[Edited_by_A._Ciancio,_C.N.R.,_Bari,_Italy_and_K.(Bookos.org)

Integrated Management of Arthropod Pests and Insect Borne Diseases

Integrated Management of Plant Pests and Diseases 

Published: 

Volume 1 

General Concepts in Integrated Pest and Disease Management 

edited by A. Ciancio and K.G. Mukerji 

ISBN 978-1-4020-6060-1 

Volume 2 

Integrated Management and Biocontrol of Vegetable and Grain 

Crops Nematodes 


ISBN 978-1-4020-6062-5 

Volume 3 

Integrated Management of Diseases Caused by Fungi, Phytoplasma 

and Bacteria 


ISBN 978-1-4020-8570-3 

Volume 4 

Integrated Management of Fruit Crops Nematodes 


ISBN 978-1-4020-9857-4

Integrated Management of 

Arthropod Pests and Insect 

Borne Diseases 

Edited by 

A. Ciancio 

C.N.R., Bari, Italy 

and 

K.G. Mukerji 

University of Delhi, India

Editors 

Aurelio Ciancio 

Consiglio Nazionale delle 

Ricerche 

Istituto per la Protezione delle 

Piante 

Via G. Amendola, 122/D 

70126 Bari 

Italy 

ciancio@area.ba.cnr.it 

K.G.Mukerji † 

University of Delhi 

Dept. Botany 

New Delhi-110007 

India 

kgmukerji@rediffmail.com 

ISBN 978-90-481-2463-3 e-ISBN 978-90-481-8606-8 

DOI 10.1007/978-90-481-8606-8 

Springer Dordrecht Heidelberg London New York 

Library of Congress Control Number: 2010921597 

c○ Springer Science+Business Media B.V. 2010 

No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by 

any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written 

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Printed on acid-free paper 

Springer is part of Springer Science+Business Media (www.springer.com)

PREFACE 

This is the last volume of the IPMD series. It aims, in a multi-disciplinary approach, 

at reviewing and discussing recent advances and achievements in the practice of crop 

protection and integrated pest and disease management. This last effort deals with 

management of arthropods, and is organized with a first section on biological control 

in citrus orchards, a second one on advanced and integrated technologies for insect 

pest management and a last section, dealing with mites and their biological control. 

A wide and exaustive literature already covers several aspects of chemical or 

biological control of insects and mites, but there is still a need for a more holistic 

vision of management, accounting for different problems and solutions, as they are 

applied or developed, in different regions and cropping systems, worldwide. In this 

series we attempted to fill this gap, providing an informative coverage for a broad 

range of agricultural systems and situations. 

As for the other volumes of the IMPD Series, also this book is organized in 

chapters mainly centered on crops, with a particular emphasis given on citrus 

production, which by itself covers the first section. Citrus is one of the main crops in 

which biological control and management of pests proved successful worldwide, and 

the experience gained in this field may indeed result helpful for IMP efforts deployed 

on other crops and/or cropping systems, in other cultivated areas. Chapters grouped 

in Section 2 review the advancements of the integration of insect management 

options with other crop problems in extensive cropping systems (i.e. pecan, Chapter 

6), the application of remote sensing technologies (Chapter 7), the status of 

knowledge about plant defense compounds and their potentials (Chapter 8). For IPM 

of invasive species, Chapter 9 provides an update experience gained on the field to 

manage and counteract the Red Palm Weevil (RPW) in Egypt, a serious invasive 

pest spreading in all the mediterranean regions. Long-term technological solutions 

are described in Chapter 10, which deals with the extensive management of forests 

and park areas through aerial treatments of bacterial spores. Finally, in Section 3, an 

updated review about current knowledge on IPM through microbial control agents of 

mites is provided (Chapter 11), followed by a final chapter concerning features of 

predatory mites. 

In conclusion of this series, our sincere acknowledgements go to all the authors 

that provided, through their experience and dedication, a broad range of data on the 

management solutions thay studied and made available in different agricultural 

systems of the world. Thanks to their efforts, we hope we were able to contribute to 

spread the basic concepts related to the application of environment friendly and 

sustainable management practices. Our hope is that this series will result useful and 

helpful for interested readers and students, inspiring and supporting, at the same 

time, new and innovative research efforts in their daily field and laboratory work. 

v 


K. G. Mukerji †

CONTENTS 

Contributors ............................................................................................................ xv 

SECTION 1 - IPM IN CITRUS GROVES 

1 Citrus Pest Management in the Northern Mediterranean Basin 

(Spain, Italy and Greece) ................................................................................ 3 

Josep Anton Jacas, Filitsa Karamaouna, 

Rosa Vercher and Lucia Zappalà 

1. Introduction .................................................................................................. . 3 

2. Main arthropod pests and control strategies .................................................. 6 

2.1. Sampling and Monitoring ....................................................................... 6 

2.2. Biological Control .................................................................................. 6 

2.3. Chemical control .................................................................................. 21 

References ....................................................................................................... 26 

2 Main Arthropod Pests of Citrus Culture and Pest Management 

In Greece ........................................................................................................ 29 

Filitsa Karamaouna, Panagiotis Mylonas, Dimitrios Papachristos, 

Dimitrios Kontodimas, Antonios Michaelakisand Eleftheria Kapaxidi 

1. Introduction ................................................................................................. 29 

2. Pest Status and Control Measures ............................................................... 30 

2.1. The Mediterranean Fruit Fly, Ceratitis capitata ................................... 31 

2.1.1. Monitoring .................................................................................. 32 

2.1.2. Mass Trapping ............................................................................ 33 

2.1.3. Biological Control ...................................................................... 33 

2.1.4. Cultural Practices........................................................................ 34 

2.1.5. Biotechnical Methods. ................................................................ 34 

2.1.6. Chemical Control........................................................................ 34 

2.1.7. Recommended IPM Strategies. .................................................. 36 

2.2. Scale Insects ......................................................................................... 36 

2.2.1. Sampling and Monitoring . .......................................................... 37 


2.2.3. Cultural Practices ....................................................................... 38 


2.2.5. Recommended IPM Strategies ................................................... 39 

2.3. Whiteflies. ............................................................................................ 40 


2.3.2. Biological Control and Cultural Practices .................................. 40 

vii

viii 

CONTENTS 



2.4. The Citrus Leafminer, Phyllocnistis citrella. ....................................... 42 


2.4.2. Biological Control. ..................................................................... 43 

2.4.3. Cultural Practices ....................................................................... 44 



2.5. Aphids. ................................................................................................. 45 





2.6. The Citrus Flower Moth, Prays citri .................................................... 48 





2.7. Thrips ................................................................................................... 49 

2.8. Mite Pests. ............................................................................................ 50 




3. Arthropod IPM in Citrus Throughout the Year ........................................... 53 

References ....................................................................................................... 53 

3 Biological Control in Citrus in Spain: from Classical to Conservation 

Biological Control ......................................................................................... 

Josep Anton Jacas and Alberto Urbaneja 

1. Introduction. ................................................................................................ 61 

2. The Origins: Classical Biological Control in Citrus. ................................... 64 

3. Augmentation Versus Inoculation ............................................................... 65 

4. Fortuitious Biological Control ..................................................................... 66 

5. The Cornerstone: Conservation ................................................................... 66 

5.1. The First Step: Pesticide Side-Effect Testing ....................................... 67 

5.2. Alternative Host and Banker Plants. .................................................... 67 

5.3. Ground Cover Mangement Strategies .................................................. 69 

Conclusions ..................................................................................................... 70 

References ....................................................................................................... 70 

61

CONTENTS 

ix 

4 Citrus Integrated Pest Management in Italy. .............................................. 73 

Lucia Zappalà 

1. Introduction ................................................................................................. 73 

2. Main Pests and Their Control Methods ....................................................... 74 

2.1. Aonidiella aurantii (Maskell). .............................................................. 75 

2.2. Aspidiotus nerii Bouché ....................................................................... 79 

2.3. Phyllocnistis citrella (Stainton) ............................................................ 80 

2.4. Planococcus citri (Risso). .................................................................... 87 

2.5. Ceratitis capitata (Wiedemann). .......................................................... 89 

3. Secondary Pests ........................................................................................... 93 

References ....................................................................................................... 94 

5 Entomopathogenic Nematode Ecology and Biological Control 

in Florida Citrus Orchards ............................................................................................ 101 

Raquel Campos-Herrera, Robin J. Stuart, Fahiem El-Borai, 

Carmen Gutierrez and Larry Duncan 

1. Introduction. .............................................................................................. 101 

2. IPM of the Diaprepes-Phytophthora Complex ......................................... 104 

2.1. Diaprepes Economic Importance, Biology and Management ............ 104 

2.2. EPN Biology and Use in IPM Programs ............................................ 105 

2.3. Spatial Relationships Between Soils, Root Weevils and 

Endemic EPNs ..................................................................................... 107 

3. From Augmenting to Conserving EPNs .................................................... 110 

3.1. Soil Food Webs and EPN Spatial and Temporal Patterns .................. 111 

3.2. Identifying Factors that Regulate EPN Abundance and Efficacy ...... 113 

Conclusions ................................................................................................... 123 

References ..................................................................................................... 123 

SECTION 2 - ADVANCED IPM TECHNOLOGIES 

6 Integration of Insect and Mite Management with Disease and Weed 

Control in Pecan Production . ..................................................................... 133 

James D. Dutcher, Lenny Wells, Timothy B. Brenneman 

and Michael G. Patterson 

1. Pests Impede the Versatility of the Pecan Tree ......................................... 133 

2. Pest Control Methods. ............................................................................... 136 

2.1. Insect and Mite Pest Management in Pecan Orchards. ...................... 137 

2.2. Pecan Disease Management. .............................................................. 140 

2.3. Weed Management in Pecan Orchards .............................................. 143 

3. Benefits of Crimson Clover and Legumes Use in Pecan Orchards. .......... 146 

3.1. Pecan Nitrogen Use and Compatibility with Crimson Clover............ 147 

3.2. Enhancement of Pest Management .................................................... 148 

3.3. Soil Building and Sustainability. . ....................................................... 149

x 

CONTENTS 

3.4. Wildlife Benefits ................................................................................ 151 

3.5. Establishment and Maintenance. . ....................................................... 151 

3.6. Costs and Savings .............................................................................. 152 

4. Integrated Pest Management in Pecan Orchards ....................................... 152 

References ..................................................................................................... 156 

7 Locust Habitat Monitoring and Risk Assessment Using Remote Sensing 

and GIS Technologies ................................................................................. 163 

Alexandre V. Latchininskyand Ramesh Sivanpillai 

1. Introduction. .............................................................................................. 163 

2. Remote Sensing, Geographic Information 

Systems (GIS), and Global Positioning Systems (GPS)............................ 165 

2.1. Remote Sensing ............................................................................... 165 

2.2. Information Extraction ..................................................................... 169 

2.3. Geographic Information Systems (GIS) .......................................... 169 

2.4. Global Positioning Systems (GPS) .................................................. 171 

3. Remote Sensing and Locust Pest Management ......................................... 172 

3.1. Desert Locust Biology and Habitat Requirements ............................. 173 

3.1.1. Habitat Mapping and Post-Damage Assessment. ..................... 174 

3.2. Migratory Locust Biology and Habitat Requirements ....................... 177 

3.2.1. Habitat Mapping and Post-Damage Assessment ...................... 177 

3.3. Australian Plague Locust ................................................................... 179 

3.3.1. Habitat Mapping and Post-Damage Assessment ...................... 179 

3.4. Other Locusts ..................................................................................... 181 

Conclusions ................................................................................................... 182 

References ..................................................................................................... 183 

8 Plant Defenses Against Insect Herbivory .................................................. 189 

Farha-Rehman, Fareed A. Khan, Shoeba B. Anis and S. M. A. Badruddin 

1. Introduction. .............................................................................................. 189 

2. Plant Defense Mechanisms ........................................................................ 190 

3. Insect Diversity and Crop Damage ............................................................ 192 

4. Herbivory .................................................................................................. 193 

4.1. Insect Herbivores ............................................................................... 193 

4.2. Plant Responses to Insect Herbivory .................................................. 194 

4.3. Plant Reaction to Previous Herbivores ............................................... 194 

4.4. Impact of Herbivory on Ecosystem .................................................... 195 

4.5. Herbivore Strategies ........................................................................... 196 

4.6. Simulation of Herbivory ..................................................................... 197 

5. Defense Strategies ..................................................................................... 198 

5.1. Plant Defense Strategies . .................................................................... 198 

5.2. Plant Receptor Molecules ................................................................... 199

CONTENTS 

xi 

5.3. Defense Genes in Plants ..................................................................... 199 

5.4. Tri-Trophic Plant Signalling .............................................................. 201 

Conclusions ................................................................................................... 203 

References ..................................................................................................... 205 

9 IPM of the Red Palm Weevil, Rhynchophorus ferrugineus ...................... 209 

Mohamed Samir Tawfik Abbas 

1. Introduction ............................................................................................... 209 

2. Habitat, Infestation and Damage ............................................................... 210 

2.1. Infestation Spreading.......................................................................... 210 

3. Biology ...................................................................................................... 211 

3.1. Morphological Characters .................................................................. 211 

3.2. Life Cycle ........................................................................................... 211 

3.2.1. Oviposition ............................................................................... 211 

3.2.2. Feeding ..................................................................................... 212 

3.2.3. Locomotion .............................................................................. 214 

4. Natural Enemies ........................................................................................ 214 

4.1. Parasitoids .......................................................................................... 214 

4.2. Predators ............................................................................................. 215 

4.3. Pathogens ........................................................................................... 215 

4.4. Nematodes .......................................................................................... 216 

5. Control ....................................................................................................... 216 

5.1. Chemicals ........................................................................................... 216 

5.1.1. Spraying.................................................................................... 216 

5.1.2. Injection .................................................................................... 217 

5.2. Aggregation Pheromone Traps ........................................................... 218 

5.2.1. Trap Design and Components .................................................. 218 

5.2.2. Trap Installation ....................................................................... 219 

5.2.3. Density of Traps ....................................................................... 219 

5.2.4. Utilization of Pheromone Traps ............................................... 220 

5.2.4.1. Traps Efficiency .......................................................... 220 

5.2.4.2. Estimating RPW Population Fluctuations ................... 222 

5.2.4.3. Estimating Reduction of RPW Populations ................. 222 

5.2.4.4. Estimating Sex Ratios ................................................. 223 

5.3. Entomopathogenic Nematodes .......................................................... 224 

5.3.1. Pathogenicity to RPW .............................................................. 224 

5.3.2. Field trials ................................................................................. 226 

5.3.3.1. Injection of Nematodes ............................................... 226 

5.3.3.2. Spraying Nematodes .................................................... 227 

Trunk Spraying ........................................................... 227 

5.4. Soil Treatments .................................................................................. 228 

5.5. Semi-Field Trials ................................................................................. 229 

References ..................................................................................................... 230

xii 

CONTENTS 

10 Control of Urticating Lepidoptera Outbreaks with 

Bacillus thuringiensis Aerial Treatments ................................................... 235 

Pio Federico Roversi, Leonardo Marianelli, Lorenzo Marziali, 

Michele Squarcini and Gianpaolo Barzanti 

1. Introduction ............................................................................................... 235 

2. Urticating Lepidoptera ............................................................................... 236 

3. Aerial Control ............................................................................................ 240 

References ..................................................................................................... 243 

SECTION 3 - MITES BIOLOGICAL CONTROL AND IPM 

11 IPM Potentials of Microbial Pathogens and Diseases of Mites ............... 249 

Leo P. S. van der Geest 

1. Introduction ............................................................................................... 249 

2. Virus Diseases ........................................................................................... 250 

3. Diseases Caused by Bacteria ..................................................................... 254 

4. Diseases Caused by Fungi ......................................................................... 260 

4.1. Zygomycota ....................................................................................... 261 

4.1.1. Course of Infection ................................................................... 263 

4.1.2. Natural Entomophthoraceous Infections .................................. 267 

4.1.3. Role of Neozygites floridana in the Field ................................. 268 

4.1.4. The Cassava Green Mite and Neozygites tanajoae ................... 269 

4.2. Deuteromycetes .................................................................................. 272 

4.2.1. Hirsutella infections in mites ................................................... 273 

4.2.2. Other Deuteromycetes Infecting Mites ..................................... 282 

4.3. Ascomycota ........................................................................................ 285 

5. Diseases Caused by Eukaryotic Microparasites ........................................ 286 

5.1. Apicomplexa Infections in Mites ....................................................... 290 

5.2. Microspora Infections in Mites .......................................................... 291 

6. Other Diseases ........................................................................................... 294 

6.1. Symptoms Ascribed to Poor Condition .............................................. 294 

6.2. Identification of Pathogens ................................................................. 295 

7. Prospects of acaropathogens for integrated pest management .................. 296 

References ..................................................................................................... 300 

12 IPM Strategies Through Specialist and Generalist 

Phytoseiids (Acari, Mesostigmata) ............................................................. 311 

Sauro Simoni and Marisa Castagnoli 

1. Introduction ............................................................................................... 311 

2. Concepts on Natural Enemies and/or Antagonists in IPM ........................ 313 

3. Why Phytoseiids? ...................................................................................... 314 

3.1. Mass Rearing ...................................................................................... 314 

3.2. Fitness and Adaptation Characters ..................................................... 316

CONTENTS 

xiii 

3.3. Life Style Types ................................................................................ 317 

3.4. Single or Multiple Antagonists Release ............................................ 320 

3.5. Cannibalism and Intraguild Predation ............................................... 321 

Conclusions ................................................................................................... 321 

References ..................................................................................................... 322 

Index ..................................................................................................................... 327

CONTRIBUTORS 

Mohamed S. T. Abbas 

Plant Protection Research Institute, 

Dokki, Cairo, Egypt 

Shoeba B. Anis 

Deptartment of Zoology, 

Aligarh Muslim University, 

202002 Aligarh, UP, India 

S. M. A. Badruddin 

Department of Zoology, 



Gianpaolo Barzanti 

Agricultural Research Council, 

Research Centre For Agrobiology 

and Pedology, 

Cascine Del Riccio, 

50125 Firenze, Italy 

Timothy B. Brenneman 

Plant Pathology Department, 

University of Georgia, 

Tifton, GA, USA 

Raquel Campos-Herrera 

University of Florida, IFAS 

Citrus Research and 

Education Center, 

FL 33850, Lake Alfred, USA 

Marisa Castagnoli 


Research Centre For Agrobiology 

and Pedology, via di Lanciola 12/A, 

Cascine Del Riccio, 


Larry Duncan 


Citrus Research and Education Center, 

Lake Alfred, FL 33850, USA 

James Dutcher 

Entomology Department, 



Fahiem El-Borai 



Lake Alfred, FL 33850, USA; 

Plant Protection Department, 

Faculty of Agriculture, 

Zagazig University, Zagazig, Egypt 

Carmen Gutierrez 

Depto de Agroecología, 

Instituto de Ciencias Agrarias, CSIC 

Centro de Ciencias Medioambientales, 

28006 Madrid, Spain 

Josep Anton Jacas 

Universitat Jaume I (UJI), 

Unitat Associada d’Entomologia 

Agrίcola, 

E-12071 Castelló de la Plana, Spain 

Fareed A. Khan 

Department of Botany, 



Eleftheria Kapaxidi 

Benaki Phytopathological Institute, 

145 61 Kifissia, Greece 

Filitsa Karamaouna 



Dimitrios Kontodimas 



Alexandre V. Latchininski 

University of Wyoming, 

xv

xvi 

CONTRIBUTORS 

Department of Renewable Resources 

Laramie, WY 82071, USA 

Leonardo Marianelli 

CRA Research Centre for Agrobiology 

and Pedology, Cascine del Riccio, 


Lorenzo Marziali 




Antonios Michaelakis 



Panagiotis Mylonas 


8 Stefanou Delta str., 


Dimitrios Papachristos 



Michael G. Patterson 

Department of Agronomy and Soils, 

Auburn University, 

Auburn, AL, USA 

Farha-Rehman 

Department of Botany 



Pio Federico Roversi 




Sauro Simoni 


and Pedology, via di Lanciola 12/A, 

Cascine del Riccio, 


Ramesh Sivanpillai 

Department of Botany and Wyoming 

Geographic Information Science Center, 

University of Wyoming, 


Michele Squarcini 




Robin J. Stuart 




Alberto Urbaneja 

Institut Valencià d’Investigacions 

Agràries (IVIA), Unitat Associada 

d’Entomologia Agrícola UJI-IVIA, 

E-46113 Montcada, Spain 

Leo P. S. van der Geest 

IBED, Section Population Biology, 

University of Amsterdam, 

1098SM Amsterdam, The Netherlands 

Rosa Vercher 

Universidad Politécnica de Valencia 

Instituto Agroforestal Mediterráneo 

(UPV), 

46022 Valencia, Spain 

Lenny Wells 

Horticulture Department, 



Lucia Zappalà 

Dipartimento di Scienze e Tecnologie 

Fitosanitarie, University of Catania, 

95123, Catania, Italy

OBITUARY NOTICE 

Prof. K. G. Mukerji 

Professor Krishna Gopal Mukerji passed away suddenly, aged 75. He was born on 

4th May 1934 at Lucknow as fourth child of Mr. Davendra Nath Mukerji and Mrs. 

Leela Mukerji. He received his early education in Lucknow and obtained his B.Sc. 

and M.Sc. degrees from Lucknow University in 1953 and 1955, respectively. In 

1955, he started his teaching career as Lecturer in Botany at Lucknow University, 

from where he also obtained his Ph.D. in Botany in 1962, with a thesis entitled 

“Microfungi of Usar Soil of India”. He was then appointed Lecturer in Botany at 

Banaras Hindu University in 1962, where he worked for 2 years. He then joined the 

Department of Botany at the University of Delhi as Lecturer (1964), to be later 

appointed Reader and Professor in 1969 and 1982, respectively. He became Head of 

the Department of Botany, University of Delhi during the years 1985–1988. During 

his scientific career he was actively engaged in research on different aspects of 

microbial ecology, with particular reference to soil fertility and plant productivity. 

His significant contributions concerned different areas of mycology, plant 

pathology, microbial ecology and biotechnology. In his research work he 

investigated, discovered and described several species and genera of fungi, including 

mycorrhizae from Indian soils. Professor Mukerji had keen interest in culture 

collections and received advanced training in fungal taxonomy at the 

Commonwealth Mycological Institute (CMI) in Kew, England (1968), where he was 

also offered a permanent position as mycologist, in 1968. He also worked at the 

Institute of Seed Pathology at Copenhagen, Denmark (1974), at the Institute of 

Meeresforschung, Bremerhaven, Germany (1973) and at the Centraalbureau voor 

Schimmelcultures, Baarn, The Netherlands (1974). 

As visiting professor or scientist, professor Mukerji visited various Institutes, 

Culture Collections and Laboratories throught America, Asia, Australia and Europe. 

His career lasted 40 years and included taxonomy and ecology of fungi from soil, 

photosphere and roots, as well as mycorrhizae, plant surface, organic matter and 

seeds. More than 200 students received their Ph.D. and M.Ph. degrees from the 

Delhi University, studying various aspects of mycology, plant pathology, microbial 

xvii

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O 

BITUARY 

N 

OTICE 

ecology and microbial biotechnology under his supervision. Professor Mukerji was a 

widely traveled botanist and attended several national and international conferences 

and symposia, presenting key notes and invited papers. He was a member of 

numerous societies and associations, also as Treasurer (Mycological Society of 

India, 1973–1976), Vice-President (Mycological Society of India, 1980–1981 and 

Association of Tropical Microbial Ecology, 1980–1984), President (Society for 

Advancement of Botany, 1987, and Society for Environment scientists, 1988–1991). 

He was member of several editorial boards, inlcuding the Transactions of the 

Mycological Society of India (1979–198l), Phytologia, the Journal of the Indian 

Botanical Society and the Journal of Phytology Research (since 1988). He was also 

Editor or Advisory Committee member for several journals, including the Indian 

Journal of Microbial Ecology, Frontiers in Applied Microbiology, CRC Critical 

Reviews on Biological Control of Plant Pests, Diseases and Weeds (since 1990). 

Professor Mukerji was also Councillor for the International Society of Root 

Research and the Nitrogen Fixing Tree Association. He authored or co-authored 

more than 550 research papers on various aspects of mycology, plant pathology, 

microbial ecology and biotechnology, and co-authored, edited and co-edited more 

than 45 books, dealing with various aspects of microbial ecology and biotechnology. 

Professor Mukerji retired as Senior Professor from the University of Delhi in 2004 

but continued his intense editorial and publication activity until this year. As one of 

the most distinguished mycologist and microbial ecologist from India he is still 

credited for his research contributions, which are recognized all over the world. His 

death is a great loss for India as well as for the international scientific community. 

Those who had the priviledge of sharing with him some work time will remember a 

very gentle and kind person, and a bright, experienced and outstanding scientist. We 

convene our sincere and heartfelt condolences at this most difficult of times to his 

beloved wife and son. He will be greatly missed. 


Zuzana Bernhart

Section 1 

IPM IN CITRUS GROVES

1 

CITRUS PEST MANAGEMENT IN THE NORTHERN 

MEDITERRANEAN BASIN (SPAIN, ITALY AND 

GREECE) 

JOSEP ANTON JACAS 1 , FILITSA KARAMAOUNA 2 , ROSA 

VERCHER 3 AND LUCIA ZAPPALÀ 4 

1 Universitat Jaume I(UJI),Unitat Associada d’Entomologia 

Agrίcola UJI-IVIA, E-12071 Castelló de la Plana, Spain 

2 Benaki Phytopathological Institute, 

14561 Kifissia, Greece 

3 Instituto Agroforestal Mediterráneo, 

Universidad Politécnica de Valencia, 46022 Valencia, Spain 

4 Dipartimento di Scienze e Tecnologie Fitosanitarie, 

University of Catania, 95123 Catania, Italy 

Abstract. Main management options for arthropod pests of citrus and species recently introduced in the 

northern Mediterranean regions are reviewed. Available control strategies are discussed, including visual 

inspection practices, insect trapping methods and natural enemies release in augmentative or classical 

biological control. IPM practices and side effects of pesticides are also reviewed. 

1. INTRODUCTION 

The most widely cultivated citrus species in the Mediterranean region include 

orange [Citrus sinensis (L.) Osbeck], lemon [Citrus limon (L.) Burman f.], mandarin 

(Citrus reticulata Blanco), tangerine (Citrus deliciosa Tenore), grapefruit (Citrus 

paradisi Macfadyen), sour orange (syn. Chinese bitter orange, bigarade orange, 

Seville orange) (Citrus aurantium L.), lime [Citrus aurantifolia (Christm.) Swingle] 

and citron (Citrus medica L.) (Katsoyannos, 1996). Minor citrus species are pumelo 

(syn. shaddock) [Citrus maxima (Burm.) Merrill, syn. C. grandis (L.) Osbeck, C. 

All authors contributed equally to this chapter. 

A. Ciancio, K.G. Mukerji (eds.), Integrated Management of Arthropod Pests 

and Insect Borne Diseases, Integrated Management of Plant Pests and Diseases 5, 

DOI 10.1007/978-90-481-8606-8_1, © Springer Science+Business Media B.V. 2010 

3

4 

J.A. JACAS ET AL. 

decumana L.], bergamot (Citrus bergamia Risso) and chinotto or myrtle-leaved 

orange (Citrus myrtifolia Raf.). 

The total area of citrus production in the Mediterranean region sums up to 

1,036,878 ha (Franco, García-Marí, Ramos, & Besrí, 2006; ISTAT, 2007; El- 

Otmani, Srairi, & Benhaddou, 2007; Laajimi & Ben Mimoun, 2007; MAPA, 2007; 

Salama Eid, Latif, & Hassan, 2007) with more than 2/3 of the entire area 

concentrated in Spain, Italy, Egypt and Turkey (Table 1). Integrated Pest 

Management is performed on a percentage of this area that varies in each country 

from less than 1% in France (Corsica) to 100% in Israel. In Italy, Morocco and 

Portugal 10–20% of the total citrus production area is under IPM, while in Turkey 

this management strategy is applied on 30% of this area. Integrated production (IP) 

is only reported in Spain, Italy, Portugal and France ranging between 0.4% 

(Portugal) and 10% (Italy) of the total citrus area (Franco et al., 2006). 

Table 1. Total area of citrus production and percentage of integrated pest 

management (IPM) and integrated production (IP) in Mediterranean countries 

(modified from Franco et al., 2006. N.a. stands for not available). 

Country 

Citrus production area 

(ha) 

IPM (%) IP (%) 

Spain 311,004 Most of the area 5 

Italy 164,938 10–20 10 

Egypt 151,075 n.a. n.a. 

Turkey 150,000 30 – 

Morocco 80,000 10–20 – 

Greece 57,526 Most of the area – 

Algeria 45,400 n.a. – 

Portugal 27,755 14 0.4 

Tunisia 18,600 n.a. n.a. 

Israel 17,300 100 – 

Georgia 11,000 n.a. – 

France (Corsica) 1,800

CITRUS PEST MANAGEMENT IN THE MEDITERRANEAN BASIN 5 

IPM/IP guidelines are defined at regional level in Greece, Portugal and Turkey, 

and at both regional and national level in Israel, Italy and Spain. IPM/IP certification 

companies are reported in Italy, Spain and Portugal (Franco et al., 2006). 

Guidelines for Integrated Production of Citrus have been produced by the 

IOBC/WPRS Commission “IP-Guidelines and Endorsement” (IOBC/WPRS, 2004), 

and they mainly concern standards for the IP organizations in order to develop 

national or local guidelines. According to these standards and in relation to 

integrated plant protection, all available preventive (indirect) plant protection 

measures must be applied before direct control techniques are used. Priority should 

be given to natural, cultural, biological, genetic (GMOs are generally excluded and 

permission may be given on a case-by-case study) and biotechnical methods of pest 

control and the use of agrochemicals should be minimized. 

The decision for the application of direct control methods must be based on 

economic thresholds, wherever possible, risk assessments and forecasts, including 

those provided by official forecasting services. A restricted list of the key pests, 

diseases and weeds that require regular attention must be established by the IP 

organizations and their populations should be regularly monitored and recorded. In 

addition at least three key natural enemies in each crop must be identified in 

national/regional guidelines. Furthermore, the use of plant protection products toxic 

to these beneficial arthropods should be reduced to a minimum and always in 

periods of low activity of the natural enemies, or of low risk for them. Populations 

of key natural enemies must be preserved and incremented. 

With regard to pesticides, all those locally or nationally available must be 

classified by the IP organizations in two lists: the “green list” including the 

permitted products and the “yellow list” including those pesticides permitted with 

restrictions. The pesticides categorization is based on several criteria (i.e. toxicity to 

man, toxicity to key natural enemies, toxicity to other natural organisms, pollution 

of ground and surface water, ability to stimulate pests, selectivity, persistence, 

incomplete information, necessity of use), and it is already established for certain 

pesticides and pesticide groups as follows: 

- Not permitted: pyrethroid insecticides and acaricides, non-naturally 

occurring plant growth regulators (their use can only be allowed when 

absolutely necessary), organochlorine insecticides and acaricides, water 

polluting products and very persistent herbicides; 

- Permitted with restrictions: dithiocarbamate fungicides (normally 

maximum of three applications per season and not in succession, so that 

predatory phytoseiid mites are not affected), fosetil-Al and phosphonate 

potassium (maximum of two applications per year), metalaxyl (maximum 

of 2 g/m 2 ), residual (soil) herbicides (except toxic, polluting or very 

persistent products) in the first 3 years after planting (maximum of one 

dose-equivalent per annum). 

Officially recognized dose adjustment protocols must be used where available, in 

order to adapt dose rates to the size and density of the target trees being sprayed. 

The maximum volume of application per hectare must be defined according to the

6 


tree volume. A strategy of mandatory measures for minimizing the risk of resistance 

development of pests to pesticides (e.g. maximum number of applications per year, 

alternation of pesticides with different mode of action) must be set by the IP 

organizations. The growers/applicators must be trained in the use and the application 

of pesticides. 

2. MAIN ARTHROPOD PESTS AND CONTROL STRATEGIES 

In the citrus producing countries of the Mediterranean basin more than 140 pests and 

diseases are reported, including 108 insects, 10 mites, 1 nematode, 14 fungi, 2 

bacteria and 8 virus and virus like diseases (Franco et al., 2006). 

Among arthropods, the major pests, i.e. reported as key-pests in at least 50% of 

the countries, include the medfly Ceratitis capitata (Wiedemann) (100% of the 

countries), the California red scale Aonidiella aurantii (Maskell) (71%), the citrus 

leafminer Phyllocnistis citrella Stainton (71%) and the citrus mealybug Planococcus 

citri (Risso) (71%) (Table 2). 

Quarantine pests recently introduced in the western Mediterranean area include 

the brown citrus aphid Toxoptera citricida (Kirkaldy) (Northern Spain, from Galicia 

to the Basque Country, Madeira island and North of Portugal), the African citrus 

psylla Trioza erytreae (Del Guercio) (Madeira and Canary islands) and the citrus 

snow scale Unaspis citri (Comstock) (Azores, Malta and France). These species are 

included in the EPPO lists A1–A2 and are therefore regulated as quarantine pests in 

the whole EPPO region (EPPO, 2007). Special attention must be paid to T. citricida 

and T. erytreae as they are efficient vectors of the citrus tristeza virus (CTV) and the 

Huanglongbing agent (Candidatus Liberobacter), respectively. 

2.1. Sampling and Monitoring 

In IPM, pest control decisions are directly dependent upon knowing the status and 

population trends of the most important insect pests and their natural enemies 

(Beardsley, AliNiazee, & Watson, 1979; Cavalloro & Prota, 1983; Katsoyannos, 

1996). Sampling and monitoring are the means for acquiring this important 

knowledge. Simplified sampling guidelines for monitoring the main citrus insect 

pests in the northern Mediterranean have been advised by experts defining methods 

of visual inspection as well as trapping using food, chromotropic and sexual 

attractants for monitoring purposes (Katsoyannos, 1996) (Tables 3 and 4). 

2.2. Biological Control 

Biological Control has been proved very effective in management of insect pests in 

citrus orchards. Among 65 cases of successful biological control and 83 cases of 

satisfactory control of insect pests in various crops, which have been recorded all 

over the world, 61.5% of the first mentioned and 21.7% of the latter concern citrus 

(De Bach, 1964).


Several programmes of augmentative and classical biological control by means 

of parasitoids and predators of the main citrus pests have been conducted in most of 

the northern Mediterranean citrus growing countries (Table 5). The results vary, 

however, several successful cases have been recorded (Viggiani, 1975; Amaro, 

1992; Noyes & Hayat, 1994; Katsoyannos, 1996; Tsagarakis, Kalaitzaki, 

Lykouressis, Michelakis, & Alexandrakis, 1999; Kalaitzaki, 2004; Siscaro, Caleca, 

Reina, Rizzo, & Zappalà, 2003; Siscaro, Di Franco, & Zappalà, 2008; Gomes da 

Silva, Borges da Silva, & Franco, 2006; Jacas, Urbaneja, & Viñuela, 2006; Malausa, 

Rabasse, & Kreiter, 2008; Zappalà, Siscaro, & Longo, 2008). 

Table 2. Arthropod pests of citrus and rating of their pest status in the northern 

Mediterranean regions (modified from Franco et al., 2006)*. 

Group Order Family Species 

France (F) 

Greece (G) 

Italy (I) 

Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Insects 

Orthoptera 

Acrididae 

Tettigonidae 

Thysanoptera 

Thripidae 

Hemiptera 

Anacridium 

aegyptium (L). 0 1 0 1 1 0 

Phaneroptera 

nana Fiebre 0 0 0 2 1 0 

Frankliniella 

bispinosa (Morgan) 0 0 1 a 0 0 

Frankliniella 

occidentalis (Pergande) 1 1 1 2 1 2 

Heliothrips 

haemorrhoidalis 

(Bouché) 1 2 b 2 1 0 

Pezothrips 

kellyanus (Bagnall) 2 2 1 b 1 2 

Thrips australis (Bagnall) 0 0 1 0 0 

Thrips flavus Schrank 1 1 2 1 0 

Thrips major Uzel 1 0 2 1 2 

Thrips tabaci Lindeman 1 1 1 2 0 2 

Pentatomidae Nezara viridula (L.) 1 1 0 1 0 2 

Miridae Closterotomus trivialis 

(Costa) 2 2 0 0 1,2 0 

Flatidae Metcalfa pruinosa (Say) 3 1 1 1 0 0 

Cicadellidae Empoasca 

decedens (Paoli) 0 1 1 0 2 c 1 

Triozidae Trioza 

Erytreae (Del Guercio) 0 0 0 3 a 2 d 0

8 


Table 2 continued 


France (F) 

Greece (G) 


Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Aleyrodidae Aleurothrixus 

Floccosus (Maskell) 

3 2 2 1 3 2 2 

Bemisia 

afer (Priesner & Hosny) 0 1 0 0 1 0 

Bemisia 

tabaci (Gennadius) 2 

Dialeurodes 

citri (Ashmead) 3 2 e 1 3 0 1 1 

Dialeurodes 

citrifolii (Morgan) 0 0 0 1 a 0 0 

Parabemisia 

myricae (Kuwana) 0 1 1 0 1 1 2 

Paraleyrodes 

bondari Peracchi 0 0 0 1 a 0 0 

Paraleyrodes 

citricolus Costa Lima 0 0 0 1 a 0 0 

Paraleyrodes 

minei Iaccarino 0 0 0 1 1 2 

Aphididae Aphis craccivora Kock 2 1 1 2 1 1 2 

Aphis fabae Scopoli 2 1 1 1 1 0 

Aphis gossypii Glover 3 2 2 0 3 2 1 

Aphis spiraecola Patch 2 2 0 3 2 1 

Aulacorthum 

solani (Kaltenbach) 2 1 1 0 1 0 0 

Macrosiphum 

euphorbiae (Thomas) 2 1 1 0 1 0 0 

Myzus ornatus Laing 0 0 0 1 a 0 0 

Myzus persicae (Sulzer) 2 1 1 1 1 1 

Neomyzus 

circunflexum (Buckton) 0 0 0 0 0 0 

Rhopalosiphum 

maidis (Fitch) 0 1 0 0 

Toxoptera 

aurantii (Boyer de) 

(Fonscolombe) 3 2 2 2 3 1 2 

Toxoptera 

citricida (Kirkaldy) 0 0 0 0 3 fa 2 g 0 

Margarodidae Icerya purchasi Maskell 3 1 1 1 2 1 1 

Ortheziidae 

Orthezia 

insignis Douglas 0 0 0 1 a 0 0




France (F) 

Greece (G) 


Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Pseudococcidae 

Coccidae 

Diaspididae 

Nipaecoccus 

nipae (Maskell) 0 0 0 1 a 0 0 

Phaenacoccus 

madeirensis Green 0 1 0 0 0 

Planococcus citri (Risso) 3 3 2, 3 1 3 1, 2 3 

Pseudococcus 

calceolariae (Maskell) 0 1 0 2 1 0 

Pseudococcus longispinus 

(Targioni-Tozzetti) 

1 1 0 1 1 0 

Pseudococcus 

viburni (Signoret) 0 1 0 2 0 1 

Ceroplastes 

floridensis Comstock 1 0 0 1 ah 1 3 

Ceroplastes 

japonicus Green 1 1 0 0 0 

Ceroplastes rusci (L.) 

1 2 0 1 1 1 

Ceroplastes 

sinensis Del Guercio 3 1 1 1 2 1 0 

Coccus hesperidum L. 3 1 1 1 2 1 2 

Coccus pseudomagnoliarum 

(Kuwana) 1 1 2 0 2 

Coccus viridis (Green) 0 0 0 1 a 0 0 

Eucalymnatus 

tessellates (Signoret) 0 0 0 1 a 0 0 

Parasaissetia 

nigra (Nietner) 0 0 0 1 a 0 0 

Parthenolecanium 

persicae (F.) 0 1 0 1 0 0 

Protopulvinaria 

pyriformis ( Cockerell) 0 1 1 0 1,2 a 1 0 

Pulvinaria 

floccifera ( Westwood) 0 1 0 0 0 

Saissetia coffeae (Walker) 0 1 0 1,2 1 

Saissetia oleae (Olivier) 3 1 2 2 2 1 2 

Aonidiella 

aurantii (Maskell) 3 2 3 1 3 i 3 3 

Aspidiotus nerii Bouché 1 3 b 0 1 2 b 0 

Chrysomphalus aonidum (L.) 1 2 0 0 0 0 

Chrysomphalus 

dictyospermi (Morgan) 3 1 1 1 2 1 2

10 




France (F) 

Greece (G) 


Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Lepidoptera 

Gracillariidae 

Chrysomphalus 

pinnulifer Maskell 0 0 0 1,2 a 0 0 

Hemiberlesia 

rapax (Comstock) 0 1 0 1 1 0 

Lepidosaphes 

gloverii (Packard) 3 0 2 0 1 1 0 

Lepidosaphes 

beckii (Newman) 3 2 1 1 3 2, 3 2 

Lopholeucaspis 

japonica (Cockerell) 0 0 0 0 0 

Mycetaspis 

personata (Comstock) 0 0 0 1 a 0 0 

Parlatoria 

pergandei Comstock 3 1 2 0 2 2, 3 1 

Parlatoria 

ziziphi (Lucas) 0 2 2 0 0 1 0 

Diaspidiotus 

perniciosus (Comstock) 0 0 0 0 0 0 

Unaspis citri (Comstock) 0 0 0 0 3 h 0 0 

Unaspis 

yanonensis (Kuwana) 2 0 2 0 0 0 

Phyllocnistis 

citrella Stainton 3 2 

jk 

2 3 jk 3 j 1, 2 3 j 

Hyponomeutidae Prays citri (Millière) 3 2 2 b 0 3 b 3 b 1 b 

Tortricidae Archips rosanus (L.) 1 1 1 0 0 

Cacoecimorpha 

pronubana (Hübner) 1 1 1 2 1 2 

Geometridae Cleora 

fortunata ( Blachier ) 

0 0 0 1 a 0 0 

Gymnoscelis 

pumilata Hübner 0 1 0 0 0 

Gymnoscelis 

rufifasciata (Haw.) 0 0 0 1 0 0 

Noctuidae Helicoverpa 

armigera (Hübner) 0 0 0 1 b 1 2 

Peridroma 

saucia (Hübner) 0 0 0 1 0 0 

Pyralidae Cryptoblabes 

gnidiella ( Millière) 1 1 0 2 1 2 

Ectomyelois 

ceratoniae (Zeller) 

1 1 0 2 1 2




France (F) 

Greece (G) 


Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Nymphalidae Charaxes jasius L. 0 1 0 0 0 

Diptera 

Tephritidae Ceratitis 

capitata (Wiedemann) 

3 3 3 2, 3 e 3 3 3 lm 

Coleoptera 

Curculionidae 

Scarabaeidae 

Hymenoptera 

Formicidae 

Mites 

Acariformes 

Asynonychus 

godmani (Cratch) 0 0 0 1 0 0 

Lyxus algirus L. 0 0 0 2 1 0 

Otiorrhynchus 

aurifer Boheman 0 2 jk 0 0 0 

Otiorrhynchus 

cribricollis Gyllenhall 0 2 j k 

0 0 1 0 

Pantomorus 

cervinus (Boheman) 0 0 0 2 a 0 0 

Cetonia carthami 

0 0 0 1 0 0 

aurataeformis Curtis 

Oxythyrea funesta (Poda) 1 1 1 1 1 0 

Tropinota hirta (Poda) 1 1 1 1 0 

Tropinota squalida (Scop.) 1 1 0 1 1 0 

Camponotus 

nylanderi Emery 0 2 n 0 0 0 

Crematogaster 

scutellaris (Olivier) 0 2 n 0 0 0 

Lasius niger (L.) 

Linepithema 

0 2 n 0 2 a 1 0 

(=Iridomyrmex) 

humile (Mayr) 

Tapinoma 

0 2 n 0 2 1 0 

nigerrimum (Nylander) 

Tapinoma 

0 2 0 0 0 

simrothi Krausse 

0 0 0 2 a 1 0 

Eriophyidae Aculops pelekassi (Keifer) 2 2 2 0 0 0 

Eriophyes 

sheldoni (Ewing) 2 2 b 1 2 b 2 b 1 

Phyllocoptruta 

oleivora (Ashmead) 1 0 0 0 0 3

12 




France (F) 

Greece (G) 


Montenegro 

(M) 

Portugal 

(P) 

Spain (S) 

Turkey (T) 

Tarsonemidae 

Tenuipalpidae 

Polyphagotarsonemus 

latus (Banks) 1 2 b 0 2 bk 1 2 

Brevipalpus 

californicus (Banks) 1 1 0 1 1 0 

Brevipalpus 

phoenicis (Geijskes) 1 0 0 2 1 0 

Tetranychidae 

Eutetranychus 

banksi (McGregor) 0 0 0 3 i o 

2 0 

Eutetranychus 

orientalis (Klein) 0 0 0 0 2 c 0 

Panonychus 

citri McGregor 3 2 2 3 2 2 1 

Tetranychus 

urticae (Koch) 

1 2 1,2 1 1 1–3 2 

* Ratings: 3 = key pest, requires the application of control measures most of the years because of 

economic damage; 2 = occasional pest, may reach economic injury level; 1= potential pest, always 

below economic injury level; 0 = not reported on citrus. a = Madeira Island. b = on lemon. c = in 

Southern Spain. d = only in Canary Islands. e = limited areas. f = North of Portugal. g = not reported in 

the main citrus growing areas of Spain yet. h = Azores. i = Algarve. j = on young trees. k = in 

nurseries. l = on mandarin. m = on sweet orange. n = natural enemies disruption. o = in western 

Andalusia. Ratings of species considered key-pests in at least one country are shown in bold.


Table 3. Visual inspection practices. 

Plant parts 

During the growing season/ 

warm periods of the year 

Twigs 

Apical twigs of… 

Green twigs 

Previous flushing 

twigs 

Flowers 

Purpose – target pest 

Twigs are shaken by hand and the number of adults of 

whiteflies taking flight is noted (every week) 

Observations are made on the presence of honeydew, 

sooty mould and ants, which are associated with the 

presence of aphids, whiteflies and soft scales as well as 

on cottony egg masses which are associated with 

mealybugs. Parasitism should be also recorded 

Detection of the citrus leafminer 

Monitoring the presence of aphids (every week) and 

Closterotomus trivialis (spring) 

Monitoring the development of armoured scales (every 

2 weeks), soft scales (every 2–3 weeks) and 1st and 2nd 

instar nymphs of Icerya purchasi 

Detection of Eriophyes sheldoni-affected organs in 

spring and mid-summer 

Detection of the citrus moth 

Fruits Monitoring the development of diaspidid scales (every 2 

weeks) and locating foci of infestation 

Fruits and fruit stem inspections for mealybugs, white 

cottony egg mass, sooty mould developed on secreted 

honeydew and ants, which are associated with 

mealybugs (every 2 weeks) 

Detection of the citrus moth 

Detection of Tetranychus urticae during the summerearly 

autumn 

Detection of Ceratitis capitata as colour change begins 

In the packinghouse, presence of diaspidid scales should 

be checked 

Young leaves Detection of whitefly and soft scales foci of infestation 

in the orchard 

Observations are made on the presence of sooty mould 

and ants, which are associated with whiteflies, soft 

scales and mealybugs (every 2–3 weeks) 

Detection of the citrus mite, Panonychus citri, at the end 

of summer 

Cold periods of the year 

Twigs 

Detection of T. urticae from May to October 

Detection of 3rd instar nymphs and pre-ovipositing 

females of I. purchasi 

a Visual inspections also allow monitoring coccinellid predators on trees.

14 


Table 4. Insect pests trapping methods. 

Type of trap 

Yellow water-pan traps 

Suction traps of 12 m high 

Yellow sticky traps 

Sex pheromone-baited traps 

White traps coated with glue mixed 

with trimedlure as well as other sex 

and food attractants 

Transparent sticky band traps 

Beating branches of trees with a 

rubber-covered stick over a 1 m 2 

cloth screen 

Purpose – target pest 

Monitoring aphids: Moericke pan-traps, both square 

(60 × 60 × 10 cm) and round (30 cm in diameter), 

painted canary yellow inside and containing water 

with a spoonful of added detergent up to a depth of 

3–4 cm are commonly used; should be placed in the 

citrus orchards in mid-spring, 2–5 traps/ha, 70 cm 

above the ground, to be checked 1–2 times/week 

during the growing season 

Monitoring aphids 

Catching newly emerged whitefly adults: traps 

should be placed in the lower outside canopy of the 

south or southeast quadrant of the tree 

Catching males of Aonidiella aurantii and other 

armoured scales 

Monitoring parasitoids and detection of leafhoppers 

(Empoasca spp.) 

Attracting adult males of A. aurantii [pheromone (3Z, 

6R)-3-methyl-6-isopropenyl-3.9-decadien-l-yl 

acetate]; 2–5 traps/ha at 1.8–2.5 height above the 

ground, to be checked twice a week from early spring 

to mid-late autumn 

Attracting adult males of Planococcus citri: various 

designs of traps available, the yellow or white sticky 

trap with pheromone [(1R-CIS)-3-isopropenyl-2.2- 

dimethylcyclobutyl-methyl acetate] dispenser being 

most effective; 2–5 traps/ha; catches to be correlated 

with shifts in the population densities of female 

mealybugs 

Monitoring of the citrus moth, Prays citri 

Catching adults of Ceratitis capitata; 10 traps/ha 

Measuring the density of crawlers of A. aurantii in 

order to determine the timing of chemical treatment; 

the traps are tightly fixed around heavily infested 

twigs from mid spring onwards 

For other diaspidids and soft scales 

Monitoring coccinellid predators

CITRUS PEST MANAGEMENT IN THE MEDITERRANEAN BASIN 15

16 

J.A. JACAS ET AL.


18 

J.A. JACAS ET AL.


20 

J.A. JACAS ET AL.

2.3. Chemical Control 


Although many classical or augmentative biological control trials of arthropod pests 

have been successful in citrus, chemical control is still used. The recently finalized 

EU Review Programme on the inclusion of old active substances of plant protection 

products (registered in the EU up to 1993) in the positive list (Annex I) of the 

Directive 91/414/EEC (CEC, 1991), based on agreed and harmonised criteria for 

evaluating the safety of pesticides, resulted in a modification of the availability of 

insecticides, acaricides and insect attractants authorized for citrus pest management 

in the various member states of the E.U. (Tables 6 and 7) (Hellenic Ministry of 

Rural Development and Food, 2008; MAPA, 2008; MiPAAF, 2008). Some of these 

pesticides were also tested to evaluate their side effects on beneficial arthropods 

(Table 8). 

Table 6. Insecticides, acaricides and insect attractants (active substances) registered for use 

on citrus in Spain, Italy and Greece (June 2008). 

Country 

Spain 

Italy 

Insecticides/acaricides/insect attractants (active substances) 

Abamectin (O, L, M, G), acetamiprid (O, L, M, G), alpha-cypermethrin 

(O, L, M, G), azadirachtin (O, L, M, G), Bacillus thuringiensis var. 

kurstaki (O, L, M, G), benfuracarb (O, L, M, G), bifentrin (O, L, M, 

G), buprofezin (O, L, M, G), carbosulfan (O, L, M, G), chlorpyrifos 

(O, L, M, G), chlorpyrifos-methyl (O, L, M), cihexatin (O, L, M, G), 

clofentezine (O,L,M,G), cypermethrin (O, L, M, G), deltamethrin (O, 

L, M, G), diazinon (O, L, M, G), dichlorvos (O, L, M, G), dicofol (O, 

L, M, G), diflubenzuron (O, M, G), dimethoate (O, L, M, G), 

etofenprox (O, M, G), etoxazol (O, M), fenazaquin (O, M, G), 

fenbutatin oxide (O, M, G), fenitrothion (O, L, M, G), fenoxycarb (O, 

M, G), fenpyroximate (O, L, M, G), flufenoxuron (O, M, G), 

hexythiazox (O, L, M, G), imidacloprid (O, L, M, G), kaolin (O, M), 

lambda-cyhalothrin (O, L, M, G), lufenuron (O, L, M, G), malathion 

(O, L, M, G), methomyl (O, L, M, G), methoxyfenozide (O, M), 

mineral oil (O, L, M, G), oxydemeton-methyl (O, L, M, G), phosmet 

(O, L, M, G), piridaben (O, L, M, G), pirimicarb (O, L, M, G), 

pirimiphos-methyl (O, L, M, G), potassium salts of vegetable fatty 

acids (O, L, M), propargite (O, L, M, G), pymetrozine (O, L, M, G), 

pyriproxifen (O, L, M, G), spinosad (O, L, M, G), tau-fluvalinate (O, 

L, M, G), tebufenozide (O, L, M, G), tebufenpyrad (O, L, M, G), 

trichlorfon (O, L, M, G) 

Abamectin (O, L, M), acrinathrin (O, L, G), alfamethrin (O, L, M), 

azadirachtin (O, L, M, G), Bacillus thurigiensis var. aizawai (O, L, M), 

Bacillus thurigiensis var. kurstaki (O, L, M), Beauveria bassiana (O, 

L, M), bifentrin (O, L, M), buprofezin (O, L, M), calcium polysulfur

22 



Greece 

(O, L, M), chlorpyrifos (O, L, M), chlorpyrifos-methyl (O, L, M, C), 

clofentezine (O, L, M, Cl, G, B), cypermethrin (O, L), deltamethrin (O, 

L, M), diazinon (O) (1), dicofol (O, L, M), dimethoate (O, L, M) (2), 

ethoprophos (O, L, M), etofenprox (O, L, M, Cl, B, SO, G, P, T, C), 

etoxazol (O, L, M, Cl, B, SO, G, P, T, C), fenazaquin (O, L, M, Cl), 

fenbutatin oxide (O, L, M), fenpyroximate (O, L, Cl), flufenoxuron (O, 

M, Cl), fluvalinate (O, M), hexythiazox (O, L, M), imidacloprid (O, L, 

M, Cl), lambda-cyhalothrin (O), lufenuron (O, L, M, Cl), malathion 

(O, L, M, Cl, B, SO, G, P, T, C) (1), methomyl (O, L, M), 

methoxyfenozide (O, M, Cl), mineral oil (O, L, M, Cl), phosalone (O, 

L, M) (3), phosmet (O, L, M), pirimicarb (O, L, M), pirimiphos-methyl 

(O, L), propargite (O, L, M, G, Cl), pymetrozine (O, L, M, Cl), 

pyrethrines (O, L, M), pyridaben (O, L, M, Cl, T), pyriproxifen (O, L, 

M), rotenone (O, L, M), spinosad (as bait) (O, L, M, Cl, SO, C, G, B, 

T), spirodiclofen (O, L, M, Cl, G, B, C, SO), tebufenozide (O, L, M), 

tebufenpyrad (O, L, M, Cl, G, C, T, B), thiamethoxam (O, L, M, Cl), 

trichlorfon (O, L, M) (4), zeta-cypermethrin (O, L) 

Acetamiprid (O, L, M, and nurseries, G, C), azadirachtin (O, L, M, G), 

Bacillus thurigiensis var. aizawai (O, L, M, G, C), Bacillus 

thuringiensis var. kurstaki (O, L, M, G, C), Beauveria bassiana (M), 

buprofezin (O, L, M, G, SO, C), chlorpyrifos (O, L, M, G, P), 

chlorpyrifos-methyl (O, L, M), cypermethrin (O, M,G), deltamethrin 

(O, L, M, G, C, P), diflubenzuron (O, L, M, G, P), fatty acid potassium 

salt (O, L, M, G, C), fenoxycarb (O, L, M), flucythrinate (O, L, M, G), 

flufenoxuron (O, L), imidacloprid (O, L, M, G), methomyl (O, L, M, 

P), methoxyfenozide (O, M, G), mineral oil (O, L, M, G, SO, P), 

phosmet (O, L, M, G), pirimicarb (O, L, M, G, P), pymetrozine (O), 

pirimiphos-methyl (M), pyrethrins (O, L, M, G), pyriproxyfen (O, L, 

M), tau-fluvalinate (O, L, M, G), tebufenozide (L, M), thiamethoxam 

(O, L, M) 

Insect attractants: farnesol (O, L, M, G), nerolidol (O, L, M, G) 

O: Orange, L: Lemon, M: Mandarin, G: Grapefruit, SO: Sour orange, C: Citron, P: Pomelo, Cl: 

Clementine, T: Tangerine, B: Bergamot. 1 = Active substance not included in the Annex I of the 

directive 91/414/EC, the commercial plant production products are revoked from 6 December 2007 

and the stocks were commercialized and used until 6 December 2008. 2 = Use allowed only on 

nonproductive orchards. For some commercial plant production products the extension of the 

authorization for use on citrus to control aphids has been approved with a pre-harvest interval of 100 

days. 3 = Active substance not included in the Annex I of the directive 91/414/EC. The 

authorization of the commercial plant production products containing phosalone is revoked from 23 

June 2007. The stocks were commercialized and used until 22 June 2008. 4 = Active substance not 

included in the Annex I of the directive 91/414/EC. The authorization of the commercial plant 

production products containing this a.i. is revoked from 21 November 2007. The stocks were 

commercialized and used until 21 November 2008.


Table 7. Insecticides, acaricides and insect attractants (active substances) registered for use 

against the main arthropod pests of citrus in Spain, Italy and Greece (June 2008). 

