind of the source trees. However, it remains to be determined whether moths exhibit the behavioural capacity for ‘dosing’ themselves with enough pheromone in the field for physiological phenomena such as long-lasting adaptation to be relevant under mating disruption. Implementing a pheromone-based management programme for a pest that has been identified as easy to disrupt improves the chances for success, but it certainly does not ensure that control will be achieved or that it will be economical. The success of mating disruption in the field or orchard depends on cost-effective delivery of the active ingredient. Achieving this requires addressing the many factors or conditions, other than the moth and its pheromone, that have an impact on a mating disruption programme. We propose that, in practice, it is this set of conditions that determines the level of difficulty in meeting requirements for successful disruption of a particular pest species (Fig. 5.10). Operational requirements for successful mating disruption broadly include technical considerations, such as pheromone-delivery strategies, crop-management considerations and characteristics of the site, including initial pest density. Growers, consultants, extension personnel and others with a very applied viewpoint emphasize the need for disruption formulations that are economical relative to other control tactics, easy to use and compatible with current IPM programmes. From a technical standpoint, the delivery system that is selected must release the appropriate blend and amount of pheromone. It must also provide for an adequate distribution of the active ingredient over an extended period of time. Perhaps the most crucial management decision is the selection of an appropriate area to be treated in terms of size and pest pressure. The likelihood of failure certainly

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 107

Behaviour–modifying Chemicals








Difficult Ease of disruption

Conditions A e.g. low pest density

Conditions B e.g. moderate pest density


Conditions C e.g. high pest density


Level of difficulty in meeting requirements for successful disruption Fig. 5.10. Conceptualization of differences in the susceptibility of various species to mating disruption based on fundamental properties of the moths and their pheromones (upper). Species are red-banded leafroller (RBLR), greater peach-tree borer (GPTB), tomato pinworm (TPW), Oriental fruit moth (OFM), codling moth (CM), pandemis leaf-roller (PLR) and oblique-banded leaf-roller (OBLR). Conceptualization of differences in the level of difficulty of disrupting a particular species based on all of the factors other than the moth and its pheromone, such as physical characteristics of the site or starting pest density (lower).

increases if site selection does not minimize opportunities for immigration by mated females. In addition, the best successes for many species will be achieved where pest pressure is not too high. Operational requirements for successful disruption can vary depending on anticipated pest pressure. For example, a relatively low application rate of 500 dispensers per acre is sufficient for communication disruption and control of codling moth if pest pressure is low. The level of difficulty in meeting the requirements for successful disruption in this case is low (Fig. 5.10, conditions A). Control of codling moth can also be achieved under moderate pest pressure, but a full rate of 1000 dispensers per acre needs to be applied. Control of this pest is difficult to achieve where initial pest pressure is high, as even high application rates of at least 1000 dispensers per hectare cannot prevent mating. The difficulty in meeting the requirements for disruption of codling moth in these cases is moderate and high, respectively (Fig. 5.10, conditions B and C). Traditionally, little attention has been focused on selecting appropriate targets prior to the development of a mating-disruption formulation. As pointed out by Doane (1999), there were suggestions over 20 years ago that habituation may be easier to elicit in species

where fairly low doses impede the approach of males to a pheromone source (Cardé et al., 1975; Baker and Roelofs, 1981). Yet, since these early observations, considerable attention has been focused on some species that have proved to be difficult candidates for disruption. The apparent driving force for these efforts is the importance of the pest economically. We propose that it may not be necessary to carry out detailed sets of experiments to determine the disruption capacity (high to low) among pest species. As a starting-point, the simplest measure may be, as was suggested over 25 years ago, the dose response of a species for orienting to various loading rates of pheromone lures. Some species, such as the Oriental fruit moth and tomato pinworm, are attracted to a narrow range of concentrations. A single hollow fibre attracted significantly more tomato pinworm moths than five or more fibre lures (Wyman, 1979). For Oriental fruit moth, high doses caused arrestment of upwind progress of males as they approached the source (Cardé et al., 1975; Baker and Roelofs, 1981). A similar response was observed for spruce budworm, C. fumiferana, and Oriental fruit moth orienting to high-dose lures in wind tunnels (Sanders and Lucuik, 1996). All of these species, which are maximally attracted to low-dose lures, also appear

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 108

L.J. Gut et al.

to have a low capacity to avert communication disruption. In contrast, other species that exhibit high levels of attraction to a comparatively wider range of pheromone loadings appear to be more difficult to disrupt. Included in this second group is C. rosaceana, which is readily captured in traps baited with a wide range of dosages (Fig. 5.11). Area-wide approach The best successes with mating disruption have been achieved where large, contiguous areas have been treated with pheromone. Excellent control of Oriental fruit moth was obtained following implementation of areawide disruption programmes in 1100 ha of apples and pears in Australia (Il’ichev et al., 2002) and 1200 ha of mixed stone fruits in the Tulbagh valley in South Africa (Barnes and Blomefield, 1997). The US Department of Agriculture (USDA) sponsored the Codling Moth Area-wide Management Program (CAMP), adopting an IPM approach that relied on mating disruption technology and judicious and timely applications of insecticides for management of codling moth in pome fruit in the western USA (Calkins et al., 2000; Brunner et al., 2001). The number of CAMP sites and their size increased from an initial five sites totalling 1260 ha in 1995 to over a dozen sites totalling approximately 4000 ha by 1999. The results of this project were impressive, with pest densities, as measured by moth captures in pheromone traps and fruit injury at harvest, declining to very Mean fruit injury (%) 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0

1994 1995 1996 1997

Area 1

Area 2

Mean no. of moths per trap per week


6 5 4 3 2 1 0 0×



Relative lure dosage

Fig. 5.11. Effect of lure dosage on captures of Choristoneura rosaceana in pheromone-baited traps (L. Stelinski, 2002, unpublished data).

low levels following implementation of an area-wide approach (Fig. 5.12). In addition, direct comparisons with conventional programmes outside the project area revealed dramatic reductions in the number of insecticides applied for codling-moth control in CAMP orchards. Similar levels of success have been achieved through governmentsupported projects to control pink bollworm with pheromones in vast areas of cotton in the south-western USA (Staten et al., 1997) and Egypt (Jones and Casagrande, 2000). Season-long versus targeted use of pheromones Commercial development of disruption products has largely been geared towards

Mean moths per trap per season

Mean OP applications per season













0 Area 1


Area 2

Area 1

Area 2

Fig. 5.12. Summary of results for two locations that were part of the Codling Moth Area-wide Management Program, USA, during the year prior to using mating disruption (1994) and the first 3 years of area-wide disruption (adapted from Calkins et al., 2000; Brunner et al., 2001). OP, organophosphorus insecticide.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 109

Behaviour–modifying Chemicals

providing season-long control of a pest population. The first application of pheromone is typically applied at or prior to the start of adult flight for the targeted pest. Additional treatments are made if the residual activity of the pheromone product does not cover the entire flight period. Although certain disruption products have achieved great success season-long, there are some critical limitations to this approach. Season-long control of some multivoltine species may require maintaining pheromone in the crop for over 180 days. This may be economically prohibitive or technically infeasible. Targeted use of pheromones is an alternative approach that could provide new opportunities for some mating-disruption formulations. This strategy entails targeted use of a disruption formulation to affect a key period of adult activity. Sprayable pheromone formulations offer the greatest opportunity for incorporation into pest-management programmes in such a selective manner. We can envision microcapsules serving as a means for delivering a variety of insect pheromones. Perhaps they could be used in an ‘off-theshelf ’ approach, much like that adopted for lures used to attract pests to traps and monitor their activity. Suppliers of monitoring tools often rely on a single delivery device, such as a red septum, as the basis for a large product line. A key advantage of using pheromones in a targeted manner is that expensive matingdisruption products can be applied on an asneeded basis. This is in contrast to the preventive basis of using pheromones dictated by the season-long approach, with the disruption product typically applied prior to start of flight and often prior to any knowledge of pest density. In this situation, a grower must make an up-front investment in an expensive and, to some extent, risky technology. Microencapsulated formulations have recently been registered for suppression of Oriental fruit moth. These may be especially useful in crops such as apple, where this pest is generally only a problem late in the season. Multispecies disruption The extreme specificity of sex pheromones means there will be advantages and disad-


vantages to their use in pest management. Mating-disruption technologies are nontoxic to natural enemies. As a result, greater reliance on these highly selective tactics for pest control will increase the potential for biological control of secondary pests. On the other hand, the use of pheromone-based technology and the subsequent reduction in insecticides for a primary pest frequently result in outbreaks of other pests (Ridgway et al., 1990; Thomson et al., 1998). Growers are keenly aware of the potential risks and added costs associated with secondary-pest outbreaks. The need to control several pest species is a major factor limiting the acceptance of disruption technologies in some crop-production systems. For example, over a dozen lepidopteran species can reach damaging levels in eastern apple-production systems (Epstein and Gut, 2000). Included in this mix is a complex of leaf-rollers that have overlapping activity periods and cause similar damage. Pfeiffer et al. (1993) tested the viability of mating disruption for a complex of four tortricids using various generic blends. All formulations proved ineffective for one or more species, presumably because they were not sufficiently similar to the natural blend. It may be worth revisiting this approach as new technologies are developed. For example, newly developed polyethylene twintube dispensers offer the possibility of emitting two generic blends, one from each tube, while applying only one device for both pheromone blends. A few hand-applied dispensers containing the attractive blends for two or three species with very different pheromone components are either already commercially available or will soon be on the market. In large-plot field trials conducted over the past 2 years, multispecies formulations for codling moth and Oriental fruit moth or for these two species and oblique-banded leafroller have performed as well as the singlespecies products currently in commercial use (L.J. Gut, 2002, unpublished data). A concern with multiple-species reservoir-type dispensers is that the pheromones may interact in ways that reduce the efficacy of disruption against one or more target species. For

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 110


L.J. Gut et al.

example, Snow (1990) reported that release of only pure (E,Z)-3,13-octadecadenyl acetate (EZA) shut down captures of lesser peachtree borer, while various blends, excluding pure EZA, significantly reduced captures of greater peach-tree borer. Successful disruption of lesser and greater peach-tree borer required that the specific blends most attractive to each species were provided in separate dispensers deployed on opposite sides of trees. Other problems that need to be addressed include the application timing and chemical interactions that affect the longevity of pheromone release. The spring emergence of Oriental fruit moth occurs c. 2 weeks before that of codling moth and c. 6 weeks prior to oblique-banded leaf-roller. A multispecies dispenser containing the pheromones of all three of these pests would have to be applied either prior to or after, the beginning of flight for at least one species. In addition, blending codlemone and (Z)11–14:OAc in the same tube accelerates the release of codlemone, apparently because the acetate is a good solvent for the alcohol. Sprayable formulations are now being tested or used commercially for a number of insect pests. It is possible that future pestcontrol programmes in tree-fruit crops may include sprayable products for codling moth, oblique-banded and red-banded leaf-rollers, tufted apple bud-moth and Oriental fruit moth. The advantage of this approach is that each spray can be timed to coincide with the start of flight for each pest. This may improve efficacy and be more economical, as

expensive active ingredients are not wasted, contrary to when multispecies hand-applied dispensers are used. Implementation and demonstration programmes: a key to success A major determinant of the success of mating disruption for pest control is the extent to which growers will adopt these technologies, which are generally information-intensive, risky and expensive in comparison with conventional remedies. The best means of gaining acceptance for these sophisticated and less-certain pest-control methods is to demonstrate, on farm, that they are efficacious and economical. Investment in demonstration and implementation projects has been the key to widespread adoption of pheromone technologies in most cases where it has occurred. The rate of adoption of codling-moth mating disruption in Washington, USA, as estimated by Brunner et al. (2001) and J.F. Brunner (unpublished data), is illustrated in Fig. 5.13. Isomate-C® was registered in 1991 as the first matingdisruption product for codling-moth control in the USA. On-farm trials were immediately implemented by USDA and Washington State University researchers and comprised a large percentage of the acreage treated with pheromone in the first year. Parallel 3-year studies that followed the transition of appleorchard management with conventional or organic pest-control programmes to a pheromone-based management programme

Total hectares treated





30,000 25,000 20,000 15,000 10,000 5000 0 1990







Fig. 5.13. Use of codling-moth mating-disruption products in Washington, USA (adapted from Brunner et al., 2001).

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 111

Behaviour–modifying Chemicals

provided the foundation for educating growers about the risks and benefits of this novel technology (Knight, 1995; Gut and Brunner, 1998). The number of growers trying the technique gradually increased and, in most cases, they achieved satisfactory control. Where failures did occur they were usually associated with smaller plot sizes, especially where neighbouring orchards served as a source of immigrating mated females. The USDA-sponsored CAMP was initiated in 1995 to address the issue of border effects and the need for improved monitoring and, in general, to facilitate greater adoption of mating disruption. The apple acreage under mating disruption in Washington increased dramatically over a period of 5 years, reaching a peak in 2000 at 37,000 ha, or 50% of state’s total apple acreage. Perhaps the greatest achievement of this project was that the growers have continued coordinated efforts over large areas since the USDA terminated their role in the area-wide programme in 1999. This 10-year transition to the large-scale, sustained use of mating disruption has been replicated in other production systems and in other parts of the world. The basic approach has been to establish a partnership between government or other public enterprises and producers. These demonstration sites serve as the catalyst and educational foundation for new sites in subsequent years, culminating in a large, coordinated effort between farmers and others involved in the production system. To be successful on an area-wide scale, the project must engage the infrastructure that is already in place in making management decisions. Critical participants include, among others, farmers, suppliers of control products, consultants and university extension and research personnel. A robust implementation programme involves educational programmes, including hands-on training, economic analysis, documentation of programme efficacy, regular communication between the participants and, often, some kind of financial incentive. To be successful, it must be an evolving process that develops and incorporates new control and monitoring technologies to overcome problems that are certain to arise. We


believe this process is central to increased adoption of mating disruption.

Concluding Remarks Substantial progress in developing semiochemical-based pest-management products that are commercially viable has certainly been made over the past 10 years, with mating-disruption formulations leading the way. We have no doubt that this trend will continue over the next decade. Two factors, one practical and the other biological, appear to provide the greatest impediment to the adoption of direct controls based on the use of behaviour-modifying chemicals. Mass trapping, attack-and-kill and mating disruption are expensive techniques compared with insecticidal control. It is hoped that the direct costs of the active ingredients will fall in the future. Meanwhile, the research community, farmers and others involved in commercial production systems must work together to develop cost-effective ways of using semiochemicals. As recognized early on by Knipling (1979) and others, pest density is a very crucial limiting factor to pest control using semiochemicals. Two approaches that have successfully mitigated the problem of controlling highdensity populations are area-wide programmes and the use of companion insecticide sprays. In the second approach, insecticides are used either to reduce initial population densities or as a supplement to the semiochemical-based tactic. Wyatt (1997) proposed that, to make the task of developing mating disruption for various pests manageable, we should search for patterns and good predictors of success. We have proposed a set of criteria for predicting the success of mating disruption for a particular species or for the same species under varying conditions. Now, the challenge for us and hopefully also for others is to explore the usefulness of this scheme. There is a heightened need for both good monitoring tools and alternatives to pesticides. As we mentioned at the outset, new regulations governing the use of pesticides and the regular occurrence of resistance to

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 112


L.J. Gut et al.

chemical controls provide a strong impetus for the adoption of behavioural controls. In addition, behavioural controls have the added advantages of negligible environmen-

tal impact and increased compatibility with biological and cultural methods of control. It is truly an exciting time to be working with semiochemicals.

References Agnello, A.M., Spangler, S.M. and Reissig, W.H. (1990) Development and evaluation of a more efficient monitoring system for apple maggot (Diptera: Tephritidae). Journal of Economic Entomology 83, 539–546. Agnello, A.M., Reissig, W.H., Spangler, S.M., Charlton, R.E. and Kain, D.P. (1996) Trap response and fruit damage by obliquebanded leafroller (Lepidoptera: Torticidae) in pheromone-treated apple orchards in New York. Enviromental Entomology 25, 268–282. Akers, R.P. and O’Connell, R.J. (1988) The contribution of olfactory receptor neurones to the perception of pheromone component ratios in male redbanded leafroller moths. Journal of Comparative Physiology 163, 641–650. Almaas, T.J. and Mustaparta, H. (1990) Pheromone reception in tobacco moth, Heliothis virescens. Journal of Chemical Ecology 16, 1331–1347. Almaas, T.J., Christensen, T.A. and Mustaparta, H. (1991) Antennal receptor neurons encode several features of intra- and interspecific odorants in the male corn earworm moth Helicoverpa zea. Journal of Comparative Physiology 169, 249–258. Atanassov, A., Shearer, P.W., Hamilton, G. and Polk, D. (2002) Development and implementation of a reduced risk peach arthropod management program in New Jersey. Journal of Economic Entomology 95, 803–812. Ayyappathe, R., Poloavarapa, S. and McGuire, M. (2000) Effectiveness of thiomethoxam-coated spheres against blueberry maggot flies (Diptera: Tephritidae). Journal of Economic Entomology 93, 1473–1479. Baker, T.C. and Cardé, R.T. (1979) Courtship behavior of the Oriental fruit moth (Grapholitha molesta): experimental analysis and consideration of the role of sexual selection in the evolution of courtship pheromones in the Lepidoptera. Annals of the Entomological Society of America 72, 173–188. Baker, T.C. and Roelofs, W.L. (1981) Initiation and termination of Oriental fruit moth male response to pheromone concentrations in the field. Environmental Entomology 10, 211–218. Baker, T.C., Willis, M.A., Haynes, K.F. and Phelan, P.L. (1985) A pulsed cloud of sex pheromone elicits upwind flight in male moths. Physiological Entomology 10, 257–265. Baker, T.C., Hansson, B.S., Löfstedt, C. and Löfqvist, J. (1989) Adaptation of male moth antennal neurons in a pheromone plume is associated with cessation of pheromone-mediated flight. Chemical Senses 14, 439–448. Baker, T.C., Dittl, T. and Mafra-Neto, A. (1997) Disruption of sex pheromone communication in the blackheaded fireworm in Wisconsin cranberry marshes by using MSTRS devices. Journal of Agricultural Entomology 14, 449–457. Bakke, A. and Lie, R. (1989) Mass trapping. In: Jutsum, A.R. and Gordon, R.F.S. (eds) Insect Pheromones in Plant Protection. Wiley, Chichester, UK, pp. 67–87. Balken, J.A. (1980) Microencapsulation using coacervation/phase separation techniques. In: Kydonius, A.E. (ed.) Controlled Release Technologies: Methods and Applications, Vol. II. CRC Press, Boca Raton, Florida, pp. 83–105. Barnes, B.N. and Blomefield, T.L. (1997) Goading growers towards mating disruption: the South African experience with Grapholita molesta and Cydia pomonella (Lepidoptera: Tortricidae). IOBC WPRS Bulletin 20, 45–56. Barrett, B.A. (1995) Effect of synthetic pheromone permeation on captures of male codling moth (Lepidoptera: Tortricidae) in pheromone and virgin female moth-baited traps at different tree heights in small orchard blocks. Environmental Entomology 24, 1201–1206. Bartell, R.J. (1982) Mechanisms of communication disruption by pheromone in the control of Lepidoptera: a review. Physiological Entomology 7, 353–364. Bartell, R.J. and Lawrence, L.A. (1976a) Reduction in responsiveness of Epiphyyas postvittana (Lepidoptera) to sex pheromone following pulsed pheromonal exposure. Physiological Entomology 2, 1–6.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 113

Behaviour–modifying Chemicals


Bartell, R.J. and Lawrence, L.A. (1976b) Reduction in responsiveness of male light-brown apple moths, Epiphyas postvittana, to sex pheromone following pulsed pre-exposure to pheromone components. Physiological Entomology 2, 89–95. Bartell, R.J. and Roelofs, W.L. (1973) Inhibition of sexual response in males of the moth Argyrotaenia velutinana by brief exposures to synthetic pheromone or its geometrical isomer. Journal of Insect Physiology 19, 655–661. Beers, E.H., Brunner, J.F., Willet, M.J. and Warner, G.M. (1993) Orchard Pest Management: a Resource for the Pacific Northwest. Good Fruit Grower, Yakima, Washington, 276 pp. Borden, J.H. (1990) Use of semiochemicals to manage coniferous tree pests in Western Canada. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 281–315. Borden, J.H. (1997) Disruption of semiochemical-mediated aggregation in bark beetles. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 421–438. Bradley, S.I., Walker, J.T.S., Wearing, C.H., Shaw, P.W. and Hodson, A.J. (1998) The use of pheromone traps for leafroller action thresholds in pipfruit. Proceedings of the New Zealand Plant Protection Conference 51, 173–178. Brooks, T.W. (1980) Controlled vapor release from hollow fibers: theory and applications with insect pheromones. In: Kydonius, A.E. (ed.) Controlled Release Technologies: Methods and Applications, Vol II. CRC Press, Boca Raton, Florida, pp. 165–193. Brunner, J., Welter, S., Calkins, C., Hilton, R., Beers, E., Dunley, J., Unruh, T., Knight, A., VanSteenwyk, R. and Van Buskirk, P. (2001) Mating disruption of codling moth: a perspective from the Western United States. IOBC WPRS Bulletin 25, 207–215. Buchelos, C.T. and Levinson, A.R. (1993) Efficacy of multisurface traps and Lasiotraps with and without pheromone addition, for monitoring and mass-trapping of Lasioderma serricorne F. (Col., Anobiidae) in insecticide-free tobacco stores. Journal of Applied Entomology 116, 440–448. Calkins, C.O., Knight, A.L., Richardson, G. and Bloem, K.A. (2000) Area-wide population suppression of codling moth. In: Tan, K.-H. (ed.) Area-wide Control of Fruit Flies and Other Insect Pests. Peneritg Universiti Sains Malaysia, Pulau Pinang, pp. 215–219. Campbell, C.D., Walgenbach, J.F. and Kennedy, G.G. (1992) Comparison of black light and pheromone traps for monitoring Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in tomato. Journal of Agricultural Entomology 9, 17–24. Cardé, R.T. (1990) Principles of mating disruption. In: Ridgeway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Pest Management: Applications of Pheromones and Other Attractants. Marcel Dekker, New York, pp. 47–71. Cardé, R.T. and Elkinton, J.S. (1984) Field trapping with attractants: methods and interpretation. In: Hummel, H.E. and Miller, T.A. (eds) Techniques in Pheromone Research. Springer-Verlag, New York, pp. 111–129. Cardé, R.T. and Minks, A.K. (1995) Control of moth pests by mating disruption: successes and constraints. Annual Review of Entomology 40, 559–585. Cardé, R.T. and Minks, A.K. (eds) (1997) Insect Pheromone Research, New Directions. Chapman & Hall, New York, 684 pp. Cardé, R.T., Baker, T.C. and Roelofs, W.L. (1975) Ethological function of components of a sex attractant system for Oriental fruit moth males, Grapholita molesta (Lepidoptera: Tortricidae). Journal of Chemical Ecology 1, 475–491. Chapman, R.F. (1998) The Insects: Structure and Function. Cambridge University Press, Cambridge, UK, 770 pp. Charmillot, P.-J. (1990) Mating disruption technique to control codling moth in western Switzerland. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 165–182. Charmillot, P.-J., Hofer, D. and Pasquier, D. (2000) Attract and kill: a new control of the codling moth Cydia pomonella. Entomologia Experimentalis et Applicata 94, 211–216. Christensen, T.A., Mustaparta, H. and Hildebrand, J.G. (1989) Discrimination of sex pheromone blends in the olfactory system of the moth. Chemical Senses 14, 463–477. Daly, K.C. and Figueredo, A.J. (2000) Habituation of sexual response in male Heliothis moths. Physiological Entomology 25, 180–191.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 114


L.J. Gut et al.

deLame, F.M., Hong, J.J., Shearer, P.W. and Brattsten, L.B. (2001) Sex-related differences in the tolerance of Oriental fruit moth, Grapholita molesta, to organophosphate insecticides. Pest Management Science 57, 827–832. Deland, J.-P., Judd, G.J.R. and Roitberg, B.D. (1994) Disruption of pheromone communication in three sympatric leafroller (Lepidoptera: Tortricidae) pests of apple in British Columbia. Environmental Entomology 23, 1084–1090. Den Otter, C.J. (1977) Single sensillum responses in the male moth Adoxophyes orana (F.v.R.) to female sex pheromone components and their geometrical isomers. Journal of Comparative Physiology 121, 205–222. Derrick, M.E., Van Duyn, J.W., Sorenson, C.E. and Kennedy, G.C. (1992) Effect of pheromone trap placement on capture of male European corn borer (Lepidoptera: Pyralidae) in three North Carolina crops. Environmental Entomology 21, 240–246. Dickens, J.C. (1979) Electrophysiological investigations of olfaction in bark beetles. Mitteilungen der Schweizerishce Entomologische Gesellschaft 52, 203–216. Doane, C.D. (1999) Controlled-release devices for pheromones. In: Scher, H.B. (ed.) Controlled-release Delivery Systems for Pesticides. Marcel Dekker, New York, pp. 295–317. Duan, J.J. and Prokopy, R.J. (1995) Development of pesticide-treated spheres for controlling apple maggot flies (Diptera: Tephritidae): pesticides and residue extending agents. Journal of Economic Entomology 88, 117–126. Epstein, D. and Gut, L. (2000) A Pocket Guide for IPM Scouting in Michigan Apples. Extension Bulletin E2720, Michigan State University, East Lansing, Michigan, 72 pp. Epstein, D., Waldstein, D. and Edson, C. (2002) Michigan Apple Integrated Pest Management Implementation Project. Final Narrative Report. East Lansing, Michigan, 99 pp. Evenden, M.L., Borden, J.H. and Van Sickle, G.A. (1995) Predictive capabilities of a pheromone-based monitoring system for western hemlock looper (Lepidoptera: Geometridae). Environmental Entomology 24, 933–943. Evenden, M.L., Judd, G.J.R. and Borden, J.H. (2000) Investigations of mechanisms of pheromone communication disruption of Choristoneura rosaceana (Harris) in a wind tunnel. Journal of Insect Behavior 13, 499–510. Faccioli, G., Antropoli, A. and Pasqualini, E. (1993) Relationship between males caught with low pheromone doses and larval infestation of Argyrotainia pulchellana. Entomologia Experimentalis et Applicata 68, 165–170. Färbert, P., Koch, U.T., Färbert, A. and Staten, R.T. (1997) Measuring pheromone concentrations in cotton fields with the EAG method. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 347–358. Fein, A. (1986) Excitation and adaptation of Limulus photoreceptors by light and inositol 1,4,5-triphosphate. Trends in Neuroscience 9, 110–114. Figueredo, A.J. and Baker, T.C. (1992) Reduction of the response to sex pheromone in the Oriental fruit moth, Grapholita molesta (Lepidoptera: Torticidae) following successive pheromonal exposures. Journal of Insect Behavior 5, 347–361. Fonta, C. and Masson, C. (1987) Structural and functional studies of the peripheral olfactory nervous system of male and female bumble bees (Bombus hypnorum and B. terrestris). Chemical Senses 12, 53–69. Furlong, M.J., Pell, J.K., Choo, O.P. and Rahman, S.A. (1995) Field and laboratory evaluation of a sex pheromone trap for the autodissemination of a fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth Plutella xylostella (Lepidoptera: Yponomeutidae). Bulletin of Entomological Research 85, 331–337. Gaston, L.K., Shorey, H.H. and Sario, S.A. (1967) Insect population control by the use of sex pheromones to inhibit orientation between the sexes. Nature 213, 1155. Gordon, F.C. and Potter, D.A. (1985) Efficiency of Japanese beetle (Coleoptera: Scarabaeidae) traps in reducing defoliation of plants in the urban landscape and effect on larval density in turf. Journal of Economic Entomology 78, 774–778. Gordon, F.C. and Potter, D.A. (1986) Japanese beetle (Coleoptera: Scarabaeidae) traps: evaluation of single and multiple arrangements for reducing defoliation in urban landscapes. Journal of Economic Entomology 79, 1381–1384. Gut, L. and Brunner, J. (1996) Implementing Codling Moth Mating Disruption in Washington Pome Fruit Orchards. Tree Fruit Research and Extension Center Information Series 1, Washington State University, Wenatchee, Washington, 8 pp.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 115

Behaviour–modifying Chemicals


Gut, L. and Brunner, J. (1998) Pheromone-based management of codling moth (Lepidoptera: Tortricidae) in Washington apple orchards. Journal of Agricultural Entomology 15, 387–405. Gut, L.J., Wise, J., Isaacs, R. and McGhee, P. (1999) Obliquebanded leafroller control tactics and management strategies: 1998 update. Proceedings of the Michigan State Horticulture Society 128, 97–106. Hall, D.R., Nesbitt, B.F., Marrs, G.J., Green, A.StJ., Campion, D.G. and Critchley, B.R. (1982) Development of microencapsulated pheromone formulations. In: Leonhardt, B.A. and Beroza, M. (eds) Insect Pheromone Technology: Chemistry and Applications. ACS Symposium Series Number 190. American Chemical Society, Washington, DC, pp. 131–143. Hardie, J. and Minks, A.K. (eds) (1999) Pheromones of Non-lepidopteran Insects Associated with Agricultural Plants. CAB International, Wallingford, UK, 466 pp. Haynes, K.F., Miller, T.A., Staten, R.T., Li, W.G. and Baker, T.C. (1987) Pheromone trap for monitoring insecticide resistance in the pink bollworm moth (Lepidoptera: Gelechiidae), new tool for resistance management. Environmental Entomology 16, 84–89. Howell, J.F. (1992) Control of codling moth (Cydia pomonella) using pheromone to disrupt mating (Lepidoptera: Tortricidae). In: Proceedings XIX International Congress of Entomology. Beijing, p. 202. Hu, X.P., Shasha, B.S., McGuire, M.R. and Prokopy, R.J. (1998) Controlled release of sugar and toxicant from a novel device for controlling pest insects. Journal of Controlled Release 50, 257–265. Il’ichev, A. and Sexton, S.B. (2002) Reduced application rates of mating disruption for effective control of Oriental fruit moth Grapholita molesta (Busck) (Lepidoptera: Tortricidae) on pears. General and Applied Entomology 31, 47–51. Il’ichev, A.L., Gut, L.J., Hossain, M.S., Williams, D.G. and Jerie, P.H. (2002) Area-wide approach for improved control of Oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae) by mating disruption. General and Applied Entomology 31, 7–15. Isaacs, R., Ulczynscki, M., Wright, B., Gut, L.J. and Miller, J.R. (1999) Performance of a microsprayer specifically designed for pheromone-mediated control of insect pests. Journal of Economic Entomology 92, 1157–1164. Jackson, D.M., Brown, G.C., Nordin, G.L. and Johnson, D.W. (1992) Autodissemination of a baculovirus for management of tobacco budworms (Lepidoptera: Noctuidae) on tobacco. Journal of Economic Entomology 85, 710–719. James, D.G., Bartelt, R.J. and Moore, C.J. (1996) Mass-trapping of Carpophilus spp. (Coleoptera: Nitidulidae) in stone fruit orchards using synthetic aggregation pheromones and a coattractant: development of a strategy for population suppression. Journal of Chemical Ecology 22, 1541–1556. Jenkins, J.W., Doane, C.C., Schuster, D.J., McLaughlin, J.R. and Jimenez, M.J. (1990) Development and commercial application of sex pheromone for control of the tomato pinworm. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 269–280. Johnson, R.L. and Schall, R.A. (1989) Early detection of new pests. In: Kahn, R.P. (ed.) Plant Protection and Quarantine, Vol. III. CRC Press, Boca Raton, Florida, pp. 105–116. Jones, O.T. (1998) Practical applications of pheromones and other semiochemicals. In: House, P.E., Stevens, I.D.R. and Jones, O.T. (eds) Insect Pheromones and Their Use in Pest Management. Chapman & Hall, London, pp. 261–355. Jones, O.T. and Casagrande, E.D. (2000) The use of semichemical-based devices and formulations in areawide programmes: a commercial perspective. In: Tan, K.-H. (ed.) Area-wide Control of Fruit Flies and Other Insect Pests. Peneritg Universiti Sains Malaysia, Pulau Pinang, pp. 285–293. Judd, G.J.R., Gardiner, M.G.T. and Thomson, D.R. (1996) Commercial treals of pheromone-mediated mating disruption with Isomate-C® to control codling moth in British Columbia apple and pear orchards. Journal of the Entomological Society of British Columbia 92, 23–34. Jutsum, A.R. and Gordon, R.F.S. (eds) (1989) Insect Pheromones in Plant Protection. Wiley, Chichester, UK, 369 pp. Kaissling, K.-E. (1986) Chemo-electrical transduction in insect olfactory receptors. Annual Review of Neuroscience 9, 121–145. Karg, G. and Sauer, A.E. (1995) Spatial distribution of pheromones in fields treated for mating disruption of the European grape vine moth Lobesia botrana measured with electroantennograms. Journal of Chemical Ecology 21, 1299–1314. Karg, G. and Sauer, A.E. (1997) Seasonal variation of pheromone concentration in mating disruption trials against European grape vine moth, Lobesia botrana (Lepidoptera: Tortricidae) measured by EAG. Journal of Chemical Ecology 23, 487–501.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 116


L.J. Gut et al.

Karg, G., Sauer, A.E. and Koch, U.T. (1990) The influence of plants on the development of pheromone atmospheres measured by EAG method. In: Elsner, N. and Roth G. (eds) Brain-Perception-Cognition, Proceedings of the 18th Gottingen Neurobiology Conference. Thieme Verlag, Stuttgart, p. 301. Karg, G., Suckling, D.M. and Bradley, S.J. (1994) Adsorption and release of pheromone of Epiphyas postvittana (Lepidoptera: Tortricidae) by apple leaves. Journal of Chemical Ecology 20, 1825–1841. Karlson, P. and Lüscher, M. (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183, 55–56. Klein, M.G. and Lacey, L.A. (1999) An attractive trap for autodissemination of entomopathogenic fungi into populations of Japanese beetle, Popillia japonica (Coleoptera: Scarabaeidae). Biocontrol Science and Technology 9, 151–158. Klein, M.O. (1981) Mass trapping for suppression of Japanese beetles. In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals. Plenum Press, New York, pp. 183–190. Klein, U. (1987) Sensillum-lymph proteins from antennal olfactory hairs of the moth Antheraea polyphemus (Saturniidae): Insect Biochemistry 8, 1193–1204. Knight, A.L. (1995) The impact of codling moth (Lepidoptera: Tortricidae) mating disruption on apple pest management in Yakima Valley, Washington. Journal of the Entomological Society of British Columbia 92, 29–38. Knight, A.L. (1997) Mating disruption of leafrollers in Washington’s apple orchards. La Difesa delle Piante 20, 73–77. Knight, A.L. and Croft, B.A. (1991) Modelling and prediction technology. In: van der Geest, L.P.S. and Evenhuis, H.H. (eds) Tortricid Pests: Their Biology, Natural Enemies and Control. World Crop Pests Volume 5. Elsevier, Amsterdam, pp. 301–312. Knight, A.L. and Hull, L.A. (1988) Area-wide population dynamics of Platynota idaeusalis (Lepidoptera: Tortricidae) in Southcentral Pennsylvania pome and stone fruits. Environmental Entomology 17, 1000–1008. Knight, A.L. and Hull, L.A. (1989) Use of sex pheromone traps to monitor azinphosmethyl resistance in tufted apple bud moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 82, 1019–1026. Knight, A.L. and Turner, J.E. (1999) Mating disruption of Pandemis spp. (Lepidoptera: Torticidae). Environmental Entomology 28, 81–87. Knight, A.L. and Weissling, T.J. (1999) Behavior-modifying chemicals in management of arthropod pests. In: Ruberson, J.R. (ed.) Handbook of Pest Management. Marcel Dekker, New York, pp. 521–545. Knight, A.L., Thomson, D.R. and co*ckfield, S.D. (1998) Developing mating disruption of obliquebanded leafroller (Lepidoptera: Tortricidae) in Washington State. Environmental Entomology 27, 1080–1088. Knipling, E.F. (1979) The Basic Principles of Insect Populations Suppression and Management. Agriculture Handbook 512, USDA, Washington, DC, 659 pp. Koch, U.T., Cardé, A.M. and Cardé, R.T. (2002) Calibration of an EAG system to measure airborne concentration of pheromone formulated for mating disruption of the pink bollworm moth, Pectinophora gossypiella (Saunders) (Lep., Gelechiidae). Journal of Applied Entomology 126, 431–435. Koutek, B., Hoskovec, M., Vrkocova, P., Konecny, K. and Feltl, L. (1994) Gas chromatographic determination of vapor pressures of pheromone-like compounds II. Alcohols. Journal of Chromatography 679, 307–317. Koutek, B., Hoskovec, M., Vrkocova, P., Konecny, K., Feltl, L. and Vrkoc, J. (1996) Gas chromatographic determination of vapor pressures of pheromone-like compounds III. Aldehydes. Journal of Chromatography 719, 391–400. Koutek, B., Hoskovec, M., Vrkocova, P. and Feltl, L. (1997) Gas chromatographic determination of vapor pressures of pheromone-like compounds IV. Acetates, a reinvestigation. Journal of Chromatography 759, 93–109. Kuenen, L.P.S. and Baker, T.C. (1981) Habituation versus sensory adaptation as the cause of reduced attraction following pulsed and constant sex pheromone pre-exposure in Trichoplusia ni. Journal of Insect Physiology 27, 721–726. Kydonieus, A.F. and Beroza, M. (1982) Insect Suppression with Controlled Release Pheromone Systems, Vols 1 and 2. CRC Press, Boca Raton, Florida. Lanier, G.N. (1990) Principles of attraction–annihilation. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 25–45.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 117

Behaviour–modifying Chemicals


Latheef, M.A., Witz, J.A. and Lopez, J.D. Jr (1991) Relationships among pheromone trap catches of male corn earworm moths (Lepidoptera: Noctuidae), egg numbers, and phenology in corn. Canadian Entomologist 123, 271–281. Lawson, D.S., Reissig, W.H., Agnello, A.M., Nyrop, J.P. and Roelofs, W.L. (1996) Interference with the mate-finding communication system of the obliquebanded leafroller (Lepidoptera: Tortricidae) using synthetic sex pheromones. Environmental Entomology 25, 895–905. Liburd, O.E., Gut, L.J., Stelinski, L.L., Whalon, M.E., McGuire, M.R., Wise, J.C., Willett, J.L., Hu, X.P. and Prokopy, R.J. (1999) Mortality of Rhagoletis species encountering pesticide-treated spheres (Diptera: Tephritidae). Journal of Economic Entomology 92, 1151–1156. Light, D.M., Knight, A.K., Henrick, C.A., Rajapaska, D., Lingren, B., Dickens, J.C., Reynolds, K.M., Buttery, R.G., Merrill, G., Roitman, J. and Campbell, B.C. (2001) A pear-derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.). Naturwissenschaften 88, 333–338. Lindgren, B.S. and Borden, J.H. (1993) Displacement and aggregation of mountain pine beetles, Dendroctonus ponderosae (Coleoptera: Scolytidae) in response to their antiaggregation and aggregation pheromones. Canadian Journal of Forest Research 23, 286–290. Linn, C.E. Jr and Roelofs, W.L. (1981) Modification of sex pheromone blend discrimination in male Oriental fruit moths by pre-exposure to (E)-8-dodecenyl acetate. Physiological Entomology 6, 421–429. Linn, C.E. Jr and Roelofs, W.L. (1983) Effect on varying proportions of the alcohol component on sex pheromone blend discrimination in male Oriental fruit moths. Physiological Entomology 8, 291–306. Linn, C.E., Bjostad, L.B., Du, J.W. and Roelofs, W.L. (1984) Redundancy in a chemical signal: behavioral responses of male Trichoplusia ni to a 6-component sex pheromone blend. Journal of Chemical Ecology 10, 1635–1658. Mafra-Neto, A. and Baker, T.C. (1996) Timed, metered sprays of pheromone disrupt mating of Cauda cautella (Lepidoptera: Pyralidae). Journal of Agricultural Entomology 13, 149–168. Mayer, M.S. and McLaughlin, J.R. (1991) Handbook of Insect Pheromones and Sex Attractants. CRC Press, Boca Raton, Florida, 1083 pp. McBrien, H., Judd, G.J.R. and Borden, J.H. (1994) Campylomma verbasci (Heteroptera: Miridae): pheromone-based seasonal flight patterns and prediction of nymphal densities in apple orchards. Journal of Economic Entomology 23, 1224–1229. McDonough, L.M., Brown, D.F. and Aller, W.C. (1989) Insect sex pheromones – effect of temperature on evaporation rates of acetates from rubber septa. Journal of Chemical Ecology 15, 779–790. Metcalf, R.L. and Metcalf, E.R. (1992) Plant Kairomones in Insect Ecology and Control. Chapman & Hall, New York, 168 pp. Millar, J.G. (1995) Degradation and stabilization of E8,E10-dodecadienol, the major component of the sex pheromone of the codling moth (Lepidoptera: Tortricidae). Journal of Economic Entomology 88, 1425–1432. Miller, J.R. (2004) Adsorptive interactions of insect pheromone-like compounds with inorganic solid surfaces: quantifying partitioning coefficients by gas–solid chromatography. Journal of Chemical Ecology (in review). Miller, J.R. and Cowles, R.S. (1990) Stimulo-deterrent diversion: a concept and its possible application to onion maggot control. Journal of Chemical Ecology 16, 3197–3212. Mitchell, E.R. (ed.) (1981) Management of Insect Pests with Semiochemicals. Plenum, New York, 514 pp. Mitchell, E.R., Copeland, W.W., Sparks, A.N. and Sekul, A.A. (1974) Fall armyworm: disruption of pheromone communication with synthetic acetates. Environmental Entomology 3, 778–780. Morewood, P., Gries, G., Liska, Kapitola, P., Häußler, D., Möller, K. and Bogenshutz, H. (2000) Towards pheromone-based monitoring in nun moth, Lymantria monacha (L.) (Lep., Lymantriidae) populations. Journal of Applied Entomology 124, 77–85. Morrison, R.J. and Boyd, R.N. (1974) Organic Chemistry, 3rd edn. Allin and Bacon, Boston, Massachusetts. Morse, B.W. and Kulman, H.M. (1985) Monitoring damage by yellowheaded spruce sawflies with sawfly and parasitoid pheromones. Environmental Entomology 14, 131–133. Murlis, J., Elkinton, J.S. and Cardé, R.T. (1992) Odor plumes and how insects use them. Annual Review of Entomology 37, 505–532. Nagata, K. (1989) Revue: pest control by mating disruption in Japan. Japanese Pesticide Information 54, 3–6. Noldus, L.P.J., Potting, R.P.J. and Barendrengt, H.E. (1991) Moth sex pheromone adsorption to leaf surfaces: bridges in time for chemical spies. Physiological Entomology 6, 71–86.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 118


L.J. Gut et al.

Nordlund, D.A., Jones, R.L. and Lewis, W.J. (1981) Semiochemicals: Their Role in Pest Control. John Wiley & Sons, New York, 306 pp. Norris, R.F., Caswell-Chen, E.P. and Kogan, M. (2003) Concepts in Integrated Pest Management. Prentice Hall, Upper Saddle River, New Jersey, 586 pp. Novak, M.A., Reissig, W.H. and Roelofs, W.L. (1978) Orientation disruption of Argyrotaenia velutinana and Choristoneura rosaceana (Lepidoptera: Tortricidae) male moths. Journal of the New York Entomological Society 4, 311–315. O’Connell, R.J. (1972) Response of olfactory receptors to the sex attractant, its synergist and inhibitor in the redbanded leaf roller, Argyrotaenia velutinana. In: Schneider, D. (ed.) International Symposium Olfaction Taste IV, Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp. 180–186. O’Connell, R.J. (1981) The encoding of behaviorally important odorants by insect chemosensory neurons. In: Norris, D.M. (ed.) Perception of Behavioral Chemicals. Elsevier/North-Holland Biomedical Press, New York, pp. 133–163 O’Connell, R.J. (1985) Responses to pheromone blends in insect olfactory neurons. Journal of Comparative Physioliology 156, 747–761. Ogawa, K. (1990) Commercial development: mating disruption of tea tortrix moths. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 547–551. Park, J.D. and Goh, H.G. (1992) Control of beet armyworm, Spodoptera exigua Hubner (Lepidoptera: Noctuidae), using synthetic sex pheromone. I. Control by mass trapping in Allium fistulosum field. Korean Journal of Applied Entomology 31, 45–49. Pfeiffer, D.G., Kaakeh, W., Killian, J.C., Lachance, M.W. and Kirsch, P. (1993) Mating disruption to control damage by leafrollers in Virginia apple orchards. Entomologia Experimentalis et Applicata 67, 47–56. Prokopy, R.J., Wright, S.E., Black, J.L., Hu, X.P. and McGuire, M.R. (2000) Attracticidal spheres for controlling apple maggot flies: commercial-orchard trials. Entomologia Experimentalis et Applicata 97, 293–299. Reissig, W.H., Novak, M. and Roelofs, W.L. (1978) Orientation disruption of Argyrotaenia velutinana and Choristoneura rosaceana male moths. Environmental Entomolology 7, 631–635. Rice, R.E. and Kirsch, P. (1990) Mating disruption of Oriental fruit moth in the United States. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 193–211. Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) (1990) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, 761 pp. Riedl, H., Hoying, S.A., Barnett, W.W. and Detar, J.E. (1979) Relationship of within-tree placement of the pheromone trap to codling moth catches. Environmental Entomology 8, 765–769. Riedl, H., Seaman, A. and Henrie, F. (1985) Monitoring susceptibility to azinphosmethyl in field populations of the codling moth (Lepidoptera: Tortricidae) with pheromone traps. Journal of Economic Entomology 78, 692–699. Riedl, H., Howell, J.F., McNally, P.S. and Westigard, P.H. (1986) Codling Moth Management, Use and Standardization of Pheromone Trapping Systems. Bulletin 1918, University of California, Berkeley, California, 23 pp. Riherd, C., Nguyen, R. and Brazzel, J.R. (1994) Pest free areas. In: Sharpe, J.L. and Hallman, G.J. (eds) Quarantine Treatments for Pests of Food Plants. Westview Press, Boulder, Colorado, pp. 213–223. Ritter, F.J. (eds) (1979) Chemical Ecology: Odour Communication in Animals. Elsevier/North-Holland, Amsterdam, 427 pp. Roelofs, W.H. and Novak, M. (1981) Small-plot disorientation tests for screening potential mating disruptants. In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals: Concepts and Practice. Plenum, New York, pp. 229–242. Roelofs, W.L., Glass, E.H., Tette, J. and Comeau, A. (1970) Sex pheromone trapping for red-banded leaf roller control: theoretical and actual. Journal of Economic Entomology 63, 1162–1167. Rothschild, G.H.L. (1975) Control of Oriental fruit moth (Cydia molesta [Busck][Lepidoptera, Tortricidae]) with synthetic female pheromone. Bulletin of Entomological Research 65, 473–490. Rothschild, G.H.L. (1981) Mating disruption of lepidopterous pests: current status and future prospects. In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals: Concepts and Practice. Plenum Press, New York, pp. 207–228. Rumbo, E.R. and Vickers, R.A. (1997) Prolonged adaptation as possible mating disruption mechanism in Oriental fruit moth, Cydia (=Grapholita) molesta. Journal of Chemical Ecology 23, 445–457.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 119

Behaviour–modifying Chemicals


Rybczynski, R., Reagan, J. and Lerner, M.R. (1989) A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. Journal of Neuroscience 9, 1341–1353. Sanders, C.J. (1985) Disruption of spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae), mating in a wind tunnel by synthetic pheromone: role of habituation. Canadian Entomologist 117, 391–393. Sanders, C.J. (1988) Monitoring spruce budworm population density with sex pheromone traps. Canadian Entomologist 120, 175–183. Sanders, C.J. (1997) Mechanisms of mating disruption in moths. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 333–346. Sanders, C.J. and Lucuik, G.S. (1996) Disruption of male Oriental fruit moth to calling females in a wind tunnel by different concentrations of synthetic pheromone. Journal of Chemical Ecology 22, 1971–1986. Sauer, A.E. and Karg, G. (1998) Variables affecting the pheromone concentration in vineyards treated for mating disruption of grape vine moth. Journal of Chemical Ecology 24, 289–302. Schlyter, F. and Birgersson, G.A. (1999) Forest beetles. In: Hardie, J. and Minks, A.K. (eds) Pheromones of Non-lepidopteran Insects Associated with Agricultural Plants. CAB International, Wallingford, UK, pp. 113–148. Schmitz, V., Renou, M., Roehrich, R., Stockel, J. and Lecharpentier, P. (1997) Disruption mechanisms in the European grape moth Lobesia botrana Den & Schiff. III. Sensory adaptation and habituation. Journal of Chemical Ecology 23, 83–95. Schneider, D. (1956) Electrophysical investigation on the antennal receptors of the silk moth during chemical and mechanical stimulation. Experientia 13, 89–91. Schneider, D. (1962) Electrophysical investigation on the olfactory specificity of sexual attracting substance in different species of moths. Journal of Insect Physiology 8, 15–30. Schwalbe, C.P. and Mastro, V. (1990) Use of pheromones and attractants by government agencies in the United States. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-Modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 619–630. Sexton, S.B. and Il’ichev, A. (2000) Pheromone mating disruption with reference to Oriental fruit moth Grapholita molesta (Busck) (Lepidoptera: Tortricidae): literature review. General and Applied Entomology 29, 63–68. Shapas, T.J., Burkholder, W.E. and Boush, G.M. (1977) Population suppression of Trigoderma glabrum by using pheromone luring for protozoan pathogen dissemination. Journal of Economic Entomology 70, 469–474. Shearer, P.W. and Riedl, H. (1994) Comparison of pheromone trap bioassays for monitoring insecticide resistance in Phyllonorycter elmaella (Lepidoptera: Gracillariidae). Journal of Economic Entomology 87, 1450–1454. Shearer, P.W. and Usmani, K.A. (2001) Sex-related response to organophosphorous and carbamate insecticides in adult Oriental fruit moth, Grapholita molesta. Pest Management Science 57, 822–826. Shorey, H.H. and Gerber, R.G. (1996a) Use of puffers for disruption of sex pheromone communication among navel orangeworm moths (Lepidoptera:Pyralidae) in almonds, pistachios, and walnuts. Environmental Entomology 25, 1154–1157. Shorey, H.H. and Gerber, R.G. (1996b) Use of puffers for disruption of sex pheromone communication of codling moths (Lepidoptera: Tortricidae) in walnut orchards. Environmental Entomology 25, 1398–1400. Shorey, H.H. and McKelvey, J.J. (1977) Chemical Control of Insect Behavior. John Wiley & Sons, New York, 414 pp. Shorey, H.H., Kaae, R.S. and Gaston, L.K. (1974) Sex pheromones of Lepidoptera: development of a method for pheromonal control of Pectinophora gossypiella in cotton. Journal of Economic Entomology 67, 347. Shorey, H.H., Sisk, C.B. and Gerber, R.G. (1996) Widely separated pheromone release sites for disruption of sex pheromone communication in two species of Lepidoptera. Environmental Entomology 25, 446–451. Simandl, J. and Anderbrant, O. (1995) Spatial distribution of flying Neodiprion sertifer (Hymenoptera, Diprionidae) males in a mature Pinus sylvestris stand as determined by pheromone trap catch. Scandinavian Journal of Forest Research 10, 51–55. Snow, J.W. (1990) Peachtree borer and lesser peachtree borer control in the United States. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 241–253.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 120


L.J. Gut et al.

Stanley, B.H., Reissig, W.H., Roelofs, W.L., Schwarz, M.R. and Shoemaker, C.A. (1987) Timing treatments for apple maggot (Diptera: Tephritidae) control using sticky sphere traps baited with synthetic apple volatiles. Journal of Economic Entomology 80, 1057–1063. Staten, R.T., El-Lissy, O. and Antilla, L. (1997) Successful area-wide program to control pink bollworm by mating disruption. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 383–396. Stelinski, L.L. and Liburd, O.E. (2001) Evaluation of various deployment strategies of imidaclopridtreated spheres in highland blueberries for control of Rhagoletis mendax (Diptera: Tephritidae). Journal of Economic Entomology 94, 905–910. Stelinski, L.L., Liburd, O.E., Wright, S., Prokopy, R.J., Behle, R. and McGuire, M.R. (2001) Comparison of neonicotinoid insecticides for use with biodegradable and wooden spheres for control of Rhagoletis species (Diptera: Tephritidae). Journal of Economic Entomology 94, 1142–1150. Stelinski, L.L., Miller, J.R. and Gut, L.J. (2003a) Presence of long-lasting peripheral adaptation in the obliquebanded leafroller, Choristoneura rosaceana and absence of such adaptation in the redbanded leafroller, Argyrotaenia velutinana. Journal of Chemical Ecology 29, 405–423. Stelinski, L.L., Gut, L.J. and Miller, J.R. (2003b) Concentration of air-borne pheromone required for longlasting peripheral adaptation in the obliquebanded leafroller, Choristoneura rosaceana. Physiological Entomology 29, 97–107. Stengl, M., Hatt, H. and Breer, H. (1992) Peripheral processes in insect olfaction. Annual Review of Physiology 54, 665–681. Suckling, D.M. and Brockerhoff, E.G. (1999) Control of light brown apple moth (Lepidoptera: Tortricidae) using an attracticide. Journal of Economic Entomology 92, 367–372. Suckling, D.M. and Karg, G. (2000) Pheromones and other semiochemicals. In: Rechcigl, J. and Rechcigl, N. (eds) Biological and Biotechnological Control of Insect Pests. CRC Press, Boca Raton, Florida, pp. 63–99. Suckling, D.M. and Shaw, P.W. (1992) Conditions that favor mating disruption of Epiphyas postvittana (Lepidoptera: Tortricidae): Environmental Entomology 21, 949–956. Suckling, D.M., Penman, D.R., Chapman, R.B. and Wearing, C.H. (1985) Pheromone use in insecticide resistance surveys of the light brown apple moth Epiphyas postvittana. Journal of Economic Entomology 78, 204–206. Suckling, D.M., Karg, G. and Bradley, S.J. (1996) Apple foliage enhances mating disruption of lightbrown apple moth. Journal of Chemical Ecology 22, 325–341. Swenson, D.W. and Weatherston, I. (1989) Hollow-fiber controlled-release systems. In: Jutsum, A.R. and Gordon, R.F.S. (eds) Insect Pheromones in Plant Protection. Wiley, Chichester, UK, pp. 173–197. Tamaki, Y. (1979) Multi-component sex pheromone of Lepidoptera with special reference to Adoxophyes sp. In: Ritter, F.J. (ed.) Chemical Ecology: Odour Communication in Animals. Elsevier/North-Holland, Amsterdam, pp. 169–180. Taschenberg, E.F., Cardé, R.T. and Roelofs, W.L. (1974) Sex pheromone mass trapping and mating disruption for control of redbanded leafroller and grape berry moths in vineyards. Environmental Entomology 3, 239–242. Tatsuki, S. (1990) Application of the sex pheromone of the rice stem borer moth, Chilo suppressalis. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 387–406. Thayer, G.R. (2002) The sampling range of pheromone traps baited with lures of different strengths for monitoring obliquebanded leafroller, Choristoneura rosaceana Harris (Lepidoptera: Tortricidae). MS thesis, Washington State University, Pullman, Washington, 55 pp. Thomson, D.R., Gut, L.J. and Jenkins, J.W. (1998) Pheromones for insect control. In: Hall, F.R. and Menn, J.J. (eds) Methods in Biotechnology, Vol. 5: Biopesticides: Use and Delivery. Humana Press, Totowa, New Jersey, pp. 385–412. Todd, J.L. and Baker, T.C. (1997) The cutting edge of insect olfaction. American Entomologist 43, 174–182. Trematerra, P. and Battaini, F. (1987) Control of Ephestia kuehniella Zeller by mass-trapping. Journal of Applied Entomology 104, 336–340. Trimble, R.M. (1995) Mating disruption for control of codling moth Cydia pomonella (L.) (Lepidoptera: Tortricidae), in organic apple production in Southwestern Ontario. Canadian Entomologist 127, 493–505. Van Steenwyk, R.A., Oatman, E.R. and Wyman, J.A. (1983) Density treatment level for tomato pinworm (Lepidoptera: Gelechiidae) based on pheromone trap catches. Journal of Economic Entomology 76, 440–445.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 121

Behaviour–modifying Chemicals


Varela, L.G., Shearer, P.W., Jones, V.P., Riedl, H. and Welter, S.C. (1997) Monitoring of insecticide resistance in Phyllonorycter mespilella (Lepidoptera: Gracillariidae) in four western states. Journal of Economic Entomology 90, 252–260. Vega, F.E., Dowd, P.F. and Bartelt, R.J. (1995) Dissemination of microbial agents using an autoinoculating device and several insect species as vectors. Biological Control 5, 545–552. Vickers, R.A. (1990) Oriental fruit moth in Australia and Canada. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 183–192. Vickers, R.A., Thwaite, W.G., Williams, D.G. and Nicholas, A.H. (1998) Control of codling moth in small plots by mating disruption: alone and with limited insecticide. Entomologia Experimentalis et Applicata 86, 229–239. Vogt, R.G. and Riddiford, L.M. (1986) Pheromone reception: a kinetic equilibrium. In: Payne, T.L., Birch, M.C. and Kennedy, C.E.J. (eds) Mechanisms in Insect Olfaction. Clarendon Press, Oxford, pp. 201–208. Waldstein, D.W. and Gut, L.J. (2003a) Comparison of microcapsule density with various apple tissues and formulations of Oriental fruit moth (Lepidoptera: Tortricidae) sprayable pheromone. Journal of Economic Entomology 96, 58–63. Waldstein, D.W. and Gut, L.J. (2003b) Effects of rain and sunlight on Oriental fruit moth (Lepidoptera: Tortricidae) microcapsules applied to apple foliage. Pest Management Science (in review). Wall, C. (1989) Monitoring and spray timing. In: Jutsum, A.R. and Gordon, R.F.S. (eds) Insect Pheromones in Plant Protection. Wiley, Chichester, UK, pp. 39–66. Wall, C. and Perry, J.N. (1983) Further observations on the responses of male pea moth, Cydia nigricana, to vegetation previously exposed to sex-attractant. Entomologia Experimentalis et Applicata 33, 112–116. Wall, C. and Perry, J.N. (1987) Range of action of moth sex-attractant sources. Entomologia Experimentalis et Applicata 44, 5–14. Wall, C., Sturgeon, D.M., Greenway, A.R. and Perry, J.N. (1981) Contamination of vegetation with synthetic sex attractant released from traps for the pea moth, Cydia nigricana. Entomologia Experimentalis et Applicata 30, 111–115. Wawrzynski, R.P. and Ascerno, M.E. (1998) Mass trapping for Japanese beetle (Coleoptera: Scaraaeidae) suppression in isolated areas. Journal of Arboriculture 24, 303–307. Weatherston, I. (1990) Principles of design of controlled-release formulations. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management. Marcel Dekker, New York, pp. 93–112. Weisling, T.J. and Knight, A.K. (1995) Vertical distribution of codling moth adults in pheromone-treated and untreated plots. Entomologia Experimentalis et Applicata 77, 271–275. Welch, S.M., Croft, B.A. and Michels, M.F. (1981) Validation of pest management models. Environmental Entomology 10, 425–432. Whittaker, R.H. and Feeney, P. (1971) Allelochemicals: chemical interactions between species. Science 171, 757–770. Wood, D.L., Silverstein, R.M. and Nakajima, M. (1970) Control of Insect Behavior by Natural Products. Academic Press, New York, 345 pp. Wyatt, T.D. (1997) Putting pheromones to work: paths forward for direct control. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research, New Directions. Chapman & Hall, New York, pp. 445–459. Wyman, J.A. (1979) Effect of trap design and sex attractant release on tomato pinworm catches. Journal of Economic Entomology 72, 865–868. Zhang, G.-F., Meng, S.-Z., Han, Y. and Sheng, C.-F. (2002) Chinese tortrix Cydia trasisas (Lepidoptera: Olethreutidae): suppression on street-planting trees by mass trapping with sex pheromone traps. Environmental Entomology 31, 602–607. Zufall, F. and Leinders-Zufall, T. (2000) The cellular and molecular basis of odor adaptation. Chemical Senses 25, 473–481.