Pest 

Thrips (Thysanoptera) 

Whiteflies (Aleyrodidae) 

Aleurothrixus floccosus 

Dialeurodes citri 

Aphids (Aphididae) 

Aphis gossypii 

Aphis spiraecola 

Toxoptera aurantii 

Toxoptera citricida 

Armoured scales (Diaspididae) 

Aonidiella aurantii 

Aspidiotus nerii 

Chrysomphalus dityospermi 

Lepidosaphes beckii 

Parlatoria pergandei 

Parlatoria ziziphi 

Unaspis citri 

Soft scales (Coccidae) 

Ceroplastes sinensis 

Coccus hesperidum 

Saissetia oleae 

Insecticides/acaricides (active substance) a 

Acrinathrin (I), chlorpyrifos (G), fatty acid potassium salt 

(G), malathion (I), pirimiphos-methyl (I), rotenone (I) 

Acetamiprid (S), azadirachtin (S, G), buprofezin (S, G), 

carbosulfan (S), chlorpyrifos (S), cypermethrin (I), 

deltamethrin (I), dimethoate (S), etofenprox (S), fatty acid 

potassium salt (G), fenazaquin (S, I), fenpyroximate (S), 

imidacloprid (S, I, G), lufenuron (S, I), malathion (S, I), 

methomyl (S), mineral oil (G), phosmet (S), piridaben (S), 

pyrimiphos-methyl (S), rotenone (I), zeta-cypermethrin (I) 

Acetamiprid (S, G), alpha-cypermethrin (S), azadirachtin 

(S, G), benfuracarb (S), bifentrin (S), carbosulfan (S), 

chlorpyrifos (S, G), chlorpyrifos-methyl (G), 

cypermethrin (S, I, G), deltamethrin (S, I), dimethoate (S), 

etofenprox (S), fatty acid potassium salt (G), fenitrothion 

(S), flucythrinate (G), fluvalinate (I), imidacloprid (S, I), 

lambda-cyhalothrin (I), malathion (I), methomyl (S), 

mineral oil (S, G), oxamyl (G), oxydemeton-methyl (S), 

phosmet (S), pimetrozine (S, I), pirimicarb (S, I,G), 

pyrimiphos-methyl (S, I), potassium salts of vegetable 

fatty acids (S), pymetrozine (G), pyrethrines (G), rotenone 

(I), tau-fluvalinate (S), thiamethoxam (I, G), zetacypermethrin 

(I) 

Azadirachtin (S), buprofezin (S, G), chlorpyrifos (S, G), 

chlorpyrifos-methyl (G), cypermethrin (I, G), 

flucythrinate (G), dimethoate (S), fenitrothion (S), 

fenoxycarb (S), fenpyroximate (S), malathion (S, I), 

methomyl (S, I), mineral oil (S, I, G), phosmet (S, I, G), 

pyrimiphos-methyl (S), pyriproxifen (S, I, G), rotenone (I) 

Azadirachtin (S), buprofezin (S), chlorpyrifos (S, G), 

chlorpyrifos-methyl (G), cypermethrin (S, I, G), 

deltamethrin (I), dimethoate (S), fenitrothion (S), 

fenoxycarb (S, G), fenpyroximate (S), flucythrinate (G), 

imidacloprid malathion (S), malathion (I), methomyl (S, 

I), mineral oil (S, I, G), phosmet (S, I), pyriproxifen (S, I, 

G), pyrimiphos-methyl (S), rotenone (I), tau-fluvalinate 

(S)

24 



Mealybugs (Pseudococcidae) 

Planococcus citri 

Moths 

Phyllocnistis citrella 

(Gracillariidae) 

Prays citri (Hyponomeutidae) 

Fruit flies (Tephritidae) 

Ceratitis capitata 

Mites 

Eutetranychus banksi 

Panonychus citri 

Phyllocoptruta oleivora 

Tetranychus urticae 

Azadirachtin (S), buprofezin (S, G), chlorpyrifos (S, G), 

cypermethrin (I, G), dimethoate (S), fenitrothion (S), 

flucythrinate (G), malathion (S, I), methomyl (S, I), 

mineral oil (S, I, G), phosmet (S, I, G), pyrimiphos-methyl 

(S, I), rotenone (I) 

Abamectin (S, I: P. citrella), acetamiprid (G: P. citrella 

nurseries), alpha-cypermethrin (S), azadirachtin (S, G: P. 

citrella), Bacillus thuringiensis var. aizawai (G: P. citri), 

Bacillus thuringiensis var. kurstaki (S, G: P. citri), 

benfuracarb (S), buprofezin (P. citrella), carbosulfan (S), 

chlorpyrifos (S, G), cypermethrin (S, I: P. citri, G), 

deltamethrin (S), diazinon (S), dichlorvos (S), 

diflubenzuron (S) dimethoate (S), etofenprox (S), 

fenitrothion (S), fenoxycarb (S), fenpyroximate (S), 

flucythrinate (G: P. citri), flufenoxuron (S, I, G: P. 

citrella), imidacloprid (S, I, G: P. citrella), lufenuron (S, 

I), malathion (S, I), methomyl (S, I), methoxyfenozide (I, 

G: P. citrella), mineral oil (G), phosmet (S, I), 

pyrimiphos-methyl (S, I), rotenone (I: P. citri) taufluvalinate 

(S), tebufenozide (S, I, G: P. citrella), 

thiamethoxam (I, G: P. citrella) 

Azadirachtin (S), Beauveria bassiana (G), cypermethrin 

(I, G), deltamethrin (I), dichlorvos (S), etofenprox (I), 

flucythrinate (G), imidacloprid (S), lambda-cyhalothrin 

(S, I), lufenuron (S), malathion (S, I), phosmet (S, I, G), 

pyrimiphos-methyl (I), rotenone (I), spinosad bait (I), 

trichlorfon (S, I), zeta-cypermethrin (I) 

Abamectin (S, I: T. urticae), acrinathrin (I), bifentrin (S), 

buprofezin (S), clofentezine (S, I), dicofol (S, I, G), 

etoxazol (S, I, G), fenazaquin (S, I, G), fenbutatin oxide 

(S, I, G), fenitrothion (S), fenpyroximate (S, I), 

flufenoxuron (S, I), hexythiazox (S, I), malathion (S), 

mineral oil (S, I, G), oxamyl (G), oxydemeton-methyl (S), 

propargite (S, I, G), pyridaben (S, I), pyrimiphos-methyl 

(S, I), spirodiclofen (I), tebufenpyrad (S, I, G) 

a 

G = Greece; I = Italy; S = Spain.


Table 8. Side effects of pesticides (active substances ), registered for the control of citrus 

a 

pests, on beneficial arthropods . 

Active substance 

Rodolia 

cardinalis 

Cryptolaemus 

montrouzieri 

Euseius 

stipulatus 

Lysiphlebus 

testaceipes 

Leptomastix 

dactylopii 

Cales noacki 

Abamectin 1 3–4 2–3 3–4 

Azadirachtin 3–4 1 1 1 3–4 

Bacillus thuringiensis 

var. kusrtaki 

1 1 1 1 1 1 

Benfuracarb 1 2–3 

Bifentrin 3–4 3–4 1 

Buprofezin 1–2 3 1–2 1 1–2 1 

Carbosulfan 1–2 1–2 1 2–3 

Chlorpyrifos 1–2 2 2 3 3 2–3 

Chlorpyrifos-methyl 1 1 3 3 2–4 1–2 

Clofentezine 1 2 1–2 1 

Cypermethrin 4 4 4 1 3–4 

Deltamethrin 4 3–4 4 1 4 3 

Diazinon 3 2 3 1–2 

Dicofol 1 1–4 3–4 1 3–4 2 

Diflubenzuron 1 1–2 

Dimethoate 1 4 2–3 1–2 4 2 

Fenazaquin 4 2 4 3 

Fenbutatin oxide 1 2 1 1 1 

Fenitrothion 1–2 3 1–2 4 3 

Fenoxycarb 4 1–2 2 

Flucythrinate 2 3 

Flufenoxuron 2–3 1–2 

Fosalone 2 1 3 

Hexythiazox 1 1 1 

Imidacloprid 4 2–3 1 4 3 

Lambda-cyhalothrin 3 

Lufenuron 4 1 1 1 

Malathion 2–3 4 2 3 4 3–4 

Methomyl 4 4 4 2 3–4 

Mineral oil 1 1–2 1–2 2 1 1–4 

Oxydemeton-methyl 1 3 2 1 3 1–2 

Phosmet 4 4 2–3 1 3 4 

Piridaben 4 1 

Pirimicarb 1–2 2 1–2 1 1 1 

Pyrimiphos-methyl 1–2 1–2 1–4 4 3–4 

Propargite 4 1 2–3 

Pyriproxifen 4 4 1 1–2 2–3 

Spinosad 1 1 4 3–4

26 



Tau-fluvalinate 4 3 3–4 1 3 2 

Tebufenozide 1 

Tebufenpyrad 2 

Trichlorfon 2–3 1 1 3 1–2 2 

Zeta-cypermethrin 4 4 4 1 3–4 

a Classification according to the IOBC WG “Pesticides and Beneficial Organisms” standards: 1 = 

harmless; 2 = slightly harmful; 3 = moderately harmful; 4 = harmful (sources: Jacas & García Marí, 2001; 

Pascual-Ruíz & Urbaneja, 2006; Urbaneja et al., 2008; Suma, Zappalà, Mazzeo, & Siscaro, 2009). 

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Beardsley, J. W., AliNiazee, M. T. & Watson, T. F. (1979). Sampling and monitoring. In D. W. Davis, 

S. C. Hoyt, J. A. McMurty, & M. T. AliNiazee (Eds.), Biological control and insect pest 

management (pp. 11–22). California: University of California, Division of Agricultural Sciences. 

Cavalloro, R., & Prota R. (Eds.) (1983). Proceedings of the E.C. Experts’ Meeting Integrated Control in 

Citrus: Comparison of results achieved by applying a standardized methodology (pp. 39–42). 

Siniscola-Muravera, 20–22 October 1982. 

CEC [Council of the European Communities]. (1991). Council directive of 15 July 1991 concerning the 

placing of plant protection products on the market. http://europa.eu/eur-lex/en/consleg/pdf/1991/ 

en_1991L0414_do_001.pdf 

De Bach, P. (1964). Biological control of insect pests and weeds. London: Chapman and Hall Ltd. 

El-Otmani M., Srairi I., & Benhaddou, A. (2007). National citrus sector analysis: Morocco. 

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quality and safety. Available at: http://www2.spi.pt/euromedcitrusnet/Documents/Sector%20- 

Analysis%20Report/EuroMedCitrusNet%20Sector%20Analysis%20Report-Morocco.pdf 

EPPO [European and Mediterranean Plant Protection Organization]. (2007). EPPO A1 and A2 lists of 

pests recommended for regulation as quarantine pests. September 2007. Available at: 

http://archives.eppo.org/EPPOStandards/PM1_GENERAL/pm1-02(16)_A1A2_2007.pdf 

Franco, J. C., García-Marí, F., Ramos, A. P., & Besri, M. (2006). Survey on the situation of citrus pest 

management in Mediterranean countries. IOBC/wprs Bulletin, 29(3), 335–346. 

Gomes da Silva, R., Borges da Silva, E., & Franco, J. C. (2006). Parasitoid complex of citrus leafminer 

on lemon orchards in Portugal. IOBC/wprs Bulletin, 29(3), 197–204. 

Hellenic Ministry of Rural Development and Food. (2008). Authorized plant protection products data 

base. http://www.minagric.gr/syspest/ 

IOBC/WPRS Commission “IP Guidelines and Endorsement”. (2004). Guidelines for integrated 

production of citrus. http://www.iobc.ch/IOBC_Citrusguideline_english_definitive.pdf 

ISTAT [Istituto Nazionale di Statistica]. (2007). Dati annuali sulle coltivazioni. Available at: 

http://www.istat.it/agricoltura/datiagri/coltivazioni/anno2007/ital2007.htm 

Jacas, J. A., & García-Marí, F. (2001). Side-effects of pesticides on selected natural enemies occurring in 

citrus in Spain. IOBC/wprs Bulletin, 24, 103–112. 

Jacas, J. A., Urbaneja, A., & Viñuela, E. (2006). History and future of introduction of exotic arthropod 

biological control agents in Spain: A dilemma? BioControl, 51, 1–30. 

Kalaitzaki, A. P., (2004). Study of biological parameters of parasitoids of Phyllocnists citrella Stainton 

and their impact on the dynamic of its population. PhD Thesis, Agricultural University of Athens. 

Katsoyannos, P. (1996). Integrated insect pest management for citrus in northern Mediterranean 

countries. Benaki Phytopathological Institute, Athens, Greece. 

Laajimi, A., & Ben Mimoun, M. (2007). National citrus sector analysis: Tunisia. Euromedcitrusnet 

Project, Deliverable 9. The European Union 6th Framework Programme, Food Quality and Safety. 

http://www2.spi.pt/euromedcitrusnet/Documents/Sector%20Analysis%20Report/EuroMedCitrusNet 

%20Sector%20Analysis%20Report-Tunisia.pdf


Malausa, J. C., Rabasse, J. M., & Kreiter, P. (2008). Les insectes entomophages d’intérêt agricole acclimatés 

en France métropolitaine depuis le début du 20 ème siècle. Bulletin OEPP/EPPO, 38, 136–146. 

MAPA [Ministerio de Agricultura, Pesca y Alimentación]. (2007). Anuario de Estadística Agraria. 

Madrid, Spain. 

MAPA. (2008). Registro de productos fitosanitarios. http://www.mapa.es/es/agricultura/pags/fitos/ 

registro/menu.asp 

MiPAAF [Ministero delle Politiche Agricole, Alimentari e Forestali]. (2008). Banca Dati Fitofarmaci. 

Centro di Ricerca per la Patologia Vegetale, Roma. http://www.sian.it/fitovis/ 

Noyes, J. S., & Hayat, M. (1994). Oriental parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). 

Oxon, UK: CAB International. 

Pascual-Ruiz, S., & Urbaneja, A. (2006). Lista de Efectos Secundarios de Plaguicidas sobre Fauna Útil en 

Cítricos. Levante Agrícola, 380, 186–191. 

Salama Eid, S. S, Latif, F., & Hassan E. (2007). National Citrus Sector Analysis. Euromedcitrusnet. 

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MedCitrusNet%20Sector%20Analysis%20Report%20-Egypt.pdf 

Siscaro, G., Caleca, V., Reina, P., Rizzo, M. C., & Zappalà, L. (2003). Current status of the biological 

control of the citrus leafminer in Sicily. IOBC/WPRS Bulletin, 26(6), 29–36. 

Siscaro, G., Di Franco, F., & Zappalà, L. (2008). On the presence and diffusion of Comperiella bifasciata 

How. (Hymenoptera: Encyrtidae) in Southern Italy. IOBC/wprs Bulletin, 38, 42–45. 

Suma, P., Zappalà, L., Mazzeo, G., & Siscaro, G. (2009). Lethal and sublethal effects of insecticides on 

natural enemies of citrus scale pests. BioControl, 54, 651–661. 

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and impact of introduced and native parasitoids on Phyllocnists citrella Stainton in Greece. 

Evaluating indirect ecological effects of biological control, global IOBC International Symposium, 

Montpellier, France, 17–20 October 1999. IOBC/wprs Bulletin, 22, 66. 

Urbaneja, A., Pascual Ruiz, S., Pina, T., Abad-Moyano, R., Vanaclocha, P., Montón, H., et al. (2008). 

Efficacy of five selected acaricides against Tetranychus urticae (Acari: Tetranychidae) and their 

side effects on relevant natural enemies occurring in citrus orchards. Pest Management Science, 64, 

834–842. 

Viggiani, G. (1975). La lotta biologica di tipo convenzionale. Atti del X Congresso Nazionale Italiano di 

Entomologia (pp. 161–187), Sassari 20–25 maggio 1974. 

Zappalà, L., Siscaro, G., & Longo, S. (2008). Establishment of Neodryinus typhlocybae (Ashmead) 

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2 

MAIN ARTHROPOD PESTS OF CITRUS CULTURE 

AND PEST MANAGEMENT IN GREECE 

§ 

FILITSA KARAMAOUNA, PANAGIOTIS MYLONAS, 

DIMITRIOS PAPACHRISTOS, DIMITRIOS KONTODIMAS, 

ANTONIOS MICHAELAKIS AND ELEFTHERIA KAPAXIDI 



Abstract. The key arthropod pests in the citrus producing areas in Greece comprise the Mediterranean 

fruit fly Ceratitis capitata, the California red scale Aonidiella aurantii and the citrus mealybug 

Planococcus citri. Outbreaks of the whiteflies Aleurothrixus floccosus and Dialeurodes citri, the scales 

Ceroplastes rusci and Saissetia oleae as well as the Tetranychidae mites Panonychus citri and 

Tetranychus urticae and the Eriophyiidae mites Aculops pelekassi and Aceria sheldoni may occur 

locally. The citrus leafminer Phyllocnistis citrella, aphids (Aphis spiraecola, A. gossypii, Toxoptera 

aurantii) and thrips (Heliothrips haemorrhoidalis, Pezothrips kellyanus) are of minor importance. The 

problems due to major and minor citrus pests and control measures in Greece are reviewed and 

Integrated Pest Management (IPM) strategies are recommended. 


The total citrus-producing area in Greece is 57,525.6 hectares (ha). The most 

widely cultivated Citrus species include orange Citrus sinensis (L.) Osbeck 

(40,054 ha), lemon Citrus limon Burman f. (10,497 ha), mandarin Citrus reticulata 

Blanco (6,514 ha), grapefruit Citrus paradisi Macfadyen (340 ha), citron Citrus 

medica L. (100 ha), bergamot Citrus bergamia Risso (12 ha), bitter orange Citrus 

aurantium L. (7.82 ha) and pumelo Citrus maxima (Burm) Merrill (0.78 ha) 

(Hellenic Ministry of Rural Development and Food, 2006, Unpublished data). 

Major arthropod pests in terms of importance in the citrus-growing regions of the 

country comprise the Mediterranean fruit fly Ceratitis capitata (Wiedemann) 

(Diptera: Tephritidae), the California red scale Aonidiella aurantii (Maskell) 

(Hemiptera: Diaspididae) and the mealybug Planococcus citri (Risso) (Hemiptera: 

Pseudococcidae). However, outbreaks of the woolly whitefly Aleurothrixus 

floccosus Maskell (Hemiptera: Aleyrodidae), the citrus whitefly Dialeurodes citri 

§All authors contributed equally to this chapter. 




29

30 

F. KARAMAOUNA ET AL. 

(Ashmead) (Hemiptera: Aleyrodidae), Ceroplastes rusci L (Hemiptera: Coccidae), 

the Mediterranean black scale Saissetia oleae (Bernard) (Hemiptera: Coccidae) and 

Tetranychidae and Eriophyiidae mites are recorded at small (local) scale. The 

citrus leafminer Phyllocnistis citrella (Stainton) (Lepidoptera: Gracillariidae) and 

the citrus infesting aphids and thrips are of minor importance (Hellenic Ministry of 

Rural Development and Food and Regional Plant Protection Services, 2007, 

unpublished data). 

2. PEST STATUS AND CONTROL MEASURES 

An idea for the present status of the citrus arthropod pests in the citrus-producing 

areas of Greece can be obtained from an empirical risk assessment of the Hellenic 

Ministry of Rural Development and Food, which is based on data from the 

Regional Plant Protection Services of the Ministry (2007). A rank scale from 1 to 3 

is used (1 being the most serious pest to 3 being the less serious one) so that the 

citrus arthropod pest status is as follows: the Mediterranean fruit fly Ceratitis 

capitata (1–2); the California red scale Aonidiella aurantii (1–3); the mealybug 

Planococcus citri (1–3); the woolly whitefly Aleurothrixus floccosus (1–3); the 

citrus whitefly Dialeurodes citri (Ashmead) (Hemiptera: Aleyrodidae) (1) locally 

on the island of Crete; Ceroplastes rusci (1) locally in Argolis-Peloponnese; the 

Mediterranean black scale Saissetia oleae (1) locally in Argolis; the Tetranychidae 

mites Panonychus citri and Tetranychus urticae (1–3) locally in Peloponnese; the 

Eriophyiidae mites Aculops pelekassi and Aceria sheldoni (1–3) locally in Argolis– 

Peloponnese and the western mainland; the citrus flower moth Prays citri Milliére 

(Lepidoptera: Hyponomeutidae) (2); the purple scale Lepidosaphes beckii 

(Newman) (Hemiptera: Diaspididae) (2) locally in Argolis; the rose tortrix moth 

Archips rosanus (Lepidoptera: Tortricidae) locally in Argolis; the citrus leafminer 

Phyllocnistis citrella (2–3); Citrus infesting aphids (2–3) and thrips (3) locally in 

Achaia-Peloponnese (Hellenic Ministry of Rural Development and Food and 

Regional Plant Protection Services, 2007, unpublished data). 

A forecasting/warning system concerning infestation by the main insect pests of 

the most important crops in the country, including Citrus, operates by the Regional 

Plant Protection Services of the Hellenic Ministry of Rural Development and Food. 

Forecasting of infestation is based on meteorological data, monitoring by trapping 

or sampling, historical and other data sources (literature, agronomists/consultants/ 

farmers files). Instructions for preventive plant protection measures are provided to 

the citrus growers when there is an issue of warning (Table 1). 

A review of the problems and the control measures for the main citrus arthropod 

pests in Greece i.e. the Mediterranean fruit fly Ceratitis capitata, scale insects 

(especially A. aurantii and P. citri), whiteflies (especially A. floccossus), the citrus 

leafminer P. citrella, aphids, the citrus flower moth P. citri, thrips and mites will 

be presented in the following sections.

IPM OF CITRUS PESTS IN GREECE 

31 

Table 1. Citrus arthropod pests for which plant protection instructions are provided by the 

Regional Plant Protection Services in conventional citrus culture in Greece. 

Arthropod pest Meteo data Monitoring by 

trapping/ 

sampling 

Historical 

data 

Other data a 

Ceratitis capitata Y Y/Y Y Crete: Lit, A, F 

Aonidiella aurantii Y Y/Y Y Achaia: Population 

Prediction Model 

Crete: Lit, A, F 

Planococcus citri Y Y/Y Y Achaia: Population 

Prediction Model 


Aleurothrixus 

floccosus 

N except 

Crete 

N/Y 

Y in most 

areas 


Dialeurodes citri a Y N/Y Y Crete: Lit, A, F 

Ceroplastes rusci a N N/Y Y N 

Saissetia oleae a N N/Y Y N 

Mites 

Ν except 

Argolis 

N/Y N except 

Argolis 

N 

Prays citri 

Y in some 

areas 

Y in some 

areas/Y 

Lepidosaphes 

Y N/Y Y N 

beckii a 

Citrus aphids 

Phyllocnistis citrella 

N except 

Crete 

N except 

Crete 

N/Y 

N/Y 

Y 

Ν except 

Crete 

Y in some 

areas 

N 



Thrips b N N/Y N N 

a Y = Yes; N = No; Lit = Literature, A = Agronomists, F = Farmers. Source: Hellenic Ministry of Rural 

Development and Food and Regional Plant Protection Services (2006). 

b The pests cause problems in certain regions and data refer to those regions. 

2.1. The Mediterranean Fruit Fly, Ceratitis capitata 

The Mediterranean fruit fly (medfly) Ceratitis capitata was first recorded in 

Greece by Papageorgiou in 1915 on infested citrus orchards in Attica and on the 

island of Aegina. Until today the presence of the medfly is reported almost all over 

Greece, except the highlands of the continental country and the lowland of the 

northwestern region. It infests mainly citrus fruits, pears, apples, peaches, apricots 

and figs and can cause serious yield losses (Tzimos, 1961; Mourikis, 1965;

32 


Michelakis, 1992; Zervas, Kateva, & Christopoulos, 1995; Papadopoulos & 

Economopoulos, 1997a; Katsoyannos, Kouloussis & Carey, 1998; Papadopoulos, 

1999; Papachristos, 2007). 

Adults of medfly are active from late spring until early winter and they are very 

abundant from the beginning of August until the end of October; they remain 

inactive or below detectable levels throughout the rest of the year (Zervas et al., 

1995; Katsoyannos et al., 1998; Papadopoulos, 1999; Papachristos, 2007). 

However, in the southern part of the country (the island of Crete) the adults are 

active during winter (Mavrikakis, Economopoulos, & Carey, 2000). Larvae inside 

the infested fruits and pupae in the soil are the main stages of overwintering in the 

north whereas in Crete it appears that the medfly overwinters in all development 

stages (Mourikis, 1965; Zervas et al., 1995; Papadopoulos, Carey, Katsoyannos, & 

Kouloussis, 1996; Katsoyannos et al., 1998; Papadopoulos, 1999; Mavrikakis 

et al., 2000). Moreover, patterns of fluctuation of adult population size may be 

varying significantly even in the same region depending on the host plant 

composition and availability (Katsoyannos et al., 1998). Although the precise 

determination of C. capitata generations is difficult because of a high overlapping 

between them, it is considered that C. capitata completes 5–7 generations 

depending on the region and the year (Mourikis, 1965). 

Infestation of citrus fruits starts as soon as they begin to ripen and continues until 

they are completely ripe. Among the main citrus species, the most susceptible one is 

bitter orange, followed by orange, whereas lemon seems to be immune (Katsoyannos 

et al., 1998; Mavrikakis et al., 2000; Papachristos, 2007). In most areas of Greece the 

late autumn ripening oranges escape heavy infestation because the medfly is not active 

at the particular season (Katsoyannos et al., 1998; Papachristos & Papadopoulos, 2009). 

Today the control of the medfly is mainly carried out with the use of pesticides 

(Economopoulos, 1996). Mass trapping as well as the sterile insect technique have 

also been applied with success (Zervas, Christopoulos, & Kateva, 1997; 

Economopoulos et al., 1996). 

2.1.1. Monitoring 

Detection and population monitoring of C. capitata is based on trapping of adults. A 

wide variety of traps and trophic, optical and sexual attractants are used in trapping of 

the medfly, which serves for monitoring of population or for pest control. 

Jackson traps baited with the male specific parapheromone trimedlure are 

specialized for capturing males of C. capitata but these traps have low accuracy in 

low population densities (Katsoyannos et al., 1998). The International Pheromone 

Plastic McPhail trap (IPMT), baited with a water solution of a protein hydrolysate 

(9%) and borax (3%) added as a preservative, is the most common method for 

capturing female and male adults (Katsoyannos, 1994). Another trapping method 

using the IPMTs and the food attractants ammonium acetate (AA), 1,4 

diaminobutane (putrescine) and trimethylamine (TMA) (Katsoyannos, 

Papadopoulos, Hearth, Hendrichs, & Kouloussis, 1999a, 1999b) have been proved 

effective even at low and medium population levels of the medfly. In recent


33 

experiments it was shown that putrescine may be excluded from the traps when 

monitoring established populations of C. capitata (Heath, Epsky, Midgarden, & 

Katsoyannos, 2004). 

Monitoring of C. capitata by adult trapping is advised to be supported with 

systematic fruit collection especially by the most suceptible citrus species. Fruit 

sampling is considered to be an efficient warning system for early detection of the 

fly (Katsoyannos et al., 1998). 

2.1.2. Mass Trapping 

The method of mass trapping has been applied successfully in orange orchards 

(Zervas et al., 1997). Traps of reversed cup type (Zervas, 1994) baited with 

parapheromone trimedlure were used to attract males and the modified McPhail 

trap IPMT, baited with 9% food lure (hydrolyzed protein, Dacus bait) in water 

with the addition of 3% borax were used to attract females. Attracted medflies 

were killed by the insecticide methomyl. Male capturing traps were placed on 

orange trees at the first fortnight of September (one trap every second tree) 

whereas the female capturing traps were placed on orange trees 10 days later (one 

trap every third tree). 

Aiming at the reduction of cost at the use of traps in mass trapping, Zervas 

(1994) developed three types of low cost and easy to handle medfly traps using a 

local market material. Efficacy of the new traps was similar to the commonly used 

traps. Two types of these traps were based on the utilisation of reversed plastic 

cups with trimedlure on cotton rolls as a male attractant and sugar mixted with the 

insecticide methomyl as a killing agent. In the third type a transparent bottle was 

used with a food lure (9% water solution of protein hydrolysate and 2% borax). 

Due to the easy manufacture and low cost, the last trap type is used with various 

modifications (i.e. in a lot of cases the fertilizer sulfur ammonium is placed instead 

of protein hydrolysate as a food attractant) by a lot of farmers for the mass trapping 

of medfly. 

Moreover, a variety of traps (yellow plastic spheres, flat yellow plates of plastic 

or wood, delta, glass McPhail, plastic McPhail, paper folded traps, paper envelope 

etc) combining visual, food and sexual stimuli have been evaluated in commercial 

citrus orchards with promising results (Michelakis, 1988; Liaropoulos et al., 2003; 

Katsoyannos & Papadopoulos, 2004). 

2.1.3. Biological Control 

Despite the long history of medfly in Greece, not enough data exist regarding the 

presence of native parasitoids or the establishment of exotic parasitoids that have 

been introduced in commercial citrus orchards for biological control. Older efforts 

for introduction and release of parasitoids were unsuccessful. Specifically, 

Dirhinus giffardii Silvestri (Hymenoptera: Chalcididae) was introduced but was 

not recovered (Argyriou, 1969). Test release of Opius concolor Szepligeti 

(Hymenoptera: Braconidae) on citrus showed that the parasitoid did not parasitize

34 


medfly in the field although it developed on medfly under laboratory conditions 

(Argyriou, 1969). 

Recently the presence of the parasitoid Aganaspis (Trybliographa) daci (Weld) 

(Hymenoptera: Eucoilidae) was recorded on infested figs on the island of Chios 

(Papadopoulos & Katsoyannos, 2003, 2007). The parasitoid exhibits high 

parasitism levels on medfly pupae in the field. Until today it is not known whether 

A. daci parasitizes C. capitata larvae in plant hosts other than figs or whether it is 

established in other areas of Greece. No parasitoids were found in samplings of 

medfly pupae in sweet oranges in Chios (Papadopoulos & Katsoyannos, 2007). 

Nevertheless, parasitism of C. capitata by A. daci can be an important factor for 

medfly control in citrus orchards in Greece as figs are one of the most important 

hosts contributing to the built up of C. capitata populations in late summer and 

early autumn (Katsoyannos et al., 1998; Papadopoulos, Katsoyannos, Carey, & 

Kouloussis, 2001). 

2.1.4. Cultural Practices 

The succession of host fruits and their availability throughout the year is of high 

importance in determining overall population levels of the med fly. Thus collecting 

and destroying infested fruits fallen on the ground is advised as a control strategy 

(Katsoyannos, 1996a). In citrus orchards, the presence of bitter orange and fig 

trees, which are found scattered inside or at the periphery of the orchards, seem to 

have an important role in C. capitata population dynamics (Katsoyannos, 1983; 

Katsoyannos et al., 1998; Papachristos, 2007). Early in the season (May to 

August), the rate of population built-up depends on the availability of mature bitter 

oranges whereas later in the season on the presence of figs. In addition, bitter 

oranges and figs are highly attractive for C. capitata and seem to keep females 

from attacking nearby hosts and dispersal (Katsoyannos, 1983; Katsoyannos et al., 

1998). Elimination of these fruits or their utilization as traps on the trees can 

contribute in an integrated management programme of C. capitata. 

2.1.5. Biotechnical Methods 

The sterile insect technique (SIT) is considered as an environmental friendly and 

effective control method for Tephritids fruit flies. An attempt to control C. capitata 

with SIT was performed in the valley of Fodele – Crete with encouraging results 

(Economopoulos et al., 1996; Papadopoulos & Economopoulos, 1997b). 

2.1.6. Chemical Control 

Cover and bait sprayings are the main control methods of medfly in Greece 

(Economopoulos, 1996). The sprays may be applied empirically based on the time 

of the year (Liaropoulos et al., 2003) or on systematic observations and monitoring 

of insect populations. Usually the bait sprays are applied from the ground using 

conventional sprayers and cover part of each tree or part of each two or three trees.


35 

A food attractant, mainly a compound that releases ammonia, is added in the 

pesticide solution. 

The timing of spray applications is determined by monitoring medfly population 

with traps, which are hanged on citrus trees a few weeks before fruits begin to 

mature. The monitoring of adult population may take place at field or region scale. 

Trap networks for monitoring C. capitata population have been installed and 

operate in some areas of Greece by the Regional Plant Protection Services so 

forecasting of infestation is possible based on trap captures and environmental 

conditions and warnings are released to the growers when necessary. Although 

treatment application thresholds against medfly have not been established at 

national level, those suggested by Katsoyannos (1996a) are applied in many cases 

(20 adults/trap/week in autumn on clementines approaching ripeness, 40–50 

adults/trap/week in autumn on oranges (pre-ripe and ripe stages), 10 

adults/trap/week in spring on late ripening varieties). 

When no monitoring is performed, sprayings are performed when the fruits reach 

maturity whereas the number of applications depends on the region, the season and 

the variety of citrus fruits. A spray program for orange and mandarin, which was 

recommended by the Ministry of Rural Development and Food in the past and can 

be applied even today, if using other insecticides, involves the following actions: 

(a) For bait spraying, the first application is carried out 15 days before fruit 

ripening and is repeated at 5–7 days intervals. The spray solution consists of 2% 

protein (as an attractant) and 0.3% dimethoate or fenthion or 0.5% malathion. It is 

applied on hedges and bushes in the perimeter of the orchard, on the interior and 

the upper part of the trees, mainly on branches that do not bare fruits (b) For cover 

spaying, the first application is carried out at the beginning of ripening and spraying 

may be repeated after 20 days depending on the prevailing enviromental conditions 

and the time of fruit harvest. The spray solution consists of 0.03% dimethoate or 

fenthion or other organophosphorate insecticides (Anonymous, 1973). 

In most of the orange cultivated areas in Greece the bait sprayings applied for the 

control of Bactrocera oleae (Gmelin) also contribute to a significant reduction of 

the medfly populations (Economopoulos, 1996). The same attractants (salt of 

protein hydrolysates) as those for the medfly have been used in bait sprays for B. 

oleae together with organophophorate insecticides. Applications start early in the 

summer and they are continued until the end of autumn (Broumas, 1994). 

In some cases, spray solutions are applied on an artificial medium such as a 

gunny placed on a parallelepiped plastic plate which is hanged on trees branches 

(Economopoulos, 1996). Laboratory experiments by Mavrikakis, Remboulakis, 

and Economopoulos, (2003) showed that a type of a paper surface (Vioryl) baited 

with a water solution of protein hydrolysate (6%) had a better “attract and kill” 

performance on medfly than the gunny surface baited with the same food lure. The 

insecticide (active ingredient) used as a killing agent was spinosad in a proportion 

of 0.04% v/v and it was effective for a time period more than 5 weeks. 

Some of the former mentioned insecticidal active substances used for the control of 

medfly have been withdrawn after being re-evaluated (Directive 91/414/EEC) in 

the E.C. (fenthion, malathion). Currently, the insecticides which are authorized 

for use against medfly in Greece include Beauveria bassiana (mandarin),

36 


cypermethrin (lemon, grapefruit, mandarin, orange), flucythrinate (lemon, 

grapefruit, mandarin, orange) and phosmet (lemon, grapefruit, mandarin, orange) 

(Authorized Plant Protection Products Data Base of the Hellenic Ministry of Rural 

Development and Food, 2008). 

2.1.7. Recommended IPM Strategies 

In small size citrus groves, integration of cultural and chemical control of medfly is 

recommended whereas the biological, chemical and SIT methods may be 

integrated at citrus-growing areas in large scale. Collection and destroying of 

infested fruits fallen to the ground, fruits remaining on trees after harvest as well as 

fruits without commercial value (such as bitter oranges) are cultural practices of 

significant value in order to prevent medfly built-up population. Early population 

detection is crucial for a successful control thus monitoring with IPMT traps baited 

with AA and TMA supported by systematic fruit inspection especially of the most 

preferred host (bitter oranges) are required. Bait sprayings should be preferred to 

cover sprayings. The timing of bait spray application should be based on medfly 

monitoring and on treatment application threshold. As the available treatment 

application threshold is practically empirical there is still a demanding need for its 

accurate determination. 

2.2. Scale Insects 

Scale insects have always been on the top of the list of the economically important 

insect pests in citrus in Greece. Half of the most common insect pests in the Greek 

citrus orchards belong to the superfamily Coccoidea with the California red scale 

Aonidiella aurantii and the citrus mealybug Planococcus citri being the most 

frequently found ones among all. In addition, a number of less important species 

are known to cause local outbreaks. In the past, the Mediterranean black scale 

Saissetia oleae was considered to be a major pest but after the introduction and 

successful establishment of several exotic parasitoids, its population is kept below 

the economic injury level. At present, the Chinese wax scale Ceroplastes 

floridensis and the cottony-cushion scale Icerya purchasi can cause local outbreaks 

in specific regions in Peloponnese (Stathas, personal communication) whereas high 

populations of Ceroplastes rusci, Lepidosaphes beckii and Saissetia oleae are 

occasionally recorded too (Hellenic Ministry of Rural Development and Food, 

2007, unpublished data). 

Although considerable effort has been imposed to develop sustainable control 

methods of scale insects based on the use of biological control agents and the 

minimization of the use of chemical pesticides, spraying with insecticides is still 

used for the control of scale insects in citrus. Currently the most common practice 

in control of main scales of citrus is spray applications following the forecasts and 

instructions issued by the Regional Plant Protection Services, which are based on 

population monitoring with traps and/or visual observations.


37 

2.2.1. Sampling and Monitoring 

An efficacious monitoring system is prerequisite for having a successful 

forecasting/warning system for citrus scale insects. A number of monitoring tools 

are available for citrus scales, which are used in Greece. Sex pheromone traps are 

utilized for the detection, monitoring and forecasting outbreaks of the California 

red scale A. aurantii. White sticky sex-pheromone baited traps are used for 

monitoring purposes of other armoured scales. Pheromone traps are also available 

for the citrus mealybug P. citri. Field observations and sampling are necessary for 

the detection of other citrus scales. Various detailed sampling schemes have been 

proposed for this area of concern (Katsoyannos, 1996a). 


An extended trial has been directed toward classical biological control of citrus 

scales in the past so Greece is a good example of a country where native scale 

insects have been controlled by exotic natural enemies, both parasitoids and 

predators. Eleven parasitoid species have been introduced, seven of them providing 

sufficient control whereas several predators associated with classical biological 

control of scale insects are frequently present in the Greek citrus orchards. 

Five parasitoid species, Aphytis melinus DeBach, A. lingnanensis Compere, 

A. coheni De Bach Compere (Hymenoptera: Aphelinidae), Encarsia perniciosi 

(Tower) (Hymenoptera: Aphelinidae) and Comperiella bifasciata Howard 

(Hymenoptera: Encyrtidae) were introduced and released in field trials against 

A. aurantii between 1962 and 1970. A. melinus is the leading parasitoid targeting 

the California red scale but its efficacy is reduced in cases of outbreaks. 

Comperiella bifasciata had a minor establishment whereas A. lingnanensis and A. 

coheni failed to be established (Katsoyannos, 1996a). 

Aphytis lepidosaphes Compere and Aphytis melinus DeBach were established 

after introduction in 1962 and they sufficiently controlled L. beckii and 

Chrysomphalus dictyospermi Morgan (Hemiptera: Diaspididae) respectively, 

which were major pests of citrus in the past (Katsoyannos, 1996a). 

The parasitoid Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae) was 

released in Crete twice (in 1975 and 1981) for the control of the citrus mealybug 

P. citri but failed to get established (Katsoyannos, 1996a). Moreover, three 

coccinellid predators were introduced, Nephus reunioni (1977), Nephus sidi (1992) 

and Cryptolaemus montrouzieri Mulsant (several attempts: 1933, 1964, 1965, 

1969, 1977). Establishment of the Nephus spp. was not reported, however, C. 

montrouzieri Mulsant, which was the most effective of the three species, could not 

overwinter in most regions (Katsoyannos, 1996a). 

Four parasitoid species, Metaphycus helvolus Compere, M. bartletti Annecke & 

Mynhardt, M. swirskii Annecke & Mynhardt (Hymenoptera: Encyrtidae) and 

Diversinervus elegans Silvestri (Hymenoptera: Encyrtidae) targeted the control of 

Saissetia oleae with relatively sufficient results (Argyriou, 1986). The coccinellid 

predator Rhyzobius forestieri (Mulsant) was released 25 years ago on the island of 

Chios and it is now the most abundant coccinellid found in citrus orchards. The

38 


predator preys mainly on soft scales, such as S. oleae and Coccus 

pseudomagnoliarum (Kuwana) (Hemiptera: Coccidae), which maintain at 

acceptable levels (Katsoyannos, 1997). 

Populations of the cottony-cushion scale Icerya purchasi Kaussari (Hemiptera: 

Margarodidae) were regulated by the introduced coccinellid predator Rhodolia 

cardinalis Mulsant (Katsoyannos, 1996a). Localized outbreaks of the pest have 

been occurring until recently but nowadays the predator is available to the growers 

for augmentative releases. 

Besides the classical biological control, naturally occurring biological control is 

a widespread phenomenon in Greek citrus orchards. Many indigenous parasitoids 

and predators are found to parasitize and prey on citrus scale insects. Three 

indigenous parasitoids [Aphytis chrysomphali (Mercet), Aphytis chilensis Howard 

and Encarsia citrina (Craw)] and three predators [the coccinellids Rhyzobius 

lophanthae (Blaisdell) and Chilocolus bipustulatus (L.) and the nitidulid 

Cybocephalus fodori (Endrodi-Younga)] are the most common species that 

contribute to the suppression of the armoured scales in citrus, with the predator R. 

lophanthae being the most important one (Katsoyannos, 1996a). 

A considerable number of indigenous natural enemies are related to the control 

of the citrus mealybug; the parasitoids Anagyrus pseudococci (Girault) and 

Leptomastidea abnormis (Girault) (both Hymenoptera: Encyrtidae) along with the 

predators Nephus includens (Kirsch) and N. bisignatus (Boheman) (Coleoptera: 

Coccinellidae) contribute substantially to its control (Katsoyannos, 1996a; 

Kontodimas, Eliopoulos, Stathas, & Economou, 2004). Among the various 

parasitoid species associated with soft scales in citrus, Tetrastichus ceroplastae 

(Girault) (Hymenoptera: Eulophidae) and Scutellista cyanea Motschulsky 

(Hymenoptera: Pteromalidae) are the most frequent species that parasitize 

Ceroplastes rusci and C. floridensis Comstock (Katsoyannos, 1996a; Stathas, 

Kavallieratos, & Eliopoulos, 2003). 

In general citrus-infesting scale insects are adequately retained at low levels by 

the activity of introduced and/or native parasitoids and predators. However, in 

cases where locally outbreaks occur due to various factors, further action is needed 

to suppress the infestation below the economic injury level. Augmentative releases 

of natural enemies were performed in the past against the citrus mealybug P. citri 

and the soft scales S. oleae and C. pseudomagnoliarum using the coccinellid 

predators Cryptolaemus montrouzieri and Exochomus quadripustulatus (L.) 

respectively (Katsoyannos, 1996a). Presently augmentative releases are performed 

sporadically against P. citri using the coccinellid predators Nephus includens and 

N. bisignatus with very satisfying results, especially in organic citrus orchards. Growers 

occasionally use Rhodolia cardinalis to suppress local outbreaks of I. purchasi; the 

predator has been commercially available in the Greek market since 2006. 


Cultural techniques involve a series of modifications of the standard management 

practices in order to prevent or make the environment less favorable for the


39 

reproduction, dispersal and/or survival of scale insects. Reduced fertilizers input 

and irrigation regimes are conidered to moderate the susceptibility of the trees to 

scale insects infestation. Since scale insects are favored by low light and high 

humidity conditions, which are favoured by dense foliage, pruning of trees in 

spring should be regulated to enhance air movement and sunlight infusion into the 

canopy and hence to minimize survival and establishment of high populations of 

the pests in the orchards (Katsoyannos, 1996a). 


Chemical control of citrus scale insects following monitoring of the population 

with traps and visual observations is a common practice in Greece. Insecticides 

(active substances) authorized for use against the California red scale and the citrus 

mealybug in Greece include buprofezin (citron, lemon, grapefruit, mandarin, 

orange; only A. aurantii: bitter orange), chlorpyrifos (lemon, grapefruit, mandarin, 

orange, pumelo), cypermethrin (lemon, grapefruit, mandarin, orange), flucythrinate 

(lemon, grapefruit, mandarin, orange), paraffin oil (lemon, grapefruit, mandarin, 

orange, pumelo; only A. aurantii: bitter orange), petroleum oil (lemon, grapefruit, 

mandarin, orange), phosmet (lemon, grapefruit, mandarin, orange), pyriproxyfen 

(only A. aurantii: lemon, mandarin, orange) and white oil (lemon, grapefruit, 

mandarin, orange). Some of these active substances are registered for the control of 

other armoured scales and soft scales in citrus whereas chlorpyrifos-methyl and 

fenoxycarb are added in the pesticide list against Aspidiotus nerii (only 

chlorpyrifos methyl) and Saissetia oleae (Authorized Plant Protection Products 

Data Base of the Hellenic Ministry of Rural Development and Food, 2008). 


A good monitoring system that provides the necessary information for early scale 

detection and the status of natural enemies is essential for the selection of the 

sufficient control measures. In general, natural enemies provide adequate control of 

the citrus-infesting scales except in cases that outbreaks A. aurantii occur; the lack 

of an efficient predator against the California red scale makes it difficult to 

suppress the pest at high population levels. Therefore, conservation of existing 

natural enemies and augmentative releases of insectary-reared parasitoids and 

predators are very important in maintaining the scales population at low levels. 

Accessory cultural techiques (i.e. pruning in spring and moderate use of fertilizers 

and irrigation in summer) contribute in keeping the scale numbers low. In cases 

insecticide application is required (e.g. when widespread increase of the California 

red scale populations or the citrus mealybug outbreaks occur) one or two welltimed 

cover sprays may be applied by using selective insecticides. Less selective 

chemicals should be applied only spotted or in extreme situations on heavily 

infested areas of the grove (aiming also at the protection and conservation of 

natural enemies).

40 


2.3. Whiteflies 

Three exotic whitefly species have invaded Greece during the last three decades, 

the citrus whitefly Dialeurodes citri in 1973 (Pappas & Viggiani, 1979; Pappas, 

1981), the Japanese bayberry whitefly Parabemisia myricae (Kuwana) (Hemiptera: 

Aleyrodidae) in 1989 (Michalopoulos, 1989; Michelakis & Alexandrakis, 1989) 

and the woolly whitefly Aleurothrixus floccosus in 1991 (Katsoyannos, 1991), 

which caused considerable economic yield losses in citrus orchards especially in 

the early years after the invasion. Among the three species the woolly whitefly 

caused the most serious problems to the citrus growers. Woolly and citrus 

whiteflies are still considered to be main insect pests locally (Kalaitzaki, 

Alexandrakis, Varikou, & Pervolarakis, 2003; Kontodimas et al., 2005). However, 

all three species are excellent examples of efficient biological control in practice. 


The Japanese bayberry whitefly prefers to oviposit on incompletely expanded new 

leaves whereas woolly and citrus whiteflies prefer completely expanded but not yet 

dark green young leaves. In any case, sampling of infested young leaves and their 

examination under a stereoscopic microscope is necessary in order to assess the 

infestation level and the efficiency of any natural enemies (mainly the rate of 

parasitism). At the same time visual observation should be done in order to record 

the relative infestation intensity of the citrus trees. In addition, yellow sticky traps 

could considerably help to record the first flights of the whiteflies’ adults as well as 

to monitor the annual fluctuation of the population of whiteflies and their natural 

enemies. 

2.3.2. Biological Control and Cultural Practices 

All the whitefly species were exotic, hence their biological control was based on 

the introduction of their natural enemies, especially parasitoids (classical biological 

control). 

The control of Dialeurodes citri was achieved by the introduction of the 

parasitoid Encarsia lahorensis (Howard) (Hymenoptera: Aphelinidae) on the 

island of Corfu in 1976 (Pappas & Viggiani, 1979). By 1994, the parasitoid was 

well established and was found in almost all citrus orchards in the mainland 

(Katsoyannos, 1996a); it was also imported and released on the island of Crete in 

2003 (Kalaitzaki et al., 2003). 

Control of Parabemisia myricae was attempted with the parasitoid Eretmocerus 

deBachi Rose and Rosen (Hymenoptera: Aphelinidae), which was introduced and 

released in Crete in 1990 and 1991, but no data regarding its establishment are 

available (Katsoyannos, 1996a). However, the presence of P. myricae is rare after 

the introduction of E. deBachi. 

In case of Aleurothrixus floccosus, the parasitoid Cales noacki Howard 

(Hymenoptera: Aphelinidae) was introduced in 1991 and augmentation of its 

population in the insectary followed. During the years 1992–1995 more than 30


41 

million individuals of the parasitoid were released in more than 300 sites of citrusgrowing 

areas of the country. In most of these areas the control of the woolly 

whitefly was achieved during 1995 (infestation level 1 nymph/cm 2 ) of A. floccosus is 

recommended (Katsoyannos et al., 1998). 

Rearing of C. noacki in insectaries is suggested for augmentative biological 

control of A. floccosus, which in addition could serve as a useful deposit in case of 

invasion of the quarantine pest citrus blackfly Aleurocanthus woglumi Ashby 

(Hemiptera: Aleyrodidae) (A1 EPPO List).

42 


2.4. The Citrus Leafminer, Phyllocnistis citrella 

The citrus leafminer Phyllocnistis citrella was first recorded in Greece on the island 

of Rhodes (southeastern Greece) and in Crete in June 1995 (Anagnou-Vernoniki, 

1995; Michelakis & Vacante, 1997). More recordings of the pest followed on other 

Greek islands (Cos, Astipalea, Lesvos, Chios, Samos and Paros) and in the 

mainland (Attica and Laconia-Peloponnese) in July and August, 1995 (Anagnou- 

Vernoniki, 1995). After a few months the citrus leafminer was found in almost all 

citrus growing areas of Greece (Tsagarakis, Kalaitzaki, Lykouressis, Michelakis, & 

Alexandrakis, 1999). 

Upon introduction of the pest, quarantine and other regulatory measures were 

enforced but they had a very limited impact on the spread of the pest which very 

rapidly invaded all citrus cultivated areas in the state. The growers were advised 

not to overuse and/or misuse insecticides as experience from other countries had 

shown that the chemical control was a short term and expensive solution due to the 

long vegetative period of citrus and the large number of generations of citrus 

leafminer per year. Furthermore, chemicals would have unfavorable side effects on 

the existing effective biological control of other citrus pests and there was a 

possibility of resistance development of the citrus leafminer to insecticides. 

Nevertheless, many growers tried to apply insecticides but soon they had to 

admit that chemicals were an inadequate solution to the problem. Moreover, 

chemical control using broad spectrum insecticides was indeed putting at risk the 

Integrated Pest Management of citrus insect pests, such as scales and aphids as 

well as the successful biological control of the woolly whitefly Aleurothrixus 

floccosus by disruption of the newly established exotic parasitoid Cales noacki. 

Biological control, on the other hand, was known to be the most effective method 

of managing the citrus leafminer in commercial orchards (Hoy et al., 1995; Neale, 

Smith, Beattie, & Miles, 1995; Smith & Beattie, 1996; Argov & Rössler, 1996). 

Therefore the impact of the native natural enemies was studied and classical 

biological control by introduction and release of the most promising parasitoid 

species in two sites (Crete and Peloponnese) was attempted (Kalaitzaki, 2004). In 

addition cultural measures to prevent dispersal were strongly recommended by the 

agronomists/consultants to the citrus growers (Michelakis & Vacante, 1997). 

Early studies after the implementation of the classical biological control 

programme of the citrus leafminer in Crete showed that the number of immature 

individuals of the citrus leafminer/leaf fluctuated from 0.1–3.9 to 0.01–1.06 on 

orange trees and mandarin trees, respectively (with mandarin being more resistant to 

infestation) (Kalaitzaki, 2004). Five peaks of the live immature individuals of the 

citrus leafminer/leaf were recorded on orange trees (two in summer: end of May and 

mid June and three in autumn: end of September, end of October and mid November) 

and four peaks on mandarin trees (mid June, end of September, end of October, 

beginning of December) (Kalaitzaki, 2004). Lower levels of infestation (0.017–1.76 

live immature individuals/per leaf) were recorded in Argolis-Peloponnese, the second 

area of the parasitoids’ release (Tsagarakis et al., 1999). Later studies (2004 and 

2005) on the islands of Lesvos and Chios and in western mainland revealed low 

infestation of the citrus leafminer i.e. 0.06–0.58, 0.08–0.72 and 0.04–0.82 immature


43 

individuals/leaf respectively. As a final point the citrus leafminer causes problems 

particularly on young citrus trees and overgraftings in nurseries but its damage on 

adult trees under Mediterranean conditions lacks economic importance (Garcia-Marí, 

Granda, Zaragoza, & Agusti, 2002). 


Sampling for monitoring infestation by the citrus leafminer involves collection of 

new shoots and leaves from growth flushes and observation of mines. The 

economic threshold for a chemical application on citrus leafminer has been 

estimated by several researchers; in China it is 0.74 larvae/leaf (or percentage of 

leaf damage over 20%) (Huang & Li, 1989); in Australia it is fixed at 25% of 

shoots with leaves smaller than 3 cm exhibiting mines of L1 (Beattie & Smith, 

1993); in Florida it is set at 30% of young shoots baring mines with live larvae 

(sampling should be performed when half of the trees in the orchard have young 

shoots) (Knapp et al., 1995). 


Five exotic hymenopteran parasitoid species were introduced from Cyprus in 1996 

and were subsequently mass reared in the insectary of the Institute of Subtropical 

Crops and Olive (National Agricultural Research Foundation) in Chania-Crete. The 

introduced species were the encyrtid Ageniaspis citricola Logvinovskaya 

(Hymenoptera: Encyrtidae) and the eulophids Cirrospilus quadristriatus (Subba 

Rao and Ramamani), Citrostichus phyllocnistoides (Narayanan), Quadrastichus sp. 

and Semielacher petiolatus (Girault) (Hymenoptera: Eulophidae). A small number 

of all parasitoids were released in 1996 but cultures of Ageniaspis citricola and 

Cirrospilus quadristriatus could not be kept after the first year and hence these 

species did not establish (Kalaitzaki, 2004). 

Citrostichus phyllocnistoides, Quadrastichus sp. and Semielacher petiolatus were 

released systematically (100–250 individuals/species/10 days from June to November) 

in orange and mandarin orchards in Crete (Chania) and the impact of both native and 

introduced parasitoids was studied from 1997 to 1999. Similar releases were also 

performed in Peloponnese (Argolis, Korinthia, Lakonia) (Tsagarakis et al., 1999). 

All of the released parasitoid species established in Crete and contributed to the 

reduction of the citrus leafminer population, especially Citrostichus 

phyllocnistoides which dispersed very rapidely and far from the release sites and it 

achieved the highest percentage parasitism (mean 15.2–20.8% and maximum 45.8– 

51.1% on mandarin and orange trees, respectively). 

Only a few native parasitoid species were found to parasitize the citrus leafminer in 

Crete i.e. Pnigalio pectinicornis L., Neochrysocharis formosa (Westwood) and 

Cirrospilus pictus (Nees) (all Hymenoptera: Eulophidae) in very small numbers and 

with small contribution in percentage parasitism of the citrus leafminer (Kalaitzaki, 

Lykouressis, & Michelakis 1999; Kalaitzaki, 2004). Among them, P. pectinicornis was 

the most abundant one (Kalaitzaki et al., 1999; Kalaitzaki, Lykouressis, Perdikis, &

44 


Alexandrakis, 2007). Results of the second release site differ. Th e exoti c parasitoids 

C. phyllocnistoides and S. petiolatus were recovered whereas Quadrastichus sp. was not 

recovered (Tsagarakis et al., 1999). Although the population of C. phyllocnistoides 

increased with time after the release, the exotic parasitoid did not displace the native 

species N. formosa and P. pectinicornis. Neochrysocharis formosa was the most 

abundant parasitoid for a period of 3 years after the release (Tsagarakis & Lykouressis, 

2002; Tsagarakis, Kalaitzaki, Lykouressis, Michelakis, & Alexandrakis, 2003). 

Citrostichus phyllocnistoides has been found in almost all citrus producing areas in 

Greece (Kalaitzaki, 2004). 

The parasitoids Pnigalio sp., Cirrospilus sp., N. formosa and C. phyllocnistoides 

were collected at the areas of Marathonas-Attiki, Galatas-Trizinia and Skala-Lakonia in 

1999–2000 (Anagnou-Veroniki, Doukas, & Kontodimas, 2002), Pnigalio pectinicornis 

and Cirrospilus sp. were collected on the islands of Lesvos and Chios and in western 

mainland, as were N. formosa and C. phyllocnistoides (Papanikolaou, 2005). 

The list of native parasitoids expanded with the first recording of Pnigalio soemius 

(Walker) (Hymenoptera: Eulophidae) (Papanikolaou, 2005; Papanikolaou, 

Kavallieratos, Kontodimas, & Tomanovic, 2006) and Semielacher silvicola Boucek 

(Hymenoptera: Eulophidae) in Attica, in 2005 (Vamvakas, Anagnou-Veroniki, & 

Kontodimas, 2005). 


Cultural measures advised involve some changes of the standard management practices 

in order to prevent or make the environment less favorable for the pest reproduction, 

dispersal and/or survival. Decrease of fertilization and irrigation inputs should moderate 

the susceptibility of the new flush to the citrus leafminer during summer when the pest 

is very active. Moreover, fertilization, irrigation and pruning should be regulated to 

enhance discrete flush patterns over large areas, breaking generations overlap 

(Anagnou-Veroniki, Volakakis, & Gianoulis, 1995; Michelakis & Vacante, 1997). 


The application of insecticides to control the citrus leafminer is proved to be a 

short term solution especially for plant nurseries and newly grafted trees which 

suffer more from the pest infestation. 

The insecticides (active substances) which were initially recommended were 

fenoxycarb and diflubezuron in combination with summer oils. Only the external part 

of the trees, where the flushes and hence the citrus leafminer infestation occurs, 

should be sprayed with the solutions. Fenoxycarb showed no killing effects on 

C. noacki, the parasitoid of A. floccosus (Buchelos & Foudoulakis, 2000). Later on 

more selective insecticides i.e. chlorfenapyr, abamectin, flufenoxuron, azadirachtin, 

summer oils etc. were used (Michelakis & Vacante, 1997). 

Other insecticides added in the list were acephate, diazinon, dimethoate, 

methomyl, phospanidon, fenvalarate whereas their side effects on the natural 

enemies of the pest were illustrated (Anagnou-Veroniki et al., 1995).


45 

Today the list with the registered insecticides for use against the citrus leafminer 

in Greece includes acetamiprid, (in nurseries for lemon, mandarin and orange), 

azadirachtin (grapefruit, lemon, mandarin, orange), buprofezin (bitter orange), 

flufenoxuron (lemon, orange) imidacloprid (grapefruit, lemon, mandarin, orange), 

methoxyfenozide (mandarin, orange), paraffin oil (bitter orange), tebufenozide 

(mandarin) and thiamenthoxam (lemon, mandarin, orange) (Authorized Plant 

Protection Products Data Base of the Hellenic Ministry of Rural Development and 

Food, 2008). 


Manipulation of the timing and quantities of irrigation and fertilizers provided and 

pruning in order to separate the main growth flushes (spring–summer–autumn) and 

decrease the susceptibility of the summer flush, when the citrus leafminer is active, 

contributes to maintenance of the pest populations at low levels (Anagnou-Veroniki, 

1995; Katsoyannos, 1996a, 1996b; Michelakis & Vacante, 1997). Conservation of 

the established exotic parasitoids and native beneficials is essential for the control of 

the citrus leafminer in the productive orchards. Chemical treatments using selective 

insecticides for the control of the pest should be restricted in the nurseries. 

2.5. Aphids 

Commonly, aphids can be very important pests in citrus-growing areas under 

favourable environmental conditions due to their high reproductive potential which 

results in several generations per year and the production of alate adults which can spread 

very quickly and migrate to great distances (Kavallieratos et al., 2005; Athanassiou, 

Kavallieratos, Tomanović, Tomanović, & Milutinović, 2005). Nevertheless, aphids 

infesting citrus in Greece and generally in the northern Mediterranean countries are 

most often kept in low numbers under biological control by several indigenous 

parasitoids and predators (Katsoyannos, 1996a). 

Nine aphid species have been reported to infest citrus trees in Greece, which refer 

to Aphis craccivora Koch, Aphis gossypii Glover, Aphis spiraecola Patch, 

Aulacorthum solani (Kaltenbach), Brachycaudus helichrysi (Kaltenbach), 

Macrosiphum euphorbiae (Thomas), Myzus persicae (Sulzer), Rhopalosiphum 

maidis (Fitch) and Toxoptera aurantii (Boyer de Fonscolombe) (Kavallieratos & 

Lykouressis, 1999). The exotic Aphis spiraecola and the indigenous Toxoptera 

aurantii and Aphis gossypii are the most important aphid species on citrus in the 

region (Argyriou, 1969). 

Strict monitoring and quarantine procedures must be followed for continued 

exclusion from the EPPO region of Toxoptera citricida (Kirkaldy) (EPPO A2 List, 

2004), which is the highest potency vector for Citrus Tristeza Closterovirus (CTV) 

causing the homonymous destructive virus disease of citrus. 

Aphis gosypii is also an efficient vector of many isolates of CTV, whereas T. aurantii 

is a less efficient vector. The prevention of aphids’ population outbreaks is primarily 

based on conservation and, possibly, stimulation of the activity of their natural 

enemies (Katsoyannos, 1996a).

46 



During spring, yellow water-pan traps are used and visual inspections are carrried 

out for monitoring citrus aphids. Moericke pan-traps, both square (60 × 60 × 10 cm) 

and round (30 cm in diameter), painted canary yellow inside and containing 

water up to depth of 3–4 cm with a spoonful of added detergent, are commonly 

used. They are placed in the citrus groves in mid-spring (density 2–5 traps/ha at a 

height of 70 cm above the ground) and they are checked once or twice per week 

during the growing season. Information about citrus aphids populations provided 

by 12 m high suction traps, if available, might also be useful (Katsoyannos, 

1996a). 

Inspections, especially on the apical twigs of new growth flushes, are made 

weekly during the growing season. Curled newer leaves, honeydew, sooty mould 

and the presence of ants are signs aiding the detection of foci of aphid infestation 

in an orchard. Rates of parasitism are monitored by examination of aphids on 

sampled leaves and twigs. 

Aphidophagous coccinellid population levels are monitored using visual 

inspections and by heating branches of trees with a rubber-covered stick over a 

1 m 2 cloth screen and recording the numbers of adults and larvae of the beetles thus 

dislodged (Katsoyannos, 1984). 


Control of citrus aphids is mainly based on natural enemy manipulation 

(conservation) in pest management. Aphids have several natural enemies which 

most often suppress the pests below levels of economic concern. Indigenous 

parasitoids which have been reported to parasitize aphids in Greece include the 

hymenopteran Aphidiinae parasitoids Aphidius colemani Viereck, Aphidius 

matricariae Haliday, Aphidius urticae Haliday, Diaeretiella rapae (M’Intosh), 

Ephedrus persicae Froggat, Lysiphlebus confusus Tremblay and Eady, Lysiphlebus 

fabarum (Marshall), Lysiphlebus testaceipes (Cresson), Praon volucre (Haliday), 

Binodoxys acalephae (Marshall) and Binodoxys angelicae (Haliday) (Kavallieratos & 

Lykouressis, 1999; Kavallieratos et al., 2001; Kavallieratos, Stathas, & 

Tomanović, 2002; Kavallieratos & Lykouressis, 2004). 

Alloxysta spp., Asaphes vulgaris Walker, Asaphes spp., Dendrocerus spp., 

Pachyneuron aphidis (Bouché), Pachyneuron spp., Phaenoglyphis spp. and 

Syrphophagus aphidivorus (Mayr) have been reported as hyperparasitoids that 

attack primary parasitoids of aphids infesting citrus (Santas, 1979; Kavallieratos & 

Lykouressis, 1999). 

Coccinellidae predators Coccinella septempunctata L., Adalia bipunctata L., 

Propylea quatuordecimpunctata L., Hippodamia variegate (Göeze), Oenopia 

(Synharmonia) conglobata L., Adalia decempunctata L. and Scymus (Pullus) 

subvillosus (Göeze) are frequent in Greece. Other aphid predators belong to the 

Syrphidae such as Epistrophe baiteata (De Greer), Paragus albifrons Meigen, 

Paragus majaranae Rondani, Scaeva albomaculata Macquart, Syrphus 

latefasciatus Macquart, and Sphaerophoria sp. The green lacewing Chrysoperla


47 

carnea (Chrysopidae) Stephens is a notable aphid predator in Greece too 

(Katsoyannos, 1996a). 

Conservation of these agents includes management practices e.g. avoiding 

chemical treatment, especially between mid-spring and early summer. Long-term 

positive effects on the naturally-occurring biological control of citrus aphids are 

obtained by preserving existing habitats, which function as reservoirs of the natural 

enemies, or by creating new ones where needed. 

In general, preserving sufficient plant diversity in the agroecosystem is 

desirable, since it ensures the continuous presence of other aphid species which 

serve as alternative prey of coccinellids during the summer scarcity of citrus 

aphids. Other important measures include preserving hibernation sites and 

preventing ants (Formicidae) from tending aphid colonies and disturbing the 

aphids’ natural enemies. Although, these methods are indirect and their effect is 

difficult to be evaluated, they are cost effective and easy to implement 

(Katsoyannos, 1996a). 

A classical biological control case involved the release of the predator 

Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in citrus in experimental 

fields in Marathon (Attica), on Chios island, in Leonidion (Peloponnese) and in 

Chania (Crete) in 1994. The predator was highly efficient against aphid population 

outbreaks (Katsoyannos, Kontodimas, Stathas, & Tsartsalis, 1995). However, when 

sampling was contacted between 1995 and 1999 there was no evidence for the 

establishment of H. axyridis in the release sites (Kontodimas et al., 2008). Only 

small colonies of overwintered adults (

48 


cultural practices. Conservation of aphidophagous insects is achieved mainly by 

avoiding the use of selective insecticides, especially in overall cover-spray 

treatments (Katsoyannos, 1996a). 

2.6. The Citrus Flower Moth, Prays citri 

The citrus flower moth Prays citri usually completes three generations in Greece 

whereas development time is estimated to range from 15 to 19 days in the region of 

Achaia-Peloponnese (Buchelos et al., 1963; Tzanakakis & Katsoyannos, 2003). 

The adults of the first generation appear in August and those of the second 

generation in October–November. Maximum infestation on lemons is observed at 

the end of their main florescence whereas the next generations of the pest infest the 

flowers and fruits of the subsequent florescences of multiple-flowering lemon trees 

(Buchelos, Sueref, & Tsoka-Thanasoulopoulou, 1963). The major damage concerns 

the citrus flowers and the newly formed fruits and it is more severe in lemons and 

citrons. In addition, serious damages have been reported on new overgraftings at 

warm regions in autumn (Tzanakakis & Katsoyannos, 2003). 

Control of the pest depends largely on cultural practices and methods directed 

against the adult moths, since the larvae mining within the flower tissues are not 

normally vulnerable to insecticides and insect pathogens. 


Monitoring of infestation is possible by sampling and examination of flowers and 

newly formed fruits (Cavalloro & Protta, 1983). Synthetic sex pheromone Z-7- 

tetradecenal is available in the US for monitoring (Mineo, Mirabello, del Busto, & 

Viggiani, 1983; Benfatto, 1984) or mass-trapping (120 traps/ha) of males 

(Sternlicht, Barzakay, & Tamim, 1990). 

Although no correlation exists between trap catch and level of flower damage 

(Mineo et al., 1983; Benfatto, 1984) as males of overlapping generations of the 

pest are caught throughout the growing season, both samples and trap captures are 

taken into account for accurate timing of chemical application on citrus (mainly 

lemon and citron) when required. 

The threshold of flower damage by P. citri for chemical control is estimated at 

>50% of flowers infested whereas in the case of fruits when 3% are affected 

(Cavalloro & Protta, 1983). A percentage of 20–30% of healthy flowers is 

sufficient for a satisfying production in lemons (Katsoyannos, 1996b). 


Prays citri has several natural enemies, principally parasitoids e.g. Ageniaspis 

fuscicollis (Dalman) subsp. praysincola Silvestri (Hymenoptera: Encyrtidae) and 

Elasmus flabellatus Boyer de Fonscolombe (Hymenoptera: Eulophidae), which are 

not always effective in contoling the pest (Tzanakakis & Katsoyannos, 2003).


49 

In twice-flowering lemons, good control of P. citri can be obtained by forcing 

early flowering in spring and summer, before the adult flight peaks of the pest in 

each season are observed (Calabretta & Nucifora, 1985). 


Registered insecticides (active substances), which can be used against P. citri in 

Greece, include Bacillus thuringiensis var. aizawai (citron, grapefruit, lemon, 

mandarin, orange), B. thuringiensis var. kurstaki (citron, grapefruit, lemon, 

mandarin, orange), chlorpyrifos (grapefruit, lemon, mandarin, orange, pumelo), 

cypermethrin (grapefruit, lemon, mandarin, orange), flucythrinate (grapefruit, 

lemon, mandarin, orange), paraffin oil (grapefruit, lemon, mandarin, orange, 

pumelo) and petroleum oil (grapefruit, lemon, mandarin, orange) (Authorized Plant 

Protection Products Data Base of the Hellenic Ministry of Rural Development and 

Food, 2008). 


Regulation of flowering before the adult flight peaks of the pest in secondflowering 

lemons is recommended. Selective chemicals could be applied, if 

necessary, after monitoring of infestation by sampling of flowers and newly 

formed fruits. 

2.7. Thrips 

Thrips species infesting citrus in Greece include the greenhouse thrips Heliothrips 

haemorrhoidalis (Bouché) (Thysanoptera: Thripidae) (Katsoyannos, 1996a; 

Tzanakakis & Katsoyannos, 2003) and the Kelly’s citrus thrips Pezothrips 

kellyanus (Bagnal) (Thysanoptera: Thripidae) which was first recorded in 

Peloponnese (Korinthos) in 1981 (Zur Strassen, 1986; Palmer, 1987). The 

greenhouse thrips H. haemorrhoidalis infests mainly citron and lemon whereas the 

Kelly’s citrus thrips P. kellyanus infests mainly lemon and orange with grapefruit 

following and mandarin being almost invulnerable (except the mandarin variety 

Minneola (tangelo) in Chania-Crete) (Varikou, Tsitsipis, Alexandrakis, & Mound, 

2002). 

In samplings performed in Chania – Crete in spring 2003, P. kellyanus was the 

only thrips species collected in lemon and mandarin orchards and the most 

abundant one collected in orange and grapefruit orchards. Some Thrips spp. were 

also found on mandarin and grapefruit in lower numbers whereas Frankliniella 

occidentalis was a minor species found solely in mandarin samples (Varikou, 

2006). 

In general, thrips are considered as a minor pest of citrus causing qualitative 

damage (scarring or escharosis) of the fruits (Katsoyannos, 1996a; Varikou et al., 

2002; Tzanakakis & Katsoyannos, 2003; Hellenic Ministry of Rural Resources and 

Food, 2006, unpublished data).

50 


However, escharotic fruits due to the feeding of the Kelly’s citrus thrips reached 

70% of the total produce in Chania-Crete and they were rejected for export during 

the selection process at packaging in 2001 (Varikou, 2006). Baker et al. (2005) 

refer that feeding of Kelly’s citrus thrips on young and mature fruit causes scarring 

(halo), marking and rind bleaching which typically encircles the apex of the fruit in 

the immediate vicinity of the calyx. 

Heliothrips haemorrhoidalis is a polyphagous parthenogenetic species which can 

complete six generations on citron and overwinters as an adult on citrus trees and 

on poaceous weeds. This is the reason why weed control by ploughing, in 

February, was recommended together with chemical applications in March by 

Anagnostopoulos (1939). 

The Kelly’s citrus thrips P. kellyanus is arrhenotokous (Varikou, 2006) and is 

not known to breed on any indigenous plant species of the Mediterranean region 

except Citrus sp. (Webster, Cooper, & Mound, 2005a). However, P. kellyanus 

can use the pollen of plant species other than citrus as an extra food resource. 

Biology of P. kellyanus was first studied by Varikou, Tsitsipis, Alexandrakis, 

and Hoddle, (2009a) and it was found that its lower development threshold is 

10.2 o C and its thermal constant 204.6 day degrees [whereas 504 day degrees for 

H. haemorrhoidalis (Rivnay, 1935)]. Therefore the Kelly’s citrus thrips is present 

throughout the year in Crete (Chania) with its population increasing during citrus 

flowering in spring as pollen is essential for its reproduction and development in 

the citrus orchards (Varikou, 2006; Varikou, Tsitsipis, & Alexandrakis, 2009b). 

Lemon is the best host among citrus for the survival and maintenance of the 

thrips population due to the numerous flowerings during the year. Pezothrips 

kellyanus is mostly attracted by blue colour traps (compared to yellow and white) 

at the fruiting period but not during flowering or the rest of the year (Varikou, 

2006). 

Entomophagous arthropods of the Kelly’s citrus thrips have not been studied in 

Greece. A predatory mite, Iphiseius (Amblyseius) degenerans (Berlese) 

(Phytoseiidae), has been found in citrus orchards with high thrips populations in 

Italy but its efficacy to control the thrips has not been not proved (Conti et al., 

2001). Hence, chemical control is applied at present. 

Registered insecticides (active substances) for the control of thrips in citrus in 

Greece include chlorpyrifos, fatty acid potassium salt and oxamyl (Authorized 

Plant Protection Products Data Base of the Hellenic Ministry of Rural 

Development and Food, 2008). 

2.8. Mite Pests 

Citrus are infested by a large number of mite species in Greece i.e. the tetranychids 

Panonychus citri (Koch) and Tetranychus urticae Koch (Tetranychidae) and the 

eriophyiids Aculops pelekassi (Keifer) and Aceria sheldoni (Ewing) (Eriophyidae), 

which can cause serious damage on fruit production when outbreaks of the 

population occur (Papaioannou-Souliotis, 1985, 1991, 1996; Papaioannou-Souliotis, 

Tsagarakou, & Dermatas, 1992). However, the damages by mites are usually


51 

occasional and locally restricted as the natural enemies maintain the pest numbers 

under economic injury level in the citrus orchards. 

Panonychus citri was first recorded on Citrus spp. in Greece in 1986 

(Emmanouel & Papadoulis, 1987). It exists throughout the year and can complete 

many generations but the population is high in spring and fall (Papaioannou- 

Souliotis et al., 1992; Emmanouel, Papadoulis, Karkazi, & Papadima, 1994). 

Tetranychus urticae was first recorded in the country in 1962 (Pelekassis, 1962). 

Its population densities are higher during summer whereas in citrus orchards near 

the coast it is present throughout the year (Papaioannou-Souliotis, 1995). 

Aculops pelekassi was first found in 1958 and since then its presence is frequent 

all over the country (Papaioannou-Souliotis, 1985; Papaioannou-Souliotis, Ragusa 

di Chiera, & Tsolakis, 1996). It is active during mild winters and can develop more 

than five generations per year. In population outbreaks it can cause up to 60% loss 

of yield (Papaioannou-Souliotis, 1985). Aceria sheldoni has been found in all 

Greek citrus-growing regions, causing damage mainly in lemons, which can be 

significant only during years with high population (Papaioannou-Souliotis, 1985). 

Sampling for monitoring infestation involves collection of leaves and counting the 

number of mites. 


Many phytoseiid predatory species are found in citrus orchards such as Euseius 

stipulatus (Athias-Henriot), Typhlodromus athenas Swirski and Ragusa, 

Amblyseius andersoni (Chant) and Iphiseius degenerans Berlese. Euseius 

stipulatus is the most frequent phytoseiid predator and is the majority (80%) of the 

phytoseiid population in citrus groves (Papaioannou-Souliotis, 1991). Moreover it 

does not diapause and all the developmental stages may be present during winter 

(Papaioannou-Souliotis, Tsagkarakou, & Nomikou, 1997). 

Generalist predators like E. stipulatus can control the phytophagous mite 

populations at low densities (McMurtry, Morse, & Johnson, 1992) and especially 

the tetranychids when other food resources (e.g. pollen) are also available for their 

good development (Bouras & Papadoulis, 2005). Collection of the infested fruits is 

a practice which may decrease the population of mites. 


Low toxicity selective acaricides are used to control P. citri with applications in 

spring (when the first symptoms appear) and late October. The number of 

applications depends on the acaricide but more than two applications per year are a 

common practice (Papaioannou-Souliotis, 1985; Papaioannou-Souliotis, 1991; 

Papaioannou-Souliotis et al., 1992). Selective acaricides can be applied against A. 

pelekassi in summer (beginning of June) and autumn (mid September to mid 

November) and against A. sheldoni in spring and at the beginning of June 

(Papaioannou-Souliotis, 1985).

52 

F. KARAMAOUNA ET AL.


53 

Registered acaricides (active substances) for control of citrus mite pests include 

acrinathrin (P. ulmi), azocyclotin (P. ulmi and eriophyiids), clofentezine (P. ulmi), 

dicofol (all species), etoxazol (tetranychids), fenazaquin (tetranychids), fenbutatin 

oxide (all species), fenpyroximate (P. ulmi), paraffin oil (all species), petroleum oil 

(eriophyiids), propargite (tetranychids), pyridaben (P. ulmi), tebufenpyrad 

(tetranychids) and white oil (eriophyiids) (Authorized Plant Protection Products 

Data Base, Hellenic Ministry of Rural Development and Food, 2008). 


Usually the phytoseiid predators (mainly E. stipulatus) keep the tetranychid mites 

at low populations on citrus. Monitoring of the mite population in citrus groves is 

very important for the early detection of mite infestation and hence the limited use 

of acaricides. Furthermore the use of selective acaricides highly contributes to 

conservation of the phytoseiid predatory mites. 

3. ARTHROPOD IPM IN CITRUS THROUGHOUT THE YEAR 

Following the IPM strategies recommended for each citrus insect pest separately, 

the outline of an overall IPM programme referring to these pests throughout the 

year is presented in Table 2 (Lykouressis, 1991; Katsoyannos, 1996a; 

Katsoyannos, 1996b; Alexandrakis et al., 2001). 

REFERENCES 

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citrus insect pests (pp. 73–83). Proccedings 3rd National Meeting of Plant Protection, Plant 

Protection in Integrated Crop Production, 6–8 March 2001, Larisa-Greece. 

Anagnostopoulos, P. T. (1939). Pests of fruit trees. Athens. 

Argov, Y., & Rössler, Y. (1996). Introduction, release and recovery of several exotic natural enemies for 

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Anagnou-Veroniki, M. (1995). First record of citrus leafminer, Phyllocnistis citrella (Stainton) on citrus 

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citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), in Greece. VII 

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Anagnou-Veroniki, M., Volakakis, I., & Gianoulis, I. (1995). The citrus leafminer. A new insect pest in 

Greece. Georgia kai Ktenotrofia, 6, 10–15. 

Anonymous (1973). Handbook for crop protection. Athens, Greece: Ministry of National Economics, 

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Argyriou, L. C. (1969). Biological control of citrus in Greece (Vol. 2, pp. 817–822). Proceedings of the 

1st International Citrus Symposium, March 1968, Riverside, CA. 

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Australian Journal of Entomology, 44, 67–74. 

Zervas, G. A. (1994). Development of new traps for the Mediterranean fruit fly, Ceratitis capitata Wied 

(pp. 117–126). Proceedings 4th Hellenic Entomological Congress, Volos. 

Zervas, G. A., Christopoulos, A. D., & Kateva, A. C. (1997). Control of the Meditteranean fruit fly 

Ceratitis capitata, Wied. (Diptera: Tephritidae) by mass trapping in an orange orchard in Korinthia


59 

(pp. 450–456). Proceedings 6th Hellenic Entomological Congress, Chania, 31 October–3 November 

1995. 

Zervas, G. A., Kateva, A. C., & Christopoulos, A. D. (1995). Ways of overwintering of the medfly 

Ceratitis capitata (Wied) (Diptera: Tephritidae) (pp. 105–112). Proceedings of the 5th Hellenic 

Entomological Congress, Athens, Greece, 8–10 November 1993.

3 

BIOLOGICAL CONTROL IN CITRUS IN SPAIN: FROM 

CLASSICAL TO CONSERVATION BIOLOGICAL 

CONTROL 

JOSEP ANTON JACAS 1 AND ALBERTO URBANEJA 2 

1 Universitat Jaume I (UJI), Unitat Associada d’Entomologia Agrícola 

UJI-IVIA, E-12071 Castelló de la Plana, Spain 

2 Institut Valencià d’Investigacions Agràries (IVIA), Unitat Associada 

d’Entomologia Agrícola UJI-IVIA, E-46113 Montcada, Spain 

Abstract. The status of citrus pest management in Spain and of biological control, including classical 

biological control strategies, is reviewed. The augmentative versus inoculation-based control, and the use 

of invertebrate biological control agents in citrus orchards and nurseries are described. Fortuitous and 

conservation biocontrol strategies, as well as exploitation of resident species, either native or naturalized, 

are discussed. Pesticide side-effect testing on natural enemies, presence of alternative hosts and use of 

banker plants are described, together with ground cover mangement strategies. 


Spain is one of the largest producers of citrus for the fresh market worldwide 

(5,129,110 Mg in 2004; MAPA, 2007), mainly oranges, mandarins and lemons. 

Many potential pests are kept under excellent or satisfactory natural control by either 

exotic or indigenous natural enemies [e.g. Panonychus citri (McGregor) (Acari: 

Tetranychidae) by Euseius stipulatus (Athias-Henriot) (Acari: Phytoseiidae)] (Table 

1). Exotic biological control (BC) agents were imported during the last century into 

Spain following classical (= inoculative) BC programs and are now naturalized in 

our country [e.g. Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae)] (Table 

2). However, the fact that most of Spanish citrus production goes to the fresh market 

(84.1%; MAPA, 2007) has important consequences on the status of some citrus 

pests which directly damage the fruit. Because these species are subjected to 

cosmetic thresholds, which are commonly very low (Hare, 1994), BC is considered 




61

62 

J.A. JACAS & A. URBANEJA 

insufficient on a limited, but important, number of pests, such as scales [e.g. 

Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae)] or spider mites 

(Tetranychus urticae Koch) (Acari: Tetranychidae). Furthermore, because of the 

quarantine pest status of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) 

(Diptera: Tephritidae), thresholds are nil for fruit exported to C. capitata-free 

countries (Jacas, Palou, Beitia, & del Rio, 2008). Hence efforts to improve the BC of 

these species are underway. On the one hand, classical BC is a very powerful tool 

against exotic pests of an exotic crop such as citrus is in the Mediterranean basin, 

and this is one of the reasons why this type of BC has been so widely used in the 

region (Jacas, Urbaneja, & Viñuela, 2006). In recent years, though, concerns about 

the potential non-target effects of these exotic species on indigenous food webs have 

arisen worldwide (Lenteren, van Bale, Bigler, Hokkanen, & Loomans, 2006; Lynch 

& Thomas, 2000; Lookwood, Howarth, & Purcell, 2001; Stiling, 2004) and citrus is 

not an exception (Michaud, 2002). 

Table 1. Status of citrus pests in Spain and its relation to biological control (BC). 

Pest species 

Natural 

control a Key mortality factor b BC 

strategy c 

Icerya purchasi E Imported NE C 

Insulaspis gloverii E Imported NE C 

Aleurothrixus floccosus S Imported NE C 

Ceroplastes sinensis S Climate-Native NE C 

Chrysomphalus dyctiospermi S Native NE C 

Coccus hesperidium S Climate-Native NE C 

Panonychus citri S Native NE C 

Phyllocnistis citrella S Imported NE C 

Planococcus citri S Imported NE A 

Saissetia oleae S Climate-Native NE C 

Aonidiella aurantii I Native & imported NE A 

Aphis gossypii I Native & imported NE C, A 

Aphis spiraecola I Native & imported NE C, A 

Ceratitis capitata I Native & imported NE I, C 

Cornuaspis beckii I Native & imported NE C 

Parlatoria pergandii I Native & imported NE C 

Tetranychus urticae I Indigenous NE C, A 

Toxoptera aurantii I Native & imported NE C, A 

a E: excellent; S: satisfactory; I: insufficient. 

b NE: natural enemies. 

c C: Conservation; A: augmentation; I: inoculation. 

A European Union (EU)-harmonized legislation on Invertebrate Biological 

Control Agents (IBCA) is expected to change the current situation of import and 

release of exotic IBCAs in the EU. As a consequence, classical BC will probably 

lose its prevalence in the European citrus industry in favor of other BC strategies 

focused on existing IBCAs (either indigenous or naturalized) and their management.

CLASSICAL AND CONSERVATION BIOCONTROL 

63 

In this scenario both augmentative and conservation strategies aimed at increasing 

the impact of these natural enemies on citrus key pests will become the cornerstone 

of future Integrated Pest Management (IPM) in Spain. 

Table 2. Classical BC Programs developed in Spain against citrus pests. 

Target pest Year Natural enemy Establishment Success a 

Diaspididae 1908 Rhyzobius lophanthae Yes P 

C. dictyospermi 1936 Comperiella bifasciata No – 

Icerya purchasi 1922 Rodolia cardinalis Yes C 

1997 Cryptochaetum iceryae No – 

Saissetia oleae

64 


2. THE ORIGINS: CLASSICAL BIOLOGICAL CONTROL IN CITRUS 

Classical BC has been profusely practiced in Spanish citrus orchards (Jacas et al., 

2006). Up to 20 programs have been developed during the last century (Table 2). 

Citrus are an imported crop group in the Mediterranean basin and most of the pest 

species associated with them originate from Australasia, the area of origin of citrus. 

These are the typical conditions for pests to become the target of classical BC 

programs (Barbosa & Segarra-Carmona, 1993). Therefore, this strategy has been 

repeatedly applied not only in Spain, but in most Mediterranean countries (e.g. Cohen, 

1975; Garrido & Ventura, 1993; Katsoyannos, 1996), as well as in most other citrus 

growing areas under Mediterranean climate, such as California (UC, 1991), Australia 

(Smith, Beattie, & Broadley, 1997) or South Africa (Charleston et al., 2003). 

Scales are predominant among the target pests (Table 2) and this can not be 

considered an accident. Coccoidea represent 50.0% (n = 8) of them, and Homoptera 

as a whole represent 81.3% (n = 13). Well-protected insects, such as most 

homopterans, and those presenting concealed ways of life, like leaf miners, borers, 

etc. are often more likely to be successfully amenable by BC than free living ones 

(Hall & Bennett, 1994; Hespenheide, 1991; Khan, Overholt, & Ng’eny-Mengech, 

2003; Knipling, 1995). This could partly explain why the citrus leaf miner, 

Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), ranks first, together with 

the Mediterranean fruit fly, or Medfly, C. capitata, according to the number of 

natural enemies introduced against each of them (n = 6). 

Whereas the Medfly is considered one of the world's most damaging fruit pests 

(IAEA, 2003; White & Elson-Harris, 2004), P. citrella is considered a secondary 

citrus pest. The case of this leaf miner can be considered a paradigm. As in similar 

situations (Michaud, 2002), the appraisal of urgency when P. citrella was detected in 

Spanish citrus orchards in 1993 prompted funding agencies to prioritize BC projects 

based on the rearing and release of imported natural enemies. Therefore, P. citrella 

became an automatic target for the classical BC approach without a critical evaluation 

if such an approach was useful. Pre-introduction studies (Lenteren & Woets, 1988; 

Barbosa & Segarra-Carmona, 1993; FAO, 1996; EPPO, 1999, 2000) were very limited 

(Urbaneja, Llácer, Tomás, Garrido, & Jacas, 2000; Urbaneja, Llácer, Garrido, & Jacas, 

2003) and 6 different parasitoids (Table 2), were introduced in less than 5 years. The 

host specific A. citricola successfully established on the Canary Islands, but from the 

remaining eulophids, only C. phyllocnistoides finally succeeded in establishing on the 

mainland (Karamaouna et al., 2009). 

Although the introductions of exotic natural enemies focused on C. capitata 

began in 1931 (Servicio Fitopatológico Agrícola, 1933), no success has been 

achieved so far. A classical BC program against this pest is being carried out at 

present (Jacas et al., 2006) and both Fopius arisanus (Sonan) and Diachasmimorpha 

longicavdata (Ashmead) (Hymenoptera: Braconidae) will be probably released from 

quarantine confinement during 2010. 

Success has been higher for introductions aimed at regulating homopteran pests 

(Table 2). In fact, some of these natural enemies, like Rodolia cardinalis (introduced 

against I. purchasi), Cales noacki Howard (Hymenoptera, Aphelinidae) [imported in 

1971 against Aleurothrixus floccosus (Maskell) (Hemiptera: Aleyrodidae)] and


65 

Lysiphlebus testaceipes (Cresson) (Hymenoptera, Braconidae) [introduced in 1977 

against Aphis gossypii Glover and A. spiraecola Pagenstecher (Hemiptera: 

Aphididae)], are considered nowadays key natural enemies in Spanish citrus 

orchards (Urbaneja et al., 2008). 

3. AUGMENTATION VERSUS INOCULATION 

A few IBCAs primarily introduced in classical BC programs, namely the parasitoids 

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) and Leptomastix dactylopii 

(Howard) (Hymenoptera: Encyrtidae) and the predator Cryptolaemus montrouzieri 

Mulsant (Coleoptera: Coccinellidae) failed to satisfactorily establish in Spain and 

consequently do not usually reach numbers high enough to naturally regulate their 

target pests below economic thresholds (Table 2). 

Table 3. IBCAs used in augmentative BC strategies in Spanish citrus orchards and nurseries. 

Natural enemy Target pest Strategy 

Cryptolaemus 

montrouzieri 

Leptomastix 

dactylopii, 

Anagyrus 

pseudococci 

Aphytis 

melinus 

Neoseiulus 

californicus, 

Phytoseiulus 

persimilis 

Phytoseilus 

persimilis 

Planococcus 

citri 

Planococcus 

citri 

Aonidiella 

aurantii 

Panonychus 

citri, 

Tetranychus 

urticae 

Tetranychus 

urticae 

From end of April – July, if gravid females are 

present, release 3–10 individuals per tree 

Repeat at 2–3 week intervals. 

From May – July, when third instar nymphs and 

young females are present, release 10–20 

individuals per infested tree 

Repeat at 2–3 week intervals 

From the end of winter, if parasite susceptible 

stages (NII, males and young females) are present, 

release 50–150 ⋅ 10 3 wasps/ha in 5 – 8 releases, 15 

days apart from each other 

In severely infested orchards, releases should be 

combined with petroleum spray oils a . 

In nurseries, hot spot releases of 10 – 30 individuals 

per infested young tree b . 

Hot spot releases of 100 – 500 individuals per tree 

when economic threshold (20% occupied leaves) is 

exceeded c . 

a Summer releases should be carefully considered due to hot temperatures and low relative humidity. 

Releases after summer are only recommended in orange orchards. 

b 

Against P. citri, only recommended in nurseries if Euseius stipulatus is not present. 

c Experimental strategy under development.

66 


Since the cost of production of these natural enemies is relatively low, the current 

use of these IBCAs involves augmentative releases against their respective target pests 

(Table 3). These strategies are also in use in other Mediterranean countries 

(Katsoyannos, 1996), as well as in areas with a similar climate, such as Australia, 

California, or South Africa (Charleston et al., 2003; UC, 1991; Smith et al., 1997). 

As shown in Table 3, augmentative releases include both exotic and native 

natural enemies. Consistent with latest trends in EU agriculture, which emphasizes 

the role of indigenous natural enemies, Anagyrus pseudococci (Girault) 

(Hymenoptera: Encyrtidae), a native parasitoid of the citrus mealybug, Planococcus 

citri Risso (Hemiptera: Pseudococcidae), has been recently studied and could 

successfully substitute the exotic L. dactylopii in the future (Campos & Martínez- 

Ferrer, 2003). Similarly, studies are in progress to establish conditions for using the 

native predatory mite Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) 

against the two spotted spider mite, Tetranychus urticae Koch (Acari: 

Tetranychidae) another native mite which is considered a key pest for clementine 

mandarins in Spain (Aucejo, Gómez-Cadenas, & Jacas, 2004; Ansaloni, Pascual- 

Ruiz, Hurtado, & Jacas, 2008). Likewise, releases of Neoseiulus californicus 

(McGregor) (Acari: Phytoseiidae) and P. persimilis have also been proposed against 

the citrus mite, Panonychus citri, and T. urticae, respectively, in nurseries (Table 3) 

(Abad-Moyano, Pina, Pérez-Panadés, Carbonell, & Urbaneja, 2009). 

4. FORTUITOUS BIOLOGICAL CONTROL 

Anagyrus pseudococci is not the only example of an indigenous natural enemy 

having a significant impact on an exotic pest. Although such pests are usually the 

target of the Classical BC strategy, indigenous natural enemies can sometimes result 

in excellent BC, which is then called fortuitous BC. 

The native predator E. stipulatus provides a good example of such a situation in 

Spain. This species is the most abundant Phytoseiidae in Spanish citrus (Ferragut et al., 

1988). If undisturbed, its populations are usually able to regulate Panonychus citri 

populations below their economic threshold (Ripollés, Marsá, & Martínez, 1995). 

Therefore E. stipulatus is considered as one of the most relevant natural enemies in 

Spanish citrus orchards and its conservation is a key factor for IPM success (Urbaneja 

et al., 2008). Most other indigenous natural enemies do not have such a dramatic 

impact on their host/prey pests (Table 1). However, both the increasing legal 

restrictions for importing exotic natural enemies into the EU (Bigler et al., 2005) and 

the disappearance of many pesticides in the EU following the process of re-evaluation 

of all pesticide active ingredients under EU Directive 91/414/EEC, have lead to a 

renewed interest on these native species and their conservation (Table 1). 

5. THE CORNERSTONE: CONSERVATION 

Conservation biological control exploits resident, either native or naturalized, 

natural enemies. This strategy is especially useful in permanent ever-green crops 

(Barbosa, 1998; Landis, Wratten, & Gurr, 2000), such as citrus, where both pests 

and their natural enemies are active and abundant throughout the year (Garrido &


67 

Ventura, 1993). One of the most popular tactics used for the conservation of natural 

enemies in the Spanish citrus industry has been the use of pesticides with a reduced 

impact on beneficial arthropods by exploiting either their intrinsic or their ecological 

selectivities (Croft, 1990). The use of reservoir plants and, more recently, studies 

focused on both the management of the ground cover and the use of banker plants to 

enhance the performance of resident natural enemies are providing citrus growers 

new tools for implementing conservation BC in their orchards. 

5.1. The First Step: Pesticide Side-Effect Testing 

Citrus IPM has since long recognised the need for the evaluation of the impact of 

pesticides on the most relevant natural enemies. Pesticide side-effect testing was 

routinely done by Spanish researchers for many years for advisory purposes. As a 

consequence, in 2001, a database including around 270 records referred to 6 

important citrus IBCAs and 80 different pesticides was published (Jacas & García- 

Marí, 2001). The natural enemies were the parasitoids C. noacki, L. dactylopii, L. 

testaceipes and the predators C. montrouzieri, E. stipulatus and R. cardinalis. Some 

of the products tested up until that moment are no longer permitted in the EU 

whereas some new active ingredients have been registered. Therefore, there is a 

need for regularly updating that list. Pascual-Ruiz and Urbaneja (2006) recently 

revised the database. 

Results specifically dealing with acaricides have been recently published 

(Urbaneja et al., 2008). Products recommended for IPM in citrus orchards in the 

Region of Valencia have been listed in Table 4. When available, their residual 

toxicity on the selected IBCAs is provided. These products are effective against their 

target pests whereas their effects on IBCAs are usually low (Bacillus thuringiensis, 

Fenbutatin oxide, Hexithiazox, Mineral oils, Pirimicarb, Spinosad) and/or shortlasting 

(Mineral oils, Chlorpyrifos). In a few cases, some harmful products are 

allowed provided that ecological selectivity is exploited. This is the case of 

imidacloprid, which is prohibited from April till July to protect R. cadinalis which 

typically invades citrus orchards at that time. 

5.2. Alternative Hosts and Banker Plants 

There are two well-known examples of conservation BC in Spanish citrus orchards 

consisting of providing alternative hosts to natural enemies. One of them exploits 

Nerium oleander L. (Gentianales: Apocynaceae), a bush native to the Mediterranean 

basin, as a reservoir for aphid natural enemies. Aphis nerii Boyer de Fonscolombe 

(Hemiptera: Aphidae) is a stenophagous aphid feeding on N. oleander which can not 

survive on citrus. Because both A. nerii and citrus aphids, such as A. gossypii and 

A. spiraecola, are attacked by the same guild of natural enemies (different aphidiine 

parasitoids and predators like syrphids, cecidomyids and coccinellids), Spanish 

citrus growers have long used N. oleander to establish wind breaks and hedgerows 

in their orchards. However this strategy should not be used in lemon orchards

68 


because N. oleander hosts a key pest for this crop, the oleander scale, Aspidiotus 

nerii (Bouché) (Hemiptera: Diaspididae). 

Table 4. Residual toxicity of active ingredients allowed under IP label in the Region of 

Valencia (CAPA, 2004). Classification according to the IOBC WG “Pesticides and Benefial 

Organisms” standards (1: harmless; 2: slightly harmful; 3: moderately harmful; 4: harmful). 

Active ingredient 

Target pests 

R. cardinalis 

C. 

montrouzieri 

E. stipulatus 

L. testaceipes 

L. dactylopii 

C. noacki 

Abamectin Mites, leaf miner 1 3–4 2–3 3–4 

Acetamiprid a Whiteflies, aphids, leaf miner 

Azadirachtin Leafminer 3–4 1 1 1 3–4 

B. thuringiensis Citrus moth 1 1 1 1 1 1 

Benfuracarb Aphids 1 2–3 

Buprofezin Diaspididae, whiteflies 1–2 3 1–2 1 1–2 1 

Chlorpyrifos Coccoidea, citrus moth, aphids 1–2 2 2 3 3 2–3 

Chlorpyrifos-methyl Medfly, coccoidea, citrus moth 1 1 3 3 3–4 1–2 

Clofentezine Mites 1 2 1–2 1 

Dicofol Mites 1 1–4 3–4 1 3–4 2 

Etoxazol a 

Mites 

Fenazaquin Mites 4 2 4 3 

Fenbutatin oxide Mites 1 2 1 1 1 

Fenperoximate a Mites 

Hexithiazox Mites 1 1 1 

Imidacloprid Leaf miner 4 2–3 1 4 3 

Mineral oil Mites, coccoidea, whiteflies 1 1–2 1–2 2 1 1–4 

Piridaben Mites 4 1 

Pirimicarb Aphids 1–2 2 1–2 1 1 1 

Pirimiphos-methyl Coccoidea, whiteflies 1–2 1–2 1–4 4 3–4 

Propargite Mites 4 1 2–3 

Pymetrozine a Aphids 

Pyriproxifen Coccoidea 4 4 1 1–2 2–3 

Spinosad Medfly 1 1 4 

Tebufenpyrad Mites 2 

a 

Products allowed under IP label whose side effects on citrus natural enemies are yet to be described. 

Source: Jacas and García Marí (2001), Pascual-Ruíz and Urbaneja (2006) and Urbaneja et al. (2008). 

A similar situation applies to Oxalis pes-caprae L. (Oxalidales: Oxalidaceae). 

This is an herbaceous plant indigenous of South Africa which was introduced long 

time ago into Spanish citrus orchards. It is an annual plant which produces a bulb 

that insures its survival. It usually dries during the dry Mediterranean summer, but 

reappears as the fall rainy season starts. Petrobia hartii (Ewing) (Acari: 

Tetranychidae) is an O. pes-caprae inhabitant which can not feed on citrus. Because 

this mite can serve as an alternative prey for the same Phytoseiid mites feeding on 

other phytophagous mites occurring on citrus, such as P. citri or T. urticae, the 

conservation of O. pes-caprae in citrus orchards was included in some citrus IPM


69 

guidelines (Aucejo et al., 2003). More recently, studies are underway to ascertain the 

usefulness of banker plants as a source of aphid parasitoids in citrus, using the same 

strategy already in use in protected crops (Calvo & Urbaneja, 2004). Barley plants 

infested with cereal-specific aphids, such as Rhopalosiphum padi (L.), parasitized by 

aphidiine parasitoids, such as Aphidius colemani Viereck, are produced by 

commercial insectaries and introduced into the orchards before citrus aphid 

populations peak during early spring. This strategy could prove very useful when 

grassy covers [e.g. Festuca arundinacea Schreb (Poales: Poaceae), see below] 

providing food to these specific aphids are also used. 

5.3. Ground Cover Management Strategies 

Spanish citrus orchards are quite commonly grown on bare soil by either use of 

herbicides or mechanical means. This is not the ideal situation and the use of a cover 

crop as an ecological infrastructure (Boller, Häni, & Poehling, 2004) is encouraged 

by IPM guidelines. However, little is still known about the fauna inhabiting this 

stratum in citrus and the ecological relationships occurring between the ground and 

the tree arthropodofaunas. Therefore, the ground cover management is being 

investigated at this moment as a means of conserving ground-dwelling natural 

enemies and enhancing their impact on some citrus pests (top-down control), as well 

as a means of providing bottom-up control of these pests. This is the case of both 

T. urticae and C. capitata. 

Tetranychus urticae is a serious problem in clementine mandarins in the Eastern 

coast of Spain. Infestations downgrade fruit and, because T. urticae can feed on 

more than 900 plant species (Bolland, Gutiérrez, & Flechtmann, 1998), cover crop 

management can dramatically affect the dynamics of T. urticae populations on the 

trees. In 2003, a survey of the acarofauna associated to the most common weeds 

appearing in citrus orchards showed that Poaceae presented the lowest ratio 

T. urticae/Phytoseiidae from the 45 weed species studied (Aucejo et al., 2003). 

Therefore, a cover of Festuca arundinacea Schreb (Poales: Poaceae), a grass that 

had been previously selected as a citrus ground cover for other agronomic favorable 

characteristics, has been compared to a wild cover and to bare soil during the last 2 

years (2006–2007). 

The results obtained so far show that the F. arundinacea-sown cover has resulted 

in the lowest populations of T. urticae on the trees and could consequently be 

recommended to growers. The mechanisms explaining these results could be related 

both to a host-feeding specialization by T. urticae (bottom-up control) and to the 

composition of the beneficial acarofauna associated to the ground cover (top-down 

control), which resulted more diverse and balanced on both F. arundinacea and the 

trees grown on that particular cover than on both the wild cover and the bare soil 

systems (Aguilar-Fenollosa, Pascual-Ruiz, Hurtado-Ruiz, & Jacas, 2008, 2009). In 

addition to T. urticae, other citrus pests spend part of their life cycle on the ground 

cover, such as aphids, or in the soil, like C. capitata, which pupates in it. In recent 

years, different groups of ground-dwelling predators have been catalogued in 

Spanish citrus orchards (Monzó et al., 2005; Urbaneja et al., 2006). These studies

70 


showed that rove beetles (Coleoptera: Staphylinidae) were the most abundant-active 

group representing about 38.6% of the total number of predators collected, followed 

by spiders (Arachnida: Araneae) (28.9%), earwigs (Dermaptera) (18.0%), ground 

beetles (Coleoptera: Carabidae) (12.7%) and tiger beetles (Coleoptera: Cicindelidae) 

(1.8%). A recent study (Monzó, Urbaneja, Sabater-Muñoz, Castañera, 2007; Monzó, 

Mollá, Castañera, & Urbaneja, 2009) indicates that the wolf spider Pardosa cribata 

Simon (Araneae: Lycosidae), the most abundant ground-dwelling spider in the 

Valencian citrus orchards, could play an important role in controlling those pests. 

CONCLUSIONS 

Biological control has been and will definitively be an increasingly important part of 

citrus crop protection practices. Because of the present European limitations on the 

importation of exotic IBCAs, straightforward protocols to evaluate candidate species 

are urgently needed. Simultaneously, studies focused on the role of indigenous 

IBCAs in the citrus agrosystem and the conservation of both native and naturalized 

natural enemies, have to be emphasized. Augmentative and conservation BC will 

probably play a gradually more important function in the Spanish citrus industry and 

the first changes are already happening. 

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4 

CITRUS INTEGRATED PEST MANAGEMENT 

IN ITALY 

LUCIA ZAPPALÀ 

Dipartimento di Scienze e Tecnologie Fitosanitarie, 

University of Catania, 95123 Catania, Italy 

Abstract. Main insect pests of citrus in Italy are presented, with details on their biology and main natural 

enemies. They are the California red scale, Aonidiella aurantii, the Oleander scale, Aspidiotus nerii, the 

Citrus mealybug, Planococcus citri, the Citrus leafminer, Phyllocnistis citrella and the Mediterranean fruit 

fly, Ceratitis capitata. Management of A. aurantii is generally based on integrated control strategies 

supported by a monitoring system through pheromone traps. Natural enemies include predatory beetles and 

endoparasitoids. Aspidiotus nerii is controlled by predatory beetles and Aphelinid parasitoids. Management 

relies on pruning, chemical control and monitoring through sticky tapes. Several predators (spiders, true 

bugs, lacewings and ants) feed on P. citrella, with over 90 parasitoid species. Natural enemies of P. citri 

include predators and endoparasitoids, which provide satisfactory control. Ceratitis capitata is the main pest 

of citrus; biological control with parasitoids had limited success. Its populations are limited by 

microorganisms and occasional predators, cultural methods, chemicals and attractive traps. Management and 

control of secondary pests of citrus, like whiteflies, some scales and moths, are also discussed. 


In Italy citrus are cultivated on around 170,,000 ha, the majority of which is 

represented by sweet orange (60%), followed by lemon (19%), clementine (13.8%), 

mandarin (6.1%) and minor species (bergamot, grapefruit, citron and chinotto) 

(1%). 

The pests reported on this crop are nearly 100 but among them only around 30, 

mainly sap-sucking species, may require control. In the last 30–40 years the picture 

of the main arthropod pests deeply changed. The major reason of this modification 

can be found in the repeated applications of large spectrum pesticides that altered 

the bio-ecological equilibrium of this complex agro-ecosystem. However, the 

changes are also related to the effect of modifications in cultural techniques 

(fertilization, use of phytoregulators, irrigation, pruning, weeding, new varieties, 




73

74 

L. ZAPPALÀ 

etc.) that modified the cultivated ecosystem. Besides, an additional cause of 

modifications in the citrus orchard fauna is represented by the accidental 

introduction of new exotic pests. Among these, the most significant in the last 30–40 

years have been Aphis spiraecola Patch, Aleurothrixus floccosus (Maskell), 

Dialeurodes citri (Ashmead), Parabemisia myricae (Kuwana), Coccus 

pseudomagnoliarum (Kuwana) and other scales [such as Aonidiella citrina (Coquet), 

Pseudococcus calceolariae (Maskell) and Unaspis yanonensis (Kuwana)], 

Phyllocnistis citrella Stainton, Pezothrips kellyanus (Bagnall) and the red spider 

mite Panonychus citri (McGregor). Recently (April 2008) a new record was added 

to the list of citrus pests in Italy: the Orange spiny whitefly Aleurocanthus spiniferus 

Quaintance (Porcelli, 2008). This species, which is included in the “EPPO A1 List of 

pests recommended for regulation as quarantine pests” and in the EU Annex II/A1: 

“Pests known not to occur in the EU, whose introduction into, and/or whose spread 

within, all EU Member States is prohibited, with reference to specific plants or plant 

products”, is a further example of fortuitous introduction of exotic species on citrus. 

The reasons of all these introductions are not easily explicable but they’re most 

probably related to increased commercial exchanges, as well as to continuous 

changes in climate. The flow of exotic arthropods towards the Mediterranean basin 

in general and Italy in particular is unceasingly active. There are several potential 

invasive species, among which the Brown citrus aphid Toxoptera citricidus (Kirk.), 

the most efficient vector of the Citrus Tristeza Virus, represents a real risk, 

considering its recent establishment in some limited areas of Spain and Portugal 

(Madeira island and Northern region). Other species that are most likely to be 

introduced or spread out in Italy are the whiteflies Aleurocanthus woglumi Ashby, 

Aleurodicus dispersus Russell, Aleuroclava jasmini (Takahashi) (which are all 

present in the Middle East); the psyllid Diaphorina citri Kuwayama (vector of the 

Greening disease and present in Saudi Arabia and in Madeira island); the scales 

Ceroplastes floridensis Comstock (recorded in the Middle East) and Chrysomphalus 

aonidum (L.) (up to now only occasionally reported on citrus in Italy), as well as the 

longhorned beetle Anoplophora chinensis (Forster) (reported in Northern Italy on 

other host plants). 

The introduction of exotic species is not only detrimental because of their direct 

damage but most of the time because of the measures adopted to control their 

populations, often chemical treatments, that may in fact disrupt comprehensive 

integrated control strategies carefully developed over the years. However, many of 

the newly introduced species have been the object of classical biological control 

programs with importation of natural enemies from the areas of origin of the pests 

and the majority of them achieved substantial results ensuring effective control. 

2. MAIN PESTS AND THEIR CONTROL METHODS 

In Italian citrus orchards the key arthropod pests are presently the California red 

scale Aonidiella aurantii (Maskell), the Oleander scale Aspidiotus nerii Bouché (on 

lemon), the Citrus mealybug Planococcus citri (Risso), the Citrus leafminer 

P. citrella (on young trees and in nurseries), the Mediterranean fruit fly Ceratitis

CITRUS PEST MANAGEMENT IN ITALY 

75 

capitata (Wiedemann) and the Two spotted spider mite Tetranychus urticae (Koch) 

(on lemon) (Barbagallo, 2000). Together with these species, some others such as the 

Citrus green bug Closterotomus trivialis (Costa), the Cotton or Melon aphid Aphis 

gossypii (Glover), the Chaff scale Parlatoria pergandii Comstock, the Olive black 

scale Saissetia oleae (Olivier), the Fig wax scale Ceroplastes rusci (L.) and the 

Leafroller Archips rosanus (L.), have been showing recrudescent infestations over 

the last decades. 

2.1. Aonidiella aurantii (Maskell) 

The armoured scale A. aurantii (Hemiptera: Diaspididae), commonly known as 

California red scale, is native to South-Eastern Asia (Southern China and 

Indochinese peninsula) but is spread almost worldwide. 

The armour of the mature female is almost round in shape (1.6–2.1 mm), clear 

brown almost translucent with the nymphal exuviae located at the centre. Generally 

the scale appears reddish in colour because of the red body visible through the 

cover. The shield remains tightly attached to the substrate when the scales are 

moulting or reproducing. A characteristic, well developed, whitish ventral coating 

isolates the body of the female from the plant tissues. Before mating the body of the 

female is pear-shaped, pale yellow and its cover assumes a greyish colour; soon after 

mating, due to the production of eggs, the cephalothoracic portion of the body 

rapidly develops and reaches the apex of the abdomen. The crawlers that 

progressively emerge from under the female, move around to find a suitable place to 

settle and begin to produce a white cottony circular cover (“white cap” stage). 

Starting from the second instar, males begin to develop in a different way forming 

an elongated and usually clearer cover. The adult male (1.6–1.7 mm) emerges after 

four moults and is yellowish-orange, with some brown sclerified portions on the 

dorsal region. 

Figure 1. Aonidiella aurantii colonies on Tarocco orange.

76 

L. ZAPPALÀ 

Aonidiella aurantii is extremely polyphagous, it has been recorded on more than one 

hundred hosts including agricultural (almond, avocado, carob, grape, jujube, loquat, 

mango, mulberry, olive, peach, pear, walnut, etc.), forest (alder, conifer, eucalyptus, 

maple tree, oaks, etc.) and ornamental plants (acacia, aralia, araucaria, bougainvillea, 

boxwood, camellia, crossvine, dracaena, euonymus, magnolia, oleander, palm, privet, 

etc.). However, its preferential host plants are citrus (Fig. 1), in decreasing susceptibility 

order: lemon, grapefruit, orange and mandarin, on which it can certainly be still 

considered as one of the key pests in arid and semiarid regions worldwide (Moreno & 

Luck, 1992; Franco, García–Mari, Ramos, & Besri, 2006; Grafton-Cardwell, 2006). This 

is related to the direct damage to the trees, due to the infestations on all aerial parts of the 

plant from which the scale sucks sap and inoculates toxic saliva causing leaf yellowing 

(Fig. 2), deformation and drop, dieback of twigs and limbs, cortical lesions on branches 

and trunk, sometimes with production of gum, but also mainly because of the 

commercial damage linked to fruit downgrading caused by the simple presence of instars 

on the peel (Walker, Zareh, & Arpaia, 1999). 

Figure 2. Leaf yellowing caused by Aonidiella aurantii on citrus. 

The general difficulty in chemically controlling armoured scales, the easy 

development of resistance by A. aurantii to chemical compounds (Forster, Luck, & 

Grafton–Cardwell, 1995; Grafton-Cardwell, Ouyang, Striggow, Christiansen, & 

Black, 2004; Martínez Hervás, Sots, & García–Marí, 2006) and the spread of 

integrated and organic citriculture, led to the search for alternative control methods.


77 

Management of this pest is generally based on integrated control strategies 

supported by a monitoring system by means of pheromone traps. The captures allow 

identifying the flights of male scales, which correspond to the generations annually 

performed by the scale in the field, and also indicate which orchards or areas of the 

orchard have higher levels of scale population. The flight data together with the 

Degree-Days calculation, help to determine the right time for chemical or biological 

control. Pheromone traps have to be placed in the field in February-beginning of 

March. The sticky cards are then changed weekly and the pheromone dispensers 

monthly through October. Two to four pheromone traps per uniform 4-ha block are 

used, adding two traps for each additional 4 ha. 

Narrow range petroleum oil sprays can be used to reduce scale populations, with 

reduced negative effects on the complex of the natural enemies. Other commonly 

used chemicals, such as chlorpyrifos, imidacloprid or insect growth regulators 

(buprofezin, pyriproxifen), can negatively impact ladybeetle and lacewing 

populations and their use is therefore incompatible with a rational integrated 

management of the orchard. Pheromone traps, however, are not reliable predictors of 

red scale populations when insect growth regulators are used, since males are more 

sensitive than females to these compounds. In this case the traps may underestimate 

the scale population (Rill, Grafton–Cardwell, & Morse, 2007). 

The complex of natural enemies feeding on California red scale includes the 

predatory beetles Chilocorus bipustulatus (L.), C. kuwanae Silv., C. nigritus (F.), 

Exochomus quadripustulatus (L.), Rhyzobius lophanthae (Blaisdell) (Coleoptera: 

Coccinellidae), Cybocephalus rufrifrons Reitter (Coleoptera: Cybocephalidae), the 

dipteran Lestodiplosis aonidiellae Harris (Diptera: Cecidomyidae), and the mite 

Typhlodromus cryptus Athias-Henriot (Acari: Phytoseiidae). The scale is also 

controlled by the endoparasitoids Encarsia perniciosi (Tower) (Hymenoptera: 

Aphelinidae) and Comperiella bifasciata Howard (Hymenoptera: Encyrtidae), and 

by the ectoparasitoids Aphytis chrysomphali (Mercet), A. lingnanensis Compere, A. 

melinus DeBach and A. proclia (Walker) (Hymenoptera: Aphelinidae). 

Figure 3. Aphytis melinus adult female.