05IntpestManCh5.QXD 14/4/04 2:24 pm Page 122

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 123


Transgenic Insecticidal Cultivars in Integrated Pest Management: Challenges and Opportunities

Julio S. Bernal, Jarrad Prasifka, M. Sétamou and K.M. Heinz Department of Entomology, Biological Control Laboratory, Texas A&M University, College Station, TX 77843-2475, USA E-mail: [emailprotected]

Introduction Transgenic insect-resistant cultivars were first developed in the mid-1980s and were commercially available starting in the mid1990s (Hilder et al., 1987; Vaeck et al., 1987). Transgenic potato cultivars expressing a toxic protein derived from the bacterium Bacillus thuringiensis Berliner (hereafter Bt) were available to farmers in 1995, while maize and cotton varieties also expressing Bt toxins were available 1 year later. All three commercial introductions were made in the USA, but currently a number of transgenic cultivars are planted in different countries worldwide (e.g. cotton in Australia and Mexico). Thus far, development of insectresistant cultivars has followed two broad approaches. One approach seeks to develop transgenic cultivars by incorporating genes of plant origin that express proteins that interfere with protein and sugar metabolism, whereas the other seeks to incorporate genes of bacterial origin, largely from Bt, which are acutely toxic to insects (Hilder et al., 1987; Vaeck et al., 1987). Crop losses due to insect pests account for a substantial portion of total crop losses worldwide. One estimate indicates that c. 13% of total crop production

is lost annually to insect pests in the USA (Pimentel et al., 1993). However, perhaps more significant than the extent of losses is the failure, despite ample research investments, to make any substantial progress towards reducing these losses. Losses due to insect pests in the first half of the 20th century were on average ~9%, while losses in the latter half were ~13% (Pimentel et al., 1993). Moreover, while losses did not decrease, insecticide use increased tenfold in the period ~1950–1990, although losses during this period were offset by widespread planting of high-yielding varieties and greater use of fertilizer and other inputs (Pimentel et al., 1993). A suite of problems associated with widespread and heavy pesticide use are now well known and have been discussed at length elsewhere (e.g. Perkins, 1982; Regev, 1984; Repetto, 1985; McConnell and Hruska, 1993; NRC, 1993; Bottrell and Weil, 1995; Lichtenberg and Zimmerman, 1999; Porter et al., 1999). Increasing concern over such problems is one of the principal factors driving the development of integrated pest management (IPM) strategies for many crops worldwide. A formal concept of IPM was first articulated in the late 1950s (Stern et al., 1959). This

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


06IntpestManCh6.QXD 14/4/04 2:25 pm Page 124


J.S. Bernal et al.

first conception was reductionistic in that emphasis was largely restricted to integration of chemical- and biological control tactics. Subsequent definitions expanded the concept to include the use of all available tactics in a harmonious manner so that pest populations are maintained below levels causing economic injury (FAO, 1967; Smith and van den Bosch, 1967), while others emphasized natural mortality factors, such as natural enemies, climate and crop management (Board on Agriculture, 1989). The discussion presented in this chapter is based on a concept of IPM in which biological control and plant resistance are fundamental components. The goal of IPM remains unchanged: maintain pest populations below levels at which they cause economic injury, while maintaining productive, societal and environmental impacts at acceptable levels. Moreover, the IPM concept adhered to herein includes an agroecosystem-level focus. The different crops within an agroecosystem share pest and natural-enemy populations, so pest-management tactics implemented within one crop are likely to have impacts across crops and across seasons. Thus, regional crop management (i.e. distribution in space and time) is also an important component of IPM. Crop-specific IPM strategies should take into account the potential impacts of production practices, including pest-management practices, on pest and natural-enemy populations of neighbouring and subsequent crops, as well as effects of prior crops. IPM with an agroecosystem-level focus is similar to area-wide pest management (Chandler and Faust, 1998) in that pests are managed across large geographical areas, the boundaries of which are defined by pestcolonization and dispersal capabilities. However, the strategies differ in that areawide pest management typically focuses on single or a few key pests, such as pink bollworm, Pectinophora gossypiella (Saunders), in California, codling moth, Cydia pomonella (Linnaeus) in north-western USA and maize rootworms, Diabrotica spp., in various US states. It frequently relies on single or a few management tactics (e.g. baculovirus sprays against Helicoverpa and Heliothis and

malathion sprays against boll-weevil, Anthonomus grandis grandis Boheman, in southern US cotton), and infrequently takes into account natural-enemy populations. Insecticidal transgenic cultivars, as a form of plant resistance, are attractive novel tactics and may play central roles in IPM strategies. A number of reasons make transgenic cultivars attractive tactical components of IPM strategies, particularly in relation to the use of insecticides: (i) plants are protected throughout the growing season; (ii) pests are treated at their most susceptible stage; (iii) protection is independent of weather; (iv) pests protected from natural enemies and insecticides by living within plant tissues are exposed to the insecticidal effect of plants; (v) only insects feeding on the crop are directly affected; (vi) the insecticidal factor is confined to plant tissues and therefore does not leach into the environment; and (vii) the insecticidal factor is biodegradable and therefore does not accumulate in the environment (Gatehouse et al., 1991). However, several of these advantages may also be disadvantages. For instance, pest-management decisions are made prior to planting and thus without knowledge of subsequent pestpopulation levels. Subeconomic pest populations are targeted along with economic populations. Such preemptive management tactics may have a significant impact on the sustainability of transgenic cultivars, a situation aggravated by extensive and continuous planting. Additional significant impacts are likely if the resistance factor of a transgenic cultivar is also an important and valuable insecticide, as in the case of Bt. Other important and likely impacts concern non-target, secondary pests of transgenic crops. Typically, populations of secondary-pest species are maintained below economic levels by the action of natural-enemy populations. It is conceivable that transgenic crop plants might impair natural enemies of secondary pests to the extent that biological control is relaxed and these pests become economically important. Commercially available transgenic crop cultivars, such as Bt-expressing cotton, maize and potatoes, are now widely grown in the USA and to a lesser extent worldwide.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 125

Transgenic Insecticidal Cultivars

Recent reports indicate that areas planted in the USA exceed 7.0 million ha for maize, 1.4 million ha for cotton and 20 thousand ha for potatoes and that they are likely to increase in each case (Gianessi and Carpenter, 1999; NRC, 2000). Worldwide, the total area probably exceeds 35 million ha for these crops (ISAAA, 2002). Moreover, novel transgenic cultivars are being developed for numerous crops worldwide and evaluated for introduction in the near term into many countries (McLaren, 2000). The evident widespread planting of transgenic cultivars and projections for greater areas, particularly in the USA, indicate that these cultivars are quickly becoming mainstream IPM tactics. Thus, it is imperative that the compatibility of transgenic cultivars with biological control and regional crop management, both fundamental tactics of IPM strategies, is evaluated. The goals of this chapter are to identify challenges and opportunities pertinent to widescale adoption of transgenic crop cultivars as an IPM tactic and to suggest lines of research that it is critical to address prior to widespread acceptance. Emphasis is placed upon likely interactions of transgenic crop cultivars with biological control and impacts on pest population levels at the agroecosystem level.

Types of Transgenic Plants Currently Available or Being Developed for Pest Management Development of insect-resistant transgenic crop cultivars has thus far focused on two distinct approaches: (i) integration of bacterial genes encoding for production of toxic proteins, especially from Bt; and (ii) integration of plant genes encoding for production of enzyme inhibitors and sugar-binding lectins. Both approaches were pioneered in the mid-1980s and thus have developed in parallel (Hilder et al., 1987; Vaeck et al., 1987). However, the first approach, based in particular on integration of δ-endotoxin genes derived from various subspecies of Bt, has undoubtedly received more attention and thus enjoyed greater progress. To date, all commercially available insect-resistant trans-


genic cultivars express semi-active Bt toxins, whereas cultivars expressing insecticidal plant proteins are not currently available outside of research laboratories.

Cultivars expressing Bacillus thuringiensis endotoxin genes Bt is a ubiquitous soil bacterium that was first isolated and described in the early 1900s (Federici, 1999). Commercial products based on Bt toxins and consisting of sporulated, lysed cells of fermented isolates have been used for many years (Dulmage, 1981; Federici, 1999). The insecticidal activity of Bt depends on intracellular, insecticidal crystal proteins produced by the bacterium during sporulation, which accumulate as parasporal bodies adjacent to spores. The mode of action depends on a complex process, in which, following ingestion by susceptible insects, parasporal bodies are solubilized in the alkaline environment (pH 8–10) of the midgut, thereby releasing large protoxin molecules (130–140 kDa), which are then reduced through proteolytic cleavage to smaller (~55–70 kDa), active toxins (Gill et al., 1992; Cannon, 1996; Schnepf et al., 1998). Activated toxins paralyse and kill insects by destroying the mid-gut epithelium through lysis of epithelial cells, which allows movement of gut contents into haemolymph, leading to an increase in haemolymph pH (Gill et al., 1992; Cannon, 1996; Schnepf et al., 1998; Federici, 1999). Transgenic crop cultivars express semiactivated Bt toxins (~69 kDa); thus, toxic activity does not require solubilization in the insect mid-gut and requires relatively little protoxin-to-toxin conversion (Perlak et al., 1990; Koziel et al., 1993). The abridged mode of action of Bt expressed in transgenic crop cultivars has significant implications for the selectivity of these cultivars because both solubilization and protoxin–toxin conversion are important for the specificity of Bt activity (Visser et al., 1993; Cannon, 1996). For example, it is feasible that insects unable to solubilize parasporal bodies may have appropriate receptors in the mid-gut epithelium for semiactive Bt toxins expressed in transgenic plants (Hilbeck et al., 2000).

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 126


J.S. Bernal et al.

Cultivars expressing plant-derived enzyme inhibitors and lectins Transgenic crop cultivars expressing plant genes are a valuable alternative to cultivars expressing Bt toxins. One significant advantage of using plant genes as a source of crop resistance is their broad spectrum of activity across several orders, including sap-sucking insect pests, such as hom*optera (Gatehouse and Gatehouse, 1998). Indeed, plant genes expressing chemical products responsible for plant resistance to insects are probably available against all pest species because they presumably evolved in response to herbivory by insects. Thus far, a number of economically important crop plants, such as tobacco, potato, tomato, rice, sugarcane, oilseed rape, among others, have been genetically transformed to express various genes of plant origin (Gatehouse and Gatehouse, 1998; Legaspi et al., 2004). In many of these cases, significant effects of the plant genes were evident on target-pest mortality rates and/or developmental and reproductive parameters (Gatehouse and Gatehouse, 1998; Legaspi et al., 2004). Numerous plant chemical defensive compounds have been identified to date, and these compounds are the bases for developing transgenic cultivars expressing plant genes. The number of compounds identified to date potentially provides an unending array of opportunities for developing transgenic crop cultivars effective against virtually any pest species. However, many plant defensive compounds are products involving multiple enzyme pathways and genes, and hence transfer and expression of these products in crop plants is beyond current capabilities (Gatehouse and Gatehouse, 1998). None the less, a number of defensive compounds are protein products of single genes and these have been transferred successfully to various crops. Largely, plant transformation involving plant genes has focused on: (i) protease inhibitors; (ii) α-amylase inhibitors; and (iii) lectins (Gatehouse and Gatehouse, 1998). The varied modes of action and levels of specificity of these gene products increase the potential target-pest range of transgenic cultivars and

allow the possibility of combining (pyramiding) genes that are active at various target sites within a pest insect or against various pests. However, levels of protection provided by genes of plant origin are typically lower than those provided by genes expressing Bt toxins. Frequently, effects on target insects are sublethal, including reductions in feeding, weight gain, developmental rates and fecundity (Gatehouse and Gatehouse, 1998; Legaspi et al., 2004). Yet transgenic cultivars with sublethal or chronic effects on target pests may be more attractive components of IPM strategies than cultivars with acute toxic effects because they are more likely to be compatible or act synergistically with biological control, as discussed below.

Role of Transgenic Plants in Pest Management Insect resistance via transgenes is a form of plant resistance against insect pests. However, unlike insect-resistant cultivars developed via conventional breeding methods, commercially available transgenic cultivars, all of which express Bt toxins: (i) are acutely toxic against their target pests; and (ii) were developed largely by private enterprises and remain within the commercial realm. The acute toxicity of commercially available transgenic cultivars has two significant implications for IPM. First, these cultivars exert strong selection pressures on target-pest populations, which consequently are expected to rapidly evolve resistance in the absence of effective resistance management strategies. Secondly, the acute toxicity of transgenic cultivars in many cases translates into significant indirect effects on upper-trophic-level consumers, such as natural enemies, and such effects will probably affect naturally occurring biological control. Both implications are further discussed below. Private development of commercial transgenic cultivars has meant that publicly supported IPM researchers are largely excluded from evaluating these cultivars prior to their widespread deployment. At present, participation in research on transgenic cultivars by IPM researchers remains largely restricted to eval-

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 127

Transgenic Insecticidal Cultivars

uating their effectiveness against target pests and developing resistance management strategies intended to delay the evolution of resistant pest populations. The top-down manner in which commercially available transgenic cultivars were deployed and their rapid adoption by farmers left IPM researchers with little time to adequately integrate these cultivars into existing pestmanagement strategies. Thus, transgenic cultivars are rapidly becoming stand-alone control tactics against their target pests. Many of the potential ecological and environmental problems that have been identified to date associated with transgenic cultivars, and which remain to be addressed, are a direct result of the top-down and rapid deployment of these cultivars. Moreover, because transgenic cultivars thus far have been entirely appropriated by private industry, external costs such as potentially negative environmental and pest-management impacts, will probably tend to be neglected. A number of these problems are discussed below. Crop-plant resistance against insects involves either physical (e.g. pubescence) or chemical (e.g. DIMBOA) defences. In general, transgenic cultivars rely on chemically based antibiosis as their plant resistance mechanism. Resistant plants expressing antibiosis produce significant negative physiological effects (e.g. slow development, reduced growth and fertility, death of young individuals, etc.) on susceptible herbivores feeding on their tissues. ‘Apparency theory’ (Feeny, 1976; Rhoades and Cates, 1976) provides a useful framework for discussing plant resistance to insects and the types of transgenic cultivars that may be most useful in agriculture. Chemical defences involved in antibiosis can be broadly categorized as toxins (qualitative defences) or digestibility reducers (quantitative defences), and apparency theory predicts that plants should rely on either type of chemical defence, depending on the probability of herbivore colonization (Feeny, 1976; Rhoades and Cates, 1976). Apparent plants, such as crop species, will predictably be colonized by large numbers of insect herbivores over evolutionary time and, because insects reproduce at a greater rate than plants, reliance on


toxins for chemical defence will rapidly lead to the evolution of resistant herbivore populations. Thus, apparency theory predicts that apparent plants will rely on digestibility reducers for chemical defence. In contrast, unapparent or rare plants will be colonized by fewer insect herbivores, will not support high and continuous insect populations and will thus exert relatively low selection pressure on herbivore populations. These plants are predicted to rely on toxins for chemical defence. However, all commercially available transgenic cultivars express toxins and are acutely toxic to target pest species. The prediction of apparency theory is clear in this case, and current widespread and deep concern over the sustainability of commercial transgenic cultivars due to the evolution of resistance in pest populations points to its high likelihood. In short, the strategy of developing transgenic cultivars that express toxins is not evolutionarily sustainable. Because crop species are akin to apparent plants, one evolutionarily sustainable approach is to develop crop cultivars that rely on digestibility reducers (e.g. plant-derived enzyme inhibitors and lectins). Moreover, digestibility reducers are more likely than toxins to be compatible with biological control (see below). If a long-term objective of developing IPM strategies for specific crops is to rely more on biological control and plant resistance and less on non-biological alternatives, then emphasis should be placed on developing transgenic cultivars that act synergistically or at least additively with biological control. This requires greater interaction during cultivar development between plant breeders and biological control researchers than currently occurs. One promising approach is to develop antibiosis-expressing transgenic cultivars that reduce yield losses while rendering pests more susceptible to parasitism and predation by natural enemies. For example, plant resistance via digestibility reducers that decrease the amount of feeding and prolong the developmental period of pests may act synergistically with biological control by increasing the length of time during which pests are susceptible to parasitism and predation. Examples are documented in which longer developmental times in herbivores led to increased para-

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 128


J.S. Bernal et al.

sitism or predation rates and more effective biological control (Price et al., 1980; Haggstrom and Larsson, 1995; Luck et al., 1995; Benrey and Denno, 1997; Devine et al., 2000). Moreover, existing cultivars that are known to produce alternative foods (e.g. floral nectar, extrafloral nectar, pollen) at high levels or of high quality or that support (and tolerate) substantial populations of alternative hosts or prey may be targeted for transformation to express digestibility reducers active against target pests. Numerous studies have demonstrated the importance of the availability of alternative food sources or hosts/prey in maintaining natural-enemy populations at levels that effect biological control of target pests (Hagen, 1986; Jervis et al., 1993; Bottrell et al., 1998; Ferro and McNiel, 1998; Thompson and Hagen, 1999). An alternative approach is to develop transgenic cultivars that rely on antixenosis as a resistance mechanism. Resistant plants expressing antixenosis are refractory to colonizing herbivores and hence frequently lead to increased levels of activity and movement of susceptible herbivores on and between plants. Examples are documented in which greater herbivore movement led to greater parasitism rates, and such increments may lead to improved biological control (Pair et al., 1986; Annis and O’Keefe, 1987). Other plant traits not directly targeted against insect pests but that may interact positively with biological control if transferred to crop cultivars are discussed by Hoy et al. (1998). Some examples include improved tolerance to diseases, which would raise the threshold level for insect vectors, and altered plant architecture and leaf surfaces, which may affect the exposure of pests to natural enemies. The development and deployment of transgenic cultivars should be pursued within a context of ecological, evolutionary and economic considerations. Ideally, transgenic cultivars should be developed as tactical components of IPM strategies and their compatibility with biological control tactics should be considered a priority during development. The ecological goal should be to promote a transition to true ecologically based pest management, which maintains populations of potential pests at low levels, and in so doing, obviates the need to apply

remedial control measures, such as insecticide applications. The evolutionary goal should be to deploy transgenic cultivars that will not rapidly select for resistant pest populations and consequently will be sustainable in the medium to long term with nil or minimal intervention. The economic goal should be to deploy transgenic cultivars that do not significantly add to production costs and therefore have a cost : benefit ratio that is largely independent of market and yield fluctuations. Transgenic cultivars should be a viable alternative for farmers in marginal as well as high-yielding areas. In sum, a longterm goal of developing transgenic cultivars should be to facilitate transition to ecologically based IPM strategies for major crops worldwide, while maintaining the economic and evolutionary sustainability of the cultivars. However, the context in which commercial transgenic cultivars are developed and deployed may not be compatible with such a goal. It remains to be seen whether future development of transgenic cultivars will be dictated by market opportunities and technological limitations (e.g. single-gene transformations), rather than the needs of farmers and interest in the long-term sustainability of agricultural production. Developing and deploying transgenic cultivars simply because the necessary technology is now available is not justifiable if a long-term goal of IPM research is to develop strategies that contribute to agricultural sustainability. Farmers’ needs should be considered prior to transgenic-cultivar development, and the likely ecological, environmental and socio-economic impacts closely examined to the extent that current science allows so that scientifically informed decisions supersede those based on commercial interests.

Challenges and Opportunities in Deploying Transgenic Cultivars as Tactical Components of IPM Systems Interactions of transgenic crop cultivars with IPM tactics As discussed in this chapter, IPM has its foundations in biological control and plant

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 129

Transgenic Insecticidal Cultivars

resistance, and benefits from regional crop management that has an impact on levels of pest and natural-enemy populations within crops. Because transgenic crop cultivars are a form of plant resistance, it is likely that they will increasingly occupy central roles within IPM strategies, a trend that is rapidly becoming evident in the case of Bt-transgenic cultivars in the USA. In consequence, it is important that potential impacts, whether positive or negative, of transgenic crop cultivars on herbivore (including non-target species) and natural-enemy populations at the agroecosystem level are identified and measured. The levels of pest populations found in crops are influenced by movement of pestand natural-enemy populations between crops and seasons within agroecosystems. Thus, pest levels and biological control are likely to be affected by deployment of transgenic crop cultivars, particularly if these cultivars affect a wide range of herbivores and are widely planted within agroecosystems. Thus far, a number of studies have documented the occurrence of significant negative effects of transgenic cultivars on non-target insects, while others have shown negligible, non-existent, or positive effects (Bell et al., 1999; Birch et al., 1999; Losey et al., 1999; Schuler et al., 1999; Hilbeck et al., 2000; Jesse and Obrycki, 2000; Wraight et al., 2000; Sétamou et al., 2002a,c). The magnitude and direction of potential effects of transgenic crops on IPM strategies will depend on the degree to which herbivore and naturalenemy populations are affected. Transgenic cultivars that have sublethal effects on herbivores and natural enemies will have a different impact on their populations from that of cultivars that have lethal effects. At the same time, transgenic cultivars that have negligible effects on natural enemies will probably have positive impacts on IPM strategies. Because transgenic crop cultivars are a form of plant resistance, a tactic that occupies a central role in modern IPM strategies, they will interact with other cornerstone IPM tactics. Frequently, IPM strategies rely on biological control and are affected by regional crop management. Thus, biological control and transient populations of natural


enemies and herbivores are likely to be most affected by widespread deployment of transgenic crops. Such impacts may be negative, and thus pose challenges to be redressed, or positive, and thus offer opportunities to be exploited. Redressing any challenges and taking advantage of any opportunities are crucial if transgenic cultivars are to be adequately integrated into IPM strategies.

Biological control Natural enemies important in biological control include parasitoids, predators, and pathogens. Of these, parasitoids are perhaps the most important as they are responsible for most documented examples of biological control. For example, c. three-quarters of 1193 species of predators and parasitoids included in a world review of biological control programmes were parasitoids (Gordh et al., 1999). Predators are widely recognized as important mortality factors, particularly in ephemeral crops (Kogan et al., 1999), even if their impact on pest populations is frequently unappreciated or underestimated. Moreover, the importance of predation for pest management is well established in several crops for which transgenic cultivars are commercially available (e.g. cotton: Hagen et al., 1976; González and Wilson, 1982). Pathogens are not widely relied upon for insect-pest management, although in many cases they are believed to be important short-term regulators of insect populations (Federici, 1999). Indeed, only one pathogen, Bt, is widely used for pest management. Thus, the discussion that follows focuses largely on likely and known impacts of transgenic cultivars on parasitoids and biological control by natural enemies other than pathogens. Parasitoids, mostly in the order Hymenoptera, have larvae that typically consume and kill single hosts, while adults are free-living or only secondarily carnivorous, feeding on host-derived haemolymph. The biology of parasitoid larvae and their relationships with hosts have two important implications for the suite of potential impacts of transgenic cultivars on biological

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 130


J.S. Bernal et al.

control. First, parasitoid larvae are typically unable to search for a new host if the available host is unsuitable. Secondly, parasitoids are frequently capable of exploiting only a small number of closely related species as hosts. Thus, it is likely that, if a transgenic cultivar affects a parasitoid’s main host, all alternative host species will be similarly affected. In consequence, parasitoid females searching for hosts within a transgenic crop are likely to encounter only hosts that are susceptible to the transgenic cultivar, and their offspring are restricted to developing on these hosts. The likely effects of transgenic crop cultivars on parasitoids are summarized in Fig. 6.1. The potential effects of transgenic cultivars on parasitoids are divided into individual- and populationlevel effects. At the individual level, the likely effects are further divided into those affecting parasitoid larvae and adults. At the population level, the likely effects are those relating to impacts on biological control as a population-level process. Specifically, the effects are divided into negative (e.g. impacts of wide-scale depletion of host populations), synergistic (e.g. greater parasitism levels due to weakened host immune responses) and additive effects (e.g. parasitism of individuals surviving the effects of transgenic plants). Each of these likely effects of transgenic cultivars on parasitoids and biological control by parasitoids is briefly discussed below. Individual-level effects The most direct and obvious effect of transgenic crop cultivars on parasitoid larvae occurs in hosts susceptible to the transgenic cultivar and is the result of the acute toxicity of the cultivar to the host (Fig. 6.2). In this case, parasitoid eggs or larvae are unable to complete their development due to premature death of their host. Such effects on parasitoids are likely to be less important in transgenic cultivars that are not acutely toxic to the targeted pests such as cultivars expressing enzyme inhibitors and lectins or toxins at low doses. The effects on parasitoid larvae via hosts tolerant of the transgenic cultivar are less obvious and can be either direct or indirect

Individuals Potential effects on parasitoids

Populations – biological control





Additive Fig. 6.1. Levels at which transgenic insecticidal crop cultivars may have an impact on parasitoids and some likely directions of impacts.

(Fig. 6.2). For example a direct positive effect on parasitoid larvae was evident in a recent study in which it was suggested that the immune-defence reactions of hosts were compromised by feeding on artificial diet containing 2% of the lectin Galanthus nivalis agglutinin (GNA) (Bell et al., 1999; Fig. 6.2). Broods of the gregarious parasitoid Eulophus pennicornis (Nees) developing on tomato moth larvae, Lacanobia oleracea (Linnaeus) fed an artificial diet containing 2% GNA were more than twice as large (21 adult parasitoids per host) as broods developing on hosts fed a diet without GNA (nine adult parasitoids per host) (Bell et al., 1999). However, a similar effect was not evident when hosts were fed transgenic potato leaves expressing GNA at 0.8%. In contrast, direct negative impacts on parasitoid larvae are evident in studies showing decreased survival of parasitoids developing on hosts feeding on transgenic plant tissues due to exposure to toxins (Fig. 6.2). For example, a recent study showed that egg–adult survivorship was c. 90% in parasitoids developing on hosts fed non-transgenic maize tissue, while it was c. 40% in those whose hosts were intoxicated after feeding on transgenic maize tissue (Bernal et al., 2002). Similar effects on survivorship are evident in predators fed prey intoxicated after feeding on transgenic maize tissue versus those fed healthy prey (Hilbeck et al., 1998). Indirect effects of transgenic cultivars on parasitoid larvae are probably common as

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 131

Transgenic Insecticidal Cultivars

Susceptible host


Parasitoid death/ failure to develop Positive

Impaired immune response


Exposure to toxin

Larvae Direct

Tolerant host


Altered host quality

Fig. 6.2. Likely impacts of transgene products on parasitoid larvae developing on/in hosts feeding on transgenic insecticidal crop cultivars.

they derive from effects on a herbivore’s quality as a host. For instance, both target and non-target pests of transgenic cultivars are frequently sublethally affected by these cultivars, and negative effects, such as lower weight and nutritional quality, will probably affect developing parasitoid larvae (Fig. 6.2). A number of studies have shown that hosts fed transgenic plant tissue weighed less than hosts fed non-transgenic plant tissue, and that these differences in weight resulted in smaller, less fit parasitoids, smaller parasitoid broods and a lower ratio of female offspring (Adamczyk et al., 1998; Lynch et al., 1999; Couty et al., 2001; Sétamou et al., 2002a,b). In contrast, differences in susceptibility between target and non-target pests of transgenic cultivars may result in indirect positive effects such as improved quality as a host in the latter pests (Fig. 6.2). For example, non-target pests may have greater tolerance than target pests, and may benefit (e.g. increased weight gain) from feeding on transgenic cultivars that express low levels of insecticidal proteins or toxins (De Leo et al., 1998; Sétamou et al., 2002b). Any benefits for parasitoid larvae of feeding on improved-quality hosts, however, will depend on their susceptibility to insecticidal proteins, which may accumulate in their host’s gut and haemolymph (Fitches and Gatehouse, 1998; Bell et al., 1999). Transgenic cultivars may affect parasitoid adults via effects on larvae that develop on tolerant hosts, as discussed above (Fig. 6.2).

The effects on parasitoid adults will thus be determined by the susceptibility of the developing larvae to the transgenic cultivar as mediated by the host, or the effects on larvae of developing on hosts of altered quality. In addition, transgenic cultivars may affect parasitoid adults independently of effects on their larvae by interfering with different components of the host-finding process, and these effects may be mediated by the transgenic cultivar itself or by hosts feeding on transgenic plants (Fig. 6.3). For example, plants are known to emit volatiles that attract natural enemies, particularly when they are under attack by herbivores (Turlings and Benrey, 1998; Venzon et al., 1999; Pels and Sabelis, 2000). It is conceivable that volatiles emitted by transgenic cultivars are qualitatively different from those emitted by non-transgenic cultivars. One recent study failed to find differences between herbivore-damaged transgenic and non-transgenic oil-seed rape plants in their attractiveness to the parasitoid Cotesia plutellae (Kurdyumov) (Schuler et al., 1999). However, the results of another study showed that when given a choice, sugarcane borer, Diatraea saccharalis (Fabricius), and Mexican rice borer, Eoreuma loftini (Dyar), adults prefer non-transgenic over transgenic GNA-expressing sugarcane for oviposition, suggesting that differences exist between the sugarcane cultivars in their attractiveness to these herbivores (Bernal and Sétamou, 2003). It is conceivable that these differences may also extend to adult parasitoids searching for

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 132


J.S. Bernal et al.


Interfere with host habitat location, synomone production and threshold, alternative food sources Kairomones

e.g. faeces, honeydew


e.g. elicitors




Less defence, more movement, less noise

Fig. 6.3. Likely impacts of transgenic insecticidal crop cultivars on parasitoid adults as mediated by the transgenic plant or by hosts feeding on transgenic plants.

sugarcane borer or Mexican rice borer hosts infesting sugarcane plants. In addition to direct effects, transgenic cultivars may also affect parasitoid adults indirectly via their hosts (Fig. 6.3). Currently, all transgenic cultivars are active on their target pest’s gut or digestive processes. Parasitoids in general are known to rely on chemical cues (kairomones) from their hosts (e.g. pheromones) or host products (e.g. frass, honeydew) during the host-searching process. It is conceivable that chemical cues emanating from host products, such as frass or honeydew, may be altered in herbivores feeding on transgenic cultivars. For example, females of the parasitoid Cotesia marginiventris (Cresson) were more attracted to frass of fall armyworm, Spodoptera frugiperda (J.E. Smith) that had fed on non-transgenic versus transgenic maize tissue (Bernal et al., unpublished data). Also, the lectin GNA was found in similar to higher concentrations in the honeydew relative to the diet of rice brown planthopper, Nilaparvata lugens (Stal) between 24 and 72 h after feeding on a GNA diet (Powell et al., 1998). Similarly, production of herbivore-induced chemical cues (synomones) by plants is dependent on elicitors from herbivores, and these elicitors are associated with herbivore feeding (Turlings and Benrey, 1998). It is plausible that the chemical composition of these elicitors is altered in herbivores feeding on transgenic cultivars. However, few data are currently available that address potential differences

in herbivore chemical cues, products or elicitors between herbivores feeding on transgenic versus non-transgenic cultivars, or in the attractiveness of these cultivars to parasitoids searching for hosts. In contrast, available data suggest that transgenic cultivars may affect parasitoid adults via alterations in the behaviour of their hosts (Fig. 6.3). The positive effect of increased herbivore movement on parasitism rates (Pair et al., 1986; Annis and O’Keefe, 1987) was discussed above, and it is likely that pests intoxicated or weakened after feeding on transgenic cultivars may be less able to defend themselves against natural-enemy attack. Some studies show that host aggression against parasitoid adults can result in high levels of parasitoid mortality during host handling (Potting et al., 1999). In contrast, natural enemies that rely on airborne or substrate-borne vibratory or visual cues for locating hosts or prey may be less successful if hosts/prey show decreased activity levels when feeding on transgenic cultivars. For example, Mexican rice borer, a stem-boring pest, is less active and produces less noise inside artificial tunnels and consequently is parasitized less frequently when feeding on diet containing GNA versus diet free of GNA (Tomov et al., 2003). Population-level effects Finally, transgenic cultivars may affect parasitoids at the population level, and conse-

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 133

Transgenic Insecticidal Cultivars

quently may have an impact on the degrees of biological control they achieve (Fig. 6.4). The effects at the population level may be evident at the agroecosystem level if transgenic cultivars eliminate host populations to the extent that parasitoid populations are unable to persist locally (negative direct) or suffer in terms of their quality (negative indirect), or they will be extensions of effects on parasitoid larvae and adults at the individual level, as discussed above (synergistic or additive) (Fig. 6.4). Agroecosystem-level effects on natural-enemy populations and biological control are further discussed below. Synergistic effects of transgenic cultivars on biological control will arise when pest mortality due to plant resistance and natural enemies within transgenic fields is greater than the expected sum of the mortality from both these factors. However, synergism with biological control is more likely in transgenic cultivars that are sublethal to the targeted pest. For example, greater than expected parasitism of tobacco budworm, Heliothis virescens (Fabricius), by the parasitoid Campoletis sonorensis (Cameron) was evident in transgenic tobacco expressing a low level of Bt endotoxin relative to non-transgenic tobacco (Johnson and Gould, 1992). In this case, the greater parasitism was attributed to longer developmental times for tobacco budworm larvae and the ensuing longer window of opportunity for parasitism, which should be increasingly important where natural ene-


mies are able to exploit only a narrow range of host/prey instars or sizes. Comparable differences in parasitism rates, albeit not significant, were reported in a study involving tobacco budworm, maize earworm, Helicoverpa zea (Boddie), and transgenic tobacco (Warren et al., 1992). Similar synergistic interactions are plausible if transgenic cultivars have other sublethal effects, such as weakening a host’s immune system or impairing its ability to defend itself from parasitoids, as discussed above. A significant interaction may be lacking between transgenic cultivars and biological control in the field, with any effects merely being additive (Fig. 6.4). Additivity between transgenic cultivars and biological control through parasitism or predation of pest individuals surviving after feeding on transgenic plants has significant implications for the evolution of resistance in pest populations to transgenic cultivars, because surviving individuals are likely to be genetically resistant to the antibiotic effects of these cultivars. For example, genetic models show that natural enemies may double to quadruple the numbers of generations necessary for the evolution of resistance to transgenic cultivars in pest populations (Johnson and Gould, 1992; Arpaia et al., 1997). However, more comprehensive models indicate that natural enemies may increase, decrease or not affect the rate of resistance evolution in pest populations (Gould et al., 1991).


Depletion of host populations


Reduction of quality in host population


Populations – biological control Synergistic

Extended ‘window’, weak immune system and defensive reactions


Parasitism of surviving individuals

Fig. 6.4. Likely impacts of transgenic insecticidal crop cultivars, and their direction, on parasitoid populations and biological control.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 134


J.S. Bernal et al.

Other important interactions between transgenic cultivars and biological control are likely to occur via secondary pests, which typically are not targeted during transgenic cultivar development. In this case, the most obvious effects will derive from two likely effects of transgenic cultivars. First, secondary pests may be sublethally affected by transgenic cultivars due to greater tolerance of the insecticidal toxins or proteins expressed by these cultivars relative to target (primary) pests. In this case, the expected effects would be similar to those discussed above for sublethally affected primary (i.e. target) pests, as well as the agroecosystemlevel effects discussed below. Secondly, a positive interaction between transgenic cultivars and biological control may occur if deployment of these cultivars results in reduced usage of broad-spectrum insecticides against primary pests, which may lead to improved biological control of secondary pests through conservation of natural enemies. A number of examples in which Bt-transgenic potato cultivars support greater and more diverse natural-enemy communities are discussed by Hoy et al. (1998). However, it will be important that applications of broad-spectrum insecticides are indeed reduced if transgenic cultivars are to enhance conservation biological control of secondary pests. Currently, some studies indicate that lesser amounts of insecticides are applied in transgenic crops, such as Bt maize and cotton, whereas others fail to find significant reductions in the use of broadspectrum insecticides (Fernández-Cornejo and McBride, 2000).

Effects on agroecosystems Beyond effects on individuals and populations lies the issue of how deployment of transgenic cultivars may alter the agroecosystem outside single transgenic field boundaries. Both contemporaneous and sequential crops affect neighbouring fields, in part because the arthropod faunas of annual crops are often produced by immigration from nearby crops (Kieckhefer and Miller, 1967; Poston and Pedigo, 1975; Ives,

1981; Honêk, 1982; Vorley and Wratten, 1987; Brazzle et al., 1997; Kennedy and Storer, 2000). Indeed, interconnections of both pest and natural-enemy populations in common transgenic crops to other crops in regional production systems are well established. Common pests of agroecosystems in North Carolina are unquestionably linked. The European corn borer, Ostrinia nubilalis (Hübner), colonizes potatoes and wheat (Anderson et al., 1984; Umeozor et al., 1986; Jones, 1994) before infesting maize and cotton (Savinelli et al., 1986, 1988; Umeozor et al., 1986). Maize earworm, H. zea, populations initially develop in maize and later colonize cotton and soybean crops in the area (Neunzig, 1963, 1969), while two-spotted spider mites, Tetranychus urticae (Koch), from maize become pests in nearby groundnuts (Brandenburg and Kennedy, 1982; Margolies and Kennedy, 1985). A similar relationship exists for natural enemies in Texas cropping systems. Parasitoids such as Trichogramma pretiosum Riley, C. sonorensis (Cameron) and Microplitis croceipes (Cresson) all parasitize maize earworm or tobacco budworm, H. virescens in several crops, including lucerne, maize and potatoes early in the season and lucerne, maize, cotton and grain sorghum later in the season (Puterka et al., 1985). Predators, including spiders, convergent lady bird, Hippodamia convergens Guérin-Méneville, and minute pirate bugs, Orius tristicolor (White) and Orius insidiosis (Say), move between cotton and grain sorghum throughout their coincident cultivation, apparently responding to local prey abundances (Prasifka et al., 1999). Maize and grain sorghum also appear to provide the H. convergens colonists that later reproduce and sustain ladybird populations in cotton (J. Prasifka and K.M. Heinz, unpublished data). Many other examples support the assertion that pest and natural-enemy populations interact across landscapes and seasons, suggesting that interactions between transgenic and non-transgenic crops are likely. However, because current research on the effects of transgenic cultivars is performed on a much smaller scale, agroecosystem effects must be predicted on the bases of lim-

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 135

Transgenic Insecticidal Cultivars

ited studies, whose results vary widely (see previous section). In the absence of a clear indication of what can be expected at the individual-field level, possible detrimental and beneficial impacts from the spread of transgenic insecticidal cultivars are considered in turn. Challenges to IPM in agroecosystems Transgenic cultivars are typically highly effective against target pests, suggesting that natural-enemy populations using these pests as prey or hosts will also suffer great numerical declines. The results of this across agroecosystems (space and time) could have at least three unwelcome effects, including: (i) target-pest resurgences or secondary-pest outbreaks in non-transgenic cultivars when large areas of transgenic cultivars are concurrently grown; (ii) pest epidemics in other non-transgenic crops; and (iii) chronic secondary-pest outbreaks in transgenic crops through effects on natural-enemy and pest populations. The potential for pest problems in nontransgenic fields of the same crop is based on the connectivity between fields. Typically, extensive plantings of one annual crop harbour small, non-independent components of mobile pest and natural-enemy metapopulations (Settle et al., 1996; Kennedy and Storer, 2000). Insecticide treatments in one area may decimate natural enemies there, but mobile predators and parasitoids can repopulate treated fields from nearby untreated ones (Wratten and Thomas, 1990). In contrast, transgenic fields in which high pest and natural-enemy mortality occurs represent sinks from which little or no recolonization can be expected. Because of the cost:benefit guessing game that can be required to plant transgenic cultivars (Rice and Pilcher, 1998), some non-transgenic fields will be planted in addition to required refuge plantings. If insecticides are applied to non-transgenic fields, insufficient natural enemies may recolonize these fields, causing pest populations to significantly increase. Pest epidemics in other crops might also result from reduced abundance or diversity of natural enemies in transgenic fields. If low


levels of both pests and natural enemies exist within transgenic fields, the natural process of arthropod colonization of nearby crops will be disrupted and natural biological control compromised. For example, pests may colonize from a weedy host, and a transgenic crop that traditionally supplied natural enemies will probably fail to control the pest, requiring remedial insecticide treatments. Even if the natural-enemy-to-pest ratio remains the same, reduced abundance of colonists favours pests. Herbivorous pests colonize crops in advance of the arrival of natural enemies (Price, 1976), allowing them to exploit abundant resources unchecked. Predators and parasitoids arrive later and ideally halt the exponential growth of pest populations, but they typically operate as density-dependant mortality factors. This argument overlooks the most obvious problem, that some pests will be unaffected by transgenic insecticidal cultivars, while key natural-enemy numbers are reduced. If the effects of transgenic insecticidal cultivars commonly include those proposed above, then by extension, there will probably be problems throughout the agroecosystem, including chronic secondary pest problems in the transgenic cultivars themselves. Predator and parasitoid populations are not only linked spatially (among crops), but are related temporally (over seasons), with a cycle of natural-enemy colonization repeating annually (Wissinger, 1997). The combination of pest outbreaks and insecticide treatments outside transgenic fields and the recurrent natural-enemy sink caused by transgenic cultivars could reduce the available natural-enemy pool each year until an entirely new pest complex emerges, as has occurred in the past due to overuse of conventional insecticides. Opportunities for IPM in agroecosystems While the potential for misuse and unintended side effects of widespread plantings of transgenic crops unquestionably exists, transgenic cultivars potentially represent a tremendous advance in crop protection. In the best case, transgenic cultivars offer not only a novel tool for managing target pests,

06IntpestManCh6.QXD 5/5/04 2:08 pm Page 136


J.S. Bernal et al.

but also a chance to incorporate biological controls into IPM to an unprecedented level. Among the possible benefits to agroecosystems are: (i) a reduction of pest outbreaks through conservation of natural enemies; (ii) successful area-wide management of mobile, polyphagous crop pests; and (iii) incidental control of various susceptible, non-target pests. Apart from control of target pests, the effect most often touted by proponents of transgenic insecticidal cultivars is conservation of natural enemies. Insecticidal toxins, such as those produced by Bt-transgenic cultivars, are relatively specific and may reduce the overall need for broad-spectrum insecticide applications. With this reduction in insecticide applications, predator and parasitoid (particularly generalists and those not dependent on the target pests of transgenic cultivars) populations should increase and be better able to prevent pest outbreaks, especially of pesticide-induced secondary pests. When the natural-enemy faunas of multiple crops are intimately linked, the presence of one widely grown transgenic cultivar could have benefits across the agroecosystem by providing greater numbers of colonizing natural enemies for other crops. Transgenic cultivars also provide a unique potential to manage mobile, polyphagous pests on an area-wide basis. Extensive use of transgenic cultivars is advantageous for this application because extensive plantings can exert continuous pressure over both space and time. Areawide control of European corn borer through increased areas planted to Bt cultivars has been proposed (Rice and Pilcher, 1998), but only potential benefits to maize were considered. However, if few non-crop hosts were available, one or more transgenic crops could eliminate this and other polyphagous pests as problems in entire multiple-crop agroecosystems. In cases where non-target pest populations are also reduced by transgenic cultivars, improved control and reduced outbreaks in other susceptible crops (e.g. due to reduced maize earworm movement between maize and cotton) could also be realized. As alluded to above, the use of transgenic

crop cultivars can have unanticipated management benefits against non-target pests. Depending on the levels of toxicity against these pests, other primary or secondary pests could be reduced in status or completely eliminated. For example, Bt cotton cultivars developed against bollworm, tobacco budworm and pink bollworm also showed a larval mortality of > 85% against cabbage looper, Trichoplusia ni (Hübner), salt-marsh caterpillar, Estigmene acrea (Drury), cotton leaf perforator, Bucculatrix thurberiella Busck, and European corn borer. Minor insecticidal effects were also shown against beet armyworm and fall armyworm, with larval mortality of 20–25% (Wilson et al., 1992, 1994; Bradley, 1995; Moore et al., 1999).

Potential Role in Developing-country Agriculture Developing-country agriculture is characterized by a mosaic of production systems, ranging from high-input agriculture that seeks maximum economic returns to subsistence agriculture that seeks maximum yields with minimal variance. The former is typical of export and plantation crops (e.g. cotton, bananas, tomatoes), whereas the latter is typical of staple crops (e.g. maize, potatoes, rice). The focus of this section is on subsistence agriculture, but cotton is included because transgenic cotton cultivars are currently available and because cotton cultivation is frequently viewed as a source of foreign currency in developing countries and figures prominently in agricultural development projects (Murray, 1994). Several characteristics of subsistence agriculture should be highlighted prior to discussing the potential role of transgenic crop cultivars within pest-management strategies. First, capital available to subsistence farmers for investing in crop production in general and pest management in particular is limited. Thus, the IPM tactics most readily accessible to subsistence farmers are those that do not entail direct economic expenditures. Biological control by natural-enemy conservation and plant resistance (exclusive of commercial transgenic crops) are both free of cost

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 137

Transgenic Insecticidal Cultivars

and fundamental tactics of IPM strategies and should form the bases of IPM systems in subsistence agriculture. Secondly, subsistence agriculture is, by definition, not typically a major source of income, and subsistence farmers must engage in other activities to procure expendable income (e.g. day labour). Thus, pest-management tactics that require minimal time investments will be more appropriate than and favoured over tactics requiring greater time investments. For example, the opportunity costs associated with monitoring pest populations as a basis for insecticide applications will detract from the appeal of insecticide-based IPM strategies even when insecticides are a tenable alternative. Again, plant resistance and biological control are especially appropriate because they require minimal to nil time investments by farmers. Moreover, IPM strategies centred upon insecticidal control tactics may not be appropriate in the context of subsistence farming. Insecticide use within IPM systems is based on the concepts of economic threshold and economic injury levels. These concepts are based on the difference between the costs of intervention (i.e. insecticide application) and non-intervention (i.e. yield loss due to pests), and may not be useful in the context of subsistence agriculture because losses associated with non-intervention are typically not quantified in economic units. It is clear that plant resistance and biological control are particularly appropriate tactics for pest management in subsistence agriculture and that they should form the bases of IPM strategies in that context. Thus, transgenic cultivars have a great potential to play significant roles in developing-country agriculture. However, it will be crucial that the interactions between transgenic cultivars and biological control are closely examined prior to cultivar deployment. Specifically, breeding efforts should seek to develop cultivars that interact positively (i.e. synergistically) with biological control. This requires greater than current degrees of interaction between plant breeders and biological control researchers. Cultivars that have additive interactions with biological control should be left as second alternatives, while those with negative interactions should be


avoided prima facie. IPM systems that are proactive should be developed by seeking positive interactions between transgenic cultivars and biological control. Examples of plant resistance mechanisms likely to result in positive interactions between transgenic cultivars and biological control were discussed above. Positive interactions between transgenic cultivars and biological control will contribute to maintaining pest populations at low levels, which should minimize the need for remedial control tactics such as insecticide applications. Transgenic cultivars have the potential to generate significant benefits for developingcountry agriculture. Among the main benefits lies the potential for reducing pesticide use in cash crops, such as cotton, which are notorious for their reliance on insecticidal control of major pests. For example, reductions in the numbers of insecticide applications to cotton have been documented where Bt cotton is planted in the USA, and similar reductions can be expected in developing countries (ERSUSDA, 1999; but see Fernández-Cornejo and McBride, 2000). Moreover, transgenic cultivars may allow recultivation of crops in areas where they were discontinued due to severe pest-management problems. For example, cotton production was largely discontinued in north-eastern Mexico by 1970 and Central America by 1990 following upsets of secondary pests, including species of Heliothis, Spodoptera and Trichoplusia, and the inability to manage these pests economically based on unilateral use of insecticides (DeBach and Rosen, 1991; Murray, 1994). Bt-transgenic cotton may significantly contribute to expanding cotton production in those and other areas where lepidopteran pests are major factors limiting cotton production (e.g. Africa; Silvie et al., 2001). However, it is uncertain whether mere transfer of Bt-transgenic cultivars from developed to developing countries will lead to substantial benefits in the latter unless locally important pests are targeted and locally adapted crop varieties are transformed. Pest complexes and their susceptibility to Bt toxins, as well as desirable agronomic characters, probably differ between most regions. Transgenic cultivars expressing plant-

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 138


J.S. Bernal et al.

derived enzyme inhibitors and lectins are particularly promising alternatives to Bttransgenic cultivars in developing countries. Unlike Bt-transgenic cultivars, those expressing enzyme inhibitors and lectins are largely being developed by national and international public research institutions and universities and thus are more likely to remain outside the commercial realm. For example, numerous lectin-expressing transgenic crop lines are currently in various stages of development and evaluation (Gatehouse et al., 1991; Legaspi et al., 2004). Moreover, transgenic lines of staple crops of major importance in developing countries, such as potatoes and rice, are in various stages of development and numerous genes expressing activity against pests of these crops have been isolated and are currently being evaluated (Gatehouse et al., 1998; Shu et al., 2000; Machuka, 2001; Legaspi et al., 2004). As discussed above, transgenic cultivars expressing plant-derived genes are more likely than Bt-expressing cultivars to act synergistically with biological control, thus potentially decreasing the need for remedial control tactics, such as insecticide applications. Along with the likely benefits derived from deployment of transgenic cultivars in developing countries are potentially important disadvantages. A few are briefly discussed here in reference to commercially available Bt-expressing cultivars. One major concern associated with Bt-transgenic cultivars in countries where they are available commercially is the development of resistant pest populations (Gould, 1998), and this concern should be greater in developing countries. In the absence of adequate knowledge and regulation, transgenic cultivars could become a transitional technology, available only as long as resistance development can be postponed, which could ultimately lead to higher levels of pesticide use (Hubbell and Welsh, 1998). For instance, recent development projects in Central America emphasize the production of non-traditional export crops, such as fruits, vegetables and cut flowers (Thrupp, 1995; Nicholls and Altieri, 1997), while cotton remains an attractive and potentially important source of foreign income (Murray, 1994). Production of these

crops is heavily dependent on the use of broad-spectrum insecticides, which has led to serious environmental, ecological and human health problems (McConnell and Hruska, 1993; Murray, 1994; Thrupp, 1995; Nicholls and Altieri, 1997). A promising alternative to broad-spectrum insecticides is the use of Bt-based insecticides, which have been increasingly employed against cotton pests in Central America, starting in the 1980s (Murray, 1994). Resistance to Bt toxins could rapidly evolve if Bt-cotton cultivars are widely deployed and planted in Central America, precluding further use of Bt-based insecticides in non-traditional export crops and guaranteeing in the short term a continued heavy dependence on broad-spectrum insecticides for pest control. A number of likely obstacles must be overcome for widespread and sustainable use of transgenic cultivars in developing countries, and these are particularly important in the case of existing Bt-transgenic cultivars. One obstacle is the low adoption rate of commercial seed varieties in many developing countries. For example, the areas planted with improved hybrid maize seed in Mexico and Central America are currently below 20% of the total areas planted to maize (Morris and López-Pereira, 1999). Similarly, it remains to be seen whether resistance management programmes, based on non-transgenic refuge crops and designed for developed-country agriculture, will be appropriate for developing-country agriculture. A pervasive feature of subsistence agriculture is the relatively small size of land allocations per farmer. It is uncertain whether land-limited subsistence farmers will be willing to set aside a portion of their crop as a non-transgenic refuge susceptible to high levels of pest damage. Moreover, resistancemanagement programmes require active industry, government and farmer participation to be effective. Past failures, despite strong national and international interests, in maintaining regional IPM programmes in various crops in developing countries caution against placing too much confidence in the long-term viability of regional resistancemanagement programmes (Holl et al., 1990; Murray, 1994; Thrupp, 1995; Nicholls and

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 139

Transgenic Insecticidal Cultivars

Altieri, 1997). Finally, other potential problems associated with the deployment of transgenic cultivars in developing countries relate to the unknown consequences of potential gene flow between crops and wild relatives and within crops, and intellectualand genetic-property issues. These issues have been discussed elsewhere and are not addressed here (e.g. Shand, 1991; De Souza Silva, 1995; Bhat, 1999; Ellstrand et al., 1999; King and Eyzaguirre, 1999). Major staple crops, such as maize, rice, cowpeas and potatoes, have their centres of origin and genetic diversity in developing countries, and therefore it is essential that these issues are addressed in advance of transgenic-cultivar deployment rather than in retrospect.

Conclusions Transgenic insecticidal cultivars are a novel form of host-plant resistance and, as such, may play major roles in future IPM strategies in many crops worldwide, in both developed and developing countries. Transgenic cultivars are novel because foreign genes confer their resistance, but host-plant resistance is a long-standing and fundamental IPM tactic. They may play major roles in future IPM strategies because, unlike traditionally bred insect-resistant cultivars, they rely on genes and gene products transferred between species, which substantially broadens the opportunities for developing new transgenic cultivars. The development of new transgenic cultivars effective against specific pests appears limited only by our ability to discover and successfully transfer genes between species. As discussed above, genes conferring resistance against all major pests are probably available because insects as a group are major herbivores and plants have evolved diverse chemical defences against herbivory by insects. However, because of their tremendous promise, it is imperative that transgenic cultivars are designed to be sustainable. Transgenic cultivars should be developed within an IPM context, rather than as stand-alone technologies against target pests because of a number of potential problems, discussed above. Specifically,


transgenic cultivars should be designed to act synergistically with other IPM tactics, especially biological control. Some of the major challenges facing transgenic-cultivar development in the future stem from the need for developing cultivars that are compatible with biological control and consequently are more likely to be sustainable bases for IPM strategies. A first challenge will be to develop a sound understanding of the interactions between transgenic plants, herbivores and natural enemies, particularly parasitoids and predators. Moreover, interactions should be studied at the individual, population and community levels. This should facilitate the development of transgenic cultivars that act synergistically with biological control and thus are compatible with IPM. A second challenge will be to better understand the effects of transgenic cultivars on the movement and colonization patterns of herbivore and natural-enemy populations across entire agroecosystems. This will facilitate the development of regional crop-management strategies that include transgenic cultivars and contribute to regional pest-management efforts by managing the movement and colonization patterns of pest and natural-enemy populations. Finally, a third challenge will be to develop and deploy transgenic cultivars against major pests of crops that have little commercial potential, such as pests of staple crops in developing countries and of lowvalue crops in developed countries. One model which if emulated may prove useful is that followed to develop -carotene-rich, ‘golden’ rice through joint public and philanthropic funding, which allowed scientists to develop a (non-insecticidal) transgenic cultivar with little commercial potential in developing countries (Ye et al., 2000). In conclusion, transgenic cultivars, in general, are a valuable tool in our arsenal of pest-management technologies and therefore it is imperative that they are used according to established IPM principles. However, recent experiences with commercial Bt cultivars suggest that basic IPM principles are ignored following deployment of these cultivars: Bt toxins are used prophylactically as a first resort, with no regard to established

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 140


J.S. Bernal et al.

pest threshold levels, and the control of key pests relies on a single tactic. This disregard for IPM principles has serious implications for the sustainability of these cultivars and for IPM strategies that depend on Bt toxins. Tacit acceptance that Bt cultivars are being used in a manner that is unsustainable is implicit in our deep preoccupation with Btresistance management. It will be imperative for the compatibility of transgenic cultivars

in general with biological control, and therefore IPM, to be addressed during the development process so transgenic cultivars are designed to be sustainable. Increasing our understanding of the interactions between transgenic cultivars and herbivore and natural-enemy populations is necessary and urgent in order to develop transgenic cultivars that play central roles, along with biological control, within IPM strategies.

References Adamczyk, J.J., Holloway, J.W., Church, G.E., Leonard, B.R. and Graves, J.B. (1998) Larval survival and development of the fall armyworm (Lepidoptera: Noctuidae) on normal and transgenic cotton expressing the Bacillus thuringiensis CryIA(c) δ-endotoxin. Journal of Economic Entomology 91, 539–545. Anderson, T.E., Kennedy, G.G. and Stinner, R.E. (1984) Distribution of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), as related to oviposition preference of the springcolonizing generation in eastern North Carolina. Environmental Entomology 13, 248–251. Annis, B. and O’Keefe, L.E. (1987) Influence of pea genotype on parasitization of the pea weevil, Bruchus pisorum (Coleoptera: Bruchidae) by Eupteromalus leguminis (Hymenoptera: Pteromalidae). Environmental Entomology 16, 653–655. Arpaia, S., Gould, F. and Kennedy, G.G. (1997) Potential impact of Coleomegilla maculata predation on adaptation of Leptinotarsa decemlineata to Bt-transgenic potatoes. Entomologia Experimentalis et Applicata 82, 91–100. Bell, H.A., Fitches, E.C., Down, R.E., Marris, G.C., Edwards, J.P., Gatehouse, J.A. and Gatehouse, A.M.R. (1999) The effect of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on Eulophus pennicornis (Hymenoptera: Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae). Journal of Insect Physiology 45, 983–991. Benrey, B. and Denno, R.F. (1997) The slow growth-high mortality hypothesis: a test using the cabbage butterfly. Ecology 78, 987–999. Bernal, J.S. and Sétamou, M. (2003) Fortuitous antixenosis in transgenic sugarcane: antibiosis-expressing cultivar deters oviposition by herbivore pests. Environmental Entomology 32, 886–894. Bernal, J.S., Griset, J.G. and Gillogly, P.O. (2002) Impacts of developing on Bt maize-intoxicated hosts on fitness parameters of a stemborer parasitoid. Journal of Entomological Science 37, 27–40. Bhat, M.G. (1999) On biodiversity access, intellectual property rights, and conservation. Ecological Economics 29, 391–403. Birch, A.N.E., Geoghegan, I.E., Majerus, M.E.N., McNicol, J.W., Hackett, C., Gatehouse, A.M.R. and Gatehouse, J.A. (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding 5, 75–83. Board on Agriculture (1989) Alternative Agriculture. National Academy of Sciences, Washington, DC. Bottrell, D.G. and Weil, R.R. (1995) Protecting crops and the environment: striving for durability. In: Juo, A.S.R. and Freed, R.D. (eds) Agriculture and the Environment: Bridging Food Production and Environmental Protection in Developing Countries. American Society of Agronomy, Madison, Wisconsin, pp. 55–73. Bottrell, D.G., Barbosa, P. and Gould, F. (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annual Review of Entomology 43, 347–367. Bradley, J.R. (1995) Expectations for transgenic Bt cotton: are they realistic? In: Herber, D.J. and Richter, D.A. (eds) Proceedings of the Beltwide Cotton Conference. National Cotton Council of America, Memphis, Tennessee, pp. 763–765. Brandenburg, R.L. and Kennedy, G.G. (1982) Intercrop relationships and spider mite dispersal in a corn/peanut agro-ecosystem. Entomologia Experimentalis et Applicata 32, 269–276. Brazzle, J.R., Heinz, K.M. and Parrella, M.P. (1997) Multivariate approach to identifying patterns of Bemisia argentifolii (hom*optera: Aleyrodidae) infesting cotton. Environmental Entomology 26, 995–1003.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 141

Transgenic Insecticidal Cultivars


Cannon, R.J.C. (1996) Bacillus thuringiensis use in agriculture: a molecular perspective. Biological Reviews 71, 561–636. Chandler, L.D. and Faust, R.M. (1998) Overview of area wide management of insects. Journal of Agricultural Entomology 15, 319–325. Couty, A., de la Viña, G., Clark, S.J., Kaiser, L., Pham-Delegue, M.-H. and Poppy, G.M. (2001) Direct and indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potatoaphid parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). Journal of Insect Physiology 47, 553–561. DeBach, P. and Rosen, D. (1991) Biological Control by Natural Enemies. Cambridge University Press, Cambridge. De Leo, F., Bonadé-Bottino, M.A., Ceci, L.R., Gallerani, R. and Jouanin, L. (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiolology 118, 997–1004. De Souza Silva, J. (1995) Plant intellectual property rights: the rise of nature as commodity. In: Peritore, N.P. and Galve-Peritore, A.K. (eds) Biotechnology in Latin America: Politics, Impacts, and Risks. SR Books, Wilmington, North Dakota, pp. 57–67. Devine, G.J., Wright, D.J. and Denholm, I. (2000) A parasitic wasp (Eretmocerus mundus Mercet) can exploit chemically induced delays in the development rates of its whitefly host (Bemisia tabaci Genn.). Biological Control 19, 64–75. Dulmage, H.T. (1981) Insecticidal activity of isolates of Bacillus thuringiensis and their potential for pest control. In: Burgess, H.D. (ed.) Microbial Control of Pests and Plant Diseases 1970–1980. Academic Press, London, pp. 193–223. Ellstrand, N.C., Prentice, H.C. and Hanco*ck, J.F. (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology and Systematics 30, 539–563. ERS-USDA (1999) Genetically Engineered Crops for Pest Management. Available at http://www.econ. FAO (1967) Report of the First Session of the FAO Panel of Experts on Integrated Pest Control. FAO, Rome. Federici, B.A. (1999) Bacillus thuringiensis in biological control. In: Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego, California, pp. 575–593. Feeny, P. (1976) Plant apparency and chemical defence. In: Wallace, J.W. and Mansell, R.L. (eds) Recent Advances in Phytochemistry, Vol. 10, Biochemical Interaction Between Plants and Insects. Plenum Press, New York, pp. 1–40. Fernández-Cornejo, J. and McBride, W.D. (2000) Genetically Engineered Crops for Pest Management in US Agriculture: Farm-level Effects. Agricultural Economic Report No. 786, Economic Research Service, US Department of Agriculture, Washington, DC. Ferro, D.N. and McNiel, J.N. (1998) Habitat enhancement and conservation of natural enemies of insects. In: Barbosa, P. (ed.) Conservation Biological Control. Academic Press, San Diego, California, pp. 123–132. Fitches, E. and Gatehouse, J.A. (1998) A comparison of the short and long term effects of insecticidal lectins on the activities of soluble and brush border enzymes of tomato moth larvae (Lacanobia oleracea). Journal of Insect Physiology 44, 1213–1224. Gatehouse, A.M.R. and Gatehouse, J.A. (1998) Identifying proteins with insecticidal activity: use of encoding genes to produce insect-resistant transgenic crops. Pesticide Science 52, 165–175. Gatehouse, A.M.R., Boulter, D. and Hilder, V.A. (1991) Novel insect resistance using protease inhibitor genes. In: Dennis, E.S. and Llewellyn, D.J. (eds) Molecular Approaches to Crop Improvement. SpringerVerlag, Vienna, pp. 63–77. Gianessi, L.P. and Carpenter, J.E. (1999) Agricultural Biotechnology: Insect Control Benefits. National Center for Food and Agricultural Policy. Available at: Gill, S.S., Cowles, E.A. and Pietrantonio, P. (1992) The mode of action of Bacillus thuringiensis endotoxins. Annual Review of Entomology 37, 615–636. González, D. and Wilson, L.T. (1982) A food-web approach to economic thresholds: a sequence of pests/predaceous arthropods on California cotton. Entomophaga 27, 31–43. Gordh, G., Legner, E.F. and Caltagirone, L.E. (1999) Biology of parasitic Hymenoptera. In: Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego, California, pp. 355–381. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 142


J.S. Bernal et al.