78 

L. ZAPPALÀ 

Although numerous natural enemies are associated with California red scale and 

their relative importance varies according to the differences in the climatic 

conditions as well as the host stage preferences, some of them are considered more 

effective and employed in biological control programs. In particular the aphelinid 

ectoparasitoid Aphytis melinus (Fig. 3) is the most commonly used biocontrol agent 

of A. aurantii in Italy as well as worldwide through augmentative releases (Furness, 

Buchanan, George, & Richardson, 1983; Moreno & Luck, 1992; Forster et al., 1995; 

Luck, Forster, & Morse, 1997; Rizqi, Nia, Abbassi, & Nadori, 2001; Rizqi, 

Bouchakour, Aberbach, & Nia, 2006). The technique consists in releasing about 

200,000 parasitoids/ha/year starting in February–March (when the average 

temperature is around 18°C or after the first captures of males on the pheromone 

traps) and following a bi-weekly interval. Half of the total amount of parasitoid 

adults should be released before mid-June, then the releases can be suspended for 1 

or 2 months (depending on the climatic conditions) when second and third instar 

scale are not available and then completed generally through mid-November. 

The effectiveness of biocontrol agents depends on careful monitoring and use of 

selective insecticides. Besides, a critical point is represented by the control of ants 

which can severely disrupt red scale parasites while protecting and maintaining this 

species and honeydew-producing pests, such as soft scales or mealybugs. In the last 

years some trials were carried out in Southern Italy (Tumminelli et al., 2000, 2006a; 

Mazzeo, Benfatto, Palmeri, & Scazziotta, 2004) which gave inconsistent results and 

therefore the effectiveness of A. melinus releases has not been clearly demonstrated. 

The explanation of these results can be searched in the mutual relationship between the 

biology and behaviour of the parasitoid and its host, in the methodology of release, in the 

difficulty to involve uniform areas and in the low quality of the parasitoids used. In 

2005–2006 a further trial was carried out (Zappal à et al., 2008), trying to eliminate some 

of these elements of uncertainty, therefore conducting the experiment in a uniform 

integrated citrus orchard, releasing A. melinus locally produced by the insectary of the 

Regional Phytosanitary Services, regularly submitted to quality control tests (Zappalà 

Siscaro, Saraceno, Palmeri, & Raciti, 2006). Evenly distributed release points were used, 

according to a scheme supported by a parallel trial on the dispersal capacity of A. melinus 

(Palmeri, Campolo, Grande, Siscaro, & Zappalà, 2008). The data obtained suggest that 

A. melinus contributes to the control of California red scale infestations, but cannot be 

considered as the key solution, at least in Sicilian conditions. In any case the results 

obtained highlighted that the elimination of chemical treatments in the released plots as 

well as in the surroundings, restored a biological equilibrium ensuring a consistent 

presence of fundamental natural enemies (Zappalà et al., 2008). 

Further investigations presently focus on the evaluation of the actual role played 

by endoparasitoids, namely C. bifasciata, which was recovered several years after its 

first introduction (1988–1994). This species showed to be well adapted in Eastern 

Sicily where it has colonized a wide area, 50 km, on average, far away from the first 

release site. The presence of C. bifasciata both in organic and conventionally 

managed orchards is of particular interest and could be of great help in the quick 

diffusion of the encyrtid, already successfully started, in all citrus growing areas of 

Southern Italy (Siscaro, Di Franco, & Zappalà, 2008). Future studies will also regard 

the interactions between A. aurantii, its natural enemies and the most common


79 

species of ants in Sicilian citrus orchards. Interesting hints could come from the 

evaluation of the effect of joint releases of predators, such as for example 

C. bipustulatus, which has an impressive “cleaning effect” on dense colonies, mostly 

on branches and trunk, and is less sensitive to high temperatures. 

2.2. Aspidiotus nerii Bouché 

Commonly known as Oleander scale, A. nerii (Hemiptera: Diaspididae) is almost 

worldwide distributed on citrus and in the Mediterranean basin it normally 

completes 3 generations per year. It mainly overwinters as virgin female and 

immature male on branches of various size. The reproduction is sexual or 

parthenogenetic and each female produces an average of 100 eggs with the 

parthenogenetic biotypes performing a lower fecundity. This scale insect is 

extremely polyphagous and attacks citrus (mainly lemon), acacia, asparagus, carob, 

ivy, jojoba, kiwi, mulberry, oleander, olive, palm, peach, pear, plum. 

The armour of the female is pale brown in colour, about 1.5–2.5 mm in diameter, 

round shaped. The body of the insect is yellowish. The nymphal exuviae are yellow 

and located centrally or slightly laterally. The ventral shield is white and very thin. 

The pygidium has 3 pairs of lobes, the central ones have a sclerified basal region 

while the external ones are poorly developed; dorsal ducts are short and spiracles are 

not provided with glands. 

Male armour is slightly smaller, white and almost oblong in shape, 1–1.5 mm in 

length. The adult male (1 mm in length) has only one pair of wings, like all the other 

scales, and is characterized by a long aedeagus. It is yellow in colour with blackishbrown 

appendages. 

The pest infests branches, leaves and fruits. Heavy attacks may cause loss of 

vigour, deformation of infested plant parts, chlorotic spots on leaves and leaf drop. 

On the fruits the feeding sites of the scales remain green and do not develop 

normally while the rest of the rind changes colour at maturity and grows evenly. 

The Oleander scale is controlled by the predatory beetles Chilocorus 

bipustulatus, Exochomus quadripustulatus, Rhyzobius lophanthae and Scymnus spp. 

(Coleoptera: Coccinellidae). The species is also parasitized by the Hymenoptera 

Aphelinidae Aphytis chilensis How., A. chrysomphali, A. diaspidis (How.), A. 

hispanicus (Mercet) and Encarsia citrina (Craw). 

Regular pruning represents an important tool in controlling this scale as well as 

all the other scales. Chemical control can be performed using mineral oils before the 

scale moves on the fruits and, in case of heavier infestations, the use of an IGR 

(buprofezin) can be considered. The timing of treatments is made harder by the 

absence of an efficient monitoring system. Pheromone traps were tried in the field 

but they were not commercially developed. A method which proved effective in 

monitoring the scale populations, and particularly in placing the chemical 

treatments, was based on wrapping sticky tape around 1-year-old branches that have 

both old and new wood and are infested by live female scales, in order to capture the 

crawlers as they emerge from the females and move across the twigs (Tumminelli, 

Perrotta, Raciti, & Colazza, 2006b). The economic threshold varies considerably,

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depending on the market and crop yield, but it normally corresponds to 3–5% of fruits 

infested with more than 10 scales in the fall. If this threshold is exceeded at harvest, 

monitoring crawlers the following spring, together with visual inspection of fruit, may be 

a valid method to correctly place a treatment. This should be avoided at petal fall on the 

peak of crawlers of the first generation (around May) because it may increase fruit drop 

and be toxic to honeybees. It could instead be applied on the peak of crawlers of the 

second generation which normally takes place in July (Tumminelli et al., 2006b). 

2.3. Phyllocnistis citrella (Stainton) 

The Citrus leafminer (CLM), P. citrella (Lepidoptera: Gracillariidae), native to 

South-East Asia, has spread worldwide, throughout almost all citrus growing areas 

in the last decades (Hoy & Nguyen, 1997; CAB International, 2003; Grafton- 

Cardwell, Godfrey, Headrick, Mauk, & Peña, 2008). In Italy it was first reported in 

1994 (Benfatto, 1995). 

Adults are about 2 mm long with a wingspan of about 4 mm. They have narrow 

long fringed wings; the anterior pair is silvery and shining white with brown and 

white markings as well as a distinct black spot on each wing tip. Hind wings are 

whitish and extremely slender, both costal and inner margins have long setae. 

Antennae are filiform and made of about 30 segments. 

The egg (0.35 × 2 mm) is lenticular and the chorion is smooth and transparent. The 

larvae are pale yellow from the first to the third instar with the last abdominal segment 

bifurcate. Their size is 1.7 – 2 × 0.3 – 0.4 mm. The fourth instar larva or prepupa is 

yellow in colour, cylinder shaped and without bifurcation on the last abdominal segment. 

It stops feeding but remains quite active. It forms a silken cocoon within the mine and as 

the silk dries the leaf curls over the pupal cell. The pupa is yellow to light brown, turning 

darker with age. It is characterized by the presence of a cephalic spine which is used to 

make an opening at the anterior of the chamber, to let the adult emerge. The last two 

abdominal segments are fused in the female pupa while they are distinct in the male. 

Figure 4. Phyllocnistis citrella larva and mine on a citrus leaf.


81 

Leafminers are most active from dusk to early morning. Soon after emergence 

the female emits a sex pheromone that attracts males. Females lay 30–70 eggs 

during their 2–12 days life span, deposited singly along the midrib on the lower 

surface of new tender terminal leaves. Eggs hatch within 2–3 days at 26–27°C; 

however, it may take up to 12 days at lower temperatures. Newly born larvae begin 

feeding immediately in shallow, winding mines under the leaf cuticle. As the larva 

increases in size, the mine becomes more visible because of the air that penetrates 

and because of the central frass trace within the mine (Fig. 4). Larvae molt 4 times, 

each larval stage lasting about 1 day, while the pupal stage lasts 7–10 days at 26°C. 

Mature larvae pupate within the mine inside a silken chamber under the rolled edge 

of the leaf. From egg to adult the life cycle takes about 15–17 days to complete at 

26°C and 70–80% humidity, but it may last up to 7 weeks depending on temperature 

and humidity conditions. Up to 13 generations per year occur in tropical areas. The 

population dynamics and the activities of the Citrus leafminer vary in relation to 

differences in climatic conditions and flushing of citrus trees. In Italy the spring 

flushing escapes P. citrella infestation since temperatures are not suitable for the 

leafminer development. The attacks of the pest occur during summer-fall. 

Several predators, mainly spiders, bugs, lacewings and ants, have been observed 

feeding on the pest (Browning & Peña, 1995). Besides, over 90 hymenopterous 

parasitoid species, belonging to the families Braconidae, Encyrtidae, Eulophidae, 

Eurytomidae, Eupelmidae and Pteromalidae have been reported (Heppner, 1993; 

Hoy & Nguyen, 1997; Schauff, Lasalle, & Wijesekara, 1998). Among these species, 

about 70 are considered as primary parasitoids and only 6 are classified as 

preferentially living on P. citrella. Indigenous natural enemies, mainly parasitoids, 

detected on the CLM never reached an effective control in all newly infested citrus 

areas, such as Florida (Hoy & Nguyen, 1997), Israel (Argov & Rössler, 1996), Spain 

(Garrido Vivas, 1995), Turkey (Uygun et al., 1996) and Italy (Barbagallo et al., 

1998; Caleca & Lo Verde, 1998; Giorgini, Pedata, & Viggiani, 1998). 

Since in the native areas of the leafminer the host-specific enemies represent the 

main biological mortality factor of the pest (Binglin & Mingdu, 1996; Morakote & 

Nanta, 1996; LianDe, MinSheng, Jin, & Qing, 1999), a classical biological control 

program has been started in 1995 in Italy by introducing exotic natural enemies. 

Three Hymenoptera parasitoids [Ageniaspis citricola Logvinovskaya (Encyrtidae), 

Quadrastichus sp. (now Quadrastichus citrella Reina & La Salle) and Citrostichus 

phyllocnistoides (Narayanan) (Eulophidae)] have been introduced, reared and 

released. Moreover, in 1998 the Australasian ectoparasitoid Semielacher petiolatus 

(Girault) (Hymenoptera: Eulophidae) was recorded for the first time in Italy. The 

species probably spread naturally after its introduction in other countries of the 

Mediterranean basin (Mineo, Caleca, & Massa, 1998; Siscaro, Longo, Maugeri, 

Reina, & Zappalà, 1999a). 

Ageniaspis citricola (Fig. 5) is a poliembryonic koinobiont endoparasitoid of P. 

citrella eggs and young larvae (Edwards & Hoy, 1998; Zappalà & Hoy, 2004). The 

species shows several biological features which characterize effective parasitoids, 

such as host-specificity, high reproductive rate (more than 180 eggs/female, femalebiased 

sex ratio and short cycle), host discrimination capacity, high dispersal and 

searching rate (Hoy & Nguyen, 1997; Zappalà & Hoy, 2004). Therefore, the

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L. ZAPPALÀ 

encyrtid A. citricola, native to Taiwan, Thailand and Vietnam, has been used in 

biological control programs in several citrus regions: Algeria, Argentina, Australia, 

Bahamas, Brazil, Cyprus, Colombia, Florida, Greece, Honduras, Israel, Louisiana, 

Morocco, Mexico, Oman, Peru, Syria, Spain, Texas, Tunisia, Turkey and Venezuela 

(Berkani & Mouats, 1998; Schauff et al., 1998; Siscaro, Longo, & Mineo, 2000). 

Figure 5. Ageniaspis citricola, ovipositing adult female. 

In Italy, the encyrtid has been introduced and reared since 1995 (Siscaro, 

Barbagallo, Longo, & Patti, 1997; Siscaro & Mazzeo, 1997). Nearly 15,000 adults 

have been released in Eastern Sicily and Calabria during 1996–2000 (Siscaro, 

Longo, & Mineo, 2000). The species was recovered in some coastal lemon orchards 

where it overwintered in 1998 (Siscaro et al., 1999a) and this strain, collected in the field, 

has been reared and released in the following years, although without any permanent 

establishment (Siscaro, Barbagallo, Longo, Reina, & Zappalà, 1999b). The encyrtid is, 

however, one of the major CLM antagonists in several countries (Argentina, Australia, 

Bahamas, Brazil, Canary Islands, Florida, Honduras, Louisiana and Venezuela), where it 

has permanently established. Therefore A. citricola appears to be climatically adapted to 

humid tropical and subtropical climates (Hoy & Nguyen, 1997). 

Laboratory observations have shown that the species, at the pupal stage, has a great 

resistance to low temperatures (5–10°C); adults survive longer at 10°C while individuals 

exposed to temperatures higher than 25°C die in less than 24 h. High mortality of adults 

at 25–35°C suggests that the parasitoid is unsuitable to the biological control of P. 

citrella in Mediterranean citrus orchards (Zappalà & Siscaro, 2004). 

Quadrastichus citrella is an ectoparasitoid of CLM second and third instar 

larvae. Its biological cycle lasts about 20 days at 20°C and R.H. > 80%. At the same 

temperature the adults survive up to 40 days (Argov & Rössler, 1998; Llácer,


83 

Urbaneja, Jacas, & Garrido, 1998). The parasitoid, native to China, Japan, Taiwan 

and Thailand, has been introduced in Morocco (Smaili, Afellah, Aarab, & Zrida, 

1999), Cyprus, Greece, Spain and Israel (Schauff et al., 1998; Kalaitzaki, 2004), with 

no evidence of establishment (Argov, 2000), except in Spain where the species 

temporarily established in the Valencia area (Vercher, García–Mari, Costa–Comelles, 

Marzal, & Villalba, 2003). In 1996 this eulophid was introduced in Southern Italy and 

about 3,000 specimens were released in more than 30 sites. Although preliminary 

observations indicated that the ectoparasitoid seemed to have a good adaptability to 

Italian citrus areas (Longo & Siscaro, 1997), it has not overwintered in any release site 

(Barbagallo, Longo, Siscaro, Reina, & Zappalà, 2000). 

Citrostichus phyllocnistoides is reported as larval ectoparasitoid of P. citrella 

(Subba Rao & Ramamani, 1965; Bouček, 1988; Neale, Smith, Beattie, & Miles, 

1995). Nevertheless it has been recovered in India on Trioza obsoleta Buckton 

(Homoptera: Psyllidae) feeding on Diospyros melanoxylon (Roxb.) (Dash & Das, 

1997). Further studies (Massa, Rizzo, & Caleca, 2001; Massa & Rizzo, 2001; Lo 

Duca, Massa, & Rizzo, 2002) have shown that C. phyllocnistoides parasitizes also 

Lepidoptera Nepticulidae (Acalyptris minimella (Rebel) on Pistacia lentiscus L., 

Stigmella sp. on Rubus ulmifolius Schott and an unidentified nepticulid on Salix alba 

L.). It prefers second and third instar CLM larvae both for ovipositing and host 

feeding, while first instar larvae are selected only for host feeding (Reina & Siscaro, 

2004). The female lays one or more eggs (up to 5), but only one will complete its 

development (Subba Rao & Ramamani, 1965). Its cycle lasts 12–13 days at 22–26°C 

(Ding, Li, & Huang, 1989). Sex ratio is female-biased, 80% of females is obtained 

from third instar larvae, while 70% of males from second instar larvae. The eulophid is 

reported on P. citrella in Afghanistan, China, India, Indonesia, Japan, Oman, Pakistan, 

South Africa, Sudan, Swaziland, Taiwan and Thailand (Schauff et al., 1998). It has 

been introduced in Australia, Cyprus, Greece, Israel (Schauff et al., 1998) and Spain 

(García-Marí et al., 2000). Its permanent establishment has been recorded in all these 

areas with the exception of Australia (Argov, 2000; García-Marí et al., 2000). 

Moreover, in Portugal the accidental immigration and establishment (ecesis) of this 

species was reported in 2003 (Gomes da Silva, Borges da Silva, & Franco, 2006). 

Figure 6. Semielacher petiolatus adult female.

84 

L. ZAPPALÀ 

In Italy C. phyllocnistoides was introduced in 1999 (Mineo & Mineo, 1999a) and 

in the same year about 600 specimens were released in Western Sicily (Mineo, 

Mineo, & Sinacori, 2001). In 2000–2001 more than 3,000 specimens were released 

in Eastern Sicily (Conti, Raciti, Campo, Siscaro, & Reina, 2001). The eulophid was 

recovered in all the release sites (Conti et al., 2001) and also overwintered far from 

them (Mineo et al., 2001). Observations carried out in the following years showed 

its permanent establishment with a contribution to parasitization which increased 

from around 5% in 1999–2000 to almost 60% in 2001–2007. 

Semielacher petiolatus (Fig. 6) is a solitary ectoparasitic wasp which lays eggs 

on P. citrella second and third instar larvae (Fig. 7), although it frequently 

parasitizes also prepupae (Bouček, 1988; Argov & Rössler, 1998; Mineo & Mineo, 

1999b; Ateyyat, 2002; Lim & Hoy, 2005). It has been observed developing on 

alternative hosts, such as Diptera Agromyzidae Agromyza hiemalis Becker on 

Urtica spp., Chromatomyia horticola (Goureau) on Sonchus spp. and Liriomyza sp. 

on Merculiaris annua L. and Lepidoptera Cosmopterix pulchrimella Chambers 

(Cosmopterigidae) on Parietaria diffusa M. & K., Stigmella aurella (Fabr.) 

(Nepticulidae) on Rubus ulmifolius Schott and Dialectica scalariella Zeller 

(Gracillariidae) on Echium sp. (Massa & Rizzo, 2000; Massa et al., 2001). 

Figure 7. Semielacher petiolatus egg (yellow arrow) laid close to a CLM larva. 

The parasitoid, after various larval instars, pupates in host mines (Fig. 8) and 

parasitized CLM larvae will not complete their development. The life cycle is 

completed in 10 days at 25°C. Host feeding was observed in the laboratory (Argov 

& Rössler, 1998). Semielacher petiolatus has been recovered on P. citrella in 

Australia (Bouček, 1988) and in Solomon Islands (Schauff et al., 1998). The 

eulophid has been introduced in Cyprus, Israel, Morocco, Oman, Syria, Tunisia, 

Turkey (Schauff et al., 1998), Egypt (Hamed, Reckhaus, Mahrous, Soliman, & 

Gassert, 1999), Greece (Michelakis, 1997) and Spain (García-Marí et al., 1997). In 

2003 adults of S. petiolatus were imported from Italy to Florida but after the 

evaluation in the quarantine facilities in order to verify the potential effectiveness of


85 

S. petiolatus as a natural enemy of the Citrus leafminer in Florida it was decided not 

to release it in the field (Lim & Hoy, 2005; Lim, Zappalà, & Hoy 2006). In Italy the 

parasitoid has been detected for the first time on P. citrella in 1998 (Mineo et al., 

1998), performing interesting parasitism activity (Caleca, Lo Verde, Blando, & Lo 

Verde, 1998). Further observations have shown its spontaneous diffusion in all 

citrus orchards in Southern Italy (Viggiani, 2001). This record together with 

Algerian (Schauff et al., 1998) and Jordanian ones (Mineo, 1999), reveals its 

dispersal capability in Mediterranean citrus areas (Siscaro et al., 2000). 

Figure 8. Semielacher petiolatus larva (left) and pupa (right). The leaf cuticle has been 

removed to reveal the parasitoid instars. 

As reported for C. phyllocnistoides, also for S. petiolatus accidental 

immigration and establishment was observed in Portugal in 2003 where the 

parasitoid is now very frequently present (Gomes da Silva et al., 2006). In 1999– 

2000 S. petiolatus contribution to the total CLM biological control in Italy was 

around 90% (Mineo & Mineo, 1999b; Conti et al., 2001). In summer 2001 the 

eulophid was still the most efficient P. citrella parasitoid, showing an incidence on 

the total parasitization activity near 80%. Nevertheless during fall of the same year, 

the main biological control was also due to C. phyllocnistoides. In the following 

years the role of this last species greatly increased (up to 60%) being still more 

active in the final part of the CLM infestation season (September–October), while S. 

petiolatus is mainly active in early summer. 

Several indigenous Hymenoptera parasitoids belonging to the family Eulophidae 

have been obtained from samples collected in Italian citrus groves infested by 

P. citrella. The main species were Cirrospilus pictus (Nees) and Pnigalio agraules 

(Walker) and, as observed in other Mediterranean citrus growing areas (Garrido

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L. ZAPPALÀ 

Vivas, 1995; Argov, Rössler, & Rosen, 1995), the incidence of the first one on the 

parasitization has reached 80–90% (Caleca et al., 1998; Caleca & Lo Verde, 1998; 

Conti et al., 2001). Moreover, the following species have been occasionally detected 

in Sicily: Apotetrastichus postmarginalis (Bouček), A. sericothorax (Szelényi), 

Asecodes delucchii (Bouček), A. erxias (Walker), Neochrysocharis formosa 

(Westwood) and Ratzeburgiola incompleta Bouček. Finally, other eulophids have 

been rarely recovered: Aprostocetus spp., Baryscapus sp., Chrysocharis pentheus 

(Walker), Cirrospilus diallus Walker, C. nr. lyncus (Nees), C. vittatus Walker, 

Diglyphus isaea (Walker) and Pnigalio soemius (Walker) (Viggiani & Giorgini, 

1995; Benfatto, 1996; Caleca, Lo Verde, & Massa, 1996; Liotta, Peri, Salerno, Di 

Cristina, & Manzella, 1996; Caleca et al., 1998; Caleca & Lo Verde, 1998; Giorgini 

et al., 1998; Lo Pinto & Salerno, 1998; Mineo, 1999; Conti et al., 2001). 

Starting from 1999 to 2002 the exotic eulophids C. phyllocnistoides and 

S. petiolatus have progressively substituted almost all the indigenous parasitoids 

previously detected on P. citrella, inducing a decrease of their parasitism to less than 

one third of what had been recorded, up to 1998. 

The high degree of specificity reached by P. citrella parasitic complex represents 

an important element in the biological control of this pest. The data collected in the 

main Italian citrus growing areas from 1996 up to now reveal an activity of the 

parasitoids (including both parasitization and host feeding) that has grown from 32% 

(1996–1998) up to 65% in more recent years (Siscaro & Reina, 2005), mainly 

thanks to the biocontrol activity of the 2 exotic eulophids S. petiolatus and C. 

phyllocnistoides. These species permanently established in Sicilian citrus groves 

showing a contribution of 90% to the total parasitization (Siscaro, Caleca, Reina, 

Rizzo, & Zappalà, 2003). Besides, a seasonal alternation in their activity was 

highlighted: S. petiolatus parasitization is in fact mainly concentrated in the first 

months of CLM infestation (June–August), while C. phyllocnistoides activity is 

more intense in the second part of the season (September–October) (Siscaro et al., 

2003). 

The establishment of the introduced eulophids is most likely related to the 

presence of alternative hosts (Massa et al., 2001; Massa & Rizzo, 2001; Lo Duca et 

al., 2002), and their seasonal alternation could be partly explained by the different 

biological and ecological attitudes the two species showed on hosts of native flora 

(Rizzo, 2003). Therefore it is important to maintain a rich biodiversity in citrus 

groves in order to provide alternative food and shelter to CLM parasitoids, mainly in 

winter and spring, when CLM populations are at their minimum levels. 

Biological control, together with cultural techniques based on reducing irrigation 

and fertilization with the aim of containing excessive vegetation, has proved 

effective in containing P. citrella infestations in adult citrus orchards. The situation 

is different on young and re-grafted trees, as well as in nurseries where damage 

caused by the leafminer may be more serious. In these cases chemical treatments can 

be applied using cytotropic or systemic insecticides, or insect growth regulators 

which, for their mode of action, should be employed sooner than the previous 

compounds. Mineral oils also have a repellent action on egglaying females and a 

reduced impact on the ecosystem. They can be used at a dose of 0.5–1 l/hl which 

protects the plants for 6–10 days, without rain, and the treatments must be applied


87 

sooner than the other larval insecticides in the infestation season (Siscaro & 

Zappalà, 2004). 

2.4. Planococcus citri (Risso) 

This mealybug (Hemiptera: Pseudococcidae), commonly known as Citrus mealybug, 

is reported as citrus pest in the Mediterranean basin together with five other 

mealybug species. It has uncertain origins, but recent findings on its main 

parasitoids indicate that it has spread from central Africa (Franco, Suma, Borges de 

Silva, Blumberg, & Mendel, 2004) and is now present almost worldwide. 

The adult female (1.6–3 mm long) has a convex body covered with a waxy 

secretion and is surrounded by 18 pairs of lateral filaments, with slightly increasing 

length from the head to the abdomen. Antennae and legs are well developed. A 

ventral circulus is present on the ventral part of the abdomen. The ovipositing 

female produces a white ovisac that covers the eggs. The light yellow crawlers are 

highly mobile. 

It is a very polyphagous species which can infest almost all species and varieties 

of citrus with a different degree of susceptibility (Franco et al., 2004), as well as 

several other agricultural and ornamental crops such as ficus, gardenia, jasmine, 

oleander, persimmon, pothos, pittosporum, rhododendron, etc. 

It mainly overwinters as immature female but also younger instar nymph, which 

can be found in crevices on trunks and branches. It performs several generations per 

year (more than 5) and is favoured by warm and humid climate. Small colonies of 

the mealybug start settling in early summer, near the calyx of little fruits, in the 

contact points between them or, for some varieties, in the navel. High population 

levels are reached in late summer-fall. Several agronomic factors can favour the 

presence of P. citri, such as particularly dense and dark canopy, clusters of fruits, 

presence of navel, excess in nitrogen fertilization and irrigation. A very important 

role in the growth and dispersal of P. citri colonies is played by ants, which usually 

breed the mealybug, carrying it in good feeding sites in order to increase the 

production of honeydew which they feed on. Ants also protect P. citri from its 

natural enemies, thus disrupting biological control. 

Planococcus citri infestations can produce a reduction in plant growth and in 

fruits size, as well as fruit downgrading, caused by the presence of colonies with 

chlorotic areas surrounding the mealybug feeding sites and sooty mould developing 

on honeydew. High infestations can also cause defoliation, fruit splitting and fruit 

drop. Besides, some secondary pests such as the Honeydew moth Cryptoblabes 

gnidiella (Millière) (Lepidoptera: Pyralidae), may develop on fruits infested by the 

Citrus mealybug. 

Several species of indigenous natural enemies are reported, such as the predators 

Sympherobius spp. (Neuroptera: Hemerobiidae), Scymnus spp. (Coleoptera: 

Coccinellidae), Dicrodiplosis spp. (Diptera: Cecidomyiidae) and Leucopis spp. 

(Diptera: Chamaemyiidae), and the parasitoids Anagyrus pseudococci s.l. and 

Leptomastidea abnormis (Girault) (Hymenoptera: Encyrtidae). They all actively 

contribute to the control of the Citrus mealybug, although this is essentially due to

88 

L. ZAPPALÀ 

the activity of the two encyrtids which can reach parasitization levels respectively of 

up to 60% A. pseudococci (Raciti, Barraco, & Conti, 2001) and 18–60% L. abnormis 

(Viggiani, 1974; Longo, 1985). The first species is already present in June, even 

though at very low densities, and it shows peaks of activity in August–September 

(Raciti et al., 2001). 

The control of P. citri represents a very good example of application of IPM 

strategies. Satisfactory results have been achieved with inoculative releases of the 

endoparasitoid Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae). This 

species is native to Central America and was introduced in Italy for the first time in 

1955 for the biological control of P. citri (Zinna, 1960). Later, it was re-introduced 

in almost all Italian citrus growing regions (Longo, Mazzeo, & Siscaro, 1994). 

However, in the climatic and ecologic conditions of North-Mediterranean citrus 

growing areas, L. dactylopii is not able to overwinter and therefore needs to be 

reared and periodically inoculated in the field through releases replicated every year 

(Katsoyannos, 1996; Longo et al., 1994). The releases must be preceded by the 

localization of infested trees, on which 20–30 adult parasitoids per tree will be 

inoculated around May–June. In this period the average temperature is higher than 

15°C and the first young Citrus mealybug females start moving from the trunks to 

the fruits or the initial small colonies begin settling (Longo et al., 1994). The 

releases can be repeated, if necessary, in June–July up to a total of 2,000 

specimens/ha (Raciti et al., 2001). However, the encyrtid has proved effective in 

controlling the Citrus mealybug, reaching parasitization levels in some cases higher 

than 90% (Mineo & Viggiani, 1976; Longo & Benfatto, 1982; Spicciarelli, 

Battaglia, & Tranfaglia, 1994; Fronteddu, Basoni, Canu, Fancello, & Nanni, 2000). 

Other exotic species that were introduced to control the Citrus mealybug are the 

predators Cryptolaemus montrouzieri Mulsant and Nephus reunioni Fürsch 

(Coleoptera: Coccinellidae) and the parasitoid Coccidoxenoides perminutus Girault 

(Hymenoptera: Encyrtidae). Cryptolaemus montrouzieri was first introduced in Italy 

in 1908 and established in Italian citrus orchards but in case of unfavourable 

climatic conditions or irrational chemical treatments its populations can be strongly 

reduced and need to be reintegrated by means of inoculative releases. Nephus 

reunioni was instead introduced in Italy in 1985 but didn’t manage to establish and 

its predatory activity was unsufficient to control P. citri populations (Longo & 

Benfatto, 1987). The parasitoid C. perminutus established, but occurs in the field at 

very low densities (Franco et al., 2004). 

Pheromone traps may be used to monitor the pest population dynamics in the 

field but, given the inconsistent correlation between the number of captures and the 

levels of infestation on fruits (Franco et al., 2001; Franco, Gross, Silva, Dunkelblum, 

& Mendel, 2002), this technique should be joined by the direct observation of fruits 

(10 fruits on 10% of the trees) to verify the levels of infestation in relation to the 

economic threshold (5–10% of infested fruits). 

However, the traps, if placed early in May, are a very useful tool to detect the 

beginning of the mealybug activity in order to plan eventual releases of natural 

enemies after evaluating the presence of overwintering females on the trunk and 

branches, identifying the infested trees to be used as release spots and evaluating the 

occurrence and the activity of ants. These may in fact protect honeydew producing


89 

pests from their natural enemies thus disrupting their control action (Delabie, 2001; 

Eubanks, Blackwell, Parrish, Delamar, & Hull-Sanders, 2002; Kaplan & Eubanks, 

2002). The negative role played by ants in biological control programs suggests to 

manage their populations using one of the various available techniques, including 

cultural methods such as canopy pruning to avoid contact with weeds and soil tillage 

to disturb their nests, as well as chemical or mechanical methods using insecticidetreated 

baits, sticky or insecticide-treated bands placed around the trunk and ground, 

trunk or foliar treatments with insecticides (Tumminelli, Saraceno, & Conti, 1997; 

Benfatto, 1999; Franco et al., 2004). In Italian citrus orchards the most common ant 

species that are known to have interactions with honeydew-producing insects, thus 

potentially disrupting the control activity of their natural enemies, are Lasius alienus 

(Förster), Tapinoma nigerrimum (Nylander) and Camponotus nylanderi Emery (La 

Pergola, Alicata, & Longo, 2008). Pheidole pallidula Nylander is also quite 

abundant in citrus orchards and although it is a typical terricolous species, it has 

been seen foraging on colonies of sapsucking insects (La Pergola, 2008). 

Chemical control of P. citri should be applied in case of high infestations, using 

IGRs, such as buprofezin, in summer-fall or, in the fall, organophosphates such as 

chlorpyrifos-methyl. Good results can also be obtained with mineral oils. 

Present researches focus on the enhancement of the activity of native parasitoids 

(namely A. pseudoccocci s.l.) by using semiochemicals (Franco et al., 2008). 

2.5. Ceratitis capitata (Wiedemann) 

This species, commonly known as Mediterranean fruit fly, is widely distributed in 

Sub-Saharian Africa (from where it probably originated), in the Mediterranean basin 

(including France and the Balkans up to Hungary), in the Middle East, in Saudi 

Arabia, in Central and South America, in Western Australia and in Hawaii. In 

Germany it has been observed several times attacking fruit but it is not permanently 

established. In Mexico, Florida and California its occurrence has been faced through 

eradication programs, however hypothesis of permanent establishment have been 

formulated. 

The adult is 3.5–5 mm long, yellowish with brown tinge, especially on abdomen 

and legs. Eyes are reddish-purple and ocellar bristles are present. Male has a pair of 

bristles with enlarged spatulate tips next to the inner margins of the eyes. Thorax is 

creamy white to yellow, with characteristic pattern of black blotches. Light areas 

with very fine white bristles are present as well as humeral bristles. Scutellum is 

enlarged and shiny black. Abdomen is oval with fine black bristles scattered on 

dorsal surface and 2 narrow transverse light bands on basal half. Ovipositor, when 

extended, is 1.2 mm long. Wings, usually held in a drooping position on live flies, 

are broad and hyaline with black, brown and brownish yellow markings. One 

longitudinal orange-yellowish band crosses middle of wing, two similar transversal 

bands are present on the caudal part of the wings. 

The egg is shiny white, elongate, slightly curved, tapering and 1 mm long, with 

micropylar region distinctly tubercular. The mature larva is 7–9 mm long,

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yellowish-white, slender, elongate, tapering anteriorly. The pupa is reddish-brown, 

4.5 mm long. Some strains have pupae of different colour in the two sexes. 

The Mediterranean fruit fly is known to attack more than 260 different fruits, 

flowers, vegetables and nuts. Thin-skinned, ripe succulent fruits are preferred (apple, 

apricot, coffee, fig, Indian fig, loquat, peach, pear, persimmon, strawberries, etc.). 

Although it may be a major pest of citrus (Fig. 9), often it is a more serious pest of 

some deciduous fruits, such as peach, pear, and apple. 

Using the oviscapt the female lays eggs in clusters of 1–15 (in relation to the size 

of the fruit), about 2–5 mm deep under the skin of fruits. Oviposition may take from 

2 to 20 min. Although each female after oviposition normally labels the fruit with 

deterrent substances, several females may lay eggs in the same fruit and up to 80 

eggs may be found. This might be related to the decreased deterring efficacy on 

large fruits. One single female may lay as many as 22 eggs/day and as many as 800 

during her lifetime (usually about 300). The females are attracted by visual and 

olfactory cues and normally choose the same kind of fruit during each oviposition 

cycle. Females usually die soon after they stop laying eggs. When the eggs hatch, 

the larvae promptly begin feeding on the pulp of fruits and about 15 days at a mean 

temperature of 25°C are necessary to complete their development. 

Figure 9. Ceratitis capitata adult female on a citrus fruit. 

Larvae pass through 3 instars. In cooler regions the species usually overwinters 

as pupa (while in warm climates it develops without interruptions), buried a few 

centimetres deep in the soil. In southern areas, a small number of individuals may 

also survive on late-season oranges. The pupa does not survive if temperatures are 

lower than 2°C for a week. 

Development of this fruit fly is mainly dependant on temperature. The optimum is 

around 32°C, which allows a generation to be completed in 2 weeks. Females will not 

oviposit when temperatures drop below 16°C, except when exposed to sunlight for


91 

several hours. Development stops at 10°C. Pupae carry the species through 

unfavourable conditions. During warm weather eggs hatch in 1.5–3 days. The duration 

of the egg stage is considerably increased by lower temperatures. Larval life may be as 

short as 6–10 days when the mean temperatures average 25-26.1°C. The kind and 

ripening conditions of the fruit often influence the length of the larval stage. In citrus 

fruits, especially limes and lemons, it appears to be longer. Thus, larvae require 14–26 

days to reach maturity in a ripe lemon, as compared with 10–15 days in a green peach. 

Mature larvae, which are able to jump, leave the fruit in largest numbers at or just after 

daybreak and pupate in soil. Minimum duration of the pupal stage is 6–13 days when 

the mean temperature ranges from about 24.4 to 26.1°C. 

The largest numbers of adults emerge early in the morning during warm weather 

and more sporadically during cool weather. They can actively fly short distances, 

although they can cover longer distances carried by the wind. Newly emerged adults 

are not sexually mature. Males often show sexual activity 4 days after emergence. 

They produce a sexual pheromone which attracts females but is also perceived by 

other males and even by human olfaction. Both sexes are sexually active throughout 

the day. When the daily mean temperature averages 24.4–25.6°C most females are 

ready to mate from 6 to 8 days after eclosion. Mating lasts from 2 to 4 h; males 

usually mate several times, while 60% of females mate only once. 

The Mediterranean fruit fly is one most noxious fruit pests in the world. Because 

of its worldwide distribution, its ability to tolerate colder climates better than most 

other species of fruit flies, and its wide range of hosts, it is ranked first among 

economically important fruit fly species. In some of the Mediterranean countries, 

only the earlier varieties of citrus are grown, because the flies develop so rapidly 

that late season fruits are too heavily infested to be marketable. Harvesting before 

complete maturity also is practiced in Mediterranean areas generally infested with 

this fruit fly. 

The damage caused by C. capitata is considerable, particularly in summer and 

autumn. Infestation is indicated on the fruit by a variously coloured area, depending 

on the host, surrounding the oviposition puncture. Rotting of the underlying tissue 

causes a depression on the surface and the fruit drops prematurely. Even if a fruit 

has only been pierced for egg laying (without actual presence of living instars), it is 

totally unsaleable. On citrus fruits the oviposition punctures cause acceleration in the 

ripening process of the external tissues and the subsequent early drop of the fruits, 

also because of the occurrence of secondary infestations and infections. 

The constant global exchanges of goods and people may greatly facilitate 

transportation of the Mediterranean fruit fly in areas where it is not yet present, 

therefore making the efforts to contain it within its current distribution almost 

useless. Once the species is established, eradication efforts may be extremely 

difficult and expensive. In addition to reduction of crop yield, infested areas have 

the additional expense of control measures and costly sorting processes for both 

fresh and processed fruit and vegetables. Besides, the presence of C. capitata may 

strongly affect exportation to those countries where the species is not present or 

permanently established. 

Several species of entomophagous have been reported in the entire area of 

distribution of this fruit fly. Some of them have been imported from Africa and

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L. ZAPPALÀ 

Australia. Effective parasitoids of C. capitata are Psyttalia concolor (Szlep.) 

(Hymenoptera: Braconidae) and Pachyneuron vindemmiae (Rond.) (Hymenoptera: 

Pteromalidae). Efforts have been made to develop biological control programs using 

P. concolor, but with very limited success. This is mainly due to the high intrinsic 

rate of increase of the Mediterranean fruit fly and also to the behaviour of larvae, 

which feed and develop inside the fruits and therefore easily escape parasitization by 

braconid wasps, especially when infesting large fruits. In the Mediterranean basin, 

natural control is mainly carried out by microorganisms and occasional predators 

(Coleoptera Carabidae and Staphylinidae, Hymenoptera Formicidae of the genus 

Crematogaster), mostly active in soil against larvae and pupae. 

Cultural control methods, such as reducing the favourable host plants 

consociations, eliminating the infestation site and destroying infested fruits, are 

fundamental elements in field programs aiming at reducing the Mediterranean fruit 

fly populations. 

Chromotropic and chemotropic traps are used to attract adults. Males of C. 

capitata are known to be attracted by essential oils from Angelica archangelica L., 

which contain several sesquiterpene hydrocarbons (α-copaene, α-ylangene, etc.). 

The same kind of molecules are also contained in coriander, mint, thyme and citrus 

essence. However, none of these compounds found practical application, differently 

from what happened for esters of the methylcyclohexanecarboxylic acid: siglure, 

medlure, trimedlure. Other attractants commonly used are also ammonium 

compounds (diammonium phosphate) and hydrolyzed proteins. These compounds 

attract both males and females (while parapheromones attract only males) within a 

range of 20 m, but they mainly attract females looking for proteins. However these 

attractants are less selective towards beneficials. 

A possible control method is the “attract and kill” technique which is based on 

the use of devices pre-treated with a pyrethroid (mainly deltamethrin or lambdacyhalothrin) 

and activated with trimedlure or with hydrolyzed proteins. This 

technique is suggested on orchards with a minimum extension of 5 ha, unless they 

are isolated enough. 

Chemical control can be performed using deltamethrin, etofenprox, phosmet and 

spinosad bait which has been recently authorized on citrus in Italy. In order to 

contain the negative secondary effects on the biocenosis it is highly recommended to 

perform localized treatments adding protein baits to the toxic compound. The 

treatments should be started in mid-July and repeated every 25–30 days, spraying 

trees only partially on one every two–three rows, and using around 200 l of solution 

per hectare. The treatments should be extended to the whole orchard when 20 or 

more adults are captured on the traps and/or after the first punctures on the fruits are 

observed. The results of trials carried out to evaluate in the field the repellent and 

oviposition deterrent effect of clays and copper products, that can also be used in 

organic groves, showed that kaolin can be applied to reduce the percentange of 

infested fruits (showing C. capitata punctures) at harvest (Caleca, Lo Verde, 

Palumbo Piccionello, & Rizzo, 2008). 

In several countries severe quarantine measures are applied, strongly affecting 

importation, in order to avoid the introduction and the permanent establishment of 

the Mediterranean fruit fly. Infested or potentially infested fruits are rejected or


93 

treated with fumigants or with low temperatures (2 weeks at 1°C), in order to 

eliminate all living instars present inside the fruits. 

3. SECONDARY PESTS 

Whiteflies, and namely the Woolly whitefly A. floccosus, are among the arthropod 

pests whose infestations in Italy greatly decreased over the last decades. Initially A. 

floccosus was considered of great economic importance because of the serious 

damage it can cause, mainly due to the very large amount of phloem sap sucked out 

from all parts of the tree both by the adults and the nymphs and the consequent 

production of huge amounts of honeydew. In case of strong infestations by this 

whitefly, blacken of citrus plants by sooty moulds is conspicuous and in such 

situations, honeydew, sooty mould and waxy secretions tend to mix up together, 

forming a continuous and hardly permeable cover on the lower surface of the leaves. 

Moreover, this whitefly has a strict relation with ants which protect the colonies 

interfering with the activity of natural enemies of this and also of other pests. 

However, biological methods have proved effective in controlling this species. 

In particular after the arrival of A. floccosus in Italy (in the 1970s), the parasitoid 

Cales noacki Howard (Hymenoptera: Aphelinidae) was introduced. This species, 

native to South America, had already been imported in France in the 1970s (Onillon 

& Onillon, 1972) and was then introduced in Southern Italy in 1980 (Liotta & 

Maniglia, 1983; Longo, 1985). The beneficial insect was reared on its natural host, 

feeding on citrus trees both in insectaries and in the field. From these “bank plants” 

branches bearing parasitized whitefly colonies were collected and used to spread out 

the parasitoid in the field, directly by farmers. The parasitoid showed an intense 

activity reaching levels of parasitization higher than 80%, and managed to 

permanently establish also feeding on other hosts. It did not require further 

inoculations, except in orchards submitted to several chemical treatments (Longo et 

al., 1994). In the citrus growing areas where the climatic conditions are not 

unfavourable to the parasitoid (it is mainly affected by high summer temperatures) 

and where integrated pest management is performed with rational use of pesticides, 

the Woolly whitefly is almost always kept under adequate control by the aphelinid, 

without requiring further specific control treatments. 

Together with C. noacki, another parasitoid, the platygastrid Amitus spiniferus 

(Bréthes) was introduced, reared and released following the same technique used for 

the aphelinid. Although this second entomophagous was at first only found in low 

numbers and immediately after the releases, it is now quite widespread in all citrus 

growing areas and contributes to the control of A. floccosus infestations. Chemical 

control is therefore normally not necessary against the Woolly whitefly, at least in 

areas where natural enemies are protected and their action is promoted. 

Similarly, two other exotic whitefly species, D. citri and P. myricae, have been 

successfully contained in the framework of classical biological control programs. 

The first species, native to India, was first recorded in Italy in 1965 and initially 

caused very heavy infestations. Presently it has almost disappeared, thanks to the 

effective control performed by the parasitoid Encarsia lahorensis (Howard)

94 

L. ZAPPALÀ 

(Hymenoptera: Aphelinidae) introduced in Italy from California in 1973 (Viggiani 

& Mazzone, 1978). The entomophagous was distributed throughout the main citrus 

growing areas of Southern Italy using plants or parts of plants bearing Citrus 

whitefly parasitized colonies. It permanently established and managed to effectively 

control the populations of the pest which rapidly became a species of minor 

importance in Italian citrus orchards (Longo et al., 1994). 

In 1990 the Japanese bayberry whitefly, P. myricae, was reported for the first 

time in Italy (Rapisarda, Siscaro, Leocata, & Asero, 1990). This polivoltine, 

polyphagous homopteran, with a strong tendency to parthenogenesis, is highly 

efficient in colonizing new areas. It mainly develops on new shoots and frequently 

lays eggs along the leaf margin which at maturity show a typical serrate aspect. 

Several parasitoids, such as the aphelinids C. noacki and Encarsia meritoria Gahan, 

adapted to develop on this whitefly without, however, successfully containing its 

populations. Therefore, in order to enlarge the parasitic complex, the aphelinid 

Eretmocerus debachi Rose & Rosen was imported from Israel in several citrus 

growing regions. The newly introduced entomophagous established, rapidly reached 

parasitization levels of 20–30% and showed a remarkable spreading capacity. 

Thanks to these characteristics the endoparasitoid managed to successfully control 

the whitefly as it had already happened in other Mediterranean citrus growing areas 

(Rose, De Bach, & Woolley, 1981). The Japanese bayberry whitefly is now only 

very rarely present in citrus orchards and no chemical treatment is required, because 

of the effective control performed by its natural enemies. 

Finally, other pests, which are normally considered as secondary since they are 

kept under control by a rational agronomic management of the orchard, by a reduced 

use of pesticides and by an effective natural enemies complex, are: the soft scales 

Ceroplastes rusci, Coccus hesperidum L. and Saissetia oleae, the armoured scale 

Parlatoria pergandii, the moths Prays citri Mill. and Archips rosanus. Three species 

of aphids [Aphis spiraecola, A. gossypii and Toxoptera aurantii (B.d.F.)] are 

considered particularly noxious to young and regrafted trees. However, the direct 

damage caused by these pests is by far less important than the indirect damage 

related to their capacity of transmitting viral diseases and namely the Citrus Tristeza 

Virus. In particular A. gossypii is considered, in the Mediterranean basin as well as 

in other citrus growing regions of the world, the main vector of this virus in those 

areas where its most efficient specific aphid vector (Toxoptera citricidus) is still 

absent (Bar-Joseph & Loebenstein, 1973; Yokomi, Joost, & Backus, 2005). 

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5 

ENTOMOPATHOGENIC NEMATODE ECOLOGY 

AND BIOLOGICAL CONTROL IN FLORIDA 

CITRUS ORCHARDS 

RAQUEL CAMPOS-HERRERA 1 , ROBIN J. STUART 1 , FAHIEM 

EL-BORAI 1, 2 , CARMEN GUTIERREZ 3 AND LARRY DUNCAN 1 

1 University of Florida, IFAS 



2 Plant Protection Department, 

Faculty of Agriculture, 

Zagazig University, Zagazig, Egypt 

3 Departamento de Agroecología, Instituto de Ciencias Agrarias, 

Centro de Ciencias Medioambientales CSIC, 

Madrid 28006, Spain 

Abstract. Biological control through augmentation of entomopathogenic nematodes (EPNs) in soil is an 

important component of integrated pest management (IPM) of the root weevil, Diaprepes abbreviatus, in 

Florida citrus orchards for over 20 years. However, to improve the effectiveness of EPNs for weevil 

control substantial information is needed about the post-application biology of EPNs as well as the 

ecology and importance of endemic species for weevil management. Current status of EPNs 

augmentation as a weevil control tactic, their role in soil food webs in different habitats, and the 

biocontrol potentials of endemic EPN communities, are reviewed. We also discuss molecular approaches 

to assess EPN population distribution and dynamics, and how these techniques could contribute to our 

understanding of nematodes ecology to enhance EPNs in biocontrol. Basic and applied study of EPNs 

increased during the past half-century, accelerating awareness of limitations for many conventional 

management practices. Understanding the EPNs population biology is necessary to discover and exploit 

new ways to increase their efficacy and reliability for biological control in managed ecosystems. 


Since the era of synthetic pesticide development accelerated in the mid-twentieth 

century, the management of citrus groves worldwide has generally evolved from a 

heavy reliance on prophylactic insecticide use to a more rational application of these 

101 



DOI 10.1007/978-90-481-8606-8_5, © Springer Science+Business Media B.V. 2010

102 

R. CAMPOS-HERRERA ET AL. 

chemicals within integrated pest management (IPM) programs. IPM typically 

reduces pesticide use by monitoring both pest and beneficial organisms, and 

predicting crop loss as the basis for management decisions (Timmer & Duncan, 

1999). Nevertheless, the quantities of synthetic pesticides used in orchards remain 

significant and pose serious threats to the environment, especially natural biological 

control processes, wildlife, groundwater contamination, resource depletion, and 

human health and safety (Edwards, 1993; Pimentell et al., 1993). Recognition of 

these concerns has led to increased interest in organic methods for crop and pest 

management in citriculture; and biological control, whether conducted as classical, 

augmentation or conservation biological control, necessarily plays a pivotal role. 

When considering the costs and benefits of various management paradigms, it is 

noteworthy that increased chemical inputs do not necessarily result in increased 

output per unit area. In the Mediterranean Basin, Spanish and Italian citrus growers 

use 4-fold and 15-fold greater quantities of pesticides than do Greek growers, but 

obtain similar citrus production per hectare (Gutiérrez et al., 2005). Nevertheless, 

pest management is of frequent and critical concern in all agricultural endeavours, 

and the development of sustainable pest management systems requires a 

fundamental understanding of how populations of pests and their natural enemies 

behave in specific crop habitats (Hoy & Herzog, 1985; Flint & Dreistadt, 1998; 

Rechcigl & Rechcigl, 2000; Horowitz & Ishaaya, 2004). 

In Florida citrus orchards, pesticide use during the last quarter of the twentieth 

century decreased steadily as a succession of pests were shown to be manageable 

through biological control by endemic or introduced natural enemies. Growers 

learned that fruit destined for juice processing could usually be produced without the 

use of insecticides and that fruit grown for the fresh market often required no more 

than a few well-timed pesticide treatments to manage mites and fungi that cause rind 

blemishes. Copper sprays and petroleum oils were the primary pesticides used 

during this period, and serious outbreaks of scale and other soft body pests were rare 

and almost always associated with disruption of biological control through 

unnecessary use of pesticides. 

Unfortunately, the limited use of pesticides and widespread success of 

biological control in Florida citrus groves came to an abrupt halt when the 

devastating bacterial disease known as “Huanglongbing” or “citrus greening” caused 

by the bacterium Candidatus Liberibacter asiaticus, was detected in the state for the 

first time in 2005. Citrus greening is vectored by the Asian Citrus Psyllid, 

Diaphorina citri, infects all known citrus cultivars, spreads rapidly, and is lethal to 

trees. Growers attempt to slow the spread of the disease by removing infected trees 

and suppressing the vector with frequent applications of systemic and topical 

insecticides. Consequently and predictably, many secondary pests are increasing in 

Florida citrus orchards, and psyllid resistance to most classes of insecticides is 

becoming widespread. Moreover, the increased production costs and diminishing 

effectiveness of these intensive pest management practices are coinciding with lower 

citrus prices, largely due to the increased availability of other fruit juices, to 

significantly lower the profitability of Florida citriculture. In view of this crisis, the 

future of the Florida citrus industry is uncertain. However, fundamental research to 

understand and control citrus greening is being heavily supported by federal, state

IPM THROUGH ENTOMOPARASITES 

103 

and private sources, and hopefully will lead to new and more effective strategies to 

deal with this problem. 

Prior to the introduction of citrus greening and its psyllid vector into Florida, 

the Diaprepes Root Weevil, Diaprepes abbreviatus, was considered the most 

important insect pest of citrus, and it remains a serious problem (Graham, McCoy, & 

Rogers, 1996; Graham, Bright, & McCoy, 2003; Duncan, Shapiro, McCoy, & 

Graham, 1999; McCoy, 1999). Like citrus greening, the weevil can kill trees and 

cause entire orchards to become non-profitable in just a few years (Fig. 1) but, 

fortunately unlike greening, the most severe devastation appears limited to certain 

areas and grove conditions. For nearly 20 years, biological control through the 

augmentation of entomopathogenic nematodes (EPNs) to citrus soils has been an 

important component of weevil IPM in Florida and it continues to be an effective 

strategy in many groves. Moreover, recent research to improve the effectiveness of 

EPNs for weevil control has revealed substantial information about their postapplication 

biology as well as the ecology and potential importance of endemic EPN 

species for weevil management. In this chapter, we review the current status of EPN 

augmentation as a weevil control tactic in Florida citrus groves, the role of EPNs in 

soil food webs of different habitats in Florida, and possibilities for better exploiting 

the biocontrol potential of endemic EPN communities. 

Figure 1. Twenty-four-year-old citrus trees in flatwoods soil exhibiting typical 

symptoms of Diaprepes/Phytophthora pest-disease complex.

104 


2. IPM OF THE DIAPREPES-PHYTOPHTHORA COMPLEX 

2.1. Diaprepes Economic Importance, Biology and Management 

Diaprepes abbreviatus is highly polyphagous and a major economic pest not only of 

citrus, but of numerous ornamentals, vegetables, sugarcane, and other crops. It is 

native to the Caribbean where it has long been considered a serious agricultural pest 

(Wolcott, 1936). It was first detected in Florida in 1964 (Woodruff, 1964) and has 

spread to all citrus producing areas of the state. In 1997, the weevil was known to 

infest over 13,000 ha of commercial citrus and 50,,000 ha of other crops in 20 

Florida counties (Lapointe, Shapiro, & Bowman, 1999). Over the past 40 years, 

many citrus growers have experienced devastating losses of trees and entire groves 

due to D. abbreviatus. Annual losses and cost of control for the Diaprepes root 

weevil in Florida citrus were estimated at $72 million, whereas losses in 

ornamentals and vegetables were estimated at $2 million (Pena & Amalin, 2000). 

Diaprepes abbreviatus recently became established in Texas and California where it 

is considered a major threat to agriculture and is the subject of quarantine and 

eradication programs. 

The life cycle of this weevil is marked by lack of synchrony and extensive 

variability, characteristics that make it particularly difficult to control (McCoy, 1999). 

In Florida, adult D. abbreviatus emerge from soil throughout the year with a 

significant peak in spring and sometimes autumn (Stansly, Mizell, & McCoy, 1997; 

Duncan, McCoy, Stansly, Graham, & Mizell, 2001). The adults feed on new foliage, 

mating occurs in the canopy, and eggs are laid in masses glued between leaves by the 

ovipositing female. Individual females can produce more than 20,000 eggs during a 

lifetime that can last almost a year. The larvae hatch, drop to the soil, and burrow 

down to the roots where they begin feeding. As they grow, the larvae feed on larger 

roots, and pupation occurs in the soil after 9–11 larval instars. Typically, a broad range 

of instars occur in the soil simultaneously (Woodruff, 1985; Quintela, Fan, & McCoy, 

1998; McCoy, 1999; McCoy, Stuart, & Nigg, 2003; Nigg et al., 2003). 

Diaprepes abbreviatus feeding damage to the roots of citrus trees can be 

extensive (Fig. 2). Major structural roots are often girdled and killed; and, if the 

crown is girdled, then the tree dies. However, tree damage is greatest in the presence 

of the plant pathogenic oomycetes Phytophthora nicotianae or P. palmivora, which 

invade the roots at weevil feeding sites. The pest-disease complex is particularly 

severe in poorly drained soils that favor infection by the fungal zoospores (Graham 

et al., 1996; Duncan et al., 1999; McCoy, 1999). 

Control measures for D. abbreviatus include chemical insecticides, which can 

be applied as adulticides, egg sterilants, or soil barrier treatments for neonates 

(McCoy et al., 2009). The efficacy of all treatments is short-lived; and, therefore, in 

order to kill the maximum number of insects, growers are advised to monitor adult 

weevils as they emerge from soil and occupy the tree canopy. Pesticides should be 

applied at the onset of egg-laying, approximately 10 days following peak adult 

emergence. Nevertheless, because of the non-synchronous life cycle of this weevil, 

pesticides must be applied repeatedly to be effective, and such repeated applications 

can disrupt natural enemies and lead to additional pest problems. Moreover, the


105 

present chemical controls are only marginally effective compared to the 

organochlorine soil pesticides that were used previously and are now banned for 

environmental reasons (Duncan et al., 1999; McCoy, 1999). 

At present, the only recommended control for D. abbreviatus larvae in soil is the 

application of EPNs twice per year (Bullock, Pelosi, & Kidler, 1999; Duncan & McCoy, 

1996; Duncan, McCoy, & Terranova, 1996, Duncan et al., 2007; McCoy, 1999; McCoy, 

Shapiro, Duncan, & Nguyen, 2000). In the absence of pesticides, EPN augmentation 

twice annually in orchards on coarse sandy soil was shown to reduce adult weevil 

populations by more than half (Duncan et al., 2003, 2007). 

Figure 2. Excavated root system of 3-year-old citrus tree heavily damaged by 

Diaprepes abbreviatus larval feeding. Note the deep channels in major roots which 

provide infection courts for Phytophthora spp. 

2.2. EPN Biology and Use in IPM Programs 

Entomopathogenic nematodes in the genera Steinernema and Heterorhabditis are 

obligate lethal parasites of insects and are an attractive alternative to chemical 

insecticides because they kill insect pests very quickly, are safe to mammals, and have 

little or no direct effect on nontarget organisms (Bathon, 1996; Georgis, Kaya, & 

Gaugler, 1991). These nematodes typically occur in the soil and have an 

environmentally-resistant non-feeding infective juvenile (IJ) stage that actively seeks 

out and kills insect hosts (Kaya, 1990; Lewis, Gaugler, & Kaya, 1992; Grewal & 

Georgis, 1998). The nematodes kill their hosts with the aid of symbiotic 

entomopathogenic bacteria in the genera Photorhabdus and Xenorhabdus for

106 


Heterorhabditis and Steinernema, respectively. The bacteria are carried in the nematode 

intestine and released into the host upon infection (Poinar, 1990). Insect death usually 

occurs within 72 h of infection, and the nematodes feed, develop to adults, and 

reproduce within the host, often completing 2–3 generations, before producing a new 

generation of specialized IJs, which emerge from the cadaver and seek new insect hosts 

(Poinar, 1990). Because of their established safety to non-target organisms, EPNs are 

exempt from pesticide registration with the Environmental Protection Agency in the 

United States and are similarly exempt in many other countries. 

EPNs have been used effectively in classical biological control programs. For 

example, Steinernema scapterisci was discovered in Uruguay, near the presumed 

center of origin of the mole cricket (Scapteriscus spp.). The nematode was 

introduced into Florida where it is now established and, in combination with 

introduced parasitoids, provides effective biological control of several invasive mole 

cricket species (Nguyen & Smart, 1990; Adjei, Smart, Frank, & Leppla, 2006). Most 

commonly, however, EPNs are used for augmentation biological control where they 

function as biopesticides and treatment efficacy is expected to be of short duration, 

typically a matter of 1–2 weeks (McCoy et al., 2000; Duncan et al., 2003, 2007). In 

such programs, EPNs function in the same manner as non-persistent chemical 

pesticides and are applied repeatedly, as needed. 

Surveys have shown that some naturally occurring EPNs are more abundant in 

undisturbed compared to intensively farmed habitats (Campos-Herrera et al., 2008), and 

that use of various animal manure mulches can increase the prevalence of some EPNs 

(Bednarek & Gaugler, 1997; Duncan et al., 2007). Such observations suggest the 

possibility of developing conservation biological control tactics by which agricultural or 

other managed habitats are modified in ways that enhance natural control of arthropods 

by EPNs. However, reliable and effective conservation biological control tactics are as 

yet unknown and remain a matter of speculation (Lewis, Campbell, & Gaugler, 1998; 

Stuart, Barbercheck, Grewal, Taylor, & Hoy, 2006). 

In the Florida citrus industry, Steinernema carpocapsae was the first nematode to 

be developed commercially for root weevil control (Schroeder, 1987; Figueroa & 

Roman, 1990; Smith, 1994) but a further discovered species, S. riobrave (formerly S. 

riobravis) (Cabanillas, Poinar, & Raulston, 1994), was found to cause greater D. 

abbreviatus mortality (Schroeder, 1994; Duncan et al., 1996; Bullock et al., 1999) with 

some field studies reporting ~90% suppression (Duncan & McCoy, 1996; Duncan et 

al., 1996; Bullock et al., 1999). However, estimates of the efficacy and profitability of 

using EPNs for weevil control in citrus vary widely and probably reflect variation in 

factors such as product quality, application rates, suitability of edaphic conditions for 

EPNs, and experimental methods (Adair, 1994; Duncan et al., 1996; Duncan, Graham, 

& Zellers, 2002; Duncan et al., 2003; 2007; Bullock et al., 1999; Stansly et al., 1997; 

McCoy et al., 2000; McCoy, Stuart, Duncan, & Nguyen, 2002). Currently, S. riobrave 

is marketed in Florida under the brand name Bio Vector 355 (Becker Underwood Inc., 

Ames, IA) and, in 1999, approximately 19,000 ha of citrus were treated with this 

product to control citrus root weevils (Dimock, personal communication). 

Despite the evident and long-recognized potential of EPNs for insect pest 

management and the commercial development of effective EPN products for 

augmentation, their market penetration and incorporation into broadly applied IPM


107 

programs has been disappointing. In some crop-pest systems for which EPNs 

appeared promising, use of chemical pesticides or transformation of crop cultivars to 

express Bacillus thuringiensis toxins provided cheaper management options (Lewis 

et al., 1998; Shapiro-Ilan, Gouge, & Koppenhöfer, 2002). However, the greatest 

impediment to the use of EPNs is that they often appear less reliable and less 

effective than available chemical pesticides (Lewis et al., 1998). Extreme variability 

of soil physical and biological properties, even at a small scale, is probably one of 

the major causes of inconsistent performance of EPNs and most other soilborne 

biological control agents. Indeed, it would be remarkable if a single organism was 

able to provide consistently high pest control in the myriad soil habitats encountered 

in most crops. Moreover, although EPNs can be isolated from most soil habitats, 

EPN distributions are typically patchy and their equilibrium densities low, and these 

patterns tend to be quickly reestablished following an augmentation event (McCoy 

et al., 2000; Duncan et al., 2007). Habitats that support EPN equilibrium densities 

high enough and uniform enough to be suppressive to arthropod pests are apparently 

rare but, when identified, could reveal important traits and environmental conditions 

amenable to a conservation biocontrol approach involving EPNs. Advantages of 

such an approach could include an increase in the duration of EPN efficacy and, 

consequently, a reduction or elimination of the need for periodic augmentation of 

commercially formulated EPNs or use of chemical pesticides. 

2.3. Spatial Relationships Between Soils, Root Weevils and Endemic EPNs 

Damage to citrus caused by the Diaprepes root weevil is related to regional and local 

variation in orchard soils. Trees growing in finer textured soils or in low, wet areas are 

often more heavily damaged than trees growing in well drained, coarser textured soils. 

This undoubtedly is due at least in part to a higher incidence of Phytophthora spp. in 

finer, wetter soils. However, soil conditions also appear to have a large effect on 

weevil abundance. A 3-year survey of six orchards in which weevil abundance was 

measured weekly revealed a 10-fold greater weevil abundance in finer textured 

compared to coarser textured soils (Futch, Duncan, & Zekri, 2005). Florida citrus 

orchards are planted in regions characterized by different soil profiles. The “central 

ridge” is composed of very deep, well drained, uniformly sandy (>96% sand) soils. In 

contrast, the coastal and inland “flatwoods” regions have greater variation in soil 

texture and shallow water tables that require tree rows to be planted on raised beds for 

drainage and adequate rooting volume. Many flatwoods soils are sandy (80–95% 

sand), but the particle sizes of the sand fractions are smaller on average than those that 

characterize soils on the central ridge. Thus, weevil-infested orchards on the central 

ridge often exhibit little damage by D. abbreviatus, whereas orchards on fine-textured, 

poorly drained flatwoods soils are sometimes abandoned as unprofitable, due to an 

inability to manage the large weevil populations. 

Relationships between spatial patterns of D. abbreviatus and specific abiotic 

soil factors have been reported within and among sites (Li et al., 2003; Li, 

Syvertsen, McCoy, Stuart, & Schumann, 2004a; Li et al., 2007), but experimental 

evidence of direct causal relationships is lacking (Li et al., 2004b). Nonetheless, a 

growing body of evidence suggests that soils influence D. abbreviatus populations

108 


indirectly by affecting the community composition and predatory efficacy of 

endemic EPN species. Surveys that measured numbers of Diaprepes larvae falling 

from the canopy to the soil and numbers of adult weevils emerging from the soil 

over the course of 2 years concluded that the net survival rate from hatched egg to 

teneral adult is ~ 0.7–1.6% (McCoy et al., 2003). 

Figure 3. Representation of EPN population density distribution using a biplot in which 

vectors show the loading factors of the original variables on the associated factorial axes. 

(a) Association with cultural practices: NA, natural area, OPC, organic perennial crop, CPC, 

conventional perennial crop, OAC, organic annual crop, CAC, conventional annual crop. 

(b) Association with sand, silt and clay contents, available water, and organic N, Zn and Cu 

concentrations. Circles show EPN population density by increasing the diameter as 

population size increases (from Campos-Herrera et al., 2008).


109 

Therefore, if EPNs are important weevil larva predators, relatively small 

reductions in the rate at which EPNs prey on weevils could have a 

disproportionately large effect on increasing the weevil survival rate and, hence, the 

numbers of egg-laying adults in an orchard. Duncan et al. (2003, 2007) found that 

caged weevil larvae buried in orchards on the central ridge are killed, primarily by 

endemic EPNs, at an average rate of 53% per week (range 38–82%) compared to 

110 


highest on the central ridge (2.4), with significantly fewer (1.7) in the central 

flatwoods. To date, H. indica is the only species that has been encountered in 

significant numbers in the coastal flatwoods. A propensity for H. indica to occupy 

coastal habitats also has been noted in other parts of the Caribbean Basin (Fisher-Le 

Saux, Mauléon, Constan, Brunel, & Boemare, 1998; Mauléon, Denon, Briand, 2006). 

Little is known about the direct effects of soil physical and chemical properties 

on the population biology of the Diaprepes root weevil. However, the various 

findings reviewed above provide evidence for the hypothesis that patterns of D. 

abbreviatus within and among Florida citrus orchards are partly regulated by the 

ways in which soil properties affect the natural enemies of D. abbreviatus. More 

explicitly, they suggest that EPNs might help regulate D. abbreviatus on the central 

ridge to the extent that it is often a minor pest, whereas reduced EPN predation in 

some flatwoods orchards may permit D. abbreviatus populations to attain highly 

damaging levels. If the natural control of D. abbreviatus by endemic EPNs varies in 

different regions of Florida, then understanding how these habitats influence EPN 

diversity and efficacy could be especially worthwhile by indicating strategies for 

conservation biological control through the manipulation of habitats to enhance the 

biocontrol potential of EPNs. 

Table 1. The frequency (% of samples) and average dominance (population density 

as a percentage of all EPN in the sample) a of five entomopathogenic nematodes in 

citrus orchards, in three regions of Florida b . 

Species 

Steinernema 

diaprepesi 

Ridge Central Flatwoods Coastal Flatwoods 

F D F D F D 

100 36 57 29 0 0 

S. riobrave 0 0 5


111 

relative importance of biological interactions and how they may vary in different 

habitats (Kaya & Koppenhöfer, 1996). The profound complexity and variety of soil 

food webs makes it unlikely that key interactions between EPNs and other 

organisms can be identified through highly controlled experimentation. However, 

molecular methods that can be used to identify and quantify organisms at different 

trophic levels in soil provide cost-effective opportunities to survey natural soil 

communities in space and time in order to detect relationships that can then be 

studied for causality under controlled conditions. 

3.1. Soil Food Webs and EPN Spatial and Temporal Patterns 

Augmentation of EPNs in soil increases populations above an equilibrium density in 

order to increase the natural level of biological control. However, natural enemies 

of EPNs respond rapidly to the imbalance, so that EPN numbers and levels of 

biological control rarely exceed background levels for more than a few weeks 

(McCoy et al., 2000; Duncan et al., 2003, 2007; El-Borai et al., 2007). Populations 

of nematophagous mites and collembola have been shown to grow in response to 

EPN augmentation (Ishibashi, Young, Nakashima, Abiru, & Haraguchi, 1987; 

Epsky, Walter, & Capinera, 1988; Forschler & Gardner, 1991), and survival of 

augmented EPNs was inversely related to the final abundance of mites and 

collembola in field plots (Wilson & Gaugler, 2004). Jaffee and Strong (2005) 

showed that propagules of some species of nematophagous fungi (NF) increase by 2 

orders of magnitude in a localized response to the emergence of thousands of EPN 

IJs from an insect cadaver. Indeed, the bottom-up trophic cascade that results in 

more predators following EPN augmentation can apparently be large enough to 

sometimes reduce EPN populations below background levels for a short period until 

equilibrium is reestablished (Duncan et al., 2003, 2007). El-Borai et al. (2007) 

demonstrated that trophic cascades are modulated by the species and amount of 

EPNs added to the soil. 

Duncan et al. (2007) showed that treatments that either increased or decreased the 

population densities of various NF in the field also affected EPNs. Composted animal 

manure mulch reduced the abundance of trapping NF while increasing the numbers of 

sentinel insect larvae infected by EPNs. As noted above, augmenting the EPN 

community temporarily increased trapping and endoparasitic NF, and population 

growth of NF was sometimes followed by decreased sentinel infection by EPNs 

compared to non-augmented plots. The effects of these treatments suggest that NF 

population dynamics may affect the temporal and spatial patterns of EPN activity. 

However, the large variety of NF and EPN species, each with different life strategies, 

means that interactions between NF and EPNs are likely to be very complex. For 

example, during eight consecutive monthly sampling events, the prevalence of 

trapping NF in citrus field plots was inversely related to numbers of sentinel weevils 

infected by S. diaprepesi but positively related to those infected by H. zealandica in 

the succeeding month (Duncan et al., 2007). They proposed that these fungi might 

favor H. zealandica by more effectively suppressing its S. diaprepesi competitors. 

Timper and Kaya (1989) demonstrated that the NF Hirsutella rhossiliensis killed 

steinernematids much more effectively than heterorhabditids, and showed that the

112 


infection peg of fungal spores did not penetrate beyond the second stage cuticle that is 

retained as a protective sheath by IJ (3rd stage) heterorhabditids. Steinernematid IJs 

generally cast the second stage cuticle shortly after emerging into the soil from insect 

cadavers (Timper & Kaya, 1989, 1992). 

A variety of mechanisms other than protective sheaths modulate predation by 

NF on nematodes. For example, fungi that form adhesive networks trap plantparasitic 

root-knot nematodes much more effectively than cyst nematodes (neither of 

which retain a cast cuticle), whereas fungi producing constricting rings trapped both 

types of nematodes with equal efficiency (Jaffee, 1998). El-Borai et al. (2007) 

showed that in sand microcosms the predation rates of five species of endoparasitic 

and trapping NF on 5 EPN species, all commonly isolated from citrus orchards, 

were highly species specific. Two endoparasitic NF species that infect via zoospores 

were highly lethal to all EPN species except H. indica, which was unaffected by 

these fungi in the microcosm assays. Conversely, large endemic steinernematids 

such as S. diaprepesi and Steinernema sp. (previously identified as S. glaseri) were 

relatively unaffected by several species of Arthrobotrys (trapping NF), compared to 

significant predation by these fungi on the smaller exotic S. riobrave and the 

heterorhabditids H. zealandica and H. indica. Thus, the report by El-Borai et al. 

(2007) did not support causality of the relationships between NF and S. diaprepesi 

or H. zealandica reported by Duncan et al. (2007). The lack of predation by 

zoosporous NF on just H. indica is intriguing, however, since these commonly 

encountered NF require free water for zoospore movement and H. indica was the 

sole EPN species reported from several low lying coastal areas, which tend to have 

relatively wet soils (Fisher-Le Saux et al., 1998; Mauléon et al., 2006; Table 1). 

Organisms other than predators and parasites might influence the abundance of 

EPNs. Paenibacillus is a bacterial genus that is intimately associated with 

arthropods. Phoretic associations between Paenibacillus and EPNs were recently 

reported and demonstrate remarkable convergence of bacterial species adapting to 

two paraphyletic nematode genera (Enright & Griffin, 2004, 2005; El-Borai, 

Duncan, & Preston, 2005). Paenibacillus spp. associated with heterorhabditids have 

spindle shaped spores that adhere exclusively to the nematode sheath (2nd-stage 

cuticle) whereas those associated with steinernematids have oval spores that adhere 

only to the 3rd-stage cuticle (Fig. 4). Paenibacillus nematophilus spores attached to 

all tested heterorhabditid species and those in the closely-related order Stongylida 

(Enright & Griffin, 2004). In contrast, a Paenibacillus sp. associated with S. 

diaprepesi appears to be species specific (El-Borai et al., 2005). Paenibacillus spp. 

are frequently observed on all known endemic species of EPNs in Florida but not on 

the introduced species S. riobrave. Like the entomopathogenic bacteria P. popilliae 

and P. lentimorbus, the Paenibacillus species that are phoretic on EPN complete 

their life cycle in the insect cadaver but they are not entomopathogenic and they do 

not appear to affect the reproduction of EPN species. The only known adverse affect 

to the nematode is impaired motility in proportion to the degree to which a nematode 

is encumbered with spores. Spore-free steinernematids and heterorhabditids move 

further and infect more insects that do spore-encumbered nematodes. However, the 

degree to which Paenibacillus spp. can modulate EPN abundance in nature is 

unknown.


113 

In addition, some opportunistic, free living nematodes are capable of entering 

insect cadavers and appropriating the nutients produced by the EPN-bacteria 

symbiosis to the extent that the EPNs fail to reproduce (Duncan et al., 2003; 2007). 

Some species of EPNs appear to be especially susceptible to this competitive 

displacement by free living species but, again, the significance of these interactions 

on EPN population dynamics is unknown. Clearly, much remains to be done to 

understand how food web components interact to affect EPN patterns in space and 

time. 

Figure 4. Cuticle of Steinernema diaprepesi heavily encumbered by spores of 

Paenibacillus sp., a non-pathogenic bacterium that reproduces within insects killed by 

the nematode and its entomopathogenic symbiont, Xenorhabdus doucetiae. Movement 

through soil by infective juvenile nematodes is impeded by heavy infestations of 

Paenibacillus sp. Scale bar: 10 µm. 

3.2. Identifying Factors that Regulate EPN Abundance and Efficacy 

As noted previously, spatial surveys have revealed numerous relationships between 

EPN prevalence and various soil physical properties such as porosity (texture), water 

potential, chemistry, as well as cropping and management history. If causality can be 

demonstrated then some of these relationships have the potential to be exploited to 

develop cultural practices that enhance biological control. For example, some types of 

soil mulches have significantly enhanced populations of EPNs (Bednarek & Gaugler, 

1997; Duncan et al., 2007) whereas others appear to have no or negative effects on 

EPNs (Lacey, Arthurs, Unruh, Headrick, & Fritts, 2006). Bednarek and Gaugler

114 


(1997) noted the apparent usefulness of composted animal manure for conservation 

biocontrol after showing that long-term applications of manure increased EPNs by 

3-fold. Animal manure mulches likely increase availability of insect prey and were 

also shown to decrease the prevalence of some nematophagous fungi that prey on 

EPNs (Jaffee, Ferris, Stapleton, Norton, & Muldoon, 1994; Duncan et al., 2007). If a 

number of physical properties can be identified that consistently affect EPN spatial 

patterns then this information might be used to incrementally improve biological 

control achieved by either augmented or endemic EPNs. 

Understanding the basis of relationships between EPNs and other variables in 

the field can require a substantial research investment. Whereas EPN associations 

with some variables have a causative basis, others arise indirectly through the effects 

of unmeasured hidden variables. Therefore, identifying those variables that are most 

likely to modulate EPN prevalence or behavior in predictable ways is important. A 

comparison of the results of surveys using different sample criteria can be helpful in 

selecting variables of interest. 

Campos-Herrera et al. (2007) found that soil moisture was positively associated 

with EPN recovery frequency in a survey of 100 undisturbed sites (natural areas and 

field borders) in La Rioja, Spain. However, in a temporal survey of 18 agricultural 

fields with different management regimes and bordering natural areas, EPNs were 

unrelated to soil moisture but inversely related to soil disturbance (Campos-Herrera et 

al., 2008). Because greater irrigation was employed in tilled annual cropping systems 

with few EPNs than in natural areas or organically grown perennial crops with 

numerous EPNs, Campos Herrera et al. (2008) speculated that soil disturbance is more 

important than moisture in regulating EPN spatial patterns. Similarly, Campos-Herrera 

et al. (2008) reported linear correlations between EPNs and certain soil characteristics 

that were also studied by Alumai, Grewal, Hoy, and Willoughby, (2006) and Duncan 

et al. (unpublished). Differences in the survey protocols among these studies suggest 

the possibility that some of the correlations between soil properties and EPNs are due 

to the influence of soil texture on both EPNs and certain chemical properties (Fig. 5). 

Because greater sand content of soil generally favors EPNs, chemical properties 

associated in some manner with sand content would likely be similarly associated with 

EPNs. The relationships measured in Ohio and Florida (shown in small font in Fig. 5) 

are strikingly similar. Organic matter, K + and Mg ++ tended to be negatively associated 

with both EPNs and percentage sand whereas P was positively associated with both 

variables. In contrast, these relationships had exactly opposite trends in the Spanish 

survey. Nevertheless, soil chemicals in each of the three surveys were associated with 

EPNs in the same manner that they were associated with percentage sand. The Ohio 

and Florida surveys occurred on several golf courses and within a single citrus 

orchard, respectively. Thus, cultural practices were similar among sites within each of 

these surveys, and the effects of porosity and soil colloid surfaces on leaching of some 

chemicals and the adsorption of others operated on similar levels of nutrient inputs. 

However, the Spanish survey compared EPN populations in natural areas and in a 

variety of different annual and perennial cropping systems. The very different levels of 

inputs between the Spanish sample sites might have caused different relationships 

between chemicals and percentage sand and, therefore, with EPNs than seen in Ohio 

or Florida.


115 

Figure 5. Linear correlations relating soil chemical properties to either the numbers 

of entomopathogenic nematodes or percentage of sand, in samples taken to study EPN 

spatial patterns. Symbols in large font proceed from a survey of different cropping 

systems in La Rioja, Spain; remaining symbols derived from golf courses in Ohio and 

a citrus orchard in Florida. Asterisks on the left side of symbols show correlation 

significance (*, P

116 


endoparasitic fungi are obligate parasites of nematodes and some other microscopic 

metazoans (Kerry & Jaffee, 1997). 

Because the predation rate on EPNs cannot be reliably inferred from the 

abundance of many NF species in soil, more direct methods of assessing predation 

are needed. Duncan et al. (2007) developed an assay to enumerate NF species 

recovered directly from nematodes rather than soil, which better reflects levels of 

predatory rather than saprophytic behavior. Circumscribed soil cylinders were 

defined and isolated in situ by pounding PVC tubes to a depth of 20 cm in soil 

beneath the citrus tree canopy. These relatively undisturbed soil cylinders were 

baited with large numbers of EPNs and then recovered from the field after 3 days. 

The nematodes extracted from the soil cylinders were placed on water agar to allow 

growth of NF from nematode cadavers. This method effectively recovered predators 

and parasites of nematodes, which were invariably all killed within 5 days. 

However it was necessary to add fresh EPNs to the agar plates after 5 days to induce 

the formation of fungal fruiting bodies for species identification and the estimation 

of population abundance based on numbers of EPNs killed. The long period of time 

during which the fungi competed with one another on the water agar likely skewed 

the abundance estimates in favor of species best adapted to this artificial habitat. 

A more reliable estimate of NF predation rates in soil requires the identification 

of infected nematodes immediately following extraction from soil. Indeed, direct 

quantification of target populations rather than estimation from bioassays would 

facilitate understanding the roles in food webs of many organisms that are currently 

poorly understood. For example, possible effects of Paenibacillus on EPN 

prevalence can be inferred in bioassays by the degree of spore encumbrance of EPN 

IJs emerging from sentinel insects (Duncan et al., 2007). However, spore 

encumbrance increases with the length of time that IJs are in the vicinity of bacteriainfected 

cadavers in these assays, and the detection of bacteria using sentinel insects 

depends on EPN abundance in soil. Therefore, methods to directly measure the 

abundance of these bacteria in soil or on nematodes extracted from soil are needed 

to accurately assess the degree to which EPNs and Paenibacillus interact at different 

times or in different habitats. 

Real-time PCR (or quantitative PCR, qPCR) provides an efficient method of 

quantifying soilborne organisms such as bacteria and fungi using molecular probes 

(Atkins, Clark, Pande, Hirsch, & Kerry, 2005; Klob, Knief, Stubner, & Conrad, 

2003). The abundance of S. kraussei and S. affine in fields and meadows was 

recently compared using qPCR (Torr, Spiridonov, Heritage, & Wilson, 2007). The 

methods most commonly employed involve the use of fluorescent products that link 

to double stranded DNA causing increased fluorescence (e.g., SYBR Green®) or the 

design of specific fluorescent probes (e.g., TaqMan® or hydrolysis probes). In both 

cases, species-specific primers designed for the target taxon are used. Both systems 

can function with a high degree of species specificity but, due to the use of a probe 

that adds an additional level of specificity to the primers, hydolysis probes are 

generally reported to be more reliable in this regard (Holeva et al., 2006; Leal, 

Green, Allen, Humble, & Rott, 2007). In both systems, the amount of fluorescence 

increases during PCR cycling. The quantification cycle (Cq) (also called threshold 

cycle or Ct) is that at which product amplification enters an exponential phase.


117 

Standard curves of Cq values from known quantities (e.g., numbers of organisms or 

amounts of DNA) of the species in question can be developed in order to estimate 

quantities in unknown samples (Fig. 6). Developing the molecular components for a 

new target species requires several steps, each involving options that affect the cost, 

accuracy, or reliability of the final method (Fig. 7). 

Figure 6. Amplification curves for a qPCR assay with Steinernema diaprepesi as target 

species. Fluorescence intensities (a) produced by different nematode concentrations 

(1–300 infective juveniles) are shown by the different curves entering the exponential 

growth at different points (Cq) in the cycling series (NCT = negative control). Linear 

standard curve of the quantification cycle number (Cq) for the corresponding 

nematode numbers, expressed as log (b). All reactions performed in triplicate. 

The relatively few reports using qPCR to identify and quantify cryptic soilborne 

organisms vary in the adequacy with which experiments are described in order to 

reproduce the work. Bustin et al. (2009) provide useful guidelines for the accurate

118 


presentation of the methods and results obtained using qPCR. Some of methods 

reported to date are reviewed and compared. 

Most species-specific primers (and probes, if required) have been developed to 

amplify sections of the ITS region. This region of ribosomal DNA is usually well 

conserved at the species level but provides greater variability between species than 

more highly conserved regions such as D2–D3. Extensive interspecific variation is 

necessary to provide enough species-specific primer targets to identify those that 

will amplify segments of an optimum size for reliable qPCR reactions (i.e., between 

80 and 200 base pairs). Compared to other gene regions, the large ITS database in 

GenBank facilitates validating the species-specificity of ITS primers among 

organisms characterized to date. In addition to ITS, other regions used to develop 

primers/probes for use in qPCR include 18S from rDNA (Holeva et al., 2006; 

MacMillan, Blok, Young, Crawford, & Wilson, 2006), MspI satDNA monomeric 

unit (François et al., 2007), Hsp70 sequence (Leal et al., 2007) and the intragenic 

spacer (IGS) region of the 5S rRNA gene (Kang, Moon, Lee, Shin, & Lee, 2009). 

Figure 7. General protocol to develop real time qPCR primers and probes (from 

Campos-Herrera, Johnson, El-Borai, Graham, Duncan, 2009).


119 

Once the primers/probes have been validated, sampling and extraction methods 

can be selected that exploit the advantages and limitations of qPCR. Many protocols 

for sampling fungi and bacteria in soil extract DNA directly from soil samples that 

can be as small as a few grams or less. Smith and Jaffee (2009) suggest using a 

combination of culturing and molecular detection of trapping fungi because primers 

specific for a major group of trapping fungi (Orbiliales) yielded clones representing 

just 3 of 8 species that were isolated through culturing, but revealed the presence of 

18 species that had not been detected through culturing. It is unclear whether uneven 

distribution of the species in the small samples (12.5 cm 3 soil) affected the results. 

In order to optimize sampling and extraction methods, additional studies comparing 

both species-specific primers and culturing are needed, and they should involve 

DNA that has been extracted and concentrated from a range of soil sample sizes. 

MacMillan et al. (2006) accurately quantified numbers of slug-parasitic 

nematodes by extracting DNA directly from 10 g soil samples but were not able to 

do so from 1 g soil samples. However, the samples were artificially infested with 

nematodes and, in contrast to bacteria or fungal propagules, it is unlikely that the 

relatively low numbers of nematodes that occur naturally in soil can be reliably 

detected from such small samples. Studies and diagnostic services that use qPCR to 

quantify metazoans such as nematodes in soil routinely employ standard methods of 

sampling and extraction and, therefore, are able to rely on conventional sampling 

programs designed to optimize cost and accuracy (Hollaway, Ophel-Keller, Taylor, 

Burns, & McKay, 2004; Stirling et al., 2004; Ophel-Keller, McKay, Hartley, 

Herdina, & Curran, 2008; Donn, Griffiths, Nielson, & Daniell, 2008). Such 

programs employ a variety of sampling methods that address the highly aggregated 

spatial patterns of nematodes, usually by collecting large numbers of samples that 

are pooled, mixed and subsampled for nematode extraction (Been & Schomaker, 

2006). 

Subsamples of 500–1000 cm 3 are routinely processed by methods such as 

sucrose centrifugation to recover nematodes (Jenkins, 1964). There is no reason that 

such large subsamples cannot be used for molecular diagnostics although a number 

of studies report the use of smaller subsamples (Table 2), perhaps to reduce the 

recovery of soil chemicals that can interfere with DNA extraction and PCR reactions 

(see below). If the objective is estimating predation rates by measuring only those 

NF intimately associated with nematodes, the nematodes can be further separated 

from the small residue of soil remaining after sucrose centrifugation by additional 

centrifugation in a magnesium sulphate density gradient (Duncan et al., 2007). 

Preliminary experiments (Duncan et al., unpublished data) revealed less fungal DNA 

and fewer nematodes recovered following the two-step extraction procedure 

compared to just sucrose centrifugation; and there was no evidence of significant NF 

DNA in the soil residue. This observation should be confirmed using a variety of 

soils and NF targets because use of one rather than two extractions reduces time and 

cost, and the recovery of more nematodes increases the detection efficiency of the 

system. 

A variety of methods have been used to extract nematode DNA from soil or 

from nematodes recovered from soil (Table 2). Kits involve higher costs than 

standard laboratory protocols to purify DNA but are far simpler and faster to use if

120 


they perform well with material extracted from soil. When DNA was isolated 

directly from soil, the PowerMax Soil TM DNA Isolation Kit (MoBio) was more 

reliable than a standard laboratory method or the Ultra Clean Soil TM DNA Kit 

(MacMillan et al., 2006). For nematodes extracted from soil, Madami, Subbotin, and 

Moens, (2005) concluded that the use of proteinase K followed by PCR Buffer 

yielded more DNA than if it was followed by Worm Lysis Buffer. Donn et al. 

(2008) found that use of sodium hydroxide extraction, ChargesSwitch PCR CleanUp 

Kit (Invitrogen), QIAquick PCR Purification System (Invitrogen) and the Wizard 

PCR Prep DNA Purification System (Promega) all failed to provide either enough 

DNA or DNA of high enough quality for PCR whereas phenol chloroform 

extraction or Purelink PCR Purification Columns (Invitrogen) provided high 

concentrations of DNA acceptable for PCR studies. Campos-Herrera et al. (2009) 

obtained good quality DNA from nematodes extracted with sucrose-centrifugation 

using the Unltra Clean Soil TM DNA Kit (Mo Bio). 

PCR can be inhibited by chemical contaminants in soil (e.g., humic acid, 

phenolic compounds) or by use of excessive template. Inhibition can be complete or 

partial, and so it is important to calibrate qPCR with results obtained from known 

quantities of the target organism (e.g., nematodes, nematodes infected by NF, etc.) 

added to populations of nematodes extracted from soil rather than relying on PCR of 

DNA from pure cultures. Bovine serum albumin has been used to reduce the effects 

of chemical inhibitors of PCR (MacMillan et al., 2006; Torr et al., 2007; Campos- 

Herrera et al., 2009). To avoid excess template, dilution of DNA from 4 to 100-fold 

from samples of unknowns is usually necessary (Madami et al., 2005; Jones, Todd, 

& Herman, 2006; Kang et al., 2009). Because each soil sample yields a different 

quantity of DNA that might affect the reaction, the use of a standard DNA quantity 

is preferable to a standard dilution. 

Most authors report very high detection efficiency from the use of qPCR, which 

is frequently at the level of a single nematode. Several multiplex systems in which 

single reactions measure more than one nematode species or combinations of 

nematodes and fungi have been developed that can substantially reduce time and 

cost (Madami, Ward, & de Boer, 2008; Jones et al., 2006; Berry, Fargette, Spaull, 

Morand, & Cadet, 2008; Zijlstra & van Hoof, 2006). Unfortunately, the increased 

likelihood of competition between target DNA or development of interacting 

primers (primer-dimers) that increase florescence for a false signal can impede the 

development and performance of multiplex systems. Zijlstra and van Hoof (2006) 

reported a density-dependent reduction in the efficiency of multiplex qPCR and 

suggested that individual reactions would be required for precise estimation. Berry 

et al. (2008) observed similarity of melting temperatures and competition between 

the amplification of Meloidogyne javanica and Pratylenchus zeae targets, which 

made it impossible to distinguish the two species in a multiplex reaction. 

At present, studies using molecular techniques to assess EPN population 

distribution and dynamics remain rare but the development and optimization of 

these techniques could contribute much to our understanding of these nematodes and 

the kinds of strategies that might facilitate their enhanced usefulness for biological 

control in agroecosystems.

IPM THROUGH ENTOMOPARASITES 121

122 

R. CAMPOS-HERRERA ET AL.


123 

CONCLUSIONS 

Basic and applied study of the EPN/bacteria symbiosis has increased steadily during 

the past half-century, coincident with an accelerating awareness of limitations that 

characterize many conventional pest management practices. An extensive literature 

on the effectiveness of EPNs as biopesticides is in striking contrast to the paucity of 

information about the ecology of these cryptic predators of subterranean arthropods. 

Their population abundance is usually inferred from the numbers of sentinel insects 

they kill but, unlike plant parasitic and free living nematodes, there are few reports 

of the actual numbers of these worms in different soil habitats. Consequently, little 

is known about their population biology – neither the factors that govern population 

size nor the numbers of worms needed to achieve economic pest suppression in 

different habitats. The great variety of species with very different life strategies 

provides tremendous opportunities to study how food webs and soil conditions 

affect the abundance of nematodes with different traits. Understanding the 

population biology of EPNs is necessary to discover and exploit new ways to 

increase their efficacy and, more importantly, their reliability for biological control 

in managed ecosystems. For example, trophic cascades that result from augmenting 

EPNs in citrus orchards have the potential to interfere with the effectiveness of this 

IPM tactic if the non-target effect (i.e., the temporary suppression of EPNs by 

natural enemies) occurs at a peak time for D. abbreviatus egg hatch and larval 

recruitment into soil. Can better timing of EPN applications reduce this risk? Would 

the application of EPN species less susceptible to predation by NF modulate the 

trophic cascade and the potential for non-target effects? What physical 

characteristics of soils are amenable to change in ways that enhance either the 

numbers or the effectiveness of EPN? The ready availability of molecular tools to 

identify and measure EPN and their natural enemies in the soil should facilitate 

more rapid progress in our understanding of how these organisms co-exist and how 

we might better manage soils to maximize their biological control potential. 

ACKNOWLEDGEMENTS 

The authors gratefully acknowledge postdoctoral fellowship support from the 

Ramón Areces Foundation (Spain) to R. Campos-Herrera and a US-Egypt project 

for IPM in citrus (contract 260) to L. W. Duncan. 

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1262.

Section 2 

ADVANCED IPM TECHNOLOGIES

6 

INTEGRATION OF INSECT AND MITE 

MANAGEMENT WITH DISEASE AND WEED 

CONTROL IN PECAN PRODUCTION 

JAMES D. DUTCHER 1 , LENNY WELLS 2 , TIMOTHY B. 

BRENNEMAN 3 AND MICHAEL G. PATTERSON 4 

1 Entomology Department, University of Georgia, Tifton, GA, USA 

2 Horticulture Department, University of Georgia, Tifton, GA, USA 

3 Plant Pathology Department, University of Georgia, Tifton, GA, USA 

4 Department of Agronomy and Soils, Auburn University, Auburn, AL, USA 

Abstract. Pecan orchards in the southeastern US are managed to conserve resources, protect the fruit and 

foliage from injury caused by phytophagous insects, mites, and pecan scab, and remove competition from weeds 

during the establishment of newly planted trees and in the preparation of the orchard floor as a harvesting 

surface. Costs associated with pest control are significant each year and the growers use integrated pest 

management methods to increase the effectiveness of pesticide treatments and reduce control costs. A 

coordinated research and extension effort over the past 25 years in entomology, plant pathology, weed science 

and horticulture has reduced the amount of pesticide use by 35%. Four advances have been responsible for the 

reduction. First, pecan scab sprays are reduced by linking the frequency of applications to the climatic conditions 

and the cultivar susceptibiltiy. Second, pest-specific insecticides that are toxic to the pests and not toxic to 

beneficial insects and mites are used to control lepidopterous pests and conserve aphidophagous insects and mite 

predators. Third, cover crops have been developed to supplement the soil with nitrogen and organic matter and 

conserve beneficial insects. Fourth, weed studies have led to the elimination of weeds in the first 8 years after 

planting around young trees, chemical mowing methods in established orchards and selective grass control to 

increase the growth of clover cover crops. The development and implementation of these and other significant 

advances in pecan management are reviewed in this chapter. 

1. PESTS IMPEDE THE VERSATILITY OF THE PECAN TREE 

Pecan [Carya illinoinensis (Wangenh.) K. Koch, Fagales: Juglandaceae] is a large 

tree that is native to the United States and Mexico and is propagated as a shade tree, 

for timber and for the production of nuts. Although this chapter describes the recent 

integration of pest control methods in pecans grown for nut production pest 

problems arise in shade and timber trees as well. As a shade tree in the southern US, 

pecan has multiple problems and is not recommended for planting (Finch, 2001). 

However, existing trees are rarely removed and replaced by homeowners or city 

133 




134 

J.D. DUTCHER ET AL. 

managers. The canopy of a full grown tree, with dimensions of 30.5 m in height and 

16.5 m in diameter and covering up to 1/24 ha of land, is often too large for home 

sites. The main pests of pecan trees planted along the roadside and in the urban 

landscape, are the gregarious caterpillars – walnut caterpillar [Datana integerrima 

(Grote & Robinson), Lepidoptera: Notodontidae] and fall webworm [Hyphantria 

cunea Drury, Lepidoptera: Arctiidae]. These cause defoliation in the late summer 

and the fall webworm leaves unsightly webs in the canopy. Biological control with 

water-miscible formulations Bacillus thuringiensis applied as a foliar spray is 

effective against these two pests. Feeding by the pecan aphids [Monellia caryella 

(Fitch), Monelliopsis pecanis (Bissell), Melanocallis caryaefoliae (Davis), 

Hemiptera: Aphididae] also detract from the aesthetic value of pecan as a shade tree. 

Aphids egest copious amounts of honeydew (Wood, Tedders & Dutcher, 1987). 

Honeydew deposited on the leaf surface promotes the growth of sooty mold giving 

the leaves a black appearance. Honeydew deposited on the area beneath the tree 

canopy often has to be washed off cars and trucks parked beneath the trees. 

Multicolored Asian ladybeetle [Harmonia axyridis (Pallas), Coleoptera: 

Coccinellidae] was imported for biological control to the US and is an effective 

control for aphids in pecan trees in areas where the beetle is established. In pecan 

trees grown for shade, the nut crop is highly depredated by squirrels, birds and insect 

pests (Worley, 2002). 

Pecan lumber is sold as hickory and hickory is used to make tool handles, 

furniture, cabinetry, ladder rungs, dowels, sporting goods (including baseball bats, skis 

and archery equipment), flooring, veneer, plywood, fuelwood, and charcoal. Pecan 

burls and spalted pecan are sold as a specialty wood. The characteristics of hickory 

and pecan produce a strong, shock-resistant wood that has a white tinge with brown 

sapwood and red-brown heartwood. Pecan wood is difficult to season and warps 

during drying. Wood working properties are above average for hickory and slightly 

less for pecan. Problems arise in splitting while nailing. Machining and glueing the 

wood are also difficult and the wood is susceptible to bird peck. Pest populations are 

generally very low in native stands of pecan harvested for timber (Reid & Hunt, 2000). 

Yellow-bellied sapsucker, [Sphyrapicus varius (L.) Piciformes: Picidae] is a 

migratory bird that causes bird peck in hardwoods including pecan. The birds eat 

insects that are attracted to sap flowing from the holes made in the trunk by the bird 

pecks. Open bird peck holes do not decrease the value of the wood for lumber but 

they do devalue the wood used for making tool handles. When the bird peck holes 

pierce the cambium layer of the trunk then the tree produces a callus tissue to repair 

the hole (aka an occlusion) and the wood looses value. Each yellow-bellied 

sapsucker returns to the same nesting site each year and repeated annual bird peck 

damage can extend into the wood and reduce its value. Foresters control the yellowbellied 

sapsucker by applying bird Tanglefoot® on the trunk of most of the trees in 

the orchard leaving a few favored trees untreated to withstand all the injury. The 

birds nest in decaying trunks of aspen and removal of these nesting sites also 

reduces injury. Killing the birds is illegal (Ostry & Nicholls, 1978). Pecan are also 

be used as an alley crop in the southern US. The trees are planted around fields of 

row crops and the tree roots reduce nitrate leaching from the crop field to the 

groundwater (Allen et al., 2004).

IPM IN PECAN PRODUCTION 

135 

Pecan nut production in orchards is a viable agribusiness especially in the 

southern US. Pecan trees will produce a crop of nuts with little or no management. 

In fact, a large portion of the USA crop is produced on native stands with very low 

inputs. These stands have much lower average production per hectare than seedling 

or improved pecan orchards and inputs have to be held to a low cost. Pecans initially 

were harvested by hand. Harvesters would climb each tree and shake individual 

limbs or knock nuts off the limbs with bamboo poles, while coworkers would pick 

them up off the ground. Mechanical trunk and limb shakers are currently used to 

dislodge the nuts out of the tree and onto the orchard floor. Hand picking off the 

ground has been replaced by a mechanical process where the fallen limbs are raked 

over to the edge of the orchard, the nuts and leaves are swept into rows, the leaves 

are blown off the row and the nuts are picked up from the row by a mechanical 

harvester. Nuts are sorted and cleaned in the orchard and then transported to the 

shelling plant where they are sanitized, dried and then typically cracked, shelled and 

frozen. Harvesting is most efficient when the orchard floor is dry, level, and cleared 

of weeds and debris. Efficient harvesting is needed to prevent depredation of the 

nuts by birds and mammals and environmental degradation of the nuts. 

Native stands of pecans provided nuts as a source of food for indigenous 

people of America and early settlers propagated seedling trees through the southern 

US. Many of the native groves were developed, by European settlers, as a newworld 

adaptation (Brison, 1974) of the European silvopastoral systems that provided 

many of the staples of the rural community – milk, meat, hides, wood, and nuts 

(Auda, 1999). Grafting techniques were developed in the mid-1800s and improved 

cultivars with desirable characteristics were selected from native and seedling trees 

or from controlled crosses from amateur or professional plant breeders. Improved 

cultivars have been propagated across the southeastern US, and in New Mexico, 

Arizona and California to the extent that the production of nuts from improved 

cultivars often exceeds the production of native and seedling orchards (Worley, 

2002). 

Nut production in the US is currently based on ~10 million managed trees 

planted on ~200,000 ha on 20,000 farms in 24 states producing roughly 146,000 

metric tons of in-shell nuts each year. Most orchards are small in area. Sixty-two 

percent of the farms have less than 6 ha, 32% have 6–40 ha, 5.4% of the farms have 

40–200 ha and 0.7% of the farms have more than 200 ha. Orchards with less than 40 

ha comprise 56% of the production area in the USA (Wood, 2003). Improved 

cultivars have contributed to increases in pecan production. Today’s new cultivars, 

however, are only 2–3 generations removed from wild trees (Sparks, 1992) and 

pesticides – esp. fungicides – have had a more significant impact on increasing USA 

pecan production than cultivars. In fact, native groves produce approximately 30% 

of the US nut crop and seedling and improved cultivars planted in commercial 

orchards produce the remaining crop (Pollack, 2001). Pecan trees have a producing 

lifespan of at least 80 years and grow to over 30.5 m in height. Production is 

irregular from season to season. USA production per season ranges from 45.4 

to 163.2 million kg of nuts in the shell. The kernel typically comprises ~50% 

of the mass of the nut in the shell. Growers typically sell pecans in the shell for 

$1.50–5.00/kg to processors and many growers process, package, and market their

136 


own crop as higher value products such as gift boxes, whole kernels, and various 

candies. Growers in Georgia and Texas produce 60% of the US crop. 

2. PEST CONTROL METHODS 

Uncontrolled disease, insect and mite, and weedy pest populations, under favorable 

environmental conditions have the potential of reducing the pecan nut production 

often to nil. Pests attacking the nuts can take the entire crop in the current season. 

Pests attacking the foliage can cause premature defoliation in the current year and 

the trees will not produce flowers and fruit the following year As examples, the 

primary pest in the humid regions of the southeastern US is pecan scab and control 

is achieved with preventive treatment of the fruit and foliage with fungicide. Pecan 

weevil attacks the crop late in the season after the grower has invested considerable 

resources in the crop and the weevils are most effectively controlled with repeated 

sprays of insecticide during adult emergence. Black pecan aphid outbreaks defoliate 

trees quickly and treating after the outbreak does not prevent damage. Black pecan 

aphids are treated with insecticide when the population exceeds one aphid per leaf. 

Pecan leaf scorch mite is control with sprays of sulphur or miticide (Dutcher, 

Hudson & Ellis, 2003). Lack of weed control is directly related reductions in pecan 

production, esp. in young pecan trees (Smith, Cheary, & Carroll, 2005; Patterson & 

Goff, 1993; Foshee, Goodman, Patterson, Goff, & Dozier, 1997). 

Broad spectrum pesticides and airblast sprayer technology and orchard floor 

management significantly increase the ability of growers to quickly control these 

key pests and large portions of the nut crop were conserved by the use the pesticides. 

Production of nuts increased leading to a period of reliance on chemical control of 

insects, mites and diseases. Broad spectrum pesticides are crucial to commercial 

pecan production, offering highly effective control methods that prevent pecan scab 

and pecan weevil damage, control outbreaks of black pecan aphids, and prepare 

weed-free herbicided strips along the tree rows. 

Pest control in differs in each of the three cultural regimes for pecan nut 

production (Dutcher et al., 2003). In native stands and groves where nuts are 

harvested from naturally occurring trees, the orchard floor is cleared at harvest time 

and the nuts are collected and managers use nitrogen fertilization, mechanical nut 

harvest rely primarily on natural controls to regulate pest populations with limited 

use of insecticides (Reid & Mulder, 2003). In seedling orchards where trees are 

produced from seed and not grafted, and in improved orchards where seedlings are 

grafted in a nursery to a known cultivar and then planted in an orchard, orchard 

managers potentially can use all available pest control methods and are limited by 

the need to balance the costs of control with production potential each season. Each 

seedling tree produces a unique pecan nut and the harvested product lacks the 

homogeneity of the nut crop harvested from an improved orchard. However, 

seedling orchards have greater genetic diversity than improved orchards and pest 

outbreaks (especially for pecan scab, pecan weevil and black pecan aphid) develop 

to different levels of severity in each tree. Improved orchards are more susceptible to 

pest outbreaks over the entire orchard.


137 

Weed control is important and functions to: remove plants that compete with 

the trees for nutrients and plants that provide food for kernel-feeding hemipterans; 

and, to the preparation of the orchard floor for mechanical harvesting (Smith & 

Carroll, 2004). Weed control initially consisted of disking and rolling the soil so that 

the nuts could be collected from bare soil surface. This method made harvesting 

easier but the harrow would often open a wound at the base of the trunk of each tree 

and crown gall [Agrobacterium tumefaciens Smith & Townsend, Proteobacteria: 

Rhizobiales: Rhizobiaceae] would infest the wounded trees and destroy a fair 

portion of the root system. Growers shifted to a mowed surface between tree rows 

with an herbicided strip along the tree row to prevent damage to the tree trunks. 

Through the years the types of herbicides changed but the basic design remained the 

same. Trees on land that is flooded part of the year along river systems or with flood 

irrigation have either a bare soil surface maintained with herbicides or the annual 

weeds are periodically mowed. In the last 30 years, growers have started an 

integrated approach to weed control by seeding the orchard with various cool season 

legumes. These are grown as intercrops in the mowed strip or as cover crops over 

the entire orchard floor. The plants supply nitrogen and increase soil organic matter 

and also enhance beneficial insects. In the last 5 years, growers have enhanced the 

growth of the legumes by removing grasses during the winter and spring with, 

sethoxydim, a selective herbicide. 

Agricultural chemical usage in US pecan orchards varies considerably between 

states and has increased significantly since the domestication of pecan began in the 

early 1900s. Nitrogen fertilizer, pesticides and new cultivars have increased US 

production per hectare. Pesticide usage is significant, for example, commercial 

pecan producers currently use approximately 1/3 million kg of insecticide (active 

ingredient) each season on 320,000 acres in Georgia and Texas (Smith, Harris, Lee, 

McEachern, & Ree, 2002; Guillebeau, 2001). The most recent survey results 

(USDA/NASS, 2000) indicate that approximately 69% of the US pecan acreage is 

treated each year with supplemental nitrogen fertilizer, 67% is treated with 

insecticides, 47% is treated with fungicides, and 44% is treated with herbicides. 

2.1. Insect and Mite Pest Management in Pecan Orchards 

The insect complex associated with pecan in native and improved systems includes 

180 species of phytophagous insects and mites (Payne & Johnson, 1979; Harris, 

1983) and each is associated by a diverse array of natural enemies (Tedders, 1985). 

Insect management strategies range from total reliance on natural enemies to 

intensive integration of chemical and biological controls (Table 1) (Dutcher et al., 

2003). The fruit and foliage in pecan orchards are susceptible to insect injury that 

can result in economic losses for 7 months. Preventive cover sprays of insecticides 

or miticides are not practical and the control of pecan insect and mite pests has 

developed into a management scheme. Insects and mites and tree phenology are 

monitored determine the abundance of the pests and the susceptibility of the tree to 

injury. Direct control measures are applied when pest abundance exceeds an action 

threshold and the tree is susceptible to injury. This prevents high costs, resistance,

138 


replacement and resurgence problems associated with repeated treatment with 

insecticides and miticides (Dutcher, Fonsah, & Hudson, 2006). 

Table 1. Control methods for the eight major pecan arthropod pests in North American. 

Pest Control method for pest a Relative efficacy b 

Pecan weevil 

Curculio caryae (Horn) 

Pecan nut casebearer 

Acrobasis nuxvorella (Neunzig) 

Hickory shuckworm 

Cydia caryana Fitch 

Black pecan aphid 

Melanocallis caryaefoliae Davis 

Yellow pecan aphid 

Monelliopsis pecanis Bissell 

Blackmargined aphid 

Monellia caryella Fitch 

Pecan leaf scorch mite 

Eotetranychus hicoriae 

(McGregor) 

Kernel-feeding Hemipterans – 

Pentatomidae and Coriedae 

Broad spectrum insecticides 

Quarantine 

Risk rating and spot treatment 

Trunk treatment 

Entomopathogens, nematodes 

Red imported fire ant as predator 


Biorational insecticides 

Mating disruption 


Biorational insecticides 

Sanitation 

Organophosphate insecticides 

Neonicitinoid insecticides 

Insecticidal soap 

Harmonia axyridis (Pallas) 

Interplanting crape myrtles 

Systemic insecticides 




Introduced parasites 

Systemic insecticides 




Introduced parasites 

Miticides 

Sulphur 

Predatory mite release 

Dormant oil sprays 


Trap crops 

Removing alternate host plants 

High 

High 

Moderate 

Moderate 

Low 

Low 

High 

High 

Low 

High 

High 

Moderate 

High 

Moderate 

High 

Moderate 

Low 

High 

High 

High 

Low 

Low 

High 

High 

High 

Low 

Low 

High 

High 

Moderate 

Low 

Moderate 

Low 

Low 

a 

b 

Control methods listed in the table have shown benefits greater than the costs. 

Efficacy ratings: total = 100%; high = 91–100%; moderate = 80–90%; low < 80%. 

Insecticides offer the single most effective control method for nut-feeding 

insects. Carbaryl, phosmet, esfenvalerate and cypermethrin are used during the late 

season for control of pecan weevil, hickory shuckworm and kernel-feeding


139 

hemipterans. Pyrethroid insecticides are also used but have a shorter residual activity 

and lower toxicity against the pecan weevil. Broad spectrum insecticides are not 

ideal and sprays often destroy beneficial insects leading to resurgence of secondary 

foliage-feeding pests. Pecan growers with resurgence problems have to apply 

additional costly and specific aphidicides, systemic insecticides and/or miticides to 

keep the foliage on the trees. 

Systemic insecticides or foliar sprays of insecticides are the most effective 

controls for outbreaks of foliage feeding insects. Phosmet and chlorpyrifos are used 

effectively for control of late season outbreaks of the black pecan aphid. These two 

organophosphate insecticides may become obsolete through reassessment. 

Imidacloprid sprays and biological control with multicolored Asian ladybeetle are 

effective against the pecan aphids. Efficacy varies between the three different 

species and selective control of two aphid species and not the third species opens the 

feeding niche the third leading to outbreaks. The control of all three species of pecan 

aphids can leave the foliage open to attack by phytophagous mites and typically 

leads to an outbreak of pecan leaf scorch mite (Dutcher et al., 2006). Alternative 

controls for control of nut-feeding pests that do not destroy beneficial insects 

associated with foliage-feeding pests are possible with the use of selective 

insecticides. 

Growers also adopt insect pest management to reduce the cost of production for 

pecans. Pecan growers typically minimize the number of spray applications and rely 

on natural control by predators, parasites and pathogens for many insect pests. One of 

the most effective biologically-based control techniques for pecan growers is selective 

insecticides coupled with effective monitoring techniques. to control pecan nut 

casebearer (Knutson & Ree, 2000) and hickory shuckworm. Replacement of broad 

spectrum insecticides with biorational insecticides has reduced the incidence of 

secondary pest resurgence after treatments for these pests. Initially, insect growth 

regulators were evaluated for insect control against pecan weevil and lepidopterans 

(Payne & Dutcher, 1985; Tedders, 1977). Efficacy was much lower than the broadspectrum 

insecticides and registration was not pursued. Broad-spectrum insecticides 

became the main control measures for preventing pest damage. Recently, newer and 

more effective insect growth regulator insecticides, such as, diflubenzuron and 

tebufenozide, have gained acceptance among growers for control of lepidopteran 

pests. Broad spectrum insecticides are currently the only effective controls for pecan 

weevil, kernel-feeding hemipterans and black pecan aphid. 

Pecan insects have sufficient reproductive capacities to overcome the mortality 

caused by control methods and growers are continually battling recurring pest 

problems each season. The bionomics information for the reproductive capacity and 

generation time of pecan weevil (Ree, Knutson, & Harris, 2005), pecan nut 

casebearer (Mulder & Grantham, 2002), yellow pecan aphid, blackmargined aphid, 

black pecan aphid (Tedders, 1978; Kaakeh & Dutcher, 1992), and pecan leaf scorch 

mite (Hall, 2001) (Table 2) indicates that only 0.1–70% of the populations need to 

survive from one season to the next to sustain the pest populations. 

Pecan weevil survival of 2.6% per generation is needed to sustain the current 

population level. Since there is a generation every 2–3 years, an annual mortality of 

30.1% per season (for weevils with a 3-year generation time) or 83.4% per season

140 


(for weevils with a 2-year generation time) would cause a decrease in weevil from 

one generation to the next. Multiple generations occur for pecan nut casebearer, 

aphids and pecan leaf scorch mite and yearly survivals of 0.1–0.2% will ensure a 

increase in theses pest populations from season to season. Efficacies required to 

prevent pecan nut casebearer populations from increasing from season to season 

exceed 99% and two or more control methods often have to be combined to prevent 

pest outbreaks in an integrated pest management program (cf. Tables 1 and 2). The 

better chemical control methods typically have efficacies near 95–99%. The impacts 

of natural controls – e.g. rainfall events (Kaakeh & Dutcher, 1993a) and temperature 

extremes (Kaakeh & Dutcher, 1993b) on pecan aphids – are important but pests also 

may increase in the orchard by immigration. Consequently, growers continue to 

have pest problems from season to season. Pecan weevil problems may be solvable 

with the integration of several techniques over an extended period. 

Table 2. The mortality needed each season to cause a reduction in the season to season 

abundance estimated from literature values for the reproductive capacity (RC) and 

generations per year (G), for certain pecan insect and mite pests with the equation: 

Mortality (%) = 100 ⋅ (1 – (1 / (SR ⋅ RC) G )), where the sex ratio (SR) is assumed to be 

1.0 for aphids and 0.5 for weevils, casebearers and mites. 

Pest a Reproductive capacity Generations 

per year 

Mortality 

per season (%) 

Pecan weevil 75 eggs/female 0.3– 0.5 30–83 

Pecan nut casebearer 50–150 eggs/female 2 99.8–99.9 

Black pecan aphid 35 nymphs/female 26 99.9 

Yellow pecan aphid 38 nymphs/female 32 99.9 

Black margined aphid 125 nymphs/female 16 99.9 

Pecan leaf scorch mite 9–36 eggs/female 7-8 99.9 

a Two pest listed in Table 1 are not listed here. The reproductive capacity of the hickory shuckworm has 

not been measured and the moths have 2–5 generations per year. Kernel-feeding hemipterans do not 

reproduce in the pecan trees and increases in abundance by immigrating from alternative host plants. 