Gould, F., Kennedy, G.G. and Johnson, M.T. (1991) Effects of natural enemies on the rate of herbivore adaptation to resistant plants. Entomologia Experimentalis et Applicata 58, 1–14. Hagen, K.S. (1986) Ecosystem analysis: plant cultivars (HPR), entomophagous species and food supplements. In: Boethel, D. and Eikenbary, R.D. (eds) Interactions of Plant Resistance and Parasitoids and Predators of Insects. Ellis Horwood, New York, pp. 151–198. Hagen, K.S., Bombosch, S. and McMurtry, J.A. (1976) The biology and impact of predators. In: Huffaker, C.B. and Messenger, P.S. (eds) Theory and Practice of Biological Control. Academic Press, New York, pp. 93–142. Haggstrom, H. and Larsson, S. (1995) Slow larval growth on a suboptimal willow results in high predation mortality in the leaf beetle Galerucella lineola. Oecologia 104, 308–315. Hilbeck, A., Baumgartner, M., Fried, P.M. and Bigler, F. (1998) Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Environmental Entomology 27, 480–487. Hilbeck, A., Meier, M.S. and Raps, A. (2000) Review on Non-target Organisms and Bt-plants. Report to Greenpeace International, Amsterdam. Ecostrat, Zurich. Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, F. and Boulter, D. (1987) A novel mechanism of insect resistance engineered into tobacco. Nature 330, 160–163. Holl, K., Daily, G. and Ehrlich, P.R. (1990) Integrated pest management in Latin America. Environmental Conservation 17, 341–350. Honêk, A. (1982) The distribution of overwintered Coccinella septempunctata L. (Col., Coccinellidae) adults in agricultural crops. Zeitschrift für Angewandte Entomologie 94, 311–319. Hoy, C.W., Feldman, J., Gould, F., Kennedy, G.G., Reed, G. and Wyman, J.A. (1998) Naturally occurring biological controls in genetically engineered crops. In: Barbosa, P. (ed.) Conservation Biological Control. Academic Press, San Diego, California, pp. 185–205. Hubbell, B.J. and Welsh, R. (1998) Transgenic crops: engineering a more sustainable agriculture? Agriculture and Human Values 15, 43–56. ISAAA (International Service for the Acquisition of Agri-biotech Applications) (2002) Global GM Crop Area Continues to Grow and Exceeds 50 Million Hectares for First Time in 2001. Available at: Ives, P.M. (1981) Estimation of coccinellid numbers and movement in the field. Canadian Entomologist 113, 981–997. Jervis, M.A., Kidd, N.A.C., Fitton, M.G., Huddleston, T. and Dawah, H.A. (1993) Flower-visiting by hymenopteran parasitoids. Journal of Natural History 27, 67–105. Jesse, L.C.H. and Obrycki, J.J. (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125, 241–248. Johnson, M.T. and Gould, F. (1992) Interaction of genetically engineered host plant resistance and natural enemies of Heliothis virescens (Lepidoptera: Noctuidae) in tobacco. Environmental Entomology 21, 586–597. Jones, K.D. (1994) Aspects of the biology and biological control of the European corn borer in North Carolina. PhD thesis, North Carolina State University, Raleigh, North Carolina 127 pp. Kennedy, G.G. and Storer, N.P. (2000) Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annual Review of Entomology 45, 467–493. Kieckhefer, R.W. and Miller, E.L. (1967) Trends of populations of aphid predators on South Dakota cereal crops – 1963–1965. Annals of the Entomological Society of America 60, 516–518. King, A.B. and Eyzaguirre, P.B. (1999) Intellectual property rights and agricultural biodiversity: literature addressing the suitability of IPR for the protection of indigenous resources. Agriculture and Human Values 16, 41–49. Kogan, M., Gerling, D. and Maddox, J.V. (1999) Enhancement of biological control in annual agricultural environments. In: Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego, California, pp. 789–818. Koziel, M.G., Carozzi, N.B., Currier, T.C., Warren, G.W. and Evola, S.V. (1993) The insecticidal crystal proteins of Bacillus thuringiensis: past, present and future uses. In: Tombs, M.P. (ed.) Biotechnology and Genetic Engineering Reviews, Vol. II. Intercept Press, Andover, Massachusetts, pp. 171–228. Legaspi, J.C., Legaspi, B.C., Bernal, J.S. and Sétamou, M. (2004) Insect resistant transgenic crops expressing plant lectins. In: Koul, O. and Dhaliwal, G.S. (eds) Transgenic Crop Protection: Concepts and Strategies. Science Publishers, New Hampshire. Lichtenberg, E. and Zimmerman, R. (1999) Adverse health experiences, environmental attitudes, and pesticide usage behavior of farm operators. Risk Analysis 19, 283–294.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 143

Transgenic Insecticidal Cultivars


Losey, J.E., Rayor, L.S. and Carter, M.E. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214. Luck, R.F., Tauber, M.J. and Tauber, C.A. (1995) The contributions of biological control to population and evolutionary ecology. In: Nechols, J.R., Andres, L.A., Beardsley, J.W., Goeden, R.D. and Jackson, C.G. (eds) Biological Control in the Western United States, Accomplishments and Benefits of Regional Research Project W-84, 1964–1989. Division of Agriculture and Natural Resources, University of California, Oakland, California, pp. 25–45. Lynch, R.E., Wiseman, B.R., Plaisted, D. and Warnick, D. (1999) Evaluation of transgenic sweet corn hybrids expressing CryIA(b) toxin for resistance to corn earworm and fall armyworm (Lepidoptera: Noctuidae). Journal of Economic Entomology 92, 246–252. Machuka, J. (2001) Agricultural biotechnology for Africa: African scientists and farmers must feed their own people. Plant Physiology 126, 16–19. Margolies, D.C. and Kennedy, G.G. (1985) Movement of the twospotted spider mite, Tetranychus urticae, among hosts in a corn–peanut agroecosystem. Entomologia Experimentalis et Applicata 36, 193–196. McConnell, R. and Hruska, A. (1993) An epidemic of pesticide poisoning in Nicaragua: implications for prevention in developing countries. American Journal of Public Health 83, 1559–1562. McLaren, J.S. (2000) The importance of genomics to the future of crop production. Pest Management Science 56, 573–579. Moore, C.C., Benedict, J.H., Fuchs, T.W., Friesen, R.D. and Payne, C. (1999) Bt Cotton Technology in Texas: a Practical View. Bulletin B-6107, Texas Agricultural Extension Service, College Station, Texas. Morris, M.L. and López-Pereira, M.A. (1999) Impacts of Maize Breeding Research in Latin America 1966–1997. CIMMYT, Mexico. Murray, D.L. (1994) Cultivating Crisis: the Human Cost of Pesticides in Latin America. University of Texas Press, Austin, Texas. Neunzig, H.H. (1963) Wild host plants of the corn earworm and the tobacco budworm in eastern North Carolina. Journal of Economic Entomology 56, 135–139. Neunzig, H.H. (1969) The Biology of the Tobacco Budworm and the Corn Earworm in North Carolina with Particular Reference to Tobacco as a Host. Technical Bulletin 196, North Carolina Agricultural Experiment Station, Raleigh, North Carolina. Nicholls, C.I. and Altieri, M.A. (1997) Conventional agricultural development models and the persistence of the pesticide treadmill in Latin America. International Journal of Sustainable Development and World Ecology 4, 93–111. NRC (Committee on Pesticides in the Diets of Infants and Children) (1993) Pesticides in the Diets of Infants and Children. National Academy Press, Washington, DC. NRC (Committee on Genetically Modified Pest-protected Plants) (2000) Genetically Modified Pest-protected Plants: Science and Regulation. National Academy Press, Washington, DC. Pair, S.D., Wiseman, B.R. and Sparks, A.N. (1986) Influence of four corn cultivars on fall armyworm (Lepidoptera: Noctuidae) establishment and parasitization. Florida Entomologist 69, 566–570. Pels, B. and Sabelis, M.W. (2000) Do herbivore-induced plant volatiles influence predator migration and local dynamics of herbivorous and predatory mites? Experimental and Applied Acarology 24, 427–440. Perkins, J.H. (1982) Insects, Experts, and the Insecticide Crisis: the Quest for New Pest Management Strategies. Plenum Press, New York. Perlak, F.J., Deaton, R.W., Armstrong, T.A., Fuchs, R.L., Sims, S.R., Greenplate, J.T. and Fischoff, D.A. (1990) Insect resistant cotton plants. Bio/Technology 8, 939–943. Pimentel, D., McLaughlin, L., Zepp, A., Lakitan, B., Kraus, T., Kleinman, P., Vancini, F., Roach, W.J., Graap, E., Keeton, W.S. and Selig, G. (1993) Environmental and economic effects of reducing pesticide use in agriculture. Agriculture, Ecosystems and Environment 46, 273–288. Porter, W.P., Jaeger, J.W. and Carlson, I.H. (1999) Endocrine, immune, and behavioral effects of aldicarb (carbamate), atrazine (triazine), and nitrate (fertilizer) mixtures at groundwater concentrations. Toxicology and Industrial Health 15, 133–150. Poston, F.L. and Pedigo, L.P. (1975) Migration of plant bugs and the potato leafhopper in a soybean–alfalfa complex. Environmental Entomology 4, 8–10. Potting, R.P.J., Vermeulen, N.E. and Conlong, D.E. (1999) Active defence of herbivorous hosts against parasitism: adult parasitoid mortality risk involved in attacking a concealed stemboring host. Entomologia Experimentalis et Applicata 91, 143–148. Powell, K.S., Spence, J., Bharathi, M., Gatehouse, J.A. and Gatehouse, A.M.R. (1998) Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). Journal of Insect Physiology 44, 529–539.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 144


J.S. Bernal et al.

Prasifka, J.R., Krauter, P.C., Heinz, K.M., Sansone, C.G. and Minzenmayer, R.R. (1999) Predator conservation in cotton: using grain sorghum as a source for insect predators. Biological Control 16, 223–229. Price, P.W. (1976) Colonization of crops by arthropods: non-equilibrium communities in soybean fields. Environmental Entomology 5, 605–611. Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N. and Weiss, J.E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41–65. Puterka, G.J., Slosser, J.E. and Price, J.R. (1985) Parasites of Heliothis spp. (Lepidoptera: Noctuidae): parasitism and seasonal occurrence for host crops in the Texas Rolling Plains. Environmental Entomology 14, 441–446. Regev, U. (1984) An economic analysis of man’s addiction to pesticides. In: Conway, G.R. (ed.) Pest and Pathogen Control: Strategic, Tactical, and Policy Models. John Wiley & Sons, New York, pp. 441–453. Repetto, R. (1985) Paying the Price: Pesticide Subsidies in Developing Countries. World Resources Institute, Washington, DC. Rhoades, D.F. and Cates, R.G. (1976) Towards a general theory of plant antiherbivore chemistry. In: Wallace, J.W. and Mansell, R.L. (eds) Recent Advances in Phytochemistry, Vol. 10, Biochemical Interaction Between Plants and Insects. Plenum Press, New York, pp. 168–213. Rice, M.E. and Pilcher, C.D. (1998) Potential benefits and limitations of transgenic Bt corn for management of the European corn borer (Lepidoptera: Crambidae). American Entomologist 44, 75–78. Savinelli, C.E., Bacheler, J.S. and Bradley, J.R. Jr (1986) Nature and distribution of European corn borer (Lepidoptera: Pyralidae) larval feeding damage to cotton in North Carolina. Environmental Entomology 15, 399–402. Savinelli, C.E., Bacheler, J.S. and Bradley, J.R. Jr (1988) Ovipositional preferences of the European corn borer (Lepidoptera: Pyralidae) for field corn and cotton under field cage conditions in North Carolina. Environmental Entomology 17, 688–690. Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J. and Feitelson, J. (1998) Bacillus thuringiensis and its pesticidal proteins. Microbiology and Molecular Biology Reviews 62, 775–806. Schuler, T.H., Poppy, G.M., Kerry, B.R. and Denholm, I. (1999) Potential side effects of insect-resistant transgenic plants on arthropod natural enemies. Trends in Biotechnology 17, 210–216. Sétamou, M., Bernal, J.S., Legaspi, J.C. and Mirkov, T.E. (2002a) Effects of snowdrop lectin (GNA) expressed in transgenic sugarcane on fitness of Cotesia flavipes (Cameron), a parasitoid of the nontarget pest Diatraea saccharalis F. Annals of the Entomological Society of America 95, 75–83. Sétamou, M., Bernal, J.S., Legaspi, J.C., Mirkov, T.E. and Legaspi, B.C. Jr (2002b) Evaluation of lectinexpressing transgenic sugarcane against stalkborers (Lepidoptera: Pyralidae): effects on life history parameters and damage. Journal of Economic Entomology 95, 469–477. Sétamou, M., Bernal, J.S., Legaspi, J.C. and Mirkov, T.E. (2002c) Parasitism and location of sugarcane borer hosts by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) on transgenic and conventional sugarcane. Environmental Entomology 31, 1219–1225. Settle, W.H., Ariawan, H., Astuti, E.T., Cahyana, W., Hakim, A.L., Hindayana, D., Lestari, A.S. and Sartanto, P. (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77, 1975–1988. Shand, H. (1991) There is a conflict between intellectual property rights and the rights of farmers in developing countries. Journal of Agricultural and Environmental Ethics 4, 131–142. Shu, Q., Ye, G., Cui, H., Cheng, X., Xiang, Y., Wu, D., Gao, M., Xia, Y., Hu, C., Sardana, R. and Altosaar, I. (2000) Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran rice pest species. Entomologia Experimentalis et Applicata 6, 433–439. Silvie, P., Deguine, J.P., Nibouche, S., Michel, B. and Vaissayre, M. (2001) Potential of threshold-based interventions for cotton pest control by small farmers in West Africa. Crop Protection 20, 297–301. Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Kilgore, W.W. and Doutt, R.L (eds) Pest Control: Biological, Physical, and Selected Chemical Methods. Academic Press, New York, pp. 295–340. Stern, V.M., Smith, R.F., van den Bosch, R. and Hagen, K.S. (1959) The integrated control concept. Hilgardia 29, 81–101. Thompson, S.N. and Hagen, K.S. (1999) Nutrition of entomophagous insects and other arthropods. In: Bellows, T.S. and Fisher, T.W. (eds) Handbook of Biological Control. Academic Press, San Diego, California, pp. 594–692. Thrupp, L.A. (1995) Bittersweet Harvests for Global Supermarkets: Challenges in Latin America’s Agricultural Export Boom. World Resources Institute, Washington, DC.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 145

Transgenic Insecticidal Cultivars


Tomov, B.W., Bernal, J.S. and Vinson, S.B. (2003) Impacts of transgenic sugarcane expressing GNA lectin on parasitism of Mexican rice borer by Parallorhogas pyvalophagus (Marsh) (Hymenoptera: Braconidae). Environmental Entomology 32, 866–872. Turlings, T.C.J. and Benrey, B. (1998) Effects of plant metabolites on the behaviour and development of parasitic wasps. Ecoscience 5, 321–333. Umeozor, O.C., Van Duyn, J.W., Bradley, J.R. Jr and Kennedy, G.G. (1986) Intercrop effects on the distribution of populations of the European corn borer, Ostrinia nubilalis, in maize. Entomologia Experimentalis et Applicata 40, 293–296. Vaeck, M., Reynaerts, A., Höfte, H., Jansens, S., De Beuckeleer, M., Dean, C., Zabeau, M., Monatgu, M.V. and Leemans, J. (1987) Transgenic plants protected from insect attack. Nature 328, 33–37. Venzon, M., Janssen, A. and Sabelis, M.W. (1999) Attraction of a generalist predator towards herbivoreinfested plants. Entomologia Experimentalis et Applicata 93, 305–314. Visser, B., Bosch, D. and Honée, G. (1993) Domain function studies of Bacillus thuringiensis crystal proteins: a genetic approach. In: Entwistle, P.F., Cory, J.S., Bailey, M.J. and Higgs, S. (eds) Bacillus thuringiensis, an Environmental Biopesticide: Theory and Practice. John Wiley & Sons, Chichester, UK, pp. 71–88. Vorley, V.T. and Wratten, S.D. (1987) Migration of parasitoids (Hymenoptera: Braconidae) of cereal aphids (Hemiptera: Aphididae) between grassland, early-sown cereals and late-sown cereals in southern England. Bulletin of Entomological Research 77, 555–568. Warren, G.W., Carozzi, N.B., Desai, N. and Koziel, M.G. (1992) Field evaluation of transgenic tobacco containing a Bacillus thuringiensis insecticidal protein gene. Journal of Economic Entomology 85, 1651–1659. Wilson, F.D., Flint, H.M., Deaton, W.R., Fischhoff, D.A., Perlak, F.J., Armstrong, T.A., Fuchs, R.L., Berberich, S.A., Parks, N.J. and Stapp, B.R. (1992) Resistance of cotton lines containing a Bacillus thuringiensis toxin to pink bollworm (Lepidoptera: Gelechiidae) and other insects. Journal of Economic Entomology 85, 1516–1521. Wilson, F.D., Flint, H.M., Deaton, W.R. and Buehler, R.E. (1994) Yield, yield components, and fiber properties of insect-resistant cotton lines containing a Bacillus thuringiensis toxic gene. Crop Science 34, 38–41. Wissinger, S.A. (1997) Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biological Control 10, 4–15. Wraight, C.L., Zangerl, A.R., Carroll, M.J. and Berenbaum, M.R. (2000) Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proceedings of the National Academy of Science USA 97, 7700–7703. Wratten, S.D. and Thomas, C.F.G. (1990) Farm-scale spatial dynamics of predators and parasitoids in agricultural landscapes. In: Bunce, R.G.H. and Howard, C.G. (eds) Species Dispersal in Agricultural Habitats. Belhaven Press, London, pp. 219–237. Ye, X.D., Al-Babili, S., Kloti, A., Zhang, J., Lucca, P., Beyer, P. and Potrykus, I. (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287, 303–305.

06IntpestManCh6.QXD 14/4/04 2:25 pm Page 146

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 147


Plant Resistance against Pests: Issues and Strategies

C. Michael Smith Department of Entomology, Kansas State University, Manhattan, KS 66506–4004, USA E-Mail: [emailprotected]

Introduction The production of crop plants with heritable arthropod-resistant traits has been recognized for more than 100 years as a sound approach to crop protection (Painter, 1951; Smith, 1999). Today, hundreds of arthopod-resistant crop cultivars are grown globally, representing the products of many successful cooperative research efforts between entomologists and plant breeders. These efforts have significantly improved world food production, helped to alleviate hunger, improved the nutrition of many populations and transformed many food-importing nations into food exporters. Numerous authors have chronicled the development of plant resistance as a science and as a valuable tool in integrated pest management (IPM) (Snelling, 1941; Painter, 1951; Chesnokov, 1953; Russell, 1978; Lara, 1979; Panda, 1979; Maxwell and Jennings, 1980; Smith, 1989; Dhaliwal and Dilawari, 1993; Smith et al., 1994; Panda and Khush, 1995; Dhaliwal and Singh, 2004).

Benefits of Resistance Insect-resistant cultivars are highly costeffective components of IPM systems, and many examples demonstrate how they provide substantial returns on economic invest-

ment. In the USA, insect-resistant sorghum cultivars increase producer profits by several hundred million dollars each year (Eddleman et al., 1999). The use of Bacillus thuringiensis (Bt) transgenic maize hybrids (see below and Fig. 7.1) currently increases US maize producer profits by approximately 7% per year. In Morocco, Hessian-flyresistant bread wheats have been shown to provide a 9:1 return on investment of research (Azzam et al., 1997). The economic value of genetic resistance in wheat to all major worldwide arthropod pests amounts to more than US$250 million/year (Smith et al., 1999). The multiple insect-resistant rice cultivar IR36 provided approximately US$1 billion of additional annual income to rice producers and processors in Asia for over 20 years (Khush and Brar, 1991). The returns on resistant-cultivar research compared with insecticides range from 100:1 to 10:1, making them a valuable component of crop production and greatly improving the competitiveness of crop producers in many countries. Insect resistant-cultivars also provide substantial environmental benefits and contribute to reduced crop insecticide use and insecticide residues, thus improving the food, health and safety of consumers. The production of insect-resistant cultivars also helps to protect groundwater from pesticide contamination.

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


07IntpestManCh7.QXD 14/4/04 2:25 pm Page 148


C.M. Smith

70 Percentage of hectares grown

1996 60



1998 1999





20 10 0 Cotton


Fig. 7.1. Percentage of cotton and maize cultivars produced in the USA from 1996 to 2001 containing Bacillus thuringiensis delta endotoxins (from James, 2000; Anon., 2001).

Issues and Strategies: Recent and Future There were three predominant scientific issues that affected the thoughts and actions of plant-resistance scientists in the decade of the 1990s. These issues were the development and deployment of the first transgenic insect-resistant cultivars, the discovery of the first molecular markers linked to plant genes for arthropod resistance and the first cloning and sequencing of a plant gene expressing insect resistance. Transgenes from the bacterium, Bt, which encode δ-endotoxin insecticidal proteins, were expressed in the first commercial transgenic cotton, maize and potato cultivars. Although controversial, Bt crops are currently marketed and produced in Australia, Canada, China, India, South Africa and the USA. There is a trend towards Bt crops becoming more prevalent in global agriculture. Many other proteins toxic to arthropods have been identified and transgenes encoding several of these inhibitors have been used to transform plants expressing insect resistance. Molecular markers have been used to map conventional insect-resistance genes in several crops (Yencho et al., 2000). Nevertheless, the Meu-1.2 gene of wild tomato, Lycopersicon peruvianum, which expresses resistance to the potato aphid, Macrosiphum euphorbiae

(Thomas), and three Meloidogyne spp. nematodes, is the only insect-resistance gene to be sequenced (Milligan et al., 1998). Bioinformatic computational tools to analyse, interpret and utilize huge amounts of data being generated by genomics research on several major crop plants have already provided genetic maps, physical maps and expressed sequence tag (EST) complementary DNA (cDNA) libraries of several major cropplant genomes. Future insect-resistance gene cloning and sequence determination will probably proceed by ‘data-mining’ the genomic information from plant resistancegene analogues (RGAs), defence response (DR) genes and EST libraries. Each of these issues has been researched, debated and implemented to varying degrees. In the following sections, information is presented to demonstrate how each issue has become or potentially will become a strategy used by many plant-resistance practitioners in the 21st century.

Transgenic Insect Resistance A major change occurred in the development of insect-resistant varieties near the end of the 20th century, when Agrobacterium transformation systems and biolistic projectile devices were used to transfer genes encoding

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 149

Plant Resistance against Pests

insecticidal crystal (cry) toxins from the soil bacterium Bt into the genome of naïve plant cells. Transformed plants resulting from cell and tissue culture were grown to maturity and produced transgenic seed. When transgenic plant foliage is fed upon by pest insects, ingested crystals are solubilized in the alkaline gut environment, where active toxic fragment(s) are released by insect digestion, and these fragments bind to specific receptors on the midgut cells of susceptible larvae, causing colloid osmotic lysis of those cells, resulting in insect death. Numerous other proteins toxic to insects have also been identified and expressed in transgenic plants (see reviews by Sharma et al., 2000; Oppert, 2001; Lawrence and Koundal, 2002). These include the carbohydrate-binding proteins lectins; proteinase inhibitors from maize, potato, rice and tomato; proteinase inhibitors from insects; chymotrypsin and trypsin inhibitors from cowpea and sweet potato; and α-amylase inhibitors from common bean. Transgenes encoding several of these inhibitors have been transferred into various crop plants, including bean, cotton, potato and rice. Despite these impressive accomplishments, the general usefulness of transgenic plants containing non-Bt toxic proteins in plant protection remains to be implemented. Many transgenic Bt crop plants have been developed (see review by Huang et al., 1999), but only cotton, maize and potato cultivars with transgenes expressing resistance to Coleoptera and Lepidoptera have been produced and marketed. These crops are essentially insecticidal plants, which has complicated their deployment. Bt crop-plant production and use have met with strong opposition by environmentalists, primarily in Europe and the USA. The marketing of the first Bt cultivars in 1994 launched an intense scientific debate on how much Bt is sufficient for effectiveness without selecting for pest population resistance to Bt. By 1998, Bt maize production had increased to approximately 20% of the US crop and the first Bt educational publications were published to provide a scientific basis for the debate (Rissler and Mellon, 1996; Wayland et al., 1998).


Initial experiments by Losey et al. (1999) indicated that Bt maize pollen applied at very high concentrations to leaves of the milkweed plant was toxic to larvae of the monarch butterfly, Danaus plexippus (Linnaeus), feeding on milkweed. Wraight et al. (2000) reported no mortality of the larvae of black swallowtail, Papilio polyxenes Fabricius, on food plants located at varying distances from field plantings of Bt maize, no matter how close the larval food plants were to the pollen-shedding Bt maize plants. Subsequent studies by Sears et al. (2001) and Stanley-Horn et al. (2002) concluded that the risk from Bt maize to monarchs is not significant. One Bt maize cultivar on only 2% of the annual US crop hectarage was shown to be toxic to monarch larvae and has been eliminated from production. Pimentel and Raven (2000) classified the effects of Bt pollen on the food plants of several non-target US butterfly species as relatively insignificant, in comparison with maize pesticide applications and butterfly abiotic mortality factors, such as habitat destruction. Several studies have shown that Bt maize has limited effects on beneficial arthropods in maize agroecosystems (Johnson and Gould, 1992; Pilcher et al., 1997; Al-Deeb et al., 2001). By 1999, the American Phytopathological Society proclaimed that threats to human health were reduced by Bt maize production because of reduced incidence of potentially dangerous mycotoxins (APS, 1999). Nevertheless, differences in media coverage of transgenic crops, European public perceptions of transgenic crops and greater European cultural sensitivities about transgenic crops than those of the US public brought out strong European concerns about transgenic crops (Gaskell et al., 1999). The concerns resulted in the US government developing an independent scientific approval process for Bt crops and other genetically modified organisms. Public activism peaked between 1999 and 2001, when US government and private agricultural research facilities valued at more than US$4 million were destroyed by bioterrorists in California, Hawaii, Maine, Michigan, Minnesota, New York, Oregon, Washington and Wisconsin. In addition, greenhouse and

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 150


C.M. Smith

field experiments involving genetically modified rape, flowers, fruits, maize, oats, onions, trees and wheat were destroyed (Service, 2001). Consumer support for transgenic food crops in the USA is strong despite these bioterrorism events. A consumer survey conducted in August 2002 indicated that 71% of the US population favoured purchasing produce that had been enhanced through biotechnology, in order for it to be protected from insect damage and require fewer pesticide applications (IFIC, 2002). Nevertheless, the majority of European countries continue to oppose the use of Bt (and other genetically modified) crops. Exceptions are occurring in several European countries, such as the Czech Republic, where Bt maize was fieldtested in 2002. Improved governmental decision-making processes, better genetically modified food risk/benefit communication, an increasing volume of research data and an endorsem*nt by the United Nations Food and Agriculture Organization (FAO) have led to increased production of Bt cotton and maize in countries other than the USA, including Argentina, China, India and South Africa (see below). In spite of these successes, the FAO has voiced concerns that the majority of transgenic crops focus on reducing chemical inputs and labour costs in large corporate farms of developed countries, and not on increasing food supplies for the populations of underdeveloped countries. To date, there has been little corporate or public investment in important food crops of the semi-arid tropics, such as sorghum, millet, pigeon pea, chickpea or groundnut. Over the past several years, farm trials in India show Bt cotton yield increases of approximately 60% more than those of conventional non-Bt cultivars (Qaim and Zilberman, 2003). In 2001, more than a quarter of the maize produced in the USA, and over half of the cotton produced was from planting of Bt cultivars (Anon., 2001; Fig. 7.1). Data from a 10-year study conducted by Carrière et al. (2003) in Arizona indicate that production of Bt cotton significantly suppressed populations of the pink bollworm, Pectinophora gossypiella Saunders, and that

the deployment of Bt cotton cultivars contributed to reducing the need for insecticide sprays. Similar results have been reported for bollworm control in South Africa, where Bt cotton use shifted from 7% in the 1997/98 growing season to 90% in the 2001/02 growing season on both small and large farms (Kirsten and Gouse, 2002). The primary benefits have been increased yields from improved bollworm control and related decreased production costs from greatly reduced insecticide usage. Sachs et al. (1996) transformed a high-terpenoid-content cotton cultivar with the CryIA(b) protein for increased resistance to the tobacco budworm, Heliothis virescens (Fabricius). However, no such conventional gene– transgene combinations have been marketed commercially. Insecticide use against one US insect pest of maize, the European corn borer, Ostrinia nubilalis (Hubner), has dropped by approximately 30% since after the commercialization of Bt maize in North America. Bt maize has proved to be a particularly effective means of borer control, because larvae feed inside maize stalks and are impossible to kill by conventional foliar insecticide-spray applications (Rice and Pilcher, 1998). In contrast, demand for Bt potatoes resistant to the Colorado potato beetle, Leptinotarsa decemlineata (Say), peaked in 1995, when growers planted them on 22,260 ha in North America. By 2000 that hectarage had declined by 50%, and in 2001 sales of Bt potato seed ceased in the USA and Canada, primarily because food-processing companies were concerned about consumer food preferences and reluctantly chose not to market transgenic foods. The successes of Bt maize and cotton globally in both developed and several developing countries, as well as the lack of success of Bt potatoes, point to the critical importance of risk communication in developing consumer and producer understanding of new technologies. Abbott et al. (2001) have shown that the media coverage of the development and use of Bt maize has followed a predictable pattern similar to that of many other risk issues. The pattern is one in which scientific developments are initially communicated by the media to the public in

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 151

Plant Resistance against Pests

a positive way, albeit at low levels, and research and industry sources are stressed, without perceptions of public advocacy groups. A ‘triggering event’, in the case of Bt maize the initial Losey et al. (1999) data, caused a dramatic increase in media coverage. These events allow increased inclusion of information from advocacy groups, who elect (in the case of Bt) to exploit negative scientific data, both real and perceived. A trend to report ‘for and against’ information rather than scientific truth follows, deluging the public with conflicting information in a short period of time. Public attention to these sources then declines as other issues come forward or new information is publicized. The current US–European dichotomy over the acceptance of biotechnology illustrates this point well, with the perceived benefits of Bt crops allowing US consumer acceptance and the perceived detriments continuing European rejection of them. Future transgenic-technology education and risk communication efforts may benefit from integrating the educational capabilities of different agencies involved in food production, processing and distribution. Such initiatives are illustrated by the development of the International Food Information Council- and the US Environmental Protection Agency (EPA)-led development of Bt integrated risk-management programmes (see below). In order for transgenic-crop risk-assessment training to be effective, however, educators may consider using hazard analysis critical control point (HACCP) principles, described by Cuperus et al. (1991) for use in food-safety education. HACCP principles have been used extensively to reduce microbiological contamination in the foodprocessing industry. The HACCP approach assesses hazards and risks associated with growing, harvesting, processing, manufacturing, marketing and distribution of food products and determines critical control points (CCPs) (a point where loss of control may result in an unacceptable health risk). For a given CCP, critical limits are identified, monitoring procedures are established and corrective actions are taken if necessary. Application of HACCP principles may serve


to demonstrate how certain perceived risks are in fact not significant. The history of the scientific development of Bt-crop technology is much less complicated, although at some points involving controversy. Before the development of Bt transformants, numerous studies determined that insects became resistant to the cry toxin gene after prolonged exposure to a high dose of Bt (Huang et al., 1999), in the same manner that insect biotypes develop resistance to high doses of conventional pesticides or high levels of conventional gene expression (Llewellyn et al., 1994). Insect biotypes are well documented in the interactions between genes of the gall midge, Orseolia oryzae (Wood-Mason), and brown planthopper, Nilaparvata lugens (Stal), and rice (Tanaka, 1999; Pani and Sahu, 2000) and the Hessian fly and wheat (Ratcliffe and Hatchett, 1997). Biotype occurrence is influenced by the genetic plasticity of the pest insect, its ecological fitness, the number of resistance genes expressed, the resistance category expressed, the fraction of the crop cultivated in an insect-resistant cultivar and the overall efficacy of the IPM programme used to control the pest. Some of these same concepts have been used to develop Bt crop-plant deployment strategies. In order to obtain their maximum longevity, Bt insect-resistant transgenes in maize and cotton are deployed with non-Bt plant ‘refuges’ that enable the survival of pest moths from susceptible larvae to mate with moths produced from larvae resistant to Bt. Shifting the mortality of larvae heterozygous for resistance from 50 to 95% provides a tenfold delay in time before the development of resistance (Gould, 1998). A refuge portion of the crop was not commercially or sociologically acceptable at first, but the US EPA coordinated industry and academic research efforts to establish a mechanism to prevent the development of resistance to Bt by key maize insect pests. In 2001, these efforts led to the creation of an insect resistance management (IRM) compliance assurance programme to promote grower compliance and preserve the effectiveness of Bt maize. Manufacturers sponsor an annual survey of Bt maize growers, con-

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 152


C.M. Smith

Table 7.1. Comparisons of conventional and transgenic resistance in crop plants (from Daly and Wellings, 1996). Criteria



Resistance category Mechanism(s) Efficacy Expression Management Sociology Stability Technology transfer

Antibiosis, antixenosis, tolerance Chemical and physical Moderate Constitutive and induced Optional Simple High Moderate

Antibiosis Chemical High Constitutive Required Complex High Fast

ducted by an independent third party, and growers not in compliance with IRM requirements over 2 consecutive years are denied additional access to Bt-maize seed. Bt-crop producers must plant at least a 20% non-Bt maize refuge, except in certain cotton-growing areas, where at least a 50% non-Bt maize refuge is required. Refuge-planting options include blocks within fields, strips across fields or separate fields. Bt-maize fields must be planted within 0.8 km of a refuge. The IRM programmes are a first ever type of government–industry-regulated IPM tecnology. As such, US crop-management programmes relying on transgenic technology have entered a new era in crop production. The IRM programmes are an overall success, although some producers have failed to meet the minimum requirements for non-Bt refuge plantings. In an initial 2000 survey, 29% of producers were not in compliance, but since that time participation has improved. In 2001 only 13% of the producers surveyed were not in compliance and in 2002 14% were non-compliant (Byrne et al., 2003). The continued (and improved) successes of these producer–regulatory–industry partnerships will depend on a combination of good science, communication and common sense in making decisions about Bt-crop cultivar selection and refuge composition. Daly and Wellings (1996) contrasted aspects of conventional and transgenic plant resistance to insects (Table 7.1). Conventional plant resistance genes are expressed as antibiosis or antixenosis effects on insects and tolerance of the resistant cultivar to an insect pest. Many biochemical and biophysi-

cal mechanisms have been identified to explain resistance (Smith, 1989). Transgenic resistance is expressed solely as antibiosis, due to a digestive toxin. While conventional resistance may have both constitutive and induced components, transgenic resistance is fully constitutive. Both types of resistance genes have high stability and, although transgenes have been part of IPM systems for less than 10 years, the transfer of transgenic technology has occurred very quickly. The major difference in the two types of resistance genes is the management (IRM) plan for transgenes. Although the initial IRM schemes for Bt maize are functional, we do not know if they will continue to be effective. Bt maize with resistance to the western maize rootworm, Diabrotica virgifera LeConte, a far more damaging pest than the European corn borer, has recently been approved by the US EPA (Knight, 2003). A 20% refuge similar to that for European corn borer has been adopted for initial production purposes, but an advisory panel had recommended a much larger 50% refuge to sufficiently dilute Bt virulence alleles in surviving maize rootworm larvae. European corn borer-resistant Bt-maize cultivars produce high doses of toxin, but the rootwormresistant maize cultivars cause only 50% rootworm larval mortality. This reduced maize rootworm Bt efficiency and decreased refuge size may lead to a different outcome for maize rootworm-resistant Bt maize from that currently developing for Bt cultivars resistant to lepidopterous larvae. If the Lepidoptera IRM schemes (and others) continue to function successfully, they may

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 153

Plant Resistance against Pests

serve as workable models for the deployment of conventional plant resistance genes that are expressed as high levels of antibiosis (insect mortality), in order to delay the development of resistant biotypes.

Molecular Marker-assisted Selection of Plant Genes for Insect Resistance The tagging and mapping of plant genes for insect resistance has accelerated tremendously since the mid-1990s. This progress has been facilitated by the construction of high-density genetic maps of barley, maize, rye, soybean and wheat (Cregan et al., 1999; Hernández et al., 2001; Korzun et al., 2001; Boyko et al., 2002; Sharopova et al., 2002). Yencho et al. (2000) reviewed molecular markers in many of these same crops linked to genes expressing resistance to several major insect pests. In the premolecular age of plant resistance to insects, phenotypic evaluations determined the initial identity of a source of resistance or progeny from crosses made between resistant and susceptible parents. The marker-assisted selection (MAS) of plants based on genotype, before the phenotypic trait for resistance is expressed, is now being used in many plant-improvement programmes. Demonstrating that a molecular marker is linked to a plant resistance gene, however, involves identifying a phenotypic source of resistance, isolating DNA from resistant and susceptible parent plants, hybridizing or amplifying DNA of resistant and susceptible plants with molecular markers from known chromosome locations to identify those that differentially hybridize or amplify DNA in a polymorphic (informative) pattern via gel electrophoresis, and genotypically screening individual plants from segregating populations for linkage to putative molecular markers. Molecular markers have been identified that are linked both to single major genes for resistance and to groups of loci controlling the expression of quantitative resistance, known as quantitative trait loci (QTLs). Linkages of a resistance gene and a molecular marker may vary greatly. They may be completely linked, where no crossing over


occurs between the resistance gene and the marker during meiosis, and the gene and marker are always linked together from one generation to another. They may be incompletely linked and crossing over may occur between the gene and the marker during meiosis. They may have no linkage, because the gene and the marker are located on different chromosomes or are far apart on the same chromosome. Estimates of the recombination between the resistance gene and a linked marker are measured as the recombination frequency (RF). RF values are measured among segregating F2 plants or F2:3 families by matching the phenotype and genotype of each progeny and subjecting the paired data to MAPMAKER (Lander et al., 1987), an interactive computer package for calculating genetic distance and constructing genetic-linkage maps. The linkage between QTLs and marker loci is determined by the way distribution patterns for the resistance character(s) are linked with the segregation of the resistance gene and the molecular marker at each locus.

Why molecular markers? Many practitioners ask ‘Why use molecular markers?’, given the additional time and labour required to define a molecular marker linked to an insect resistance gene. The answer lies in the fact that there are several advantages to adopting this technology. Restriction fragment length polymorphism (RFLP) markers and microsatellite or simplesequence repeat (SSR) markers (see below) behave in a codominant manner to detect heterozygotes in segregating populations of progeny from crosses between resistant and susceptible parents. In contrast, morphological markers behave in a dominant/recessive manner and do not detect heterozygotes (Staub et al., 1996). In general, the allelic variation detected by molecular markers in natural plant populations is considerably greater than that detected by morphological markers. Molecular markers are unaffected by environment and thus phenotype-neutral, while several examples exist to indicate that morphological markers are highly affected

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 154


C.M. Smith

by environmental variations (see review by Smith, 1999). Finally, morphological markers may interact epistatically and molecular markers do not, which greatly increases the number screened in a single population.

Types of molecular markers Several types of molecular markers have been used to determine the locations of insect-resistance genes. They include RFLP markers, mentioned previously, sequencetagged site (STS) markers, random amplified polymorphic DNA (RAPD) markers, amplified fragment length polymorphism (AFLP) markers and SSRs or microsatellite markers. RFLP markers detect differences between genotype DNA when restriction enzymes cut genomic DNA at specific nucleotide sequences (binding sites) to yield variable-size fragments of DNA base pairs. The digested DNA is electrophoresed and transferred to a nylon membrane via Southern blotting, and the membrane is probed with a 32P–labelled dinucleotide sequence of known chromosome location. The membrane-bound DNA is denatured by heat, allowing probe sequences to bind with complementary sites in the restriction digest and providing information about the putative location of the resistant gene. RFLP probes allow very fine mapping of loci linked to resistance genes, since initially they were more numerous in some crop genomes than other types of molecular markers. Disadvantages of RFLP linkage analysis include the time required to complete (7–10 days) and the use of radioactive isotopes. RFLP analysis has been used to map insect-resistance gene loci in barley, cowpea, mung bean, sorghum, rice and wheat (Moreira et al., 1999; Smith, 1999; Huang et al., 2001; Katsar et al., 2002; Xu et al., 2002). DNA analysis was revolutionized with the discovery of the polymerase chain reaction (PCR) technique (Mullis, 1990). PCR allows the in vitro enzymatic amplification of specific DNA sequences present between two convergent oligonucleotide primers hybridizing to opposite DNA strands. The

commercialization of PCR resulted in the thermal cycler, in which PCR primers of known chromosome location are reacted with template DNA, and the amplification products are electrophoresed to identify primers (markers) yielding polymorphisms. Compared with RFLP hybridization, PCR reactions are much faster (2–3 h) and nonradioactive. However, compared with many RFLP genomic maps, there are fewer PCR primers. Several types of PCR primers identify insect-resistance genes in plants. RAPD PCR primers are short random DNA sequences that alone do not reveal heterozygotes and chromosome-linkage information per se. However, RAPD-generated DNA polymorphic bands can be end-sequenced to design location-specific sequence-characterized amplified regions (SCARs). SCARs have been used to identify and map genes for resistance to the rice gall midge, O. oryzae (Sardesai et al., 2001), and the brown planthopper, N. lugens (Renganayaki et al., 2002). AFLPs are based on the selective PCR amplification of restriction enzyme-digested DNA fragments, as in RFLP analysis (Vos et al., 1995). However, the DNA bands generated in each amplification contain DNA markers of random origin, which result in many more amplified DNA bands. AFLP markers have been used successfully to identify insect-resistance genes in apple, rice and wheat (Murai et al., 2001; Cevik and King, 2002; Weng and Lazar, 2002). SSR or microsatellite primers are tandem arrays of 2–5 base repeat units (particularly dinucleotide repeats), which have been found to be widely distributed in eukaryotic DNA. Microsatellite primers have proved to be very useful in crops where they have been developed, such as maize, soybean and wheat. As a result of a rapidly expanding library of microsatellite markers, SSRs are being used with increasing frequency to identify and map genes for insect resistance in wheat (Liu et al., 2001, 2002; Miller et al., 2001). STS markers – PCR markers sequenced from ends of RFLP sequences – have been used to map genes for insect resistance in barley (Nieto-Lopez and Blake, 1994) and rice (Katiyar et al., 2001).

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 155

Plant Resistance against Pests

MAS of plants is accelerating the accuracy and rate at which a resistance gene can be tracked in the development of arthropodresistant cultivars. There are few comparisons of the efficiency of MAS of resistant plants with phenotypic selection. MAS of genes for Russian wheat aphid, Diuraphis noxia Mordvilko, resistance in wheat and cereal cyst nematode, Heterodera avenae Woll. resistance in barley can be accomplished approximately 30 times faster for approximately 75% more cheaply per evaluation compared to plant phenotypes (Kretshmer et al., 1997; C.M. Smith and X.E. Liu, unpublished). A US MAS genotyping centre for barley and wheat is developing QTLs linked to resistance for fusarium head blight, caused by Fusarium graminearum Schwabe (teleomorph Gibberella zeae (Schwein.)), in order to genotype plants in breeding populations (Van Sanford et al., 2001). QTL analysis has successfully identified loci containing insect-resistance genes in maize (Cardinal et al., 2001; Jampatong et al., 2002), rice (Huang et al., 1997, 2001; Xu et al., 2002), soybean (Rector et al., 1998, 2000), tomato (Moreira et al., 1999) and wheat (Castro et al., 2001). Narvel et al. (2001) used SSR markers to assess US soybean breeding lines and cultivars developed over a 30-year period using conventional phenotypic selection for resistance to foliar feeding by several Lepidoptera. Although some resistance has been transferred, very few minor resistance QTLs have been transferred. MAS has been used to develop near-isogenic soybean lines with multiple insect-resistant QTLs, suggesting that the use of MAS in soybean is justified. Extensive research comparing the use of conventional selection of phenotypic resistance in maize to feeding damage by the southwestern corn borer, Diatraea grandiosella Dyar, to QTL mapping of resistance-gene loci suggests that QTL-MAS and conventional selection methods are equivalent in their ability to improve the level of resistance (Willcox et al., 2002). Although the cost of MAS alone is approximately one-tenth the cost of conventional selection, the accurate identification of QTL position and the cost of generating these initial data as the first step in the MAS process


of QTL analysis makes conventional selection more cost effective.

Cloning and Sequencing Plant Resistance Genes The examples described above demonstrate how plant resistance to insects is mediated by constitutive gene effects. As mentioned previously however, the only insect-resistance gene identified to date is the Meu1.2 gene from wild tomato, L. peruvianum, which confers resistance to the potato aphid, M. euphorbiae (Kaloshian et al., 1995, 1997; Rossi et al., 1998; Vos et al., 1998) and to three species of the root-knot nematode, Meloidogyne spp. (Roberts and Thomason, 1986). Meu1.2 is a member of the nucleotidebinding site–leucine-rich region (NBS–LRR) family of disease- and nematode-resistance genes (Milligan et al., 1998). The LRR region of Meu1.2 functions to signal localized cell death and programmed cell death (Hwang et al., 2000; Wang et al., 2001). Similarities in the sequence and function of other pestresistance genes are beginning to show patterns. RGA sequences (see below) from barley map to loci in regions involved in resistance to the maize leaf aphid, Rhopalosiphum maidis (Fitch). These same sequences are similar to the wheat NBS-LRR Cre3 gene for resistance to the cereal cyst nematode, H. avenae (Lagudah et al., 1997). Other NBS–LRRrelated sequences have also been mapped to regions controlling resistance to the melon aphid, Aphis gossypii Glover (Brotman et al., 2002).

Functional genomics During the past decade, the genomes of Arabidopsis and rice were sequenced, opening huge opportunities for in-depth studies of the molecular bases of plant resistance. The sequencing of extremely large genomes such as wheat, however, remains well in the future. In the interim, plant resistance researchers are data-mining information about Arabidopsis and rice gene sequence, function, and expression, in order to provide

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 156


C.M. Smith

new information about the biochemical and physiological pathways involved in the resistance of other plants to insects. RGAs are conserved amino acid motifs (such as NBS and LRR motifs) derived from sequence comparisons of predominant classes of insect-, disease-, and nematoderesistance genes. RGAs have been isolated in Arabidopsis, barley, lettuce, maize, rice, soybean and wheat (Seah et al., 1998; Shen et al., 1998; Speulman et al., 1998; Leister et al., 1999; Mago et al., 1999; Tada, 1999; Graham et al., 2000). Many cereal-crop RGAs map to orthologous positions in different cereal species. The fact that Meu-1.2 and Mi are active against two organisms as distantly related as aphids and nematodes supports the hypothesis that RGAs can also be used to clone or design genes for insect resistance in crops. Map positions of RGAs in the Triticeae indicate that these genes occur in clusters and are more closely linked physically than those in other regions with similar genetic distances (Feuillet and Keller, 1999; Li et al., 1999; Boyko et al., 2002). For this reason,

Gb 610 Dn 47 Ssg 1, 2, 96 QBph513

Grh11 Dn 98

Triticeae hom*oeologous Group 1

knowledge of the chromosome locations and genome organizations of RGAs in wheat and other crops will be of great value in candidate resistance-gene analyses. The genomes of cereal crops, such as barley, maize, rice, rye, sorghum and wheat, are highly conserved, i.e. the arrangement of many of the genes in a region of a chromosome of one species is similar to that of a chromosome region of another plant species in DNA sequence (Ahn et al., 1993; Paterson et al., 1995; Boyko et al., 1999). Resistancegene maps in barley, sorghum, rice and wheat demonstrate the synteny among loci of these crops linked to genes expressing resistance to several species of pest aphids and planthoppers (Fig. 7.2). The exploitation of such conserved gene order to identify pest-resistance loci of interest will greatly stimulate efforts to clone insect-resistance genes in cereals and other crops as functional genomics becomes more of a reality in agricultural research. For example, using syntenous areas of barley, rice and wheat chromosomes where resistance genes have Ssg 69 Dn 1, 2, 5, 6, 8, x7,8 Gby2 Gb3,5 QBph1 QBph1113 Ssg 86 Dn 29 Gb 312 Gb 54 Gb x14 Gb z14 QBph113

Triticeae hom*oeologous Group 7

Fig. 7.2. Map positions of Heteroptera-resistance gene loci in barley, rice, sorghum and wheat on Triticeae hom*oeologous chromosome groups 1 and 7 (relative loci positions for illustration only, not ordered). Gb, greenbug, Schizaphis graminum (Rondani), resistance gene in wheat; Dn, Russian wheat aphid, Diuraphis noxia (Mordvilko), resistance gene in wheat; Ssg, greenbug-resistance gene in sorghum; QBph, main effect brown planthopper, Nilapartava lugens (Stal), resistance QTL in rice; Grh, green rice leafhopper, Nephotettix cincticeps (Uhler), resistance gene in rice. 1Alam and Cohen, 1998; 2 Boyko et al., 2002; 3Castro et al., 2001; 4 Dubcovsky et al., 1998; 5 Moharramipour et al., 1998; 6 Katsar et al., 2002; 7 Liu et al., 2002; 8 Liu et al., 2001; 9 Miller et al., 2001; 10 C.M. Smith and S. Starkey, unpublished; 11 Tamura et al., 1999; 12 Weng and Lazar, 2002; 13 Xu et al., 2002; 14 L. Zhu, C.M. Smith, E. Boyko and S. Starkey, unpublished.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 157

Plant Resistance against Pests

been mapped, specific candidate rice bacterial artificial chromosome (BAC) contiguous segments can be subjected to in silico analyses to identify sequences similar to those of known resistance genes.

Expressed plant resistance genes Plants use both constitutive and induced defences to protect themselves from insect attack. From a plant-breeding standpoint, plant resistance genes are viewed as constitutively active (always transcribed) in order to identify them in breeding programmes. With the advent of cDNA technologies, however, information about plant genes expressed in reaction to disease and insect attack has exploded, with more than 3000 articles published since 1995 (see reviews of Walling, 2000; Kessler and Baldwin, 2001; Heil and Bostock, 2002). When plant tissues are damaged, messenger RNA (mRNA) signals are translated to proteins. Unique mRNA gene transcripts expressed in resistant plants can now be identified by reverse transcription, where an RNA molecule is copied back into its cDNA by reverse transcriptases. cDNA populations from infested and uninfested plants can be subjected to subtractive suppressive hybridization to remove the hybridized sequences common to both populations. The unhybridized sequences unique to the resistant plant then become a ‘subtracted’ library of resistant cDNAs, which is then sequenced to determine the function of the putative resistance genes. Several studies of expressed insectresistance genes are currently in progress. Messenger RNA differential display, a related technique, was used by Hermsmeier et al. (2001) to study Nicotiana attenuata responses to feeding by tobacco hornworm, Manduca sexta (Johannsen), in the first experiment to identify mRNA transcripts produced after insect attack. Over 500 genes were involved in plant response, and 27 were verified as differentially expressed and sequenced. Transcripts encoding a Thr deaminase gene and a pathogen-inducible α-dioxygenase gene (see below), both involved in the plant defence response (Fig.


7.3), were expressed at significantly increased levels. Complementary DNA libraries can also be probed with molecular markers of known genome function and location, in order to determine the degree of involvement of the expressed gene(s) in resistance. Finally, unique cDNAs can be used to probe oligonucleotide microarrays (gene chips) as a means of determining resistance-gene function based on mRNA expression levels. Commercial oligonucleotide microarrays now allow rapid screening of plant cDNAs expressing potential resistance, with over 14,000 expressed Arabidopsis thaliana sequences. Reymond et al. (2000) constructed a small-scale microarray of 150 ESTs implicated in Arabidopsis defence to demonstrate differences in genes activated by Pieris rapae (Linneaus) feeding, mechanical wounding, and water stress. Several hundred thousand cereal cDNA ESTs are currently being produced publicly for macro- or microarrays that will soon allow searches for expressed genes related to or involved in insect resistance in cereal crops (http://www.ncbi.nlm.nih. gov/dbEST/).

Insect-resistance elicitors Plant reactions to both insect and disease attack may include hypersensitive cell death, as in the case of Meu1.2, activation of DR genes and the redirection of normal cellmaintenance genes to plant defence. In DRgene activation, plants produce elicitors that activate plant gene expression and the synthesis of volatile and non-volatile allelochemicals. The similarities of plant elicitors in response to attacks by different insect species may be the result of common insect salivary enzymes, although some elicitors regulate very insect species-specific responses (van de Ven et al., 2000; Walling, 2000). In addition, chewing insects cause extensive plant-tissue damage, which elicits different plant responses from those induced in response to feeding by piercing/sucking insects, which cause comparatively less tissue damage (Fidantsef et al., 1999; Stout et al., 1999; Walling, 2000). Plant responses to

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 158


C.M. Smith

Insect-feeding injury

salicyclic acid

plant membrane lipids phospholipases O2 + α-linolenic acid

peroxidases α-dioxygenase (PIOX) lipoxygenases (LOX2), (LOX-H3) β-1,3 glucosidase (BGL2) pathogen-response gene (PR-1)

fatty acid peroxides unknown, non-JA signal

hydroperoxide lyase (HPL) 12-oxododecenoic acid (traumatin)

hexenal, 3-hexenal

allene oxide synthase (AOS) 12-oxo-phytodienoic acid (12-OPDA) OPDA reductase jasmonic acid (JA), methyl jasmonate (MeJA) defensin peptide (PDF1.2) β-glucosidase (BGL1) hevein-like protein (HEL) hydroxamic acids monosaccharide H+ symporter (STP4) metallopeptidase-like protein (SLW-1) peroxidases, chitinases, polyphenol oxidases phenolics and polymers phenylalanine ammonia lyase (PAL1) Thr deaminase (TD) proteinase inhibitors vegetative storage proteins (VSP1, 2)


β-glucosidase-like protein (SLW-3)

Fig. 7.3. A generalized diagram of known induced plant-resistance elicitors, genes and gene products produced by insect damage to plant tissues. Substrates shown in shaded grey boxes, enzymes in between. Italics indicate gene(s) expression of compounds involved in insect resistance. For detailed explanations, see individual references (Bergvinson et al., 1994; Bell et al., 1995; Lee et al., 1997; Botha et al., 1998; Fidantsef et al., 1999; Royo et al., 1999; Stout et al., 1999; Forslund et al., 2000; Reymond et al., 2000; Stotz et al., 2000, 2002; van de Ven et al., 2000; Walling, 2000; Halitschke et al., 2001; Hermsmeier et al., 2001; Kessler and Baldwin, 2001; Moran and Thompson, 2001; Slesak et al., 2001; Vancanneyt et al., 2001.)

mechanical damage also differ from those involved in response to feeding damage (Botha et al., 1998; Forslund et al., 2000; Halitschke et al., 2001; Winz and Baldwin, 2001). When insects damage plant tissues during feeding, the death of tissues results in the production of an oxidative ‘burst’. This event triggers the degradation of linolenic acid, which involves elicitors that signal the need of the production of allelochemical plant defences, such as proteinase inhibitors, phenolics and enzymes involved in the eventual production of plant structural defences (Fig. 7.3).

Lipoxygenases involved in cell membrane lipid degradation contribute to the production of jasmonic acid (JA) signals. Transcripts encoding LOX and LOX2 genes have been shown to be strongly induced by feeding of the potato aphid, M. euphorbiae, on tomato (Fidanstef et al., 1999) and the green peach aphid, Myzus persicae (Sulzer), feeding on Arabidopsis (Moran and Thompson, 2001). LOX H3 genes in potato regulate resistance to the beet armyworm, Spodoptera exigua (Hubner), and Colorado potato beetle, but the resistance is not regulated by JA production (Royo et al., 1999). The related enzyme hydroperoxide lyase plays a role in the resis-

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 159

Plant Resistance against Pests

tance of potato to the green peach aphid (Vancanneyt et al., 2001). In some plants, wounding also induces increased ethylene production, which blocks the JA signal but induces allene oxide synthase (AOS) production. Increased AOS levels induced by tobacco hornworm feeding are thought to help sustain JA production (Ziegler et al., 2001). Pathways involving jasmonates (JA and methyl jasmonate (MeJA)), ethylene (ET) and salicylic acid (SA) induce plant defences after insect attack, and some types of induced resistance are elicited by unknown and as yet unexplained types of elicitors. For example, both JA and ET induce the squash gene SLW-1 for resistance to feeding by the silverleaf whitefly, Bemisia argentifolii Bellows and Perring, but an additional gene (SLW-3) is regulated by an unknown elicitor (van de Ven et al., 2000). The majority of induced responses identified to date in plants resulting from insect attack involve the jasmonate pathway. Methyl JA-treated wheat plants produce increased amounts of the defensive compound hydroxamic acid and sustain reduced phloem ingestion by bird cherry oat aphid, Rhopalosiphum padi (L.), compared with control plants (Slesak et al., 2001). Methyl JAinduced accumulation of ferulic acid and phenolic polymers leads to cell-wall strengthening and increased insect resistance in barley and maize (Bergvinson et al., 1994; Lee et al., 1997). As cDNA library techniques have become employed, genes encoding specific defence compounds have been identified in the transcriptomes of insectchallenged plants of several families of plants. These include genes for a hevein-like protein (HEL) (Reymond et al., 2000), a metallopeptidase-like protein (SLW-1) (van de Ven et al., 2000), vegetative storage proteins (VSP1, 2) (Bell et al., 1995), a novel β-glucosidase gene (BGL1) (Stotz et al., 2002) and genes encoding the defensin peptide (PDF1.2), phenylalanine ammonia lyase (PAL1) and a monosaccharide symporter (STP4) (Moran and Thompson, 2001). SA promotes the development of systemic acquired resistance, a broad-range resistance against pathogens and some insects.


Hermsmeier et al. (2001) found that N. attenuata plants fed on by tobacco hornworm were strongly induced to produce high amounts of transcripts encoding the gene for α-dioxygenase (PIOX), a pathogen-inducible plant enzyme. The same plants expressed high levels of Thr deaminase (TD), a metabolic catalyst in the production of structural and chemical defences (Fig. 7.3). Interestingly, the results of Moran and Thompson (2001) also demonstrated that green peach aphid feeding on Arabidopsis induces major increases in the expression of the PR-1 and BGL2 genes, both of which are associated with the SA defence signalling pathway. In related defence signal ‘crosstalk’ studies, several authors have noted that defence responses induced by JA and ET may be antagonized by those induced by SA (Dong, 1998; Reymond and Farmer, 1998; Bostock, 1999; Pieterse and van Loon, 1999; Stotz et al., 2002). Herbivore-specific elicitors that induce plant defence responses have also been isolated from oral secretions of some lepidopterous larvae. These include the lytic enzyme β-glucosidase, isolated from salivary secretions of larvae of the imported cabbageworm, Pieris brassicae (Linnaeus) (Mattiacci et al., 1995) and fatty acid conjugates isolated from the larval regurgitant of the tobacco hornworm (Halitschke et al., 2001) and the beet armyworm (Alborn et al., 1997). In the tobacco hornworm–Arabidopsis interaction, the application of the caterpillar fatty acid conjugates to wounded leaf tissue elicits a JA burst and the production of volatile plant defence compounds (Turlings and Benrey, 1998; Halitschke et al., 2000, 2001). For additional discussion of the interactions between different plant-defence elicitors, readers are referred to the excellent reviews of Kessler and Baldwin (2001) and Heil and Bostock (2002). Elicitor-induced responses play a role in induced plant resistance to insects. However, JA-induced responses also lower plant fitness and reduce seed yields, suggesting that plants bred to respond with heightened levels of insect resistance when attacked may be counter-productive in relation to efficient crop production (Baldwin et al., 1997;

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 160


C.M. Smith

Baldwin, 1998). There are many gaps in the level and extent of knowledge about this exciting area of resistance-expression pathways. Additional research at both the biochemical and molecular levels will be critical to a better understanding of how different species of plants integrate separate and multiple elicitor signals generated as part of the defences against both insects and diseases.

Recommendations and Future Strategies Resistant cultivars have proved to be ecologically and socially acceptable to consumers and economically feasible for producers for over 100 years. Future insect-resistant crops will play a very important role in world sustainable agricultural systems, and the benefits of their use will become more prominent as world food needs increase, especially in the developing countries of the semi-tropics. In spite of their successful use in developed countries, the high level of Bt expression, similar to high doses of conventional pesticide or high levels of conventional gene expression, may promote the development of insects resistant to Bt crop plants. The longevity of Bt transgenes should be extended however, due to the advent of the use of IRM programmes centred on nontransgene refuges that allow the survival of hom*ozygous susceptible pest individuals. In addition, current Bt cultivars are based on the differences in only four active protein domains of toxin expression. This should be a concern of future plant-resistance research efforts, and strategies need to be developed that will allow the development and commercialization of transgenic plants containing non-Bt toxic proteins in IPM systems. Future insect-resistant (primarily transgenic) crop-development strategies and efforts need to address the growing need to increase food supplies for the populations of underdeveloped countries. Conventional resistancebreeding efforts have made strides to improve crops such as sorghum, millet, pigeon pea and chickpea during the past several decades. However, major corporate and public investments are urgently needed now to use conventional and molecular

methods to develop increased levels of insect resistance in these important food crops of the semi-arid tropics. There are hundreds of insect-resistance genes deployed in improved cultivars globally, but the continual evolution of virulent biotypes dictates the need for the identification of new sources of resistance and for MAS systems to identify and track these genes. The refinement and increased use of MAS techniques and MAS centres should be encouraged in order to accelerate the rate and accuracy of breeding crop plants for insect resistance. Our knowledge of how plants recognize insect-feeding attacks and the elicitors they produce in response to insect feeding is increasing rapidly. The evolving model of the differences in plant defence-response elicitors must be researched, challenged and modified to better understand induced resistance function and how plant metabolism can possibly be modified to use induced crop-plant resistance in insect pestmanagement programmes. There is also a great need for additional information about the sequence and function of expressed cDNAs unique to both resistant and susceptible plants under attack. The use of mRNA differential display and subtractive suppressive hybridization studies should be encouraged to accomplish this goal. In addition to the sequence information provided by unique cDNAs, they can be used to probe oligonucleotide macroand microarrays, in order to determine expressed resistance-gene function based on mRNA expression levels. The existence of RGAs in many crop plants suggests that current and future plantresistance researchers should increasingly utilize these genetic resources to provide in silico information about the location and function of candidate resistance genes. As a more complete knowledge (and eventual sequencing) of the genomes of additional crop plants develops, the use of genomic macro- and microarrays will also become valuable tools to answer questions about where resistance genes are located and what biochemical and biophysical gene products mediate their function.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 161

Plant Resistance against Pests

The ultimate goal of resistance-gene expression studies, genomic studies and MAS systems should be to identify plant genes that can be cloned and used to trans-


form crop plants for insect resistance in the same way that they have been transformed with Bt and other related transgenes toxic to insects.