2.2. Pecan Disease Management 

There are multiple diseases of pecan that can impact production by reducing yield or 

quality of nuts in the present year, or reducing the ability of the trees to produce in 

subsequent seasons. This is particularly true in the southeastern US where fungal 

diseases thrive in the warm, humid climate present during the growing season. 

Production areas of the western US have much drier climates and few problems with 

fungal diseases. Therefore most of the following comments will pertain to disease 

control practices in the wetter production areas from east-central Texas through 

South Carolina. In this region the most damaging disease by far is pecan scab caused


141 

by Fusicladosporium effusum (G. Winter) Partridge and Morgan-Jones. Most years 

disease losses are not that high, but growers often spend more money for fungicides 

than any other production input. In Georgia alone the cost of scab control is 

estimated to be about $15 million annually, and in a wet year like 2003 the 

combined cost of lost yield and fungicide sprays was approximately $45 million 

(Williams-Woodward, 2003). There are other diseases that can cause local damage 

on some cultivars, but they are generally controlled by fungicides applied for scab. 

These secondary diseases include Downy Spot (Mycosphaerella caryigena), 

Phytopthora Shuck and Kernel Rot (Phytophthora cactorum), Powdery mildew 

(Microsphaera penicillata), Zonate leaf spot (Cristulariella pyrimidalis), 

Anthracnose (Glomerella cingulata), Bacterial leaf scorch (Xylella fastidiosa), 

Crown gall (Agrobacterium tumefaciens), and a number other minor diseases that 

rarely cause significant crop loss. 

Because losses to disease can be severe under favorable conditions, growers 

have a high awareness of the need for control programs. This may include practices 

such as pruning lower tree branches or clearing fence rows around orchards, 

planting in wide row spacing’s, closely mowing the orchard floor, and designing 

orchards so that prevailing winds flow through it (Latham & Goff, 1991). All these 

practices are designed to increase air flow, thus reducing leaf wetness periods and 

therefore levels of infection. General orchard sanitation practices are also utilized, 

and may include shaking previously harvested trees to dislodge shucks that harbor 

overwintering pathogen inoculum. 

In spite of these practices, growers in areas with frequent rainfall rely heavily 

on multiple fungicide applications applied with large air-blast sprayers or 

occasionally airplanes. Fungicides used include triphenyltin hydroxide (TPTH), 

various sterol demethylation inhibitors (DMI’s), dodine, strobilurins, and 

thiophanate methyl. There have been issues recently with fungicide resistance, and 

ongoing concerns that it will become an increasing problem (Stevenson, Bertrand, & 

Brenneman, 2004). These concerns are based on the known risks associated with the 

fungicides used, the inherent ability of the pathogen to develop resistance, the heavy 

use of fungicides, and the fact that pecan is a perennial crop and therefore not 

subject to crop rotation which can greatly reduce the buildup of resistant isolates. 

However, growers generally still get good disease control if they apply sprays 

correctly and on a timely basis. Most growers in the southeastern states use a 2–3 

weeks spray interval for a total of 7–10 sprays per year, whereas those in more arid 

areas of the west may make few if any fungicide applications. 

Early sprays (i.e. prepollination) are applied to protect the young leaves which 

are very susceptible to scab infections. Overwintered lesions on stems are a major 

source of this initial inoculum. Large numbers of conidia are produced from stem 

lesions in late March and early April, although small numbers are found as late as 

August (Stevenson, 1995). Therefore one function of the early sprays is to prevent 

leaf infections that will in turn sporulate and provide secondary inoculum for nut 

infections that are even more damaging. Scab susceptibility of leaves decreases 

rapidly with age (Gottwald, 1985), although later season growth flushes can become 

infected. Late-season fungicide sprays are of questionable benefit when applied after 

shell hardening according to work by Gottwald and Bertrand (1989). They

142 


demonstrated that scab initiated at this time of the season was largely cosmetic since 

it occurred after the nuts had fully expanded. However, many growers still apply 

fungicides at this time. 

In an effort to reduce the cost of production in areas prone to scab 

development, several programs have been developed to enable growers to spray only 

when the environmental conditions are conducive for disease development. The 

program currently recommended in Georgia is AU-Pecan which is based on the 

number of rainfall events as well as the predicted chance of rain for the next 5 days. 

This model has been shown to reduce the total number of sprays in most seasons 

while maintaining the same level of control, and is available on a site-specific basis 

for individual orchards using Doppler radar precipitation estimates. A different 

model based on scab hours, i.e. periods with temperatures > 21.1°C and relative 

humidity >90%, is being used in Oklahoma (Von Broembsen, Driever, Smith, 

Duthie, & Carlson, 1999). One limitation to implementation of any advisory is the long 

time needed for many growers to spray their orchards. This time frame is commonly 1–2 

weeks, which necessitates spraying on more of a calendar-based schedule since response 

to an advisory is too slow. The AU-Pecan model compensates for this to some degree by 

utilizing the 5-day chance of rain to recommend applications prior to favorable infection 

periods, rather than waiting until after they occur. 

Another consideration in scheduling fungicide sprays based on scab biology 

alone is the potential development of other diseases. For example, Stuart has been a 

more scab-resistant cultivar in some areas and often receives fewer sprays than more 

scab-susceptible cultivars. However, it is very susceptible to downy spot. Downy spot 

infections occur very early in the season, and prepollination fungicide sprays are 

essential for control. The spectrum of activity for a given fungicide must also be 

considered when designing a spray program. A product must have activity on scab, but 

some excellent scab fungicides do not control other diseases as well. One common 

example of this is the lack of activity of TPTH and dodine on zonate leaf spot. Both of 

these fungicides provide excellent control of nut scab, but are weak on zonate leaf spot 

which also occurs during nut fill. In orchards where zonate can be a problem, other 

classes of fungicides (particularly DMI’s) should be incorporated into post-pollination 

spray programs to insure control of this potentially damaging disease. 

One problem that is exacerbated by fungicide sprays is pecan aphids. As 

discussed earlier, several species of aphid can be very detrimental to pecan, but there 

is a beneficial fungus in the Neozygitaceae that can cause high aphid mortality 

(Ekbom & Pickering, 1990). Unfortunately this fungus is very sensitive to TPTH, 

and fungal-induced aphid mortality was reduced by 50% in trees sprayed with this 

commonly used fungicide (Pickering, Dutcher, & Ekbom, 1990). Therefore, 

reductions in fungicide use not only save money, they also make it less likely that a 

grower will have to spray insecticides later in the year for aphid control (Pickering, 

Hargrove, Dutcher, & Ellis, 1990). 

Virulence of the pecan scab fungus has been shown to be very cultivar specific 

(Converse, 1960). Early researcher (Demaree & Cole, 1929) demonstrated that 

repeated inoculations on the same cultivar increased pathogenicity on that cultivar, 

and the history of scab-resistant cultivar introductions has consistently been that 

they become more susceptible to damaging scab epidemics each year (Gottwald,


143 

1989). The basis for this specificity is not fully known, but it occurs sometime later 

than 4 days after inoculation during the stage of subcuticular growth (Bracewell & 

Stevenson, 1999). Intercropping a mixture of cultivars has been shown to 

successfully reduce epidemics of foliar pathogens in other crops (Mundt, 2002), and 

computer simulations based on apple scab show disease reductions of 65–79% after 

six generations when planting three cultivars versus a single cultivar (Gessler & 

Blaise, 1994). While utilizing that model to guide cultivar placement in new 

orchards has been discussed among pecan growers and researchers, the benefits of 

planting cultivars in blocks for other management purposes usually outweigh the 

potential benefits related to scab control. 

The race structure of pecan scab populations and their ability to adapt to new 

cultivars has raised questions regarding the objectives of pecan breeding programs 

which involve selecting for scab resistance. Breeders have selected for scab resistance 

for years, and there have also been attempts to introduce new resistance factors from 

other members of the hickory family via interspecific crosses (Graves & Diehl, 1991). 

It has generally been recognized that there is a “grace period” after the introduction of 

a new cultivar before scab becomes adapted to it, and the length of this grace period 

varies considerably among cultivars. One objective of the Georgia breeding program is 

to introduce new cultivars with high quality nuts with different resistance genes that 

can be transitioned into orchards to maintain diversity (Conner, 2003). The current 

Georgia program is also utilizing DNA markers for resistance genes and examining 

the physiological basis for scab resistance. Hopefully these efforts will lead to more 

durable field resistance in new pecan cultivars. 

2.3. Weed Management in Pecan Orchards 

Weeds are present throughout the world and many interfere with the optimum 

production of food and fiber. Holm, Doll, Holm, and Pancho (1997) state that 

approximately 200 plant species world wide are found to cause widespread 

problems in our crops. Many of these weeds occur in fruit and nut crops. Pecans are 

grown in the southern US and Mexico, an area that accounts for over 98% of the 

world’s pecan production (Pena, 2006). Vines, including annual vines such as the 

morningglories (Ipomoea species) and perennial vines such as trumpet creeper 

(Campsis radicans), and both annual and perennial grasses such as crabgrass 

(Digitaria spp.), goosegrass (Eleusine indica), bahiagrass (Paspalum notatum) and 

bermudagrass (Cynodon dactylon), are some of the most common and troublesome 

weeds in pecans (Southern Weed Science Society, 2006). Other species commonly 

found in pecan orchards include nutsedge (Cyperus species), horsenettle (Solanum 

species), arrowleaf sida (Sida rhombifolia), spurges (Euphorbia species), horseweed 

(Conyza canadensis), and pigweed (Amaranthus species) Colour pictures and 

descriptions are found in the Weed Identification Guide published by the Southern 

Weed Science Society (2007). 

Numerous weed-competition studies have shown the adverse effects of weeds 

on agronomic, vegetable, and fruit crops (Zimdahl, 2004). These studies generally 

document the effects of individual weed species on the growth and/or yield of a

144 


crop. Density studies have determined the effect of increasing weed density in 

season-long competition with the crop. Period of competition studies have 

determined the length of time the crop can tolerate competition from a specific weed 

at a specific density without incurring yield loss; or conversely, how long the crop 

must be maintained free of this weed before it can produce an optimum crop. 

Different types of information can be obtained with these studies. The critical period 

of weed control (CPWC) has been defined by Knezevic, Evans, Blankenship, Van 

Acker, and Lindquist (2002), as the time interval between two measured crop-weed 

competition components: (i) the maximum amount of time early-season weed 

competition can be tolerated by the crop before a yield loss occurs, and (ii) the 

weed-free period required from planting to obtain optimum yield (independent of 

other confounding factors, i.e. late season drought, insects, diseases, etc.). This 

period has been shown to vary from zero up to several weeks in work done with 

annual crops and weeds (Knezevic et al., 2002). In layman terms this answers the 

questions; how long must I maintain weed control in the crop to obtain optimum 

growth and yield, or how late can I wait to initiate and maintain weed control 

without incurring yield loss? Because most of the weed-competition studies were 

conducted using annual crops grown in narrow spacings (< 1 m) competing with 

annual weeds, weed control measures were generally applied on a “broadcast” basis. 

This is generally not the case with weed management in pecan orchards. 

Current weed management in pecan orchards involves weed control within a 

narrow strip centered on the pecan tree row. Also, many of the most troublesome 

weeds in pecan orchards are perennials. The CPWC has never been determined for 

pecan and would probably take several years research to determine. Smith (1999) 

determined that substantial reduction in growth of pecan trees occurred by weed 

competition from cutleaf eveningprimrose (Oenothera laciniata), a cool-season 

species, implying that the presence of weeds results in reduced growth of pecans 

even in cool months. 

Although several methods of orchard floor management have been used in the 

past, including mowing and cultivation (Ark, 1954), the use of registered herbicides 

is currently the most common method used by far (Alabama Cooperative Extension 

System, 2007; Georgia Cooperative Extension Service, 2007; Smith & Carroll, 

2004). Herbicidal active ingredients used to maintain weed control in pecan orchards 

include oryzalin, pendimethalin, diuron, simazine, norflurazon, fluazifop, 

sethoxydim, clethodim, flumioxazin, halosulfuron, paraquat, glufosinate, 

glyphosate, and carfentrazone. These herbicides can be used at different times and 

for specific weeds in orchard floor management. Some are restricted to non-bearing 

trees only, and some to trees established at least 2–3 years in the orchard. Most 

orchard floor management programs use a combination of these products to 

maintain season-long control in a weed-free strip centered on the tree row. 

Combinations of registered herbicides used in both preemergence and 

postemergence programs can provide optimum growth and yield (Faircloth, 

Patterson, Foshee, Nesbitt, & Goff, 2007). 

The area between tree rows is traditionally maintained in grass sod to facilitate 

movement of spray equipment that is used for fungicide and insecticide applications 

during the growing season. Consequently, this is known as the “sod-strip” method of


145 

orchard floor management. Maintaining a clean (bare ground) strip in the tree row 

also facilitates harvest in the fall since nuts can be blown away from the trees into 

the sod strips for pickup by harvesting equipment. 

There is also some use of herbicide in subduing unwanted vegetation in the 

traffic lanes where equipment runs between the tree rows. If there is a sod middle, 

“chemical mowing” with low rates of glyphosate is a common practice to reduce 

excess growth and reduce the need to mow (Alabama Cooperative Extension 

System, 2007; Georgia Cooperative Extension Service, 2007). Low rates of 

glyphosate are also applied just prior to harvest to reduce regrowth that might 

interfere with harvest, as mowing once nuts are on the ground is no longer an option. 

A recent practice has been the use of rolling wiper applicators with glyphosate to 

remove tall weeds from low-growing desirable plants like “Durana” white clover. 

Table 3. Yields of pecans were significantly influenced by weed control in irrigation and 

nonirrigated, Fairhope, Alabama USA (Patterson & Goff, 1993). 

Irrigation and 

weed control program 

Irrigated 

Total weed control w/ herbicides 

Disking 

Mowing 

Grass control w/ selective herbicides 

No weed control 

Mean value for irrigated trees 

LSD (P

146 


without weed control growing in both irrigated and not irrigated situations produced 

only 18.2 and 17.5% of the yield, respectively, that was produced by trees where 

total weed control was maintained over the first 8 years of growth (Table 3). This 

research also shows that mowing around newly planted trees, while controlling 

annual broadleaf weeds, allowed perennial grasses like bahiagrass to grow, thus 

robbing the young trees of fertilizer and moisture. Trees in the study that were 

mowed only as a means of managing the orchard floor produced 35.6 and 21.4% of 

the yield (irrigated and not irrigated respectively) produced by trees where total 

weed control was maintained using registered herbicides. This research was 

conducted using a treated area of 3 m(dia), centered on the tree row. The 3 m treated 

area was arbitrarily selected for this study. Additional research conducted following 

this initial study shows that weed-free areas of 3 m(dia) or greater maintained from 

planting provided optimum growth and yield while areas of 1.8 m (dia) or less 

reduced growth and eventual yield in the first 2 years of nut bearing (Patterson et al., 

1990). Although the significant and detrimental impact of weeds on pecan growth 

and yield has been documented, weeds can also serve as a host for insect pests 

(Norris & Kogan, 2005), and negatively influence concentrations of nutrients in 

young pecan trees (Goff, Patterson, & West, 1991). 

3. BENEFITS OF CRIMSON CLOVER AND LEGUMES USE IN PECAN 

ORCHARDS 

In the last 30 years, growers have started an integrated approach to weed control by 

seeding the orchard with various cool season legumes. These are grown as 

intercrops in the mowed strip or as cover crops over the entire orchard floor. The 

intercrop and cover crop plants supply nitrogen, suppress weeds, improve the soil, 

enhance beneficial insects and benefit wildlife. For centuries, legumes have been 

used to enhance the fertility and structure of agricultural soils. Historical references 

as far back as the Roman Empire refer to the benefits these plants can provide. Cato 

the Elder (234–149 B.C.) suggested improvements to poor vineyard land by interplanting 

a legume crop. This crop was then turned under before the plants set seed. 

The Chinese have also used legumes to maintain soil fertility through centuries of 

cultivation. Legume use was introduced to pecan orchard management in the early 

twentieth century. Pecan producers quickly realized the benefits of such plants as 

blue lupine, vetch, and crimson clover as winter cover crops for the orchard. 

Proper orchard management occurs at two separate, yet connected levels. The 

orchard floor influences the tree crop and its management based on the type of 

vegetation or lack thereof found in the orchard. An efficient orchard floor cover does 

not compete heavily with trees for moisture and nutrients and is compatible with 

orchard insect populations. Weed competition with tree roots is significant 

throughout the life of the tree. In a newly planted orchard, weed competition can 

significantly reduce young tree survival and can stunt tree growth (Patterson, 2005a, 

2005b). In the case of the mature orchard, vegetative competition can rob the soil of 

water and nutrients intended for the crop, reducing tree growth and yield, while also 

promoting alternate bearing. Pecan orchards generally consist of sod culture on the 

orchard floor with a weed-free herbicide strip approximately 2–4 m wide along the


147 

tree row. Row middles are maintained by mechanical mowing or by chemical 

mowing. The mowed sod middle improves wet weather passage for spraying, 

harvesting, and other orchard operations. 

Pecan trees have an extensive root system, consisting of a tap root which can 

penetrate as deep as the soil structure and water table permit, and small feeder roots 

located near the soil surface. While the deeper roots are an aid to survival of the tree 

in difficult environmental conditions, the feeder roots in the upper 6–18 in. of soil 

supply the bulk of the pecan’s nutritional needs and come into direct competition 

with vegetation on the orchard floor. 

Cool season legumes, such as crimson clover, posses a variety of characteristics 

that make them compatible with pecan production. Cool season legumes are not 

especially competitive with trees for soil moisture until mid to late spring. They also 

serve as an effective source of organically bound nitrogen (N). In addition, cool 

season legumes stimulate an early increase in beneficial insect populations. The 

environmental benefits of cool season legumes make their use an especially 

attractive practice. In addition to the benefits mentioned above, legumes can reduce 

weed competition, aid in the cycling of nutrients, build soil organic matter, prevent 

soil erosion and runoff, and serve as an effective source of food and habitat for a 

variety of wildlife species. 

3.1. Pecan Nitrogen Use and Compatibility with Crimson Clover 

Prior to World War II, legumes were commonly used as an orchard floor cover due 

to their N-fixing properties. The arrival of cheap fertilizer sources and mowed sod 

culture in the orchard led to a decline in the use of legumes as a floor cover in later 

years (White, Beaty, & Tedders, 1981). 

Of all nutrients applied to pecans, N most commonly limits pecan growth and 

orchard profitability. This element has a dominant influence on vegetative growth 

and crop production. In recent years, the rising cost of fuel, and its effect upon 

synthetic fertilizer production, has once again led to a need for alternative sources of 

N in many orchard operations. Leguminous plants are one very efficient source of 

organic N. 

All legumes, including crimson clover, utilize soil-dwelling bacteria that convert 

nitrogen from the air into a form that can be used by plants. This is termed “nitrogen 

fixation”. Only particular strains of bacteria provide optimum N production for each 

group of legumes. When the roots of a leguminous plant come into contact with the 

appropriate bacteria, the root hairs encircle the bacteria to create a nodule which 

houses the bacteria. These lumps on the root surface may range in size from a BB to 

a kernel of corn. 

Perennial legumes “fix” N during any time of active growth, usually peaking at 

flowering. With seed formation, N fixation ceases and the nodules slough from the 

roots. While they are alive, legumes release little to no nitrogen from the soil. As 

they die and are decomposed by soil micro-organisms, the N in the roots, stalks, 

leaves, and seeds are converted to a form available to other plants.

148 


Clover and other legumes are capable of supplying significant amount of N to 

orchard soils. Studies in Oklahoma suggest that a mixture of legumes including 

crimson clover, hairy vetch, red clover, and white clover planted to the orchard floor 

provided over 100 kg of N/ha. In the same study, pecan leaf N concentrations were 

maintained above a threshold of 2.25% by the above mixture, as well as by crimson 

clover alone Blue lupine can fix as much as 168 kg of N/ha, while common vetch is 

capable of fixing 92 kg of N (Smith, Shiferaw, & Rice, 1996). 

Pecans are an “irregular bearing” crop, meaning that they tend to bear heavy 

crop loads for 1–2 years, followed by very light crop loads, depending upon various 

physiological and environmental factors. A general rule of thumb for the N 

requirement of pecan trees is 4.5 kg of N for every 45.4 kg of expected crop (Wells, 

2007). Depending upon the degree of irregular bearing, mature pecan trees in the 

Southeastern USs may require from 78.5 to 168.1 kg of N annually for optimum 

production. 

Nitrogen uptake in the pecan tree is driven by demand. There are two critical 

periods of nitrogen demand during the season the first at early foliage growth and 

the second at kernel filling. The early spring foliage flush is nourished primarily 

from reserves held within the tree, while the nitrogen demand during the kernel fill 

stage is usually satisfied from soil uptake. If N is limited at kernel filling, then the 

tree will mobilize N from the foliage to the kernels. 

Studies have suggested that crimson clover over-winters dependably in the 

southeastern US and much of the US pecan belt. A vigorous stand of crimson clover 

will contribute between 78.5 and 168.1 kg of N/ha. When aided by moisture and 

warm weather to speed up decomposition, up to half the N available from legumes 

can be released within 7–8 weeks. In the light crop or “off” years, the N supplied by 

the clover alone, would be adequate for optimum production. Heavy crop or “on” 

years may require low supplemental N rates in order to bring marketable nuts to 

maturity and provide a return crop the following year. 

3.2. Enhancement of Pest Management 

Conserving and encouraging beneficial organisms is key to achieving sustainable 

pest management. The deep red blossoms of crimson clover attract various species 

of bees, which feed readily on the abundant nectar. In addition, blooms may harbor 

beneficial insects such as the minute pirate bug. Pea aphids and blue alfalfa aphids 

are commonly associated with crimson clover. Although these species are not pests 

of pecan, they serve as alternative food sources for beneficial predators such as 

ladybeetles, green lacewings, soldier beetles, predaceous stink bugs, damsel bugs, 

and hover flies. As the clover declines with the onset of warm weather in June, these 

beneficial insects move into the trees to feed on pecan aphids and other insect pests, 

reducing the need for insecticide application. 

In addition to reducing insecticide inputs through enhancing beneficial insect 

populations, the use of legumes in the orchard can also reduce herbicide use. As 

crimson clover grows, it forms a thick, living mulch. This helps to smother and 

shade out more troublesome, competitive weed species.


149 

3.3. Soil Building and Sustainability 

Clover can improve orchard soils in a number of ways. Protection against erosion is 

the most obvious benefit, but providing organic matter is an equally important, and 

more long term goal. Clover can provide habitat and/or food source for important 

soil organisms, break up compacted soil layers, and help dry out wet soils. 

Erosion deprives orchards of topsoil, the most fertile portion of soil with the 

highest amount of organic matter. When soil particles are dislodged by rainfall, they 

are more vulnerable to runoff. Cool season legumes can reduce the impact of rainfall 

on bare ground, slow the action of moving water, increase the soil’s ability to absorb 

and hold water, and help stabilize soil particles. Crimson clover produces more dry 

matter (6,237–6,683 kg/ha) than many other legumes and is recommended for soil 

erosion control because of its high early autumn dry matter production. 

Grass/crimson clover mixtures combine fibrous surface roots with long tap roots and 

have been observed to reduce herbicide runoff by 94–100%. 

As the soil–plant–atmosphere continuum cycles plant nutrients, some are 

recovered via plant uptake, some are incorporated into organic matter, some are 

adsorbed to mineral and organic surfaces, and some are precipitated as solid 

minerals. Excess nutrients are “lost” or removed from the field by runoff or 

subsurface flow, potentially ending up in water supplies. Nutrients such as N, that 

are the most water soluble and mobile in the soil, have the greatest potential for the 

pollution of ground and surface water (Havlin, Beaton, Tisdale, & Nelson, 2005). 

Over-fertilization is common in orchard crops because most growers rely on 

synthetic fertilizers. The amount of nitrogen removed by the crop in proportion to 

that applied is often far less with tree crops than with more traditional crops. 

Therefore, the leaching of nitrates into groundwater may be especially serious in 

orchard crops (Weinbaum, Johnson, & Dejong, 1992). Wiedenfeld, Fenn, 

Miyamoto, Swietlik, and Marlene (1999) suggested that sod alone on the orchard 

floor does not sufficiently reduce nitrate leaching. Green manures like cool-season 

legumes reduce the need for N application and aid in nutrient conservation by 

utilizing excess fertilizer not assimilated by the pecan trees, preventing undesirable 

nutrient levels in streams or lakes. 

Winter cover crops such as crimson clover grow primarily during a period of 

tree dormancy, when N uptake by the crop is at a minimum and percolation from 

rainfall is often the greatest. Although pecan growers have historically had little 

economic incentive to grow cool season legumes solely to prevent nitrate leaching, 

it is one of the many benefits they provide. 

Orchard floor covers can affect nitrogen uptake by the main tree crop if C:N 

ratios for the floor cover are high. In such cases, the micro-organisms responsible 

for decomposition of the highly carbonaceous plant matter require nitrogen to do so, 

and can lead to the unavailability of N for the main crop (Brady, 1974). Residue 

from a grass/legume mix has a higher C:N ratio than the legume alone. However, 

under humid conditions, the C:N ratio of such a mix is less than sod alone. In fact, 

ratios for the grass/legume mix are such that the release of N is slow, a scenario in 

which many perennial tree crops perform well. Slow release of nutrients also causes 

nutrients in the orchard soil to be less vulnerable to loss.

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Soil organic matter is composed of partially decayed and partially synthesized 

plant and animal residues. Although, the organic matter content of a mineral soil is 

generally only about 3–5%, its influence on soil properties and plant growth are 

great. 

Due to the work of soil micro-organisms, organic matter should be constantly 

renewed by the addition of plant residues. Legumes such as crimson clover break 

down quickly; however their root systems remain tough and fibrous, contributing to 

the accumulation of organic matter. The addition of organic matter to soils improves 

soil structure, increases water holding capacity, increases cation exchange capacity 

(the ability of the soil to act as a short term storage bank for positively charged plant 

nutrients), and provides more efficient storage of nutrients. 

Organic matter functions as a “granulator” of soil mineral particles. In most 

cases, the higher the soil organic matter, the more loose, easily managed, and 

productive the soil. Organic matter can also serve as a partial source of N, P and S. 

Through its effect on the physical condition of the soil, organic matter can increase 

the ability of the soil to hold moisture and make soil water more available for plant 

growth. 

Cation exchange is one of the most common and important of soil reactions. 

The cation exchange capacity (CEC) of a soil represents the capacity of the soil to 

hold cation, or positively-charged nutrients such as Ca +2 , Mg +2 , K + , and NH 4 + . The 

CEC is determined by the amount of clay or organic matter present in the soil. Soils 

with a higher clay and organic matter content have a higher cation exchange 

capacity than sandy, low organic matter soils. Hydrogen ions from the root hairs and 

soil microorganisms replace nutrient cations from the exchange complex. These 

nutrient cations are then forced into the soil solution, where they can be more readily 

assimilated by the root surface (Brady, 1974). Due to their effects on improving soil 

organic matter, legumes can aid in this process. 

Legumes help to increase the total number and diversity of soil organisms, 

which is the key to a healthy, well functioning soil. As organic matter increases, 

especially if succulent and subject to relatively rapid decay, it encourages microbial 

action of the heterotrophic organisms responsible for basic decomposition, as well as 

“free-living” bacteria, such as Azobacter, which can also fix N from the atmosphere. 

Legumes are closely associated with beneficial fungi, the mycorrhizae, which 

produce a water-insoluble protein known as glomalin, which binds and glues 

together particles of organic matter, plant cells, bacteria, and other fungi. 

Well aggregated soils are less prone to compaction. Heavy farm implements 

such as tractors, sprayers, mowers, shakers, and harvesters often make numerous 

passes over the orchard floor in a given season. Mycorrhizal fungi also have an 

efficient method of absorbing phosphorous (P) from the soil, which they pass on to 

their host. Without this relationship, P builds up in the soil. Although it is not 

leached, it can runoff into streams and rivers through soil erosion. The filaments of 

the mycorrhizal fungi effectively extend the root system and help the plants tap 

more P from the soil. Keeping P in an organic form is the most efficient way to keep 

it cycling in the soil. 

The culture of cool-season legume crops has both soil and nutrient conserving 

properties that are highly advantageous and readily applicable under most humid


151 

climatic conditions. In areas of low rainfall, the benefits of legumes will be limited. 

In such areas decomposition of the crop and its nutrient release may be too slow. 

Additionally, in such areas, moisture conservation is the primary factor governing 

soil and crop management. Thus, moisture should be conserved for the main crop. 

The residual effects of managing legumes as a cool-season cover crop in the orchard 

are also expected to be reduced on excessively sandy soils. 

3.4. Wildlife Benefits 

Due to the limited availability of suitable nesting areas in the United States for earlysuccessional 

songbirds, converting a common attribute of the southern agricultural 

landscape, such as pecan orchards, to a resource for food and reproductive habitat 

would provide some of the factors necessary to increase survival and nesting 

success. Increased abundance of birds and beneficial arthropods and higher species 

richness in agricultural fields have been linked to habitat heterogeneity (Freemark & 

Kirk, 2001). 

The sod/clover orchard floor mixture along with the pecan overstory allows for 

an increased landscape heterogeneity. Birds benefit from an increase in prey, an 

increase in cover for nesting sites and fledgelings, and a reduction in nest loss due to 

the elimination of mowing during the nesting season (Best, Whitmore, & Booth, 

1990; Rodenhouse, Best, O’Connor, & Bollinger, 1993). In addition to enhancing 

the landscape for non-game songbirds, as well as bobwhite quail, wild turkey, and 

mourning dove, cool-season legumes provide high quality forage for whitetail deer 

during the late winter when other food sources have dwindled (Rodenhouse, Best, 

O’Connor, & Bollinger, 1995). 

Clover has been shown to be highly effective at attracting high avian and 

arthropod densities, increasing wildlife and agronomic benefits compared with 

conventional management of agricultural systems (Cedarbaum, Carroll, & Cooper, 

2004; Warburton & Klimstra, 1984). The reduction of input in the clover system, 

coupled with its agricultural and environmental benefits, makes this system both a 

good choice for reducing negative impacts on wildlife and surrounding ecosystems, 

and for reducing input costs. 

3.5. Establishment and Maintenance 

In order to establish an adequate stand, crimson clover should be drilled at 16.7–20 

kg/ha or broadcast at 22.4–3.6 kg/ha. Establishment should be completed as soon as 

possible following pecan harvest, preferably in November–December. If clover is 

seeded prior to harvest, many seeds are removed from the orchard floor with the 

sweeping and harvesting process. Since legumes require the presence of rhizobial 

bacteria to effectively fix N, it is important to obtain the correct rhizobial inoculant 

for the legume being grown. Fresh inoculant and a sticking agent should be mixed 

with the seed. Otherwise, there will be few nodules and N fixation will be low. Soil 

pH should be maintained at 6.5 because Rhizobia bacteria cannot function properly 

under highly acidic conditions and will die in soils with pH below 5.0.

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Many southeastern orchards have well established populations of annual 

ryegrass. Where this occurs, the ryegrass often competes with and inhibits growth of 

clover. This can be prevented by the application of a low rate (1.12 kg/ha) of 

sethoxydim herbicide in February. The rye grass does not have to be eliminated, 

only stunted by this application in order to release clover from this competition. 

By foregoing mowing of the orchard until clover has gone to seed, producers can 

take advantage of crimson clover’s excellent natural re-seeding ability. This will allow 

a period of 3–5 years before clover will need to be re-seeded by the grower. Sandy 

sites will need to be re-seeded sooner than loamy or clay soils, therefore soil type 

should be taken into consideration when estimating the need for re-establishment. 

3.6. Costs and Savings 

The approximate cost of crimson clover seed and bacterial inoculum required to 

produce N-fixing nodules is approximately $99/ha. At 2005 N prices of $178/ha, 

this represents a difference of $79/ha. Clover can replace from 50 to 100% of 

synthetic N applied to pecan orchards, depending on the pecan crop load in a given 

year. This would save growers approximately $89–178/ha and significantly reduce 

the grower’s reliance on synthetic N. Reduced maintenance and mowing compared 

to grass covers creates further economic savings and reduces fuel consumption. 

Pecan acreage is widely dispersed and hard to track, but reliable estimates 

indicate that pecans are grown on approximately 550,000 acres in the US, with 

Georgia making up about ¼ of the total USA acreage. This would indicate a 

potential savings of approximately $19,800,000–39,600,000 in N costs, as well as a 

41,250 t reduction in the use of synthetic N nationwide with the use of N-fixing 

legume culture applied to orchard floor management. 

One of farming’s greatest challenges is to keep N in a stable, storable form 

until needed by the crop. The use of organic N, such as that produced by legumes, is 

an ideal way to accomplish this. Combining warm season sod culture and cool 

season legumes is a practical and effective strategy for conserving and supplying 

nitrogen for orchard crops, as well as enhancing stewardship of the environment 

through the enhancement of soil sustainability, beneficial insects, weed suppression, 

and wildlife. 

4. INTEGRATED PEST MANAGEMENT IN PECAN ORCHARDS 

Research indicates that biological control is effective with introduced biological 

control agents against pecan aphids (Tedders, Weaver, & Wehunt, 1973; Tedders, 

Reilly, Wood, Morrison, & Lofgren, 1990; Tedders & Schaefer, 1994; Mizell, 

1984), pecan weevil (Dutcher & Sheppard, 1983; Shapiro-Ilan, 2001; Shapiro-Ilan, 

Cottrell, & Gardner, 2004)), and pecan leaf scorch mite (Dutcher et al., 2006). Two 

biological controls that have been readily adopted by pecan growers are the 

enhancement of aphidophagous insects with orchard floor management and 

reductions in pecan weevil sprays.


153 

Orchard floor management techniques may improve biological control of 

pecan aphids. In improved orchards, tree density typically ranges from 12 to 60 trees 

per hectare. An orchard floor with mowed sod and herbicide strips in tree rows is 

excellent for harvesting the nuts but has low vegetational diversity (Dutcher, 1993). 

Natural enemies of aphids and other pecan insect pests are more abundant when the 

orchard floor is sown with plants that provide alternate prey, nectar, and pollen 

when pest populations are low. Orchards may require 15–30 trips by heavy 

machinery each year for all production and harvesting operations, leading to soil 

compaction (Bugg, Sarrantonio, Dutcher, & Phatak, 1991). Mowing can be reduced 

substantially by replacing turf grasses with clover (Rice, 1994). Previous studies 

have shown increased diversity and abundance of native aphid-feeding insects 

(aphidophaga) with alternative groundcover management in pecan Rice et al. (1998) 

found clover plus vetch to harbor significantly larger populations of ladybeetles 

(Family: Coccinellidae) than turf grass cover. Significantly higher populations of 

ladybeetles were found in various cool (Bugg, Dutcher, & McNeill, 1990) and 

warm-season (Bugg & Dutcher, 1989) covers. Unfortunately in both cases biological 

control of pecan aphids did not increase significantly. Multicolored Asian 

ladybeetle, Harmonia axyridis (Pallas), has been successfully introduced and 

established into the pecan belt since the above experiments were conducted. 

Multicolored Asian ladybeetle is a much more effective predator on pecan aphids 

than native ladybeetles. Even though Rice et al. (1998) did not find a significant 

increase in biological control overall in groundcover-enhanced orchards, they did 

observe an increase in one isolated orchard where multicolored Asian ladybeetle had 

recently become established. 

Culturing ladybeetles on alternate prey aphids on crapemyrtle plants grown on 

the orchard floor until pecan aphids become more abundant may be effective (Mizell 

& Knox, 1993). Crapemyrtle aphids is a good candidate as an alternate prey for 

aphidophaga in the pecan system because they peak on crapemyrtle plants about 2 

weeks before pecan aphids. This is ideal timing to build up aphidophaga before the 

expected peak in pecan aphids. In addition, crapemyrtle aphid and black pecan aphid 

are taxonomically similar and are attacked by the same natural enemies (Mizell & 

Schiffhauer, 1987). Intercrops sown away from the herbicide strip and in the mowed 

sod compete with grasses and not the trees and have additional benefits. Combinations 

of red and white clovers or clover plus vetch provide adequate nitrogen for pecan 

(Smith et al., 1996; Diver & Ames, 2000). Supplemental nitrogen fertilizer is effective 

in maintaining leaf nitrogen concentration at a healthy level when it is applied to the 

herbicide strip or through the irrigation system (Worley, 1994). 

Native and introduced natural enemies of the black pecan aphids do not reduce 

aphid populations with sufficient speed to prevent serious damage. The population 

dynamics are well understood (Kaakeh & Dutcher, 1992). Early warning scouting 

techniques are used to measure abundance, population distribution, and predict 

outbreaks (Dutcher & Kaakeh, 1992). Black pecan aphid feeding leads quickly to 

leaflet abscission (Wood, Tedders, & Thompson, 1985; Tedders & Wood, 1985; 

Tedders, 1978), and control is achieved by quickly resorting to chemical control 

whenever black pecan aphid abundance exceeds one aphid per compound leaf 

(Dutcher, 1983; Dutcher & Htay, 1985).

154 


Secondary predators interact with biological controls and these can enhance or 

hinder control effectiveness. For example, insects are a major source of nutrition for 

red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae). These 

ants are important predators of pests including southern green stink bug (Krispyn & 

Todd, 1982), cowpea curculio (Russell, 1981) and pecan weevil (Dutcher & 

Sheppard, 1983). Pecan weevil larval populations are consistently reduced by 33% 

after the larvae drop to the soil surface from the pecans and before they burrow into 

the ground (Dutcher & Sheppard, 1983). Red imported fire ants also interact with 

aphids and aphidophaga in the pecan trees (Tedders et al., 1990). Ant foraging can 

be partitioned with insecticide barriers sprayed on the tree trunks so that red 

imported fire ants will remain on the soil surface to prey on weevils and not interfere 

with aphidophagous insects in the trees (Dutcher, Estes, & Dutcher, 1999). The 

effect of these trunk sprays has been effective (Dutcher, 2004; Dutcher et al., 1999) 

and ineffective in reducing aphid populations (Harris et al., 2003). Red imported fire 

ants can tunnel under the insecticide barrier without becoming intoxicated and 

produce a trail to the tree crown, esp. on older trees with heavy bark. Farnesol, an 

ant repellent that form an impassable odor plume around the trunk successfully 

prevents Argentine ants from foraging in citrus trees (Shorey, Gaston, Gerber, Sisk, 

& Phillips, 1996). Current research has found that farnesol was not an effective 

repellent of ants on pecan trees but certain plant extracts (neem extract, sesbania 

extract), natural compounds (methyl anthranilate, methyl myristate) and an 

industrial repellent (methyl carbitol) are effective ant repellents that prevent foraging 

in pecan trees (Dutcher & Beaver, 2005). 

Pecan weevil has a relatively long life cycle and lower reproductive capacity in 

comparison to other pecan insect and mite pests (Table 2). Growers may achieve 

control by integrating chemical control for adults biological control with soil 

application entomopathogens and entomophillic nematodes, and red imported fire 

ants with and removal of alternate host trees from the woodlots adjacent to the 

orchard to reduce immigration of adults into the orchard. Risk rating (Mizell, 1984) 

estimates the relative probability of pest outbreak based on all pertinent information 

that is known about a particular area and may be useful in integrating control 

methods for pecan weevil. Pecan cultivars and trees of different ages (sizes) differ 

considerably to the susceptibility to injury by pecan weevil (Worley & Mullinix, 

1997). Certain pecan cultivars have a narrow window of susceptibility to pecan weevil 

oviposition with either a short kernel development time, or an early or late onset of 

kernel development (Harris, 1985). Weevil can be controlled in these cultivars with 2–3 

applications of carbaryl compared to 4–5 applications for standard cultivars. 

Precision applications of carbaryl to tree trunks and spot treatments in highly 

infested portions of the orchard stems may reduce nut damage in the pecan tree. Nut 

damage is higher in trees with higher densities of weevils emerging from the soil 

directly beneath the tree (Dutcher et al., 2003). In early replicated field trials, trunk 

sprays effectively killed adult weevils on the trunk for up 13 days after application of 

carbaryl (Cottrell & Wood, 2003). It has been estimated that 70–80% of the adult 

weevils fly to the trunk first (Raney & Eikenbary, 1968) and could thus be targeted for 

insecticide application to manage pecan weevils. This would reduce entire canopy 

sprays, which are known to be detrimental to natural enemies and flare aphid and mite


155 

populations (Dutcher & Payne, 1983). The trees in native groves have a unique nut 

phenology in each tree adding to the variability in pecan weevil distribution (Reid & 

Mulder, 2003). Pecan weevil distribution in the orchard can be estimated from tree-totree 

measurements of % nut damage, crop load, and known population parameters of 

the weevil (Harris, 1985) and then validated by extensive trapping of emerging adults 

with cone emergence traps from a known area of the soil surface (Raney, Eikenbary, 

& Flora, 1970). Accurate weevil distribution maps would allow the precision 

application of soil applied biocontrol agents and foliage and trunk sprays of carbaryl. 

Significant risk of hemipteran kernel damage is associated with soybean 

plantings (and other alternate host plants) adjacent to the pecan orchards and the 

lack of a trap crop for monitoring and control of the hemipterans. Spot treatments of 

insecticide sprays to the trees in the first two border rows adjacent to the alternate 

host plants are effective in reducing stink bug damage (kernel spot) throughout the 

orchard. Legume trap crops between the trees and the alternate host plants are 

effective and have been used by pecan growers for reducing kernel spot. Even low 

black aphid populations on less susceptible cultivars cause significant leaf damage 

and defoliation. However, on less susceptible cultivars the onset of the outbreak is 

often several weeks later than on susceptible cultivars (Wood & Reilly, 1998). 

Kernel spot is caused by several species of true bugs belonging to the families, 

Pentatomidae and Coreidae. Initially, kernel spot was thought to be caused by 

disease and treated as such until it was proven (Adair, 1927) that these conditions 

were caused by several species of kernel feeding hemipterans. The primary kernel 

feeding hemipteran pests of pecan include the southern green stink bug, Nezara 

viridula; green stink bug, Acrosternum hilare; brown stink bug, Euschistus servus; 

Dusky stink bug, Euschistus tristigmus and the leaffooted bugs, Leptoglossus 

phyllopus and L. oppositus. All of these insects are phytophagus and feed on a wide 

range of plants (McPherson & McPherson, 2000). Stinkbugs find crops such as 

cowpeas and soybeans more appealing than pecan trees when plots of these crops 

are planted near pecan orchards, gravitating toward the trap crop and away from the 

trees. 

The primary challenges pecan producers face in managing these pests include 

the lack of economic thresholds to make management decisions, the long period of 

susceptibility to damage (nut set to harvest), the difficulty in scouting for damaging 

populations and the limitations on insecticide use near harvest. Leguminous trap 

crops, sown adjacent to seedling and improved pecan orchards, effectively and 

consistently reduce the incidence of kernel spot by 50% in improved pecan orchards 

(Smith, 1996, 1999). The trap crops are sprayed as the pods mature with an 

insecticide to kill the hemipterans before they enter the orchard (Coolman, 2003). 

Growing trap crops is beneficial for owners of small pecan orchards, as well as 

people who want to grow their pecan crops organically. Growing a trap crop around 

the orchard controls stink bugs without spraying the trees. Sunflower, sorghum and 

millet are also attractive to kernel-feeding hemipterans and produce seed that is 

attractive to hemipterans in the early fall at the same time as the pecans are 

susceptible to kernel spot. In native pecan groves, trap crops or broad scale 

application of pesticides to control stink bugs populations are not practical since 

livestock and poultry are part of the system. The mid-summer weeds in the groves

156 


are attractive to kernel-feeding hemipterans and the weeds provide a place for stink 

bug populations to develop within the grove itself and mowing of these weeds is an 

alternative control technique. Trap crops also provide excellent food for quail. Many 

pecan growers already plant small grains near the orchard border in the fall to feed 

wildlife and improve hunting, esp. for quail. A pecan grower in Texas achieved 

significant reductions in the incidence of kernel spot by plant a nontreated trap crop 

of black-eyed peas (United States Environmental Protection Agency, 2004). 

Integrated pest management came to the forefront in pecan pest control after 

problems arose with pest resurgence, pesticide resistance, pest replacement, and an 

increase in virulence of the pecan scab fungus. These problems lead to outbreaks of 

aphids, mites, leafminers and pecan scab. Growers, researchers and extension 

specialists developed and implemented integrated pest management methods in 

attempts to solve many of these problems. Current pest management practices for 

pecan orchards are a genuine integration of various natural, cultural, biological and 

chemical control techniques. These include: monitoring crop load, orchard floor 

management, soil amendments, scouting pest populations, enhancement of on 

natural enemies, decision models, action thresholds, looking for pecan scab 

resistance in pecan cultivars, inoculative release of introduced insect and mite 

predators, planting intercrops, selective timing of chemical pesticide sprays and 

selective pesticides. Reducing broad spectrum insecticide spray frequency with 

improved monitoring techniques, weather models and assessments damage impact 

coupled with spot treatments has reduced the incidence of secondary pest resurgence 

after treatments for pecan weevil and kernel feeding hemipterans (Dutcher & Payne, 

1983). Biological controls and biorational or selective insecticides are under 

development for other insect and mite problems are effectively controlled with 

(Dutcher et al., 2003). 

Integrated pest management research and extension work (Dutcher et al., 2003) 

in the past 25 years has developed new methods that reduce the amount of insecticide 

used by 35% (Smith et al., 2002). The future of pecan integrated pest management lays 

in the development of reduced fungicide spray frequency in the southeastern USA 

during time periods of low humidity and leaf wetness and reduced soil compaction and 

herbicide use through orchard floor management. Integration of the tactics enhances 

aphidophagous insects, improves the soil, and reduces the production costs for the 

pecan grower. Above and beyond these improvements, integrated pest management in 

the pecan orchard is the only known strategy for avoidance of secondary pest 

resurgence, replacement of a primary pests, and pesticide resistance development. 

These phenomena can double the costs of pest control. 

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7 

LOCUST HABITAT MONITORING AND RISK 

ASSESSMENT USING REMOTE SENSING AND GIS 

TECHNOLOGIES 

ALEXANDRE V. LATCHININSKY 1 AND RAMESH 

SIVANPILLAI 2 

1 Department of Renewable Resources, University of Wyoming, 


2 Department of Botany and Wyoming 

Geographic Information Science Center, University of Wyoming, 


Abstract. Locust outbreaks occur on all continents except Antarctica and can affect the livelihoods of one 

in 10 people on Earth. To prevent economic and environmental losses, locust breeding areas should be 

periodically monitored, and an early detection-early response strategy should be in place. Traditional, 

ground survey methods are inefficient to adequately address the large spatial scale of the locust problem. 

Remote Sensing and the associated geospatial technologies can provide timely data to assess the risk of 

impending locust outbreaks. This information could be used for targeted preventive management actions 

in the locust breeding areas. Remotely sensed data are used for monitoring habitats of certain species such 

as the Desert, Migratory and Australian Plague locusts. However, the vast potential of this technology 

remains untapped for other locusts. This chapter provides a review of remote sensing and GIS concepts, 

types of data collected by various remote sensing satellites, and applications of geospatial tools for locust 

habitat monitoring and risk assessment. 


Locust outbreaks and subsequent destruction of vegetation result in ecological, 

environmental and economic problems. Locust swarms can devour green vegetation, 

including agricultural crops, across large geographic areas thereby upsetting the 

ecological processes (e.g. carbon and water cycles) of the region or any landscape. 

Rapid loss in vegetation cover can result in soil erosion and increased run off. Crop 

damages could result in catastrophic losses to farmers, and this problem could be 

acute for small, subsistence farmers throughout the world and especially for those in 

developing countries. Furthermore, locust control efforts, which involve large-scale 

applications of broad-spectrum insecticides, can produce negative impact on the 

environment and continue to be very costly, even in the twenty-first century. 

163 




164 

A.V. LATCHININSKY & R. SIVANPILLAI 

In 2003–2005 a Desert locust outbreak affected 8 million people mostly in 

Africa, with estimated damage to crops at 80–100% (Brader et al., 2006). To combat 

the outbreak, 13 million ha were treated with neurotoxins in 26 countries. The cost 

of the international campaign, including the food aid to affected populations, 

amounted to half a billion US dollars (Belayneh, 2005). 

In order to protect the farmers and the environment from such catastrophes, 

several national and international agencies and organizations are involved in a host 

of prevention and control activities. These activities are aimed at either minimizing 

the large-scale locust plagues or at quickly containing them following an initial 

outbreak. Since the geographic area involved is often large (across national 

boundaries), coordination is required in the form of information exchange on the 

status of locust swarm distribution and damage. In most countries information on 

locust nymphal development and swarm formation is collected through groundbased 

surveys. Data collected by field surveys are reported to the national locust 

control units, which then share them with other national and international agencies. 

To assess locust risks and develop preventive measures data on land cover habitat 

condition are required. Vegetation represents the essential component of the locust 

habitat, providing the insects with nutrition and shelter. 

Under the preventive mode, locust control specialists also need information on 

elevation (or topography), soil moisture, temperature and rainfall, in addition to the 

vegetation type, status and growth. Specialists use this information to set up 

effective surveys to assess locust egg-pod or nymphal distribution. During an 

outbreak, near real-time data on vegetation damage, hopper band and swarm 

movement will be essential for assessing risks and prioritizing areas for curative 

treatments. Under either circumstances reliable methods are necessary for collecting 

information on vegetation status or assessing the damage to the native vegetation or 

crops resulting from locust outbreaks. Traditional, ground-based survey methods are 

inadequate to provide accurate and timely information about an ongoing locust 

outbreak and devise efficient management approaches, since the locust hopper bands 

move several km and swarms can travel up to 200 km in a day (Uvarov, 1977). 

Remote sensing technology can provide necessary data for assessing locust 

outbreak threats and post-outbreak damage. Remote sensing technology is a means 

to rapidly collect information on vegetation and earth surface conditions for 

relatively large geographic areas. These data are routinely used for assessing the 

status of land and natural resources or for assessing the magnitude of events such as 

wildfires and hurricanes. Satellite images were used extensively to coordinate the 

rescue and recovery efforts following the tragic devastation of the South Asian 

Tsunami in 2004 (Kumar, Chingkhei, & Dolendro, 2007; Wikantika, Sinaga, Hadi, 

& Darmawan, 2007). Satellites can download these data rapidly to receiving stations 

on the ground enabling the users to visualize the data in near-real time. Currently, 

there are remote sensing satellites that collect data for the entire earth every 2 days. 

In other words, one can monitor the status of any location on the earth’s surface 

every 2 days. Advances in computing hardware and software have enabled 

sophisticated processing of large volumes of data that was not possible until a few 

years ago. Through the use of such data, information on earth surface conditions can 

be updated more frequently, in comparison to the traditional survey methods.

LOCUST REMOTE SENSING AND GIS 

165 

Image data collected by the satellites can be incorporated with other types of 

information (roads, rivers, villages and administrative boundaries) in a geographic 

information system (GIS). Using a GIS one could generate a map showing 

potential areas of interest that are within a specified distance from major roads. 

This information could be used for targeted locust field surveys or to identify the 

extent of areas that cannot be easily accessed. Also using the information on 

administrative boundaries it is possible to generate summary maps showing the 

extent of infestation and damage, per administrative unit. Such information could 

be generated in the form of both maps and reports more easily and quickly in 

comparison to the traditional cartographic methods. In the US, wildfire maps are 

updated daily using satellite data to enable the firefighters to assess the extent and 

direction of the wildfires (Keane, Burgan, & Van Wagtendonk, 2001; Hessburg, 

Reynolds, Keane, James, & Salter, 2007). Also, the Food and Agriculture 

Organization of the United Nations (FAO) uses GIS extensively to map the land 

conditions in Africa and generate monthly Desert locust information bulletins (see 

http://www.fao.org/ag/locusts/en/info/info/index.html). 

However, remote sensing technology is not capable of addressing all the 

information needs of the locust control specialists. Its potential is oversold across 

several applications resulting in bad reputation among users (Wynne & Carter, 

1997). The process of converting data to useful information is rigorous and requires 

substantial training and knowledge on the part of an image analyst. These skills are 

critical to successfully extract information off of the images. Nevertheless, several 

of these risks could be addressed by careful planning and adequate training of the 

analysts in the use of image processing for information extraction. If implemented 

correctly, remotely sensed and GIS technologies can provide essential information 

for managing locust problems worldwide. 

2. REMOTE SENSING, GEOGRAPHIC INFORMATION SYSTEMS (GIS), 

AND GLOBAL POSITIONING SYSTEMS (GPS) 

2.1. Remote Sensing 

Remote sensing is defined as the science and art of making observations and 

measurements about objects without coming into physical contact (Campbell, 2006). 

For example, a human eye remotely senses or “sees” by responding to the radiation 

emanating from the surrounding objects without any physical contact. All objects 

above absolute zero (0 K or –373°C) emit electromagnetic radiation and also interact 

with the incoming solar radiation. When solar radiation comes in contact with an 

object it can be reflected, transmitted or absorbed to be re-emitted and the pattern of 

this interaction is unique for each object, which is referred as the spectral signature 

for that object. For example, green leaves absorb radiation in the blue and red 

regions but emit in the green region, hence they appear green to human eyes. 

Changes in the leaf chlorophyll content alter the reflectance pattern which results in 

different colors of the leaves to human eyes.

166 


Table 1. Spectral ranges in the electromagnetic spectrum (in nm unless otherwise specified). 

Spectral range 

Name 


167 

Remote sensing is categorized as passive or active based on the source of the 

electromagnetic radiation. In passive remote sensing, sensors record the radiation 

emitted or reflected by earth surface features. For example, when data are recorded 

in the form of images in bright sunlight (or outdoors) without any other source of 

radiation it is termed as passive remote sensing. Black & white photos have been in 

use for more than a century and extensively in World War II to identify and destroy 

enemy targets. Color infrared photos were acquired since mid-1950s and have found 

widespread use in vegetation mapping and monitoring (Jenson, 2006). Digital 

sensors, mounted in satellites, aerial platforms and space shuttles, are used more 

frequently for collecting remotely sensed data. Digital data are available in ready-touse 

formats and can be processed more efficiently than hard copy aerial 

photographs. Availability of these data in digital format coupled with the advances 

in computing technology, have resulted in increased use of remote sensing for 

numerous applications. 

Active remote sensing systems use their own source of electromagnetic radiation 

that is targeted towards various objects and records the interacted information that 

reaches the sensor. If one uses a flash light in the camera to illuminate indoor objects 

for recording images, this is active remote sensing. Examples of active remote 

sensing data include RADAR and LIDAR images that are acquired by targeting 

electromagnetic radiation in specific regions on various features and recording their 

interaction pattern. Active remote sensing technology provides opportunities for 

acquiring images during night time or cloudy days. Both RADAR and LIDAR can 

penetrate through the top of the vegetation canopy, which is not possible in passive 

remote sensing, enabling vertical characterization of forests and other features. 

RADAR can also penetrate soil, hence it is used in archeology for locating and 

mapping large hidden structures and artifacts. 

Utility of remotely sensed data is influenced by its spatial, spectral, temporal and 

radiometric resolutions among others. Spatial resolution determines the size of the 

smallest feature that can be identified in an image. No standard rules exist to 

categorize remotely sensed data based on its spatial resolution, however certain 

guidelines have evolved over time. Images are categorized as high (

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Table 2. Remote sensing satellites and their data characteristics. 

Satellite & country Spectral bands Pixel 

size (m) 

Swath (km) 

Coarse resolution 

NOAA-GOESS (USA) 1,000 >2,000 

SPOT VEG (France) 1,000 

TERRA/MODIS (USA) 250 >2,000 

500 

1,000 

Moderate resolution 

Landsat 5 (USA) B, G, R, 3 IR 30 185 

SPOT-2 (France) G, R, 2 IR 20 120 

IRS 1C (India) G, R, 2 IR 23 70, 142 

IRS 1D G, R, 2 IR 23 70, 142 

SPOT-4 G, R, 2IR 20 120 

Landsat 7 B, G, R, 3IR 30 185 

TERRA/ASTER 

(Japan/USA) 

G, R, IR 

4 IR 

3 Thermal IR 

15 

30 

90 

EO-1 (USA) 30 37 

Proba (ESA) 18, 36 14 

SPOT-5 10 120 

IRS ResourceSat 20 24, 140, 740 

IRS-AWiFS (India) 56 350 

CBERS-2 (China/Brazil) 20 113 

FormaSat (Taiwan) 8 24 

ThaiPhat (Thailand) 36 600 

MONITOR-E-1 (Russia) 20 94, 160 

Beijing-1 (China) 32 600 

TopSat (UK) 5 10, 15 

ALOS (Japan) 10 35, 70 

60 

Temporal resolution is related to the time lapse between successive image 

acquisitions. For example, Landsat 5 – TM satellite acquires data every 16th day for 

any given location on the surface of the earth, and therefore its temporal resolution 

is 16 days. Other satellites (e.g., AVHRR) collect data on daily basis. 

Radiometric resolution is a measure of precision of the recorded data and 

measured in bits. In an 8-bit data recording device, 256 (2 8 ) levels of brightness 

values can be recorded, whereas 10-bit device can record 1024 (2 10 ) levels of 

brightness values. Satellite and aerial based remotely sensed data are available in 

difference combinations of resolutions (example, 30 m spatial, 6 spectral bands, 16 

day temporal and 8-bit radiometric resolutions) and it is up to the analyst to select 

the correct type of data for matching the informational needs of a task.


169 

2.2. Information Extraction 

Remotely sensed data are available in digital format (earlier, these images were 

printed as hard copy maps and features were manually interpreted). Analysts can 

display the images in any image processing software (Table 3). Depending on the 

specific informational needs, enhancements or classification can be carried out on 

these images. Enhancement refers to a set of image processing steps where 

information content about one or more features in the image is highlighted. 

Enhanced products can be used to prepare hard copy maps or further digital 

processing. Vegetation indices are computed from these images for monitoring 

vegetation condition. Vegetation indices computed from two different time periods 

are useful for change assessment studies. 

Table 3. Selected examples of remote sensing software. 

Software Manufacturer Website 

ENVI ITT VIS www.ittvis.com 

ERDAS imagine ERDAS Inc. www.erdas.com 

ER mapper ERDAS Inc www.erdas.com/ermapper 

IDRISI Clark Labs www.clarklabs.org 

ILWIS ITC www.itc.nl/ilwis 

Image analyst Intergraph www.intergraph.com 

PCI PCI Geomatics www.pcigeomatics.com 

Mapping earth surface features requires a suite of sophisticated image processing 

tools, such as unsupervised and supervised, neural network and fuzzy logic 

classifiers. Each algorithm has its own advantage and the analyst decides on the type 

of classifier for a given mapping project, based on the informational requirements 

and resource availability along with the time constraints. Most remote sensing 

textbooks include detailed discussion on image classification algorithms. Products 

generated from these classification routines can be printed as maps or can be 

integrated in a GIS for further analyses. Since remotely sensed data are collected on 

a routine basis, periodic updates can be generated for any area and changes in land 

cover can be assessed. 

2.3. Geographic Information Systems (GIS) 

GIS is a computer-based system for storing, displaying, manipulating and analyzing 

geographic data, that can be tied to a geographic location to be described as 

geographic data. For example, the number of locust egg-pods (data) collected in 

each county or district (geographic location) is termed as geographic data. GIS can 

store, organize and analyze diverse sets of geographic data, such as the number of 

locust egg-pods, hopper band or swarm density and area, temperature, rainfall 

received, vegetation at those sites and so on. Users can query a GIS in order to 

combine information from physical and environmental variables for any application.

170 


As physical and environmental conditions change, one can update the 

information stored in a GIS and generate new results in a relatively short time. For 

example, an analyst can select sites for field visits based on distance to roads and 

vegetation types. Information on roads and vegetation types are stored separately (as 

spatial data layers) in a GIS and can be combined to generate new or derived 

information. It is possible to combine other variables (e.g. soil type, elevation values 

etc.) to narrow down the sampling sites. A thorough discussion on GIS is beyond the 

scope of this chapter, but numerous textbooks are available. Similarly, GIS software 

has also grown in number and functionality and some of the commonly used ones 

are listed in Table 4. 

Table 4. Selected examples of geographic information system (GIS) software. 

Software Manufacturer Website 

ArcGIS ESRI www.esri.com 

AutoCAD Autodesk www.autodesk.com 

Cartalink Clark Labs www.clarklabs.org 

GeoMedia Intergraph www.intergraph.com 

GRASS US Army Labs www.cecer.army.mil 

MapInfo MapInfo www.mapinfo.com 

MicroStation Bently Systems www.bently.com 

TNTmips MicroImages Inc. www.microimages.com 

Surfer Golden Software www.golden.com 

Sage GIS DLSR www.dlsr.com.au 

GIS technology can be used for analyzing spatial patterns in insect populations. 

Georeferenced data about insect densities, crop type, and soils for a location can be 

incorporated in a GIS for producing new map layers (Liebhold, Rossi, & Kemp, 

1993). A map layer, generally composed of only one type of data, thus has a theme. 

Furthermore, themes that represent similar areas can be combined to form a full GIS 

database. The GIS serves as a tool for analyzing interactions within and between the 

various spatially referenced data themes. Management and analysis of large spatial 

databases would be impossible without this type of software. 

GIS is being widely used in conjunction with remotely sensed data (satellite 

imagery) in Africa and Australia for mapping locust habitats (Bryceson, 1989; 

Cressman, 1997; Voss & Dreiser, 1997). FAO Scientific Advisory Committee 

considered GIS as the most appropriate technology to aid locust forecasters and 

researchers (FAO, 1989). GIS is able to improve the specialists’ ability to assess and 

interpret current and historical data on locusts and the environment (Healey, 

Robertson, Magor, Pender, & Cressman, 1996). Since Desert locust records are 

among the most complete which exist for an insect pest, a specific GIS “SWARMS” 

(Schistocerca WARning Management System) has been developed offering 

researchers and decision makers improved information for studying population 

dynamics and for displaying and testing alternative control strategies (Cressman, 

1997; Magor & Pender, 1997).


171 

GIS techniques have also been applied to grasshopper ecology in temperate 

regions, especially in the US. In Montana, with the use of GIS, regional spatiotemporal 

grasshopper outbreak characteristics have been examined (Kemp, Kalaris, 

& Quimby, 1989; Cigliano, Kemp, & Kalaris, 1995). In Wyoming, GIS was 

implemented to reveal the historic spatial characteristics of grasshopper outbreaks 

(1960–1993), as well as for spatial analysis of ecological factors related to 

grasshopper population dynamics (Schell, 1994; Lockwood & Schell, 1995). Schell 

(1994) studied the spatial properties of grasshopper infestations in Wyoming and 

found that 72% of grasshopper outbreaks are confined to a particular soil type which 

has a very limited distribution range (1% of the state). Thus, the GIS analysis 

revealed that a certain ecological factor was highly correlated with the potential of a 

habitat to support an outbreak. The results of this study contributed greatly to the 

optimization of grasshopper survey and management in the state (Schell & 

Lockwood, 1995, 1997a, 1997b). 

2.4. Global Positioning Systems (GPS) 

GPS is used, among applications, for determining geographic coordinates while 

collecting data in the field. GPS consists of a constellation of satellites that transmit 

signals which are received by hand-held units called GPS Receivers, that can 

process the signals and determine precise geographic position. Time taken for these 

signals to travel from each satellite to the GPS receiver is used for computing the 

distance to each satellite. A minimum of 3 distance measures from 3 different 

satellites are required to determine a geographic position on the surface of the earth. 

Sophisticated GPS Receivers can simultaneously receive signals from 8 or more 

GPS satellites and therefore compute geographic coordinates with higher accuracy. 

Based on the precision and sophistication GPS Receivers are categorized as 

recreational, mapping and survey grade GPS. Survey grade GPS Receivers are 

expensive and provide very accurate measurements, in comparison to the other 

grades of receivers. 

GPS technology is widely used for navigation and surveys. Relatively 

inexpensive receivers are used in recreational activities while more precise GPS 

receivers are used for navigating emergency and transportation vehicles and to 

obtain their whereabouts in real time. GPS technology is used in field data collection 

for applications such as locating sampling sites or insecticide-treated areas. 

Previously researchers would mark these locations on a printed map to associate 

their samples to geographic space. With the help of GPS technology, researchers can 

record the geographic coordinates while collecting field data and later they can 

export the coordinates to image processing or GIS software. This process eliminates 

errors associated with transcribing field notes and annotated coordinates in maps. 

Several national and international agencies use GPS technology for collecting 

periodic information about events on a near-real time basis. Such methods, in 

addition to reducing the errors associated with transcribing, reduce the time required 

to generate updated information from field data obtained periodically.

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3. REMOTE SENSING AND LOCUST PEST MANAGEMENT 

Remotely sensed data collected from airplanes and satellites have been used 

for mapping locust habitats and also for assessing the damages to vegetation 

following a locust outbreak. Individual aerial photographs often cover smaller area 

on the ground in comparison to the area covered by moderate resolution satellite 

images such as Landsat (Table 2). The geographic area of some coarse resolution 

satellite images such as AVHRR and MODIS cover several thousand square km. 

Ability to monitor or map large geographic areas is particularly appealing for 

assessing locust damages in remote regions of the earth. Showler (2003) categorized 

the applications as strategic or tactical. Strategic applications include mapping 

potential or actual locust habitats and using that information to devise suitable 

prevention measures e.g., chemical treatments. Tactical applications include 

monitoring ongoing locust plagues from aerial platforms or assessing damages to the 

vegetation following locust outbreaks. Following sections focus on the habitat 

requirements and lessons learned from using remotely sensed data and technology 

for either mapping locust habitats (strategic) or assessing damages (tactical) 

following locust outbreaks. 

In the domain of locust pest management, remote sensing has been used for the 

detection of changes in vegetation and the measurement of certain meteorological 

parameters. For example, satellite images were used to detect zones of green 

vegetation (temporarily mesic habitats activated after sporadic rains) which had the 

potential for colonization by locust populations in xeric landscapes of Africa 

(Cherlet, Di Gregorio, & Hielkema, 1990; Cherlet & Di Gregorio, 1993; Voss & 

Dreiser, 1994, 1997) and Australia (McCulloch & Hunter, 1983; Bryceson & 

Wright, 1986; Bryceson, 1989). With its broad infrared electromagnetic spectrum, 

the TM sensor of the Landsat satellite appears to be a useful instrument for detecting 

different vegetation communities by their reflection in the landscape and mapping of 

locust habitats at scales up to 1:100,000 (Voss, Drieser, & Popov, 1992, 1993a, 

1993b, 1994). 

As for the detection of the entomogenic effects on the vegetation, satellite 

imagery has proved to be useful in forest entomology (Dottavio & Williams, 1983; 

Rencz & Nemeth, 1985). It also has potential for determining the crop losses due to 

locusts (Wewetzer, Krall, & Schultz, 1993). An attempt to use satellite imagery in 

the context of rangeland grasshopper ecology (Schell & Lockwood, 1996) strongly 

suggested that combinations of thermal and infrared wavelengths can distinguish 

infested lands from the surrounding areas. Thus, active infestations are apparently 

revealed by a combination of entomogenic effects, including: (1) more rapid heating 

of the habitat, perhaps due to increased exposure of soils upon removal of forage by 

grasshoppers (thermal), (2) decreased plant/soil moisture, perhaps as a consequence 

of grasshopper feeding (mid-infrared), and (3) changes in plant cell structure, 

perhaps as a consequence of herbivory-induced stress (near-infrared). A 

characteristic “halo” effect has been found with active outbreaks, which suggests a 

gradient of forage loss emanating from a high-density locust band. 

Coupled with field observation, remote sensing can be employed to identify 

soils, vegetation and land use characteristics, and from this initial information,


173 

potential and active outbreak areas can be identified. The objective is to discriminate 

vegetation areas from bare soil and to monitor the changes in vegetation densities 

and qualities over time. This is achieved using specific indices, such as the 

Normalized Difference Vegetation Index (NDVI) (Tucker, Hielkema, & Roffey, 

1985). The methodology is well developed in Africa. An application of this method 

allowed identification of potential habitats of the Desert locust from remotely sensed 

data (Tappan, Moore, & Knausenberger, 1991; Cherlet & Di Gregorio, 1993) and to 

create corresponding habitat maps (Voss & Dreiser, 1997). 

3.1. Desert Locust Biology and Habitat Requirements 

The invasion area of the Desert locust (Schistocerca gregaria) occupies 29 million 

km 2 in Africa, S. Europe and SW Asia. During recessions, when population 

densities are low, the Desert locust inhabits arid and semi-arid lands covering 16 

million km 2 from the Atlantic Ocean to NW India (COPR, 1982). Breeding occurs 

in the areas with 20–25 mm direct rainfall. Preferred oviposition sites are in sandy 

soils with a mosaic of grasses, herbs and shrubs. Although rain over the area is 

largely erratic, it tends to fall seasonally. Consequently locust breeding also takes 

place seasonally in different geographic locations (Fig. 1). The summer breeding 

zones include the Sahel, West Africa, Sudan, Eritrea, Ethiopia, and the India- 

Pakistan border. The winter/spring breeding zones include NW Africa, Iran, 

Pakistan, the Red Sea and the Gulf of Aden coasts, and the interior of Saudi Arabia 

and Yemen (FAO, 2001). 

Figure 1. Desert locust seasonal breeding zones and population movements 

between them (modified from FAO, 2001). 

Such complicated spatio-temporal pattern and an extremely large scale of the 

Desert locust population dynamics make its survey and forecasting extremely 

difficult. Furthermore, the pest’s breeding areas are often concentrated in very 

remote zones with low resident population or in the zones of the ongoing/imminent

174 


military conflicts such as Darfur, Ethiopia-Eritrea or India-Pakistan borders. Ground 

survey in such zones is difficult or impossible. The international cooperation 

between bordering countries is crucial, but it is not always in place for the efficient 

survey of the invasion area of the Desert locust which covers 65 countries. 

3.1.1. Habitat Mapping and Post-damage Assessment 

Pedgley (1974) was the first to apply satellite data to the Desert locust habitat 

monitoring. Tucker et al. (1985) recognized the potential of the remotely sensed data 

for the locust survey and forecasting. Hielkema (1981), Hielkema, Roffey, and 

Tucker, (1986) and Ghaout (1990) used Landsat imagery to map vegetation in the 

critical locust’s gregarization areas in West Africa. Louveaux, Ghaout, and Gillon 

(1990) studied the functioning of the winter breeding area of the Desert locust in 

Mauritania using, among other techniques, the Landsat data. Successful 

implementation of a preventive Desert locust control strategy requires early and 

reliable knowledge of areas where vegetation emerges after rainfall, providing 

suitable conditions for oviposition, egg hatching and hopper development. Cherlet 

and Di Gregorio (1993) tested the reliability of the NOAA AVHRR satellite data for 

these purposes. They attempted to calibrate different NOAA vegetation indices 

including NDVI, using extensive ground-collected field data from Niger. Their 

proposed calibration included two steps: (1) masking out the areas with no 

ecological potential for locust breeding; (2) correction of the vegetation index with a 

factor derived from the soil brightness. This methodology allowed the authors to 

detect some changes in the low cover vegetation. However, the lack of the 

background historical database on both, the vegetation and the locusts in certain key 

Desert locust breeding areas remains a major obstacle precluding the introduction of 

the remote sensing tools into the survey practice. 

Mapping of the Desert locust habitats using satellite imagery was done by the 

group of the late Prof. Dr. F. Voss in the 1990s. Dreiser (1994) used the Landsat 

Thematic Mapper data to produce the locust habitat maps for certain areas of Sudan, 

Mali and Mauritania at the scale of 1:200,000. Voss and Dreiser (1994) used the 

NDVI to detect the vegetated areas and then classified them with the maximum 

likelihood technique. The reliability of the resulting maps depended largely on the 

extensive ground observations and experience of the renowned locust expert Popov 

(1997) who participated in these studies. Such expertise is often unavailable in other 

Desert locust breeding areas which hinders the verification of the maps derived from 

satellite images. The authors concluded that the Landsat data were useful to assess 

the potential suitability of the Desert locust habitats. However, the actual habitats 

could be identified using higher temporal resolution imagery like NOAA AVHRR in 

combination with actual meteorological data from Meteosat and other similar 

satellites, which involve higher acquisition and processing costs (Voss & Dreiser, 

1997). Despland, Rosenberg and Simpson (2004) used the vegetation indices 

derived from NOAA AVHRR data to connect the Desert locust gregarization and 

band formation areas in Mauritania and Sudan to landscape structure. The authors 

concluded that the spatial resolution was insufficient to detect the initial


175 

gregarization zones. Similarly, Babah Ebbe (2008) was not able to distinguish the 

vegetation from bare soil in Mauritania using the NDVI derived from the Landsat 

TM data. The author concluded that the very low vegetation density in the Saharan 

and Sub-Saharan zones does not allow for a reliable Desert locust habitat inventory 

using the Landsat tools. These findings are in line with those of the Desert Locust 

Information Service (DLIS) of the FAO UN which uses satellite data for forecasting 

locust outbreaks (http://www.fao.org/ag/locusts/en/activ/DLIS/satel/index.html). 

Until recently, DLIS relied on 1 km resolution SPOT-VGT imagery to monitor 

ecological conditions in a locust breeding areas. Although the sensor was 

specifically designed for vegetation monitoring, it has become clear that it is 

difficult to detect the sparse vegetation in the desert – vegetation that appears to be 

dry to the satellite yet, sufficiently green for Desert locust survival and breeding, 

resulting in under-prediction of the pest threat. Consequently, DLIS turned to higher 

resolution imagery, that of 250 m resolution MODIS, consisting of 16-day 

cumulative images. Analysis of individual channels provides an even more accurate 

estimation of ecological conditions in Desert locust habitats which are subsequently 

verified with survey results. 

Besides the vegetation, rainfall is another essential parameter necessary for 

accurate Desert locust forecast and risk assessment. DLIS uses rainfall estimates 

derived from METEOSAT, mainly infrared and visible channels, to understand 

better the spatial and quantitative distribution of rainfall in the Desert locust 

breeding areas. Although images are available every 15 min and estimates every 

three hrs, DLIS uses daily 24-h cumulative estimates as well as decadal estimates of 

rainfall processed by Columbia University's International Research Institute for 

Climate and Society (IRI). DLIS combines satellite-derived estimates with those that 

originate from meteorological models. Whenever possible, these are verified with 

ground data. 

DLIS collaborates with a variety of universities and other partner institutes such 

as the IRI, the Italian Institute of Biometeorology (IBIMET), the European 

Commission Joint Research Centre (JRC), NASA's World Wind Project, and the 

Catholic University of Louvain (Belgium) in improving the application of remote 

sensing imagery for Desert locust monitoring and forecasting. SPOT-VGT and 

MODIS imagery is made available every 10 and 16 days respectively to locustaffected 

countries. These products are used to help guide national survey teams to 

potential areas of green vegetation where Desert locust may be present. 

Active remote sensing in the form of Vertically Looking RADAR (VLR) was 

used to observe the Desert locust flights over the Sahara as early as in 1968 (Roffey, 

1969). This technique provided novel measurements of aerial density, orientation, 

direction and speed of flight of solitarious locusts (Schaefer, 1969, 1976). Despite its 

very promising first results, the use of the RADAR devices for monitoring of the 

locust swarm migrations was considered impractical, mostly because of the timeconsuming 

nature of the data analysis (Reynolds, 1988; Riley, 1989). Subsequent 

attempts to use VLR showed its potential to distinguish between the flying Desert 

locusts and other insects (Smith, Riley, & Gregory, 1993). The obtained data could 

be a useful complement for the routine locust surveys (Riley & Reynolds, 1997; 

Chapman, Reynolds, & Smith, 2003).

176 


Finally, it is necessary to point out that currently available satellites are not able 

to directly detect individual locusts or locust swarms and hopper bands. An attempt 

of Kibasa (2006) to detect the actual locust groups with the high-resolution Spot 5 

data failed, confirming that it was not possible to distinguish the insects from the 

background soil. 

With regard to the GIS applications, the analyses of the enormous amount of 

geospatial information collected by both, the satellites and field surveys from the 

vast geographic area of the Desert locust would be impossible without appropriate 

GIS tools (Hielkema & Snijders, 1994). The GIS SWARMS which was developed 

by the FAO in collaboration with Natural Resources Institute and the University of 

Edinburgh (UK) specifically for these purposes contains a number of databases 

including historical locust data for nearly 100 years, weather data, and background 

information such as soils and topography (Healey et al., 1996). SWARMS has been 

used operationally for locust early warning since 1996; it is being constantly revised 

and updated. 

One of the major hurdles in effective Desert locust forecasting is the collection 

and recording of data in the field and their subsequent transmission to a national 

locust center in near-real time. FAO DLIS developed, in collaboration with 

Novacom (France), a handheld device named eLocust2 for field locust officers 

(http://www.fao.org/ag/locusts/en/activ/DLIS/earlywarning/index.html) to enter and 

send geo-referenced data in real time. The field officer enters and saves the data into 

a rugged handheld device which automatically determines the coordinates of the 

location of the survey or control operation using GPS technology. With a press of a 

button, the officer sends these data via satellite to the national locust center where 

they are received as an email attachment, downloaded, decoded and imported into a 

GIS. This GIS named RAMSES is used for the management and analysis of field 

results and of locust and environment data at a national level. eLocust2 data from 

the field are automatically imported into RAMSES and then are exported to FAO 

DLIS for further analysis, forecasting and early warning. 

Furthermore, FAO DLIS utilizes several specialized tools to supplement its 

analysis and forecasts (Ceccato, Cressman, Giannini, & Trzaska, 2007). A 

Trajectory Model (developed by Meteo Consult) estimates the source and 

destination of swarm migrations forward and backward in time. Rainfall estimates 

and MODIS satellite imagery provided by IRI at Columbia University (New York, 

USA) are used to try to understand where it has rain and where vegetation is green 

in the desert. Seasonal predictions of temperature and rainfall 6 months in advance 

are analyzed. Another model is used that estimates the developmental times of 

locust eggs and hoppers. The use of these tools in combination with the GIS allows 

the best possible analysis from which forecasts and early warning can be issued. 

Another tool potentially useful for locust forecasting is geostatistics. 

Woldewahid (2003) used geostatistics to predict the Desert locust densities at distant 

locations in the Red Sea coastal plains of Sudan, by spatial interpolation through 

kriging. He found a strong relationship between the Desert locust densities and the 

millet croplands despite the fact that these croplands occupied only a limited 

proportion of the study area (5%).


177 

3.2. Migratory Locust Biology and Habitat Requirements 

Migratory locust Locusta migratoria has the largest distribution area among all 

grasshoppers and locusts covering almost entirely the temperate and tropical zones 

of the eastern hemisphere (Fig. 2). Yet the ecological requirements of the species are 

rather narrow. Within this vast range the locust breeding areas are restricted to 

grasslands on light soils, often in the wetlands with reed stands along rivers or lakes. 

There are about 10 subspecies or geographic races of the Migratory locust slightly 

differing biologically and morphologically (COPR, 1982). The tropical races 

develop continuously without diapause, while the temperate ones are univoltine. 


To date, remote sensing tools were applied to habitat mapping and damage 

assessment for two subspecies, L. m. migratoria in Central Asia and L. m. 

manilensis in China. In Kazakhstan and Uzbekistan, remotely sensed data collected 

from satellite platforms were used for mapping potential habitats of the Asian 

Migratory locust L. m. migratoria (AML). Throughout Central Asia, the AML 

spends most of its life cycle in common reed (Phragmites australis) stands, usually, 

in river deltas. 

Figure 2. Distribution area of the subspecies of the Migratory locust Locusta 

migratoria (modified from COPR, 1982 by Latchininsky et al., 2002). Locusta 

migratoria migratoria and other northern subspecies___; L. m. cinerescens - - - ; L. m. 

burmana •••••; Indian subspecies …-; L. m. migratorioides - . - . L. m. capito …+…; 

Arabian subspecies ++++; L. m. manilensis ….; Australian subspecies -+-+-. 

To identify the AML habitats, one approach is to map the reed distribution 

annually or at specific times of the year coinciding with AML developmental stages 

(e.g., hatching of eggs or oviposition). Sivanpillai, Latchininsky, Driese, and

178 


Kambulin (2006), and Sivanpillai and Latchininsky (2007) demonstrated the utility 

of information derived from Landsat and MODIS satellites to estimate reed 

distribution in the River Ili (Kazakhstan) and Amudarya River (Uzbekistan) deltas 

respectively. Results from these studies showed that satellite data could accurately 

map the reed stands when they are dominant (>80% classification accuracy). 

However, satellite data had relatively lower accuracy in detecting reeds growing 

together with other vegetation like shrubs and sedges (Latchininsky, Sivanpillai, 

Driese, & Wilps, 2007; Sivanpillai & Latchininsky 2008). Navratil (2007) used the 

higher resolution multispectral data collected by the SPOT satellite (Table 2) to map 

the reed distribution for a portion of the Amudarya River delta. Landsat Thematic 

Mapper 5 data could be used for mapping emerging reeds in the spring 

(Latchininsky et al., 2007). This time period coincides with the hatching of AML 

eggs and the satellite-derived information could be used for directing the ground 

survey towards potential nymphal habitats. Distribution of reeds coinciding with the 

locust oviposition (late summer) was mapped by Sivanpillai and Latchininsky 

(2008). Such information could be used for locating locust egg-beds. Satellitederived 

information could assist the government pest management agencies to 

devise treatment plans. Since satellites collect data on a regular basis, reed 

distribution maps can be updated periodically, providing basis for targeted locust 

surveys and treatments. 

Satellite data acquired prior and after an outbreak have been used for quantifying 

damages to vegetation. Ji, Xie, Li, Li, and Zhang (2004) used the pre- and postdamage 

MODIS images for assessing the damages caused by the Oriental Migratory 

locust L. m. manilensis in China’s Hebei Province. Using the NDVI values derived 

from these images, the researchers were able to identify the affected areas. The extent 

of vegetation damage was grouped into light, moderate, and heavy damage categories. 

Although MODIS images have relatively coarse spatial resolution (250 m), it was 

possible to identify 89% of the impacted areas. The authors concluded that satellitederived 

information could be more efficient than the traditional ground surveys. 

Zha, Gao, Ni, and Shen (2005) assessed the utility of MODIS data acquired over 

the growing season for monitoring Oriental Migratory locust outbreak in China. 

Tian, Ji, Xie, Li, and Li (2008) repeated the work conducted by Ji et al. (2004) using 

Landsat ETM+ data and reported higher classification accuracies compared to 

MODIS data. Ma et al. (2005) used Landsat ETM+ data to assess damage to 

vegetation caused by L. m. manilensis in China’s Dagang region. The ground-based 

locust monitoring stations established in the 1950s were unable to survey the 

expanded infested areas. Using the Leaf Area Index values derived from pre- and 

post-damage images, the authors demonstrated the value of satellite data for routine 

monitoring of vegetation condition. Tian et al. (2008) repeated the pre- and postdamage 

assessment work conducted by Ji et al. (2004) but using Landsat ETM+ 

data, and reported a very high accuracy of 98% for determining the geographic 

extent of the locust damage. However, the accuracy was slightly lower (92%) when 

they attempted to categorize the severity of the locust damage from Landsat images. 

Using soil moisture indices derived from MODIS data, Liu et al. (2008) 

demonstrated significant differences in soil moistures during severe (2001–2002)


179 

and moderate (2003–2004) outbreak years in 3 regions prone to Oriental Migratory 

locust outbreak in China. 

Applications that used satellite data for mapping Migratory locust habitats, 

assessing risks of infestation and evaluating vegetation damage were comparatively 

fewer than the number of applications that focused on Desert locust (Section 3.1) or 

the Australian Plague locust (Section 3.3). 

3.3. Australian Plague Locust 

Australian Plague locust Chortoicetes terminifera occurs throughout Australia (Fig. 

3). Its ideal habitats consist of a mosaic of bare ground for basking and egg-laying, 

short grass cover for feeding and taller sparse tussocks for night shelter (COPR, 

1982). The locust can produce three annual generations under favorable weather 

conditions, primarily sufficient moisture. Hoppers form dense bands which move 

several 100 m per day. Plagues originate from several recession areas in SW 

Queensland, Central New South Wales, and NW Victoria where locusts are always 

present. Usually the onset of the plague is triggered by abnormally heavy rains from 

late November to January in the recession areas of the Australian dry interior. 

From these outbreak centers the huge swarms of adults migrate into agricultural 

zones covering distances of several 100 km. Rangeland forage is the preferred food 

for the Australian Plague locust. Migrating swarms, however, inflict severe damage 

to cereal crops, vineyards, orchards and vegetable gardens. 


Breeding zones of the Australian Plague locust situated in remote and semi-desert 

locations, the Australian entomologists were among the first to use remotely sensed 

data for locust habitat mapping. One of the earlier attempts to relate information 

derived from Landsat data with locust data was conducted by McCulloch and Hunter 

(1983). This study demonstrated that locust presence was confined to the following 

three map classes: stony downs, stony plains and high-level flood plains. Further 

development of the remote sensing tools was done by Bryceson (1984): he was able 

to detect even small area of vegetative growth after rains with Landsat data. 

Bryceson and Wright (1986) used several Landsat images modelled the origin and 

spread of the 1984 Australian Plague locust outbreak. In this study they concluded 

that it was feasible to use satellite data to monitor changes in vegetation condition 

which could then be associated with locust breeding areas. 

In yet another study, Bryceson (1989) used Landsat MSS data to track the eggbed 

areas of the Australian Plague locust in New South Wales. Furthermore, the 

author showed that satellite data were instrumental in identifying the source areas 

from which the locust plagues developed (Bryceson, 1990, 1991).

180 


Figure 3. Australian Plague locust habitat (shown as shaded areas) map (Courtesy: Dr. 

Hunter and Mr. Deveson, Australian Plague Locust Commission, Canberra, Australia). 

In Australia, locust monitoring and control are executed by a federal agency, the 

Australian Plague Locust Commission (APLC), specifically created for these 

purposes. This facilitated the introduction of the meteorological remotely sensed 

data into the practice of locust forecasting (Bryceson & Cannon, 1990; Bryceson, 

1993; Bryceson, Hunter, & Hamilton, 1993; Hamilton & Bryceson, 1993). Multiple 

information sources, including remotely sensed vegetation and weather data as well 

as locust infestation data, were integrated into a decision support system developed 

at APLC (McCulloch, Bie, & Spurgin, 1994; Deveson & Hunter, 2000, 2002; 

Deveson, 2001). 

Locust swarm migrations were tracked in Australia by active remote sensing in 

the form of vertically-looking RADAR (Drake, Harman, & Hunter, 1998; Drake 

et al., 2001; Deveson, Drake, Hunter, Walker, & Wang, 2005). The methodology


181 

proved useful. However, high costs of the installation and maintenance of the 

RADAR stations precluded it from practical use. 

Hunter, McCulloch, and Spurgin (2008) demonstrated the possibility of detecting 

the locust nymphal bands from a low-flying aircraft, as a useful survey option. 

Australia remains an international leader in the operational use of remote sensing 

and GIS applications in locust management. 

3.4. Other Locusts 

About a dozen other locust species exist in addition to those described in earlier 

sections and their distribution ranges often cover vast, sparsely populated and 

remote areas. These locust species can cause economic and environmental impact 

similar to any of the locusts discussed above. For example, the Moroccan locust 

(Dociostaurus maroccanus) habitats extend over 10,000 km across N. Africa, 

Middle East and Central Asia. Moroccan locusts can destroy valuable agricultural 

crops and adversely impact the livelihood of farmers in these regions. Chemical 

treatments can be effective only if they are coordinated by all impacted countries. 

Similarly, the Central American locust (Schistocerca piceifrons piceifrons) poses a 

threat to agricultural operations in Mexico and neighboring countries. Other locusts 

affect South Africa, South America and Southeast Asia. National Plant Protection 

Agencies in these regions spend considerable amount of resources for monitoring 

and managing the locust populations every year. 

Applications of the remote sensing and GIS technologies for monitoring and 

management of the locust species other than the Desert, the Migratory and the 

Australian plague locusts are very scarce. To our knowledge, such studies were done 

for only two other locusts. Franc (2007) used high resolution SPOT satellite data to 

trace habitats of the Red locust Nomadacris septemfasciata in Madagascar. 

Comparing two SPOT images, one dated 1986 and the other dated 2004, he 

calculated the areas of deforested zones which served as migration pathways for this 

locust in the basin of the River Sofia. The accuracy of the image classification (77%; 

Kappa = 0.75) was verified through ground surveys. In 1986, the combined area of 

such “corridors” was 41,677 ha but as a result of intensive deforestation it increased 

to 67,607 ha by 2004. The newly cleared areas provided new migration pathways for 

the Red locust which produced spectacular outbreaks in the early 2000s for the first 

time ever in Madagascar. 

Sivanpillai, Latchininsky, Peveling, and Pankov (2009) used the Indian Remote 

Sensing (IRS) P6 Satellite –Advanced Wide Field Sensor (AWiFS) data to map the 

Italian locust Calliptamus italicus habitats in a very heterogenic landscape of NE 

Kazakhstan, consisting of active and fallow croplands, shrub lands, grasslands and 

riparian zones. This locust species inhabits primarily abandoned agricultural fields 

(fallows) covered with sagebrush (Artemisia spp.) and other broadleaved weeds. 

Despite its relatively coarse spatial (56 m) and spectral (4 bands) resolutions, the 

AWiFS data were sufficient to identify most landscape features.

182 


CONCLUSIONS 

The idea of using remotely sensed data to identify locust habitats became plausible 

with the introduction of non-military satellites in the 1970s. Distribution ranges of 

many locust species cover vast, sparsely populated and remote areas, and the 

satellite data appeared to be tailor-made to address the spatio-temporal extent of the 

locust habitats. However, in the last two decades of the twentieth century, the 

practical use of the satellite data was impeded by inadequate computational 

hardware capacities and lack of specialized training for locust specialists in remote 

sensing data acquisition and processing. Hence, after a period of over-enthusiastic 

claims and views of the remote sensing as a panacea for solving locust problems, the 

research reports in the beginning of the 2000s sounded more cautious, if not 

skeptical (Despland et al., 2004; Tratalos & Cheke, 2006). In the present chapter we 

attempted to summarize the most important achievements and drawbacks of the 

applications of the remote sensing and GIS technologies to locust monitoring and 

risk assessment. Out of about a dozen locust species worldwide, this technology has 

been developed for only three species, the Desert, the Migratory, and the Australian 

Plague locusts. Numerous advances have been made in the use of satellite remote 

sensing data for monitoring the Desert locust habitats in Africa. Similarly, the 

habitats of the Australian Plague locust are being monitored through satellites, aerial 

photographs and RADAR imaging (active remote sensing) technologies. Satellite 

data from different platforms were used for habitat monitoring and crop loss 

assessment for the Migratory locust in Asia. For two other species, the Red and the 

Italian locusts, only pilot studies were done in this domain. 

The use of remotely-sensed information including the data from meteorological 

satellites became a routine part of the forecasting done by the FAO UN Desert locust 

Information Service (DLIS). Yet the efficacy of the forecasts is challenged by the 

vast geographic extent of the monitored territory of the Desert locust recession area 

(16 million km 2 ) and, consequently, by the huge amount of information to be 

collected and processed in near-real time (Van Huis, Cressman, & Magor, 2007). 

Habitats of the Migratory locusts, which are confined to reeds around water 

bodies, can be identified even with satellite platforms of relatively coarse spatial 

resolution (e.g. MODIS). Continuous reed stands are easily distinguishable 

spectrally from other land cover classes except when the reeds are mixed with 

shrubs of other vegetation. For such cases a higher temporal resolution of satellites 

with a shorter revisiting time is instrumental in following the phenological changes 

in the vegetation throughout the growing season. 

The Australian Plague locust management is implemented by the governmental 

entity, the APLC, which uses satellite and GIS technologies for locust monitoring 

and forecasting across a vast area of inner Australia. This country was one of the 

pioneers in practical introduction of the remote sensing as well as other technologies 

such as RADAR and aerial photography in locust population management. 

Applications of remote sensing and GIS technologies for mapping and 

monitoring the habitats of most other locusts throughout the world lag behind. Some 

of these habitats are situated in active agricultural areas of countries such as 

Kazakhstan, Uzbekistan and Mexico. Locust pest outbreaks in these areas adversely


183 

impact the economy and environment. Governments of these countries either 

independently or jointly (with their neighbors) are engaged in periodic monitoring 

and treatments to control locust populations and prevent them from damaging 

agricultural crops. Recently, efforts are underway to form a group of Central Asian 

and Caucasian countries to coordinate the locust population monitoring and control 

activities. 

Future locust habitat monitoring and surveying activities should incorporate 

remote sensing and GIS technologies for optimizing the resources available in these 

countries. Future work should also focus on testing the utility of remotely sensed 

data for mapping and monitoring the habitat of locust species that are yet to be 

studied. It is also encouraging that both the number of remote sensing satellites and 

the countries that launch them have increased since early 1970s. In addition to 

government agencies several private companies have also launched remote sensing 

satellites that are collecting data for different parts of the world. With this increased 

availability of remotely sensed data (Table 2), users have a wide range of choice in 

terms of spatial, spectral and temporal resolutions while selecting imagery for a 

particular application. For example, images can be acquired more frequently by 

obtaining data from different remote sensing satellites with complementary spatial 

and spectral resolutions (Section 2) providing the required information about locust 

habitat. Plant protection agencies and international organizations must capitalize on 

these developments in terms of increased data availability. 

With more and more remotely sensed data distributed via the internet the time 

associated with obtaining the data has reduced tremendously. Previously data were 

mailed in tapes and discs and it could take several weeks thus reducing its 

usefulness. It is also important to note that not all countries or regions have access to 

high-speed internet. However, most remote sensing data can be downloaded directly 

from the satellites to ground receiving stations and processed in any country or 

region, thus avoiding the need to transfer large volumes of data through internet. 

Such activities require collaboration among international agencies (i.e., FAO), 

impacted countries, and satellite data vendors and agencies. 

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8 

PLANT DEFENSES AGAINST INSECT HERBIVORY 

FARHA-REHMAN 1 , FAREED A. KHAN 1 , SHOEBA B. ANIS 2 

AND S. M. A. BADRUDDIN 2 

1 Department of Botany, Aligarh Muslim University, 

Aligarh-202002, UP, India 

2 Department of Zoology, Aligarh Muslim University, 

Aligarh-202002, UP, India 

Abstract. Herbivory, the act of consumption of plant biomass by specialist animals, regulates the cycling 

of biotic and abiotic ecosystem components, through a complex process transferring materials among 

various trophic levels. Herbivores include insects and mammals of varying sizes, the former being most 

important due to their high diversity. Insects consume the biomass in varying proportions, depending on 

their size and density. Apparent checks and balances between prey and predators or hosts and parasites 

are chemically governed functions. Plants and herbivores receive and send signals to each other as well as 

to organisms in higher trophic levels (predators) through volatile chemicals. Besides several 

morphological defence mechanisms, plants evolved specific chemical defences against insects. Among 

herbivores, insects also co-evolved mechanisms to overcome the volatile chemical arsenals of plants. In 

this review the role of plant defense against insect herbivory is discussed. The plant responses to repel 

insects and the synthesis of volatile chemicals to attract predatory insects or parasites are reviewed. Plants 

evolved genes (activated on insect attack) inducing the secretion of volatile chemicals. Such signalling 

attracts predators or parasites and is absent in plants when they are experimentally injured. Signalling is 

caused by the reaction with elicitors contained in the oral secretions of herbivorous insect. Through 

chemically operated keys, plants and insects regulate ecosystem functioning, allowing co-existence in 

wild and natural ecosystems. 


Agriculture is one of the major sectors of the Indian economy, since about 70% of 

human population is dependent on it for livelihood, other than food. The agriculture 

sector contributes over 40% of the gross national production, but food production 

has always remained a matter of great concern. During the past few months, the 

inadequate grain production has added to the global concern. Among other threats to 

crop productions, herbivorous insects and pests pose a very serious threat to plants 

in India, as well as all over the world. 

Herbivory, the feeding on living plants by animals or insects, is a key ecosystem 

process whose widely recognized effects on primary production, vegetation structure 

189 




190 

FARHA-REHMAN ET AL. 

and composition depend on the type and intensity of feeding. Different types of 

herbivory affect several plant tissues, besides affecting primary production, 

translocation and accumulation of photosynthates to varying degrees. Herbivory 

affects a variety of ecosystem properties, primarily through differential changes in 

survival, productivity and growth of plant species. 

In evolutionary terms, the rise of insects represented a major selective force on 

plants evolution, and led to the selection of plants by their ability to generate 

defensive adaptations. Insect herbivores are mostly mandibulated that either bite or 

chew vegetation. The rise of vascular plants led to the co-evolution of sap-sucking 

feeders, and several other forms of herbivores such as leaf mining, gall forming and 

nectar feeding insects. The study of plant defense against insect herbivory is not 

only important from an evolutionary point of view, but is also useful in 

understanding the extent of its impact on agriculture, human and livestock food 

sources, as well as on the utility and survival of commodity plants or species of 

medicinal use. As an example of insects damage due to high rates of herbivory, 

grasshoppers feed on a wide range of plants and organic material, and voraciously 

consume green forage approximately one-half of their body weight, every day. 

In the present review emphasis is given to herbivory and plant defense 

mechanisms, as well as to the chemical signalling among plants, herbivorous and 

predatory insects. In fact, it is worth to determine these mechanisms before either 

using pesticides or employing other biotechnological means, i.e. genetically 

manipulated (GM) plants. It is known that the use of pesticides may indeed alter 

some ecosystem processes or introduce a structural change in density dependent or 

population regulation mechanisms, apart from the effects related to health hazard 

implications and costs. Finally, GM plants have several environmental and 

ecological complications, including the developement of insect resistance in a way 

similar to resistance to some insecticides. Insect management is in effect a complex 

and difficult task, as suggested by the insects and plants co-evolution and survival 

for the past 97 million years (Labandeira, Dilcher, Davis, & Wagner, 1994). 

2. PLANT DEFENSE MECHANISMS 

Plants curb insect herbivory by synthesizing and releasing complex blends of 

volatiles. Some of these compounds provide important host-location cues to predator 

insects or parasites, that are natural enemies of insect herbivores. Synthesis and 

release of these chemical signals by attacked plants are active physiological 

processes, triggered by chemical elicitors or substances contained in the oral 

secretion of attacking herbivores. Certain chemicals contained in the saliva of 

grazing insect (herbivores) activate the synthesis and release of plant volatiles. The 

process of attracting predatory insects involves the interaction of specific blends of 

plant volatiles, with highly sensitive receptor molecules of the predators (De 

Moraes, Mescher, & Tumlinson, 2001). 

Plant volatiles represent a language through which attacked plants send signals 

to healthy plants in their vicinity and also invite predators or parasites of their 

herbivores. This adaptation is genetically fixed and controlled by a set of genes 

present in plants. In particular, a set of five defense genes are induced when a plant

HERBIVORY & PLANT DEFENSE 

191 

is exposed to volatiles proceeding from neraby co-specific leaves infested with 

insects. All these genes were not induced in healthy plants when exposed to the 

blend of volatiles from artificially wounded leaves. At least three terpenoids in the 

infested leaves were responsible for the gene activation process, leading to the 

release of special blends of volatiles (Arimura et al., 2000). 

Volicitin, N-(17-hydroxylinolenoyl)-L-glutamine and β-glucosidase are elicitors 

of plant volatiles and are released only on insect chewing. Volacitin is a component 

of the oral secretion of beet worm caterpillars, which induce corn seedlings to 

synthesize and release volatile chemical signals. β-glucosidase is present in the 

regurgitant of Pieris brassicae caterpillar (Mattiacci, Dicke, & Posthumus, 1995). 

Generally, plant defenses can be categorized into two groups, such as constitutive 

and induced defenses. Constitutive defenses are always present in plants, while 

induced defenses are synthesized at or mobilized to the site of attack, when a plant is 

injured. Constitutive defenses range from mechanical defenses to the accumulation of 

digestibility reducers and toxins. Induced defenses include secondary metabolic 

products and may induce morphological and/or physiological changes. Both these 

defenses (inducible and constitutive) are known to increase the defensive ability and 

effectiveness of attacked plants, against a wide range of insect herbivores. 

Wounding by herbivores activates the systemic expression of defense genes 

through the octadecanoid signal pathway. The insect saliva, containing chemical 

elicitors such as volicitin, also triggers the attacked plant to release a bouquet of 

volatile compounds which attract parasitic or predatory insects to check the 

attacking herbivore. Volicitin stimulates release of volatiles through the 

octadecanoid pathway and thereby raises the possibility of cross talk between this 

molecule and the wound-induced expression of defense genes (Farmer, 1997). 

In controlled trials, corn seedlings and cotton plants damaged by caterpillars 

were observed to release volatiles attracting parasitic wasps, laying their eggs in the 

caterpillar’s body (Turlings, Tumlinson, & Lewis, 1990). The hatching eggs 

produced wasp larvae feeding on the host, which eventually killed the caterpillar. 

Over 15 plant species, 10 herbivore and 10 predatory insect species were observed 

to form a stable, tri-trophic food web (Takabayashi & Dicke, 1996). 

Another example of chemical signalling is given by nocturnal moths which lay 

their eggs on healthy plants, on which newly hatched larvae feed during day light. 

The plants attacked by the larvae were found to attract parasitic insects. In particular, 

De Moraes et al. (2001) reported that tobacco (Nicotiana tabacum) plants under 

attack from caterpillars produced two different blends of volatiles during night or 

day periods. The night time blends of volatiles were small, unsaturated derivatives 

of fatty acids and discouraged pregnant nocturnal herbivore moths (Heliothis 

virscens) for laying eggs. Night time herbivory food chain was thus discouraged, to 

avoid further plant damage (De Moraes et al., 2001). At the same time, repelling the 

night time pregnant moths by a specific blend of volatiles also reduced caterpillars 

competition with other day time herbivorous insects and also the attacks on their 

larvae by the predators already invited by diurnal caterpillars. It is important to note 

that the hatching larvae of nocturnal moths feed during the day time. However, it is 

not clear whether the night time blends of volatiles are specifically produced or if

192 


they are by-products of diurnal volatiles (De Moraes et al., 2001). The dual function 

of volatiles released on herbivores attack is believed to have evolved 

simultaneously. The release of night time blends of volatiles of tobacco plant are 

also constituents of the set of volatiles released during attacks from diurnal insects, 

and defended tobacco plants from both diurnal and nocturnal herbivore caterpillars 

(De Moraes et al., 2001). 

If the full range of volatile signals used by plant to communicate with each 

other and with insects could be exploited, and its relevance in ecology also 

understood (including the identification of genes responsible for volatiles synthesis), 

plants could then be activated to emit specific blends of defensive volatiles at an 

appropriate day and night time, well before insects attack. The synthesis of these 

volatiles even in traces would then contribute to minimize the use of environment 

detrimental pesticides (Ryan, 2001). 

3. INSECT DIVERSITY AND CROP DAMAGE 

In spite of the fact that a large number of insect species are yet to be described and 

reported, about 1.7 ⋅ 10 6 species of insects are already known, representing 56% of 

all members in the whole animal kingdom. According to another estimate, insects 

account for 64% of the whole animal biodiversity. Insects are known to have 

evolved several adaptation mechanisms making them one of the best fitting group in 

almost all climate and environment conditions (Atwal & Dhaliwal, 2003). The small 

body size, strong exoskeleton, high mobility through flight, efficient water 

conservation mechanism, rapid reproduction and resistance allowed their adaptation 

to diverse climates, and the maintenance of their own biodiversity. Honey bees, silk 

worm, Lac insect (pigment producers) and pollinators are also economically 

important species, as also the predators and parasites of herbivorous species. Their 

life cycle may be small, covering one season only, or last longer, for more seasons. 

There are varying reports concerning crop losses due to insect pests attacks. The 

losses caused by pests, diseases and weeds on a global scale are considered to vary 

between 35 and 37% (Atwal & Dhaliwal, 2003; Haq, Atif, & Khan, 2004; Brewer, 

2001). Crop losses due to various pest categories are very high in both developed 

and developing countries. In North America, Europe and Japan, estimates of crop 

losses are 10–30% (Atwal & Dhaliwal, 2003). However, crop losses due to pests are 

very high in developing regions. In India, estimated crop losses due to insect 

herbivores until a few decades ago were 18% for cotton, 10% for rice, 5% for 

oilseed and 5% for pulse crops (Atwal & Dhaliwal, 2003). Older (>50 years) 

estimates of crop losses due to insects ranged around 13%, whereas other pathogen 

losses averaged 12%. Arthropod pests, with more than 9,000 species including 

insects and mites, contributed towards major losses to agriculture crops, not only by 

direct damages, but also acting as vectors and transmitting various plant diseases 

(Griswold, 1953). Among all grazers, insect herbivores account today for a 50% of 

total biomass consumption. Among all herbivores, insects are far most significant 

grazers as they co-evolved feeding strategies besides the deploy of plants 

defence mechanisms (Ehrlich & Ehrlich, 1970).


193 

According to a recent report, insects may consume about 10–20% of a crop 

(Ferry, Edwards, Gatehouse, & Gatehouse, 2004). From previous global estimates, 

insect pests resulted in crop losses around $7 billion, while $3 billion annually were 

spent in the US on pest control efforts in the early sixties (Janick, Schery, Woods, & 

Ruttan, 1974). In India, Rangaswami (1983) estimated annual economic crop losses 

around Rs. 150 thousand million (≈ US$ 3191 million). Another estimate of total 

losses of field crops and food grain (pre and post harvest) caused by insects was 

around Rs. 336.6 billion (approx. US$ 7.17 billion) per year on a global scale (Atwal 

& Dhaliwal, 2003). Control of insect pests has hence a high potential in increasing 

crops production and farmers’ revenues, with a potential estimated increase of yields 

by 13.1–18.7 million tonnes per year. As an example, control of herbivory (flies and 

pod borers) may reduce total crop damage up to 30%, with an increase of sugarcane 

yield by 20% or of groundnut production by 15% (Atwal & Dhaliwal, 2003). 

The loss to leaf area caused by herbivores varies from 4.8 to 32.5% (Lowman & 

Box, 1983). Chemical changes in leaf composition are also produced by insect 

attacks. For example, the insect attack may result into accumulation of phenolics 

which may reduce in turn grazing intensity by other species (Lowman & Box, 1983). 

In red alder (Alnus rubra), plant memories to insect attacks, in terms of the 

durability of chemical or physical defense, also varied depending on the feeding 

insect species (Williams & Myers, 1984). 

Further estimates of plant damage due to herbivory may be derived by assays on 

annual crops or observations on perennial plants. The loss of maize (Zea mays) to 

herbivory by the grasshopper Choroedocus illustris follows a density dependent 

pattern. The damage intensity to the leaf area due to adult grasshoppers varied from 

1.64 to 3.55% as 10, 20 and 40 adults attacked, respectively, 32.5, 60.9 and 79% 

leaves of all plants (Farha-Rehman, 2008). Furthermore, in damaged maize leaves, 

the insect attack during 15 days led to a proportionate loss of leaf proteins and an 

increase in proline accumulation (Farha-Rehman, 2008). In the insect herbivory on 

the Australian woodland eucalypt (Eucalyptus blakelyi), Journet (1981) noted that 

herbivorous insects caused 40% annual foliage damage. The abscission of damaged 

foliage further enhanced the total annual foliage damage up to 70%. 

4.1. Insect Herbivores 

4. HERBIVORY 

Insects are the primary herbivores in many ecosystems and their size vary from the 

tiny aphids to very large species. They feed on a vast variety of plants, ranging from 

algae to angiosperms. The insect grazers form a complex system at the herbivory 

level in food webs. About 80% of plant material consumed by insects, and their 

secondary production, can equal or exceed the plant biomass consumed and rebuilt 

as secondary productivity by vertebrate grazers in grassland. 

During the evolution of life on earth, insects have been the most significant 

herbivores and co-evolved with land plants, since they are dependent on plants for 

food and shelter. The herbivores co-evolved mechanisms to obtain food from plants 

despite the set-up of a diverse range of plant defenses. Herbivore adaptations to

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plant defense have been attributed to the offensive traits linked with promoting 

increased feeding and use of a suitable host. 

Relationship between herbivores and their host plants often resulted in 

reciprocal evolutionary changes. For example, some herbivores co-evolved ways to 

hijack plant defenses by sequestering defensive chemicals and using the modified 

blend to protect themselves from predators. 

4.2. Plant Responses to Insect Herbivory 

A number of volatile chemicals produced by plants promote or reduce herbivory. 

The increase of nitrogen, stored as accumulated proline and valine residues, was 

observed to stimulate grasshopper herbivory during drought stress (Haglund, 1980). 

Experimental evidence suggested that grasshoppers detect and preferentially feed on 

grasses treated with the amino acid proline and valine, whose accumulation levels in 

plants commonly increase under drought. This adversity may lead to insect 

concentration on drought stressed plants (Haglund, 1980). 

Leaf toughness, total phenols and condensed tannins increased in the leaves of 

five tree species of Australian rain forest, because of insect grazing (Lowman & 

Box, 1983). In most of these trees leaf toughness and chemical toxicity increased 

with leaf aging, leading to a corresponding decrease in insect grazing. The herbivory 

caused leaf area losses between 4.8 and 32.5%, but losses were positively correlated 

with leaf toughness rather than phenolic contents. Lowman and Box (1983) inferred, 

from these findings, an interaction of factors including physical and chemical 

characteristics of leaves, with spatial and temporal factors that induced the variation 

in insect grazing intensities. 

Leaf structure and organization may also protect plants from herbivores, 

although with complex outcomes. As an example, the tiny hooked trichomes on 

leaves and stems of Mentzelia punila (Family Loasaceae) entrapped and killed not 

only herbivore aphids (Macrosiphum mentzeliae) but also incapacitated a coccinellid 

beetle (Hippodamia convergens) that preys upon the aphid enemy (Eisner, Eisner, & 

Hoebeke, 1998). 

Besides leaf age, the pattern of herbivory may vary with the plant species. 

Intraspecific variation in the pattern of herbivory on young and mature leaves of 

Trichilia cipo (Meliaceae) and Cecropia insignis (Moraceae), two tropical trees, was 

observed in a lowland rain forest in Panama. Mature leaves of Cecropia suffered a 

five fold greater damage than Trichilia, irrespective of the differences in life history, 

habitat, defensive characteristics and damage levels (Coley, 1983). 

4.3. Plant Reaction to Previous Herbivores 

The previous herbivore attack of Western tent caterpillar, Malacosoma californicum 

pluviale, on red alder was observed to improve food quality for fall webworm 

(Hyphantria cunea) larvae. Three hypothesis concerning the insect-plant interactions 

were tested by rearing fall webworm larvae in the laboratory on foliage collected 

from red alder trees, with different histories of western tent caterpillar herbivory.


195 

Fall webworm larvae grew relatively faster, with heavier pupil weight, when raised 

on foliage with previous history of herbivory (caused by moderate densities of 

western tent caterpillar during two previous summers) in comparison to those fed on 

foliage from unattacked trees. This finding did not fit the hypothesis that previous 

history of herbivory induced the production of plant defensive chemicals in red 

alders. Growth patterns of webworms were the same, either fed on foliage from 

unattacked trees adjacent to those attacked by fall webworm larvae or on the foliage 

of red alder trees, growing at a longer distance from attacked trees. This study 

showed, however, that continued insect attacks can deteriorate the food quality of 

attacked trees (Williams & Myers, 1984). 

Seed consuming larvae reduced seed production in turtlehead, Chelone obliqua. 

Seed production was also reduced due to severe herbivory by specialist folivores 

(Stamp, 1987). 

Plant defense signalling can also be induced by biotic attacks. In some 

interactions, defense was enhanced prior to attack by another organism, whereas in 

other species, signals were conflicting. Below ground attack may also influence 

responses to above ground attack and vice versa, due to systemic induction of 

defense metabolism pathways (Bruce & Pickett, 2007). 

4.4. Impact of Herbivory on Ecosystem 

In a study on the impact of insect herbivory on eight plant species (including 

perennial forbs and grasses), the size variability in plant populations influenced 

insect herbivory, which in turn affected the fitness of individuals under natural 

successions. The size variability was reduced with herbivores abundance. Insect 

herbivory reduced size and survival of plants as did competition, which directly 

affected the size and distribution of plants (Gange & Brown, 1989). 

Insect herbivory may also act as a plant population regulatory factor (Williams, 

1990). Herbivory limited the distribution of Eucalyptus pauciflora in sub-alpine 

forest in Australia which was replaced by E. dives due to increased herbivory 

preferences. The co-occurrence of E. dalrympheana with E. dives and E. pauciflora 

was maintained by a density-dependent stabilizing mechanism, caused by leaf 

parasites. The leaf damage by insect on the ligno-tuberous seedlings of these three 

subalpine eucalypts was not consistent, but the damage levels in the seedlings of E. 

dalrympleana were lower than those of E. pauciflora and E. dives (Williams, 1990). 

Insect herbivory by grasshoppers accelerated nutrient (nitrogen) cycling, plant 

production and abundance, and thereby influenced plant species composition over a 

period of 5 years (Belovsky & Slade, 2000). Enhancement in plant abundance 

depended on consumption rate of grasshoppers and, under some conditions, 

grasshoppers decreased nutrient cycling and plant density (Belovsky & Slade, 2000). 

The nocturnal plant volatiles induced by caterpillars were observed to repel cospecific 

females (De Moraes et al., 2001). Tobacco plants released herebivore 

induced volatiles night and day. The volatile compounds released exclusively at 

night were highly repellent to female moths H. virescens. In fact, tobacco plant 

released temporarily different volatile blends and lipidopteran herbivores used night 

time plant volatile signals to select suitable oviposition sites. In night, attacked

196 


tobacco plant released volatiles that repelled nocturnal pregnant moths looking for 

the site of oviposition. In the day, tobacco plants under attack by herbivores released 

blends attracting parasitic or predatory insects (De Moraes et al., 2001). These 

responses were beneficial for tobacco plants and the herbivorous insect involved 

(De Moraes et al., 2001). These findings indicate that host plant on one hand 

attracted predators of herbivorous caterpillars during day time and female moth coevolved 

to avoid such plants for oviposition using some exclusive night time blends 

to avoid predators of larvae. This co-evolution between tobacco and pregnant female 

moth maintained ecosystem functioning. 

A co-evolutive adaptation was observed as the result of plant-insect interactions 

(Wittstock et al., 2004). For example, maize rapidly mobilizes the accumulation of a 

33-kDa cysteine protease in response to feeding of caterpillars, thereby posing 

resistance to herbivory. The accumulation of the 33-kDa cystein protease in the maize 

midwhorl significantly reduced caterpillar growth due to impaired nutrient utilization 

(Pechan, Cohen, Williams, & Luthe, 2002). The larvae of the specialist insect, Pieris 

rapae (cabbage white butterfly, Lepidoptera) also appear adapted to the glucosinolatemyrosinase 

system, a defensive chemical arsenal of the host plants. 

Trotter, Cobb, and Whitham (2002) studied herbivory, plant resistance and 

climate in the tree ring records and noted that interactions distorted climatic 

reconstructions. The resistance or susceptibility of pines to herbivore and climate 

interaction in the tree ring record were detectable, due to hereditary characteristics. 