References Abbott, E.A., Lucht, T., Jensen, J. and Jordan-Conde, Z. (2001) Handling of GM crop issues by the mass media. In: Proceedings Illinois Crop Protection Technology Conference. University of Illinois, Urbana, Illinois, pp. 11–12. Ahn, S.N., Anderson, J.A., Sorrells, M.E. and Tanksley, S.D. (1993) hom*oeologous relationships of rice, wheat and maize chromosomes. Molecular and General Genetics 241, 483–490. Alam, S.N. and Cohen, M.B. (1998) Detection and analysis of QTLs for resistance to the brown planthopper, Nilapavata lugens, in a doubled-haploid rice population. Theoretical and Applied Genetics 97, 1370–1379. Alborn, T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276, 945–949. Al-Deeb, M.A., Wilde, G.E. and Higgins, R.A. (2001) No effect of Bacillus thuringiensis corn and Bacillus thuringiensis on the predator Orius insidiosus (Say) (Hemiptera: Anthocoridae). Environmental Entomology 30, 625–629. American Phytopathological Society (APS) (1999) Threats to health reduced with Bt corn hybrids. Available at: http://www.scisoc. org/opae/media/btcorn.htm Anon. (2001) Corn and Biotechnology Special Analysis. National Agricultural Statistic Service, USDA, Washington, DC. Azzam, A., Azzam, S., Lhaloui, S., Amri, A., El Bouhssini, M. and Moussaoui, M. (1997) Economic returns to research in Hessian fly (Diptera: Cecidomyidae) resistant bread-wheat varieties in Morocco. Journal of Economic Entomology 90, 1–5. Baldwin, I.T. (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the USA 95, 8113–8118. Baldwin, I.T., Zhang, Z.-P., Diab, N., Ohnmeiss, T.E., McCloud, E.S., Lynds, G.Y. and Schmelz, E.A. (1997) Quantification, correlations and manipulation of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 210, 397–404. Bell, E., Creelman, R.A. and Mullet, J.E. (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 92, 8675–8679. Bergvinson, D.J., Arnason, J.T. and Pietrzak, L.N. (1994) Localization and quantification of cell wall phenolics in European corn borer resistant and susceptible maize inbreds. Canadian Journal of Botany 72, 1243–1249. Bostock, R.M. (1999) Signal conflicts and synergies in induced resistance to multiple attackers. Physiological and Molecular Plant Pathology 55, 99–109. Botha, A.M., Nagel, M.A.C., Van der Westhuizen, A.J. and Botha, F.C. (1998) Chitinase isoenzymes in near-isogenic wheat lines challenged with Russian wheat aphid, exogenois ethylene and mechanical wounding. Botanical Bulletin of the Academica Sinica 39, 99–106. Boyko, E.V., Gill, K.S., Mickelson-Young, L., Nasuda, S., Raupp, W.J., Ziegler, J.N., Singh, S., Hassawi, D.S., Fritz, A.K., Namuth, D., Lapitan, N.L.V. and Gill, B.S. (1999) A high-density genetic linkage map of Aegilops tauschii, the DS-genome progenitor of bread wheat. Theoretical and Applied Genetics 99, 16–26. Boyko, E.V., Kalendar, R., Korzun, V., Korol, A., Schulman, A. and Gill, B.S. (2002) A high density genetic map of Aegilops tauschii includes genes, retro-transposons, and microsatellites which provide unique insight into cereal chromosome structure and function. Plant Molecular Biology 48, 767–790. Brotman, Y., Silberstein, L., Kovalski, I., Perin, C., Dogimont, C., Pitrat, M., Klingler J., Thompson, G.A. and Perl-Treves, R. (2002) Resistance gene hom*ologues in melon are linked to genetic loci conferring disease and pest resistance. Theoretical and Applied Genetics 104, 1055–1063. Byrne, P., Ward, S., Harrington, J. and Fuller, L. (2003) Transgenic plants: an introduction and resource guide. Available at: html#stillbreaking

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 162


C.M. Smith

Cardinal, A.J., Lee, M., Sharopova, N., Woodman-Clikeman, W.L. and Long, M.J. (2001) Genetic mapping and analysis of quantitative tratit loci for resistance to stalk tunneling by the European corn borer in maize. Crop Science 41, 835–845. Carrière, Y., Ellers-Kirk, C., Sisterson, M., Antilla, L., Whitlow, M., Dennehy, T.J. and Tabashnik, B.E. (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proceedings of the National Academy of Sciences of the USA 100, 1519–1523. Castro, A.M., Worland, A., Vasicek, A., Clua, A.A., Gimenez, D., Ellerbrook, C. and Tacaliti, M.S. (2001) Mapping a QTL involved with greenbug and Russian wheat aphid resistance. In: Proceedings 4th International Triticeae Symposium. Consejenia de Agricultura y Pesca, Cordoba, Spain, pp. 345–349. Cevik, V. and King, G.L. (2002) High-resolution genetic analysis of the Sd-1 aphid resistance locus in Malus spp. Theoretical and Applied Genetics 105, 346–354. Chesnokov, P.G. (1953) Methods of Investigating Plant Resistance to Pests. National Science Foundation, Washington, DC (Israel Program for Scientific Translation). Cregan, P., Jarvik, T., Bush, A.L., Shoemaker, R.C., Lark, K.G., Kahler, A.L., Kaya, N., VanToai, T.T., Lohnes, D.G., Chung, J. and Specht, J.E. (1999) An integrated genetic linkage map of the soybean genome. Crop Science 39, 1464–1490. Cuperus, G.W., Kendall, P., Rehe, S., Frisbee, R., Hall, K., Bruhn, C., Deer, D., Woods, F., Branthaver, B., Weber, G., Poli, B., Buege, D., Linker, M., Andress, E., Wintersteen, W., Dost, F., Hegley, F., Aselhage, J., Stelltflug, L., Doe, R. and Murray, G. (1991) Integration of Food Safety and Water Quality Concepts Throughout the Food Production, Processing and Distribution Educational Programs using HACCP Philosophies. Circular E-903, Cooperative Extension Service, Oklahoma State University, Stillwater. Daly, J.C. and Wellings, P.W. (1996) Ecological constraints to the deployment of arthropod resistant crop plants: a cautionary tale. In: Floyd, R.B., Shepard, A.W. and De Barro, P.J. (eds) Frontiers of Population Ecology. CSIRO Publishing, Melbourne, pp. 311–323. Dhaliwal, G.S. and Dilawari, V.K. (eds) (1993) Advances in Host Plant Resistance to Insects. Kalyani Publishers, New Delhi. Dhaliwal, G.S. and Singh, R. (eds) (2004) Host Plant Resistance to Insects: Concepts and Applications. Panima Publishing Corporation, New Delhi. Dong, X. (1998) SA, JA, ethylene, and disease resistance in plants. Current Opinions in Plant Biology 1, 316–323. Dubcovsky, J., Lukaszewski, A.J., Echaide, M., Antonelli, E.F. and Porter, D.R. (1998) Molecular characterization of two Triticum speltoides interstitial translocations carrying leaf rust and greenbug resistance genes. Crop Science 38, 1655–1660. Eddleman, B.R., Chang, C.C. and McCarl, B.A. (1999) Economic benefits from grain sorghum variety improvement in the United States. In: Wiseman, B.R. and Webster, J.A. (eds) Economic, Environmental, and Social Benefits of Resistance in Field Crops. Thomas Say Publications, Entomological Society of America, Lanham, Maryland, pp. 17–44. Feuillet, C. and Keller, B. (1999) High genome density is conserved at syntenic loci of small and large grass genomes. Proceedings of the National Academy of Sciences of the USA 96, 8265–8270. Fidantsef, A.L., Stout, M.J., Thaler, J.S., Duffey, S.S. and Bostock, R.M. (1999) Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology 54, 97–114. Forslund, K., Perrersson, J., Bryngelsson, T. and Jonnson, L. (2000) Aphid infestation induces PR-proteins differentially in barley susceptible or resistant to the birdcherry-oat aphid. Physiologia Plantarum 110, 496–502. Gaskell, G., Bauer, M.W., Durant, J. and Allum, N.C. (1999) Worlds apart? The reception of genetically modified foods in Europe and the U.S. Science 285, 384–387. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726. Graham, M.A., Marek, L.F., Lohnes, D., Cregan, P. and Shoemaker, R. (2000) Expression and genome organization of resistance gene analogs in soybean. Genome 43, 86–90. Halitschke, R., Kessler, A., Kahl, J., Lorenz, A. and Baldwin, I.T. (2000) Ecophysiological comparison of direct and indirect defences in Nicotiana attenuata. Oecologia 124, 408–417. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty amino-acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiology 125, 711–717.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 163

Plant Resistance against Pests


Heil, M. and Bostock, R.M. (2002) Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Annals of Botany 89, 503–512. Hermsmeier, D., Schittko, U. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth-and defence-related plant mRNAs. Plant Physiology 125, 683–700. Hernández, P., Dorado, G., Prieto, P., Giménez, M.J., Ramírez, M.C., Laurie, D.A., Snape, J.W., and Martín, A. (2001) A core genetic map of Hordeum chilense and comparisons with maps of barley (Hordeum vulgare) and wheat (Triticum aestivum). Theoretical and Applied Genetics 102, 1259–1264. Huang, F., Higgins, R.A. and Buschman, L.L. (1999) Transgenic Bt-plants: successes, challenges, and strategies. Pestology 23, 2–29. Huang, N., Parco, A., Mew, T., Magpantay, G., McCouch, S., Guiderdoni, E., Xu, J.C., Subudhi, P., Angeles, E.R. and Khush, G.S. (1997) RFLP mapping of isozymes, RAPD and QTLs for grain shape, brown planthopper resistance in a doubled haploid rice population. Molecular Breeding 3, 105–113 Huang, Z., He, G., Shu, L., Li, X. and Zhang, Q. (2001) Identification and mapping of two brown planthopper resistance genes in rice. Theoretical and Applied Genetics 102, 929–934. Hwang, C.F., Bhakta, A.V., Truesdell, G.M., Pudlo, W.M. and Williamson, V.M. (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12, 1319–1329. International Food Information Council (IFIC) (2002) U.S. consumer attitudes toward food biotechnology survey: 23 September, 2002. Available at: pdf James, C. (2000) Global Status of Commercialized Transgenic Crops. ISAAA, Briefs 21, Preview. ISAAA Ithaca, NY. Available at: Jampatong, C., McMullen, M.D., Barry, D.B., Darrah, L.L., Byrne, P.F. and Kross, H. (2002) Quantitative trait loci for first- and second-generation European corn borer resistance derived from the maize inbred Mo47. Crop Science 41, 584–593. Johnson, M.T. and Gould, F. (1992) Interaction of genetically engineered host plant resistance and natural enemies of Heliothis virescens (Lepidoptera: Noctuidae) in tobacco. Environmental Entomology 21, 586–597. Kaloshian, I., Lange, W.H. and Williamson, V.M. (1995) An aphid-resistance locus is tightly linked to the nematode-resistance gene, Mi, in tomato. Proceedings of the National Academy of Sciences of the USA 92, 622–625. Kaloshian, I., Kinser, M.G., Ullman, D.E. and Williamson, V.M. (1997) The impact of Meu1-mediated resistance in tomato on longevity, fecundity, and behaviour of the potato aphid, Macrosiphum euphorbiae. Entomologia Experimentalis et Applicata 83, 181–187. Katiyar, S.K., Tan, Y., Huang, B., Chandel, G., Xu, Y., Zhang, Y., Xie, Z. and Bennett, J. (2001) Molecular mapping of gene Gm-6(t) which confers resistance against four biotypes of Asian rice gall midge in China. Theoretical and Applied Genetics 103, 953–961. Katsar, C.S., Paterson, A.H., Teetes, G.L. and Peterson, G.C. (2002) Molecular analysis of sorghum resistance to the greenbug (hom*optera: Aphididae). Journal of Economic Entomology 95, 448–457. Kessler, A. and Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144. Khush, G.S. and Brar, D.S. (1991) Genetics of resistance to insects in crop plants. Advances in Agronomy 45, 223–274. Kirsten, J. and Gouse, M. (2002) Bt cotton in South Africa: adoption and impact on farm incomes amongst small- and large-scale farmers. ISB News Report. Available at: http://www.isb. Knight, J. (2003) Agency ignoring its advisers over Bt maize. Nature 422, 5. Korzun, V., Malyshev, S., Voylokov, A.V. and Börner, A. (2001) A genetic map of rye (Secale cereale L.) combining RFLP, isozyme, protein, microsatellite and gene loci. Theoretical and Applied Genetics 102, 709–717. Kretshmer, J.M., Chalmers, K.J., Manning, S., Karakousis, A., Barr, A.R., Islam, M.R., Logue, S.J., Choe, Y.W., Barker, S.J., Lance, R.C.M. and Langridge, P. (1997) RFLP mapping of the Ha2 cereal cyst nematode resistance gene in barley. Theoretical and Applied Genetics 94, 1060–1064. Lagudah, E.S., Moullet, O. and Appels, R. (1997) Map-based cloning of a gene sequence encoding a nucleotide binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome 40, 659–665.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 164


C.M. Smith

Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. (1987) MAPMAKER: an interactive computer package for constructing primary genetic maps of experimental and natural populations. Genomics 1, 174–181. Lara, F.M. (1979) Principios de Resistancia de Plantas a Insectos – (in Portugese). Piracicaba, Livroceres, Brazil. Lawrence, P.K. and Koundal, K.R. (2002) Plant protease inhibitors in control of phytophagous insects. Electronic Journal of Biotechnology 5, 15 April. Available at: content/vol5/issue1/full/3/index.html Lee, J.E., Vogt, T., Hause, B. and Lëbler, M. (1997) Methyl jasmonate induces an O-methyltransferase in barley. Plant Cell Physiology 38, 851–862. Leister, D., Kurth, J., Laurie, D.A., Yano, M., Sasaki, T., Graner, A. and Schulze-Lefert, P. (1999) RFLP- and physical mapping of resistance gene hom*ologues in rice (O. sativa) and barley (H. vulgare). Theoretical and Applied Genetics 98, 509–520. Li, W.L., Faris, J.D., Chitmoor, J.M., Leach, J.F., Hulbert, S.H., Liu, D.J., Chen, P.D. and Gill, B.S. (1999) Genomic mapping of defence response genes in wheat. Theoretical and Applied Genetics 98, 226–233. Liu, X.M., Smith, C.M., Gill, B.S. and Tolmay, V. (2001) Microsatellite markers linked to six Russian wheat aphid resistance genes in wheat. Theoretical and Applied Genetics 102, 504–510. Liu, X.M., Smith, C.M. and Gill, B.S. (2002) Mapping of microsatellite markers linked to the Dn4 and Dn6 genes expressing Russian wheat aphid resistance in wheat. Theoretical and Applied Genetics 104, 1042–1048. Llewellyn, D., Cousins, Y., Mathews, A., Hartweck, L. and Lyon, B. (1994) Expression of Bacillus thuringensis insecticidal protein genes in transgenic crop plants. Agriculture, Ecosystems & Environment 49, 85–93. Losey, J.E., Rayor, L.S. and Carter, M.E. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214. Mago, R., Nair, S. and Mohan, M. (1999) Resistance gene analogues from rice: cloning, sequencing and mapping. Theoretical and Applied Genetics 99, 50–57. Mattiacci, L., Dicke, M. and Posthumas, M.A. (1995) Beta-glucosidase – an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences of the USA 92, 2036–2040. Maxwell, F.G. and Jennings, P.R. (1980) Breeding Plants Resistant to Insects. John Wiley & Sons, New York. Miller, C.A., Altinkut, A. and Lapitan, N.L.V. (2001) A microsatellite marker for tagging Dn2, a wheat gene conferring resistance to the Russian wheat aphid. Crop Science 41, 1584–1589. Milligan, S., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V. (1998) The root-knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10, 1307–1319. Moharramipour, S., Tsumki, H., Sato, K. and Yoshida, H. (1997) Mapping resistance to cereal aphids in barley. Theoretical and Applied Genetics 94, 592–596. Moran, P.J. and Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defence pathways. Plant Physiology 125, 1074–1085. Moreira, L.A., Mollema, C. and van Heusden, S. (1999) Search for molecular markers linked to Liriomyza trifolii resistance in tomato. Euphytica 109, 149–156. Mullis, K. (1990) The unusual origin of the polymerase chain reaction. Scientific American April, 262, 56–65. Murai, H., Hashimoto, Z., Sharma, P.N., Shimizu, T., Murata, K., Takumi, S., Mori, N., Kawasaki, S. and Nakamura, C. (2001) Construction of a high resolution linkage map of a rice brown planthopper (Nilaparvata lugens Stal) resistance gene bph2. Theoretical and Applied Genetics 103, 526–532. Narvel, J.A., Walker, D.R., Rector, B.G., All, J.N., Parrott, W.A. and Boerma, R. (2001) A retrospective DNA marker assessment of the development of insect resistant soybean. Crop Science 41, 1931–1939. Nieto-Lopez, R.M. and Blake, T.K. (1994) Russian wheat aphid resistance in barley: inheritance and linked molecular markers. Crop Science 34, 655–659. Oppert, B.S. (2001) Transgenic plants expressing enzyme inhibitors and the prospects for biopesticide development. In: Koul, O. and Dhaliwal, G.S. (eds) Phytochemical Biopesticides. Harwood Academic Publishers, Amsterdam, pp. 83–95. Painter, R.H. (1951) Insect Resistance in Crop Plants. University of Kansas Press, Lawrence, Kansas. Panda, N. (1979) Principles of Host-Plant Resistance to Insect Pests. Allanheld, Osmun & Co. and Universe Books, New York. Panda, N. and Khush, G.S. (1995) Host Plant Resistance to Insects. CAB International, Wallingford, UK. Pani, J. and Sahu, S.C. (2000) Inheritance of resistance against biotype 2 of the Asian rice gall midge, Orseolia oryzae. Entomologia Experimentalis et Applicata 95, 15–19.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 165

Plant Resistance against Pests


Paterson, A., Lin, Y.-R., Li, Z., Scherta, K.F., Doebley, J.F., Pinson, S.R.M., Liu, S.-C., Stansel, J.W. and Irvine, J.E. (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269, 1714–1718. Pieterse, C.M and van Loon, L.C. (1999) Salicylic acid-independent plant defence pathways. Trends in Plant Science 4, 52–58. Pilcher, C.D., Obrycki, J.J., Rice, M.E. and Lewis, L.C. (1997) Preimaginal development, survival, field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environmental Entomology 26, 446–454. Pimentel, D.S. and Raven, P.H. (2000) Bt corn pollen impacts on nontarget Lepidoptera: assessment of effects in nature. Proceedings of the National Academy of Sciences of the USA 97, 8198–8199. Qaim, M. and Zilberman, D. (2003) Yield effects of genetically modified crops in developing countries. Science 299, 900–902. Ratcliffe, R.H. and Hatchett, J.H. (1997) Biology and genetics of the Hessian fly and resistance in wheat. In: Bobdari, K. (ed.) New Developments in Entomology. Research Signpost, Scientific Information Guild, Trivandrum, pp. 47–67. Rector, B.G., All, J.N., Parrott, W.A. and Boerma, H.R. (1998) Identification of molecular markers linked to quantitative trait loci for soybean resistance to corn earworm. Theoretical and Applied Genetics 96, 786–790. Rector, B.G., All, J.N., Parrott, W.A. and Boerma, H.R. (2000) Quantitative trait loci for antibiosis resistance to corn earworm in soybean. Crop Science 40, 233–238. Renganayaki, K., Fritz, A.K., Sadasivam, S., Pammi, S., Harrington, S.E., McCouch, S.R., Kumar, S.M. and Reddy, A.S. (2002) Mapping and progress toward map-based cloning of brown planthopper biotype-4 resistance gene introgressed Oryza officinalis into cultivated rice, O. sativa. Crop Science 42, 2112–2117. Reymond, P. and Farmer, E.E. (1998) Jasmonate and salicylate as global signals for defence gene expression. Current Opinions in Plant Biology 1, 404–411. Reymond, P., Weber, H., Damond, M. and Farmer, E.E. (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707–719. Rice, M.E. and Pilcher, C.D. (1998) Potential benefits and limitations of transgenic Bt corn for management of the European corn borer (Lepidoptera: Crambidae). American Entomologist 44, 75–78. Rissler, J. and Mellon, M. (1996) The Ecological Risks of Engineered Crops. MIT Press, Cambridge, Massachusetts. Roberts, P.A. and Thomason, I.J. (1986) Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease 70, 547–551. Royo, E., Leon, J., Vancanneyt, G., Albar, J.P., Rosahl, S., Ortego, F., Castanera, P. and Sanchez-Serrano, J.J. (1999) Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests. Proceedings of the National Academy of Sciences of the USA 96, 1146–1151. Rossi, M., Goggin, F.L., Milligan, S.B., Klaoshian, I., Ullman, D.E. and Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the USA 95, 9750–9754. Russell, G.E. (1978) Plant Breeding for Pest and Disease Resistance. Butterworth Publishers, Boston, Massachusetts. Sachs, E.S., Benedict, J.H., Taylor, J.F., Stelly, D.M., Davis, S.K. and Altman, D.W. (1996) Pyramiding CryIA(b) insecticidal protein and terpenoids in cotton to resist tobacco budworm (Lepidoptera: Noctuidae). Environmental Entomology 25, 1257–1266. Sardesai, N., Kumar, A., Rajyashri, K.R., Nair, S. and Mohan, M. (2001) Identification and mapping of an AFLP marker linked to Gm7, a gall midge resistance gene and its conversion to a SCAR marker for its utility in marker aided selection in rice. Theoretical and Applied Genetics 105, 691–698. Seah, S., Sivasithamparam, K., Karalousis, A. and Lagudah, E.S. (1998) Cloning and characterisation of a family of disease resistance gene analogs from wheat and barley. Theoretical and Applied Genetics 97, 937–945. Sears, M.K., Hellmich, R.L., Stanley-Horn, D.E., Oberhauser, K.S., Pleasants, J.M., Mattila, H.R., Siegfried, B.D. and Dively, G.P. (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proceedings of the National Academy of Sciences of the USA 98, 11937–11942. Service, R.F. (2001) Arson strikes research labs and tree farm in Pacific Northwest. Science 292, 1622–1623.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 166


C.M. Smith

Sharma, H.C., Sharma, K.K., Seetharama, N. and Ortiz, R. (2000) Prospects for using transgenic resistance to insects in crop improvement. Electronic Journal of Biotechnology 3, 15 August. Available at: Sharopova, N., McMullen, M.D., Schultz, L., Schroeder, S., Sanchez-Villeda, H., Gardiner, J., Bergstrom, D., Houchins, K., Melia-Hanco*ck, S., Musket, T., Duru, N., Polacco, M., Edwards, K., Ruff, T., Register, J.C., Brouwer, C., Thompson, R., Velasco, R., Chin, E., Lee, M., Woodman-Clikeman, W., Long, M.J., Liscum, E., Cone, K., Davis, G. and Coe, E.H. Jr (2002) Development and mapping of SSR markers for maize. Plant Molecular Biology 48, 463–481. Shen, K.A., Meyers, B.C., Islam-Faridi, M.N., Chin, D., Stelly, D.M. and Michelmore, R.W. (1998) Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Molecular Plant–Microbe Interaction 11, 815–823. Slesak, E., Slesak, M. and Gabrys, B. (2001) Effect of methyl jasmonate on hydroxamic acid, protease activity, and bird cherry-oat aphid Rhoplaosiphum padi L. probing behavior. Journal of Chemical Ecology 12, 2529–2543. Smith, C.M. (1989) Plant Resistance to Insects – A Fundamental Approach. John Wiley & Sons, New York. Smith, C.M. (1999) Plant resistance to insects. In: Rechcigl, J. and Rechcigl, N. (eds) Biological and Biotechnological Control of Insects. Lewis Publishers, Boca Raton, Florida, pp. 171–205. Smith, C.M., Khan, Z.R. and Pathak, M.D. (1994) Techniques for Evaluating Insect Resistance in Crop Plants. Lewis Publishers, Boca Raton, Florida. Smith, C.M., Quisenberry, S.S. and du Toit, F. (1999) The value of conserved wheat germplasm possessing arthropod resistance. In: Clement, S.L. and Quisenberry, S.S. (eds) Global Plant Genetic Resources for Insect Resistant Crops. CRC Press, Boca Raton, Florida, pp. 25–49. Snelling, R.O. (1941) Resistance of plants to insect attack. Botany Reviews 7, 543–586. Speulman, E., Bouchez, D., Holub, E. and Beynon, J.L. (1998) Disease resistance gene hom*ologs correlate with disease resistance loci of Arabidopsis thaliana. Plant Journal 14, 467–474. Stanley-Horn, D.E., Dively, G.P., Hellmich, R.L., Mattila, H.R., Sears, M.K., Rose, R., Jesse, L.C.H., Losey, J.E., Obrycki, J.J. and Lewis, L. (2002) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proceedings of the National Academy of Sciences of the USA 98, 11931–11936. Staub, J.E., Serquen, F.C. and Gupta, M. (1996) Genetic markers, map construction, and their application in plant breeding. HortScience 31, 729–741. Stotz, H.U., Pittendrigh, B.R., Kroyman, J., Weniger, K., Fritsche, J., Bauke, A. and Mitchell-Olds, T. (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptain cotton worm but not diamond back moth. Plant Physiology 124, 1007–1017. Stotz, H.U., Koch, T., Biedermann, A., Weniger, K., Boland, W. and Mitchell-Olds, T. (2002) Evidence for regulation of resistance in Arabidopsis to Egyptian cotton worm by salicylic and jasmonic acid signaling pathways. Planta 214, 648–652. Stout, M.J., Fidantsef, A.L., Duffey, S.S. and Bostock, R.M. (1999) Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopsericon esculentum. Physiological and Molecular Plant Pathology 54, 115–130. Tada, T. (1999) PCR-amplified resistance gene analogs link to resistance loci in rice. Breeding Science 49, 267–273. Tamura, K., f*ckuta, Y., Hirae, M., Oya, S., Ashikawa, I. and Yagi, T. (1999) Mapping of the Grh1 locus for green rice leafhopper resistance in rice using RFLP markers. Breeding Science 49, 11–14. Tanaka, K. (1999) Quantitative genetic analysis of biotypes of the brown planthopper Nilaparvata lugens: heritability of virulence to resistant rice varieties. Entomologia Experimentalis et Applicata 90, 279–287. Turlings, T.C.J. and Benrey, B. (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. EcoScience 5, 321–333. Vancanneyt, G., Sanz, C., Farmaki, T., Paneque, M., Ortego, F., Castañera, P. and Sánchez-Serrano, J. (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proceedings of the National Academy of Sciences of the USA 98, 8139–8144. van de Ven, W.T.G., LeVesque, C.S., Perring, T.M. and Walling, L.L. (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12, 1409–1424. Van Sanford, D.V., Anderson, J., Campbell, K., Costa, J., Cregan, P., Griffey, C., Hayes, P. and Ward, R. (2001) Discovery and deployment of molecular markers linked to fusarium head blight resistance: an integrated system for wheat and barley. Crop Science 41, 638–644.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 167

Plant Resistance against Pests


Vos, P., Hogers, R., Bleeker, M., Rijans, M., Van de Lee, T., Hornes, M., Frijters, A., Pot, J., Kuiper, M. and Zabeau, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414. Vos, P., Simons, G., Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J., Diergaarde, P., Reijans, M., Fierens-Onstenk, J., de Both, M., Peleman, J., Liharska, T., Hontelez, J. and Zabeau, M. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 16, 1315–1316. Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulators 19, 195–216. Wang, Y.H., Garvin, D.F. and Kochian, L.V. (2001) Nitrate-induced genes in tomato roots: array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiology 127, 345–359. Wayland, S., Mulkey, M., Johnson, S., Green, J., Kearnes, D., Barnes, D., Ellis, V., Anderson, J., Hutton, P. and Dorsey, L. (1998) The Environmental Protection Agency’s White Paper on Bt Plant-pesticide Resistance Management. US Environmental Protection Agency, Washington, DC, 84 pp. Weng, Y. and Lazar, M.D. (2002) Amplified fragment length polymorphism- and simple sequence repeatbased molecular tagging and mapping of greenbug resistance gene Gb3 in wheat. Plant Breeding 121, 218–223. Willcox, M.C., Khairallah, M.M., Bergvinson, D., Crossa, J., Deutsch, J.A., Edmeades, G.O., Gonzalez-deLeon, D., Jiang, C., Jewell, D.C., Mihm, J.A., Williams, W.P. and Hoisington, D. (2002) Selection for resistance to southwestern corn borer using marker-assisted selection and conventional backcrossing. Crop Science 42, 1516–1528. Winz, R.A. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating N-methyltransferase transcripts. Plant Physiology 125, 2189–2202. Wraight, C.L., Zangerl, A.R., Carroll, M.J. and Berenbaum, M.R. (2000) Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proceedings of the National Academy of Sciences of the USA 97, 7700–7703. Xu, X.F., Mei, H.W., Luo, L.J., Cheng, X.M. and Li, Z.K. (2002) RFLP-facilitated investigation of the quantitative resistance of rice to brown planthopper (Nilaparvata lugens). Theoretical and Applied Genetics 104, 248–253. Yencho, G.C., Cohen, M.B. and Byrne, P.F. (2000) Applications of tagging and mapping insect resistance loci in plants. Annual Review of Entomology 45, 393–422. Ziegler, J., Keinanen, M. and Baldwin, I.T. (2001) Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry 58, 729–738.

07IntpestManCh7.QXD 14/4/04 2:25 pm Page 168

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 169


The Pesticide Paradox in IPM: Risk–Benefit Analysis

Paul Guillebeau Department of Entomology, University of Georgia Cooperative Extension Service, Athens, GA 30602, USA E-mail: [emailprotected]

Introduction By definition, integrated pest management (IPM) combines a variety of tactics into a comprehensive system to manage pest populations. As much as possible, it is important to use components that are compatible with one another. Otherwise, the pest-management programme may become overly reliant on a single tactic. Such a programme is not IPM, and the strategy carries greater risks. The failure of a single tactic may allow a rapid increase in the pest population. In a truly integrated programme, the failure of a single component is less likely to be catastrophic because pest populations are controlled through a variety of techniques. Pesticides are one of the tools available to IPM practitioners, and many pest-management programmes depend on the efficient use of pesticides. Unfortunately, some pesticides impair or eliminate other components of an IPM system. This occurs most commonly when broad-spectrum insecticides destroy populations of beneficial arthropods. The primary pest population may rebound or secondary pests may become a problem. In many situations, a marketable product cannot be produced economically without pesticides, but the focus of modern pest control is IPM. This chapter discusses the role of

pesticides in IPM programmes; situations that result in incompatibility; and ways to better incorporate pesticides into an IPM system.

Integrated pest management and pesticides, defining the terms A number of people consider pesticides and IPM to be incompatible. In many ways, however, this apparent paradox is a function of the broad and dynamic definitions of both ‘pesticide’ and ‘integrated pest management’. The Environmental Protection Agency (EPA) regulates pesticides in the USA; the Agency defines a pesticide as ‘any substance or mixture of substances intended for preventing, destroying, repelling, or mitigating any pest’ (US EPA, 2002b). This definition comprises many highly toxic, broadspectrum chemicals, but it also includes materials with a non-toxic mode of action, such as pheromones. Likewise, IPM is broadly defined, and the definition has changed substantially over the last few decades. The idea of integrated control is generally credited to Hoskins et al. (1939). They stated: [B]iological and chemical control are considered … as the two edges of the same sword … nature’s own balance provides the major part

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


08IntpestManCh8.QXD 14/4/04 2:25 pm Page 170


P. Guillebeau

of protection … insecticides should be used so as to interfere with natural control of pests as little as possible.

This definition sounds much like some current definitions discussed below, but one must remember that Hoskins et al. practised pest management before the era of modern pesticides. Because the pesticides available at that time had limited value in many situations, pest management relied more heavily on non-chemical options. By the 1960s, definitions of IPM reflected the use of more effective pesticides: Integrated control is a pest population management system that utilizes all suitable techniques either to reduce pest populations and maintain them at levels below those causing economic injury or to so manipulate the populations that they are prevented from causing such injury. (Smith and Van den Bosch, 1967)

The focus of IPM was agricultural efficiency and avoiding economic losses, both strong incentives for grower acceptance of IPM. Two decades later, Flint and van den Bosch (1981) published a definition that acknowledged the role of pesticides while making it clear that chemicals should be the secondary line of defence: IPM is an ecologically based pest control strategy that relies heavily on natural mortality factors … and seeks out control tactics that disrupt these factors as little as possible. IPM uses pesticides, but only after systematic monitoring of pest populations and natural control factors indicates a need.

By the 1990s, the reduction of pesticide use had become a basic tenet of IPM definitions: Integrated pest management, or IPM, is an approach to pest control that utilizes regular monitoring to determine if and when treatments are needed and employs physical, mechanical, cultural, biological and educational tactics to keep pest numbers low enough to prevent intolerable damage or annoyance. Least-toxic chemical controls are used as a last resort. (Olkowski and Daar, 1991)

In 1993, the EPA, the US Department of Agriculture (USDA), and the US Food and Drug Administration (FDA) pledged to have

75% of the US agricultural acreage under IPM by the year 2000 and to reduce the use of pesticides (US EPA, 2002a). A government report criticized IPM because there has been no significant reduction in the use of pesticides in US agriculture (US Congress Office of Technology Assessment, 1995). Part of the criticism may be an artefact of the imprecise measurement of IPM adoption. Monitoring and application thresholds are key elements of most IPM definitions, and these parameters have been commonly used to measure IPM adoption (Vandeman et al., 1994). This method of measuring IPM provides little information about the intensity of pesticide application. Because of the myriad definitions of IPM and the apparent lack of pesticide reduction, some authors have suggested new terms. Frisbie and Smith (1991) proposed ‘biointensive IPM’ with its focus on biological controls, host-plant resistance and cultural controls. Likewise, the National Research Council (1996) published a report on Ecologically Based Pest Management that would mitigate environmental, economic and safety risks. New terms have limited value, however, because these same concepts are expressed in many of the earlier definitions for IPM. Although groups differ in their interpretations, IPM remains a useful compromise between environmental/human-health advocacy groups and industries that may need chemicals to manage out-of-control pest populations. Additionally, modern practitioners agree that pesticides must be used judiciously if biological control is to play a significant role in IPM. In this context, the working definition of IPM includes the goal of reducing pesticide risks to non-target organisms, rather than focusing strictly on reducing pesticide use. Beyond that point, however, generalizations about pesticides and IPM are of limited value. The impact of pesticides in a particular situation depends on the pesticide, the pest and the management situation. Ironically, widespread application of an organophosphate insecticide made possible the greatest reduction of pesticide use and concomitant increase in biological control for an IPM programme.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 171

Risk–Benefit Analysis of Pesticides

Pesticides and Cotton IPM The boll-weevil invasion was the beginning of a pesticide treadmill for cotton that lasted for more than 50 years. By 1917, every Georgia county that produced cotton reported bollweevils (Hunter, 1917), and cotton yields had already decreased by 32% compared with pre-weevil production (Anon., 1917; Floyd and Treanor, 1944). In 1920, cotton growers across the South applied 10 million lb. of calcium arsenate to control boll-weevil (Coad, 1920). Growers in 1940 were advised to apply calcium arsenate based on a threshold of weevil infestation. Even with a threshold, cotton growers in Georgia alone applied 1.5 million lb. of calcium arsenate (Anon., 1940). Organophosphate insecticides were introduced for boll-weevil control in the 1950s (Rainwater and Gaines, 1951). By 1968, cotton growers in the South were applying from ten to 18 treatments of insecticides per season (Martin et al., 1968). Boll-weevil was a major target; however, growers were also using multiple pesticide applications to control other pests, primarily the bollworm complex, namely, Helicoverpa zea (Boddie) and Heliothis virescens (Fabricius) (Haney et al., 2001). Numerous arthropod predators and parasitoids attack bollworms (Whitcomb and Bell, 1964); cotton was clearly on a pesticide treadmill as bollworm populations were released from biological controls by earlyseason sprays. Cotton production in the southern USA remained heavily dependent on insecticides until the boll-weevil eradication programme. Intense pesticide application was a key element of the boll-weevil eradication programme (Haney et al., 2001). In 1987, the Georgia programme added an average of 8.4 treatments per acre of azinphos-methyl to the normal in-season spray schedule. In total, more than 287,000 lb. of azinphosmethyl was applied. In 1988 and 1989, each cotton acre received an average of 9.1 and 12.4 additional applications, respectively, of malathion; nearly 350,000 lb. of malathion was applied each year. After the first 3 years, pesticide applications to control boll-weevil dropped substantially. In 1990, the average number of


pesticide applications to control boll-weevil had fallen to 2.7; in 1991, the average number of applications was 0.5. By 1996, pesticide applications were no longer made to control boll-weevil except for spot treatments made when boll-weevils were detected in traps (Haney et al., 2001). The overall pesticide reductions associated with boll-weevil eradication are enormous. In 1971, growers applied 73 million lb. of insecticide active ingredient (Ridgeway et al., 1983) to 11.5 million acres of cotton in the USA (Anon., 1993), with an average of 6.8 lb. of active ingredient per acre. In 1992, 20 million lb. of insecticide active ingredient was applied to 11.1 million acres of cotton (Anon., 1993; Gianessi and Anderson, 1995), or 1.8 lb. of active ingredient per acre. The average number of insecticide applications per acre in Georgia dropped from 16.5 from 1987 to 1992 to less than 3.5 from 1993 to 1999 (Haney et al., 2001). The eradication of boll-weevil allowed cotton farmers to place greater emphasis on biological control agents. Prior to boll-weevil eradication, the economic impact (yield losses + cost of control) of Spodoptera exigua (Hubner) in Georgia averaged nearly 2% of the cotton crop’s value (Haney et al., 2001). During the pesticide-intensive eradication period, the economic impact of S. exigua increased to nearly 7%. Since the boll-weevil programme ended, the economic impact has remained at less than 1% (Haney et al., 2001). Ruberson et al. (1994) concluded that the pesticidal disruption of biological controls was a key factor in the outbreaks of this typically minor and sporadic pest. The IPM advantages of boll-weevil eradication are also clear for major cotton pests like bollworms, H. zea and H. virescens. Before boll-weevil eradication, annual economic losses from these two pests averaged more than 26% of the cotton value in Georgia. After boll-weevil eradication, the economic impact of bollworms fell to approximately 8.5% annually (Haney et al., 2001). A key reason for this decline is the abundance of natural control agents that attack bollworms; until the eradication programme, insecticides applied for boll-weevil also eliminated most biocontrol agents.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 172


P. Guillebeau

Pesticides and Biological Controls Every pesticide is compatible with some other IPM techniques. Pesticide applications do not preclude cultural controls, such as ploughing, host-plant resistance or physical barriers, such as screens or mesh. As the definition and techniques of IPM have evolved, however, there is greater emphasis on biological control organisms. Currently, biological control relates chiefly to the management of insects although there are examples of biological control agents for weeds and plant diseases.

Pesticides and biological control of insects Many pesticides have broad-spectrum activity against a variety of insects. A 1956 review of the literature found a large number of studies that discuss the effects of pesticides on populations of beneficial arthropods (Ripper, 1956). Similar reports throughout the years have demonstrated that insecticides can devastate populations of beneficial insects (Turnipseed et al., 1975; Wilkenson et al., 1979; Roach and Hopkins, 1981). However, even the impact of broadspectrum insecticides is unpredictable. Predator resistance to pesticides has been documented and even selected in some situations. Guillebeau and All (1989) noted similar-sized populations of striped lynx spider, Oxyopes salticus Hentz, in control plots and plots treated with the organophosphate insecticide, methyl parathion. Redmond and Brazzel (1968) reported methyl-parathion resistance in populations of O. salticus in an area with a long history of methyl-parathion use. Predatory mites have been selected in laboratory and field trials for resistance to a variety of pesticides, including carbamates and organophosphates (Croft and Stickler, 1983; Hoy, 1985). Trials with other predators have not produced stable resistance at levels that are valuable for field application (Adams and Cross, 1967; Grafton-Cardwell and Hoy, 1986). Other studies reported predator/parasitoid tolerance of some non-selective insecticides even when resistance was not

suspected. In a pecan study, pyrethroids were not toxic to larvae and adult stages of the predatory lacewing, Chrysoperla rufilabris (Bermeister), but organophosphates and carbamates were (Mizzell and Schiffhauer, 1990). Conversely, pyrethroids were toxic to the predatory lady beetle, Olla v-nigrum Say, but the organophosphates phosalone, methidathion, ethion and malathion were relatively non-toxic. All of the pyrethroids and the organophosphates tested were toxic to another lady beetle, Hippodamia convergens (Guerin-Meneville), but lindane was not. The impacts upon beneficial populations vary even within a single class of pesticides. Among the pyrethroids, Wright and Verkerk (1995) report that cypermethrin is generally less toxic than permethrin to parasitoids; however, the reverse is true against predators. Similarly, the organophosphates comprise many of the compounds that have the greatest impact on beneficial populations, but some of the compounds are much less damaging to natural enemies (Theiling and Croft, 1988). A new class of chemicals, the neonicotinoids, also vary in effects on predatory arthropods (Mizell and Sconyers, 1992). Introduced in the 1990s, the neonicotinoid imidacloprid is widely used, with activity against sucking insects (e.g. aphids) and some species of beetles, flies and moths (Elbert et al., 1990, 1991). Some spiders, some predatory Coleoptera and some predatory Heteroptera are tolerant of imidacloprid (Kunkel et al., 1999; Elzen, 2001), but other closely related Coleoptera and Heteroptera are highly susceptible to imidacloprid (Delbeke et al., 1997; Sclar et al., 1998). Bacillus thuringiensis is recommended for organic production and IPM because of its low risk to non-target organisms, including biological control organisms (Abbott Laboratories, 1982). However, even a biorational like B. thuringiensis can interfere with IPM. The introduced cinnibar moth, Tyria jacobaeae (Linnaeus), has been used successfully as a biocontrol agent for the noxious weed tansy ragwort, Senecio jacobaea L. (McEvoy et al., 1991). B. thuringiensis may also be used in the same areas to control gypsy moth, Lymantria dispar (Linnaeus), and western spruce budworm, Choristoneura occidentalis Freeman

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 173

Risk–Benefit Analysis of Pesticides

(Morris, 1982). Some instars of cinnabar moth are killed by B. thuringiensis, and field experiments suggest that B. thuringiensis applications could interfere with IPM programmes to manage tansy ragwort (James et al., 1993). As a group, insecticides have the greatest impact on beneficial arthropod populations, but the potential effects of other types of pesticides should also be considered in IPM programmes. The fungicide zineb is toxic to the parasitoid Trichogramma cacoeciae Marchal (Franz and Fabrietius, 1971; Van Driesche et al., 1998). Theiling and Croft (1988) and Mizell and Schiffhauer (1990) report, however, that commonly used fungicides and acaricides were compatible with arthropod predators observed in a pecan study. Some herbicides have also been shown to affect beneficial populations (Theiling and Croft, 1988). Although the greatest impacts of pesticides have been reported on arthropod populations, pesticides may also affect populations of vertebrate predators that feed on insects. The US EPA restricted the insecticides carbofuran and diazinon because of adverse effects on bird populations (EXTOXNET, 2002a,b). Triazine herbicides have recently been shown to emasculate frogs and toads (Hayes et al., 2002). Other broad-spectrum insecticides, such as aldicarb and methyl parathion, are toxic to a wide range of vertebrate insect predators occurring in agricultural production systems (EXTOXNET, 2002c). Sublethal effects of pesticides further complicate the impact of pesticides on beneficial arthropods. Bracon hebetor Say laid fewer viable eggs after sublethal exposure to the carbamate insecticide carbaryl (Grosch, 1975). Parker et al. (1976) reported decreased fecundity for the coccinellid Menochilus sexmaculatus (Fabricius) after sublethal doses of malathion, an organophosphate. Repellent effects of pyrethroid insecticides have been reported since the 1980s (Riedl and Hoying, 1983; Jacobs et al., 1984). Sublethal exposures to imidacloprid, azinphos-methyl (organophosphate), carbaryl or malathion have increased egg production in some pest arthropods and some predatory arthropods


(Lowery and Sears, 1986; Morse and Zareh, 1991; James, 1997). The discussion of sublethal effects continues indefinitely with many unanswered questions if multitrophic effects, ecological interactions, behavioural effects, etc. are included. An exhaustive treatise is beyond the scope of this chapter, but Croft (1990) edited a comprehensive review of the relationship between arthropod biological controls and pesticides. Wright and Verkerk (1995) discuss multitrophic evaluation of pesticide applications.

Fungicides and biological control of insects Insect pests are attacked by naturally occurring fungal pathogens. Early in the 20th century, researchers noted that fungicide applications could result in the rebound of arthropod pest populations (Rolfs and Fawcett, 1908). Since that time, several studies have linked increases in pest populations to the fungicide effects on fungal entomopathogens; Olmert and Kenneth (1974) provide a review of early experiments. Modern pesticides can have similar effects. Nomuraea rileyi Farlow fungus is a naturally occurring control agent for velvet bean caterpillar, Anticarsia gemmatalis (Hubner). Johnson et al. (1976) showed that applications of benomyl alone and in combination with insecticides reduced the infection rate of velvet bean caterpillar up to tenfold, with a concomitant reduction in yield. Aphids are a serious pest of pecans and cotton; naturally occurring epizootics caused by fungi help control populations. This phenomenon is of particular interest because pecan aphid pests are resistant to many insecticides (Dutcher, 1983; Dutcher and Htay, 1985). Pickering et al. (1990) reported that aphid mortality due to fungal infection was significantly reduced in pecans by the application of triphenyltin hydroxide fungicide. Smith and Hardee (1996) discovered that the application of a granular fungicide at planting could reduce the prevalence of the entomopathogenic fungus Neozygites fresenii Batkow, which helps control populations of the cotton aphid Aphis gossypii Glover.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 174


P. Guillebeau

In many areas of potato (Solanum tuberosum L.) production, growers must protect the crop from a major insect pest, Colorado potato beetle, Leptinotarsa decemlineata (Say), and fungal diseases (primarily early blight, Alternaria solani (Ell. and Mart.) Jones and Grout, and late blight, Phytophthora infestans (Mont. de Bary). The Colorado potato beetle is of particular concern because this pest has become resistant to nearly every available insecticide (Insecticide Resistance Action Committee, 2003). Additionally, environmental risks escalate as growers apply higher rates of pesticides to control resistant populations of Colorado potato beetle. Research suggests that the fungal pathogen Beauvaria bassiana (Balsamo) Vullemin may be a useful biological control agent for Colorado potato beetle (Boiteau, 1988). If B. bassiana can be used effectively, growers would have an additional tool to manage resistance. Furthermore, B. bassiana would not have many of the undesirable environmental consequences associated with broad-spectrum conventional insecticides. Using B. bassiana to control Colorado potato beetle in potatoes is challenging because disease management in potatoes relies on regular applications of fungicides (University of Idaho, 1999). Todorova et al. (1998) reported that field applications of six common fungicides (chlorothalonil, maneb, thiophanate-methyl, mancozeb, metalaxyl + mancozeb, and zineb) inhibited the growth and sporulation of B. bassiana; a herbicide, glufosinate-ammonium, also inhibited B. bassiana. Surprisingly, the herbicide diquat synergized the insecticidal activity of B. bassiana. Other researchers found similar results using chlorothalonil and mancozeb (Jaros-Su et al., 1999). However, they reported that applications of the fungicide copper hydroxide had relatively little effect on B. bassiana, suggesting that it may be possible to integrate B. bassiana with some types of fungicides.

Pesticides and biological control of weeds The US federal government and numerous state agencies have programmes to actively control noxious weeds (USDA-APHIS, 2002).

An IPM strategy is the focus of most noxious-weeds programmes, including pesticides and biological controls. It is important to use pesticides selectively to avoid disruption of the biological components of the IPM programme. The California Department of Food and Agriculture has several projects to control noxious weeds in non-agricultural settings. As part of their programme to control purple loosestrife (Lythrum salicaria L.), the Department releases two species of leaf beetle (Galerucella spp.) that attack this weed. However, these beetles are considered to be very susceptible to pesticides, and newly released colonies should be protected from broad-spectrum insecticides (Pitcairn, California, 2003, personal communication). Several releases of Galerucella spp. were made into riparian zones, but the beetles could not be found shortly after release (Pitcairn, California, 2003, personal communication). Repeated, similar incidents caused the project team to investigate and speculate about possible causes. Although the disappearance of the beetles was not resolved with certainty, the team conjectured that malathion applications made to control mosquitoes in the riparian zone also killed the beetles. The North Dakota State University Extension Service (1997) and bulletins from other states caution that insecticides used for adult mosquito control will also kill Galerucella beetles. Water hyacinth, Eichhornia crassipes Mart., is the target of another California weed control project. Neochetina spp. weevils attack water hyacinth, and they are a component of the California strategy. However, herbicides are also widely used to control hyacinth. If the hyacinth is killed before the weevils complete development, the weevils also die. During the 1980s and 1990s, the programme to release Neochetina spp. weevils was nearly scuttled because other programmes were applying herbicides to water hyacinth in the weevil-release areas (Pitcairn, California, 2003, personal communication). Eventually, better cooperation and communication between the various programmes fostered the use of both herbicides and weevils as part of an IPM programme.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 175

Risk–Benefit Analysis of Pesticides

Many states have IPM programmes to control the invasive musk thistle, Carduus nutans L. The head weevil, Rhinocyllus conicus Froelich, and the rosette weevil, Trichosirocalus horridus (Panzer), are biological control agents released to help control musk thistle. Herbicide applications are also commonly used to manage musk thistle. If the herbicides are applied while the weevils are still in the larval stage, the weevils are killed along with the plant. To provide maximum protection for the weevils, herbicide should not be applied to musk thistle in Oklahoma from mid-May to mid-July. However, late May is a good time for growers to apply a single application of herbicide to control a spectrum of weeds (Medlin et al., 2003). Because musk thistle is a ubiquitous problem, conflict may arise between adjacent properties if all parties do not control for thistle. Unlike herbicide application, weevil release does not produce an immediate, obvious effect on musk thistle. The Oklahoma Extension Service has developed a sign to indicate a weevil-release site, so that nearby property owners will not think that no action was taken against musk thistle (Bolin, Oklahoma, 2003, personal communication).

Making Pesticides More Compatible with IPM Clearly, pesticides can have a variety of negative impacts on populations of biocontrol agents. However, the effects are largely unpredictable, even within closely related groups of organisms or chemical classes. Even with risk and uncertainty, however, pesticides remain a critical component of IPM. Van Emden (2002) calls chemical control, biological control, cultural control and host-plant resistance the four main buildingblocks of IPM. Pesticides will continue to be an integral and necessary part of IPM for the foreseeable future, especially in cropping systems with multiple pests (Graves et al., 1999). The challenge for pest managers is to use pesticides in ways that maintain the value of the other IPM components. To many people, organic farming is the antithesis of conventional farming in terms


of pesticide use. However, organic growers still need pesticides, although they are limited to a list of pesticides approved for organic production. The particular chemicals vary somewhat with the government or organization certifying organic production. Insecticidal soaps and oils are permitted in most programmes. Natural products, such as pyrethrum and rotenone, are also widely accepted (Frick, 2002). In the USA, there is an official National List of Allowed and Prohibited Substances for growers that wish to be certified as organic by USDA (USDA, 2002). Like conventional operations, organic production tries to use pesticides in ways that are compatible with other pest-management techniques. In his review, Ripper (1956) points out that biological controls and pesticides are important components of pest-management systems. He suggests that research should aim to reduce the negative impacts of pesticides in two ways: (i) manipulate application techniques for non-selective pesticides; and (ii) develop selective pesticides with fewer adverse effects on beneficial populations. The quarantine use of pesticides is an important tool for IPM because new pest species do not become established. Quarantines often mandate the use of pesticides. For example, nursery stock, grass sod and other regulated articles cannot be shipped out of the US quarantine area for imported fire ants until the materials have been treated with an approved insecticide (USDA-APHIS, 1997). Japan requires fumigation of plant materials with methyl bromide or approved substitutes if foreign pests are detected (Japanese Market Information, 2002). Although quarantine use of pesticide is a critical tool for IPM, there is little or no impact on beneficial populations of arthropods. Even though pesticides are the primary method of control recommended for many turf pests, producers are implementing new ideas to attenuate the unwanted effects of pesticides. Sampling schemes and degreeday models have been developed for the chinch bug complex, Blissus leucopterus Montandon, Blissus inularis Barber and Blissus leucopterus (Say), and identification of the species combination determines the need

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 176


P. Guillebeau

for insecticide applications (Reinert et al., 1995). The Handbook of Turfgrass Insect Pests, edited by Brandenburg and Villani (1995), provides an overview of turf IPM and the role of pesticides for management of other turf insect pests. Pesticide selectivity can be improved by manipulating spray parameters, such as placement or timing. Watson (1975) reported that applying azinphos-methyl to the lower two-thirds of the plant could control cotton pests as predatory anthocorids (Orius spp.) increased in the upper third of the plant. Applying herbicides around the base of cotton plants conserved a complex of beneficial arthropods (Stam et al., 1978). Careful timing of pesticide applications minimizes contact between the beneficial organism and the pesticide. It was already recognized in the 1950s that the proper timing of dichlorodiphenyltrichloroethane (DDT) applications minimized negative impacts on beneficials in walnut and melon pestmanagement systems (Michelbacher and Middlekauff, 1950; Bartlett and Ortega, 1952). Applications of paraquat or glyphosate to control orchard weeds during the spring harms populations of the predatory mite Neoseiulus fallacies Garman occupying the ground cover (Pfeiffer, 1986); herbicide applications made in the autumn have much less impact on the predatory mites because most of them have moved into the tree canopy. Selective techniques enhance the role of pesticides in IPM for apples, peaches and other stone fruits. Alternate-row middle spraying is a recommended practice in some circ*mstances (Horton et al., 2002; Washington State University, 2002). Growers apply pesticide only to the middle of every other row; this method reduces pesticide impacts on beneficial organisms. Ironically, increasing herbicide use improves insectpest management. Stinkbugs and plant bugs are key pests of stone fruits in the southern USA because these insects scar the fruit. This complex of pests is less common in orchards with effective broadcast control of broadleaved weeds (Horton et al., 2002). Pesticides are often applied at planting to control early-season pests. Typically, the pesticide is applied in a continuous stream in the

row, while the seeds are placed at discrete intervals within the row. A new technique limits the pesticide application to the row space adjacent to the seeds. Lohmeyer et al. (2003) report that precision placement of the pesticide may reduce the pesticide rate by more than 50% without sacrificing efficacy. Growers still gain the benefits of the pesticides in their IPM programmes, but the impacts on beneficial populations are greatly reduced. Spot applications, alternate-row middle applications, precision applications and selective spray timing all create spatial or temporal refugia for beneficials where they do not come in contact with the pesticide. Effective use of refugia requires thorough knowledge of the interactions between the plant, the pest and the biocontrol agent, and information about how the interactions change over time (Verkerk, 2002). Few studies of tritrophic interactions have been published; more data are needed to use refugia more effectively (Verkerk et al., 1998). Scientists recognized early that pesticide selection was an important factor in preserving beneficial populations (Lord, 1949; Ripper et al., 1951; Bartlett, 1952; van den Bosch and Stern, 1962). Growers now have greater flexibility as pesticide companies introduce products with fewer impacts on beneficial arthropods. Rapid-CP (2002) uses data from the USDA Interregional Research Project Number 4 and USDA Office of Pest Management policy to create a comprehensive database to track potential, pending and recently registered new products. Pymetrozine, indoxacarb, spinosad, bifenzate, methoxyfenozide, tebufenozide and pyriproxyfen are new insecticides that are reported to have low toxicity for beneficial insects. Because of EPA incentives to register reduced-risk pesticides, growers will probably have an increased number of options with fewer effects on biological controls. Formulation can also improve the selectivity of pesticides. Ripper et al. (1948) demonstrated that a coating of cellulose made insecticide significantly less toxic to beneficials, although there was only a slight reduction in efficacy against the target pests. Franz and Fabrietius (1971) reported that rates of parasitism varied from 2 to 89% in the pres-

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 177

Risk–Benefit Analysis of Pesticides

ence of various formulations of zineb. Parasitism may be affected by either the inert ingredients or some interaction between the pesticide and the inert ingredients. In general, dust formulations are more toxic to beneficials than wettable powders or emulsifiable concentrates. Bartlett (1951) demonstrated that dusts can kill hymenopteran parasitoids even in the absence of a pesticide. Carbamate and organophosphate insecticides were more toxic to spiders when applied as dusts instead of emulsion (Yoo et al., 1984). Encapsulation of pesticide can increase selectivity, but results vary. Dahl and Lowell (1984) reported 70–100% mortality for nabids and coccinellids in lucerne sprayed with encapsulated methyl parathion but little or no mortality for spiders. They further recounted low mortality for coccinellids and high mortality for hymenopterans in cotton treated with encapsulated methyl parathion. Asquith et al. (1976) and Hull (1979) found that encapsulated methyl parathion had little or no effect on mite predators found on apple trees. Greater pesticide selectivity is sometimes gained with granular formulations. Foliar pesticide applications to control lesser cornstalk borer on groundnuts disrupted natural controls and promoted secondary outbreaks of mites and lepidopteran pests, but granular formulations controlled the pest without secondary problems (Newsom et al., 1976). Granular applications of carbofuran and thiofanox did not significantly reduce numbers of coccinellids, chrysopids or parasitized aphids in barley, but foliar applications of the same materials caused substantial reductions (Ba-Angood and Stewart, 1980). Using pesticides systemically will protect populations of some kinds of beneficial arthropods. Ripper (1957) showed that systemic use of schradan and oxydemetonmethyl had little or no effect on predatory coccinellids or syrphids. Populations of the spider Lycosa pseudoannulata Boesenberg were not greatly reduced by systemic use of carbofuran on rice, but populations of the predatory bug, Cyrtorhinus lividipennis Reuter were nearly eliminated (Dyck and Orlido, 1977). Systemic use of aldicarb on


cotton caused high mortality for the heteropteran Nabis and Geocoris spp., but populations of spiders, Chrysoperla larvae and hymenopteran parasitoids were nearly unaffected (Ridgeway et al., 1967). In rice and cotton, the affected predator species were facultative plant feeders. The EPA classifies pheromones as pesticides even though they often have a nontoxic mode of action. Additionally, pheromones typically affect a single species or a small group of closely related species (Nordland et al., 1981). Consequently, pheromones have little or no effect on biological control agents in most cases. Pheromones are used directly to disrupt mating in a number of lepidopteran pest species, including codling moth, Cydia pomonella (Linnaeus), and pink bollworm, Pectinophora gossypiella Saunders (Carde and Minks, 1995). Pheromones are commonly used to monitor pest populations so that pesticide applications can be made at the optimum time and place. Pheromones and/or food baits are also used in combination with toxic agents. Programmes to contain or eradicate Mediterranean fruit fly populations typically include a combination of an attractant and a poison (Roessler, 1989). As more pheromones become available, pest managers will have greater flexibility to integrate pesticides into IPM. Baits do not always provide as much selectivity as pheromones because they can attract a broader range of arthropods. Nasca et al. (1983) reported that malathion bait applications to control fruit flies were less toxic to predacious lacewings. Surprisingly, greater selectivity was gained by applying the bait to the entire tree instead of offering the bait on plastic strips. Conversely, Ehler et al. (1984) found that a malathion-bait spray applied for fruit flies greatly reduced populations of gall-midge parasitoids, allowing gall-midge populations to increase 90-fold.

Policies to Improve Compatibility of Pesticides and IPM Pest Management and the Environment in 2000 was an international symposium to discuss

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 178


P. Guillebeau

the future of pest management (Aziz et al., 1992). One conclusion was that pesticides would continue to be an essential component of IPM (Perfect, 1992). He also points out a common paradox of pesticides and IPM. Misapplication of pesticides is the greatest threat to many IPM programmes; however, the overuse of pesticides may also be the impetus for IPM with greater emphasis on non-chemical controls. Resistance to pyrethroid insecticides caused Helicoverpa armigera (Hubner) to become one of the most economically damaging pests in Indian agriculture (Sharma, 1991). In response, the Indian Council of Agricultural Research instigated a major programme for natural controls of H. armigera, including nuclear polyhedrosis virus and parasitoid wasps (Perfect, 1992). Although the future of IPM includes pesticides, new chemicals will be quite different from the broad-spectrum pesticides first developed for agricultural-pest management. The EPA Office of Pesticide Programs (OPP) has several programmes to accelerate the introduction of pesticides with fewer risks to the environment, including biological control organisms (Andersen et al., 1996). The EPA 25b rule exempts very low-risk products, including some biological agents and common food substances (e.g. eugenol and soybean oil), from regulation; a complete list of 25b-exempted materials can be found on the Internet ( oppbppd1/biopesticides/regtools). Regulatory relief will encourage research and marketing of these products because a large investment will not be necessary to fulfil EPA requirements for registration of conventional pesticides. Andersen et al. (1996) report that the Biopesticides and Pollution Prevention Division (BPPD) of OPP streamlines the registration process for biological pesticides, including microbials, plant-incorporated protectants and biochemicals active through a non-toxic mode of action (e.g. pheromone traps). Biopesticides generally affect only the target pest and closely related organisms (US EPA BPPD, 2002b). As part of an IPM programme, biopesticides can greatly decrease the use of conventional pesticides and main-

tain high crop yields. At the end of 2001, the EPA had listed approximately 195 registered biopesticide active ingredients and 780 products (US EPA BPPD, 2002a). The OPP reduced-risk programme encourages the registration of conventional pesticides that fit low-risk criteria, including compatibility with IPM (OPP, 2002). The EPA offers greatly reduced registration time as an economic incentive. Reduced-risk pesticides are registered in an average of 16 months versus 38 months for a conventional pesticide not classified as reduced risk. The pesticide can be marketed sooner, and the registrant has several more growing seasons with their pesticide under patent. The USDA developed a strategic plan for IPM that was released in 2003 (IPM, 2002). Among other goals, the plan defines specific targets to reduce levels of hazardous pesticides detected in surface drinking-water supplies and pesticide residues in the major foods consumed by infants and children. The strategy calls for alternatives to pesticides that result in unacceptable residue levels in food-crop commodities. The USDA plan clearly recognizes the role of pesticides in IPM. One target calls for improvement of pesticide application methods, timing and placement that results in improved efficacy with reduced pesticide residues in raw agricultural commodities. In some European countries, laws were not specifically crafted to promote IPM, but growers are likely to use more non-chemical pest-control methods as pesticides become less available. Sweden, Denmark and The Netherlands mandated a 50% or greater reduction in total pesticide use by 2000 (Matteson, 1995). Sweden’s plan included regional plant-protection centres promoting IPM. A number of developing countries promote IPM or pesticide reduction through official policies or regulation (Elkstrom, 2002). China introduced the Green Certificate programme and banned highly toxic pesticides from vegetable crops. Biological control is a national priority for Cuba; the new policy is intended to make IPM biointensive, with 80% of pests managed through biological control. Iran formed the High Council of

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 179

Risk–Benefit Analysis of Pesticides

Policy and Planning for Reduction of Agricultural Pesticides. A National IPM Committee in Malaysia is reducing pesticide use and increasing farmer knowledge of other pest-management techniques. Nepal, the Philippines, Sri Lanka and Indonesia have adopted national IPM policies. The Food and Agriculture Organization and the World Health Organization work with the international community and developing nations to develop pesticide policy, but many developing countries have only rudimentary regulation of pesticide use (Schaefers, 1996). Although most growers incorporate some elements of IPM (e.g. monitoring for pests), many modern production systems are overly dependent on pesticides that disrupt natural controls. Reliance on pesticides has undoubtedly slowed the progress of IPM. Pest management should not be chemically dependent, but it is imprudent to ignore the benefits associated with the judicious use of


pesticides. The most efficient and sustainable IPM programmes will recognize a critical role for pesticides. As IPM and pesticides evolve, the use of pesticides is likely to increase as new chemicals and new application techniques make pesticides more compatible with biological controls and other IPM components. The pesticide industry is emphasizing new products with greater selectivity for natural enemies and minimal environmental impact (Sengonca, 2002). Governmental programmes and regulations encourage the introduction of pesticides with fewer non-target effects. Improved application techniques allow us to use pesticides more precisely, with less offtarget deposition. Research is providing greater insight into interactions between biological controls, pests, hosts and pesticides. This knowledge will help IPM practitioners use pesticides in ways that conserve natural controls.

References Abbott Laboratories (1982) Toxicology Profile: Dipel, Bacillus thuringiensis Insecticide. Chemical and Agricultural Products Division, Chicago, Illinois. Adams, C.H. and Cross, W.H. (1967) Insecticide resistance in Bracon mellitor, a parasite of the boll weevil. Journal of Economic Entomology 60, 1016–1020. Andersen, J., Leslie, A., Matten, S. and Kumar, R. (1996) The Environmental Protection Agency’s programs to encourage the use of safer pesticides. Weed Technology 10, 966–968. Anon. (1917) Annual Report of the Georgia Department of Agriculture. Georgia Department of Agriculture Monthly Bulletin 5, 130–131. Anon. (1940) Annual Report of the Georgia Agriculture Extension Service. Georgia Agriculture Extension Service, pp. 5–7 Anon. (1993) Agricultural Statistics 1993. National Agricultural Statistics Service, USDA, Washington, DC, 57 pp. Asquith, D., Hull, L.A. and Mowry, P.D. (1976) Apple, tests of insecticides (1975). Insecticide and Acaracide Tests 1, 17–19. Aziz, A., Kadir, S.A. and Barlow, H.S. (eds) (1992) Pest Management and the Environment in 2000. CAB International, Wallingford, UK, 401 pp. Ba-Angood, S.A. and Stewart, R.K. (1980) Effect of granular and foliar insecticides on cereal aphids and their natural enemies on field barley in southwestern Quebec. Canadian Entomologist 112, 1309–1313. Bartlett, B.R. (1951) The action of certain inert dust materials on parasitic hymenoptera. Journal of Economic Entomology 44, 891–896. Bartlett, B.R. (1952) A study of insecticide resistance in strains of Drosophila melanogaster. Canadian Entomologist 84, 189. Bartlett, B.R. and Ortega, J.C. (1952) Relation between natural enemies and DDT-induced increases in frosted scale and other pests of walnuts. Journal of Economic Entomology 45, 783–785. Boiteau, G. (1988) Control of the Colorado potato beetle Leptinotarsa decemlineata: learning from the Soviet experience. Bulletin of the Entomological Society of Canada 20, 9–15. van den Bosch, R. and Stern, V. (1962) The integration of chemical and biological control of arthropod pests. Annual Review of Entomology 7, 367–368.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 180


P. Guillebeau

Brandenburg, R.L. and Villani, M.G. (eds) (1995) Handbook of Turfgrass Insect Pests. Entomological Society of America Press, Lanham, Maryland, 140 pp. Carde, R.T. and Minks, A.K. (1995) Control of moth pests by mating disruption: successes and constraints. Annual Review of Entomology 40, 559–586. Coad, B.R. (1920) Killing boll weevils with poison dust. United States Department of Agriculture Yearbook 1920, 241–252. Croft, B.A. (1990) Arthropod Biological Control Agents and Pesticides. John Wiley & Sons, New York, 723 pp. Croft, B.A. and Stickler, K. (1983) Natural enemy resistance to pesticides: documentation, characterization, theory and application. In: Georghiou, G.P. and Saito, T. (eds) Pest Resistance to Pesticides. Plenum, New York, pp. 669–702. Dahl, G.H. and Lowell, J.R. (1984) Microencapsulated pesticides and their effects on nontarget insects. In: Scher, H.B. (ed.) Advances in Pesticide Formulation Technology. American Chemical Society, Washington, DC, pp. 141–150. Delbee, F., Vercruysse, P., Tirry, L., DeClerq, P. and Degheele, D. (1997) Toxicity of diflubenzuron, pyriproxyfen, imidacloprid, and diafenthruion to the predatory bug, Orius laevigatus (Heteroptera: Anthocoridae). Entomophaga 42, 349–358. Dutcher, J.D. (1983) Pecan pest management – where are we? In: Payne, J.A. (ed.) Pecan Pest Management – Are We There? Miscellaneous Publication 13, Entomological Society of America, College Park, Maryland, pp. 133–140. Dutcher, J.D. and Htay, U.T. (1985) Impact assessment of carbaryl, dimethoate, and dialifor on foliar pecan and nut pests of pecan orchards. Journal of the Georgia Entomological Society 18, 495–507. Dyck, V.A. and Orlido, G.C. (1977) Control of the brown planthopper, Nilaparvata lugens, by natural enemies and timely application of narrow-spectrum insecticides. International Rice Research Institute Annual Report 1976, 28–72. Ehler, L.E., Endicott, P.C., Herlein, M.B. and Alvarado-Rodriguez, B. (1984) Medfly eradication in California: impact of malathion bait sprays on an endemic gall midge and its parasitoids. Entomologia Experimentalis et Applicata 36, 201–208. Elbert, A., Overbeck, H., Iwaya, K. and Tsuboi, S. (1990) Imidacloprid, a novel systemic nitromethylene analogue insecticide for crop protection. Proceedings Brighton Crop Protection Conference on Pests and Diseases 1, 21–28. Elbert, A., Becker, B., Hartwig, J. and Erdelen, C. (1991) Imidacloprid: a new systemic insecticide. Pfanzenshutz Nachrichten Bayer 44, 113–116. Elkstrom, G. (2002) Pesticide reduction in developing countries. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 598–605. Elzen, G.W. (2001) Lethal and sublethal effects of insecticide residues on Orius insidiosus (Hemiptera: Anthocoridae) and Geocoris punctipes (Hemiptera: Lygaeidae). Journal of Economic Entomology 94, 55–59. EXTOXNET (2002a) Pesticide information profiles: diazinon. Available at: mfs/01/pips/diazinon.htm EXTOXNET (2002b) Pesticide information profiles: carbofuran. Available at: cgi-bin/mfs/01/pips/carbofur.htm EXTOXNET (2002c) Pesticide information profiles: aldicarb. Available at: mfs/01/pips/aldicarb.htm Flint, M.L. and van den Bosch, R. (1981) Introduction to Integrated Pest Management. Plenum Press, New York, 240 pp. Floyd, D.L. and Treanor, K. (1944) Georgia agricultural facts. University of Georgia Agriculture Extension Service Bulletin 511, 28–29. Franz, J.M. and Fabrietius, K. (1971) Testing the sensitivity to pesticides of entomophagous arthropods – trials using Trichogramma. Zeitschrift für Angewandte Entomologie 68, 278–288. Frick, B. (2002) Organic farming. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 554–557. Frisbie, R.E. and Smith, J.W. Jr (1991) Biologically intensive integrated pest management: the future. In: Menn, J.J. and Steinhauer, A.L. (eds) Progress and Perspectives for the 21st Century. Entomological Society of America Press, Lanham, Maryland, pp. 151–64. Gianessi, L.P. and Anderson, J.E. (1995) Pesticide Use in the U.S. Crop Production: National Summary Report. The National Center for Food and Agricultural Policy, Washington, DC, 280 pp.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 181

Risk–Benefit Analysis of Pesticides


Grafton-Cardwell, E.E. and Hoy, M.A. (1986) Genetic improvement of common green lacewing, Chrysoperla carnea (Neuroptera: Chrysopidae): selection for carbaryl resistance. Environmental Entomology 15, 1130–1136. Graves, J.B., Leonard, B.R. and Ottea, J.A. (1999) Chemical approaches to managing arthropod pests. In: Ruberson, J. (ed.) Handbook of Pest Management. Marcel Dekker, New York, pp. 449–486. Grosch, D.S. (1975) Reproductive performance of Bracon hebetor after sublethal doses of carbaryl. Journal of Economic Entomology 68, 659–662. Guillebeau, L.P. and All, J.N. (1989) Impact of weekly applications of selected new pyrethroids or improved Bacillus thuringiensis Berliner on the arthropod predator complex in cotton. PhD dissertation, University of Georgia, Athens, Gorgia. Haney, P.B., Herzog, G. and Roberts, P.M. (2001) Boll weevil eradication in Georgia. In: Boll Weevil Eradication in the U.S. through 1999. Cotton Foundation Reference Book Series No. 6, Memphis, Tennessee, pp. 258–88. Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C. and Vonk, A. (2002) Feminization of male frogs in the wild. Nature 419, 895–896. Horton, D., Bellinger, B., Gorsuch, C. and Ritchie, D. (2002) Southeastern Peach, Nectarine, and Plum Pest Management and Culture Guide. Bulletin 1171, Cooperative Extension Service, University of Georgia, Athens, Georgia, 42 pp. Hoskins, W.M., Borden, A.D and Michelbacher, A.E. (1939) Recommendations for a more discriminating use of insecticides. In: Proceedings of the 6th Pacific Scientific Congress, Vol. 5, Davis, California, pp. 119–123. Hoy, M.A. (1985) Recent advances in genetics and genetic improvement of the Phytoseiidae. Annual Review of Entomology 30, 345–370. Hull, L.A. (1979) Apple, tests of insecticides 1978. Insecticide and Acaricide Tests 4, 20–22. Hunter, W.D. (1917) The boll weevil program with special reference to means of reducing damage. USDA Farmers’ Bulletin 848, 1–40. Insecticide Resistance Action Committee (2003). Resistance depleting potato growers’ arsenal. Available at: IPM (2002) IPM roadmap will be unveiled at meeting. Issue no. 105. Available at: Jacobs, R.J., Kouskolekas, C. and Gross, H. (1984) Responses of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) to residues of permethrin and endosulfan. Environmental Entomology 13, 355–358. James, D.G. (1997) Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae). Experimental and Applied Acarology 21, 75–82. James, R.R., Miller, J.C and Lighthart, B. (1993) Bacillus thuringiensis var. kurstaki affects a beneficial insect, the cinnabar moth (Lepidoptera: arctiidae). Journal of Economic Entomology 86, 334–339. Japanese Market Information (2002) Fresh fruits. Available at: Jaros-Su, J., Groden, E. and Zhang, J. (1999) Effects of selected fungicides and the timing of fungicide application on Beauvaria bassiana induced mortality of the Colorado potato beetle. Biological Control 15, 259–269. Johnson, D.W., Kish, L.P. and Allen, G.E. (1976) Field evaluation of selected pesticides on the natural development of the entomopathogen, Nomuraea rileyi, on the velvet bean caterpillar in soybean. Environmental Entomology 5, 964–966. Kunkel, B.A., Held, D.W. and Potter, D.A. (1999) Impact of halofenozide, imidacloprid, and bendiocarb on beneficial invertebrates and predatory activity in turfgrass. Journal of Economic Entomology 92, 922–930. Lohmeyer, K.H., All, J.N., Roberts, P.M. and Bush, P. (2003) Precision application of aldicarb to enhance efficiency of thrips (Thysanoptera: Thripidae) management in cotton. Journal of Economic Entomology 96, 748–754. Lord, F.T. (1949) The influence of spray programs on the fauna of apple orchards in Nova Scotia II: oystershell scale. Canadian Entomologist 79, 196–209. Lowery, D.T. and Sears, M.K. (1986) Stimulation of reproduction of the green peach aphid (hom*optera: Aphididae) by azinphosmethyl applied to potatoes. Journal of Economic Entomology 79, 1530–1533. Martin, N.R., Nix, J.E., McArthur, W.C. and Brannen, S.J. (1968) Effects of alternative production practices on costs and returns in producing cotton in selected areas of Georgia. University of Georgia College of Agriculture Experimental Station–USDA Research Bulletin 34, 1–38.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 182


P. Guillebeau

Matteson, P.C. (1995) The 50% pesticide cuts in Europe: a glimpse of our future. American Entomologist 41, 210–220. McEvoy, P., Cox, C. and Coombs, E. (1991) Successful biological control of ragwort, Senecio jacobaea, by introduced insects in Oregon. Ecological Applications 4, 430–442. Medlin, C., Bolin, P., Roduner, M. and Stritske, J. (2003) Integrated Control of Invasive Thistles in Oklahoma. Bulletin F-7318 Stillwater, Oklahoma, Oklahoma Cooperative Extension Service, Oklahoma State University. Michelbacher, A.E. and Middlekauff, W.W. (1950) Control of the melon aphid in northern California. Journal of Economic Entomology 43, 444–447. Mizell, R.F. and Schiffhauer, D.E. (1990) Effects of pesticide on pecan aphid predators Chrysoperla rufliabris (Neuroptera: Chrysopidae), Hippodamia convergens, Cylconeda sanguinea, Olla v-nigrum (Coleoptera: Coccinellidae), and Aphelinus perpallidus (Hymenoptera: Encyrtidae). Journal of Economic Entomology 83, 1806–1812. Mizell, R.F. and Sconyers, M.C. (1992) Toxicity of imidacloprid to selected arthropod predators. Florida Entomologist 75, 277–280. Morris, O.N. (1982) Bacteria as pesticides: forest applications. In: Kurstak, E. (ed.) Microbial and Viral Pesticides. Marcel Dekker, New York, pp. 239–287. Morse, J.G. and Zareh, N. (1991) Pesticide induced hormoligosis of citrus thrips (Thysanoptera: Thripidae) fecundity. Journal of Economic Entomology 84, 1169–1174. Nasca, A.J., Fernandez, R.V., De Herrero, A.J. and Manzur, B.E. (1983) Incidence of chemical treatment for control of fruit flies on chrysopids and hemerobiids on citrus trees. CITRON 1, 47–73. National Research Council (1996) Ecologically Based Pest Management: New Solutions for a New Century. National Academy, Washington, DC, 35 pp. Newsom, L.D., Smith, R.F. and Whitcomb, W.H. (1976) Selective pesticides and selective use of pesticides. In: Huffaker, C.B. and Messenger, P.S. (eds) Theory and Practice of Biological Control. Academic Press, New York, pp. 565–591. Nordland, D.A., Jones, R.L. and Lewis, W.J. (1981) Semiochemicals: Their Role in Pest Control. Wiley, New York, 306 pp. North Dakota State University Extension Service (1997) Biological control agents released for purple loosestrife control. North Dakota Pesticide Quarterly 15, 9. Olkowski, W. and Daar, S. (1991) Common Sense Pest Control. Taunton Press, Newtown, Connecticut, 715 pp. Olmert, I. and Kenneth, R.G. (1974) Sensitivity of the entomopathogenic fungi to fungicides and insecticides. Journal of Economic Entomology 31, 371–372. OPP (2002) General overview: reduced-risk pesticide program. Available at: oppfod01/trac/safero.htm Parker, F.D., Ming, N., Pend, T. and Singh, G. (1976) The effect of malathion on fecundity, longevity, and geotropism of Menochilus sexmaculatus. Environmental Entomology 5, 495–501. Perfect, T.J. (1992) IPM in 2000. In: Aziz, A., Kadir, S.A. and Barlow, H.S. (eds) Pest Management and the Environment in 2000. CAB International, Wallingford, UK, pp. 47–53. Pfeiffer, D.G. (1986) Effects of field applications of paraquat on densities of Panonychus ulmi Koch and Neoseiulus fallacies Garman. Journal of Agricultural Entomology 3, 322–325. Pickering, J., Dutcher, J.D. and Ekbom, B.S. (1990) The effect of a fungicide on fungal-induced mortality of pecan aphids in the field. Journal of Economic Entomology 83, 1801–1805. Rainwater, C.F. and Gaines, J.C. (1951) Seasonal decline in the effectiveness of the certain insecticides against boll weevil. Journal of Economic Entomology 44, 971–974. Rapid-CP (2002) Recent Ag Products in Defence of Crop Plants. Available at: http://cipmtest.ent.ncsu. edu/rapidcp/ Redmond, K.R. and Brazzel, B.R. (1968) Response of the striped lynx spider, Oxyopes salticus, to commonly used pesticides. Journal of Economic Entomology 61, 327–328. Reinert, J.A., Heller, P.R. and Crocker, R.L. (1995) Pest information: chinch bugs. In: Brandenburg, R.L. and Villani, M.G. (eds) Handbook of Turfgrass Insect Pests. Entomological Society of America Press, Lanham, Maryland, pp. 38–42. Ridgeway, R.L., Lingren, P.D., Cowan, C.B. and Davis, J.W. (1967) Populations of arthropod predators and Heliothis spp. after applications of systemic insecticides to cotton. Journal of Economic Entomology 60, 1012–1016.

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 183

Risk–Benefit Analysis of Pesticides


Ridgeway, R.L., Lloyd, E.P. and Cross, W.H. (1983) Cotton Insect Management with Special Reference to the Boll Weevil. Agriculture Handbook 589, Agricultural Research Service, United States Department of Agriculture, Washington, DC. Riedl, H. and Hoying, S. (1983) Toxicity and residual activity of fenvalerate to Tryphlodromus occidentalis (Acari: Tetranychidae) on pear. Canadian Entomologist 115, 807–813. Ripper, W.E. (1956) Effect of pesticides on balance of arthropod populations. Annual Review of Entomology 1, 403–439. Ripper, W.E. (1957) Selective insecticides and the balance of arthropod populations. Agricultural Chemistry 12, 36–37, 103, 105. Ripper, W.E., Greenslade, R.M., Health, J. and Barker, K. (1948) New formulation of DDT with selective properties. Nature 161, 484. Ripper, W.E., Greenslade, R.M. and Hartley, G.S. (1951) Selective insecticides and biological control. Journal of Economic Entomology 44, 448–459. Roach, S.H. and Hopkins, A.R. (1981) Reduction in arthropod predator populations in cotton fields treated with insecticides for Heliothis spp. control. Journal of Economic Entomology 74, 454–457. Roessler, Y. (1989) Insecticidal bait and cover sprays. In: Robinson, A.S. and Hooper, G. (eds) Fruit Flies, Their Biology, Natural Enemies, and Control. Elsevier, Amsterdam, pp. 329–336. Rolfs, P.H. and Fawcett, H.S. (1908) Fungus diseases of scale insect and whitefly. Bulletin, Florida Agriculture Experiment Station, Gainesville, Florida, 17 pp. Ruberson, J.R., Herzog, G.A., Lambert, W.R. and Lewis, W.J. (1994) Management of the beet armyworm in cotton: role of natural enemies. Florida Entomologist 77, 440–453. Schaefers, G.A. (1996) Status of pesticide policy and regulations in developing countries. Journal of Agricultural Entomology 13, 213–222. Sclar, D., Gerace, D. and Crenshaw, W.S. (1998) Observations of population increases and injury by spider mites (Acari: Tetranychidae) on ornamental plants treated with imidacloprid. Journal of Economic Entomology 91, 250–255. Sengonca, L. (2002) Conservation of natural enemies. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 141–143. Sharma, D. (1991) India battles to eradicate major crop pest. New Scientist 150, 10 August, 15. Smith, M.T. and Hardee, D.D. (1996) Influence of fungicide on development of an entomopathogenic fungus in the cotton aphid. Environmental Entomology 25, 677–687. Smith, R.F. and van den Bosch, R. (1967) Integrated control. In: Wendell, W., Kilglore, W.W. and Doutt, R.L. (eds) Pest Control: Biological, Physical and Selected Chemical Methods. Academic Press, New York, pp. 295–340. Stam, P.A., Clower, D.F., Graves, J.B. and Schilling, P.E. (1978) Effects of certain herbicides on some insects and spiders found in Louisiana cotton fields. Journal of Economic Entomology 71, 477–480. Theiling, K.M. and Croft, B.A. (1988) Pesticide side-effects on arthropod natural enemies: a database summary. Agriculture, Ecosystems, and the Environment 21, 191–218. Todorova, S.I., Coderre, D., duch*esne, R. and Cote, J. (1998) Compatibility of Beauvaria bassiana with selected fungicides and herbicides. Biological Control 27, 427–433. Turnipseed, S.G., Todd, J.W. and Campbell, W.V. (1975) Field activity of selected foliar insecticides against geocorids, nabids, and spiders in soybeans. Journal of Entomological Science 10, 272–277. United States (US) Congress Office of Technology Assessment (1995) Biologically Based Technologies for Pest Control. US Government Printing Office, New York, 204 pp. United States Department of Agriculture (USDA) (2002) National List of Allowed and Prohibited Substances. The National Organic Program. Available at: United States Department of Agriculture Animal Plant Health Inspection Service (USDA-APHIS) (1997) Federal Domestic Quarantines. Available at: United States Department of Agriculture Animal Plant Health Inspection Service (USDA-APHIS) (2002) Federal Noxious Weed Program. Available at: United States Environmental Protection Agency (US EPA) (2002a) Inception of Pesticide Environmental Stewardship Program – IPM and Reduced Risk. Available at: PESP/inception.htm United States Environmental Protection Agency (US EPA) (2002b) What is a pesticide? Available at: http://www.epa./pesticides. United States Environmental Protection Agency Biopesticides and Pollution Prevention Division (US EPA BPPD) (2002a) Pesticides: biopesticides. Available at:

08IntpestManCh8.QXD 14/4/04 2:25 pm Page 184


P. Guillebeau

United States Environmental Protection Agency Biopesticides and Pollution Prevention Division (US EPA BPPD) (2002b) What are biopesticides? Available at: University of Idaho (1999) Potato late blight. Available at: ag/plantdisease/plbchc.htm Vandeman, A.J., Fernandez-Cornejo, S., Jans, S. and Lin, B.H (1994) Adoption of Integrated Pest Management in United States Agriculture. Bulletin No. 707, Economic Research Service Agriculture Information, United States Department of Agriculture, 26 pp. Van Driesche, R.G., Mason, J.L., Wright, S.E. and Prokopy, R.J. (1998) Effect of reduced insecticide and fungicide on parasitism of leafminers (Phyllonorycter spp.) (Lepidoptera: Gracillariidae) in commercial apple orchards. Environmental Entomology 27, 578–582. Van Emden, H.F. (2002) Integrated pest management. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 413–415. Verkerk, R.H.J. (2002) Refugia for pests and natural enemies. In: Pimentel, D. (ed.) Encyclopedia of Pest Management. Marcel Dekker, New York, pp. 685–688. Verkerk, R.H.J., Leather, S.R. and Wright, D.J. (1998) The potential for manipulating crop–pest–natural enemy interaction for improved insect pest management. Bulletin of Entomological Research 88, 493–501. Washington State University (2002) Crop Protection Guide for Tree Fruits in Washington. Washington State University Cooperative Extension Service Bulletin EB0914, 84 pp. Available at: http://cru.cahe.wsu. edu/CEPublications/eb0419/eb0419.pdf Watson, T.F. (1975) Practical consideration in the use of selective insecticides against major crop pests. In: Street, J.C. (ed.) Pesticide Selectivity. Marcel Dekker, New York, pp. 47–65. Whitcomb, W.H. and Bell, K. (1964) Predaceous insects, spiders, and mites of Arkansas cotton fields. Arkansas Agriculture Experiment Station Bulletin 690, 1–84. Wilkenson, J.D., Biever, K.D. and Ignoffo, C.M. (1979) Synthetic pyrethroids and organophosphates against the parasitoid, Apanteles marginventris and the predators Georcoris punctipes, Hippodamia convergens, and Podisus maculiventris. Journal of Economic Entomology 72, 473–475. Wright, D.J. and Verkerk, R.H.J. (1995) Integration of chemical and biological control systems for arthropods: evaluation in a multitrophic context. Pesticide Science 44, 207–218. Yoo, J.K., Kwon, U.W., Park, H.M. and Lee, H.R. (1984) Studies on the selective toxicity of insecticides for rice insect pests and a predacious spider, Pirata subpiraticus. Korean Journal of Plant Protection 23, 166–171.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 185


Manipulation of Host-finding and Acceptance Behaviours in Insects: Importance to IPM

Richard S. Cowles Connecticut Agricultural Experiment Station, Valley Laboratory, PO Box 248, Windsor, CT 06095, USA E-mail: [emailprotected]


Host Finding and Acceptance

Manipulating host-finding and acceptance behaviours can be used to shift much of a highly mobile and discriminating insect population to plants or traps outside our valued crops. Using a trap crop, insect-refuge crop, diversionary crop or mass trapping may directly reduce the population density in the valued crop below an economic threshold. Behavioural manipulation alone may often be inadequate for plant protection, but, when combined with appropriately chosen antibiosis factors (insecticides or resistant varieties), a pest-management system incorporating a behavioural dimension can yield evolutionarily stable and favourable results. The ability not only to prevent the evolution of insecticide resistance but to select against physiological resistance (both to insecticides and to varietal resistance) is an important outcome that could make behavioural manipulation an essential tool in modern agriculture. Behavioural manipulation can also lead to greater sustainability in agricultural systems by improving the efficiency of biologically based population suppression by concentrating the insect-pest population in a pesticide-free diversionary crop.

The adult female of most insects is responsible for finding appropriate hosts and laying eggs where the resources can sustain her young. With a few notable exceptions (such as ballooning larvae), the developing larvae of holometabolous insects have limited dispersal capabilities; therefore the host-seeking and host-acceptance ‘decisions’ made by the mother determine to a large degree the spatial distribution of larvae within patchy and unpredictable environments and the success or failure in larval development (Courtney and Kibota, 1989; Mayhew, 1997). For other mobile pests, such as adult hemipterans, alate aphids and thrips, arrestment on hosts and subsequent feeding may lead to direct crop injury and virus transmission (Kennedy et al., 1961). Insect behaviour adaptive for selecting favourable hosts should involve the relatively simple algorithm: move if the conditions are poor, and stop (and either feed or lay eggs) if the conditions are good. The study of insect behaviour, physiology and chemical ecology contributes to the understanding of the principles of hostfinding and acceptance by insects. With herbivorous insects, this has been a rich area for study in the field of insect–plant

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


09IntpestManCh9.QXD 14/4/04 2:25 pm Page 186


R.S. Cowles




External inhibitory inputs

External excitatory inputs

Internal excitatory inputs


Rolling fulcrum


Internal inhibitory inputs


Fig. 9.1. The rolling-fulcrum model for host-plant acceptance or rejection by insects. Sensory stimuli from each sense may contain a mixture of positive and negative factors, which, when taken in balance, determine the overall quality of the host. Acceptance or rejection events (for feeding or oviposition) are also mediated by the physiological state of the insect, which is determined by internal hormonal factors and by the negative feedback from host-acceptance or -rejection events. (Redrawn with permission from Miller and Strickler, 1984.)

interactions. Insects use intensive examining behaviours, during which cues from multiple sensory modalities combine either synchronously or sequentially, while sampling the environment to measure the potential host’s qualities. All sensory modalities may participate: olfaction, taste (comprised of any contact chemoreception), vision and tactile stimulation (Miller and Strickler, 1984; Harris and Miller, 1986; Papaj, 1986; Prokopy, 1986; Harris and Rose, 1990). At the same time that host examining is taking place, the internal physiology of the insect determines an acceptance threshold, which governs whether those external stimuli are sufficient to trigger consummatory behaviours, such as sustained feeding or egg laying. The interaction between external stimuli and internal physiological conditions was investigated in pioneering work by Dethier (1982), and later described by the physical analogy, the ‘rolling-fulcrum model’ (Miller and Strickler, 1984). This physical model depicts a seesaw (Fig. 9.1), where the sum of behavioural inputs registering positive host

stimuli (activants) contributes a downward ‘force’ on the left side. If there is sufficient force, the left side of the balance is depressed so that it triggers a host-acceptance event. However, there are also sensory stimuli from deterrents or repellents that contribute a downward force on the opposing or inhibitory side. If these inhibitory stimuli have sufficient ‘force’, the balance will tip sufficiently to trigger a host-rejection event. The physiological state influences the outcome by determining the position of the fulcrum, which rolls to the right under a state of deprivation (hunger or absence of an ovipositional outlet), thus making it easier for fewer or less intensely positive stimuli to trigger a host-acceptance event. With satiety or depleted ovaries, the fulcrum would be expected to roll far to the left, making hostacceptance events unlikely. The arrows beneath the rolling fulcrum indicate a negative-feedback control mechanism: each acceptance event contributes a signal that increases the internal inhibitory inputs, while rejection events increase internal excitatory inputs.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 187

Host Finding and Acceptance in Insects

Insect behaviour cannot be expected to work exactly like the physical model of the rolling fulcrum, because individuals may change their response to the same set of cues over time due to learning (Papaj, 1986; Papaj and Prokopy, 1988; Bernays, 2001). The rolling-fulcrum model may apply to two or more levels of sensory integration, which introduces ambiguity into our understanding of how sensory inputs affect behavioural outcomes. Even at the level of the sensory neurone, a well-defined stimulus can result in different output depending on its complex interaction with other positive and negative external stimuli and the insect’s physiological condition. For example, in the generalistfeeding gypsy moth, Lymantria dispar (Linneaus), and tent caterpillars, Malacosoma americanum (Fabricius), the firing rate of sugar receptors found on the maxillae was modulated by the presence of tannins. Thus, the caterpillar might sense the substrate containing the mixture of phagostimulants and deterrents as simply being less sweet than the same substrate without the presence of tannins (Dethier, 1982). Therefore, the ‘weight’ of the sugar stimulus apparently changes, depending on the combination of other stimuli present, making a peripheral sense organ respond virtually instantaneously, like the rolling-fulcrum model. The ability within a single sensory modality to integrate stimuli in a complex manner can make behavioural dissection of the response to host chemical stimuli very difficult. For example, green-leaf volatiles are important in the response of Colorado potato beetle to hosts, and yet each component individually has little effect on beetle behaviour (Visser and Ave, 1978). In another example, a combination of chemical compounds is required to evoke maximal upwind anemotactic response to host volatiles (Evans and AllenWilliams, 1998). Stimulus interaction can occur across several modalities over time and space with the whole animal, too. This is most easily observed with behavioural assays measuring the response of individuals or groups of insects to host models. The simplest quantitative method is to count the behavioural end result, such as numbers of eggs laid or


feeding bouts. With examples ranging from Thysanoptera to Orthoptera, Lepidoptera, Diptera, Coleoptera and others, insects appear to usually respond synergistically to combinations of visual, chemical and tactile host cues (Harris and Miller, 1982, 1986; Papaj, 1986; Gray and Borden, 1989; Harris and Rose, 1990; Judd and Borden, 1991; Szentesi et al., 1996). It is unlikely that all host cues are simultaneously processed to generate an instantaneous ‘Gestalt’ (total image) of host-plant quality; rather, the insect is selectively ‘attentive’ to particular subsets of stimuli during sequential habitatseeking, host-finding and examining behaviours (Bernays, 1996; Spencer et al., 1999). It follows, then, that several examining behaviours may be required to fully assess host qualities. For larger, strongly flying insects, detection by receptive insects of host odours can lead to odour-conditioned anemotaxis, which may take place as sustained flight or short, hopping flights (Visser and de Jong, 1987; Haynes and Baker, 1989; Evans and Allen-Williams, 1993, 1998; Byers, 1996; Szentesi et al., 1996; McDonald and Borden, 1997; Petterson et al., 1998; Barata and Araujo, 2001). Response to these odours may in turn lead to heightened responsiveness to appropriate visual cues (Bernays, 1996). Weaker fliers, such as aphids and thrips, may fly toward visual targets and simply settle on to plants as a chemokinetic response (flight arrestment) upon intercepting appropriate odour cues (Teulon et al., 1999). Sequential processing of different aspects of host stimuli could explain how information integrated over time leads to synergistic responses, and gives some insight into the evolution of efficient information processing in neurally constrained systems (Bernays, 2001). Synergism in these instances at least partly results from the effect a specific stimulus has on the insect’s probability to transition to the next finding or examining behaviour. For example, in my laboratory comparison of onion-fly finding and examining behaviours on host models, landing on red foliage was reduced by approximately 45% compared with the green foliar model, equivalent to the per cent reduction in oviposition. The presence of cinnamaldehyde

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 188


R.S. Cowles

reduced oviposition by 86%, irrespective of foliar colour, and did not measurably influence behavioural transition probabilities prior to substrate probing. The placement of this ovipositional deterrent was at the base of the foliage model, allowing interruption of the transition from foliar-examining behaviours to ovipositor probing. When considered together, these two effects, foliar colour and the presence of deterrents, are indeed synergistic, but the mechanism is through independent influence on the probability that one examining behaviour will proceed to another (Cowles, 1990). Harris and Miller (1983) also investigated the influence of foliar colour on host-acceptance behaviours, but found that, in addition to influencing foliar landing, yellow colour also influenced the post-alighting behaviours of stem-runs and substrate probing with the ovipositor. Whether an insect is attentive to one or a few host characteristics at any given time, when several steps in a sequence of behaviours lead to the insect accepting the resource, the end result is a function of the joint probability of the transition from each behaviour to another, a multiplicative function. Using Bernays’s (2001) concept of ‘selective attention’, onion flies do seem attentive first to host-associated odours, which stimulate upwind movement, followed temporally by responsiveness to visual cues (Judd and Borden, 1989, 1991). Thus, it seems parsimonious that each examining behaviour is likely to be associated with assessment of a particular subset of sensory cues from the potential host. Another example of temporal synergism is given by the study of stimulus interaction within the chemical senses of Plutella xylostella (Linnaeus) (Spencer et al., 1999). During short-term evaluation of moth behaviours, neither alkanes nor sinigrin alone stimulates much oviposition. Individual moths on substrates with stimulatory alkanes (and no sinigrin) spent a longer time on potential host substrates: affected behaviours in the presence of alkanes included arrestment components, including longer residence time, reduced movement rates and increased turning on the substrate. Sinigrin alone did not evoke arrestment or additional host-examining. There was increased oviposition when

evaluating sinigrin in overnight studies with caged moths, which can probably be attributed to their increased ovipositional deprivation. Alkanes and sinigrin in combination led to enhanced arrestment of moths on the substrate and rapidly proceeded to a critical examining behaviour and antennal swabbing (seen only in the presence of joint presentation of alkane and sinigrin), which usually immediately preceded oviposition. Perhaps additional high-resolution behavioural observation studies will lead to similar understanding of the particular cues to which insects are ‘attentive’ during specific hostexamining behaviours (Spencer et al., 1999). Investigators need to be careful when conducting studies of stimulus interactions to avoid confounding host stimuli with additional, semiochemical-based cues. For example, in the onion fly example, visual and chemical resources (presented alone) each received 2.8% of the total eggs deposited in this laboratory choice test, but the combination visual + chemical resources received 78% of the eggs (Miller and Harris, 1985). Part of this extreme degree of synergism may have been due to the additional responsiveness of examining flies to previously laid eggs and aggregation pheromones (Judd and Borden, 1992), causing a positive-feedback dynamic. Thus, the presence of egg-associated pheromones may have interfered with isolating the response to host cues, and each subsequent oviposition event was probably influenced by prior egg-laying events. Since the presence of eggs acts as an additional activant for gravid onion flies, the only way to tease out the effect of host stimuli would be to present a fly with a new host model following each egg-laying event (Judd and Borden, 1992). This example also demonstrates the importance of non-host cues (in this case, the presence of conspecifics) in the calculus of host-quality assessment.

Manipulation of Host Acceptance Behaviour: the Push–Pull Approach Insect behaviours may follow generalizable patterns that can allow us to better understand how either to ‘jam’ their signals by

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 189

Host Finding and Acceptance in Insects

making otherwise acceptable hosts deterrent or to key in on specific cues that lead to increased resource acceptance. The focus of these efforts should be to maximize the differential between those resources attracting insects and those that are deterrent. As I clarify below, neither approach alone can be expected to be entirely satisfactory, but the combined use might be successful if deterrents were applied to valued crops and attractants applied to diversionary (or trap) crops. This strategy has variously been called the ‘push–pull’ or ‘stimulo-deterrent’ approach, and was independently conceptualized in the USA by Miller (1986) and in Australia by Rice (1986). The efforts of these groups were focused on manipulating the behaviour of the onion fly (Miller and Cowles, 1990; Cowles and Miller, 1992) and of Heliothis spp. (Pyke et al., 1987). A good example for the failure of unilaterally presented attractants exists with efforts to mass-trap Japanese beetles to protect adjacent host plants. Japanese beetles appear to follow the commonly observed host-seeking modus operandi of strongly flying insects with the following features: (i) host-finding in a patchy environment probably uses upwind anemotaxis, triggered by detection of host odours by a physiologically receptive beetle; (ii) upwind flight probably increases the responsiveness of the beetle to visual cues; and (iii) the beetle lands on visually detected potential hosts within the odour plume (Bernays, 2001). Placed in this context, we can expect potent chemical attractants to lead not only to excellent trap catches, but also to increased damage by the pest in host vegetation downwind from the odour source. This was observed for Japanese beetle adult feeding close to florallure-baited traps, in which defoliation of hosts increased in relation to intensity of attractant used (the number of traps), proximity of the traps to the hosts and the location of the hosts downwind from the attractant odour source (Gordon and Potter, 1985). The same principle in host-finding behaviours is seen with the use of aggregation pheromones on trees to concentrate the attack of bark beetles (Borden et al., 1983; Gray and Borden, 1989). The release of the


mountain pine beetle’s three-component semiochemical blend resulted in attraction of beetles to the vicinity of the pheromone source and achieved the objective: to concentrate beetle attack in a small area suitable for removal of the population through logging. However, the beetles attacked not only the tree upon which the pheromone was released but also adjacent trees, presumably because these trees were downwind within the pheromone plume. This result was expected, because beetles responding to aggregation pheromones orient visually to trees while flying within the plume, with greater response towards larger-diameter trees. Arrestment prior to arriving at the source of supernormal odour stimuli (stimuli more active than those found in nature) poses a potential for damage anywhere downwind from the odour source where a responding insect may become arrested at a host. Supernormal visual stimuli, on the other hand, should not have this characteristic, because insects can directly locate the source of the visual signal (Miller and Strickler, 1984). However, even if insects take flight in response to supernormal visual stimuli, they may become arrested by odour cues prior to reaching that visual target, such as was seen with thrips (Teulon et al., 1999). These observations suggest that an especially valuable strategy would be to apply deterrents to hosts close to attractive traps or crops. Such a placement could elicit pest movement until the pest encounters the trap or attractive crop. Unilateral deployment of deterrents, repellents or crops resistant via antixenosis can also be expected to fail. The most important prediction from the rolling-fulcrum model is that insects will become accepting of deterrent, repellent or resistant hosts when deprived of highly acceptable hosts. Acceptance by insects confined to deterrent plants has been observed by many workers, and fits a theoretical framework for individual females to maximize their lifetime fitness (Roitberg and Prokopy, 1983; Fitt, 1986; Mangel, 1989; Mangel and Roitberg, 1989; Aluja and Boller, 1992). Behavioural models also predict that, if readily accepted hosts are made available,

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 190


R.S. Cowles

insects will release their consummatory behaviour on these hosts, the insect may never enter a deprived physiological state and deterrent hosts will continue to be rejected. This phenomenon can be measured in the field and the laboratory as the difference between no-choice and choice environments in the acceptance of deterrent hosts. As early as 1871, Colorado potato beetle was found to accept several resistant varieties of potato grown as monocultures (a no-choice environment), whereas in small-plot trials (with several varieties in proximity) these varieties were rejected (Casagrande, 1987). Therefore, superior ovipositional or feeding resources may have to be provided as part of the crop system if repellents or deterrents are to be useful. The practical aspects of deploying the push–pull strategy will involve: (i) finding and using stimuli that cause host rejection; (ii) finding and using stimuli that attract the pest, especially if they can be presented as supernormal stimuli; and (iii) understanding the effect of these factors on pest movement so that the two alternatives can be spatially presented in an optimal manner.

Potential Tools for Implementing the ‘Push–Pull’ Strategy What tools have potential for manipulating insect behaviour in an agricultural setting? The answer is that there are almost limitless possibilities waiting for creative investigators to exploit. The interaction of multiple sensory modalities in host recognition by insects may allow the manipulation of a very wide menu of plant or environmental characteristics to affect host finding and recognition. In a crop system designed to avoid pest deprivation, the full potential for manipulating pest behaviour has to take into account attracting and arresting pests at traps, trap crops, refuge crops or diversionary crops, while at the same time deterring or repelling the same pests from valued crops. An entire suite of cues could be used to maximize the differential movement of pests away from the valued crop and into diversionary crops, an approach not yet fully tested.

Deterrents and activants can be considered opposite sides of the same coin – investigation of host-acceptance behaviours often discloses features of hosts that are suboptimal or even deterrent. For example, fractionation of host-plant chemicals can yield both activants and deterrents (Lundgren, 1975; Doss, 1983; Renwick and Radke, 1987; Scarpati et al., 1993; Huang et al., 1994; Grant and Langevin, 1995; Honda, 1995). These examples suggest that manipulation of host biochemistry could lead to changes in the balance of attractants, phagostimulants and ovipositional deterrents in plants. Plant breeding is an obvious option for manipulation of host-plant chemistry. However, even a subtle shift in host chemistry can yield unexpected changes in acceptance by insects. For example, cucumber plants inoculated with plant growth-promoting rhizosphere bacteria emit fewer cucurbitacins, elicit reduced feeding by cucumber beetle vectors and thereby decrease the transmission of Erwinia tracheiphila (Zehnder et al., 2001). In another example, varying the nitrogen fertilization of crops can also influence the acceptance of strawberry foliage by adult black vine weevils, which probably also influences their fecundity and the spatial pattern of oviposition (Cram, 1965; Hesjedal, 1984; R.S. Cowles, unpublished data). Other chemical cues may be indirectly derived from the host plant through its interaction with insect herbivores. Olive fruit flies, Bactrocera oleae (Gmelin), cause sap to exude from olive fruits into which they have laid eggs. This sap contains several compounds, both hydrophilic and lipophilic, which act as a marking pheromone that reduces the likelihood of subsequent oviposition into that fruit (Girolami et al., 1981). Bacteria colonizing plant tissues can also modify insect response. Chemical factors maximally stimulating onion-fly oviposition are elicited not by healthy onion plants, but by onion tissue colonized by soft-rot bacteria, particularly Erwinia carotovora (Dindonis and Miller, 1980, 1981; Hausmann and Miller, 1989). If bacterial growth could be prevented in this tissue, then emission of these potent volatile cues could be reduced. While some of the chemical stimuli have

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 191

Host Finding and Acceptance in Insects

been characterized, the full complement of chemical stimuli that release onion-fly examining and oviposition is not yet completely understood (Hausmann and Miller, 1989). Perhaps the most behaviourally potent chemical cues can be expected from the pheromones and allomones of conspecifics and competitors, respectively. As recently reviewed by Borden (1997), engraver beetles are a group rich in pheromonal communication systems that can be manipulated. Complexes of species have co-evolved and compete with each other for the limited resource of susceptible phloem tissue in trees. Colonizing beetles produce volatile aggregation pheromones, which at some concentrations, along with host kairomones, attract additional conspecifics to the same tree. Mass attack of the tree, up to a certain point, is adaptive because it allows the beetles to overwhelm the tree’s defensive mechanisms (sap or resin flow). At higher concentrations, the same aggregation pheromone (with certain species) may act as an anti-aggregation pheromone, and there are several examples where the aggregation pheromone of one species can act as a deterrent for another species. These pheromones have been successfully deployed in push–pull strategies to cause outbreaks to implode rather than continuing to expand. Two examples suggest that synthetically derived attractants may perform as well as or better than compounds found naturally occurring in hosts. Males of several tephritid species are attracted to the components of trimedlure, compounds for which the natural significance remains unknown (Foster and Harris, 1997). Structure–activity relationship work with cinnamyl compounds discovered potent attractants for Diabrotica spp. that probably do not occur naturally in cucurbit flowers (Metcalf and Lampman, 1989). Thus, synthetic compounds may fit insects’ receptors and could take the place of natural compounds for use in behavioural manipulation. Lepidopteran eggs are usually deposited on the leaf surface, often accompanied by pheromones deterring oviposition by conspecifics (Behan and Schoonhoven, 1978; Klijnstra, 1986; Schoonhoven, 1990;


Schoonhoven et al., 1990; Poirier and Borden, 1991; Dempster, 1992; Gabel and Thiery, 1992; Thiery et al., 1992). Ovipositional deterrents associated with eggs have also been found with weevils (Stansly and Cate, 1984; Messina et al., 1987; Kozlow ´ ski, 1989; Credland and Wright, 1990; Ferguson and Williams, 1991; Mbata and Ramaswamy, 1995). Tephritid eggs deposited internally in fruit perhaps may not be detectable by conspecifics; however, adult females of this group commonly lay down marking pheromones on the fruit surface, which usually deters subsequent oviposition (Prokopy, 1981; Hurter et al., 1989; Straw, 1989; Aluja and Boller, 1992; Papaj et al., 1992). Oviposition-deterring pheromone has also been detected with cecidomyiids (Quiring et al., 1998), and agromyzids (Quiring and McNeil, 1984). Hessian flies may not use oviposition-deterring pheromones, but do appear to assess previous colonization of hosts and avoid infested plants when laying eggs (Kanno and Harris, 2002). The presence of other cues associated with the presence of conspecifics, such as frass (Renwick and Radke, 1980; Dittrick et al., 1983; Anderson and Lofqvist, 1996), pulverized larvae (Gross, 1984) and oral secretions (Poirier and Borden, 2000), can act as deterrents for oviposition or feeding. Presence of other herbivores on the host can also deter oviposition or feeding (Jones et al., 1988; Finch and Jones, 1989; Schoonhoven et al., 1990). Each of these examples suggests that application of synthetic pheromone could be used to prevent feeding or oviposition on plants we wish to protect. Wilson and Bossert (1963) provide a framework for understanding the behavioural consequences and longevity of pheromone cues related to their physical chemical properties. We should expect that, unlike social-insect alarm pheromones, which are small molecules that dissipate rapidly (Wilson and Bossert, 1963), oviposition-deterring pheromones will have relatively long persistence and low volatility. In one instance, the oviposition-deterring pheromone of Pieris brassicae (Linnaeus) was found to persist for 14 days on cabbage leaves under laboratory conditions

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 192


R.S. Cowles

(Schoonhoven et al., 1981). In another example, the ovipositional deterrent associated with Callosobruchus subinnotatus eggs dissipated over 4 weeks following the removal of those eggs (Mbata and Ramaswamy, 1995). Long-residual properties of synthetic ovipositional deterrents could make their application useful in agricultural systems (Averill and Prokopy, 1987; Klijnstra and Schoonhoven, 1987). Experience from field tests of specific semiochemical-based ovipositional deterrents has varied from suggesting potential for economically relevant suppression of oviposition with the host-marking pheromone of cherry fruit fly (Boller et al., 1987) to being rather disappointing with P. brassicae (Klijnstra and Schoonhoven, 1987). P. brassicae responded to its own ovipositiondeterring pheromone by decreasing contact with treated plants and flying to the edge of the field cage, where they then proceeded to lay their eggs. Unfortunately, this did not observably reduce the number of eggs laid. Together, these experiments highlight one important feature of deterrents: movement can be expected to exhibit fewer turns and longer bouts of straight travel following encounter with deterrents; this can be expected to increase the insect’s displacement from the deterrent source (Roitberg et al., 1984). Furthermore, the effectiveness of the deterrent can be expected to decrease over time if exposure is continuous and the insect becomes deprived (Roitberg and Prokopy, 1983; Aluja and Boller, 1992). As reviewed by Gould (1984) and Lockwood et al. (1984), one consequence of insecticide application is the evolution not only of physiological resistance but also of behaviours that allow the insect to avoid toxic residues. Therefore, insecticides applied to crops may already in some cases be acting as repellents or deterrents. The unfortunate side to using insecticides for deterrent or repellent properties is that these products would still have the same negative environmental consequences as if they had been applied to directly kill pests. Perhaps structure–activity relationship studies could be undertaken, using bioassays and pest populations that have evolved behavioural

avoidance responses, to find non-toxic alternatives to mimic the pesticides’ deterrent properties. Many workers have investigated plantprotective chemistry, such as essential oils, to deter or repel insects (e.g. Cowles et al., 1990). This idea is appealing, for, if we can make a plant appear to the insect sufficiently like a non-host, oviposition or feeding should be averted. One of the challenges in working with repellents is that, because they are volatile, controlled-release formulations might be necessary to allow more than a few days of effect. Larger compounds with low volatility should have better residual properties. Therefore, deterrents may have more practical value. Two compounds are particularly interesting and may play useful roles: azadirachtin has behavioural as well as insect growth-regulator properties, and so can be used as a feeding deterrent (Simmonds and Blaney, 1996). Capsaicin has nearly unique pungent flavour qualities – organisms ranging from barnacles to bears are deterred by this compound. Insects are also sensitive to capsaicin (Cowles et al., 1989). However, application of such a powerful irritant can be very unpleasant unless the operator is wearing full protective clothing. Prokopy and Owens (1983) reviewed disruption of visual stimuli used in host finding. Foliage colour may be a useful trait for plant breeders to protect some crops. For example, red varieties of cabbage were less accepted by ovipositing Delia radicum (Linnaeus) than they were of green varieties (Prokopy et al., 1983), just as red-leaf cotton varieties were less preferable to boll-weevil compared with those with green leaves (Maxwell, 1977). Reflective mulches have been investigated extensively, and have been successful in reducing transmission of viruses by aphids and thrips (Prokopy and Owens, 1983). The recent registration of kaolin-based plant protectants should give a tool for changing not only the colour characteristics but also the surface texture of plants, and perhaps even the ability of an insect to sense the plant’s surface chemistry. Kaolin is highly reflective of ultraviolet light; as such it can be used to deter aphid landing in the

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 193

Host Finding and Acceptance in Insects

same way that reflective mulches have been used in the past (Bar-Joseph and Frenkel, 1983; McBride, 2000). Other aspects of ‘jamming’ the visual system could include camouflaging plants with interplanted vegetation to obscure hosts, or even the use of lights to attract night-flying moths (Prokopy and Owen, 1983). Physical characteristics of the leaf, particularly the presence of trichomes, can dramatically affect insect feeding or oviposition. For example, black vine-weevil adult feeding preference for strawberry foliage of the commercial variety ‘Totem’ vs. the species Fragaria chiloensis, was experimentally demonstrated to be mediated by leaf hairs (Doss et al., 1987). In a similar way, obscure root-weevil adult feeding preference for different species of rhododendron is largely mediated by trichome characteristics (Doss, 1983). Pubescence of leaves can also influence ovipositional preference, as demonstrated with Chilo partellus (Swinhoe) on maize (Kumar, 1992). Leaf texture also influences pre-ovipositional behaviour in diamondback moths and Hessian flies, but these characteristics may be difficult to manipulate (Harris and Rose, 1990; Spencer et al., 1999). Perhaps application of temporarily sticky or filamentous barriers on the surfaces of plants will offer a direct method for interfering with host-examining barriers by insects on the leaf surface, and thereby prevent egg laying or feeding. Ongoing work with ethylene vinyl acetate fibres, in appearance like candy floss, has shown promise as a deterrent for onion and cabbage maggots (Friedlander, 2002). The fact that several chemicals can act together synergistically to increase host acceptance should give us hope that the opposite may also be true: that chemical deterrents in concert may synergistically decrease oviposition or feeding. Studies of onion-fly deterrents (Cowles, 1990) were inconclusive and could not reject the hypothesis that different compounds were acting in an additive fashion. Chemical deterrents may affect herbivore specialist and generalist species differently (Bernays et al., 2000; Bernays, 2001); so controlled studies investigating this hypothesis should ideally include close relatives representing both.


How might combinations of visual and chemical deterrents perform? Gravid onion flies were tested in the laboratory with various negative (or simply less positive) ovipositional stimuli, with the general resulting observation that stimuli tended to have a multiplicative effect on egg-laying behaviour (Cowles, 1990). For example, there were twice as many eggs deposited around the green as around the red foliar models and ten times as many eggs laid around models without cinnamaldehyde (a deterrent) as the one with cinnamaldehyde. The green model without deterrent elicited 33 times as much oviposition as the red model combined with cinnamaldehyde, not significantly different from the 20-fold difference predicted by a behavioural model using independent reductions in behavioural transitions. A multiplicative model for interaction between deterrents of different sensory modalities leads to an interesting result: it may be difficult to completely deter consummatory behaviours on host plants. If, for example, we could decrease oviposition with a visual deterrent by 60%, and with a chemical deterrent by 25%, the combination might be expected to reduce oviposition not by 85%, but by 70% (1 − [1 − 0.6] × [1 − 0.25]). Certain materials could dramatically change the tactile, flavour or visual appearance of plants for many species of insects, such as ethylene vinyl acetate fibres, capsaicin and kaolin, respectively. These tools may have commercial advantages for disrupting host finding and acceptance by insects in agriculture over specific deterrents (e.g. oviposition-deterring pheromones), because, like conventional pesticides, they could provide ‘broad-spectrum’ aspects for managing pest insects.

Demonstrated Application of Behavioural Manipulation in Trap Crops Manipulation of host-finding and acceptance behaviours has been practised with trap cropping for many years. Trap crops, reviewed by Hokkanen (1991), provide a resource that is more attractive to mobile pests so that they are partitioned away from

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 194


R.S. Cowles

a valued crop, thereby providing some degree of protection to the valued crop. The trap crop may be the same variety as the main crop, but planted earlier so that the older, larger plants can produce more attractants, be more visible and thus be more apparent to the mobile pest. Alternatively, the crop may be of a different species or variety from that of the main crop, and be selected for its use because it is highly attractive and receives more eggs or feeding in choice tests with the main crop. Usually, reproduction of the pest in the trap crop is prevented, either through insecticide use or crop destruction. Occasionally the trap crop is justified as a means for aggregating the pest in a crop for which control options are available, whereas these options cannot be used on the valued crop (Hunt and Whitfield, 1996; Pair, 1997). A variant of the trap crop concept is the attract–annihilate or attracticide approach, which uses behavioural manipulation to bring insects to traps, baits or insecticide deposits, with or without the presence of hosts. Behavioural manipulation for the attracticide approach has recently been reviewed (Foster and Harris, 1997). Trap crops have been used to concentrate the pest population on fewer plants, allowing a smaller area to be treated with insecticides to reduce the pest population (e.g. Pair, 1997). In rare examples, growers do not need to apply insecticides, either in the trap crop or in the valued crop. A recent example used every fifth row planted to Nicotiana kawakamii to divert oviposition by Heliothis virescens (Fabricius) from Nicotiana tabacum. The N. kawakamii appeared to not only divert oviposition from the interplanted tobacco, but may also have diverted oviposition from nearby monoculture tobacco plots, making comparison of the trap-crop effect difficult. The cultural practice of topping plants could make insecticide applications unnecessary for control of H. virescens in a valued crop of tobacco or a diversionary crop of N. kawakamii, perhaps permitting biological control agents to become better established (Jackson and Sisson, 1998). Radin and Drummond (1994) used squash as a diversionary crop to protect cucumbers from

striped cucumber beetles. A diversionary crop area of 15 and 50% of the area grown in the valued crop was equivalent for reducing pest populations in the valued crop, and prevented the cucumbers from having to be sprayed. Potatoes have been used to divert Colorado potato beetles from feeding and reproducing on tomatoes (Hunt and Whitfield, 1996). In this instance, one row of potatoes for every eight of tomatoes provided protection, as long as the potato plants were able to grow and provide sufficient resources to accommodate the beetles. Plantings of wheat have been effective as a diversionary crop for concentrating wireworms, Agriotes obscurus (Linnaeus), in strips displaced laterally from where strawberries were being planted (Vernon et al., 2000). The interplanted wheat reduced the mortality of strawberry plants from 43 to 5.3%. In the strip cropping system developed to prevent lygus damage to cotton, lucerne was kept growing in a lush manner. Preventing senescence of the lucerne required mowing two alternate strips on a 14-day schedule, which coincidentally also caused significant mortality to lygus-bug immature stages. The lygus population remained within the lucerne crop to the degree that cotton bolls were protected from feeding. An additional benefit was the reproduction of several species of generalist predators within the lucerne crop, which then aided management of other insect pests in cotton (Godfrey and Leigh, 1994). In some respects, insect pests diverted away from the valued crop system could be thought of in the same way as agronomists think of weeds. A weed can be defined as a plant growing where it is not wanted, whereas the same plant growing outside a crop might be considered a wild flower. In a parallel reasoning, populations of insects normally considered to be ‘pests’ that develop in a place or on hosts that are not intended for harvest may not be considered an economic threat, and so are not truly pests. These insect populations developing outside the valued crop may serve important ecological functions, especially as a nursery for the propagation of natural enemies and as a population reservoir that is not exposed to insecticides. Under most circ*mstances,

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 195

Host Finding and Acceptance in Insects

some intervention to prevent unconstrained reproduction of a pest in a refuge crop is necessary, otherwise a burgeoning population could have devastating consequences due to their movement from the diversionary crop to other crops more sensitive to pest feeding (Kennedy et al., 1987). However, if a pest population is highly concentrated in a diversionary crop, many density-dependent population-regulation mechanisms, including intraspecific competition, more efficient predation, parasitization and disease epizootics, may be able to suppress the population without additional intervention. Physical destruction of part of the diversionary crop to manipulate pest survival may have greater pest-management value than treating it with insecticides, as the former strategy will minimize the selection for insecticide resistance and the environmental impact on natural enemies, which may disperse to the diversionary crop remnant.

Implications for Insecticide-resistance Management Manipulation of insect behaviour in the push–pull strategy is immediately relevant to issues of insecticide resistance. Partitioning the insect population into two habitats permits survival of a non-selected population, which may, through interbreeding with the selected population, maintain the resistance allele(s), principally in a heterozygous condition (Comins, 1977). As a practical issue, these factors have been the basis for the attempt to prevent the development of resistance to insecticidal transgenic crops (valued crops) through mandated planting of non-transgenic crops as refuges (Gould, 1998). Including behavioural manipulation as part of the valued crop/refuge crop design could optimize the use of refugia by minimizing the amount of space planted to the refuge crop, while at the same time reducing the proportion of the population that ends up being selected within the valued crop. Genetic models needed for predicting the evolutionary outcome when there are interactions between behavioural traits and phys-


iological resistance can be quite complex. Gould (1984) discusses a two-gene, twoallele model with selection on behavioural traits associated with deterrency vs. physiological resistance (such as to insecticides or a crop with antibiosis-based insect resistance). Factors that need to be taken into consideration include: the quality of the treated and untreated habitats for pest survival (calculated as though the antibiosis-related mortality factor were not present), mortality due to pesticide exposure, the manner in which insect behaviour partitions the population into the two habitats and possible pleiotropic effects of carrying physiological-resistance or behavioural-avoidance alleles (i.e. fitness costs for these alleles). I included each of the components described by Gould’s (1984) model, with some modifications, into my own simulation model. For example, I incorporated a userdefined dosage-dependent mortality function for each genotype, so that manipulation of pesticide concentration on the resulting selection could be compared (Taylor and Georghiou, 1979). Gould showed the results as adaptive landscapes, in which the mean fitness for every gene-frequency combination is calculated. Theoretically, selection forces populations up the nearest ‘slope’ to increase their mean fitness. Unfortunately, the fitness for each gene-frequency combination is not mathematically unique, because each genefrequency combination can actually be represented by a large number of combinations of genotype frequencies, each with its own mean fitness value (Lewin, 1988). To display the results in my model, each combination of physiological-resistance allele frequency and behavioural-avoidance allele frequency is characterized by its evolutionary outcome. Thus, each figure is divided into four regions (at most), showing those combinations of initial gene frequencies for which subsequent generations are ‘attracted’ by selection to a ‘corner’ where the alleles become fixed. To make these figures unambiguous, a modified program tracked the gene frequencies for sample populations, starting at specific gene frequency combinations. Selection in these sample populations is shown with arrows that track the population through successive

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 196


R.S. Cowles

generations. This deterministic model operates according to the following principles: 1. The behavioural trait and physiological resistance alleles are not genetically linked. 2. There is random mating for the entire population. 3. The first generation in the model assigns Hardy–Weinberg equilibrium frequencies for the nine genotypes. 4. Each genotype’s frequency is governed by a random combination of the haploid gametes according to their proportion following selection. 5. The insects partition themselves between habitats based on the strength of habitat discrimination as determined by the avoidance trait. 6. The survival to the next generation is determined by the action on immature stages of the antibiosis factor (pesticide concentration), the quality of the habitat and the action of any pleiotropic fitness cost associated with carrying the physiological-resistance or behavioural-avoidance allele. The user of this model defines the following parameters: (i) the slope and median lethal dose (LD50) for the three physiologicalresistance genotypes; (ii) the treated and untreated habitat suitability; (iii) the probability that the AA and aa genotypes are found in the treated habitat; and (iv) the fitness cost for carrying R or a alleles. The fit-

ness costs were not used in the following simulation results. Results from this model are shown in the following figures, with the accompanying parameter values for running the models given in Table 9.1. Variations tested with this simulation model included the following pest-management strategies: a conventional insecticide-only crop with minimal pest development in a non-treated refuge with both very low (Fig. 9.2A) and high (Fig. 9.2B) dose uses of insecticides, an attracticide or lethal trap-crop approach (Fig. 9.3), a refugecrop system (Fig. 9.4) and push–pull systems investigating variations in diversionary-crop findability (Fig. 9.5) and suitability for insect development (Fig. 9.6). In the insecticide-only simulation (Fig. 9.2), the crop is assumed to be somewhat more suitable for insect development than the difficult-to-find alternative hosts, which are envisioned perhaps to consist of weeds outside the field. A consequence of the alternative crop being difficult to find, even for potential ‘avoiding’ genotypes, is that selection rapidly favours the evolution of physiological resistance. The extreme selection for physiological resistance in the low-dose situation (Fig. 9.2A) results from the disproportionate removal of hom*ozygous susceptible individuals from the population. In many respects the high-dose strategy results in a variation of the refuge-crop principle: as

Table 9.1. Parameters used for running the population-genetics simulation model presented in Figs 9.2–9.6. The use of the parameters is as described by Gould (1984). No pleiotropic fitness costs were used. Mortality from insecticide Habitat quality Fig. no. 9.2A 9.2B 9.3 9.4 9.5A 9.5B 9.6A 9.6B 9.6C

Proportion in

in treated habitat

treated habitat









0.4 0.4 0.5 0.4 0.5 0.5 0.3 0.7 0.2

0.5 0.5 0.5 0.5 0.4 0.4 0.5 0.5 0.1

0.91 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

0.49 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99

0.09 0.79 0.79 0.79 0.79 0.79 0.79 0.79 0.79

1.00 1.00 0.90 0.90 0.90 0.95 0.90 0.90 0.90

0.95 0.95 0.50 0.85 0.70 0.50 0.60 0.60 0.50

0.90 0.90 0.10 0.80 0.50 0.05 0.30 0.30 0.10

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 197

1.0 0.9


0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0

Gene frequency A (behavioural avoidance)

Gene frequency A (behavioural avoidance)

Host Finding and Acceptance in Insects


1.0 0.9


0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Gene frequency R (physiological resistance)

Gene frequency R (physiological resistance)

Fig. 9.2. Population-genetics simulation for an insecticide-based strategy for controlling the population in the valued crop and with no refuge designed in the crop system. (A) Low-dose strategy, (B) high-dose strategy. See Table 9.1 for parameter values used in the simulation.

1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Gene frequency R (physiological resistance)

Fig. 9.3. Population-genetics simulation results for an attracticide strategy, which could entail either a kairomone plus insecticide bait system, a pheromone plus insecticide or an insecticidetreated trap crop. The population would initially respond to the attractant (an aa population) and evolves to either not respond to or to avoid the attractant. See Table 9.1 for parameter values used in the simulation.

for resistance to an antibiosis factor is initially too high (Fig 9.2B), the population evolves to an avoiding and physiologically resistant genotype. In these conventional Gene frequency A (behavioural avoidance)

Gene frequency A (behavioural avoidance)

long as there is some alternative untreated habitat available, selection to a non-physiologically resistant, behaviourally avoiding population is possible. If the gene frequency

1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Gene frequency R (physiological resistance)

Fig. 9.4. Population-genetics simulation results for the high-dose refuge-crop strategy for controlling the population in the valued crop and with no behavioural modifiers used to direct the pest population to the refuge designed in the crop system. See Table 9.1 for parameter values used in the simulation.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 198

R.S. Cowles

1.0 0.9



0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Gene frequency R (physiological resistance)

Gene frequency A (behavioural avoidance)

Gene frequency A (behavioural avoidance)


1.0 0.9




0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Gene frequency R (physiological resistance)

Fig. 9.5. Population-genetics simulation results for the push–pull strategy. The high-dose approach controls the population in the valued crop, a refuge (diversionary crop) is designed into the crop system and behavioural modifiers direct the pest population to the refuge. (A) Lower findability for diversionary crop, (B) higher findability for diversionary crop. See Table 9.1 for parameter values used in the simulation.

Fig. 9.6. Population-genetics simulation results for the push–pull strategy. The high-dose approach controls the population in the valued crop, a refuge (diversionary crop) is designed into the crop system and behavioural modifiers direct the pest population to the refuge. (A) Low suitability for diversionary crop, (B) higher suitability for diversionary crop, (C) highly findable diversionary crop, with low suitability for both the valued crop and the diversionary crop. See Table 9.1 for parameter values used in the simulation.

insecticide systems, the avoidance factor is considered to be any behavioural trait that can permit the insect to detect differences between the insecticidal and untreated habitats. As an unmanipulated component to the management system, the insect’s population could easily start out either as principally avoiding (high frequency of A allele) or nonavoiding (high frequency of a allele). As Gould (1984) points out, deterrents could be added to insecticide formulations to be certain that the insect population can detect insecticides, and so will automatically start out in the upper left corner, which can be selected to an AArr population, rather than the unfavourable AARR or even less favourable aaRR genotypes. Attracticidal approaches are represented in Fig. 9.3. Representative crop systems would include trap crops, in which the pest is killed with insecticides in the trap crop, and also kairomonal insecticide (e.g. Pair,

1997) or pheromone fibre-insecticide combinations (e.g. Butler and Las, 1983). The assumption in running this model is that initial conditions for the insect population are a high degree of response to the attractant (starting predominantly as the aa genotype), and that evolution of avoidance behaviours would imply loss of the attraction. While genetic variation might be presumed to be minimal for altered response to sex pheromones or host kairomones, this model does raise the concern that the evolutionary outcome when using the attracticide system is unfavourable, and that resistance to such a strategy is likely if genetic variation for response to the attractant exists. The complex blends of pheromone components in some natural communication systems suggest that insects may already have adapted to a crowded chemical communication channel. Species using complex blends may thus be more of a concern than those using single

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 199

Host Finding and Acceptance in Insects

compounds. Insect attraction to kairomones is also complex, so there ought to be many ways in which insect populations can adapt to kairomone-based attracticides. In the high-dose refuge crop system (Fig. 9.4), populations may be selected to any of the four ‘corners’ depending on the initial gene frequencies. This model was run with the assumption that the refuge crop is not easily distinguished by the insect from the insecticidal crop, and that, if the insecticidal trait were not present, insect survival in the valued crop would be slightly better than in the refuge crop (perhaps due to a greater presence of natural enemies in the noninsecticidal habitat). By including an alternative habitat in which the pest population can develop, the gene frequency would have to be quite high to lead to selection for the physiological-resistance trait. The push–pull approach (Figs 9.5 and 9.6) is different from the refuge crop system principally in the insects’ ability to detect differences and discriminate between habitats. The pest population would initially have a high frequency for the A or avoidance allele because this would be the character(s) we would manipulate to effect discrimination between habitats (deterrents, repellents and attractants). Parameters affecting the evolutionary outcome of the push–pull approach are given, with simulations that assess combinations of the diversionary crop findability (low vs. high) and suitability (low vs. high), relative to the valued crop, which is always presumed to be protected with insecticides or genetically based antibiosis traits. In all of these simulations, the advantage to using a diversionary crop becomes apparent: behavioural avoidance is maintained


and gene frequencies need to be exceedingly high to allow selection of the population to fix the physiologically resistant R allele. One of the surprises in performing these simulations was that fairly major differences in diversionary-crop findability (Fig. 9.5) and suitability (Fig. 9.6) had little effect on the resulting selection outcomes. Although the transition line shows the expected shift to the right with improved findability and with high suitability of the diversionary crop, the overall outcome is virtually the same. Nearly any initial gene frequency will eventually lead to fixation of the A or avoidance trait, which is favourable for pest management because it maintains the pest population in the diversionary crop. I have also included an example of the kinds of parameters that I feel would be most favourable to try to design into a crop system (Fig. 9.6C). In this simulation, there is poor survival of the pest in the valued crop, slightly greater survival in the diversionary crop and high discrimination between the two habitats. With these conditions, we would have low overall survival, maintenance of behavioural preference for the diversionary crop and continued susceptibility of the population to the physiological antibiosis factor. With all simulation efforts, the user should beware of assumptions underlying the results. The assumptions of large populations mating randomly, used in these simulations, may not reflect reality. However, I hope that the overall favourable evolutionary results suggested here will spur others to investigate behavioural manipulation as a necessary component for developing sustainable agricultural systems.

References Aluja, M. and Boller, E.F. (1992) Host marking pheromone of Rhagoletis cerasi: foraging behavior in response to synthetic pheromonal isomers. Journal of Chemical Ecology 18, 1299–1311. Anderson, P. and Lofqvist, J. (1996) Oviposition deterrents from potato, wheat germ, larval frass, and artificial diet for Agrotis segetum (Lepidoptera: Noctuidae). Environmental Entomology 25, 653–658. Averill, A.L. and Prokopy, R.J. (1987) Residual activity of oviposition-deterring pheromone in Rhagoletis pomonella (Diptera: Tephritidae) and female response to infested fruit. Journal of Chemical Ecology 13, 167–177. Barata, E.N. and Araujo, J. (2001) Olfactory orientation responses of the eucalyptus woodborer, Phoracantha semipunctata, to host plant in a wind tunnel. Physiological Entomology 26, 26–37.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 200


R.S. Cowles

Bar-Joseph, M. and Frenkel, H. (1983) Spraying citrus plants with kaolin suspensions reduces colonization by the spirea aphid (Aphis citricola van der Goot). Crop Protection 2, 371–374. Behan, M. and Schoonhoven, L.M. (1978) Chemoreception of an oviposition deterrent associated with eggs in Pieris brassicae. Entomologia Experimentalis et Applicata 24, 163–179. Bernays, E.A. (1996) Selective attention and host plant specialization. Entomologia Experimentalis et Applicata 80, 125–131. Bernays, E.A. (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annual Review of Entomology 46, 703–727. Bernays, E.A., Oppenheim, S., Chapman, R.F., Kwon, H. and Gould, F. (2000) Taste sensitivity of insect herbivores to deterrents is greater in specialists than in generalists: a behavioral test of the hypothesis with two closely related caterpillars. Journal of Chemical Ecology 26, 547–563. Boller, E.F., Schöni, R. and Bush, G.L. (1987) Oviposition deterring pheromone in Rhagoletis cerasi: biological activity of a pure single compound verified in semi-field test. Entomologia Experimentalis et Applicata 45, 17–22. Borden, J.H. (1997) Disruption of semiochemical-mediated aggregation in bark beetles. In: Cardé, R.T. and Minks, A.K. (eds) Insect Pheromone Research: New Directions. Chapman & Hall, New York, pp. 421–438. Borden, J.H., Chong, L.J. and Fuchs, M.C. (1983) Application of semiochemicals in post-logging manipulation of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). Journal of Economic Entomology 76, 1428–1432. Butler, G.D. and Las, A.S. (1983) Predaceous insects: effect of adding permethrin to the sticker used in gossyplure applications. Journal of Economic Entomology 76, 1448–1451. Byers, J.A. (1996) Temporal clumping of bark beetle arrival at pheromone traps: modelling anemotaxis in chaotic plumes. Journal of Chemical Ecology 22, 2133–2155. Casagrande, R.A. (1987) The Colorado potato beetle: 125 years of mismanagement. Bulletin of the Entomological Society of America 33, 142–150. Comins, H.N. (1977) The development of resistance in the presence of migration. Journal of Theoretical Biology 64, 177–197. Courtney, S.P. and Kibota, T.T. (1989) Mother doesn’t always know best: selection of hosts by ovipositing insects. In: Bernays, E.A. (ed.) Insect–Plant Interactions, Vol. 2. CRC Press, Boca Raton, Florida, pp. 161–188. Cowles, R.S. (1990) Manipulating oviposition of the onion fly, Delia antiqua (Meigen): a stimulo-deterrent diversionary approach. Doctoral Dissertation, Michigan State University, East Lansing, Michigan. Cowles, R.S. and Miller, J.R. (1992) Diverting Delia antiqua (Diptera: Anthomyiidae) oviposition with cull onions: field studies on planting depth and a greenhouse test of the stimulo-deterrent concept. Environmental Entomology 21, 453–460. Cowles, R.S., Keller, J.E. and Miller, J.R. (1989) Pungent spices, ground red pepper, and synthetic capsaicin as onion fly ovipositional deterrents. Journal of Chemical Ecology 15, 719–730. Cowles, R.S., Miller, J.R., Hollingworth, R.M., Abdel-aal, M.T., Szurdoki, F., Baur, K. and Matolcsy, G. (1990) Cinnamyl derivatives and monoterpenoids as nonspecific ovipositional deterrents of the onion fly. Journal of Chemical Ecology 16, 2401–2428. Cram, W.T. (1965) Fecundity of the root weevils, Brachyrhinus sulcatus and Sciopithes obscurus on strawberry at different conditions of host plant nutrition. Canadian Journal of Plant Science 45, 219–225. Credland, P.F. and Wright, A.W. (1990) Oviposition deterrents of Callosobruchus maculatus (Coleoptera: Bruchidae). Physiological Entomology 15, 285–298. Dempster, J.P. (1992) Evidence of an oviposition-deterring pheromone in the orange-tip butterfly, Anthocharis cardamines (L). Ecological Entomology 17, 83–85. Dethier, V.G. (1982) Mechanism of host-plant recognition. Entomologia Experimentalis et Applicata 40, 49–56. Dindonis, L.L. and Miller, J.R. (1980) Host finding responses of onion and seedcorn flies to healthy and decomposing onions and several synthetic constituents of onion. Environmental Entomology 9, 467–472. Dindonis, L.L. and Miller, J.R. (1981) Onion fly and little house fly host finding selectively mediated by decomposing onion and microbial volatiles. Journal of Chemical Ecology 7, 419–426. Dittrick, L.E., Jones, R.L. and Chiang, H.C. (1983) An oviposition deterrent for the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), extracted from larval frass. Journal of Insect Physiology 29, 119–121.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 201

Host Finding and Acceptance in Insects


Doss, R.P. (1983) Root weevil feeding on rhododendron: a review. Journal of Environmental Horticulture 1, 67–71. Doss, R.P., Shanks, C.H. Jr, Chamberlain, J.D. and Garth, J.K.L. (1987) Role of leaf hairs in resistance of a clone of beach strawberry, Fragaria chiloensis, to feeding by adult black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae). Environmental Entomology 16, 764–768. Evans, K.A. and Allen-Williams, L.J. (1993) Distant olfactory responses of the cabbage seed weevil, Ceutorhynchus assimilis. Physiological Entomology 18, 251–256. Evans, K.A. and Allen-Williams, L.J. (1998) Response of cabbage seed weevil (Ceutorhynchus assimilis) to baits of extracted and synthetic host-plant odor. Journal of Chemical Ecology 24, 2101–2114. Ferguson, A.W. and Williams, I.H. (1991) Deposition and longevity of oviposition-deterring pheromone in the cabbage seed weevil. Physiological Entomology 16, 27–33. Finch, S. and Jones, T.H. (1989) An analysis of the deterrent effect of aphids on cabbage root fly (Delia radicum) egg-laying. Ecological Entomology 14, 387–391. Fitt, G.P. (1986) The influence of a shortage of hosts on the specificity of oviposition behaviour in species of Dacus (Diptera: Tephritidae). Physiological Entomology 11, 133–143. Foster, S.P. and Harris, M.O. (1997) Behavioral manipulation methods for insect pest-management. Annual Review of Entomology 42, 123–146. Friedlander, B.P. (2002) Cornell entomologist uses ‘cotton candy’ to protect crops as maggots and worms develop resistance to insecticides. Cornell News, 13 Feb., 2002. Available at: Gabel, B. and Thiery, D. (1992) Biological evidence of an oviposition-deterring pheromone in Lobesia botrana Den. et Schiff. (Lepidoptera, Tortricidae). Journal of Chemical Ecology 18, 353–358. Girolami, V., Vianello, A., Strapazzon, A., Ragazzi, E. and Veronese, G. (1981) Ovipositional deterrents in Dacus oleae. Entomologia Experimentalis et Applicata 29, 177–188. Godfrey, L.D. and Leigh, T.F. (1994) Alfalfa harvest strategy effect on lygus bug (Hemiptera: Miridae) and insect predator population density: implications for use as a trap crop in cotton. Environmental Entomology 23, 1106–1118. Gordon, F.C. and Potter, D.A. (1985) Efficiency of Japanese beetle (Coleoptera: Scarabaeidae) traps in reducing defoliation of plants in the urban landscape and effect on larval density in turf. Journal of Economic Entomology 78, 774–778. Gould, F. (1984) Role of behavior in the evolution of insect adaptation to insecticides and resistant host plants. Bulletin of the Entomological Society of America 30, 34–51. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, 701–726. Grant, G.G. and Langevin, D. (1995) Oviposition deterrence, stimulation, and effect on clutch size of Choristoneura (Lepidoptera: Tortricidae) species by extract fractions in host and nonhost foliage. Environmental Entomology 24, 1656–1663. Gray, D.R. and Borden, J.H. (1989) Containment and concentration of mountain pine beetle (Coleoptera: Scolytidae) infestations with semiochemicals, validation by sampling of baited and surrounding zones. Journal of Economic Entomology 82, 1399–1405. Gross, H.R. Jr (1984) Spodoptera frugiperda (Lepidoptera: Noctuidae): deterrence of oviposition by aqueous hom*ogenates of fall armyworm and corn earworm larvae applied on whorl-stage corn. Environmental Entomology 13, 1498–1501. Harris, M.O. and Miller, J.R. (1982) Synergism of visual and chemical stimuli in the oviposition behavior of Delia antiqua. In: Visser, J.H. and Minks, A.K. (eds) Proceedings 5th International Symposium on Insect–Plant Relationships. Pudoc, Wageningen, The Netherlands, pp. 117–122. Harris, M.O. and Miller, J.R. (1983) Color stimuli and oviposition behaviour of the onion fly, Delia antiqua (Meigen) (Diptera: Anthomyiidae). Annals of the Entomological Society of America 76, 766–771. Harris, M.O. and Miller, J.R. (1986) Host-acceptance behavior in an herbivorous fly, Delia antiqua. Journal of Insect Physiology 34, 179–190. Harris, M.O. and Rose, S. (1990) Chemical, color, and tactile cues influencing the oviposition behavior of the Hessian fly (Diptera: Cecidomyiidae). Environmental Entomology 19, 303–308. Hausmann, S.M. and Miller, J.R. (1989) Production of onion fly attractants and ovipositional stimulants by bacterial isolates cultured on onion. Journal of Chemical Ecology 15, 905–916. Haynes, K.F. and Baker, T.C. (1989) An analysis of anemotactic flight in female moths stimulated by host odour and comparison with the males’ response to sex pheromone. Physiological Entomology 14, 279–289.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 202


R.S. Cowles

Hesjedal, K. (1984) Influence of the nitrogen content in strawberry leaves on the fecundity of the vine weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae). Acta Agricultura Scandinavica 34, 188–192. Hokkanen, H.M.T. (1991) Trap cropping in pest management. Annual Review of Entomology 36, 119–138. Honda, K. (1995) Chemical basis of differential oviposition by lepidopterous insects. Archives of Insect Biochemistry and Physiology 30, 1–23. Huang, X.P., Renwick, J.A.A. and Sachdev-Gupta, K. (1994) Oviposition stimulants in Barbarea vulgaris for Pieris rapae and P. napi oleracea: isolation, identification and differential activity. Journal of Chemical Ecology 20, 423–438. Hunt, D.W.A. and Whitfield, G. (1996) Potato trap crops for control of Colorado potato beetle (Coleoptera: Chrysomelidae) in tomatoes. Canadian Entomologist 128, 407–412. Hurter, J., Boller, E.F., Stadler, E., Raschdorf, F. and Schreiber, J. (1989) Oviposition-deterring pheromone in Rhagoletis cerasi L.: purification and determination of the chemical constitution. In: Cavalloro, R. (ed.) Fruit Flies of Economic Importance. Proceedings of the CEC/IOBC International Symposium, 7–10 April 1987, Rome, pp. 147–148. Jackson, D.M. and Sisson, V.A. (1998) Potential of Nicotiana kawakamii (Solanaceae) as a trap crop for protecting flue-cured tobacco from damage by Heliothis virescens (Lepidoptera: Noctuidae) larvae. Journal of Economic Entomology 91, 759–766. Jones, T.H., Cole, R.A. and Finch, S. (1988) A cabbage root fly oviposition deterrent in the frass of garden pebble moth caterpillars. Entomologia Experimentalis et Applicata 49, 277–282. Judd, G.J.R. and Borden, J.H. (1989) Distant olfactory response of the onion fly, Delia antiqua, to host-plant odor in the field. Physiological Entomology 14, 429–441. Judd, G.J.R. and Borden, J.H. (1991) Sensory interaction during trap-finding by female onion flies: implications for ovipositional host-plant finding. Entomologia Experimentalis et Applicata 58, 239–249. Judd, G.J.R. and Borden, J.H. (1992) Aggregated oviposition in Delia antiqua (Meigen): a case for mediation by semiochemicals. Journal of Chemical Ecology 18, 621–635. Kanno, H. and Harris, M.O. (2002) Avoidance of occupied hosts by the Hessian fly: oviposition behaviour and consequences for larval survival. Ecological Entomology 27, 177–188. Kennedy, G.G., Gould, F., DePonti, O.M.B. and Stinner, R.E. (1987) Ecological, agricultural, genetic, and commercial considerations in the deployment of insect-resistant germplasm. Environmental Entomology 16, 327–338. Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1961) Host finding by aphids in the field. III. Visual attraction. Annals of Applied Biology 49, 1–21. Klijnstra, J.W. (1986) The effect of an oviposition deterring pheromone on egglaying in Pieris brassicae. Entomologia Experimentalis et Applicata 41, 139–146. Klijnstra, J.W. and Schoonhoven, L.M. (1987) Effectiveness and persistence of the oviposition deterring pheromone of Pieris brassicae in the field. Entomologia Experimentalis et Applicata 45, 227–235. Kozlowski, M.W. (1989) Oviposition and host object marking by the females of Ceutorhynchus floralis (Coleoptera: Curculionidae). Entomologia Generalis 14, 197–201. Kumar, H. (1992) Inhibition of ovipositional responses of Chilo partellus (Lepidoptera: Pyralidae) by the trichomes on the lower leaf surface of a maize cultivar. Journal of Economic Entomology 85, 1736–1739. Lewin, R. (1988) The uncertain perils of an invisible landscape. Science 240, 1405–1406. Lockwood, J.A., Sparks, T.C. and Story, R.N. (1984) Evolution of insecticide resistance to insecticides: a reevaluation of the roles of physiology and behavior. Bulletin of the Entomological Society of America 30, 41–50. Lundgren, L. (1975) Natural plant chemicals acting as oviposition deterrents on cabbage butterflies, Pieris brassicae (L.), P. rapae (L.), and P. napi (L.). Zoologica Scripta 4, 253–258. Mangel, M. (1989) An evolutionary interpretation of the ‘motivation to oviposit.’ Journal of Evolutionary Biology 2, 157–172. Mangel, M. and Roitberg, B.D. (1989) Dynamic information and host acceptance by a tephritid fruit fly. Ecological Entomology 14, 181–189. Maxwell, F.G. (1977) Plant resistance to cotton insects. Bulletin of the Entomological Society of America 23, 199–203. Mayhew, P.J. (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79, 417–428. Mbata, G.N. and Ramaswamy, S.B. (1995) Factors affecting the stability and recognition of the oviposition marker pheromone of Callosobruchus subinnotatus (Pic). Journal of Stored Products Research 31, 157–163.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 203

Host Finding and Acceptance in Insects


McBride, J. (2000) Whitewashing agriculture. Agriculture Research 48, 14–17. McDonald, R.S. and Borden, J.H. (1997) Host-finding and upwind anemotaxis by Delia antiqua (Diptera: Anthomyiidae) in relation to age, ovarian development, and mating status. Environmental Entomology 26, 624–631. Messina, F.J., Barmore, J.L. and Renwick, J.A.A. (1987) Oviposition deterrent from eggs of Callosobruchus maculatus: spacing mechanism or artifact? Journal of Chemical Ecology 13, 219–226. Metcalf, R.L. and Lampman, R.L. (1989) Estragole analogues as attractants for corn rootworms (Coleoptera: Chrysomelidae). Journal of Economic Entomology 82, 123–129. Miller, J.R. (1986) Cull Onions as a Trap Crop for Onion Maggot. Funded proposal of USDA Competitive Research Grants Office, Washington, DC. Miller, J.R. and Cowles, R.S. (1990) Stimulo-deterrent diversion: a concept and its possible application to onion maggot control. Journal of Chemical Ecology 16, 3197–3212. Miller, J.R. and Harris, M.O. (1985) Viewing behavior-modifying chemicals in the context of behavior: lessons from the onion fly. In: Acree, T.E. and Soderlund, D.M. (eds) Semiochemistry: Flavors and Pheromones. Walter de Gruyter, Berlin, pp. 3–31. Miller, J.R. and Strickler, K.L. (1984) Finding and accepting host plants. In: Bell, W.J. and Cardé, R.T. (eds) Chemical Ecology of Insects. Chapman & Hall, New York, pp. 127–155. Pair, S.D. (1997) Evaluation of systemically treated squash trap plants and attracticidal baits for earlyseason control of striped and spotted cucumber beetles (Coleoptera: Chrysomelidae) and squash bug (Hemiptera: Coreidae) in cucurbit crops. Journal of Economic Entomology 90, 1307–1314. Papaj, D.R. (1986) Conditioning of leaf-shape discrimination by chemical cues in the butterfly Battus philenor. Animal Behavior 34, 1281–1288. Papaj, D.R. and Prokopy, R.J. (1988) The effect of prior adult experience on components of habitat preference in the apple maggot fly (Rhagoletis pomonella). Oecologia 76, 538–543. Papaj, D.R., Averill, A.L., Prokopy, R.J. and Wong, T.T.Y. (1992) Host-marking pheromone and use of previously established oviposition sites by the Mediterranean fruit fly (Diptera: Tephritidae). Journal of Insect Behavior 5, 583–598. Petterson, J., Karunaratne, S., Ahmed, E. and Kumar, V. (1998) The cowpea aphid, Aphis craccivora, host plant odours and pheromones. Entomologia Experimentalis et Applicata 88, 177–184. Poirier, L.M. and Borden, J.H. (1991) Recognition and avoidance of previously laid egg masses by the oblique-banded leafroller (Lepidoptera: Tortricidae). Journal of Insect Behavior 4, 501–508. Poirier, L.M. and Borden, J.H. (2000) Influence of diet on repellent and feeding-deterrent activity of larval oral exudates in spruce budworms (Lepidoptera: Tortricidae). Canadian Entomologist 132, 81–89. Prokopy, R.J. (1981) Oviposition-deterring pheromone system of apple maggot flies. In: Mitchell, E.R. (ed.) Management of Insect Pests with Semiochemicals. Plenum Press, New York, pp. 477–494. Prokopy, R.J. (1986) Visual and olfactory stimulus interaction in resource finding by insects. In: Payne, T.L., Birch, M.C. and Kennedy, C.E.J. (eds) Mechanisms in Insect Olfaction. Clarendon Press, Oxford, UK, pp. 81–89. Prokopy, R.J. and Owens, E.D. (1983) Visual detection of plants by herbivorous insects. Annual Review of Entomology 28, 337–364. Prokopy, R.J., Collier, R.H. and Finch, S. (1983) Leaf color used by cabbage root flies to distinguish among host plants. Science 221, 190–192. Pyke, B., Rice, M., Sabine, G. and Zalucki, M. (1987) The push–pull strategy–behavioral control of Heliothis. The Australian Cotton Grower 8, 7–9. Quiring, D.T. and McNeil, J.N. (1984) Intraspecific competition between different aged larvae of Agromyza frontella (Rondani) (Diptera: Agromyzidae): advantages of an oviposition-deterring pheromone. Canadian Journal of Zoology 62, 2192–2196. Quiring, D.T., Sweeney, J.W. and Bennett, R.G. (1998) Evidence for a host-marking pheromone in white spruce cone fly, Strobilomyia neanthracina. Journal of Chemical Ecology 24, 709–721. Radin, A.M. and Drummond, F.A. (1994) An evaluation of the potential use of trap cropping for control of the striped cucumber beetle, Acalymma vittatta (F.) (Coleoptera: Chrysomelidae). Journal of Agricultural Entomology 11, 95–113. Renwick, J.A.A. and Radke, C.D. (1980) An oviposition deterrent associated with frass from feeding larvae of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Environmental Entomology 9, 318–320. Renwick, J.A.A. and Radke, C.D. (1987) Chemical stimulants and deterrents regulating acceptance or rejection of crucifers by cabbage butterflies. Journal of Chemical Ecology 13, 1771–1776.

09IntpestManCh9.QXD 14/4/04 2:25 pm Page 204


R.S. Cowles

Rice, M. (1986) Semiochemicals and sensory manipulation strategies for behavioral management of Heliothis spp. Oshsenheimer (Lepidoptera: Noctuidae). In: Zalucki, M.P. and Twine, P.H. (eds) Heliothis Ecology Workshop 1985 Proceedings. Queensland Department of Primary Industries, Brisbane, Australia, pp. 27–45. Roitberg, B.D. and Prokopy, R.J. (1983) Host deprivation influence on response of Rhagoletis pomonella to its oviposition deterring pheromone. Physiological Entomology 8, 69–72. Roitberg, B.D., Cairl, R.S. and Prokopy, R.J. (1984) Oviposition deterring pheromone influences dispersal distance in tephritid fruit flies. Entomologia Experimentalis et Applicata 35, 217–220. Scarpati, M.L., Lo-Scalzo, R. and Vita, G. (1993) Olea europaea volatiles attractive and repellent to the olive fruit fly (Dacus oleae, Gmelin). Journal of Chemical Ecology 19, 881–891. Schoonhoven, L.M. (1990) Host-marking pheromones in Lepidoptera, with special reference to two Pieris spp. Journal of Chemical Ecology 16, 3043–3052. Schoonhoven, L.M., Sparnaay, T., van Wissen, W. and Meerman, J. (1981) Seven-week persistence of an oviposition-deterrent pheromone of Pieris brassicae on cabbage plants. Journal of Chemical Ecology 7, 583–588. Schoonhoven, L.M., Beerling, E.A.M., Klijnstra, J.W. and van Vugt, Y. (1990) Two related butterfly species avoid oviposition near each other’s eggs. Experientia 46, 526–528. Simmonds, M.S.J. and Blaney, W.M. (1996) Azadirachtin: advances in understanding its activity as an antifeedant. Entomologia Experimentalis et Applicata 80, 23–26. Spencer, J., Pillai, S. and Bernays, E.A. (1999) Synergism in the ovipositional behavior of Plutella xylostella: sinigrin and wax compounds. Journal of Insect Behavior 12, 483–500. Stansly, P.A. and Cate, J.R. (1984) Discrimination by ovipositing boll weevils (Coleoptera: Curculionidae) against previously infested Hampea (Malvaceae) flower buds. Environmental Entomology 13, 1361–1365. Straw, N.A. (1989) Evidence for an oviposition-deterring pheromone in Tephritis bardanae (Schrank) (Diptera: Tephritidae). Oecologia 78, 121–130. Szentesi, A., Hopkins, T.L. and Collins, R.D. (1996) Orientation responses of the grasshopper, Melanoplus sanguinipes, to visual, olfactory and wind stimuli and their combinations. Entomologia Experimentalis et Applicata 80, 539–549. Taylor, C.E. and Georghiou, G.P. (1979) Suppression of insecticide resistance by alteration of gene dominance and migration. Journal of Economic Entomology 72, 105–109. Teulon, D.A., Hollister, B., Butler, R.C. and Cameron, E.A. (1999) Color and odor responses of flying western flower thrips: wind tunnel and greenhouse experiments. Entomologia Experimentalis et Applicata 93, 9–19. Thiery, D., Gabel, B. and Pouvreau, A. (1992) Semiochemicals isolated from the eggs of Ostrinia nubilalis as oviposition deterrent in three other moth species of different families. Series Entomologica 49, 149–150. Vernon, R.S., Kabaluk, T. and Behringer, A. (2000) Movement of Agriotes obscurus (Coleoptera: Elateridae) in strawberry (Rosaceae) plantings with wheat (Graminae) as a trap crop. Canadian Entomologist 132, 231–241. Visser, J.H. and Ave, D.A. (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsus decemlineata. Entomologia Experimentalis et Applicata 24, 738–749. Visser, J.H. and de Jong, R. (1987) Plant odour perception in the Colorado potato beetle: chemoattraction towards host plants. Series Entomologica 41, 129–134. Wilson, E.O. and Bossert, W.H. (1963) Chemical communication among animals. Recent Progress Hormone Research 19, 673–716. Zehnder, G.W., Murphy, J.F., Sikora, E.J. and Kloepper, J.W. (2001) Application to rhizobacteria for induced resistance. European Journal of Plant Pathology 107, 39–50.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 205


Integrated Pest Management in Forestry: Potential and Challenges

Imre S. Otvos Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, 506 West Burnside Road, Victoria, B.C., V8Z 1M5, Canada E-mail: [emailprotected]

Introduction The forest ecosystem is much more complex and resilient than that of agriculture and the threshold level of damage caused by insects or pathogens is much higher in forestry than what most consumers are willing to accept on or in their fruits or vegetables. When a certain segment of the population is protesting, sometimes unlawfully, even against the proper and judicious use of pesticides in the forest environment, they should stop and think about the number of chemical sprays it takes to keep their apples and tomatoes free of blemish. They should also think of the home gardener and the number of sprays it takes to keep their roses free of aphids or other ‘creepy-crawlies’. This chapter will briefly summarize events leading up to the development of integrated pest management (IPM). Due to the vastness of the candidate subject, only the stages and progression towards IPM in forestry will be illustrated by giving Canadian examples from my perspective. The main objectives that will be dealt with and covered include a review of the biological control of forest insects in Canada (mainly parasitoid introductions and work with insect viruses). The evolution of IPM will be

illustrated with three examples, two involving native species and one an introduced species, i.e. spruce budworms (illustrating the transition from the use of chemical to biological pesticides), Douglas fir tussock moth (DFTM) (development of the first truly IPM for a defoliator) and gypsy moth (an introduced species that became established in eastern North America, but is still treated as a quarantine pest in western North America). Management of bark beetles, contributions in forest weed and plant-pathogen control and, finally, a perspective on the future potentials and challenges of IPM in forestry, exotic insects, decreasing pesticide use, genetic engineering of entomopathogens and transgenetic trees will be discussed.

Importance of Forestry in Canada Forestry is important to the Canadian economy, but this importance is not reflected in the amount of money dedicated to research of forest pest-related problems, which in many cases is lower than that provided in other countries where forestry is also an important part of the economy. Even so, it is postulated that the development of insect control in forests of other countries where

© CAB International 2004. Integrated Pest Management: Potential, Constraints and Challenges (eds O. Koul, G.S. Dhaliwal and G.W. Cuperus)


10IntpestManCh10.QXD 5/5/04 2:09 pm Page 206


I.S. Otvos

forestry is also important to the economy has followed a similar path to that of Canada. The forests of Canada occupy 45.3% (418 million ha) of the country’s total land area. Of this, 245 million ha, about 58.6%, is productive forestland (Lowe et al., 1996; FAO, 2002). Canada has 15.6% of the world’s softwood timber resource (19.3 billion m3), and is only exceeded by that of the former Soviet Union (60.4%). Canada is a major supplier of forest products in the world: in 1999, it accounted for 13.5% of the world’s total coniferous tree harvest, ranking third after the USA at 26.7% and Europe at 17.9% (Council of Forest Industries, 2000). In 1999, Canada produced 21.2% of the world’s softwood lumber, and this represented about 47.8% of the world’s softwood lumber exports (Council of Forest Industries, 2000). The value of forest-product exports in 2001 was about CAN$44.1 billion. In the same year, the net foreign-exchange earnings from forestry were about $34.4 billion. This represents the second greatest contribution to the economy of Canada after energy production (Statistics Canada, 2002). Most of the forests in Canada are publicly owned. As the land base managed for timber and other forestry use is shrinking and the size of the forest set aside for parks and ecological reserves is increasing, the appetite and demand of the increasing population has to be met from a smaller forest land base. Therefore, the losses caused by insects, disease and fire activity must be reduced. The average annual volume loss due to forest insect pests for 1988–1992 is estimated at 5.9 million m3. This is less than the estimated 20.9 million m3 volume loss caused by diseases, but is more than double the 2.7 million m3 burned from 1988–1992 and constitutes 6% of the 102.3 million m3 annual harvest (Wood and Van Sickle, 1994).

Biological Control of Forest Insects in Canada Both inoculative and inundative methods of insect control have been used in forestry, with varying degrees of success. Classical biological control has great appeal to forest

entomologists because, in forestry, pest control does not always have to be immediate and the threshold level of economic damage is higher than in agriculture or horticulture and some damage can often be tolerated. Classical biological control was first used in Canada’s forests against exotic insects, which were almost always introduced without their natural enemies. The use of biological control in Canada has a long history, starting in 1910 with the introduction of over 1000 specimens of the ichneumonid wasp, Mesoleius tenthredinis Morley, from England to control the larch sawfly, Pristiphora erichsonii Hartig (McGugan and Coppel, 1962). Since that time, considerable use has been made of the natural enemies of insects, using first insect parasitoids and predators and more recently entomopathogens. The majority of attempts to control insect pests in Canada using biological agents used only one group of organisms – parasitoids. In some cases a combination of two groups – generally parasitoids and nucleopolyhedrovirus (NPV) – were used, and occasionally three groups – parasitoids, NPV and Bacillus thuringiensis subsp. karstäki (Btk). The best known example of the latter is gypsy moth. Biological control attempts against the spruce budworm have even tried to use a fourth agent, microsporidia. Results of biological control attempts in Canada have been documented in detail in the four volumes of Biological Control Programmes Against Insects and Weeds in Canada (McGugan and Coppel, 1962; Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry, 1971; Kelleher and Hulme, 1984; Mason and Huber, 2002). Hulme (1988) has also published a brief summary of some of the highlights. Figure 10.1 shows that the biological control attempts were entomocentric, most of the targets were insects (both agricultural and forest pests) and most of the control agents introduced were also insects. Considerably fewer control programmes were conducted on weeds and there was no work done on plant pathogens until the last two decades (Fig. 10.1). Only control attempts using parasitoids and insect viruses will be discussed in this section.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 207

60 50 40 30 20 10 0

Insects Weeds

0 00

81 19

–1 69 19



96 –1

95 –1

59 19

10 19




Number of targets

IPM in Forestry

Fig. 10.1. Comparison of the number of biological control projects conducted against insects, weeds and plant pathogens in Canada between 1910 and 2000 (after Mason and Huber, 2002).

Canada was one of the leaders of classical biological control, in both agriculture and forestry. There were three main reasons for this: ● In the past, most invasive species in North America came from Europe, reflecting past trading patterns and routes (Mattson et al., 1994; Niemela and Mattson, 1996). ● The value of biological control in Canada was recognized at an early date. ‘Throughout the history of classical biological control in Canada a close link has existed between CAB International (formerly IIBC or CIBC) in Delemont, Switzerland, and Agriculture and AgriFood Canada (AFC, formerly Agriculture Canada) and Canadian Forest Service laboratories’ (Mason et al., 2002: xiii). ● ‘The first biological control laboratory was established in Canada … in Fredericton in 1912 … [then] The Dominion Parasite Laboratory was established in 1929 at Belleville [Ontario] …’ (Wallace, 1995) and was operating until 1972, when it was closed due to cutbacks and government reorganization. Regarding the Belleville laboratory, Mason et al. (2002: xiii) state: ‘This laboratory had one of the largest concentrations of biological control specialists in the world.’


Since the early 20th century, biological control attempts have been conducted against 22 exotic forest insects (Table 10.1) and 27 native forest insects (Table 10.2) in Canada. In most cases the biocontrol agents used were parasitoids, pathogens (mainly viruses and Btk) and in a few cases predators. Some of the early introductions were only explorative and tentatively assessed (McGugan and Coppel, 1962), and a re-evaluation of the outcomes of all the introductions may be in order. Of the 22 exotic forest pests, 17 had a single control-agent group (parasitoids) introduced to control them. Of the 17 species, the introduction was considered successful against eight (47%), resulting in long-term control that suppressed the pest, virtually eliminating the damage without need for further direct application of the control. The introduction of parasitoids was partially successful against two species, promising against three species, unknown in two cases and two were classified as failures. In the case of the remaining five exotic species, the introduction of two (usually parasitoid and NPV) or three natural control-agent groups occurred. The outcome of these introductions was successful with at least one of the control-agent groups (Table 10.1). When one is evaluating the control outcome of pathogen use, it is worth considering the difference between the use and success of NPV and Btk in biological control. NPV is to some degree self-propagating after it has been applied, and is usually applied only once during the course of an outbreak to achieve control, while Btk almost always has to be applied annually until the outbreak collapses or, in the case of quarantine pests, until the target insect is eradicated. In some cases, Btk has to be applied several times in a season and maybe for a number of years to achieve the desired level of control. An example of the latter is gypsy-moth eradication in western North America, where Btk is applied three or four times to the susceptible stage in the course of a year for 2–3 years until eradication is achieved. Therefore, it should be noted that although the use of bacterium (Btk) application is classified as a success, it should be classified as a ‘success’ only

Winter moth

Red-headed sawfly

European pine sawfly Swaine jack pine sawfly

Operophtera brumata (Linnaeus)

Neodiprion lecontei (Fitch)

Neodiprion sertifer (Geoffroy)

Neodiprion swainei (Middleton)


Parasitoids Parasitoids Parasitoids Parasitoids Parasitoids Parasitoids Parasitoids Parasitoids Predators Parasitoids Parasitoids Parasitoids Bacterium Parasitoids Parasitoids Predators Parasitoids Parasitoids Bacterium NPV Parasitoids Bacterium NPV Parasitoids Bacterium NPV Parasitoids NPV Predators Parasitoids NPV

Success Success Success Success Success Success Success Success Partial success Partial success Promising Promising Promising Failure Failure Unknown Unknown [Partial] success [Partial] success Partial success Success [Partial] success Partial success Success [Partial] success Success Success Success Partial success Partial success Success


The list was compiled from the four volumes of the review of biocontrol programmes in Canada (McGugan and Coppel, 1962; Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry, 1971; Kelleher and Hulme, 1984; Mason and Huber, 2002). It should be noted that the classification categories under ‘outcome’ are somewhat confusing. Success can mean: (i) the introduction was successful and the organism became established and has an impact on the original target host but it does not necessarily control the pest (e.g. parasitoid introduction or the use of Btk against the gypsy moth); or (ii) the target organism is under control now after the introduction (e.g. larch sawfly or the winter moth). These will be clarified in a later re-analysis of the control attempts.

Larch case-bearer Lecanium scale Birch leaf-miner Satin moth Introduced pine sawfly European spruce sawfly Larch sawfly Mountain ash sawfly Balsam woolly adelgid European pine-shoot moth Pine false web-worm Amber-marked birch leaf-miner Elm-leaf beetle Juniper scale Birch case-bearer Brown-tail moth Nursery pine sawfly Gypsy moth

Coleophora laricella (Hübner) Eulecanium tiliae (Linnaeus) Fenusa pusilla (Lepeletier) Leucoma salicis (Linnaeus) Diprion similis (Hartig) Gilipnia hercyniae (Hartig) Pristiphora erichsonii (Hartig) Pristiphora geniculata (Hartig) Adelges piceae (Ratzeburg) Rhyacionia buoliana (Denis and Schiffmuller) Acantholyda erythrocephala (Linnaeus) Profenusa thomsoni (Konow) Xanthogaleruca luteola (Müller) Carulaspis juniperi (Bouche) Coleophora serratella (Linnaeus) Euproctis chrysorrhoea (Linnaeus) Gilpinia frutetorum (Fabricius) Lymantria dispar (Linnaeus)

Control agent



Common name

Target pest

Table 10.1. Evaluation of the biological control attempts against exotic forest insect pests in Canada between 1910 and 2000.a

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 208

I.S. Otvos

Common name Western black-headed budworm Eastern black-headed budworm Striped alder sawfly Lodgepole needle miner Spruce seed moth Western oak looper White pine weevil Pine needle miner Balsam twig aphid Jack pine sawfly Red pine sawfly Hemlock sawfly Pine sawfly Bruce spanworm Pine bark adelgid Eastern spruce beetle Spruce budworm

Westerm spruce budworm

Jack pine budworm Hemlock looper Western hemlock looper

Target pest

Acleris gloverana (Walsingham) Acleris variana (Fernald) Hemichroa crocea (Geoffroy) Coleotechnites starki (Freeman) Cydia strobilella (Linnaeus) Lambdina fiscellaria somniaria (Hulst) Pissodes strobi (Peck) Exoteleia pinifoliella (Chambers) Mindarus abietinus Koch Neodiprion pratti Dyar Neodiprion nanulus Schedl Neodiprion tsugae Middleton Neodiprion virginianus complex Operophtera bruceata (Hulst) Pineus strobi (Hartig) Dendroctonus rufipennis (Kirby)

Choristoneura fumiferana (Clemens)

Choristoneura occidentalis Freeman

Choristoneura pinus pinus Freeman

Lambdina fiscellaria fiscellaria Guenée

Lambdina fiscellaria lugubrosa Hulst

Bacterium Bacterium Parasitoids Parasitoids Parasitoids Predators Parasitoids Parasitoids Predators Parasitoids Parasitoids Parasitoids Parasitoids NPV Predators Predators Parasitoids Parasitoids Bacterium NPV Other viruses (CPV, GV, EV) Microsporidia Bacterium NPV Other viruses (CPV, GV, EV) Bacterium NPV Parasitoids Bacterium Predator

Control agent

Table 10.2. Evaluation of the biological control attempts against native forest insect pests in Canada between 1910 and 2000.a

IPM in Forestry

Continued on next page

Partial success Partial success Success Failure Failure Failure Failure Unknown Unknown Unknown Unknown Unknown Unknown Unknown Unknown Failure Failure Partial success Partial success Partial success Partial success Partial success Partial success Partial success Partial success Success Success Failure Partial success Unknown


10IntpestManCh10.QXD 14/4/04 2:26 pm Page 209


White-marked tussock moth Douglas fir tussock moth Spruce bud moth

Balsam fir sawfly

Yellow-headed spruce sawfly

Orgyia leucostigma (J.E. Smith)

Orgyia pseudotsugata (McDunnough)

Zeiraphera canadensis Mutuura and Freeman

Neodiprion abietis (Harris)

Pikonema alaskensis (Rohwer)


Parasitoids Bacterium NPV Microsporidia Bacterium NPV Bacterium NPV Parasitoids Bacterium Nematodes Parasitoids Bacterium NPV Parasitoids Bacterium Nematodes

Success Partial success Failure Failure Partial success Success Partial success Success Failure Failure Partial success Unknown Partial success Unknown Unknown Partial success Success


The list was compiled from the four volumes of the review of biocontrol programmes in Canada (McGugan and Coppel, 1962; Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry, 1971; Kelleher and Hulme, 1984; Mason and Huber, 2002). It should be noted that the classification categories under ‘outcome’ are somewhat confusing. Success can mean: (i) the introduction was successful and the organism became established and has an impact on the original target host but it does not necessarily control the pest (e.g. parasitoid introduction or the use of Btk against the gypsy moth); or (ii) the target organism is under control now after the introduction (e.g. larch sawfly or the winter moth). These will be clarified in a later re-analysis of the control attempts.

Forest tent caterpillar

Malacosoma disstria Hübner

Control agent



Common name

Target pest

Table 10.2. Continued from previous page.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 210

I.S. Otvos

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 211

IPM in Forestry

in cases of eradication (gypsy moth from western North America). In other cases, when Btk is applied to reduce the pest population, its use should perhaps be classified as partial success, since it generally has to be applied for a number of consecutive years. Control attempts were made against 27 native forest insects using parasitoids, predators and pathogens: 15 by a single group and 12 by multiple groups of organisms (Table 10.2). Of the single-group introductions against native pests, three (12%) of the 15 were classified as successful, four (26.7%) as failures and the remaining eight (53.3%) as unknown. Of the 12 other native pests targeted with multiple-group introductions, one (eastern spruce beetle) was a failure, and for the other 11 species at least one of the biological control agents tried was successful. It should be noted that the outcome ‘success’ means that the biological control agent tried/introduced became established (in the case of parasitoids and predators), maintained its population and attacked and killed a portion of the target pest. In the case of pathogens (either virus or Btk) success meant that it infected and killed a proportion of the target insect and the introduced organisms did not necessarily produce an acceptable level of control over the pest. The case of Choristoneura fumiferana (Clemens) illustrates this point well. All the control agents listed in Tables 10.1 and 10.2 had an effect and therefore could be classified as a ‘success’, but in terms of control all five groups had only partial success because the spruce budworm still has to be controlled, i.e. by applying one of the control-agent groups listed. Data are scarce on the benefits and monetary return of the cost of developing and applying classical biological control measures. No thorough cost–benefit analysis has been done in Canada on the use of biological control. However, one such summary was compiled for biological control activities in Australia. Of the 12 biological control attempts conducted, all were analysed, twothirds were considered successful and the overall cost:benefit ratio, based on all 12 attempts, was 1:10 (Marsden et al., 1980). Hulme (1988) cited two cost : benefit estimates from Canada. Biological control of the


European spruce sawfly cost about CAN$300,000 and saved 8.5 million cords of wood valued at CAN$6 million, giving a cost : benefit ratio of 1:20 (Reeks and Cameron, 1971). In the case of another defoliating insect, the winter moth, the cost of introducing parasitoids into eastern Canada was estimated at $160,000 and the value of the oak trees killed before the introduction was estimated at CAN$2 million. The introduction of parasitoids prevented the loss of another CAN$12 million worth of oak trees. Based on these, the cost:benefit ratio was estimated at 1:12.5 (Embree, 1971).

Viral insecticides Interest in the use of viruses for forest insect control in Canada began in the late 1930s with the discovery of a polyhedrovirus that was credited with causing the collapse of a large outbreak of the European spruce sawfly, Gilpinia hercyniae Hârtig, the most important forest defoliator at that time (Balch and Bird, 1944; Cameron, 1975a). The European spruce sawfly virus had been accidentally introduced from Europe, probably along with one of the imported parasitoids of the sawfly. The impressive beneficial effect of this accidental virus introduction resulted in accelerated work with insect viruses in the hope that outbreaks of various other pests could also be terminated with viruses, similar to that of the European spruce sawfly. Most of the work to develop viral insecticides for several insect pests has been done on NPVs and granuloviruses (GV), subgroups A and B, respectively, of the family Baculoviridae. Limited work has also been conducted on cytoplasmic polyhedroviruses (CPVs – Reoviridae) and entomopox virus (EPV – Poxviridae) as potential control agents for the spruce budworm (Table 10.3; Cunningham and Kaupp, 1995). NPVs and GVs are highly host-specific, although some viruses may infect several related species in the same genus (Cunningham and Kaupp, 1995), e.g. Orgyia spp. Their high host specificity makes viral insecticides ideal from an ecological point of

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 212


I.S. Otvos

Table 10.3. Research and operational applications of insect viruses against the more important forest defoliators in Canada, 1971–2000 (Kelleher and Hulme, 1984; Mason and Huber, 2002). Target insect Common name

Scientific name



Spruce budworm Spruce budworm Spruce budworm Spruce budworm Western spruce budworm Western spruce budworm Jack pine budworm Gypsy moth Forest tent caterpillar Balsam fir sawfly European pine sawfly Red-headed pine sawfly White-marked tussock moth Douglas fir tussock moth

Choristoneura fumiferana Choristoneura fumiferana Choristoneura fumiferana Choristoneura fumiferana Choristoneura occidentalis Choristoneura occidentalis Choristoneura pinus pinus Lymantria dispar Malacosoma disstria Neodiprion abietis Neodiprion sertifer Neodiprion lecontei Orgyia leucostigma Orgyia pseudotsugata


1971–2000 1979–1980 1971–1972 1972 1976–1982 1982 1985 1982–1994 1976–1980 1999 1975–1993 1976–1995 1975–1987 1974–1993

a b c d e


Total area sprayed ha/tp 2180a 16 519 32b 252 172 50 1280c 45 4 152 5881 43 2620

Includes 16 ha sprayed with NPV and fenitrothion. Includes 16 ha sprayed with NPV + EPV and fenitrothion. Cunningham (1998). Red-headed pine sawfly NPV was registered in 1987 as Lecontvirus. Douglas fir tussock moth NPV was registered under the names Virtuss® (OpNPV produced in Orgyia leucostigmata) and TM-Biocontrol-1 (OpMNPV produced in Orgyia pseudotsugata). tp, time period.

view, but it also makes their development and commercialization less attractive for profit-making companies. Consequently, all development work and registration of viruses for forestry use in Canada was done in the laboratories of the Canadian Forest Service, in cooperation with some of the provincial governments. Field trials using viruses have been conducted on 19 species of forest insect pests in Canada; 11 Lepidoptera and eight Hymenoptera. Both aerial and ground trials were conducted on eight species, while the remainder were tested with ground applications only (Cunningham and Kaupp, 1995). The more important virus tests for ten insects are summarized in Table 10.3. The control of the European spruce sawfly, Gilpinia hercyniae (Hartig), may be the best example of a biological control programme in Canada. It was an important pest of spruce trees in eastern Canada and the USA. Twenty-seven species of parasitoids from Europe and Japan were released

between 1933 and 1951, of which nine became established (McGugan and Coppel, 1962). In the late 1930s an NPV was noticed in the sawfly populations and was the key factor in controlling this sawfly (Balch and Bird, 1944). The virus was fortuitously introduced with parasitoids from Europe. After the virus epizootic in central Canada, the virus was purposefully transferred to a number of new locations in eastern Canada (McGugan and Coppel, 1962). The outbreak collapsed in the early 1940s and the European spruce sawfly has been controlled since then by the introduced parasitoids and the virus, as no further outbreaks recurred. Similarly, the red-headed pine sawfly, Neodiprion lecontei Fitch, is one of the most important insects attacking young red pine, Pinus resinosa Aiton, plantations in eastern Canada. An NPV was found in red-headed pine sawfly in 1950 (Bird, 1961), and extensive laboratory and ground-spray trials conducted on the virus showed promise (Cunningham and de Groot, 1984;

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 213

IPM in Forestry

Cunningham et al., 1986). The virus was tested experimentally between 1978 and 1980 in Quebec in 92 plantations with a combined area of 1051 ha. The virus was also tested in Ontario between 1980 and 1990 in 478 plantations with a combined area of 3546 ha. Based on these successful applications, the virus received temporary registration in 1983 and full registration in 1987 under the trade name Lecontvirus®. The production of this and other similar viruses in colony-feeding sawflies is relatively easy and cost effective. Heavily infested plantations are treated with the virus by mist-blowers and the dead colonies are collected daily (preferably), starting 1 week after treatment (Cunningham and McPhee, 1986). Orgyia pseudotsugata (McDunnough) is a native defoliator in British Columbia, Canada and the north-western USA. Outbreaks of this defoliator recur periodically and are terminated by an epizootic caused by a native NPV. This naturally occurring virus was considered to have an excellent potential for biological control both in Canada and in the USA. The work on the virus and how the virus was incorporated into an IPM system is described later in this chapter. C. fumiferana is the most important forest insect pest in Canada and, as such, has had the greatest number of biological control agents tested against it (Tables 10.2 and 10.3). Because attempts to control it by parasitoid introduction (from Europe and Japan) or relocation (from western Canada to eastern Canada) did not provide the desired control, insect viruses were also investigated. Extensive field trials with NPV, GV and EPV showed NPV to be the most efficacious virus tested (Cameron, 1975b). Consequently, research concentrated on NPV (Cunningham and Howse, 1984; Cunningham, 1985a). NPV and GV were also tested against the western spruce budworm, Choristoneura occidentalis Freeman (Otvos et al., 1989) and the jack pine budworm, Choristoneura pinus Freeman (Table 10.3). While virus infection occurred in the treated plots, mortality was generally low (40–60%) and not sufficient to control the treated populations. Although virus does occur in budworm populations in the field, natural virus epizootics have never been


observed. Because of the economic importance of the spruce budworm, genetic manipulation of its virus to enhance its effectiveness was a high priority of the Canadian government (Cunningham and Kaupp, 1995). However, no significant advancements were made in improving virus efficacy over the last 20 years and Btk is still the only pathogen registered for budworm control.

Viruses registered for forest insect control in Canada Following the more important virus trials described above, three viral insecticides, all NPVs, received temporary registration in 1983 and full registration in Canada in 1987: one for the red-headed pine sawfly, N. lecontei, and two for the control of DFTM, O. pseudotsugata. The multicapsid isolate of the DFTM virus (OpMNPV), produced in DFTM larvae, was registered in the USA in 1976 under the trade name TM Biocontrol1®. The same product, under the same trade name, TM Biocontrol-1, was also registered for use in Canada in 1987. In addition, the same virus, produced in Canada in the white-marked tussock moth, Orgyia leucostigma (J.E. Smith), also received full registration in 1987 under the trade name Virtuss® (Cunningham and Kaupp, 1995). The recommended dosage on the label for both viruses is 2.5 1011 polyhedral inclusion bodies (PIB) per hectare (Cunningham and Kaupp, 1995). Negotiations are currently underway in Canada to transfer the production and sale of these three registered viruses to a private company for commercialization. The use of these three registered viruses is insignificant compared with the use of Btk.

Management of Spruce Budworms (Choristoneura spp.) Development of the management system currently used for the spruce budworms (Choristoneura spp.) illustrates well how the control for these important defoliators evolved, from the use of a single hard chemical to the use of the ecologically less disrup-

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 214

I.S. Otvos

Area defoliateda (’000,000 ha)


Area defoliated


Area treated



16 14


12 10


8 20

6 4



Percentage of defoliated area treated with chemical insecticides


95 19

90 19



80 19



Year Fig. 10.2. Area defoliated by spruce budworm, Choristoneura fumiferana, from 1975 to 1995 and the percentage of defoliated area treated with insecticides for the same years (from Canadian Council of Forest Ministers, 2003). a

Only areas that were moderately or severely defoliated were included in the source data.

tive bacterial insecticide Btk. Before the management system is discussed, it is worthwhile to sketch the economic importance of the insect over time. The change in economic importance has influenced our response to damage. It is also useful to mention key research activities (including attempts to use biological control agents) that were undertaken in the hope of increasing our control options for these budworm pests. The evolution of budworm control measures in Canada is representative of how control measures evolved for most forest defoliators, not only in Canada, but in other parts of the world as well. Economic importance of spruce budworms Among the forest defoliators in Canada, three budworms are the most important. These are the: ● spruce budworm, C. fumiferana (Clemens); ● western spruce budworm, C. occidentalis Freeman; ● jack pine budworm, C. pinus pinus Freeman.

All three are native to North America and outbreaks have occurred repeatedly over the last three centuries (Blais, 1985; Harris et al., 1985a). They pose a threat to approximately 60 million ha of susceptible forests in eastern Canada and the USA (Nigam, 1980; Kettela, 1983; Talerico, 1984). Budworm larvae feed on a number of conifer species, and consecutive years of defoliation result in growth reduction, top kill and, ultimately, tree mortality (Alfaro and Maclauchlan, 1992). Normally, 4–5 years of severe defoliation are required to kill susceptible trees and approximately 7–8 years to kill less vulnerable, immature stands (MacLean, 1980). Prior to the 1940s, spruce budworm damage was of little concern because its principal host, balsam fir, Abies balsamea (L.) Miller, was considered a weed species and was not utilized. As the demand for wood increased, balsam fir became an important commodity. Due to this change in forest utilization, the damage caused during the budworm outbreak in the 1940s was considered unacceptable. Extensive spray operations were initiated and had to be continued, unfortunately, almost annually somewhere in Canada

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 215

IPM in Forestry

(Prebble, 1975; van Frankenhuyzen, 1990) up to the present (Fig. 10.2). In fact, several biological control agents have been investigated over the years to evaluate their potential for control of C. fumiferana. These control agents included exotic and native parasitoids, viruses microsporidia, fungi and even irradiation. Considerable work has been conducted on mass rearing and release of the native egg parasitoid, Trichogramma minutum Riley, against C. fumiferana. These studies have shown that parasitism of budworm eggs could be high (about 80%) in the small release plots, but the cost was also high (about CAN$400/ha) (Smith et al., 2002). This approach may be justified in high-value seed orchards but is not practical for largescale use in forestry. Western spruce budworm parasitoids, not present in eastern Canada, were introduced from western Canada but did not become established. Exotic parasitoids from two closely related species from Europe (Choristoneura murinana (Hubner)) and Japan (Choristoneura diversana (Hubner)) were imported and released against C. fumiferana in eastern Canada but these did not become established either. Extensive field trials with four virus types (CPV, NPV, EPV and GV) have been conducted against both C. fumiferana (Cunningham and Howse, 1984; Cunningham, 1985a,b; Cunningham and Kaupp, 1995) and C. occidentalis (Otvos et al., 1989; Shepherd et al., 1995). The goal of initiating an epizootic to control the budworm populations was not achieved in any of these trials (Cunningham and Kaupp, 1995) and the vertical transmission of the virus decreased in subsequent years (Otvos et al., 1989). None of these biological control attempts offered a practical alternative to replace the use of insecticide. Consequently, most of the control work has concentrated on aerial treatment of larvae with insecticide, although attempts have also been made to spray spruce budworm adults with chemical insecticides during dispersal, but without the desired results (Kettela, 1995).


History of Aerial Applications of Insecticides in Canada’s Forests Use of chemical insecticides The history of the early use of insecticides was summarized in various chapters for all of Canada in Prebble (1975). Spruce budworm management, up to 1965, illustrates the first generation of control measures. Defoliator management was exclusively based on the application of chemical insecticides, using the most efficacious products (the more insects killed, the better). The first aerial applications of insecticides in forestry, using calcium arsenate dust, occurred between 1927 and 1930 on about 3200 ha against the spruce budworm, eastern hemlock looper, and the western hemlock looper (Prebble, 1975). Starting in the mid-1940s, the availability of dichlorodiphenyltrichloroethane (DDT), a wide-spectrum insecticide, and surplus aircraft from the Second World War led to the widespread use of aerial spraying to combat insect problems in Canada on a large operational scale (Figs 10.2 and 10.3). DDT and related compounds were adopted for forest insect control because they appeared very promising, based on their use in agriculture and in public health. After the early successes with DDT (i.e. contained a typhus epidemic and controlled malaria), overly optimistic statements, such as ‘mosquito-transmitted disease will disappear’, ‘some pests will become extinct’ and ‘all major pest problems appeared to be solved or solvable’, became common (Casida and Quistad, 1998: 1). DDT became the most commonly used insecticide in forestry because of its high efficacy against all defoliators and in the control of many agricultural insects. The use of DDT in the forests after the Second World War increased, but adversely affected fish populations (Logie, 1975) and DDT accumulated in birds and other components of the environment (Pearce, 1975). From 1965 to 1980 the second generation of insect control, including the spruce budworm, was based on a reactive response – waiting until there was an insect outbreak and then trying to control it. Control was largely

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 216

I.S. Otvos

Spruce budworm Jack pine budworm Eastern hemlock looper Othersb

Area treated with insecticides (’000 ha)

7000 6000

100 90 80


70 60


50 3000

40 30


20 1000


Percentage of area treated with Btk


00 20

95 19

90 19

85 19

80 19

75 19



Year Fig. 10.3. Forest area in Canada treated with all insecticidesa from 1971 to 2000 (from Canadian Forest Service, 1975, 1976, 1977, 1978; van Frankenhuyzen, 1990; Armstrong and Cook, 1993; Moody, 1993a,b; Hall, 1994, 1995, 1996; Cadogan, 1995; Canadian Council of Forest Ministers, 2002). aFor details including what insecticides were used over the years, see the source references. bOther insects include gypsy moth, Lymantria dispar, and forest tent caterpillar, Malacosoma disstria.

achieved by the application of synthetic chemical insecticides, first using wide-spectrum and then, as side effects became known, more selective chemical insecticides. The goal was to suppress the target insect populations with an efficacious product, with minimal side effects, and to protect the infested stands until harvesting could occur or the outbreak collapsed. However, public pressure was mounting to find biological alternatives to chemical insecticides. In an effort to minimize damage caused by defoliators, considerable research was conducted on their population dynamics, especially that of C. fumiferana, to try to understand how and why outbreaks developed and the role of natural control factors. The Green River Project was the first large programme conducted on any insect pest in Canada, and expectations were high. The salient points of the programme were summarized in a volume edited by R.F. Morris (1963). While the programme contributed much new knowledge, it did not solve the

management issues posed by the spruce budworm. However, it did provide new, much needed, tools to use. Coarse hazardrating systems were developed, based on the location and frequency of past outbreaks and on stand susceptibility (stands with a high proportion of balsam fir and > 60 years old) (Regniere and Lysyk, 1995). Sex pheromones were identified and used to monitor population fluctuations of the insect and to warn of impending outbreaks (Sanders, 1988). Methods were developed to sample egg masses in the autumn and the overwintering larval stage in order to forecast expected defoliation (Morris, 1954; Miller, 1957; Miller et al., 1971). The forecasted level of defoliation was, in turn, used to decide which infested areas to protect. There was a shift from treating as much infested area as possible with the available chemicals, aircrafts and funds to a more selective treatment of infested areas. As the undesirable side effects of hard chemicals (broad-spectrum insecticides)

10IntpestManCh10.QXD 5/5/04 2:10 pm Page 217

IPM in Forestry

became known, there was a shift towards more benign pesticides with fewer side effects. There was also a trend away from the reactive mode towards a proactive mode of insect management. With the proactive approach, attempts were made to predict when and where outbreaks would occur and to forecast the expected level of damage (defoliation) (Morris, 1954; Miller, 1957; Miller et al., 1971) rather than waiting until the outbreaks developed and severe damage had occurred. This was aided by the Green River Project research. Despite progressively reducing the dosages of DDT used (from 1–2 lb./acre to 0.25 lb./acre (Nigam, 1975)), effects on nontargets were still noted and deemed unacceptable. The search for more acceptable and ecologically less disruptive substitutes began as early as the 1950s and eventually led to the replacement of DDT by non-persistent organophosphates and carbamates in the late 1960s. Four organophosphates (phosphamidon, fenitrothion, trichlorfon and acephate) and two carbamates (aminocarb and mexacarbate) were registered and used extensively. Phosphamidon was used initially as a buffer spray in watershed areas to prevent DDT contamination of prime salmon fisheries waters. However, the use of DDT was extended to large-scale operations during the mid-1970s, due to a shortage of the other, more selective, insecticides. Further use of phosphamidon was discontinued in 1977 because of its negative impact on birds, even at low dosages. Fenitrothion replaced DDT in 1969 and as of 2003 it is still registered for use in New Brunswick, although there is considerable public pressure to ban its use entirely (J.C. Cunningham, 1996, personal communication). It was considered relatively safe for fish and birds, but had caused some mortality in aquatic insects and pollinators immediately after spraying (Varty, 1978). Trichlorfon was used in place of fenitrothion from 1973 to 1977 near cultivated blueberries to minimize adverse effects on pollinators and was used when non-spray buffer zones were placed around blueberry fields, precluding the use of trichlorfon. Acephate was the ‘safest’ chemical insecticide devel-


oped for aerial application on budworminfested forests, as it was relatively less toxic to fish, birds and mammals than phosphamidon, fenitrothion and trichlorfon (Nigam, 1975), but it could not compete in cost and efficacy with fenitrothion and aminocarb. Mexacarbate was used in small quantities from 1969 to 1974, until the supply was exhausted (Nigam, 1975, 1980). Fenitrothion and aminocarb were the main insecticides used during the latter part of the 1970s, when approximately 9 million kg of fenitrothion and 0.9 million kg of aminocarb were used (Nigam, 1980). The area of budworm-infested stands treated with insecticides rose dramatically during the mid-1970s in response to the increased size of budworm outbreaks (Fig. 10.3). However, the proportion of treated to infested forest declined (Figs 10.2 and 10.3) during this period due to a shortage of chemicals, economic constraints, and mounting public opposition to the wide-scale use of chemical insecticides in the forest. During the latter part of the 1970s, political reaction to public pressure over the Reye’s-syndrome controversy (Wood and Bogdan, 1986) and suspected carcinogenicity of fuel oil carrier led to a gradual decline in the treatment of infested forests in eastern Canada (Nigam, 1980). This resulted in an increase in the size of the dead or dying forests in the budworminfested stands in eastern Canada. Aerial application remained the main method of control; insecticides were applied to reduce budworm populations, protect foliage and prevent tree mortality. Of the 29.9 million ha of forest sprayed from 1944 to 1973, 43.3% was treated with DDT, 55.5% with phosphamidon and fenitrothion, 1.2% with other chemicals and only about 0.04% with biological insecticides (Prebble, 1975; Armstrong and Cook, 1993). Realizing the undesirable side effects of the chemical insecticides, potentially less disruptive alternatives were identified (especially entomopathogens), and research was initiated. During the major spruce budworm outbreak of the 1970s–1980s in eastern Canada (Kettela, 1983), significant tree mortality was first observed in 1973, when approximately 1 million ha of dead or dying timber was

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 218


I.S. Otvos

recorded. Tree mortality increased over the years and, by 1987, heavy mortality had occurred over approximately 18 million ha. The outbreak peaked in 1975, when nearly 50 million ha were infested in the eastern Canadian provinces, and close to 9 million ha were treated with phosphamidon and fenitrothion (Fig. 10.2; Nigam, 1980; Kettela, 1983). A total of 13 million kg of chemical insecticides were used to protect trees on 50 million ha, from 1965 to 1980, in eastern Canada (Nigam, 1980; Kettela, 1983). Between 1985 and 1990, approximately 2.8 million ha were treated in eastern Canada to control spruce budworm (Cunningham and van Frankenhuyzen, 1991). There were large areas defoliated between 1981 and 1990. The areas defoliated annually ranged between a low of about 20 million ha in 1986 to a high of about 55 million ha in 1990 (Fig. 10.2). A bilateral multi-year project on the spruce budworm was initiated between Canadian and American researchers in 1977 (CANUSA). The results of this project were published in an even larger volume (Sanders et al., 1985) than that of R.F. Morris (1963). However, even these additional research findings failed to provide the knowledge and recommendations needed to manage budworm outbreaks without aerial application of insecticide to prevent budworm damage. Insecticide treatment remained the only effective tool to reduce larval populations, but the use of insecticide shifted away from broad-spectrum chemicals through the more selective chemicals towards bioinsecticides. Attempts were made to develop viral insecticides. Entomopathogenic viruses had been isolated from field-collected budworm larvae as early as 1958 (Bird, 1959). Extensive laboratory and field trials were conducted with NPVs and GVs to control both the (eastern) spruce budworm and the western spruce budworm between 1974 and 1988. The field trials with these viruses were disappointing (Cunningham, 1985a; Otvos et al., 1989; Cunningham and Kaupp, 1995). Consequently, no further work was done with the naturally occurring virus strains and forest managers were left with the only other microbial agent under investigation, Btk.

Use of Bacillus thuringiensis Btk is effective against Lepidoptera (Dulmage, 1982), the order to which most forest defoliators belong. Although Btk is commonly found in soil microbiota (Martin and Travers, 1989), it has never been observed to control forest insect-pest populations in nature and must be applied as an insecticidal spray, sometimes more than once, over the infested area. It is now widely used to control several defoliating insects in Canada. Progress in the development of Btk as an operational alternative to synthetic chemical pesticides has been reviewed by Cunningham (1985b), van Frankenhuyzen (1990) and Cunningham and van Frankenhuyzen (1991). The first aerial-spray trials using Btk in Canada were against the western blackheaded budworm, Acleris gloverana (Walsingham), in British Columbia (Kinghorn et al., 1961) and spruce budworm in New Brunswick (Mott et al., 1961). Most of the early research on Btk was conducted on spruce budworm in the 1970s, in an effort, in part, to replace chemical insecticides. These early tests gave variable efficacy and population control. It took over 25 years from its first experimental use in the early 1960s to reach large-scale operational use in the mid1980s (Fig. 10.3). The following were some of the contributing factors that led to the acceptance of Btk as a replacement for chemical insecticides in defoliator control. Btk potency increased from 4 billion international units (BIU) per litre in the early 1970s to 16.9 BIU/l in the mid-1980s, by which time the dosage rate of 30 BIU/ha was routinely applied in 2.4 l of undiluted product for the control of spruce budworm. The cost of Btk decreased between 1981 and 1988 from 4.5 times to only 1.2 times more expensive than chemical insecticides. The cost of Btk was fairly constant at between 35 and 40¢/BIU from 1986 to 1990 (Cunningham and van Frankenhuyzen, 1991). The higherpotency Btk products (containing more BIU per litre) permitted using lower volumes and had the added benefits of reducing transportation costs and increasing spray-plane productivity. At the same time, Btk products

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 219

IPM in Forestry

were providing increased efficacy and reliability of control operations (van Frankenhuyzen, 1990) and foliage protection of the treated trees. Btk was finally considered a viable alternative to chemical insecticides for use against spruce budworm by 1981 (Smirnoff and Morris, 1984) and several other major forest defoliators a few years later (van Frankenhuyzen, 1990). These improvements, together with the political decision not to use chemical insecticides, as a result of public pressure and environmental concerns, led to favouring the use of biologicals, resulting in the widespread acceptance of Btk as a fully operational control option for forest defoliators. Btk is considered environmentally benign (Otvos and Vanderveen, 1993) and is the only registered and commercially available microbial agent in Canada for forest insect control. By 1993 there were 18 Btk products registered for use in insect control in Canada (Otvos and Vanderveen, 1993). Although three viruses are also registered for forest insect control, they are not available commercially. The operational use of Btk for control of spruce budworms increased from about 2% of the total area treated in 19801 to 20 in 1984, 63 in 1990 and nearly 100% by 1996 (Cunningham and van Frankenhuyzen, 1991; van Frankenhuyzen, 1993; Fig. 10.3). In most of Canada, Btk is now the only insecticide used for budworm control, apart from a recently registered biorational (Mimic). Only New Brunswick continues to use both chemical (fenitrothion) and Btk products (Cunningham and van Frankenhuyzen, 1991). By far the greatest use of Btk in Canada is for spruce budworm control, with 2.8 million ha treated between 1985 and 1990 (Cunningham and van Frankenhuyzen, 1991). Similar increases in the use of Btk have occurred in the USA and Europe (van Frankenhuyzen, 2000). Potential and constraints The use of Btk is not without problems. Depending on weather conditions in the field, Btk in spray droplets is considered to be effective for only 3–5 days following application, after which the larvae may not


acquire a lethal dose (van Frankenhuyzen, 1995). The effectiveness of Btk is questionable against high densities of spruce budworm (more than 25 larvae per branch sample). Although Btk affects only larval stages of Lepidoptera, some criticism has been raised because of its potential impact on non-target beneficial or desirable Lepidoptera. Nontarget Lepidoptera may be important in the food-chain of some insectivorous birds, or they may be rare or endangered species. The effect of Btk on non-target Lepidoptera has been investigated by several authors, including Miller (1990). Studies have shown that both numbers of non-target insects and species richness were depressed for 2–3 years following treatments. However, all but the rare species recolonized the treated areas within 2–4 years after treatment (Miller, 1990). This was confirmed by Boulton et al. (2002), who found a significantly lower abundance of non-target Lepidoptera on plants that received an operational Btk spray (30 BIU/ha) in a plot treated against western spruce budworm, than on plants that were covered and excluded Btk. The two most common insect species on the shrubs made a full recovery within 2 years of the Btk spray. However, sparsely distributed species declined on both the treated and covered plants, suggesting a general decline of Lepidoptera species independent of the spray. A different experimental study, where double the regular registered dose was used (60 BIU/ha), yielded similar results. Some species made a full recovery by the end of the second year, but this could not be demonstrated for the sparsely distributed species (Boulton, 1999; T.J. Boulton and I.S. Otvos, unpublished data). The effects of Btk treatment on non-target Lepidoptera may only be a concern when endangered insect species are in the spray area. However, the relative ‘value’ of the endangered species should be compared with the potential damage the target species will cause if no treatment takes place. The timing of Btk treatment not only is important in terms of efficacy, but may also be a factor in preventing deleterious effects on natural enemies. Conflicting data on the effects of Btk treatments on the natural

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 220


I.S. Otvos

enemies of eastern and western spruce budworm have been published. Most reports indicated no deleterious effects (Buckner et al., 1974; Reardon et al., 1982; Morris, 1983; Niwa et al., 1987). Otvos and Raske (1980a,b) reported an apparent increase in per cent parasitism by the two most common and important budworm parasitoids, i.e. Apanteles fumiferanae Viereck and Glypta fumiferanae (Viereck), while Hamel (1977) reported a negative impact. Nealis and van Frankenhuyzen (1990) indirectly confirmed the findings reported by Otvos and Raske (1980a,b) and recommended applying Btk at the peak of the fourth-instar stage to increase efficacy against the spruce budworm and to minimize or prevent negative effects on these two important budworm parasitoids. The evolution of the currently used management method to minimize spruce budworm damage is typical of most defoliator control, and is probably representative of the general approach worldwide. At first, damage caused by the insect is not considered economically important until the affected resource is desired by society. Then the most efficacious control method is used – usually chemical insecticide with broad-spectrum effects. As non-target effects become known, alternative control methods are developed. Sometimes these have minimal side effects on the environment. The use of introduced and natural enemies, such as parasitoids and pathogens, can also have some effects, even if only on the biodiversity of the region. When our food and shelter are secured, segments of the population become socially conscientious and concerned about biodiversity. It is ironic, however, that, in the same population segments, some people still insist on buying unblemished fruits and vegetables produced by repeated use of chemical insecticides.

Integrated Pest Management of Douglas Fir Tussock Moth: a Case Study The management system developed for the DFTM, integrating a pheromone-detection system with early application of the naturally occurring, laboratory-produced virus, illustrates a true IPM system.

Two morphotypes of the virus have been isolated from DFTM larvae and identified as the cause of these epizootics (Hughes and Addison, 1970). One morphotype exhibits singly occluded virus particles (OpSNPV) in the PIB. The second has multiple viral particles embedded in bundles within the PIB (OpMNPV) (Hughes and Addison, 1970). The majority of the research has been conducted on the multiple-embedded virus. The use of virus to control DFTM was considered in British Columbia as early as 1962, when the first field trial was conducted on individual trees (Morris, O.N., 1963). The first aerial spray trials using OpNPV against DFTM in British Columbia were conducted jointly by personnel of the Canadian Forest Service, the US Department of Agriculture (USDA) Forest Service and the British Columbia Ministry of Forests from 1974 to 1976 (Ilnytzky et al., 1977; Stelzer et al., 1977; Cunningham and Shepherd, 1984). Field treatments in 1975 using the laboratory-produced, naturally occurring virus caused high infection and high larval mortality, but the treated stands still sustained considerable damage because the virus was applied late in the declining phase of the outbreak. Therefore, the effect of the virus application on the course of the outbreak could not be evaluated. However, the experiment has shown that the laboratory-produced virus behaves like the naturally occurring one and can be used to cause an epizootic in the field. Based on these results and safety testing of OpMNPV conducted in the USA, the USDA Forest Service registered the viral insecticide as TM-Biocontrol-1® in 1976. The experiment conducted in 1975 raised the following questions: ● Can the virus be introduced into the population at the beginning of the outbreak, and will it cause an epizootic? ● Will such an epizootic reduce damage normally associated with a DFTM outbreak? ● Can the virus dose be reduced to lower the cost of application? ● Can DFTM populations be monitored to predict future outbreaks? To introduce the virus at the beginning of an outbreak requires a reliable monitoring sys-

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 221

IPM in Forestry

tem. It was necessary to determine where and when outbreaks were likely to occur. In a separate study, concurrent with the virus work, a dependable and sensitive pheromone monitoring system was developed for early warning of impending outbreaks (Shepherd et al., 1985).

Monitoring with pheromone traps Pheromone-baited traps were placed in susceptible stands, which were defined by overlaying maps of previous outbreaks, forest types and biogeoclimatic zones. The most susceptible stands, revealed by the overlays, tended to be located in the driest part of the range of Douglas fir, where it mixes with ponderosa pine, Pinus ponderosa P. Laws. ex C. Laws. Within this forest habitat, permanent monitoring stations were established and pheromone-baited traps were operated annually to monitor changes in male moth density over the course of an outbreak cycle to reveal patterns (Shepherd et al., 1985; Shepherd and Otvos, 1986). Population trends in pheromone-baited traps were followed from endemic to epidemic levels during the course of one outbreak. The number of successive years of upward trends of male moths caught was used to predict outbreak development. Three consecutive years in which the number of male moths caught increased and exceeded 25 moths per trap indicated that an outbreak was expected within the next 1 or 2 years (Shepherd et al., 1985). The pheromone-trap system only gives advance warning that an outbreak is imminent and signals that another, more precise sampling system should be deployed in the area. Thus, after 2 years of upward trends, additional networks of traps are placed around the indicator stations to locate the foci of the developing outbreak and refine prediction. An egg-mass survey is then initiated during the autumn or winter to determine the insect density at the centre of the developing infestation and to predict the level of potential damage the following year (Shepherd et al., 1984a). If egg masses are present, all available options for managing the insect problem should be


examined to select the most appropriate for the situation. These options include protecting infested stands by virus or insecticide application or doing nothing and letting the outbreak run its course. A stepwise selection process for control actions is provided as a guideline (Shepherd and Otvos, 1986). The use of a registered chemical insecticide with a fast knock-down power may be considered appropriate in high-use recreational areas, such as parks, because the hairs of the caterpillars and those on the egg masses may cause a severe allergic reaction called ‘tussockosis’ in some sensitive people (Perlman et al., 1976).

First experiment – 1981 A developing DFTM outbreak in southcentral British Columbia was discovered in 1980 before any defoliation occurred. This allowed an experiment in 1981 to determine if a viral epizootic could be initiated at an early phase of the outbreak, before it would occur naturally, by ground and aerial application of the virus, and whether the application would reduce damage (Shepherd et al., 1984b). Although a natural epizootic also occurred in the control plots containing high and moderate DFTM populations, the incidence of viral infection in the treated plots was considerably earlier and much higher, indicating the beneficial effects of the viral spray. Even at low population density, treatment effects were excellent, and a natural epizootic in the control plot occurred much later. The results showed that the virus can be introduced into DFTM populations at an early phase of the outbreak and that a viral epizootic can be initiated in first- and second-instar larvae by both aerial and ground treatment (Shepherd et al., 1984b). The aerially applied virus caused an epizootic among DFTM larvae at low (41 larvae/m2), medium (97 larvae/m2) and high (206 larvae/m2) population densities. Laboratory rearing of larvae collected from the field and weekly microscopic examination of the dead larvae indicated that a second wave of epizootic occurred among the survivors.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 222


I.S. Otvos

Table 10.4. Douglas fir tussock moth larval and tree mortality in virusa-treated and untreated plots, Veasy Lake, British Columbia, 1982 (from Otvos et al., 1995).


Treatmentb (PIB/ha in 9.4 l/ha)

1982 pre-spray larvae/m2

T1 T2 T3 T4

1.6 × 1010 Oil 8.3 × 1010 Oil 2.5 × 1011 Oil 2.5 × 1011 Molasses

182.8 145.8 302.0 41.8

C1 C2 C3 C4

Control Control Control Control

197.5 136.9 360.6 81.2

a b

c d

% Population reduction 6 weeks postsprayc 64.7 90.6 95.1 86.6

% Sample trees killed by DFTM 1983 0 2 0 0 χ = 0.6 53 –d 60 0 χ = 37.8

1984 0 7 4 0 χ = 2.8 60 –d 62 0 χ = 40.7

The virus used was OpMNPV produced in white-marked tussock moth (Virtuss®). PIB, polyhedral inclusion bodies; Oil, oil-based formulation containing 25% blank oil carrier and 75% water; Molasses, molasses formulation containing 25% commercial-grade molasses and 75% water. Per cent reduction was calculated by the modified Abbott’s formula (Fleming and Retnakaran, 1985). Trees in part of the plot were cut down during power-line construction.

Second experiment – 1982 In a separate experiment the following year, water and oil based formulations, and reduced dosages2 of the virus were compared to determine the most effective dose and formulation and to investigate if the recommended application rate of 2.5 × 1011 PIB/ha could be reduced and still prevent damage (Table 10.4). The initial impact of the 1982 applications was that by 2 weeks postspray 10–30% of larvae had become infected. These infected larvae died, liberated polyhedra on to the foliage and increased the amount of inoculum. A secondary wave of virus infection then developed among the surviving larvae (DFTM larvae have a long feeding period) and by 6 weeks after spraying the population had collapsed. Per cent infection, development of the epizootic among the larvae and larval mortality, corrected for natural mortality, in the treated plots were related to dosage and the second lowest dose of 8.3 × 1010 PIB/ha gave similar results (about 91% mortality) to the full dose of 2.5 × 1011 PIB/ha (95% mortality). Virus transmission was higher in plots with higher larval densities. Development of the viral

disease was temperature-dependent and the spread of the disease was influenced by host density. NPV infection was not detected in the untreated control plots until 5 weeks after spraying and at a much lower level than in the treated plots. Virus application has additional benefits besides direct larval mortality. Among the surviving larvae, sublethal effects of virus application included higher pupal mortality, lower per cent adult emergence and a shift in sex ratio. More males (about twice as many) than females emerged in the treated plots, while the sex ratio of the adults was close to 1:1 in the control plots (Otvos et al., 1987). This alteration of the sex ratio is probably due to the fact that female DFTM have one more larval instar than males, are exposed to the virus longer and consequently suffer higher mortality. This change in sex ratio among the survivors of virus treatment has been frequently reported in other insects, including the spruce budworm (Duan and Otvos, 2001). These results indicated that it is possible to control DFTM populations with OpMNPV at about one-third of the registered label dose (at least at 8.3 × 1010 PIB/ha) and poten-

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 223

IPM in Forestry

tially even lower dosages at an early stage of an outbreak. Treatment at this lower dosage also prevented significant tree mortality in the treated stands (Table 10.4).

Summary and benefits of the system The results of the experiments with pheromone traps and OpMNPV application over the past 20 years have proved that DFTM outbreaks can be prevented by a single application of virus at the beginning phase of an outbreak. Foliage protection may be negligible in the year of application, but acceptable in the following years. Tree mortality can be prevented when the treatment is applied early in the outbreak cycle and to early-instar larvae. The management system developed for DFTM was successfully tested during the 1990–1993 outbreak, and tree mortality was minimal in the stands treated with OpMNPV because early infection prevented the development of full-blown outbreaks in the treated stands. The operationally proved management system was accepted by the British Columbia Ministry of Forests, became part of the Forest Practices Code in the province and is used to manage DFTM populations. The pest-management system for the DFTM (Shepherd and Otvos, 1986) enables forest managers to predict when and where outbreaks are likely to occur so that control measures can be planned and implemented to minimize or prevent damage. It is hoped that the DFTM pest-management system described above will serve as a prototype for the development of pest-management systems for other defoliating forest pests elsewhere. Work is underway to develop a similar management system for other defoliators in British Columbia and other parts of Canada. When using such a system, one may not always be able to use naturally occurring biological control agents to reduce damage; however, it should be possible to identify stands susceptible to attack by various defoliators and this in itself will be useful to forest managers. The steps of the DFTM management system are provided below for possible adaptation and use for other insects.


Steps of the DFTM management system ● Identify stands susceptible to DFTM attack based on overlaying defoliation maps of past outbreaks, forest types and biogeoclimatic zones. ● Within susceptible stands, establish permanent monitoring stations representing the range of past DFTM outbreaks. ● Set up pheromone traps at these locations and monitor male moth catches annually for one outbreak cycle to determine the threshold of male moth catches that indicates impending outbreaks. ● Deploy additional auxiliary pheromone traps to help to locate infested stands when male moth catches reach threshold numbers. ● Search for egg masses near permanent or auxiliary pheromone traps when moth catches reach threshold numbers. ● When egg masses are found, consider all available options to manage DFTM populations and select the most appropriate one for the area. ● Implement the action chosen.

Development of IPM for the Introduced Gypsy Moth in North America The gypsy moth, Lymantria dispar (Linnaeus), presents a unique example of the progression of forest insect-pest control in North America. Probably more research has been done on the gypsy moth in North America, since its introduction c. 130 years ago, than on any other forest insect pest, either native or introduced. In spite of all of this research, the gypsy moth continues to spread. Hopefully, though, some important lessons have been learnt. The gypsy moth is a polyphagous Eurasian forest defoliator that is known to feed on over 300 species of trees and shrubs, with oaks as the most favoured hosts (Leonard, 1981). Two strains of L. dispar are commonly recognized, one from Europe and the other from Asia. In Europe, the gypsy moth feeds mainly on deciduous trees, but in Asia it also feeds on conifers, primarily larch. The females of the European strain, although

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 224


I.S. Otvos


British Columbia Alberta Sask.


Man. Ontario



Point of introduction in Massachusetts c. 1869 Area regulated for established populations (2000) Recent infestations in western North America Fig. 10.4. Current extent of infestation and recent introductions of gypsy moth into North America (after Nealis, 2002). Sask., Saskatchewan; Man., Manitoba; Nfld, Newfoundland; NB, New Brunswick; NS, Nova Scotia.

winged, cannot fly, while females of the Asian variety can fly (Baranchikov, 1989; Wallner, 1989). This makes the latter a potentially more destructive strain than the European variety if introduced into Canada (where most of the trees are conifers), in terms of both its potential faster rate of spread and greater potential damage to the forests of Canada. These two strains of gypsy moth hybridize in the laboratory (Keena et al., 1995) and in the field (Prasher and Mastro, 1995), and both sexes of the hybridized offspring (F1 and F2) can fly (Keena et al., 1995).

The European strain of gypsy moth in eastern North America The European strain was introduced under unusual circ*mstances at Bedford, near Boston, Massachusetts, USA, in 1869 (McManus and McIntyre, 1981; Liebhold et

al., 1989). Leopold Trouvelot, a naturalist, intentionally brought the insect from France to North America and the insect escaped from his laboratory during a storm. Although he reported the incident immediately, nothing was done at the time. The gypsy-moth infestation increased in extent and defoliation began to appear about 10 years after the initial escape. The spread of the gypsy moth since that time is well documented (McManus and McIntyre, 1981; Montgomery and Wallner, 1988). An eradication programme was started in 1889 and appeared to be working, reducing the infestation to such a degree that in 1900 the eradication programme was stopped by the state of Massachusetts (McFadden and McManus, 1991). This was a fatal mistake, with serious unforeseen consequences. Within 5 years of stopping the eradication programme, gypsymoth infestations increased drastically and new infestations were discovered in three adjacent states (McManus and McIntyre,

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 225

IPM in Forestry

1981), by which time the European strain of gypsy moth was well established in eastern North America (Fig. 10.4). A prompter response and eradication programme against this quarantine threat might have prevented the vast harm resulting from this incidence of pest introduction (Dunlap, 1980). The gypsy moth spread west between 1906 and 1920, at an estimated rate of 9.6 km/year. In an effort to halt the spread of the gypsy moth and the subsequent damage to plants, the Domestic Plants Quarantine Act was created in 1912 in the USA (and in 1924 in Canada) to regulate the movement of plant material from gypsy-moth-infested areas. A barrier zone was established in 1923, from the Canadian border (Quebec) south along the Hudson River Valley to Long Island (New York), to prevent the westward spread of the gypsy moth. Infestations inside and west of this barrier zone were to be eradicated, while infestations to the east were to be controlled or managed by suppression, using various means (McFadden and McManus, 1991). Eradication programmes were designed to eliminate isolated populations of the gypsy moth, while suppression programmes were designed to protect foliage and/or reduce larval populations and slow the spread. The barrier zone became infested in 1939, and eradication attempts were terminated in 1941. However, the barrier zone was reinstituted in 1953 after the gypsy-moth populations exploded in 1951/52. The European gypsy moth can spread in two ways: natural dispersal or accidental transport of pupae or egg masses by humans. Natural dispersal occurs over only short ranges when first- or second-instar larvae are transported by wind as female moths cannot fly (Mason and McManus, 1981; Elkinton and Liebhold, 1990; McFadden and McManus, 1991). This spread of first and second instar larvae by natural dispersal was estimated to be about 2 km/year (Liebhold et al., 1992). Inadvertent transport of cocoons and/or egg masses from infested areas to uninfested areas by humans (through vacationing, moving and transporting goods) can be over much larger distances and is much more


important in the spread of the gypsy moth than natural spread. For example, in 1983, ten gypsy-moth infestations were found in California about 3200 km from the infestation in the east, despite aggressive quarantine inspection at the California State border. In 1983, these infestations were treated with chemical insecticides to eradicate them at an estimated cost of US$1.5 million (McFadden and McManus, 1991).

Chemical control At first, the broad-spectrum insecticides Paris green, lead arsenate and DDT were used in both eradication and suppression projects. Of the chemical insecticides used, DDT was considered so effective that, between 1949 and 1959, 3.7 million ha of gypsy-moth-infested stands were treated (Liebhold and McManus, 1999). However, the environmental damage caused by the extensive use of DDT against the gypsy moth was cited as a specific example of unacceptable chemical pollution in Rachel Carson’s book Silent Spring (1962). Even though only about 50 ha of defoliation was noted, the eradication was discontinued in 1958 because of concerns about the environmental persistence of DDT. ‘Hopes of eradicating the gypsy moth were abandoned [in 1958] and long overdue emphasis was placed on research’ (McFadden and McManus, 1991). In 1959, carbaryl (Sevin®) replaced DDT for use in suppression programmes. Over time, the control products selected and used in suppression projects evolved from broad-spectrum insecticides, such as carbaryl (Sevin®), trichlorfon (Dylox®), acephate (Orthene®) and diflubenzuron (Dimilin®) to the much more selective and environmentally more acceptable biological insecticides, such as Btk and virus, as well as the use of pheromones in the 1980s (Liebhold and McManus, 1999). This gradual change in use pattern of controlling/suppressing the gypsy-moth populations in the eastern USA is illustrated in Fig. 10.5A. The use of Btk, virus and sex pheromones will be discussed separately under biological control.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 226


I.S. Otvos




Sevin 600

Dylox Gypchek/disparvirus Bacillus thuringiensis

Area treated (’000 ha)






00 20

95 19

90 19

85 19

80 19





Year 2500


3 40 ,09 ,2 4 14 49 ,1 12 75 ,9 33 51 ,9 36 56 ,5 77


Dimilin 2000


Area treated (ha)

Gypchek/Disparvirus Bacillus thuringiensis










85 19

80 19



0 Year

Fig. 10.5. Total area treated with insecticides during suppression and eradication programmes to control the gypsy moth (A) in the USA, 1970–2002, (from, 2003); (B) in Canada, 1975–2000 (from Armstrong and Cook, 1993; Mason and Huber, 2002).

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 227

IPM in Forestry

Biological control Natural enemies Classical biological control (the introduction of natural enemies to control recently introduced pests), started in 1905, was the first line of defence. Importation of exotic parasitoids and predators for gypsy-moth control was one of the largest programmes in the history of biological control (Brown, 1961). About 150 species of parasitoids have been reared from the gypsy moth throughout its distribution in Eurasia (Doane and McManus, 1981). Over the years, about 60 of these natural enemies, mainly from Europe, Asia and Japan (obtained from high and moderately high gypsy-moth populations), were introduced into the USA. Early attempts at parasitoid introductions (1905–1914 and 1922–1933) were successful, but later introductions (1960–1977) failed (Reardon, 1981). By 1933, 44 species of parasitoids and nine species of predators had been introduced and, of these, 13 parasitoids and one predator became established (Dowden, 1962). Most researchers agree that classical biological control did not prevent the spread of the gypsy moth, but it very probably contributed to the collapse of some outbreaks and possibly slowed the spread. The introduced parasitoids may have also kept the populations at endemic levels after the collapse of an outbreak (Ticehurst et al., 1978). Augmentative releases of some of the established parasitoids resulted in increased parasitism in the release areas (treatment) compared with the controls in three different studies (Weseloh and Anderson, 1975; Hoy, 1976; Blumenthal et al., 1978). However, the augmentative parasitoid releases did not appear to significantly reduce gypsy moth egg-mass density (a measure of success) after the releases. Pathogens During the late 1950s and early 1960s, in response to public concern over the use of chemical insecticides, efforts were intensified to develop environmentally acceptable control alternatives. Entomopathogenic microorganisms offered such alternatives and


considerable work has been done on the use of pathogens for gypsy-moth control. The pathogens investigated include Bacillus thuringiensis (Dubois, 1981), an NPV (Lewis, 1981) and a fungus (Entomophaga maimaiga) (Hajek et al., 1990a; Elkinton et al., 1991; Hajek, 1997). Research into the use of Btk for the suppression of gypsy moth began in earnest in the early 1960s (Cantwell et al., 1961) and, by the 1980s, it was accepted as an effective alternative to chemical insecticide for gypsymoth control (Dubois, 1981). Btk use began in 1980 and increased gradually, reaching a peak in 1985 when about 481,900 ha were treated with Btk (Fig. 10.5A). According to Campbell and Podgwaite (1971), the gypsy-moth NPV (LdNPV) was probably introduced inadvertently with the gypsy moth or with one of its parasitoids (Glaser, 1915). It was considered to be the most important natural control agent of the gypsy moth until 1980 (Campbell, 1963; Doane, 1970, 1976; Podgwaite and Campbell, 1972). The development of LdNPV as a biopesticide began shortly after its effectiveness in reducing larval populations was realized. Considerable research into strain selection, production, and laboratory and field testing (Lewis, 1981) and other factors (see section 6.3 of the gypsy-moth compendium, edited by Doane and McManus (1981)) preceded registration of the gypsymoth NPV in 1978 as Gypchek for gypsymoth control (Lewis, 1981). Unfortunately, commercial production of Gypchek did not follow registration. Its greatest attribute, high host specificity, is also its greatest shortfall, as it makes it economically unattractive for private companies to produce and sell it. Large companies are only interested in developing products that generate US$40–50 million in sales per year (Podgwaite, 1999), while the market for Gypchek is only about US$5 million per year. To date, every company that tried to produce Gypchek commercially has failed economically (Podgwaite, 1999). Consequently, the US Forest Service (USFS) continues to produce Gypchek and make it available on a limited basis through cooperative suppression programmes (Podgwaite,

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 228


I.S. Otvos

1999). Since the registration of Gypchek in 1978, only about 20,200 ha have been treated with it in the USA. This represents less than 1% of the total area treated for gypsy-moth control (Podgwaite, 1999; Fig. 10.5A). There is some confusion about the origin of the gypsy-moth fungus that causes epizootics in North America (Hajek et al., 1995). A fungal pathogen of the gypsy moth was introduced from Japan (where it causes extensive epizootics) into the USA on two separate occasions. The early introductions and releases were in 1910 and 1911 (Speare and Colley, 1912) and then later in 1985 and 1986 via infected larvae (Hajek et al., 1995). No evidence was found indicating establishment of the fungus from either of these releases within a few years following introduction (Hajek et al., 1995). After its second release, the fungus introduced from Japan was described as a new species, E. maimaiga Humber, Shimazu & Soper (Soper et al., 1988). An epizootic of this fungus was discovered in 1989 (Andreadis and Weseloh, 1990) and surveys in the same year showed the fungus occurring in seven states and in virtually all samples collected from areas that were infested by the gypsy moth prior to 1980 (Hajek et al., 1990a). More intensive surveys in the following year showed that E. maimaiga occurs in ten states in the northeastern USA (Elkinton et al., 1991) and in Ontario (Welton, 1991; Nealis et al., 1999), where the fungus must have spread on its own as no intentional introduction of the fungus has occurred there. Large-scale epizootics caused by E. maimaiga were widespread in areas colonized by the gypsy moth prior to 1980 (Elkinton et al., 1991), but not in areas invaded more recently (Hajek et al., 1996). The wide geographical distribution of the fungal epizootic suggests that the fungus probably became established in the New England states from the first intentional releases of E. maimaiga near Boston in 1910 and 1911 (Andreadis and Weseloh, 1990; Hajek et al., 1990a; Elkinton et al., 1991). The first authors to report on the 1989 discovery of the E. maimaiga epizootic summarized it the best by saying, ‘the current epizootic may have resulted from the survival and inapparent spread of an early introduction in

1910–1911’ (Andreadis and Weseloh, 1990: 2461). Before the discovery of E. maimaiga in North America in 1989, NPV was generally credited with causing the collapse of gypsymoth outbreaks (Hajek et al., 1996). LdNPV epizootics generally occur at high host densities in dry years, when rainfall is low (Elkinton et al., 1991), while E. maimaiga can cause high levels of infection across a wide range of host densities (Hajek et al., 1996). Since 1989, E. maimaiga epizootics have been shown to decimate gypsy-moth populations at both low and high host densities in years with higher than normal precipitation (Elkinton et al., 1991; Hajek and Roberts, 1991; Smitley et al., 1995) and even when NPV is present (Smitley et al., 1995). Several authors have noted a positive correlation between the intensity of the epizootic and rainfall (Andreadis and Weseloh, 1990; Elkinton et al., 1991; Hajek et al., 1993; D’Amico and Elkinton, 1995). This is not surprising, since E. maimaiga-killed larvae discharge conidia in the presence of dew or when relative humidity is greater than 90% (Hajek et al., 1990b; Hajek and Soper, 1992). In dry weather, fungal-killed gypsy moth have the same appearance as NPV-killed larvae (Hajek and Roberts, 1992). This holds true for other insects and Entomophthorales fungi (I.S. Otvos, personal observation). For example, epizootics in the eastern hemlock looper, Lambdina fiscellaria fiscellaria (Guenee), in Newfoundland were attributed to an undetermined wilt (viral) disease for over 20 years. The true cause of the epizootics, infection by two fungal pathogens, was only determined in 1969 (Otvos, 1973; Otvos et al., 1973). The absence of external fruiting bodies on the insect cadavers makes distinguishing between mortality caused by these pathogens in dry weather in the field difficult. Given this information, it is not hard to imagine that earlier identifications of viral infection in the field would have also included some fungal-infected insects. The fungus has spread dramatically between 1989 and 1992 and is prevalent in areas not recently colonized by the gypsy moth (it does not occur in recently colonized

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 229

IPM in Forestry

infestations), causing up to 100% mortality of late-instar gypsy-moth larvae (Reardon and Hajek, 1993). The fungus is considered by some to be a more important pathogen than NPV (Hajek, 1997). Consequently, it has been intentionally ‘spread’ or introduced, especially to areas newly invaded by the gypsy moth (Hajek et al., 1996; Smitley et al., 1995). E. maimaiga resting spores can be translocated or even introduced into new fungusfree areas and along the leading edge of the spreading gypsy-moth infestation by the purposeful introduction of resting spores (Smitley et al., 1995; Hajek et al., 1996) by moving soil with resting spores from areas where fungal epizootics have recently occurred. However, care must be taken to ensure that pathogens, such as Armillaria mellea rhizomorphs, are not spread unintentionally as well (Reardon and Hajek, 1993). ‘E. maimaiga is now a dominant natural enemy associated with gypsy moth in North America’ (Hajek, 1997: 67) and might be considered more important than NPV in moister environments. The fungus might be an excellent candidate for introduction around lakes, on islands and on the west coast of North America should the gypsy moth become established in that region.

Combinations of biological control agents In order to increase their control impact, some biological control agents have been used in combination, such as parasitoids and pathogens. The parasitoid Apanteles melanoscelus (Ratzeburg) was used in combination with Btk, and their combined use resulted in higher population reduction and foliage protection than when each was used alone (Reardon, 1981). Studies have also shown that parasitoids contaminated with NPV in the laboratory can transmit the virus to the gypsy moth, both in the laboratory and in the field (Reardon, 1981). Dual or mixed infection by LdNPV and E. maimaiga has been reported from the gypsy moth (Hajek and Roberts, 1991; Weseloh and Andreadis, 1992; Malakar et al., 1999). Generally, E. maimaiga out-competes LdNPV when both the fungus and the virus infect


the host at about the same time, because the fungal infection develops faster. Sex pheromones Disparlure is used in pheromone traps to monitor (survey and detect) gypsy-moth populations (Cameron, 1974; Schwalbe, 1981) and to suppress populations through mating disruption (Beroza et al., 1975; Reardon et al., 1998). Decrease in mating success was found to be inversely dependent on the density of the moths and directly related to the amount of disparlure used. Greater mating disruption occurred in lower-density gypsy-moth populations than in higher density populations. Because of the cost of disparlure production, gypsy-moth population suppression by mating disruption is only practised when low doses are used against low-density insect populations (Webb et al., 1990). A double application of 75 g disparlure/ha in 1 year delayed population increase by 1 to 4 years. In low-density populations, mating disruption with aerially applied disparlure (at 75 g/ha)4 is an effective control of gypsy-moth populations (Leonhardt et al., 1996), reducing mating and the number of fertile egg masses laid by 70–85% (Webb et al., 1990). Work is continuing to evaluate the efficacy of lower dosages of disparlure to achieve mating disruption, making it more cost effective (Reardon et al., 1998).

Use of the barrier concept in gypsy-moth management Between 1920 and the 1950s, several largescale ‘barrier’ programmes were implemented to prevent the westward expansion of the gypsy moth (McManus and McIntyre, 1981; McFadden and McManus, 1991; Sharov et al., 1998). Until the early 1980s, the main goal of the barrier-zone management concept was eradication of infestations outside the barrier zone and suppression of the moderate- and high-density populations inside the barrier zone by various means (Sharov et al., 1998; Liebhold and McManus, 1999). The largest outbreak on record occurred in 1981

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 230


I.S. Otvos

when 5.2 million ha were defoliated by the gypsy moth, of which 150,000 ha were treated mostly with Dylox® (58.4%) and Sevin® (32.2%). The second largest outbreak was in 1990, when 2.9 million ha were defoliated and more than 660,000 ha of gypsymoth-infested stands were treated with Btk (59.0%) and Dimilin® (40.8%) (Fig. 10.5A). The barrier zone management concept was abandoned when the USFS embraced the IPM concept and different alternative approaches were tried (Reardon, 1991) to prevent gypsy-moth populations from expanding. These alternative approaches were tested in two pilot projects. The first alternative approach, tried in a pilot project (Maryland IPM 1983–1987) to manage low to moderate populations of gypsy moth using IPM, involved annual surveillance of insect densities using pheromone traps to determine gypsy-moth distribution and density to maximize natural control and the use of direct control measures when necessary in an environmentally acceptable way (Reardon et al., 1987). This approach was later modified in a second pilot project over a much larger area (Reardon, 1991). The Appalachian Integrated Pest Management Gypsy Moth Project (AIPM 1987–1992) was designed ‘to demonstrate the effectiveness of new and existing management technology in an IPM approach to minimize the spread and adverse effect of the gypsy moth’ (Reardon, 1991: 108). In the first phase of this second project, three products (Btk, Gypchek and disparlure) were tested on a small scale before applying them operationally (Reardon, 1991). During this project, areas with high gypsy-moth density were treated with Btk, Dimilin®4 and virus. Areas with low-density gypsy moth were treated with synthetic flakes impregnated with sex pheromones (disparlure) to reduce the number of fertile egg masses through mating disruption. Following these two projects, a third one, the Slow-the-Spread (STS) pilot project (1993–1998), was initiated by the USDA Forest Service with participating state agencies. This study determined the feasibility of using IPM strategies to slow the spread of the gypsy moth, with reduced pesticide use

and management costs compared with AIPM, over large geographical areas (Leonard and Sharov, 1995; Sharov and Liebhold, 1998a). Extensive monitoring of low-level gypsy-moth populations was conducted with pheromone traps. Isolated populations, well in advance of the infestation front (100–150 km), were suppressed or preferably eradicated. Btk, Gypchek and Dimilin® were used to eradicate or suppress gypsy moth in high-density populations and Gyplure (mating disruption) to manage lowdensity populations (Leonard and Sharov, 1995; R.C. Reardon, March 2003, personal communication). The effectiveness of the treatments applied during the STS gypsy-moth project conducted by the USDA Forest Service (on 188,064 ha) were analysed and compared (Sharov et al., 2002b). Disparlure treatment (93 blocks) was significantly more effective against isolated low-density populations of gypsy moth than Btk treatments (173 blocks). A large-scale evaluation of operational disparlure treatment of gypsy-moth populations has shown that this method is effective in isolated, well-defined, low-density infestations, but does not appreciably disrupt mating in high-density populations (Sharov et al., 2002b). The development of mating disruption has become the key element to the success of the STS programme (Sharov et al., 2002a). Analysis of gypsy-moth spread data has also shown that the STS programme has reduced the spread of this insect by more than 50% (Sharov et al., 2002a). In the past, the tendency was to eradicate isolated infestations as soon as they were detected. However, analysis of the treatments of gypsy-moth populations during the STS programme, from 1993 to 2001, suggested that it is better to postpone treatment until the gypsy-moth population is well delineated with a dense grid of pheromone traps (Sharov et al., 2002b). Since 1999, the STS strategy has become a comprehensive long-term national programme to protect the trees and forests in the USA from gypsy moth along the entire length of the expanding gypsy-moth front. STS coordinates efforts by the USDA Forest Service, the Animal and Plant Health

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 231

IPM in Forestry

Inspection Service (APHIS) and several states where the gypsy moth is not yet established (Sharov et al., 2002a). It uses three strategies: ● Suppressing populations within generally infested areas. ● Slowing the spread of gypsy moth to delay the impacts and costs associated with managing gypsy-moth outbreaks. ● Eradicating isolated infestations outside generally infested areas. In the USA, the approach currently used is to control the advancing front of increasing gypsy-moth populations to slow the expansion of this insect’s range. Pheromone traps are used to detect new outbreaks on the leading edge of the infestation, and environmentally benign insecticides, such as Btk, LdNPV or mating disruption, are used in the suppression or eradication programmes. Eradication is implemented in areas where the gypsy moth is detected well in front (100–150 km) of the spread. Suppression projects are conducted to reduce damage in areas where the gypsy moth is well established. Analysis of the historical records of the gypsy-moth spread in the eastern USA, revealed three distinct time periods with different rates of spread or expansion (Liebhold et al., 1992). From 1900 to 1915 the rate of spread was slow, about 9 km/year. The spread was reduced to c. 3 km/year from 1916 to 1965. This reduction was very probably due to the aggressively managed ‘barrier zone’ (e.g. detection, suppression and eradication) to reduce the gypsy moth’s westward movement. From 1966 to 1989, the rate of spread was very high (c. 21 km/year) (Liebhold et al., 1992, 1995). The STS project demonstrated the feasibility of reducing the rate at which insect infestations spread. Btk, Dimilin®, Gypchek and disparlure were tested to determine their efficacy against different densities of gypsymoth infestation. Btk, Dimilin® and Gypchek (LdNPV) are used to eradicate outlier or to suppress moderate to high gypsy-moth populations, while mating disruption using Gyplure is used to manage low-density populations (Reardon et al., 1994, 1998; Leonard


and Sharov, 1995). Mating disruption with disparlure was significantly more effective than Btk in reducing isolated low-density gypsy-moth populations (Sharov et al., 2002b). The gypsy-moth virus (Gypchek), because of its long incubation period and inconsistent efficacy (Podgwaite, 1999), is not the best choice for defoliation prevention. Dimilin® would be a better choice for use in campsites and other areas where its nontarget effects might be tolerated. Disparlure has been shown to substantially reduce gypsy-moth populations at low to medium densities (Reardon et al., 1998), and its operational use is increasing (Sharov et al., 2002a).

Success of the STS strategy Sharov and Liebhold (1998b) developed a model predicting that the spread of gypsy moth could be slowed by as much as 50% utilizing barrier zones (Liebhold et al., 1992; Sharov and Liebhold, 1998b). In practice, the actual rate of spread in the Appalachian Mountains was reduced by 59% (Liebhold et al., 1992), from 21 km/year to 9 km/year (Sharov and Liebhold, 1998c). Sharov and Liebhold (1998b) developed a model that specifies optimal strategies for eradication and containment. Their analysis and containment model disagree with the statement by Dahlsten et al. (1989) that ‘insects that have already colonized parts of the United States or any large land mass or continent, probably should not be the targets for eradication programs in other sections of the country because of their potential for recolonization’. Sharov and Liebhold (1998a) state that their ‘analysis clearly demonstrates that this statement is wrong. Eradication of small, isolated colonies of the gypsy moth within barrier zones is not only feasible, but also economically justified because the model predicts positive net benefits under realistic assumptions.’ There is economic benefit to slowing the spread of gypsy-moth populations (Leuschner et al., 1996; Sharov and Liebhold, 1998a). The costs of slowing the spread of gypsy moth have been estimated to be about

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 232


I.S. Otvos

25% of the expected potential benefits (Sharov et al., 1998). Since about two-thirds of the potential area in the USA containing highly susceptible host trees (mainly in the south-eastern USA) remains uninfested (Liebhold et al., 1997), slowing the spread of gypsy moth into these areas is economically beneficial (Leuschner et al., 1996; Sharov and Liebhold, 1998a). Estimated benefits associated with reducing the rate of spread outweighed the cost of implementing the STS programme (detecting and treating isolated infestations along and ahead of the expanding gypsy-moth population front) by at least 3 : 1 (Leuschner et al., 1996). This perceived or real benefit is indicated by individual households5 who, when surveyed, indicated a willingness to pay between US$13 and 57/ha for gypsy-moth control (Miller and Lindsay, 1993).

Gypsy moth in eastern Canada The use of chemicals and biological insecticides for eradication, suppression and delaying the spread of gypsy-moth populations, as well as the introduction of natural enemies, followed the same general trend in Canada (Fig. 10.5B) as in the USA (Fig. 10.5A). Therefore, for the sake of brevity, only the highlights will be mentioned here. In eastern Canada, the gypsy moth was first recorded in Quebec near the US border in 1924, and covered about 90 ha. Control measures using lead arsenate commenced the following year, and within 3 years the infestation was eradicated. A second invasion of gypsy moth, detected in New Brunswick in 1936, was successfully eradicated by 1940 (Jobin, 1995). No further introductions of gypsy moth were found in eastern Canada for the next 16 years. A survey and detection programme using pheromone-baited traps was initiated in 1954 and resulted in the discovery of a third infestation in 1956, near the site of its first introduction in Quebec (Cardinal, 1967). Spray operations, initiated in 1960, to control this infestation failed. The gypsy moth was later detected in Ontario in 1969, the infestation originating from a separate invasion from

the USA. After the failure to eradicate the gypsy moth in eastern Canada, only suppression programmes were conducted against the European strain of gypsy moth. The outbreak in Quebec peaked in 1977, with 518,000 ha of defoliated stands and in Ontario in 1985, with 246,000 ha defoliated. The area infested in Ontario decreased to almost 168,000 ha of moderate to severe defoliation in 1986 (Jobin, 1995), of which 103,094 ha were treated (Nealis et al., 2002). In the aerial-spray operations conducted between 1960 and 1974, chemical insecticides, mainly Sevin® and some DDT, were used (Brown, 1975). Until 1969, the main purposes of these control operations were twofold: eradication of small, incipient infestations and suppression of larger infestations. After 1969 the principal aims of these spray operations were, as in the USA, to suppress gypsy-moth larval populations and delay the spread of gypsy moth into uninfested areas (Jobin, 1995). Between 1975 and 1989 Btk, Sevin® and Dimilin® were mainly used operationally for suppression (Jobin, 1995). Btk was used almost exclusively operationally after 1981 (Nealis et al., 2002; Fig. 10.5B). Work on the use of pathogens (Btk and LdNPV) for gypsy-moth suppression did not start in Canada until the 1970s (Griffiths and Quednau, 1984). Btk slowly gained acceptance as an effective suppression tool of gypsy-moth populations and, at its peak use in 1986, over 103,000 ha of gypsy-mothinfested stands were treated in Ontario (Jobin, 1995; Nealis et al., 2002). Although the virus (LdNPV) is also registered and effective for suppression of gypsymoth populations, it is not yet commercially available. Consequently, the virus was only used experimentally in Canada (Jobin, 1995; Nealis et al., 2002), unlike in the USA where the USDA Forest Service produces and uses it in cooperative projects. Since the establishment of the gypsy moth in North America, 26 species of parasitoids native to North America have been found to successfully attack and develop in this unwanted newcomer (Griffiths, 1976; Sabrosky and Reardon, 1976; Griffiths and Quednau, 1984). In addition, 17 native insect

10IntpestManCh10.QXD 15/4/04 2:26 pm Page 233

IPM in Forestry

predators and four mammalian predators also prey on the gypsy moth (Griffiths, 1976). Of the 26 parasitoid species that attack gypsy moth in the USA, 14 species were also reared from other hosts in southern Ontario and Quebec near the US border (Griffiths and Quednau, 1984), indicating the generalist nature of most of these parasitoids. A review of the world literature on the parasitoids and predators of the gypsy moth showed that there are close to 400 species of natural enemies associated with the gypsy moth (Griffiths, 1976). Some of these were originally introduced against the browntail moth, Euproctis chrysorrhoea (Linnaeus) (Hewitt, 1916). Of the over 50 species of exotic parasitoids and predators released in the USA, 13 species of exotic parasitoids and one predator became established, 29 parasitoids and eight predators did not (Griffiths, 1976). Of these 13 exotic species of parasitoids established in the USA, nine species spread into Canada on their own. In fact, four of these parasitoid species were recovered in southern Ontario and Quebec before the gypsy moth was recorded in the area and before any exotic parasitoids were introduced against the gypsy moth in Canada (Griffiths and Quednau, 1984). Based on the review of literature of gypsy-moth parasitoids and predators (Griffiths, 1976) and their own work (including egg parasitoids) in Canada, Griffiths and Quednau (1984) concluded, ‘The establishment of exotic insect parasites [parasitoids] on the gypsy moth in Canada is proceeding well largely through natural dispersal’ and ‘there is little more to be done in the introduction of biological control agents because there are no more suitable candidates’ (Griffiths and Quednau, 1984). However, most of the seven introduced parasitoids were collected in moderate to high gypsy-moth populations. Consequently, since 1980, work in Canada has focused on finding parasiotids in Europe that might be effective at low gypsy-moth densities. This resulted in the introduction and release of a little known tachinid fly in Canada (Mills and Nealis, 1992; Nealis and Quednau, 1996). However, it is too early to evaluate the impact of this latest introduction on the gypsy-moth population.


Gypsy moth on the west coast In western North America, neither the European nor the Asian strains of the gypsy moth have become established to date. Effective detection grids using pheromone traps around ports and in suspect areas and immediate eradication are the policy on the Pacific coast of Canada and the USA. So far, only small spot infestations of these two strains (mainly the European strain) have been found in British Columbia, Washington and Oregon, and all have been successfully eliminated through aggressive aerial and ground application of Btk, as was the infestation of the Asian strain introduced into North Carolina in 1993 on US military equipment returning from Germany, at a cost of about US$9 million (Wallner, 1996). The first interception of the gypsy moth on the west coast was in 1911 in British Columbia, when egg masses were found on ornamental Thuja trees from Japan (Brown, 1975). The egg masses were destroyed but not before a few larvae hatched (Humble and Stewart, 1994). The interceptions and repeated eradications of the gypsy moth in British Columbia (both European and Asian strains) have been summarized by Humble and Stewart (1994). In eradication programmes, application is generally from the air, although at times the less effective and more expensive ground treatments are used as a result of court challenges by environmental groups opposing the eradication programmes and/or aerial spraying of Btk or any other insecticidal product. The Asian strain was introduced in 1991 by Russian ships coming from the Far East but was also eradicated successfully in 1992 (Humble and Stewart, 1994). During this eradication, 19,000 ha were treated, at an estimated cost of CAN$6.5 million (Nealis, 2002). Since this incident, federal inspectors have banned ships from inshore waters when gypsy-moth egg masses are discovered on the superstructure of freighters during larval hatch and development (Humble and Stewart, 1994). Eradication gets complicated when noninfested countries or regions impose trade embargoes. Such was the case with the 1999

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 234


I.S. Otvos

eradication programme in British Columbia, which resulted from an unusual situation arising among the various government agencies responsible for responding to the exoticinsect threat and trying to meet trade conditions imposed by regions that are threatened by L. dispar invasion. Until 1998, the federal government’s Canadian Food Inspection Agency (CFIA) conducted eradication programmes against the gypsy moth (both European and Asian strains) in British Columbia. Following the eradication programme in 1998, CFIA announced that it would no longer consider eradication of the European gypsy moth from British Columbia and would only regulate infested areas. Consequently, the USA imposed trade restrictions on lumber and log exports from British Columbia, forcing the provincial government to pass an order-in-council to enable them to treat the 13,000 ha that had been delineated for treatment, based on pheromone-trap catches on southern Vancouver Island. This eradication programme, conducted in 1999, cost c. CAN$3.7 million (Nealis, 2002).

Management of Bark Beetles Over 200 species of scolytid bark beetles occur in Canada and Alaska (Bright, 1976). Nine are economically important and seven of these attack conifers. The most destructive conifer-attacking bark beetles, in descending economic importance, are: ● mountain pine beetle, Dendroctonus ponderosae Hopkins; ● spruce beetle, Dendroctonus rufipennis (Kirby); ● Douglas fir beetle, Dendroctonus pseudotsugae Hopkins; ● western balsam bark beetle, Dryocoetes confusus Swaine. These beetles breed in the inner bark and phloem of the main bole of their host trees. Needles of trees successfully attacked by bark beetles first fade and then turn to a reddish-brown colour (pines, firs, Douglas fir) or the faded needles fall off (spruce). The trees attacked by mountain pine beetle die

within 3 or 4 weeks of attack, but the foliage may not change colour until the following year. For the host trees attacked by the other three destructive bark-beetle species, the process of tree death is similar to that caused by the mountain-pine beetle. Periodic barkbeetle outbreaks frequently cause catastrophic economic losses. During the last outbreak (1972 to 1985) the mountain pine beetle killed approximately 195.7 million pines in British Columbia, representing an estimated potential economic loss of $14.4 to 19.6 billion, of which about $4.0 to 5.4 billion worth of beetle-killed trees could not even be salvaged (Borden, 1990). During the peak of the outbreak in 1983, an estimated 43 million mature lodgepole pine (Pinus contorta Dougl. ex. Loud. var. latifolia Engelm.), representing enough lumber to build 270,000 threebedroom homes (S.R. Whitney, 1985, personal communication), were killed in infestations that covered nearly half a million hectares of forests (Wood et al., 1983). The current mountain pine beetle outbreak in British Columbia, which started around 1992, now (2003) covers an estimated 2.0 million ha. Infestations by D. rufipennis and D. pseudotsugae occurred over an additional 1.2 million ha (British Columbia Ministry of Forests, 2003). There is no indication of a decline in the mountain pine beetle outbreak. At present, bark-beetle outbreaks of this magnitude can only be terminated by unseasonably cold temperatures (−35°C or lower for several days) (Somme, 1964) with little or no snow cover around the infested bole. The earliest control operations against bark beetles occurred in the late 1910s and were directed at D. rufipennis and D. ponderosae outbreaks in eastern and western Canada, respectively. These early control attempts involved harvesting the infested stands or performing individual tree treatments such as fell-and-burn, or peeling and burning the infested bark. By the late 1940s, the chemical insecticides ethylene dibromide (EDB), a fumigant, and benzene hexachloride (BHC (lindane)), were the most commonly used chemicals. BHC was formulated in fuel oil, usually as a 2% solution, and used as a bark-penetrating insecticide to kill broods under the bark or as a water emul-

10IntpestManCh10.QXD 5/5/04 2:11 pm Page 235

IPM in Forestry

sion for protecting trees from beetle attack. Trap trees, felled or standing, either treated or not treated with chemical insecticides, were commonly used after the 1940s, and aerial-detection surveys were used for delineating infestations. By the late 1970s, the use of BHC and EDB was phased out, owing to environmental concerns, and were replaced by a systemic pesticide, monosodium methane arsenate (MSMA).

Management methods Management options are available for two of the most important beetles: the mountain pine beetle and the spruce beetle (McMullen et al., 1986; Safranyik et al., 1990; Maclauchlan and Brooks, 1994). Bark-beetle management is based on two approaches: direct control and prevention (McMullen et al., 1986). Direct control is currently used operationally, and is most effective when a beetle infestation is small or just beginning to develop. At this time the direct-control measures are implemented to lower beetle populations to endemic levels or until one of the other management options can be implemented. There are two main operational direct-control measures: sanitary logging of infested stands and treatment of individual trees, mainly using lethal and conventional trap trees or fell-and-burn, or using sevin (carbaryl) as a bark-penetrating chemical. Silvicultural methods, such as sanitation– salvage logging or felling and burning of the infested trees (McMullen et al., 1986), will reduce beetle populations if applied in a timely fashion, that is, before the new generation of adult beetles leaves the infested trees. Individual trees are ‘treated’ by the cut–pile–burn method or by injecting the infested trees with the herbicide MSMA to kill the new brood of larvae (McMullen et al., 1986). MSMA has to be applied within a few weeks of the attack while the trees are still alive and can translocate the poison. Sanitation logging is generally used to treat larger, more diffuse infestations, and involves removing (logging) the attacked trees containing the beetle brood. In high-


value or high-impact areas, such as parks and campsities, the lower boles of trees can be treated with 2% active ingredient (AI) carbaryl in water to protect trees from lethal attack (McMullen et al., 1986). Preventive management is the preferred option, and entails long-term planning and the use of forestry practices that reduce stand susceptibility. For D. ponderosae, preventive management is based on reducing the susceptibility of lodgepole pine stands (Shore and Safranyik, 1992; Shore et al., 2000) and involves forestry practices such as spacing, age stratifying, stocking and stand conversion and species control, which may be combined with sanitary harvesting/logging. One or a combination of the following management options that prevent or delay outbreak development can reduce stand susceptibility, i.e. shorter rotation age, conversion of forest type to a less susceptible one, creation of mixed-age stands, creation of mixed-host-species stands and changing stand structure and stocking (Safranyik et al., 1974). All of these options are used in British Columbia. The spacing and thinning of stands and partial cutting have been effective in reducing losses caused by mountain pine beetle in mature lodgepole pine (Mitchell et al., 1983; Cole and McGregor, 1985) and second-growth ponderosa pine (Sartwell and Dolph, 1976) in the USA. Semiochemicals – chemicals eliciting interactions between organisms – can be used to manipulate mountain pine beetle (Borden, 1989). During the past 25 years, the use of population-aggregating pheromones became standard practice to contain and concentrate infestations in order to increase the efficacy of the control operation. The aggregation pheromone can be used in surveys to monitor beetle populations or to concentrate flying beetles in trees where they can be treated with a systemic herbicide, such as MSMA. Baiting of individual trees and small isolated stands with bark-beetle aggregation pheromone concentrates beetle attacks, decreasing the spread of the infestation and increasing the cost-effectiveness of directcontrol operations through sanitation logging (Borden et al., 1983). Treating individual or small groups of trees with anti-aggrega-

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 236


I.S. Otvos

Table 10.5. Major forestry weed species competing with the production of commercial forest crop trees in Canada (from Wall et al., 1992). Species Trees Acer macrophyllum Pursh Acer rubrum L. Acer spicatum Lambert Alnus incana (L.) Moench Alnus rubra Bongard Corylus cornuta Marshall Populus tremuloides Michaux Salix spp. Shrubs Gaultheria shallon Pursh Ribes spp. Rubus idaeus L. Rubus parviflorus Nuttall Rubus spectabilis Pursh Sambucus spp. Herbaceous plants Calamagrostis canadensis (Michx.) Palisot de Beauvois Epilobium angustifolium (L.) Kalmia angustifolia L. Pteridium aquilinum (L.) Kuhn

Common name


Big-leaf maple Red maple Mountain maple Speckled alder Red alder Beaked hazelnut Trembling aspen

Coastal British Columbia Ontario, Quebec, Maritimes Ontario, Quebec, Manitoba, Maritimes Transcontinental Coastal British Columbia Transcontinental Transcontinental



Salal Currants and gooseberries Red raspberry Thimbleberry Salmonberry Elderberries

Coastal British Columbia British Columbia, Ontario, Quebec, Maritimes Ontario, Quebec, Maritimes British Columbia Coastal British Columbia Transcontinental

Blue-joint grass

Alberta, interior British Columbia

Fireweed Sheep laurel Bracken fern

Transcontinental Newfoundland, Maritimes Transcontinental

tion pheromone is thought to repel beetles from the trees in the treated stand. Variation in the use of these aggregation and antiaggregation pheromones, as proposed and tested by Borden (1995), has met with varying degrees of success. Population-aggregating pheromones are used extensively to increase the efficacy of control programmes. Direct-control operations are guided by pretreatment population and damage assessments and an appropriate strategy and set of tactics that are based on the field assessment combined with consideration of environmental and socio-economic concerns. The management operations are guided by decision support systems that determine susceptibility and risk (Shore and Safranyik, 1992; Shore et al., 2000) and feasible strategies and tactics to be used in particular situations (Maclauchlan and Brooks, 1994).

Vegetation Management in Forestry Unwanted (weedy) vegetation is a major source of competition for water, nutrients, light and space in nurseries, plantations and areas of natural conifer regeneration (Watson and Wall, 1995). Some weeds, such as Ribes spp. and fireweed, Epilobium angustifolium (Linnaeus), are alternative hosts of important forest-tree rust diseases (Ziller, 1974; Hansen and Lewis, 1997). Competition from weedy vegetation can delay seedling establishment, reduce growth, decrease timber yield and delay harvest (increase rotation age) of conifer crop trees. The economic losses caused by weeds in forestry were not fully appreciated until recently (Walstad and Kuch, 1987). Most forest weeds are native species. Among the major competitors of crop-tree species, nine are fast-growing hardwood

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 237

IPM in Forestry


70 Chemical 60

Area treated (’000 ha)

Manual 50




30 20 10


/9 91 19



8 19



6 19

/8 85 19

/8 83 19






Year Fig. 10.6. Methods and trends of vegetation management in forest areas on crown-land in British Columbia, 1981–1993 (after Boateng, 1996).

trees, six are shrubs and four are herbaceous plants (Wall et al., 1992; Table 10.5). In most cases, the unwanted vegetation can only be managed, not eliminated. In forestry, as in agriculture, competing vegetation has to be managed to favour the growth of the crop species. A number of methods have been, and are still, used for vegetation management, as illustrated in Fig. 10.6. In British Columbia, of the vegetation management treatments conducted during a 10-year period (1981/82–1992/93), 57% were done by using herbicides alone, 36% by using manual cutting, 4% by using a combination of herbicides and cutting and 3% by sheep grazing (Fig. 10.6). Manual removal of the competing vegetation is expensive and inefficient (Pendl and D’Anjou, 1990). Mechanical methods, using various kinds of machinery for site preparation after logging, are also expensive and, in addition, favour resprouting of some weedy species and tend to compact the soil (Prasad, 1996). Prescribed fire is sometimes used in an attempt to eliminate weed seeds, unwanted seedlings and stumps. It also retards the regrowth of vegetation that would compete

with the establishment and growth of croptree species (Feller, 1996). Fire does not eliminate the roots of perennial weeds and in fact stimulates sprouting of some perennial weeds and tree species (Prasad, 1996). Grazing by animals, mainly sheep, has been tried experimentally on a relatively small scale in Australia, Canada, Ireland, New Zealand, Sweden and the USA (Sharrow et al., 1989; Cayford, 1993). Sheep grazing is now used operationally in forestry to control weeds, but only in small plantations. Mulching with allelopathic plant material (i.e. chemicals that leach out of the mulch and suppress weed growth) has been tried experimentally (McDonald and Fiddler, 1996). Mulching, as well as brush and plastic blankets, works well in nurseries and in small intensively managed plantations, but operational use of these methods is not yet practical in forestry (Jobidon et al., 1989; Jobidon, 1991a). Some microorganisms and plants produce natural herbicides that are toxic to some weed species (Duke, 1986; Duke and Lydon, 1987). For example, bialophos (aminohydroxyphospho-vinyl-butyryl-alanine), originally

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 238


I.S. Otvos

Area treated (’000 ha)

60 50 40 30 20 10

00 20

95 19

90 19

85 19

80 19



0 Year Fig. 10.7. Forest area treated with herbicidesa for weed management in British Columbia by the Ministry of Forests and Forest Companies between 1975 and 2000 (from Humphreys, 1986, 1990; Canadian Council of Forest Ministers, 2003). a Herbicides applied in large-scale operations include 2,4-D, 2,4-E, fosamine, glyphosate, hexazinone, MSMA, picloram and triclopyr. Glyphosate has been used preferentially since 1985.

isolated from the soil microbe Streptomyces viridochromogens (Jobidon, 1991b), controls red raspberry (Rubus idaeus L.) in forest plantations. However, it is expensive, is toxic to some conifers and has only limited use in forestry (Jobidon, 1991b; Prasad, 1992). Competition by herbaceous and woody vegetation frequently requires treatment with commercial herbicides. Although the use of herbicides has been part of forest management since the mid-1940s, in British Columbia, Canada, the area treated annually was small (about 5000 ha/year) until the early 1980s (DeBoo and Prasad, 1997). Chemical herbicides were the choice of treatment (mainly 2,4-dichlorophenoxyacetic acid (2, 4-D) and 2, 4, 5-trichlorophenoxyethanoic acid (2, 4, 5-T)) and have been used for vegetation management in British Columbia since the mid-1970s (Fig. 10.7) and are the most cost-effective, especially if they can be applied from the air (Thorpe, 1996). After 1983, increased funding was available for forest management, resulting in generally increased pesticide use until 1992 (Fig. 10.7). After 1985, 2,4-D and 2,4,5-T were replaced by glyphosate because of health and envi-

ronmental concerns (DeBoo and Prasad, 1997) and for political reasons (Halleran, 1990). Restrictions on pesticide use for weed control in forestry will probably increase. Therefore, it is necessary to develop one or more cost-effective and environmentally acceptable methods of weed control (i.e. alternatives to chemical herbicides) in forestry. Biological control (especially in the case of introduced organisms) and the socalled bioherbicides may offer such an option. Bioherbicides are ‘living entities’ used to deliberately suppress the growth of weeds or reduce weed populations to economically acceptable levels in areas where they compete with the desired crop grown (Watson, 1989; Auld and Morin, 1995). These controls may include insects and pathogens (bacteria, fungi and viruses). The terms biological herbicides, bioherbicides and mycoherbicides are used interchangeably in the scientific literature to describe all pathogens (Winder and Shamoun, 1991). The term mycoherbicides, however, is more appropriate when referring to herbicides based on fungal pathogens. For the purposes of this chapter, the term originally used in the paper is retained when reference is made to a particular paper. Biological control strategies in weed management in forestry include both classical (inoculative) and inundative (augmentative) inoculation with plant pathogens (Watson and Wall, 1995; Wall and Hasan, 1996). The inoculative (classical) approach is generally employed when the noxious weed was accidentally or intentionally introduced, usually from one continent to another. The natural enemy (usually a pathogen) or most promising enemies are introduced in the hope that they will spread throughout the ‘pest’ host population, resulting in control. The inundative approach is mainly employed against endemic weedy populations. The weeds are treated with a large amount of indigenous natural enemies, usually fungal pathogens of the weeds, which augment the local, naturally occurring pathogens. The remainder of this section will review the major accomplishments using these approaches for vegetation management in forestry.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 239

IPM in Forestry

The biological control of weeds in agriculture has a long history, with many notable successes (McLeod, 1962; Harris, 1984; Kelleher and Hulme, 1984), but it is relatively new in forestry (Fig. 10.1). Similar successes are also reported from the USA. The study of biological controls for vegetation and plant-pathogen management started only recently, in the last 20 years. In Canada between 1981 and 2000, there were 20 studies on the biocontrol of weeds of agricultural crops and only five on forest weeds and two on forest-tree diseases (Mason and Huber, 2002).


white-rot fungus Cylindrobasidium laeve (Pers.: Fr.) Chamois has been registered as Stumpout™ for the control of introduced wattle trees, Acacia spp. (Morris et al., 1998). However, some introductions can lead to controversy. When the gorse mite, Tetranychus lintearius Dufour, was imported to control the introduced gorse, Ulex europaeus L., in New Zealand, it became controversial because the introduction gave only variable control and the exotic mites interbred with one of the native mite species (Syrett et al., 1985).

Bioherbicides Inoculative strategy (classical biological control) The classical biological control strategy (introducing insect enemies of exotic weeds) has been used successfully in agriculture (Harris, 1984; Julien and Griffiths, 1998; Harris and Shamoun, 2002). The European blackberry (Rubus fruticosus L. agg.) has been introduced to many parts of the world and is regarded as an important weed pest in several countries, including Australia, where it invades pastures, forest and national parks (Amor and Richardson, 1980; Wall and Hasan, 1996). The rust fungus Phragmidium violaceum (Shultz) was introduced into Australia, where it controlled the European blackberry under the shady canopy of pine trees, thereby freeing pine seedlings from blackberry competition and allowing them to grow normally after the release. However, the rust was less effective on blackberries growing under the more open eucalyptus stands. This was not unexpected because the microclimate is probably drier in the more open stand of eucalyptus. A gall-forming rust fungus, Uromycladium tepperianum (Sacc.) McAlp., was introduced into South Africa against the weed tree, Acacia saligna (Labill) Wendl. Both the fungus and the host tree originated in Australia. The fungus became established in South Africa and infected and formed galls on the flowers of A. saligna, killing some of the trees (Morris, 1991, 1997). In South Africa, the

Despite three decades of research, the development of effective bioherbicides for weed control in forestry is still in its infancy. Many preliminary results indicate the great potential value derived from the use of biological control in vegetation management in forestry (Shamoun, 2000; Shamoun and DeWald, 2002; Shamoun et al., 2002, and references therein). In fact, to date, only two mycoherbicides are commercially available for controlling weeds along hydroelectric power lines and for forestry use (Morris et al., 1998; Shamoun and Hintz, 1998a,b). Of the bioherbicides tested, the manipulation of indigenous fungi probably offers the best chance for the development of mycoherbicides because they are native and generally persist at endemic levels in the environment. Research on plant pathogens as potential biocontrol agents for weed control started in the 1970s to suppress ericaceous shrubs on cut-over sites in eastern Canada (Wall, 1977) and later to control Rubus spp. (Wall, 1983). Of the biocontrol agents examined, Chondrostereum purpureum Fr./Pouzar was the most promising bioherbicide (Wall, 1990). In western Canada, research has focused on weedy trees (Acer macrophyllum Pursh, Alnus rubra Bong., Populus tremuloides Michx.), and shrubs (Rubus parviflorus Nutt., Rubus spectabilis Pursh., Gaultheria shallon Pursh.). Pathogens from all of these target species have been identified and many of them have been tested as potential biocontrol

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 240


I.S. Otvos

agents (Dorworth, 1990, 1992; Sieber et al., 1990a,b; Wall and Shamoun, 1990b). When applied to cut stumps, C. purpureum provided spectacular results and gave 90% control of black cherry (Prunus serotina Ehrhert) regrowth in conifer plantations in Holland. This level of control matched the effectiveness of the chemical herbicide glyphosate (Scheepens and Hoogerbrugge, 1989). However, in Canada, the same treatment gave somewhat less spectacular results against Populus spp., Acer spp., Betula spp., Prunus pensylvania and Alnus rubra (Wall and Shamoun, 1990a; Wall, 1994). Considerable research has also been done on C. purpureum in Canada. MycoForestis Corporation (Quebec) has registered one strain (HQ-1) under the name MycoTech™ Paste for use east of the Rocky Mountains in Canada. Another strain (PFC 2139) is currently being registered for use in western Canada and the entire USA (Shamoun and Hintz, 1998a,b). After considerable testing, C. purpureum has been adopted, with a refined formulation, and patented for control of hardwoods in North American forests (Wall et al., 1996). However, C. purpureum has not been registered as a mycoherbicide in Holland but is used only as a wood-decay promoter (Ravensberg, 1998). Presumably, it was not registered there as a herbicide because of the cost of registration and the expected return on this investment. The same economic considerations may hinder the commercial production and sale of mycoherbicide in forestry worldwide. Some bioherbicides have been tested against several hardwood trees (Shamoun et al., 2002), marsh reed grass (Calamagrostis canadensis (Michx.) Beauv) (Mallet et al., 2002), Rubus spp. (Oleskevich et al., 1998), fireweed (Epilobium spp.) (Winder, 2002), Scotch broom, Cytisus scoparius (Linnaeus) Link (Prasad, 2002a) and gorse (Ulex europaeus L.) (Prasad, 2002b). However, there are several obstacles to the development of commercial products, such as application technology, formulation to increase efficacy of the product so that it can be stored and readily applied in the field, optimum volume and droplet size to give the optimum efficiency, which are still unknown, and the

scarcity of examples proving the commercial viability of this approach. The main reason for this is due to the fact that C. purpureum can only enter through an open wound of the host tree and at present this can only be achieved through manual inoculation of the wound (cut surface) of the target plant. In forestry, on a large scale, this is probably not feasible, but it may be practical to use under hydroelectric powerlines.

Silvicultural Management of Root Diseases Root diseases caused by Armillaria ostoyae (Romagn.) Herink, Phellinus weirii (Murr.) Gilb. and Inonotus tomentosus (Fr.: Fr.) Teng. are among the most destructive pathogens of trees, mainly conifers grown for timber, in western North America. They cause significant growth loss and tree mortality in managed forests (Bloomberg and Reynolds, 1985; McDonald et al., 1987; Morrison et al., 1988, 1992; Bloomberg and Morrison, 1989; Ives and Rentz, 1993; Woods, 1994). Of these, Armillaria root disease caused by A. ostoyae, is the most important. It occurs in all forest regions of Canada. In the interior of British Columbia it is estimated to cause losses of 2–3 million m3 annually (A. Van Sickle, 1999, personal communication). Even in undisturbed stands (Morrison and Mallet, 1996), up to 80% of the trees in a stand can be infected. All three root diseases reduce merchantable volume at the end of the planned rotation, change species composition over the rotation by killing the most susceptible hosts and may lengthen the rotation age (Morrison and Mallett, 1996; Sturrock, 2000). The same management strategies can be applied to reduce the impact for all three root diseases. It is best to apply treatments at the time of harvest and at stand regeneration. The two most effective ways of reducing the root diseases and their impacts are the following: 1. Machine-assisted removal of inoculum source (infected stumps and large roots) at the time of harvesting or by push–pull logging of trees in root-diseased stands

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 241

IPM in Forestry


(Morrison et al., 1992; Sturrock et al., 1994; Morrison and Mallett, 1996; Sturrock, 2000). 2. Planting resistant trees. Birch, aspen and poplar are tolerant of A. ostoyae (Morrison and Mallett, 1996). All hardwoods are immune to P. weirii (Morrison et al., 1988, 1992) and birch is immune to I. tomentosus (Sturrock, 2000).

associated costs are justified by increased rates of return in the next rotation: that is, the volume grown on the treated sites will more than pay for the inoculum removal.

Both mechanical methods to remove sources of inoculum are called stumping (Morrison and Mallett, 1996). Stumping exposes infected roots to the sun, thus drying the roots and killing the fungi. Removal of the source of the inoculum from the soil reduces the possibility of infection in the next crop of trees. Economic analysis conducted for P. weirii in western Washington (Russell et al., 1986) and for A. ostoyae in New Zealand (Shaw and Calderon, 1977) indicates that the high disease incidence and losses that occur on non-treated sites can be reduced by removing the inoculum. The


Notes 1




The remainder was treated with the chemical insecticides fenitrothion and aminocarb (Cunningham and van Frankenhuyzen, 1991). The virus has to be produced in living insects, therefore it is expensive to make. The cost of producing enough virus to treat 1 ha at the recommended label dose of 2.51011 PIB/ha is about CAN$40–50/ha. The cost of disparlure treatment at this dose was estimated at US$64/ha, while double application of Btk cost c. US$64–69/ha (Sharov et al., 2002b). Dimilin® is a chitin synthesis inhibitor, and only affects arthropods. However, it can kill or negatively affect many non-target arthropods (Butler et al., 1994). The survey was conducted in New Hampshire and included both households that had and had not experienced gypsy-moth damage to their properties.

References Alfaro, R.I. and Maclauchlan, L.E. (1992) A method to calculate the losses caused by western spruce budworm in uneven-aged Douglas-fir forests of British Columbia. Forest Ecology and Management 55, 295–313. Amor, R.L. and Richardson, R.G. (1980) The biology of Australian weeds 2. Rubus fruticosus L. agg. Includes distribution and ecological aspects. Journal of the Australian Institute of Agricultural Science 46, 87–97. Andreadis, T.G. and Weseloh, R.M. (1990) Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proceedings of the National Academy of Sciences of the USA 87, 2461–2465. Armstrong, J.A. and Cook, C.A. (1993) Aerial Spray Applications on Canadian Forests: 1945–1990. Information Report ST-X-2, Forestry Canada, Ottawa, Ontario, 266 pp. Auld, B. and Morin, L. (1995) Constraints in the development of bioherbicides. Weed Technology 9, 638–652. Balch, R.E. and Bird, F.T. (1944) A disease of the European spruce sawfly, Gilpinia hercyniae (Htg.), and its place in natural control. Scientific Agriculture 25, 65–80. Baranchikov, Y.N. (1989) Ecological basis of the evolution of host relationships in Eurasian gypsy moth populations. In: Wallner, W.E. and McManus, K.A. (technical coordinators) Proceedings, Lymantriidae: a Comparison of New and Old World Tussock Moths, June 26-July 1, 1988, New Haven, Connecticut. General Technical Report NE-123, USDA Forest Service, Northeastern Forest Experiment Station, Broomall, Pennsylvania, pp. 319–338. Beroza, M., Hood, C.S., Trefey, D., Leonard, D.E., Knipling, E.F. and Klassen, W. (1975) Field trials with disparlure in Massachusetts to suppress mating of the gypsy moth. Environmental Entomology 4, 705–711. Bird, F.T. (1959) Polyhedrosis and granulosis virus causing single and double infections in the spruce budworm. Journal of Insect Pathology 1, 406–430. Bird, F.T. (1961) Transmission of some insect viruses with particular reference to ovarial transmission and its importance in the development of epizootics. Journal of Insect Pathology 3, 352–380.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 242


I.S. Otvos

Blais, J.R. (1985) The ecology of the eastern spruce budworm: a review and discussion. In: Sanders, C.J., Stark, R.W., Mullins, E.J. and Murphy, J. (eds) Recent Advances in Spruce Budworms Research: Proceedings of CANUSA Spruce Budworms Research Symposium, Bangor, Maine, September 16–20, 1984. Canadian Forestry Service, Ottawa, Ontario, pp. 49–59. Bloomberg, W.J. and Morrison, D.J. (1989) Relationship of growth reduction in Douglas-fir to infection by Armillaria root disease in southeastern British Columbia. Phytopathology 79, 482–487. Bloomberg, W.J. and Reynolds, G. (1985) Growth loss and mortality in laminated root rot infection centres in second-growth Douglas-fir on Vancouver Island. Forest Science 31, 497–508. Blumenthal, E.M., Fusco, R.A. and Reardon, R.S. (1978) Augmentative release of two established parasite species to suppress populations of the gypsy moth. Journal of Economic Entomology 72, 281–288. Boateng, J. (1996) Past and future trends in forest vegetation management in BC. In: Coroneau, P.G., Harper, G.J., Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation Management: Options and Applications. Proceedings of the Fifth British Columbia Forest Vegetation Management Workshop, November 29–30, 1993 Richmond, British Columbia. Forest Resource Development Agreement Report No. 251, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, pp. 1–4. Borden, J.H. (1989) Semiochemicals and bark beetle populations: exploitation of natural phenomena by pest management strategists. Holarctic Ecology 12, 501–510. Borden, J.H. (1990) Semiochemicals to manage coniferous tree pests in western Canada. In: Ridgway, R.L., Silverstein, R.M. and Inscoe, M.N. (eds) Behavior-modifying Chemicals for Insect Management: Applications of Pheromones and Other Attractants. Marcel Dekker, New York, pp. 281–315. Borden, J.H. (1995) Development and use of semiochemicals against bark and timber beetles. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 431–449. Borden, J.H., Chong, L.J., Pratt, K.E.G. and Gray, D.R. (1983) The application of behaviour-modifying chemicals to contain infestations of the mountain pine beetle, Dendroctonus ponderosae Hopk. The Forestry Chronicle 59, 235–239. Boulton, T.J. (1999) Impacts of Bacillus thuringiensis subsp. kurstaki (Btk) on the population dynamics of non-target Lepidoptera on Ribes cereum. MSc thesis, University of Victoria, Victoria, British Columbia, 287 pp. Boulton, T.J., Otvos, I.S. and Ring, R.A. (2002) Monitoring nontarget Lepidoptera on Ribes cereum to investigate side effects of an operational application of Bacillus thuringiensis subsp. kurstaki. Environmental Entomology 31, 903–913. Bright, D.E. Jr (1976) The Insects and Arachnids of Canada. Part 2: The Bark Beetles of Canada and Alaska. Coleoptera: Scolytidae. Publication 1576, Biosystematics Research Institute, Research Branch, Canadian Department of Agriculture, Ottawa, Ontario, 241 pp. British Columbia Ministry of Forests (2003) Forest Health Conditions 2002, Aerial Overview Survey Summary. Available at: Brown, G.S. (1975) Gypsy moth Porthetria dispar (L.). In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Environment Canada, Ottawa, Ontario, pp. 208–212. Brown, W.L. Jr (1961) Mass insect control programs: four case histories. Psyche 68, 75–111. Buckner, C.H., Kingsbury, P.D., McLeod, B.B., Mortensen, K.L. and Ray, D.G.H. (1974) Impact of aerial treatment on non-target organisms, Algonquin Park, Ontario, and Spruce Woods, Manitoba. In: Chemical Control Research Institute (ed.) Bacillus thuringiensis – Evaluation of Commercial Preparation of Bacillus thuringiensis With and Without Chitinase Against Spruce Budworm. Information Report CC-X-59, Chemical Control Research Institute, Ottawa, Ontario, pp. F1-F72. Butler, L., Chrislip, G.A., Kondo, V.A. and Townsend, E.C. (1974) Effect of diflubenzuron on nontarget canopy arthropods in closed, deciduous watersheds in Central Appalachian forest Journal of Economic Entomology 90, 784-779. Cadogan, B.L. (1995) Jack pine budworm, Choristoneura pinus. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 123–126. Cameron, E.A. (1974) Programs utilizing pheromones in survey or control: the gypsy moth. In: Birch, M.C. (ed.) Pheromones. American Elsevier Publication Company, New York, pp. 431–435. Cameron, J.M. (1975a) Biological insecticides. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of Environment, Ottawa, Canada, pp. 25–33.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 243

IPM in Forestry


Cameron, J.M. (1975b) Field trials of spruce budworm viruses, 1971–1973. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of Environment, Ottawa, Canada, pp. 134–137. Campbell, R.W. (1963) The role of disease and desiccation in the population dynamics of the gypsy moth Porthetria dispar (L.) (Lepidoptera: Lymantriidae). The Canadian Entomologist 95, 426–434. Campbell, R.W. and Podgwaite, J.D. (1971) The disease complex of the gypsy moth. I. Major components. Journal of Invertebrate Pathology 18, 101–107. Canadian Council of Forest Ministers (2003) National Forestry Database Programme. Available at: Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry (1971) Biological Control Programmes Against Insects and Weeds in Canada 1959–1968. Technical Communication No. 4, Commonwealth Institute of Biological Control, Commonwealth Agricultural Bureaux, Slough, UK, 266 pp. Canadian Forest Service (1975) Report of the Annual Forest Pest Control Forum. Environment Canada, Canadian Forest Service, Ottawa, Ontario, 225 pp. Canadian Forest Service (1976) Report of the Annual Forest Pest Control Forum. Environment Canada, Canadian Forest Service, Ottawa, Ontario, 341 pp. Canadian Forest Service (1977) Report of the Annual Forest Pest Control Forum. Environment Canada, Canadian Forest Service, Ottawa, Ontario, 337 pp. Canadian Forest Service (1978) Report of the Annual Forest Pest Control Forum. Environment Canada, Canadian Forest Service, Ottawa, Ontario, 443 pp. Cantwell, G.E., Dutky, S.R., Keller, J.C. and Thompson, C.G. (1961) Results of tests with Bacillus thuringiensis Berliner against gypsy moth larvae. Journal of Invertebrate Pathology 8, 228–233. Cardinal, J.A. (1967) Lutte contre la spongieuse Porthetria dispar L. (Lepidoptera: Lymantriidae) au Québec. Phytoprotection 48, 92–100. Carson, R.L. (1962) Silent Spring. Houghton Mifflin, Boston, Massachusetts, 368 pp. Casida, S.E. and Quistad, G.B. (1998) Golden age of insecticide research: past, present or future? Annual Review of Entomology 43, 1–16. Cayford, J.H. (1993) Sheep for vegetation management. The Forestry Chronicle 69, 27. Cole, W.E. and McGregor, M.D. (1985) Reducing and preventing mountain pine beetle outbreaks in lodgepole pine stands by selective cutting. In: Safranyik, L. (ed.) Role of the Host in the Population Dynamics of Forest Insects: Proceedings of IUFRO Conference, Banff, Alberta, September 4–7, 1983. Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 240 pp. Council of Forest Industries (2000) British Columbia Forest Industry Fact Book, Vancouver, British Columbia, 82 pp. Available at: Cunningham, J.C. (1985a) Status of viruses as biocontrol agents for spruce budworms. In: Grimble, D.G. and Lewis, F.B. (eds) Microbial Control of Spruce Budworms and Gypsy Moth. General Technical Report, GTR-NE-100, Northeastern Forestry Experimental Station, US Department of Agriculture Forest Service, Broomall, Pennsylvania, pp. 61–67. Cunningham, J.C. (1985b) Biorationals for control of spruce budworms. In: Sanders, C.J., Stark, R.W., Mullins, E.J. and Murphy, J. (eds) Recent Advances in Spruce Budworm Research: Proceedings of CANUSA Spruce Budworm Research Symposium, September 16–20, 1984, Bangor, Maine. Canadian Forestry Service, Ottawa, Ontario, pp. 320–349. Cunningham, J.C. (1998) North America. In: Hunter-Fujita, F.R., Entwistle, P.F., Evans, H.F. and Cook, N.E. (eds) Insect Viruses and Pest Management. John Wiley and Sons, Chichester, UK, pp. 313–331. Cunningham, J.C. and de Groot, P. (1984) Neodiprion lecontei (Fitch), redheaded pine sawfly (Hymenoptera: Diprionidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 323–329. Cunningham, J.C. and Howse, G.M. (1984) Viruses: application and assessment. In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 248–259. Cunningham, J.C. and Kaupp, W.J. (1995) Insect viruses. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 327–340. Cunningham, J.C. and McPhee, J.R. (1986) Production of Sawfly Viruses in Plantations. Technical Note No. 4, Canadian Forestry Service, Forest Pest Management Institute, Sault Ste Marie, Ontario, 4 pp.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 244


I.S. Otvos

Cunningham, J.C. and Shepherd, R.F. (1984) Orgyia pseudotsugata (McDunnough), Douglas-fir tussock moth (Lepidoptera: Lymantriidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes against Insects and Weeds in Canada, 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 363–367. Cunningham, J.C. and van Frankenhuyzen, K. (1991) Microbial insecticides in forestry. The Forestry Chronicle 67, 473–480. Cunningham, J.C., de Groot, P. and Kaupp, W.J. (1986) A review of aerial spray trials with Lecontvirus for control of red-headed pine sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae), in Ontario. Proceedings of the Entomological Society of Ontario 117, 65–72. Dahlsten, D.L., Garcia, R. and Lorraine, H. (1989) Eradication as a pest management tool: concepts and contexts. In: Dahlsten, D.L. and Garcia, R. (eds) Eradication of Exotic Pests: Analysis with Case Histories. Yale University Press, New Haven, Connecticut, 296 pp. D’Amico, V. and Elkinton, J.S. (1995) Rainfall effects on transmission of gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrodis virus. Environmental Entomology 24, 1144–1149. DeBoo, R.F. and Prasad, R. (1997) Pesticide use in forest management: the British Columbia experience since 1946. Pesticide Outlook 8, 9–14. Doane, C.C. (1970) Primary pathogens and their role in the development of an epizootic in the gypsy moth. Journal of Invertebrate Pathology 15, 21–33. Doane, C.C. (1976) Ecology of pathogens of the gypsy moth. In: Anderson, J.F. and Kaya, H.K. (eds) Perspectives in Forest Entomology. Academic Press, New York, pp. 285–293. Doane, C.C. and McManus, M.L. (eds) (1981) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, 757 pp. Dorworth, C. (1990) Use of indigenous microorganisms for forest weed biocontrol – the PFC enhancement process. In: Basset, C., Whitehouse, L.J. and Zabkiewicz, J.A. (eds) Alternatives to the Chemical Control of Weeds: Proceedings of an International Conference held at the Forest Research Institute, Rotorua, New Zealand, July 25–27, 1989. Forest Research Institute Bulletin 155, Forest Research Institute, Ministry of Forestry, Rotorua, New Zealand, pp. 116–119. Dorworth, C.E. (1992) Biological control of weeds using indigenous pathogens. In: Shrimpton, G. (ed.) Canadian Forest Nursery Weed Management Association: Proceedings of Annual Meeting. Victoria, British Columbia, July 6–8, 1992. BC Ministry of Forests, Victoria, British Columbia, pp. 17–24. Dowden, P.B. (1962) Parasites and Predators of Forest Insects Liberated in the United States through 1960. Agricultural Handbook 226, Forest Service, US Department of Agriculture, Washington, DC, 70 pp. Duan, L. and Otvos, I.S. (2001) Influence of larval age and virus concentration on mortality and sublethal effects of a nucleopolyhedrovirus on the western spruce budworm (Lepidoptera: Tortricidae). Environmental Entomology 30, 136–146. Dubois, N.R. (1981) Bacillus thuringiensis. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 445–453. Duke, S.O. (1986) Naturally occurring chemical compounds as herbicides. Reviews of Weed Science 2, 15–44. Duke, S.O. and Lydon, J. (1987) Herbicides from natural compounds. Weed Technology 1, 122–128. Dulmage, H.T. (1982) Distribution of Bacillus thuringiensis in nature. In: Kurstak, E. (ed.) Microbial and Viral Pesticides. Marcel Dekker, New York, pp. 209–237. Dunlap, T.R. (1980) The gypsy moth: a study in science and public policy. Journal of Forest History 24, 116–126. Elkinton, J.S. and Liebhold, A.M. (1990) Population dynamics of gypsy moth in North America. Annual Review of Entomology 35, 571–596. Elkinton, J.S., Hajek, A.E., Boettner, G.H. and Simons, E.E. (1991) Distribution and apparent spread of Entomophaga maimaiga (Zygomycetes: Entomophthorales) in gypsy moth (Lepidoptera: Lymantriidae) populations in North America. Environmental Entomolgy 20, 1601–1605. Embree, D.G. (1971) The biological control of the winter moth in eastern Canada by introduced parasites. In: Huffaker, C.B. (ed.) Biological Control. Plenum, New York, pp. 217–226. FAO (Food and Agriculture Organization of the United Nations) (2002) FAO Statistics. Available at: Feller, M. (1996) Use of prescribed fire for vegetation management. In: Comeau, P.G., Harper, G.J., Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation Management: Options and Applications. Proceedings of the Fifth British Columbia Forest Vegetation Management Workshop, November

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 245

IPM in Forestry


29–30, 1993, Richmond, British Columbia. Forest Resource Development Agreement Report No. 251, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, pp. 17–34. Fleming, R. and Retnakaran, A. (1985) Evaluating single treatment data using Abbott’s formula with reference to insecticides. Journal of Economic Entomology 78, 1179–1181. van Frankenhuyzen, K. (1990) Development and current status of Bacillus thuringiensis for control of defoliating forest insects. The Forestry Chronicle 66, 498–507. van Frankenhuyzen, K. (1993) The challenge of Bacillus thuringiensis. In: Entwistle, P.F., Cory, J.S., Bailey, M.J. and Higgs, S. (eds) Bacillus thuringiensis, an Environmental Pesticide: Theory and Practice. J. Wiley & Sons, New York, pp. 1–35. van Frankenhuyzen, K. (1995) Development and current status of Bacillus thuringiensis for control of defoliating forest insects. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 315–325. van Frankenhuyzen, K. (2000) Application of Bacillus thuringiensis in forestry. In: Charles, J.F., Delecluse, A. and Nielsen-LeRoux, C. (eds) Entomopathogenic Bacteria: From Laboratory to Field Application. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 355–370. Glaser, R.W. (1915) Wilt of gypsy-moth caterpillars. Journal of Agricultural Research 4, 101–128. Griffiths, K.J. (1976) The Parasites and Predators of the Gypsy Moth: a Review of the World Literature with Special Application to Canada. Information Report O-X-243, Canadian Forestry Service, Great Lakes Forest Research Centre, Sault Ste Marie, Ontario, 92 pp. Griffiths, K.J. and Quednau, F.W. (1984) Lymantria dispar (L.), gypsy moth (Lepidoptera: Lymantriidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 303–310. Hajek, A.E. (1997) Fungal and viral epizootics in gypsy moth (Lepidoptera: Lymantriidae) populations in central New York. Biological Control 10, 58–68. Hajek, A.E. and Roberts, E.W. (1991) Pathogen reservoirs as a biological control resource: introduction of Entomophaga maimaiga to North American gypsy moth, Lymantria dispar, populations. Biological Control 1, 29–34. Hajek, A.E. and Roberts, E.W. (1992) Field diagnosis of gypsy moth (Lepidoptera: Lymantriidae) larval mortality caused by Entomophaga maimaiga and the gypsy moth nuclear polyhedrosis virus. Environmental Entomology 21, 706–713. Hajek, A.E. and Soper, R.S. (1992) Temporal dynamics of Entomophaga maimaiga after death of gypsy moth (Lepidoptera: Lymantriidae) larval hosts. Environmental Entomology 21, 129–135. Hajek, A.E., Humber, R.A., Elkinton, J.S., May, B., Walsh, S.R.A. and Silver, J.C. (1990a) Allozyme and RFLP analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. Proceedings of the National Academy of Sciences of the USA 87, 6979–6982. Hajek, A.E., Carruthers, R.I. and Soper, R.S. (1990b) Temperature and moisture relations of sporulation and germination by Entomophaga maimaiga (Zygomycetes: Entomophthoraceae), a fungal pathogen of Lymantria dispar (Lepidoptera: Lymantriidae). Environmental Entomology 19, 85–90. Hajek, A.E., Larkin, T.S., Carruthers, R.I. and Soper, R.S. (1993) Modeling the dynamics of Entomophaga maimaiga (Zygomycetes: Entomophthorales) epizootics in gypsy moth (Lepidoptera: Lymantriidae) populations. Environmental Entomology 22, 1172–1187. Hajek, A.E., Humber, R.A. and Elkinton, J.S. (1995) Mysterious origin of Entomophaga maimaiga in North America. American Entomologist 41, 31–42. Hajek, A.E., Elkinton, J.S. and Witcosky, J.J. (1996) Introduction and spread of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) along the leading edge of gypsy moth (Lepidoptera: Lymantriidae) spread. Environmental Entomology 25, 1235–1247. Hall, P.J. (comp.) (1994) Forest Insect and Disease Conditions in Canada 1992. Forest Insect and Disease Survey, Forestry Canada, Ottawa, Ontario, 120 pp. Hall, P.J. (comp.) (1995) Forest Insect and Disease Conditions in Canada 1993. Forest Insect and Disease Survey, Forestry Canada, Ottawa, Ontario, 133 pp. Hall, P.J. (comp.) (1996) Forest Insect and Disease Conditions in Canada 1994. Forest Insect and Disease Survey, Forestry Canada, Ottawa, Ontario, 112 pp. Halleran, M. (1990) Forest vegetation management and the politics of environment. The Forestry Chronicle 66, 369–371.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 246


I.S. Otvos

Hamel, D.R. (1977) The effects of Bacillus thuringiensis on parasitoids of the western spruce budworm, Choristoneura occidentalis (Lepidoptera: Tortricidae), and the spruce coneworm, Dioryctria reniculelloides (Lepidoptera: Pyralidae), in Montana. The Canadian Entomologist 109, 1409–1415. Hansen, E.M. and Lewis, K.J. (eds) (1997) Compendium of Conifer Diseases. American Phytopathological Society Press, St Paul, Minnesota, 101 pp. Harris, J.W.E., Alfaro, R.I., Dawson, A.F. and Brown, R.G. (1985a) The Western Spruce Budworm in British Columbia 1909–1983. Information Report BC-X-257, Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 32 pp. Harris, P. (1984) Current approaches to biological control of weeds. In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 95–103. Harris, P. and Shamoun, S.F. (2002) Biological control of weeds in Canada: results, opportunities, and constraints. In: Claudia, R., Nantel, P. and Muckle-Jeffs, E. (eds) Alien Invaders in Canada’s Waters, Wetlands, and Forests. Canadian Forest Service, Natural Resources Canada, Ottawa, Ontario, pp. 291–302. Hewitt, G.C. (1916) The introduction and establishment in Canada of the natural enemies of the browntail and gypsy moth. The Agricultural Gazette of Canada 3, 20–21. Hoy, M.A. (1976) Establishment of gypsy moth parasitoids in North America: an evaluation of possible reasons for establishment or non-establishment. In: Anderson, J.F. and Kaya, H.K. (eds) Perspectives in Forest Entomology. Academic Press, New York, pp. 215–232. Hughes, K.M. and Addison, R.B. (1970) Two nuclear polyhedrosis viruses of the Douglas-fir tussock moth. Journal of Invertebrate Pathology 16, 196–204. Hulme, M.A. (1988) The recent Canadian record in applied biological control of forest insect pests. The Forestry Chronicle 64, 27–31. Humble, L. and Stewart, A.J. (1994) Gypsy Moth. Forest Pest Leaflet 75, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, 8pp. Humphreys, P. (1986) Pesticide Use in British Columbia Forestry 1985. Forest Service Internal Report PM–PB–26, British Columbia Ministry of Forests and Lands, Victoria, British Columbia, 31 pp. Humphreys, P. (1990) Pesticide Use in British Columbia Forestry 1989. Forest Service Internal Report PM–PB–46, British Columbia Ministry of Forests, Victoria, British Columbia, 73 pp. Ilnytzky, S., McPhee, J.R. and Cunningham, J.C. (1977) Comparison of field-propagated nuclear polyhedrosis virus from Douglas-fir tussock moth with laboratory virus. Fisheries and Environment Canada, Forestry Service, Bi-monthly Research Notes 33, 5–6. Ives, W.G.H. and Rentz, C.L. (1993) Factors Affecting the Survival of Immature Lodgepole Pine in the Foothills of West-Central Alberta. Information Report NOR-X-330, Canadian Forest Service, Northwest Region, Northern Forestry Centre, Edmonton, Alberta, 49 pp. Jobidon, R. (1991a) Some future directions for biologically based vegetation control in forestry. The Forestry Chronicle 67, 514–519. Jobidon, R. (1991b) Potential use of bialaphos, a microbially produced phytotoxin, to control red raspberry in forest plantations and its effect on black spruce. Canadian Journal of Forest Research 21, 489–497. Jobidon, R., Thibault, J.R. and Fortin, J.A. (1989) Phytotoxic effect of barley oat and wheat-straw mulches in eastern Quebec forest plantations 1. Effects on red raspberry (Rubus idaeus). Forest Ecology and Management 29, 277–294. Jobin, L. (1995) Gypsy moth, Lymantria dispar. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 133–139. Julien, M.H. and Griffiths, M.W. (1998) Biological Control of Weeds: a World Catalogue of Agents and their Target Weeds. CAB International, Wallingford, UK, 223 pp. Keena, M.A., Grinberg, P.S. and Wallner, W.E. (1995) Asian gypsy moth genetics: biological consequences of hybridization [abstract]. In: Fosbroke, S.L.C. and Gottschalk, K.W. (eds) Proceedings: U.S. Department of Agriculture Interagency Gypsy Moth Research Forum 1995, January 17–20, 1995, Loews Annapolis Hotel, Annapolis, Maryland. General Technical Report NE-213, USDA Forest Service, Northeastern Forest Experiment Station, Radnor, Pennsylvania, p. 80. Kelleher, J.S. and Hulme, M.A. (eds) (1984) Biological Control Programmes Against Weeds and Insects in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, 410 pp. Kettela, E.G. (1983) A Cartographic History of Spruce Budworm Defoliation from 1967 to 1981 in Eastern North America. Information Report DPC-X-14, Canadian Forestry Service, Maritimes Research Centre, Fredericton, New Brunswick, 8 pp.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 247

IPM in Forestry


Kettela, E.G. (1995) Attempts to develop strategies to control spruce budworm, Choristoneura fumiferana, moth populations by spraying. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 113–117. Kinghorn, J.M., Fisher, R.A., Angus, T.A. and Heimpel, A.M. (1961) Aerial spray trials against the blackheaded budworm in British Columbia. Department of Forestry, Forest Entomology and Pathology Branch, Bi-monthly Progress Report 17, 3–4. Leonard, D.E. (1981) Bioecology of the gypsy moth. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 9–29. Leonard, D.S. and Sharov, A.A. (1995) Slow the spread project update: developing a process for evaluation. In: Fosbroke, S.L.C. and Gottschalk, K.W. (eds) Proceedings: US Department of Agriculture Interagency Gypsy Moth Research Forum 1995, January 17–20, 1995, Annapolis, Maryland. General Technical Report NE-213, Northeastern Forest Experiment Station, USDA Forest Service, Radnor, Pennsylvania, pp. 82–85. Leonhardt, B.A., Mastro, V.C., Leonard, D.S., McLane, W., Reardon, R.C. and Thorpe, K.W. (1996) Control of low-density gypsy moth (Lepidoptera: Lymantriidae) populations by mating disruption with pheromone. Journal of Chemical Ecology 22, 1255–1272. Leuschner, W.A., Young, J.A., Waldon, S.A. and Ravlin, F.W. (1996) Potential benefits of slowing the gypsy moth’s spread. Southern Journal of Applied Forestry 20, 65–73. Lewis, F.B. (1981) Registration and cost effectiveness. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 514–515. Liebhold, A. and McManus, M. (1999) The evolving use of insecticides in gypsy moth management. Journal of Forestry 97, 20–23. Liebhold, A., Mastro, V. and Schaefer, P.W. (1989) Learning from the legacy of Léopold Trouvelot. Bulletin of the Entomological Society of America 35, 20–22. Liebhold, A.M., Halverson, J.A. and Elmes, G.A. (1992) Gypsy moth invasion in North America: a quantitative analysis. Journal of Biogeography 19, 513–520. Liebhold, A.M., MacDonald, W.L., Bergdahl, D. and Mastro, V.C. (1995) Invasion by Exotic Forest Pests: a Threat to Forest Ecosystems. Forest Science Monograph 30, Society of American Foresters, Bethesda, Maryland, 49 pp. Liebhold, A.M., Gottschalk, K.W., Mason, D.A. and Bush, R.R. (1997) Forest susceptibility to the gypsy moth. Journal of Forestry 95, 20–24. Logie, R.R. (1975) Effects of aerial spraying of DDT on salmon populations of the Miramichi River. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of the Environment, Ottawa, Canada, pp. 293–300. Lowe, J.J., Power, K. and Gray, S.L. (1996) Canada’s Forest Inventory 1991: the 1994 Version. An Addendum to Canada’s Forest Inventory 1991. Information Report BC-X-362E, Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, Victoria, British Columbia, 23 pp. Maclauchlan, L.E. and Brooks, J.E. (eds) (1994) Strategies and Tactics for Managing the Mountain Pine Beetle, Dendroctonus ponderosae. British Columbia Forest Service, Kamloops Region, Forest Health, Kamloops, British Columbia, 60 pp. MacLean, D.A. (1980) Vulnerability of fir-spruce stands during uncontrolled spruce budworm outbreaks: a review and discussion. The Forestry Chronicle 56, 213–222. Malakar, R., Elkinton, J.S., Hajek, A.E. and Burand J.P. (1999) Within-host interactions of Lymantria dispar (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus and Entomophaga maimaiga (Zygomycetes: Entomophthorales). Journal of Invertebrate Pathology 73, 91–100. Mallet, K.I., Macey, D.E. and Winder, R.S. (2002) Calamagrostis canadensis (Michaux) Palisot de Beauvois, Marsh Reed Grass (Poaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 298–301. Marsden, J.S., Martin, G.E., Parham, D.J., Ridsill-Smith, T.J. and Johnston, B.G. (1980) Returns on Australian Agricultural Research: Joint IAC-CSIRO Benefit Cost Study of the CSIRO Division of Entomology. Commonwealth Scientific and Industrial Research Organization, Canberra, Australia, 107 pp. Martin, P.A.W. and Travers, R.S. (1989) Worldwide abundance and distribution of Bacillus thuringiensis isolates. Applied and Environmental Microbiology 55, 2437–2442.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 248


I.S. Otvos

Mason, C.J. and McManus, M.L. (1981) Larval dispersal of the gypsy moth. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 161–202. Mason, P.G. and Huber, J.T. (eds) (2002) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, 583 pp. Mason, P.G., Huber, J.T. and Boyetchko, S.M. (2002) Introduction. In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. xi–xiv. Mattson, W.J., Niemela, P., Millers, I. and Inguanzo, Y. (1994) Immigrant Phytophagous Insects on Woody Plants in the United States and Canada: An Annotated List. General Technical Report NC-169, Forest Service, US Department of Agriculture, North Central Forest Experiment Station, St Paul, Minnesota, 27 pp. McDonald, G.I., Martin, N.E. and Harvey, A.E. (1987) Armillaria in the Northern Rockies: Pathogenicity and Host Susceptibility on Pristine and Disturbed Sites. Research Note INT-371, Forest Service, US Department of Agriculture, Intermountain Research Station, Ogden, Utah, 3 pp. McDonald, P.M. and Fiddler, G.O. (1996) Mulching: a persistent technique for weed suppression. In: Comeau, P.G., Harper, G.J., Blache, M.E., Boateng, J.O. and Gilkeson, L.A. (eds) Integrated Forest Vegetation Management: Options and Applications: Proceedings of the Fifth British Columbia Forest Vegetation Management Workshop, November 29–30, 1993, Richmond, British Columbia. Forest Resource Development Agreement Report No. 251, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, pp. 51–58. McFadden, M.W. and McManus, M.E. (1991) An insect out of control? The potential for spread and establishment of the gypsy moth in new forest areas in the United States. In: Baranchikov, Y.N., Mattson, W.J., Hain, F.P. and Payne, T.L. (eds) Forest Insect Guilds: Patterns of Interaction with Host Trees: Proceedings of a Joint IUFRO Working Party Symposium, Abakan, Siberia, USSR, August 13–17, 1989. General Technical Report NE-153, Forest Service, US Department of Agriculture, Northeastern Forest Experiment Station, Radnor, Pennsylvania, pp. 172–186. McGugan, B.M. and Coppel, H.C. (1962) Part II: Biological control of forest insects, 1910–1958. In: McLeod, J.H., McGugan, B.M. and Coppel, H.C. (compilers) A Review of the Biological Control Attempts Against Insects and Weeds in Canada. Commonwealth Agricultural Bureaux, Slough, UK, pp. 35–127. McLeod, J.H. (1962) Part I: Biological control of pests of crops, fruit trees, ornamentals, and weeds in Canada up to 1959. In: McLeod, J.H., McGugan, B.M. and Coppel, H.C. (compilers) A Review of the Biological Control Attempts Against Insects and Weeds in Canada. Commonwealth Agricultural Bureaux, Slough, UK, pp. 1–33. McManus, M.L. and McIntyre, T. (1981) Introduction: historical chronology. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 1–7. McMullen, L.H., Safranyik, L. and Linton, D.A. (1986) Suppression of Mountain Pine Beetle Infestations in Lodgepole Pine Forests. Information Report BC-X-276, Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 20 pp. Miller, C.A. (1957) A technique for estimating the fecundity of natural populations of the spruce budworm. Canadian Journal of Zoology 35, 1–13. Miller, C.A., Kettela, E.G. and McDougall, G.A. (1971) A Sampling Technique for Overwintering Spruce Budworm and its Applicability to Population Surveys. Information Report M-X-25, Department of Fisheries and Forestry, Canadian Forest Service, Maritimes Forest Research Centre, Fredericton, New Brunswick, 11 pp. Miller, J.C. (1990) Field assessment of the effects of a microbial pest control agent on nontarget Lepidoptera. American Entomologist 36, 135–139. Miller, J.D. and Lindsay, B.E. (1993) Willingness to pay for a state gypsy moth control program in New Hampshire: a contingent valuation case study. Journal of Economic Entomology 86, 828–837. Mills, N.J. and Nealis, V.G. (1992) European field collections and Canadian releases of Ceranthia samarensis (Dipt.: Tachinidae), a parasitoid of the gypsy moth. Entomophaga 37, 181–191. Mitchell, R.G., Waring, R.H. and Pitman, G.B. (1983) Thinning lodgepole pine increases tree vigor and resistance to mountain pine beetle. Forest Science 29, 204–211. Montgomery, M.E. and Wallner, W.E. (1988) The gypsy moth: a westward migrant. In: Berryman, A.A. (ed.) Dynamics of Forest Insect Populations: Patterns, Causes, Implications. Plenum Press, New York, pp. 253–275.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 249

IPM in Forestry


Moody, B.H. (comp.) (1993a) Forest Insect and Disease Conditions in Canada 1991. Forest Insect and Disease Survey, Forestry Canada, Ottawa, Ontario, 99 pp. Moody, B.H. (comp.) (1993b) Forest Insect and Disease Conditions in Canada 1990. Forest Insect and Disease Survey, Forestry Canada, Ottawa, Ontario, 115 pp. Morris, M.J. (1991) The use of plant pathogens for biological weed control in South Africa. Agriculture, Ecosystems and Environment 37, 239–255. Morris, M.J. (1997) Impact of the gall-forming rust fungus, Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa. Biological Control 10, 75–82. Morris, M.J., Wood, A.R. and den Breeyen, A. (1998) Development and registration of a fungal inoculant to prevent re-growth of cut wattle tree stumps in South Africa. In: Burge, M.N. (ed.) IV International Bioherbicides Workshops – Programmes and Abstracts, 6–7 August, 1998. University of Strathclyde, Glasgow, p. 15. Morris, O.N. (1963) The natural and artificial control of the Douglas-fir tussock moth, Orgyia pseudotsugata McDunnough, by a nuclear-polyhedrosis virus. Journal of Insect Pathology 5, 401–414. Morris, O.N. (1983) Comparative efficacy of Thuricide 16B and Dipel 88 against the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae) in balsam fir stands. The Canadian Entomologist 115, 1001–1006. Morris, R.F. (1954) A sequential sampling technique for spruce budworm egg surveys. Canadian Journal of Zoology 32, 302–313. Morris, R.F. (ed.) (1963) The Dynamics of Epidemic Spruce Budworm Populations. Memoirs of the Entomological Society of Canada 31, Ottawa, Ontario, Canada, 332pp. Morrison, D. and Mallett, K. (1996) Silvicultural management of armillaria root disease in western Canadian forests. Canadian Journal of Plant Pathology 18, 194–199. Morrison, D.J., Merler, H. and Norris, D. (1992) Detection, Recognition and Management of Armillaria and Phellinus Root Diseases in the Southern Interior of British Columbia. Forest Resource Development Agreement Report 179, Canadian Forest Service and British Columbia Ministry of Forests, Victoria, British Columbia, 25 pp. Morrison, D.J., Wallis, G.W. and Weir, L.C. (1988) Control of Armillaria and Phellinus Root Diseases: 20-year Results from the Skimikin Stump Removal Experiment. Information Report BC-X-302, Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 16 pp. Mott, D.G., Angus, T.A., Heimpel, A.M. and Fisher, R.A. (1961) Aerial spraying of Thuricide against the spruce budworm in New Brunswick. Department of Forestry, Forest Entomology and Pathology Branch, Bi-monthly Progress Report 17, 2. Nealis, V.G. (2002) Gypsy moth in Canada: case study of an invasive insect. In: Claudia, R., Nantel, P. and Muckle-Jeffs, E. (eds) Alien Invaders in Canada’s Waters, Wetlands and Forests. Natural Resources Canada, Science Branch, Canadian Forest Service, Ottawa, Ontario, pp. 151–159. Nealis, V.G. and Quednau, F.W. (1996) Canadian field releases and overwinter survival of Ceranthia samarensis (Villeneuve) (Diptera: Tachinidae) for biological control of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae). Proceedings of the Entomological Society of Ontario 127, 11–20. Nealis, V.G. and van Frankenhuyzen, K. (1990) Interactions between Bacillus thuringiensis Berliner and Apanteles fumiferanae Vier. (Hymenoptera: Braconidae), a parasitoid of the spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). The Canadian Entomologist 122, 585–594. Nealis, V.G., Roden, P.M. and Ortiz, D.A. (1999) Natural mortality of the gypsy moth along a gradient of infestation. The Canadian Entomologist 131, 507–519. Nealis, V.G., Carter, N., Kenis, M., Quednau, F.W. and van Frankenhuyzen, K. (2002) Lymantria dispar (L.), gypsy moth (Lepidoptera: Lymantriidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 159–168. Niemela, P. and Mattson, W.J. (1996) Invasion of North American forests by European phytophagous insects – legacy of the European crucible? BioScience 46, 741–753. Nigam, P.C. (1975) Chemical insecticides. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of the Environment, Ottawa, Canada, pp. 8–24. Nigam, P.C. (1980) Use of chemical insecticides against the spruce budworm in eastern Canada. CANUSA Newsletter 11, 1–3. Niwa, C.G., Stelzer, M.J. and Beckwith, R.C. (1987) Effects of Bacillus thuringiensis on parasites of western spruce budworm (Lepidoptera: Tortricidae). Journal of Economic Entomology 80, 750–753. Oleskevich, C., Shamoun, S.F., Vesonder, R.F. and Punja, Z.K. (1998) Evaluation of Fusarium avenaceum and other fungi for potential as biological control agents of invasive Rubus species in British Columbia. Canadian Journal of Plant Pathology 20, 12–18. Otvos, I.S. (1973) Biological Control Agents and Their Role in the Population Fluctuation of the Eastern Hemlock Looper

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 250


I.S. Otvos

in Newfoundland. Information Report N-X-102, Environment Canada, Newfoundland Forest Research Centre, St John’s, Newfoundland, 34 pp. Otvos, I.S. and Raske, A.G. (1980a) The Effects of Fenitrothion, Matacil, and Bacillus thuringiensis plus Orthene on Larval Parasites of the Spruce Budworm. Information Report N-X-184, Canadian Forestry Service, Newfoundland Forest Research Centre, St John’s, Newfoundland, 24 pp. Otvos, I.S. and Raske, A.G. (1980b) Effects of Aerial Application of Matacil on Larval and Pupal Parasites of the Eastern Spruce Budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Information Report NX-189, Canadian Forest Service, Newfoundland Forest Research Centre, St John’s, Newfoundland, 12 pp. Otvos, I.S. and Vanderveen, S. (1993) Environmental Report and Current Status of Bacillus thuringiensis var. kurstaki Use for Control of Forest and Agricultural Insect Pests. Joint report by Forestry Canada, Pacific Forestry Centre and British Columbia Ministry of Forests, Victoria, British Columbia, 81 pp. Otvos, I.S., MacLeod, D.M. and Tyrrell, D. (1973) Two species of Entomophthora pathogenic to the eastern hemlock looper (Lepidoptera: Geometridae) in Newfoundland. Canadian Entomologist 105, 1435–1441. Otvos, I.S., Cunningham, J.C. and Friskie, L.M. (1987) Aerial application of nuclear polyhedrosis virus against Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) (Lepidoptera: Lymantriidae): I. Impact in the year of application. The Canadian Entomologist 119, 697–706. Otvos, I.S., Cunningham, J.C. and Kaupp, W.J. (1989) Aerial application of two baculoviruses against the western spruce budworm (Lepidoptera: Tortricidae) in British Columbia. The Canadian Entomologist 121, 209–217. Otvos, I.S., Cunningham, J.C. and Shepherd, R.F. (1995) Douglas-fir tussock moth, Orgyia pseudotsugata. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 127–132. Pearce, P.A. (1975) Effects on birds. In: Prebble, M.L. (ed.) Aerial Control of Forest Insects in Canada. Department of the Environment, Ottawa, Canada, pp. 306–313. Pendl, F. and D’Anjou, B. (1990) Effect of Manual Treatment Timing on Red Alder Regrowth and Conifer Response. Forest Resource Development Agreement Report 112, Canadian Forestry Service and British Columbia Ministry of Environment, Victoria, British Columbia, 21 pp. Perlman, F.D., Press, E., Googins, J.A., Malley, A. and Poarea, H. (1976) Tussockosis: reactions to Douglasfir tussock moth. Annals of Allergy 36, 302–307. Podgwaite, J.D. (1999) Gypchek: biological insecticide for the gypsy moth. Journal of Forestry 97, 16–19. Podgwaite, J.D. and Campbell, R.W. (1972) The disease complex of the gypsy moth. II. Aerobic bacterial pathogens. Journal of Invertebrate Pathology 20, 303–308. Prasad, R. (1992) Some aspects of biological control of weeds in forestry. In: Richardson, R.G. (compiler) Proceedings of the First International Weed Control Congress, February 17–21, 1992, Monash University, Melbourne, Australia, Vol. 2. Weed Science Society of Victoria Inc., Melbourne, Australia, pp. 398–402. Prasad, R. (1996) Development of bioherbicides for integrated weed management in forestry. In: Brown, H. (ed.) Proceedings, Second International Weed Control Congress, Copenhagen, Denmark, June 25–28 1996. Department of Weed Control and Pesticide Ecology, Slagelse, Denmark, pp. 1197–1203. Prasad, R. (2002a) Cytisus scoparius (L.) Link, Scotch Broom (Fabaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 343–345. Prasad, R. (2002b) Ulex europaeus L., Gorse (Fabaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 431–433. Prasher, D. and Mastro, V.C. (1995) Genotype analyses of 1994 port specimens. In: Hilburn, D., Johnson, K.J.R. and Mudge, A.D. (eds) Proceedings of the 1994 Annual Gypsy Moth Review: Held at the Portland Hilton, Portland, Oregon, October 30-November 2, 1994. US National Gypsy Moth Management Board, Salem, Massachusetts, pp. 61–63. Prebble, M.L. (ed.) (1975) Aerial Control of Forest Insects in Canada. Environment Canada, Ottawa, Ontario, 330 pp. Ravensberg, W.J. (1998) BioChon: Effective Biological and Environmentally Friendly Product. Pest Leaflet, Koppert Biological Systems, The Netherlands, 2 pp. Reardon, R.C. (1981) Summary. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 412–413.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 251

IPM in Forestry


Reardon, R.C. (1991) Appalachian gypsy-moth integrated pest-management project. Forest Ecology and Management 39, 107–112. Reardon, R. and Hajek, A. (1993) Entomophaga maimaiga in North America: a Review. AIPM Technology Transfer, US Department of Agriculture Forest Service, Northeastern Area, Morgantown, West Virginia, 22 pp. Reardon, R.C., Johnson, D.R., Narog, M.G., Banash, S.E. and Hubbard, H.B. Jr (1982) Efficacy of two formulations of Bacillus thuringiensis on populations of spruce budworm (Lepidoptera: Tortricidae) on balsam fir in Wisconsin. Journal of Economic Entomology 75, 509–514. Reardon, R., McManus, M., Kolodny-Hirsch, D., Tichenor, R., Raupp, M., Schwalbe, C., Webb, R. and Meckley, P. (1987) Development and implementation of a gypsy moth integrated pest management program. Journal of Arboriculture 13, 209–216. Reardon, R.C., Dubois, N.R. and McLane, W. (1994) Bacillus thuringiensis for Managing Gypsy Moth: a Review. FHM-NC-01–94, National Centre of Forest Health Management, US Department of Agriculture Forest Service, Morgantown, West Virginia, 32 pp. Reardon, R.C., Leonard, D.S., Mastro, V.C., Leonhardt, B.A., McLane, W., Talley, S., Thorpe, K.W. and Webb, R.E. (1998) Using Mating Disruption to Manage Gypsy Moth: A Review. USDA Forest Service, Morgantown, West Virginia, 85 pp. Reeks, W.A. and Cameron, J.M. (1971) Current approach to biological control of forest insects. In: Canadian Department of Agriculture and Canadian Department of Fisheries and Forestry (ed.) Biological Control Programmes Against Insects and Weeds in Canada 1959–1968. Technical Communication No. 4, Commonwealth Institute of Biological Control, Commonwealth Agricultural Bureaux, Slough, UK, pp. 105–113. Regniere, S. and Lysyk, T.J. (1995) Population dynamics of the spruce budworm, Choristoneura fumiferana. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 95–105. Russell, K., Johnsey, R. and Edmonds, R. (1986) Disease and insect management for Douglas-fir. In: Oliver, C.D., Hanley, D.P. and Johnson, J.A. (eds) Douglas-fir: Stand Management for the Future. Contribution No. 55, College of Forest Resources, Institute of Forest Resources, University of Washington, Seattle, Washington, pp. 189–207. Sabrosky, C.W. and Reardon, R.C. (1976) Tachinid Parasites of the Gypsy Moth, Lymantria dispar, with Keys to Adults and Puparia. Miscellaneous Publications of the Entomological Society of America 10, Lanham, Maryland, 126 pp. Safranyik, L., Shrimpton, D.M. and Whitney, H.S. (1974) Management of Lodgepole Pine to Reduce Losses from the Mountain Pine Beetle. Forestry Technical Report 1, Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 24 pp. Safranyik, L., Simmons, C. and Barclay, H.J. (1990) A Conceptual Model of Spruce Beetle Population Dynamics. Information Report BC-X-316, Forestry Canada, Pacific Forestry Centre, Victoria, British Columbia, 13 pp. Sanders, C.J. (1988) Monitoring spruce budworm population density with sex pheromone traps. Canadian Entomologist 120, 175–183. Sanders, C.J., Stark, R.W., Mullins, E.J. and Murphy, J. (eds) (1985) Recent Advances in Spruce Budworms Research: Proceedings of CANUSA Spruce Budworms Research Symposium, Bangor, Maine, September 16–20, 1984. Canadian Forestry Service, Ottawa, Ontario, 527 pp. Sartwell, C. and Dolph, R.E. Jr (1976) Silvicultural and Direct Control of Mountain Pine Beetle in SecondGrowth Ponderosa Pine. Research Note PNW-268, US Department of Agriculture Forest Service, Pacific Northwest Forest and Range Experiment Station, Portland, Oregon, 8 pp. Scheepens, P.C. and Hoogerbrugge, A. (1989) Control of Prunus serotina in forests with the endemic fungus Chondrostereum purpureum. In: Delfosse, E.S. (ed.) Proceedings, VII International Symposium on Biological Control of Weeds, March 6–11, 1988, Rome, Italy. Commonwealth Scientific and Industrial Research Organization Publications, East Melbourne, Australia, pp. 545–551. Schwalbe, C.P. (1981) Disparlure-baited traps for survey and detection. In: Doane, C.C. and McManus, M.L. (eds) The Gypsy Moth: Research Toward Integrated Pest Management. Technical Bulletin 1584, Forest Service, US Department of Agriculture, Washington, DC, pp. 542–548. Shamoun, S.F. (2000) Application of biological control to vegetation management in forestry. In: Spence, N.R. (ed.) Proceedings of the X International Symposium on Biological Control of Weeds, 4–14 July 1999. Montana State University, Bozeman, Montana, pp. 87–96. Shamoun, S.F. and DeWald, L.E. (2002) Management strategies for dwarf mistletoes: biological, chemical,

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 252


I.S. Otvos

and genetic approaches. In: Geils, B.W., Tovar, J.C. and Moody, B. (technical coordinators) Mistletoes of North American Conifers. US Department of Agriculture Forest Service General Technical Report RMRS-GTR-98, US Department of Agriculture, Rocky Mountain Research Station, Fort Collins, Colorado, pp. 75–82. Shamoun, S.F. and Hintz, W.E. (1998a) Development and registration of Chondrostereum purpureum as a mycoherbicide for hardwood weeds in conifer reforestation sites and utility rights-of-way. In: Burge, M.N. (ed.) IV International Bioherbicide Workshop – Programme and Abstracts, 6–7 August, 1998. University of Strathclyde, Glasgow, p. 14. Shamoun, S.F. and Hintz, W.E. (1998b) Development of Chondrostereum purpureum as a biological control agent for red alder in utility rights-of-way. In: Wagner, R.G. and Thompson D.G. (compilers) Third International Conference on Forest Vegetation Management, Popular Summaries. Forest Research Information Paper No. 141, Ontario Ministry of Natural Resources, Ontario Forest Research Institute, pp. 308–310. Shamoun, S.R., Macey, D.E., Prasad, R. and Winder, R.S. (2002) Acer, Alnus, Betula, Populus and Prunus spp., weedy hardwood trees (Aceraceae, Betulaceae, Salicaceae, Rosaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 283–289. Sharov, A.A. and Liebhold, A.M. (1998a) Bioeconomics of managing the spread of exotic pest species with barrier zones. Ecological Applications 8, 833–845. Sharov, A.A. and Liebhold, A.M. (1998b) Model of slowing the spread of gypsy moth (Lepidoptera: Lymantriidae) with a barrier zone. Ecological Applications 8, 1170–1179. Sharov, A.A. and Liebhold, A.M. (1998c) Quantitative analysis of gypsy moth spread in the Central Appalachians. In: Baumgartner, J., Brandmayr, P. and Manly, B.F.J. (eds) Population and Community Ecology for Insect Management and Conservation: Proceedings of the Ecology and Population Dynamics Section of the 20th International Congress of Entomology, Florence, Italy, 25–31 August, 1996. A.A. Balkema, Rotterdam, pp. 99–110. Sharov, A.A., Liebhold, A.M. and Roberts, E.A. (1998) Optimizing the use of barrier zones to slow the spread of gypsy moth (Lepidoptera: Lymantriidae) in North America. Journal of Economic Entomology 91, 165–174. Sharov, A.A., Leonard, D., Liebhold, A.M., Roberts, E.A. and Dickerson, W. (2002a) ‘Slow the Spread’: a national program to contain the gypsy moth. Journal of Forestry 100, 30–36. Sharov, A.A., Leonard, D., Liebhold, A.M. and Clemens, N.S. (2002b) Evaluation of preventative treatments in low-density gypsy moth populations using pheromone traps. Journal of Economic Entomology 95, 1205–1215. Sharrow, S.H., Leininger, W.C. and Rhodes, B. (1989) Sheep grazing as silvicultural tool to suppress brush. Journal of Range Management 42, 2–4. Shaw, C.G. III and Calderon, S. (1977) Impact of Armillaria root rot in plantations of Pinus radiata established on sites converted from indigenous forest. New Zealand Journal of Forest Science 7, 359–373. Shepherd, R.F. and Otvos, I.S. (1986) Pest Management of Douglas-fir Tussock Moth: Procedures for Insect Monitoring, Problem Evaluation and Control Actions. Information Report BC-X-270, Canadian Forestry Service, Pacific Forestry Centre, Victoria, British Columbia, 14 pp. Shepherd, R.F., Otvos, I.S. and Chorney, R.J. (1984a) Pest management of the Douglas-fir tussock moth (Lepidoptera: Lymantriidae): a sequential sampling method to determine egg mass density. The Canadian Entomologist 116, 1041–1049. Shepherd, R.F., Otvos, I.S., Chorney, R.J. and Cunningham, J.C. (1984b) Pest management of the Douglasfir tussock moth (Lepidoptera: Lymantriidae): prevention of a Douglas-fir tussock moth outbreak through early treatment with a nuclear polyhedrosis virus by ground and aerial applications. The Canadian Entomologist 116, 1533–1542. Shepherd, R.F., Gray, T.G., Chorney, R.J. and Daterman, G.E. (1985) Pest management of the Douglas-fir tussock moth: monitoring endemic populations with pheromone traps to detect incipient outbreaks. The Canadian Entomologist 117, 839–848. Shepherd, R.F., Cunningham, J.C. and Otvos, I.S. (1995) Western spruce budworm, Choristoneura occidentalis. In: Armstrong, J.A. and Ives, W.G.H. (eds) Forest Insect Pests in Canada. Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario, pp. 119–121. Shore, T.L. and Safranyik, L. (1992) Susceptibility and Risk Rating Systems for the Mountain Pine Beetle in Lodgepole Pine Stands. Information Report BC-X-336, Forestry Canada, Pacific Forestry Centre, Victoria, British Columbia, 12 pp.

10IntpestManCh10.QXD 14/4/04 2:26 pm Page 253

IPM in Forestry