These authors found that herbivory reduced tree rings growth by 25–35% and 

distorted climate reconstruction on growth rings. Herbivory-induced changes also 

reduced preference and performance of a variety of insects for a diverse group of 

plants and ultimately increased their fitness in natural environments, as shown from 

studies on wild radish (Raphanus raphanistrum) (Agrawal, 1999). 

4.5. Herbivore Strategies 

Several factors affect herbivores feeding, including the type of available food and 

the biochemical products released during feeding. For example, the lubber 

grasshopper (Romalea guttata) feeds on a wide range of plant species and produces 

a metathoracic defensive secretion containing primarily phenolics and quinones 

(Jones, Hess, Whitman, Silk, & Blum, 1987). When reared on onion (Allium 

canadense) and an artificial diet, it secreted volatiles with fewer compounds, in 

altered proportions as compared to a set of insects reared on diets from a diverse 

group of 26 plant species, including onion. The diet diversity appeared to have a 

major impact on the quality and quantity of the autogenous defensive secretions of 

this generalist herbivore, possibly due to changes in precursors availability, owing to 

a diverse diet and/or to diet restrictions, leading to a physiological stress caused by 

partitioning of resources to defensive chemicals (Jones et al., 1987). 

Larvae of Spodoptera eridania preferred for its diet proteins of Lotus 

corniculatus, as compared to tannins (Briggs, 1990). The larvae were given a choice 

of L. corniculatus plants whose chemical profiles were altered by feeding on plants 

grown with nutrient fertilization, or with symbiotic nitrogen fixation as their only


197 

nitrogen source. The larvae preferred protein rich leaves, rather than leaves with 

higher tannin contents (Briggs, 1990). 

The caterpillar regurgitants were found to amplify the production of the wound 

induced phytohormone jasmonic acid (JA), but not of nicotine in Nicotiana 

sylvestris (McCloud & Baldwin, 1997). It was noted that herbivory and mechanical 

damage increased the concentration of the wound-signal molecule (JA) and the 

defense metabolite (nicotine) in native tobacco plants. However, the larvae of 

Manduca sexta while feeding on damaged leaves modified the plant normal 

defensive metabolites by reducing systemic JA in roots and, subsequently, the 

nicotine content in the whole plant (McCloud & Baldwin, 1997). 

4.6. Simulation of Herbivory 

Several experimental assays attempted to simulate herbivory, in order to gain an 

insight on the potentials of the biochemical changes and signals induced. Realistic 

herbivory simulations in terms of plant responses were noted on combining 50% leaf 

area clipping and JA spraying on Solidago canadensis, rather than either clipping or 

JA spraying alone (Van Kleunen, Ramponi, & Schmid, 2004). Further experimental 

assays on tomato plants showed that JA is a useful plant elicitor for pest 

management (Thaler, 1999a). 

Pontoppidan, Hopkins, Rask, and Meijer (2005) compared the effect of artificial 

mechanical wounding with herbivory by diamond-back moth larvae on rapeseed, 

Brassica napus, showing that the changes observed in myrosinase binding protein 

and myrosinase transcript levels were reflected in protein levels. In a tri-trophic 

interaction including the bacterial phytopathogen Pseudomonas syringae, Cui et al. 

(2005) reported that the bacterium manipulated the systemic plant defense against 

pathogens and herbivores. It was noted that virulent strains of P. syringae induced 

systemic susceptibility to a secondary P. syringae infection in the host plant 

Arabidopsis thaliana (L.) Heynh. The P. syringae infection elicited systemic 

induced susceptibility caused by the production of coronatine (COR), a pathogenderived 

functional and structural mimic of JA, which in turn induced a systemic 

resistance to attacks by the insect Trichoplusia ni. 

Recent studies provided evidence for specificity in the elicitation of induced 

plant responses by different attackers, suggesting that the host suitability for 

colonizing herbivores may depend on the herbivore species that initially damaged a 

plant. For example, the existence of a plant-mediated competitive asymmetry 

between herbivore species on Solanum dulcamara showed the dynamic nature of 

plant resistance, and its potential role in organizing and structuring herbivore 

communities (Viswanathan, Narwani, & Thaler, 2005). 

In simulating/testing of diet components, specific ingredients may be identified 

which play a significant role in herbivores selections. Konno et al. (2006) found that 

mulberry (Morus spp.) latex, rich in antidiabetic sugar-mimic alkaloids, affected 

caterpillars dieting. Some ingredients of the latex milky sap exudate present in veins 

of the mulberry leaves were highly toxic to caterpillars, other than the silkworm 

Bombyx mori, playing a key role in selectivity of insect herbivory. Finally, some 

ecological factors may also affect plant consumption by herbivores, as shown by

198 


Simonetti, Grez, Celis, and Bustamante (2007) who studied the herbivory and 

seedling performance in a fragmented temperate forest of Chile. These authors 

observed that forest fragmentation alters plant-animal interactions, including 

herbivory. The insects were found to be important herbivores in the Maulino forest 

and fragmentation had strong indirect effects on plant communities, as mediated 

through trophic interactions. 

5.1. Plant Defense Strategies 

5. DEFENSE STRATEGIES 

The proteinase inhibitors of tomato plants are known to provide a defense strategy 

against insect herbivory by the beet armyworm, Spodoptera exigua (Broadway, 

Duffey, Dearce, & Ryan, 1986). The insect herbivory rapidly reduced plant quality 

and in turn larval growth, as shown by the larval feeding on foliages from insect 

damaged and undamaged tomato plants. This feedback mechanism involved the 

induction of tomato proteinase inhibitors resulting from larval feeding, that 

systemically reduced leaf nutritive value (Broadway et al., 1986). In Verbascum 

thapsus, herbivory was directly related to age dependent leaf pubescence (Woodman 

& Fernandes, 1991), since less pubescent leaves, of older plants, were more 

frequently attacked than the more pubescent leaves, of younger plants. The leaf hairs 

acted both as a barrier against herbivores and also prevent water loss. Similar agespecific 

mechanical defenses are widespread and effective against generalized 

chewing insects, such as grasshoppers (Woodman & Fernandes, 1991). 

The effect of leaf feeding by the larvae of Samea multiplicalis, at densities of 

0.8 and 1.6 larvae per plant, severely damaged Salvinia molesta, a floating weed, by 

reducing leaf area, plant weight and ramet numbers (Julien & Bourne, 1988). The 

root and rhizomes were spared by the moths allowing the plants to continue its 

growth, but the insect feeding altered the nitrogen balance in above and below 

ground plant parts (Julien & Bourne, 1988). 

Several experimental assays provided evidence for a key role played by JA and 

jasmonate in plant defense mechanisms. McConn, Creelman, Bell, Mullet, and Browse 

(1997) noted that jasmonate is essential for insect defense in Arabidopsis. The 

signalling pathways mounting defenses against chewing insects were complex. Mutant 

plants containing negligible levels of jasmonate showed high mortality (≈ 80%) when 

attacked by larvae of Bradysia impatiens, whereas neighbouring wild type plants were 

largely unaffected. These experiments precisely defined the role of jasmonate as 

essential for the induction of biologically effective defense in plant-insect interactions. 

The herbivory on rape seed plants by cabbage stem flea beetles (Psylliodes 

chrysocephala) induced systemic changes in glucosinolate profile (Bartlet, Kiddle, 

Williams, & Wallsgrove, 1999). A similar change was noticed when JA was applied to 

the plants cotyledons, suggesting that JA synthesis was initially induced by herbivory 

which in turn induced a negative effect on subsequent herbivory (Bartlet et al., 1999). 

Thaler, Stout, Karban, and Duffey (2001) found that jasmonate-mediated plant 

resistance may affect a community of herbivores. Several proteins induced in tomato 

foliage following herbivore damage were linked to reductions in herbivore


199 

performance under laboratory condition (Thaler et al., 2001). This induced resistance 

often suppressed many communities of herbivores. The information on the plant 

biochemistry, insect preference, performance and abundance may hence be helpful in 

developing practical tools for insect management, through natural or induced plant 

defense mechanisms (Thaler et al., 2001). 

The amounts of signalling molecule may affect the efficacy of defense 

metabolites. Quantitative relationships between induced JA levels and volatile 

emissions in maize during Spodoptera exigua herbivory have been reported by 

Schmelz, Alborn, Banchio, and Tumlinson (2003a). JA induced emission of indole 

and sesquiterpenes (volatiles) limited the plant ethylene emission and also controlled 

excessive volatile production. In another study (Schmelz, Alborn, & Tumlinson, 

2003b), volicitin from the herbivore oral secretion induced JA levels, and 

sesquiterpene volatiles were more excessively stimulated in maize than through 

mechanical damage in absence of volicitin. Relatively more significant increase in 

ethylene levels were recorded during beet army worm herbivory, than either by 

wounding or volicitin treatments (Schmelz et al., 2003b). 

Engelberth, Alborn, Schmelz, and Tumlinson (2004) reported that airborne 

signals alert plants against insect herbivore attack. Green leafy volatiles including 

six carbon aldehydes, alcohols and esters were commonly emitted by plants in 

response to mechanical damage or herbivory. These volatiles induced intact 

undamaged neighbouring corn seedlings to rapidly produce JA and emit 

sesquiterpenes. These green leaf volatiles played a key role in plant – plant 

signalling and plant-insect interactions. Heil (2004) reported that JA induced 

defenses in lima bean (Phaseolus lunatus) was beneficial under natural condition. 

Finally, Howe and Jander (2008) observed that herbivore insects use diverse 

feeding strategies to obtain nutrients from their host plants. Plants responded to 

herbivory with the production of toxins and defensive proteins that target 

physiological processes in the insect. This strategy appears as a highly dynamic form 

of immunity, initiated by the recognition of insect's oral secretions and emission of 

signals from injured plant cells. 

5.2. Plant Receptor Molecules 

Cowpea (Vigna radiata) attacked by the fall armyworm Spodoptera frugiperda 

perceived herbivory through inceptins, a proteolytic fragments of chloroplastic ATP 

synthase γ-subunit regulatory regions (Schmelz et al., 2006). Inceptins (feasibly the 

receptor molecule) induced volatile, phenylpropanoid and protease inhibitor 

defenses in cowpea, against fall armyworm. It was also noted that S. frugiperda 

larvae having previously ingested chloroplastic ATP synthase γ-subunit proteins 

induced cowpea defenses after herbivory. 

5.3. Defense Genes in Plants 

Intracellular levels of free linoleic and linolenic acids increased in tomato leaves on 

wounding (Conconi, Miquel, Browse, & Ryan, 1996). The intracellular signalling

200 


pathway for activating plant defense genes against attacking herbivores and 

pathogens is mediated by a lipid based signal transduction cascade. In this pathway, 

linolenic acid (18:3) is liberated from cell membranes and is converted to 

cyclopentanones involved in transcriptional regulation of plant defense genes 

(Conconi et al., 1996). 

A wide range of genes in plants are activated on herbivore attacks, and their 

activation is strongly correlated with the mode of herbivores feeding and degree of 

tissue damage at the feeding site (Walling, 2000). Phloem feeding whiteflies and 

aphids producing little injury to plant foliage were perceived as pathogens and 

activate the salicylic acid (SA)-dependent and JA ethylene-dependent signalling 

pathways. Volatiles blends provided specific cues to attract specialist parasites and 

predators to attack infesting herbivores (Walling, 2000). 

Herbivory on lima bean leaves induced volatiles elicitor defence genes 

(Arimura et al., 2000). In uninfested lima bean leaves, five separate sets of defense 

genes were activated on exposure to volatiles from co-specific leaves infested by 

Tetranychus urticae. All these genes were not activated when uninfested leaves were 

exposed to volatiles from artificially wounded leaves (Arimura et al., 2000). The 

expression pattern of these genes was similar to that produced on exposure to JA. At 

least three terpenoids of the released volatiles were responsible for the gene 

activation, which were released in response to herbivory but not on artificial 

wounding. Expression of these genes required calcium influx and protein 

phosphorylation/dephosphorylation (Arimura et al., 2000). 

The herbivore induced volatiles in Arabidopsis thaliana attracted the parasitoid 

Cotesia robecula (Van Poecke, Posthumus, & Dicke, 2001). The A. thaliana plants 

infested by Pieris rapae emitted volatiles from several major biosynthetic pathways, 

including terpenoids and green leaf volatiles. Haq et al. (2004) focused on the utility of 

the protein proteinase inhibitor genes in combating insects, pests, and pathogen as 

natural and engineered phytoprotection. Devoto et al. (2005) found COII as a key 

regulator of genes involved in wound. The methyl jasmonate induced secondary 

metabolism, defence and hormone interactions. COII expressed approximately 84% of 

212 genes induced by JA, and approximately 44% of 153 genes induced by wounding. 

COII displayed a pivotal role in wound and JA signalling (Devoto et al., 2005). The 

volatile emission on green leaf wounding induced the release of acetylated derivatives 

and a terpenoid in maize, and these compounds in turn induced JA production in intact 

plants (Yan & Wang, 2006). The wound-induced green leaf volatiles (GLVs) caused 

the release of acetylated derivatives and a terpenoid, (E)-4,8-dimethylnona-1, 3, 3- 

triene (DMNT) in intact maize, which may be a type of plant-plant interaction 

mediated by airborne GLVs (Yan & Wang, 2006). 

Karban and Niiho (1995) worked on plant “memory” to induce resistance and 

susceptibility to herbivory. Many plants have been found to be highly induced by 

repeated herbivory, than by a single herbivore bout. The frequency and magnitude of 

damage were confounded and thus it was not clear if a biochemical “memory” was 

involved or overall damage amplified the induced response (Karban & Niiho, 1995). In 

this experiment, the cotton plant attacked by spider mites and mechanical damage of 

cotyledon induced resistance, but damage of apical buds induced susceptibility, due to 

differentially affected hormonal regulation in both tissue types (Karban & Niiho, 1995).


201 

Van Poecke, Roosjen, Pumarino, and Dicke (2003) noted that different kind 

of herbivores induced different signal transduction pathways in A. thaliana. The 

varying blends of volatiles were recognized by specialist parasitoid (Cotesia 

rebecula) of host and non-host herbivores. 

5.4. Tri-Trophic Plant Signalling 

In many plants, Thaler (1999b) found that defence systems against herbivores were 

induced through the octadecanoid pathway, which in turn recruited natural enemies 

(predators or parasites) of herbivores. This pathway was induceable by treating 

plants with JA or by natural herbivory, as noted in case of tomato plants under insect 

herbivory. The plants induced with JA increased parasitism of caterpillar pests in an 

agricultural field (Thaler, 1999b). Either JA or herbivory induced carnivores 

attraction towards herbivores in lima bean plants (Dicke, Gols, Ludeking, 

Posthumus, 1999). Lima bean plants herbivory damage by the two spotted spider mite 

(Tetranychus urticae) led to the emission of complex blend of volatiles. These volatiles 

attracted the carnivorous mite Phytoseiulus persimilis, a specialist predator of spider 

mites which exterminated entire population of spider mites. Dicke et al. (1999) 

inferred that induction of volatile synthesis in Lima bean plants is almost similar 

either caused by JA treatment or herbivorous spider mites. 

Maize plants (var. LG11) under insect attack released large quantities of volatile 

compounds and invited parasitic wasps to attack the herbivore (Pare et al., 1998). 

Volicitin and an elicitor of plant volatile were isolated from beet army worm 

caterpillars, and were regarded as key components inducing plants to recognize 

damage caused by herbivory (Pare, Alborn, & Tumlinson, 1998). 

Figure 1. Choroedocus illustris feeding on young leaves of Zea mays.

202 


Thaler, Farag, Parepaul, and dicke (2002) found that jasmonate deficient plants 

reduced direct and indirect defenses against herbivores. Some plant species had 

negative effects on herbivores whereas others had indirect defense against herbivory, 

via invitation to the natural enemies of herbivores. It was also noted that damaged 

wild type plant were more attractive to predator mites compared with undamaged 

wild plant. In both cases, JA is reported to be an essential regulatory component for 

the expression of direct and indirect plant defences against herbivory (Thaler et al., 

2002). Van Poecke and Dicke (2004) reported that Arabiodopsis thaliana defends itself 

from pathogens, herbivorous insects and mites through induced volatiles emissions, upon 

herbivory. These volatiles guided predators or parasites to reach their herbivorous prey, 

with a benefit for both the plants and the carnivores. Similar indirect defense 

patterns have also been noted in pine, maize and lima bean. 

Figure 2. Choroedocus illustris attacking male inflorescence of Zea mays. 

The proline accumulating leaves are preferred by grasshoppers. Herbivory 

increased the population of grasshoppers in drought stressed plants (Haglund, 1980). 

Treatments with low levels of methyl jasmonate resulted in the accumulation of


203 

certain vegetative storage proteins in soybean seedlings, within 3 days of exposure. 

The protein accumulated preferably on shoot tips and primary leaf. Accumulation of 

some specific protein in response to methyl jasmonate was also noticed in 

cotyledons. It was inferred that volatile methyl jasmonate acts as gaseous messenger 

and growth regulator in plants, which alter the nitrogen partitioning (Franceschi & 

Grimes, 1991). 

In a recent study on maize, the grasshopper Choroedocus illustris attacked 

almost every part of the plant. The grasshoppers preferred young leaves mainly in 

the apical portion (Fig. 1a, b), and also male inflorescence (Fig. 2). 

CONCLUSIONS 

It is evident from the present review that insects and plant co-evolved and developed 

well defined mechanisms to regulate the uptake of a limited amount of plant organic 

matter to higher trophic levels. In this review emphasis has been given to understand 

the natural mechanism of control over herbivore consumption and the way in which 

energy is transferred from primary producers to the organisms of higher trophic 

levels. Plant and insects co-evolution allows the onset of a balanced primary 

productivity, which is partitioned to the second trophic level and beyond. During 

their course of evolution, plants not only developed morphological defense 

mechanisms active against insect herbivory, but also genetic transformations 

allowing the production of volatile chemicals. Attacked plants use these volatile 

chemicals as arsenals and signals against attacking pests. These chemicals not only 

repell herbivores but also control their population, by signalling invitations sent to 

their predators or parasites. For all these purposes plants synthesize special blends of 

volatile chemicals only after insect attack. The interaction between herbivores and 

biotic environment is thus largely based on plant mediated mechanisms, including 

constitutive traits like modifications in plants anatomy and physiology, or herbivore 

induced changes in host biochemistry (Elliot, Sabelis, Janssen, Van der Geest, & 

Berling, 2000; Ode, 2006; Ohgushi, 2005; Price et al., 1980). The plant mediated 

interactions can furthermore operate among spatially and temporally separated 

organisms, even at low herbivory levels (Ohgushi, 2005). 

The energy cost – benefit ratio between crop losses and pesticides use show that 

about 50% of losses are due to pests. Under natural conditions, the energy transfer 

from plants to herbivores has a far lower magnitude (Kormondy, 2003), even 

without use of pesticides. These compounds have in the ecosystem a far reaching 

impact, and may eliminate herbivores predators from the ecosystem. Thus, within a 

single crop cycle, the natural process of controlled biomass transfer from one trophic 

level to the higher one may be altered, in a structural way. If the process of plant 

signalling is activated and applied, it may prove to be more effective than pesticides 

in maintaining stable populations of plants, herbivores and predators. 

Plants also evolved direct strategies to repel herbivores, through induced and 

constitutive defence mechanism. The trichomes constitute a defense feature against a 

variety of insects. But plants also evolved mechanisms based on volatile substances 

acting during insect attacks that, on one hand repell an attacking insect directly,

204 


whereas on the other hand invite its predators. This mechanism becomes operational 

only on herbivore attack. The reaction of herbivores oral secretion and plant elicitors 

activates certain host genes. Thus, plants rely on a system of multiple chemical 

switches that control the partitioning of biomass to herbivores and predators, at least 

up to three trophic levels. Moreover, plants have either no or limited “memory” of 

previous insect attack, with some exceptions. Thus, an equilibrium in the transfer of 

biomass from hosts to herbivore-predators is maintained naturally, throughout the 

plants life cycle. 

Among pests response to plants arsenals, it is worth to recall how herbivorous 

insects evolved adaptive mechanism to search suitable healthy plants for oviposition. 

As shown, nocturnal pests, i.e. Heliothis veriscence avoid injured plants during day 

time for oviposition, to save their offsprings from day time predators (De Moraes 

et al., 2001). 

Herbivory caused by grasshoppers accelerated nutrients cycling and plant 

production and abundance (Belovsky & Slade, 2000). It is also reported that larvae 

of Manduca sexta modified, before feeding on damage leaves, the host normal 

defensive metabolites by reducing systemic JA in roots, and subsequently the 

nicotine content in the whole plant (McCloud & Baldwin, 1997). 

Herbivores and predators also rely on receptor molecules, starting from the 

activation of plants defense genes on an insect attack. Plant defences to herbivory 

can be simulated by JA, since in some plants the defense mechanism was brought 

under operation through JA and artificial injury together. However, more 

experiments are required to induce chemical defense and use this mechanism of 

chemical signalling for pests control, in a way that may be much more effective and 

environment friendly than using pesticides. Biological control may prove indeed to 

be more economic not only for crop losses, but also for the ecosystem maintenance. 

It must be kept in mind that elimination of one herbivore species may prove to be 

more detrimental for the ecosystem if it happens to be a keystone species. Any 

biological control strategy should seek at an equilibrium among plant biomass, 

herbivores as well as predator populations, to be maintained 

Plants adaptive mechanism evolved to ward off herbivores is both structural and 

functional (constitutive and inducible). Host plants synthesize volatile chemicals as 

part of their defense strategies against excessive herbivory. Artificial injury induced 

by leaf clipping in some species did not produce the blend of volatiles which are 

repulsive for herbivore or provide clues to the predators, since they possess specific 

genes activating the synthesis of volatiles only on an insect attack and up regulated 

by the chemicals contained in the herbivores mouth. 

The volatiles synthesized in plant tissues after insects attack were useful to ward 

off insect directly. Also, since the volatiles provide clues to the predator about 

the preys (herbivores) presence and also signal the neighbouring undamaged plants about 

the attack of the herbivores, the course of co-evolution acquired a higher level of 

complexity when certain insect species cleverly adopted to these volatiles. Some 

herbivores, furthermore, were capable to modify the blends of volatiles and thus 

used modified plant arsenals (volatiles) to defend themselves from the predator. 

Due to co-evolution, most plants had limited memory for insect attack but not in 

some perennial trees (mainly Australian eucalypts), in which the plant volatiles were


205 

synthesized for longer duration and controlled insect population. Similarly, due to 

the adaptation of herbivores to modify the blends of chemicals, the role of plant 

volatiles in inviting predators or parasites results in an ecosystem-wide effect, 

influencing the flow of material and energy along the trophic level, as well as the 

population equilibrium levels, at each trophic level. Due to co-evolution of synthesis 

of herbivore repelling volatiles in plants and their modification by herbivores, cyclic 

population changes, concerning both the herbivores and primary producers, can also 

be affected. This aspect needs attention and attempts to increase the amount of data 

through further studies and may prove useful in biological control of crop herbivory. 

ACKNOWLEDGEMENTS 

Authors acknowledge the Departments of Botany and Zoology, Aligarh Muslim 

University for necessary facilities, and funding agencies for financial assistance. 

Farha-Rehman acknowledges U.G.C. for research fellowship. S.M.A. Badruddin 

thanks ICAR for funding through the “Network Project on Insect Biosystematics”. 

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9 

IPM OF THE RED PALM WEEVIL, 

RHYNCHOPHORUS FERRUGINEUS 

MOHAMED SAMIR TAWFIK ABBAS 

Plant Protection Research Institute, 

Dokki, Cairo, Egypt 

Abstract. The Red Palm Weevil (RPW) Rhynchophorus ferrugineus is the major destructive insect 

pest of a broad range of palm trees. Infestation by RPW varies in relation to the height and age of 

palm trees and most likely is restricted to 0–1 m height above soil surface and to palms up to 10 

years old. The life cycle of the insect in the laboratory may last several months depending on the 

type of food, temperature as well as the procedure of rearing. A single female may produce more 

than 400 eggs during its life-time, which may last more than 6 months. Natural enemies recorded for 

RPW include parasitoids, predators and insect pathogens (bacteria, viruses, fungi and nematodes). 

However, such recorded natural enemies do not have considerable role against the insect. Chemical 

control with different insecticides was applied against the insect as spraying, trunk injection as well 

as fumigation, with phostoxin tablets. Alternative safe methods of control were investigated using 

entomopathogenic nematodes, fungi or aggregation pheromone traps. The latter proved to be a 

promising means of control against this insect. 


The Red Palm Weevil (RPW), Rhynchophorus ferrugineus (Coleoptera: 

Curculionidae) is the major destructive insect pest of a broad range of palms 

including date, coconut, sago, oil palm, toddy and royal palm (Nirula, 1956). It 

was first recorded in 1889 in India as the most deadly insect pest of the coconut 

palms (Leefmans, 1920). The insect was later recorded in Ceylon and 

Philippines in 1906, Indonesia in 1920 (Nirula, 1956) and later detected in the 

Gulf area in mid 1980s, the United Arab Emirates (UAE) in 1985 (FAO, 1995), 

Saudi Arabia in 1986, Qatar in 1989 (Abdulla, 1997), the Sultanate of Oman in 

1993 (Al-Kaabi, 1993), Kuwait in 1993 (FAO, 1995), Bahrain in 1995 (Hamdi, 

1998) and Iran in 1992. The insect was able to cross the Red Sea as it was then 

found in Egypt in 1992 (Cox, 1993) and in Palestine, Israel and Jordan in 1999 

(Kehat, 1999). It was also able to cross the Mediterranean Sea to become a 

serious pest in Spain, France, Italy and Greece (Manachini, Mansueto, Arizza, & 

Parrinello, 2008). 

209 




210 

M.S.T. ABBAS 

The high rate of spread of this pest is due to the human intervention, by 

transporting infested young date palm trees and offshoots from infested to 

healthy areas and countries. For example, the insect invaded Egypt when 

infested offshoots were imported from UAE in November 1992 (Cox, 1993). 

Also, as reported by Ferry and Gomez (2002), there was evidence suggesting 

that the first weevils were introduced into Spain from adult palms imported from 

Egypt. 

Leefmans (1920) published the first original investigation on the pest in 

Indonesia, and gave a complete description of the pest suggesting various 

control measures. 

2. HABITAT, INFESTATION AND DAMAGE 

The crown and trunk of the palm tree represent the natural habitats of all stages 

of R. ferrugineus. In old coconut palms the infestation is restricted to the crown, 

while in young trees of coconut and date palms it is present in the crown but 

mainly in the trunk. More often the insect resides in the trunk where it passes 

many generations, feeding into the soft tissue portions until the trunk is 

completely hollowed out and the tree falls down. The early symptom of RPW 

infestation is a brown and bad smelling sap exudated from the point of 

infestation. However, such a symptom could be invisible, especially when 

infestations occur at the base of the trunk. 

The infestation by RPW varies in relation to the height and age of the date 

palm trees. In a study in Saudi Arabia 50% of infestations occurred at heights 

between 0 and 1 m from the trunk base, whereas 38% was within 1–2 m 

(Anonymous, 2001). As for the age of palms, most of infestation was found in 

palms 5–10 years old, while prevalence was lower in palms older than 15 years. 

In a similar study in UAE, Khalifa et al. (2007) reported percentages of 

RPW infestation in different date palm plantations as 77.8% at 0–50 cm and 

20.4% at 51–100 cm (total prevalence was 98.2% within 0–1 m). No infestation 

could be detected at heights higher than 3 m. Similarly, prevalence was 12.8% at 

ages up to 5 years and gradually increased to 64.8% at 6–10 years of age. The 

infestation was noticed to decrease gradually to reach 17.1, 3.3 and 1.3% at ages 

of 11–15, 16–20 and >20 years, respectively. However, in Egypt, in old palms 

some infestations were found at the heights around 6 m, so that the palms were 

broken at that level (unpublished). This case was attributed to the fact that RPW 

infestation occurred at the crown of palm and the larvae moved, in tunnels, 

downward until the tree collapsed at that height. 

2.1. Infestation Spreading 

Once RPW is introduced into an area or even a country, it has great ability to 

disperse and expand. For example, R. ferrugineus was introduced for the first 

time in Egypt through imported offshoots transplanted in two close locations in 

Sharkyia governorate, northeastern of Cairo (Cox, 1993). Since then, great

IPM OF RED PALM WEEVIL 

211 

efforts have been done to eradicate the insect using intensive spraying of 

chemical insecticides in both locations, mass trapping by pheromone traps as 

well as by cutting, burning and burying the infested palm trees. In 1995, despite 

these efforts, a RPW infestation was detected in Ismailia governorate (50 km 

apart from initial focus) and later, in the following years, the insect spread in 

most governorates in Egypt. This extensive spread is certainly due partly to: (i) 

the exchange and transplanting of offshoots and ornamental adult palms, (ii) the 

partial burning of trunks which did not kill all insects inside such palms and (iii) 

superficial burying of burned palms, that allowed the formed RPW adults to 

emerge from soil for months. 

Another example was reported by Gomez Vives and Ferry (1999) who 

mentioned that in Spain very soon after RPW killed the first Phoenix canariensis 

in some gardens at Almufiecar, intensive chemical treatments were applied to 

affected trees. Foliage spraying was conducted with various insecticides and 

preventive treatment of all palms, even healthy ones, was repeated once a month. 

Simultaneously, a mass trapping program using aggregation pheromone was 

initiated. However, despite all such efforts, more than one thousand plants were 

killed and the area of infestation expanded to villages close to the initial focus. 

3.1. Morphological Characters 

3. BIOLOGY 

RPW male and female adults are large reddish-brown weevils about 3 cm long 

with a long curved rostrum. They are capable of flying to long distances. The 

egg is creamy-white, long oval in shape, smooth and shiny. It is about 2.5 mm 

long and 1.1 mm wide. The full-grown larva (13 segments) is a conical shaped, 

plugged in the middle and pointed towards both ends with no legs. The head is 

light brown with well-developed mouth parts. The average length of the full 

grown larva is 50 mm with an average of 20 mm in width. The newly formed 

pupa is creamy in color and turns brown gradually. It is almost 35 mm long and 

15 mm wide. The cocoon, constructed from palm tissues, is oval in shape, light 

brown in color, in average of 60 mm long and 30 mm wide (Fig. 1). 

3.2. Life Cycle 

The life cycle of RPW was investigated by many authors. In the laboratory, the 

durations of the immature stages, adult longevity, total number of eggs 

deposited by a single female and sex ratio varied, as shown in Table 1. Such 

variations could be attributed to the rearing facilities and the food substrate for 

the larvae and adults. 

3.2.1. Oviposition 

The female starts oviposition 2–11 days after emergence from cocoons, in the 

softer portion of the palm in which they feed (Nirula, 1956). It was believed that 

RPW attacks only the palms which have been injured by the beetle Oryctes

212 

M.S.T. ABBAS 

rhinoceros but it has been proved that the weevil attacks healthy and uninfested 

palms (personal observations). To oviposit, the female uses the rostrum to bore 

into the tissues, mainly under the leaf base, to form a hole in which the eggs are 

laid, then the hole is cemented to protect them from natural enemies. 

Figure 1. Life cycle of the Red Palm weevil, Rhynchophorus ferrugineus. 

3.2.2. Feeding 

RPWs feeding takes place on the soft portions of the palm. In the field, the 

weevils select a suitable site with the help of their antennae and thrust in their 

long rostrum at that spot, to feed on the juice. The feeding scars are quite 

superficial and can be readily differentiated from the oviposition holes which are 

deeper (Nirula, 1956). In the laboratory, when weevils feed on pieces of sugarcane 

or palms it was noticed that they grind such blocks by their mouth parts, 

sucking the juice and discarding the remains as ground material (personal 

observations).

IPM OF RED PALM WEEVIL 213

214 

M.S.T. ABBAS 

3.2.3. Locomotion 

Flight of the weevils is restricted to day time and they have never been observed 

as attracted by light traps (Nirula, 1956). Al-Khatri and Abd-Allah (2003) 

studied the daily active periods of R. ferrugineus in date palm plantations in 

Oman, using the pheromone traps. They found that the weevils had two periods 

of activity, the first between 6 and 9 am and the second between 6 and 9 pm 

(sunrise in that area during the period of the study was at 6:15 am and sunset 

was at 5:50 pm). The weevils were noticed to have no activity during the periods 

between 9 am and 3 pm and between midnight to 3 am. Similarly, Gunawardena 

and Bandarage (1995) reported that the periods of RPW activity in Sri Lanka 

were between 6 and 8 am and between 6 and 8 pm. 

RPW adults are capable of flying as well as crawling. When they are thrown 

in the air they fly away in a circle with a buzzing noise and quickly disappear, 

sometimes landing shortly and boring into the soil. It is believed that the insect 

is capable of either flying to a long distance or being carried by the winds. It was 

noticed that when a weevil was attracted to a pheromone trap it landed at less 

than 1 m apart from the trap, then crawled until reaching it (personal 

observation). Chinchilla, Oehlschlager, and Gonzaler (1993) reported that the 

average flight of R. ferrugineus adults was around 500 m per day and a small 

portion of the insect migrated up to 1 km per day. Abbas, Hanounik, Shahdad, 

and Al-Bogham (2006) found that when marked RPWs were released in date 

palm plantations, some of them were captured by pheromone traps in other 

plantations, 1–7 km apart from the release area. Most of such weevils were 

captured 3–5 days post release. 

4. NATURAL ENEMIES 

There are few records about the occurrence of natural enemies of R. ferrugineus, 

which might be attributed to the cryptic habitat of the eggs, larvae and pupae 

which protects them from such natural enemies. 

4.1. Parasitoids 

Scolia erratica (Hym.: Scoliidae) was reported as an ectoparasitoid of R. ferrugineus 

larvae (Nirula, 1956). However, no biological studies on this parasitoid have 

been reported. In Brazil, Moura, Mariau, and Delabie (1993) and Moura, 

Resende, and Vilela (1995) reported the tachinid Paratheresia menezesi as a 

larval-pupal parasitoid of R. palmarum and many individuals of the parasitoid 

adults emerged from a single pupa. However, attempts were carried out to rear 

this parasitoid on R. ferrugineus in the laboratory, but the results were 

unsuccessful (unpublished). Nirula (1956) mentioned that both RPW pupae and 

adults were attacked by an unknown species of parasitic mite which killed the 

pupae and reduced the longevity of adults.


215 

Peter (1989) recorded two mite species, Hypoaspis sp. and Tetrapolypus 

rhynchophori (Pymotidae) parasitizing the RPW adults and mentioned that the 

status of such mites as parasitoids was uncertain. 

4.2. Predators 

Although the earwigs (Forficulidae: Dermaptera) are considered scavengers, 

Abraham, Kurian, and Nayer (1973) recorded Chelisoches morio as a common 

predator inhabiting the crown of coconuts in Kerala, India. The authors 

mentioned that the daily average consumption by nymphs and adults of the 

predator varied between 5.3 and 8.5 R. ferrugineus eggs, or 4.2 and 6.7 larvae, 

respectively. In Saudi Arabia, the earwig, Anisolabis maritima and the 

anthocorid, Xylocorus galactinus were recorded as common predators on RPW 

eggs, larvae and pupae (Anonymous, 2001). 

Anisolabis maritima, showed a higher predatory efficiency. An assay was 

carried out in Saudi Arabia to evaluate its efficiency as a biocontrol agent 

against R. ferrugineus, on 5 year old date palm offshoots (each caged in a wirecage, 

2 × 2 × 2 m). Three pairs of RPW were introduced in each cage in which 

A. maritima was released after 24 h, at rates of 5, 10, 15 and 20 pairs per 

offshoot. One month later, 50% of the offshoots were dissected and the numbers 

of RPW larvae were recorded. The results showed that percentages of infestation 

in the treated offshoots were 50% (in offshoots with 5 predator couples), 25% 

(in offshoots with 10, 15 or 20 couples) and 100% (control). A significant 

reduction in the numbers of RPW larvae was obtained in the offshoots with 

predators, compared to the control. The larvae found in the five treatments were 

12% (in offshoots with 5 or 10 couples), 28% (in offshoots with 15 pairs), 4% 

(in offshoots with 20 pairs) and 44% (control) (Anonymous, 2001). 

The duration of the immature stages of X. galactinus were estimated when 

fed on eggs, 1st instar larvae or pupae of R. ferrugineus in the laboratory at 25°C 

in Saudi Arabia. It was found that the incubation period of the predator egg was 

3.6 days (3–4). The nymph (5 instars) lasted 16.5 days (14–19) when fed on 1st 

instar larvae and 15.5 days (14–17) when feeding on RPW pupae. The average 

daily consumption of a X. galactinus nymph was 1.2–1.8 eggs or 3 larvae. The 

adult consumed 1.8–2 eggs or 3.6 larvae, daily (Anonymous, 2001). 

Xylocorus galactinus was also obtained by M.S.T. Abbas (unpublished) in 

Egypt from a fallen date palm tree, severely infested. However, this species was 

found associated with larvae of the house fly, Musca domestica, feeding on the 

fermented decayed tissues of such a tree. In a food preference test, by exposing 

larvae of M. domestica together with eggs and 1st instar larvae of R. ferrugineus, 

the predator attacked and consumed only larvae of M. domestica. In agreement 

with this finding, Tawfik and El-Husseini (1971) recorded X. galactinus as a 

predator of M. domestica inhabiting organic manure and animal’s dung. 

4.3. Pathogens 

Banerjee and Dangar (1995) isolated the bacterium Pseudomonas aeruginosa 

from naturally infected adults of R. ferrugineus in Kerala, India. The bacterium

216 

M.S.T. ABBAS 

was found to be pathogenic to adults forced to feed on a suspension of bacterial 

cells, and mortality occurred 8 days after ingestion. 

In India, a highly potent cytoplasmic polyhedrosis virus (CPV) specific to 

RPW was also found (Gopinadhan, Mohandas, & Nair, 1990). The virus 

infected all stages of the insect and laboratory infection of late larval stages 

resulted in the development of malformed adults. 

Among fungi, Beauveria bassiana was isolated from adults of R. ferrugineus 

in UAE and Saudi Arabia, through a project operated by the Arab Organization 

for Agriculture Development (AOAD), in the period 1997–2007 (Anonymous, 

2008). The fungus was found to be highly pathogenic to both larvae and adults 

in the laboratory (Hanounik et al., 2000b; El-Safty et al., 2007). 

4.4. Nematodes 

Praecocilenchus ferruginophorus (Aphelenchida) was recorded parasitizing R. 

ferrugineus adults in India (Rao & Reddy, 1980). The size of the nematodes 

found in the haemocoel ranged from small intrauterine specimens to larger 

mature parasitic females, suggesting several simultaneous and unsynchronized 

life cycles in the weevils. Abbas, Hanounik, Mousa, and Awash (2001b) and 

Abbas, Hanounik, Mousa, and Mansour (2001c) isolated two entomopathogenic 

nematodes (EPN), namely Steinernema abbasi and Heterorhabditis indicus from 

adult R. ferrugineus. They also showed that 20–100% of the RPW adults were 

found hosting other non pathogenic, unidentified nematodes. 

5.1. Chemicals 

5.1.1. Spraying 

5. CONTROL 

Preventative and curative spraying of chemical insecticides have been the most 

common method applied for RPW control. All groups of insecticides have been 

tested and applied as foliage and trunk sprayings. For example, Soenardi and 

Hariadi (1978) reported that application of sevin or carbaryl gave effective field 

control when applied every 2 months. Also, Abraham, Koya, and Kurian (1975) 

tested seven insecticides against R. ferrugineus in Kerala, India and found that 

trichlorphon gave the best control, with 92% of the infested palms recovering 

from weevil infestation. In Egypt, El-Sebaey (2004a), concluded after field trials 

that offshoots could be protected from RPW infestation for 11–13 weeks, by 

dipping them for 15 min in a mixture of the insecticides confidor (75 ml/100 l of 

water), oshin (125 g/100 l) mixed with 250 g/l of mud, before translocation and 

re-cultivation. 

It was observed that many infested trunk bases of date palms harbored 

reliable numbers of different alive stages of RPW, below the soil surface. Such 

trunk bases last alive, after removing severely infested palms above the ground


217 

level, for a long time (El-Sebaey, 2004a). In this respect, this author carried out 

an experiment using chemical insecticides to kill all developmental stages of 

RPW surviving in such trunk bases. Big holes were made in the bases, using a 

sharp axe, to facilitate penetration of insecticides downward through the base 

tissues. Six chemical insecticides, dissolved either in water or kerosene, were 

poured at rates ranging from 5 to 10 l/base. Two weeks later, the treated bases 

were picked up using a loader machine and cut into parts to allow inspection of 

alive and/or dead RPW stages, inside the base and root system. The experiment 

showed that the insecticides Cidial (phenthoate), Basudin (diazinone) and 

Dursban (chlorpyrifos-ethyl), dissolved in kerosene, caused 100% mortality in 

larvae and pupae. As for adult weevils they caused 95.6, 95.2 and 97.6% 

mortalities, respectively. However, the same insecticides, dissolved in water, 

caused 57, 53 and 49% mortalities in larvae, 37, 55 and 48% mortalities in 

pupae, and 25, 25 and 26% mortalities in adults. The author related the 

synergistic action of kerosene to three factors: (i) its function as a good carrier 

for the chemicals throughout the wood fibers deeply inside the infested roots, 

(ii) its physical action on the wood as a dehydrated substance which caused 

wood dryness faster than insect survive, and (iii) its effect on dehydration and 

toxic action on the insects' cuticle. 

5.1.2. Injection 

Injection of insecticides into the trunk of the coconut palm was first reported by 

Rao, Subramaniam, and Abraham (1973), who demonstrated that the direct 

injection of 0.2% fenthion gave effective control of larvae in the tree. 

Muthuraman (1984) reported that 10 ml of monocrotophos or dichlorovos 

injected into a pre–drilled 10 cm deep hole above the infestation site gave 100% 

recovery of the treated infested trees. In Egypt, El-Sebaey (2004b) tested 15 

chemical insecticides against RPW infestation by injecting them at different 

concentrations in 4–10 holes (10 cm deep), drilled around the infestation site. 

This author found that all tested chemicals showed 100% recovery of infestation 

at a concentration of 10,000 ppm, while at 100 ppm dursban, curacron and cidial 

gave 80% recovery. 

An alternative to injecting insecticides into the tree is sealing, inside the tree, 

a tablet form of a slow release fumigant. Phostoxin tablets (aluminum 

phosphide) applied at a rate of 0.5–1 tablet per tree was effective in killing 

larvae, pupae and adults of RPW on coconut (Rao et al., 1973). 

Muthuraman (1984) used two 3 g celphos (aluminum phosphide) tablets 

crushed, placed in holes in date palms and sealed with a paste of cement and 

copper oxychloride. 

Abd-Allah and Al-Khatri (2000a) compared the effectiveness of injecting 

chemical insecticides and using fumigation tablets (aluminum phosphide) 

against RPW infestation. In this experiment, three holes (30 cm deep and 1.9 cm 

wide) were drilled into the tree: one at the point of infestation (where the brown 

bad smell sap was oozing), the second 20 cm above and the third 20 cm below 

the first hole. Into each hole 50 ml of the insecticide formothion 33% was 

poured using a plastic tube (45 cm long and 1.3 cm diameter). The holes were

218 

M.S.T. ABBAS 

sealed with moistened clay. In case of fumigation tablets, the part of the trunk 

where oozing occurred was cleaned and the decaying tissues and grubs were 

removed as much as possible. One aluminum phosphide tablet (3 g) was placed 

in the formed cavity then sealed with moistened clay. 

The treated palm trees were inspected at 2-week intervals for 10 weeks. The 

experiment showed that injecting formothion in the infested date palms was 

much more effective compared to the fumigation tablets. The authors concluded 

that aluminum phosphide was not effective in controlling RPW in infested trees. 

They attributed this failure to (i) the escape of gas through many crevices in the 

tree and (ii) the feces and frass which, forming a thick paste, block the larval 

tunnels so that it is difficult for the gas to diffuse to reach the larvae. 

5.2. Aggregation Pheromone Traps 

Trapping of palm weevils started with utilizing insecticide – treated palm stems 

(Mariau, 1968; Griffith, 1969) followed by utilizing treated fruits or sugar-cane 

in plastic buckets hung on the trunk at heights of 1–1.5 m (Delgado & Orellana 

Moreno, 1986). A male–produced aggregation pheromone was first identified 

for R. palmarum by Rochat, Gonzales, Mariau, Villanueva, and Zagatti (1991a) 

and Rochat et al. (1991b). Chinchilla et al. (1993) reported that the most 

efficient and convenient traps for R. palmarum infesting oil palm consisted of 

19 l plastic buckets, containing such a pheromone and carbofuran-treated 

sugarcane. 

Hallett et al. (1993) demonstrated that 4-methyl-5-nonanol (ferrugineol) is an 

aggregation pheromone to R. ferrugineus and R. vulneratus. While another 

compound, 4-methyl-5-nonanone (ferrugineone) was found to have bioactivity 

only for R. ferrugineus. In field trials, these authors found that R. ferrugineus 

was captured in traps with ferrugineol alone or in a 10:1 ratio with 

ferrugineone. Increasing amounts of ferrugineone significantly decreased 

attraction of R. ferrugineus. Interestingly, they also found that using 10 alive males 

of R. ferrugineus in trap instead of ferrugineol and ferrugineone (in 10:1 ratio), 

was as attractive as the latter for both R. ferrugineus and R. vulneratus. 

5.2.1. Trap Design and Components 

Abd-Allah and Al-Khatri (2000b) evaluated nine different designs of pheromone 

traps (20 l plastic bucket hung on tha palm trunk at a height of 1.7 m), for their 

rate of capturing R. ferrugineus adults. They found that the most efficient 

pheromone trap was the open one (without a lid) followed by the trap with a 

plastic lid. The latter had six lateral holes (3 cm in diameter) and four similar 

holes on the lid. Both traps contained a pack of commercial aggregation 

pheromone attached to one side of the bucket. The traps were provided also with 

1 kg of dates, 5 g of yeast and 5 l of water. 

A modification in the trap with a lid was made through a project for RPW 

biological control adopted by AOAD, carried out in Gulf countries in 1997–2007


219 

(Anonymous, 2000). A pack of kairomone (synthetic volatile material induced 

by palm tissues which attracts RPW) is attached beside the pack of the 

aggregation pheromone on the inner surface of the lid, to enhance the rate of 

capture. Recently, some companies are producing a pack of a mixture of 

aggregation pheromone and kairomone. 

A field trial was carried out to evaluate the rate of catch of the pheromone 

plus kairomone traps, compared to those with pheromone only. The trial 

revealed that the pheromone plus kairomone traps captured more weevils than 

the traps without kairomone. However, the difference in capture rates between 

traps was insignificant. Pieces of palm tissues, date fruits or sugar-cane were 

considered to have a role in pheromone traps. The catch of R. ferrugineus in 

pheromone traps containing the commercial aggregation pheromone and dates 

was hence compared to the catch in traps containing either the pheromone alone 

or dates alone. The numbers of RPW captured in 16 traps during a year were 

1,752, 181 and 54 insects for the three treatments, respectively (Al-Saoud, 

2007). Similarly, Chinchilla et al. (1993) reported that pheromone traps of R. 

palmarum captured 6–30 times more weevils than traps containing palm tissues 

or sugar-cane alone. 

Figure 2. Pheromone terrestrial traps. 

5.2.2. Trap Installation 

Pheromone traps were reported to be attached or hung close to palm trees at 1– 

1.7 m height (Oehlschlager, Chinchilla, & Gonzales, 1992; Chinchilla et al., 

1993; Abd-Allah & Al-Khatri, 2000b). In field trials, rate of catch of RPW was 

evaluated in pheromone traps with plastic lids in three date palm plantations 

installed at a rate of 1 trap per ha (Anonymous, 2000). In each plantation, 6 traps 

were buried in the soil up to the lateral holes below the lid of the trap (terrestrial 

traps, Fig. 2) and another 6 were hung on the palms trunks at a height of 1.5 m 

(aerial traps). The weevils from both traps in the three plantations were collected 

weekly, from April to November, and transferred to laboratory where their 

numbers were recorded. It was found that the monthly average capture of 

terrestrial traps was 2–3 folds the aerial traps (Fig. 3). 

5.2.3. Density of Traps 

A field trial was carried out in UAE to compare the catch of pheromone traps 

installed at rates of 1, 2 or 4 traps per ha, in three date palm plantations

220 

M.S.T. ABBAS 

(Anonymous, 2001). Such plantations contained close total numbers of date 

palm trees of the same age, as well as similar levels of infestation. The trial 

revealed that the total number of RPW captured within 5 months at the 4 traps 

per ha density was 2.4 and 2 fold the 1 trap per ha and the 2 traps per ha, 

respectively. However, the calculated annual costs and labor for the 4 traps per 

ha was almost 4-fold the 1 trap per ha density. Chinchilla et al. (1993), in 

contrast, reported that trap density of 1 per ha was just as effective as 6 traps per 

ha, in capturing R. palmarum. 

Figure 3. Average monthly numbers of Red Palm Weevils captured by 

terrestrial and aerial pheromone traps. 

5.2.4. Utilization of Pheromone Traps 

Pheromone traps could be utilized for different purposes, including reducing the 

population of R. ferrugineus, or estimating the insect population fluctuation and 

its sex ratio in nature. 

5.2.4.1. Traps Efficiency 

Performance of the pheromone traps could be evaluated by estimating 

percentages of RPW capture in date palm plantations. An evaluation was carried 

out by Abbas et al. (2006) in Ras Al-Khaima, UAE during 2000 and 2001 by 

releasing marked RPW in three date palm plantations and estimating the rate of 

capture of the released insects by pheromone traps, installed at a density of 1 

trap per ha. Adults RPW were marked using small pieces of thin colored plastic, 

glued onto the thorax of the insect. Different colors and different shapes were 

used, representing different date palm plantations (one color per plantation) and 

different dates of release (one shape per release date). Releases were carried out


221 

at rates of 10–40 individuals per release and plantation. During the period from 

April to December 2000, only males were released in three date palm 

plantations, representing three locations 10–20 km apart from each other (each 

plantation contained 12 pheromone traps). Such pheromone traps were inspected 

3–4 days post release, and the captured weevils were collected and transferred to 

laboratory where the marked specimens were counted. 

During January–December, 2001 both males and females of RPW were 

marked and released in only two plantations (n. 1 and 2). In addition, groups of 

marked males and females were released, periodically, in other four date palm 

plantations. Such plantations were among 130 date palm plantations in Ras Al- 

Khaima provided with pheromone traps at a rate of 1 trap per ha. 

This trapping system was carried out by the Ministry of Agriculture in UAE 

as a method for controlling RPW. All captured weevils were collected weekly 

and transferred to the laboratory, thus allowing the monitoring of the released 

marked weevils. Percentages of capture by pheromone traps did not include 

those marked weevils which were captured in the successive weeks after the first 

capture (3–4 days post release). Also, they did not include the marked weevils 

captured in date palm plantations other than those where they were released. The 

study revealed that monthly percentage of marked RPW captured by pheromone 

traps, 3–4 days post release, from April to December 2000 ranged from 0 to 7% 

in plantation 1, from 6 to 27.5% in plantation 2 and from 12 to 33% in plantation 

3 (Fig. 4). The respective averages in 2001 ranged from 0 to 12.5% in plantation 

1 and from 3.6 to 31.7% in plantation 2. 

Figure 4. Average captures (%) of marked Red Palm Weevils released in three 

date palm plantations in 2000 and 2001. 

The captures of the released weevils did not occur in all releases as no 

marked weevils could be captured from 15 releases in plantation 1, 10 releases 

in plantation 2 and three releases in plantation 3, out of the 32 releases in each 

plantation performed during the year 2000. Similarly, no marked weevils could 

be captured from 19 releases in plantation 1 and 11 releases in plantation 2, out 

of 41 releases in 2001. However, the rate of capture reached 80% when 16

222 

M.S.T. ABBAS 

marked weevils were captured out of 20 released in plantation 2 in the last week 

of December, 2000. The percentage of capture of marked females did not differ 

significantly from that of marked males in the six plantations in 2001. Averages 

of 12.2% of marked males were captured compared to 11.9% marked females. 

This study showed that pheromone traps capture both sexes of RPW almost 

equally. 

The low capture rate in plantation 1 could be attributed to the high rate of 

infestation by RPW as well as the high incidence of weeds in this plantation. 

The high rate of infestation by RPW led to the production of high rate of natural 

aggregation pheromone (secreted by males) and kairomones (volatilized from 

infested palms), which were much more attractive to released males than 

synthetic pheromone and kairomone. Kalshoven (1981) reported that volatiles 

from infested palms and from fermenting palm sap (as a result of infestation) 

were well known to attract palm weevils. The high incidence of weeds, in turn, 

attracted the weevils as a habitat providing shade and shelter. In contrast, the 

high rate of capture in plantation 3 could be attributed to the very low rate of 

infestation by RPW, as well as to the old age of the palm trees (more than 20 

years old) in this plantation. Thus, the pheromone and kairomone in the traps 

were more attractive to the released marked weevils. 

5.2.4.2. Estimating RPW Population Fluctuations 

Population fluctuation of R. ferrugineus was studied using pheromone traps at a 

rate of one trap per ha, to assess the variations in numbers of resident weevils 

from 1 plantation to another, to provide epidemiological data about the 

infestation levels. Also the study determined the peak(s) of RPW populations 

which can help in identifying the best timing of application of protective 

chemicals. Abbas et al. (2006) studied the population fluctuation of R. 

ferrugineus in three date palm plantations (1, 2 and 3) in Ras Al-Khaima, UAE 

during 2000 and 2001, using the terrestrial pheromone traps. The study revealed 

that the populations of the weevils increased gradually to reach a peak in March 

or April, and then gradually decreased til the end of the year. 

The study showed also that the RPW population was much less prevalent in 

plantation 3 compared to plantations 1 and 2 (Fig. 5). The results showed that 

protective chemical insecticidal sprays against RPW in this province should be 

started in March, followed by a further spray in April. 

5.2.4.3. Estimating Reduction of RPW Populations 

Continuous use of pheromone traps, changing the pheromone pack and the food 

substrate (dates or palm tissues) in the proper time, should result in a progressive 

decrease of the R. ferrugineus population in the treated areas. The total numbers 

of weevils captured by pheromone traps in the above mentioned three 

plantations (1, 2 and 3), for example, were much lower in 2001 compared to 

2000. A total of 65,000 weevils were captured within 18 months by pheromone


223 

traps installed in more than 130 date palm plantations in Ras Al-Khaima, site of 

the three tested plantations. In agreement with such observations, Oehlschlager 

et al. (1993) reported that mass trapping with aggregation pheromone traps 

reduced R. palmarum populations and the incidence of the associated red ring 

disease in oil palm plantations. As for R. ferrugineus, Oehlschlager (2007) 

mentioned that there was a strong evidence that trapping, in combination with 

chemical spraying, decreased infestation by 64%, while smaller scale 

experiments indicated that trapping alone reduced infestation by 71%. 

Muralidharan, Vaghasia, and Sodagar (1999) obtained similar results and 

reported that trapping reduced the capture rate of R. ferrugineus by 75%, within 

3 years. 

Figure 5. Population fluctuations of Red Palm Weevilsl in three date palm 

plantations in the years 2000 (a) and 2001 (b). 

5.2.4.4. Estimating Sex Ratios 

In field trials no significant differences were observed between response patterns 

of female and male R. ferrugineus or R. vulneratus to the aggregation 

pheromone (Hallett et al., 1993). In agreement with this report, Abbas et al. 

(2006) found that when marked RPW males and females were released in date 

palm plantations the frequencies of captured females did not differ significantly

224 

M.S.T. ABBAS 

from that of males. Abraham, Faleiro, Shuaibi, and Alabdan (2001), however, 

reported that R. ferrugineus captured by pheromone traps were most likely 

female dominated, as the sex ratio in captured weevils was 1 male:2.7 females. 

El-Garhy (1996) found this ratio to be 1 male:2 females (in Ismaelyia, 

Egypt) while Abbas et al. (2006) found that out of 18,047 RPW captured from 

five date palm plantations (Ras Al-Khaima, UAE) during 2000 and 2001, the 

females represented 60.2% of the total catch, while males represented 39.8% 

(almost 1 male:1.51 females). Finally, Abd-Allah and Al-Khatri (2005) compared 

the catch of different colours of pheromone traps hung on the palm trees at 1 m 

height in Sultanate of Oman. These authors found that the orange or red traps 

captured almost 2-fold RPW compared to the blue ones. However, sex ratio in 

the captured weevils was almost 1 male:1.1 females, in the 3 traps. 

5.3. Entomopathogenic Nematodes 

EPN from the families Steinernematidae and Heterorhabditidae are widely 

regarded as being excellent biological control agents for a number of insect pests 

in soil and cryptic habitats (Gaugler & Kaya, 1990; Kaya & Gaugler, 1993). 

They possess many positive attributes including their wide range hosts, safety to 

vertebrates, plants as well as non target organisms, exemption from registration 

in many countries, ease of in vitro production and application using standard 

spray equipments. The two families bear mutualistic bacteria in the intestine, 

belonging to the genera Xenorhabdus (in Steinernematidae) and Photorhabdus 

(in Heterorhabditidae). 

The free-living, non-feeding 3rd instars (infective juveniles) of these 

nematodes possess attributes of both insect parasitoids or predators and 

entomopathogens. Like parasitoids and predators, they have chemo-receptors 

and are motile; like pathogens, they are highly virulent, killing their host victims 

within 24–48 h. 

5.3.1. Pathogenicity to RPW 

Several laboratory studies were carried out to evaluate the efficiency of EPNs 

against larvae and adults of R. ferrugineus. Abbas and Hanounik (1999) tested 

the virulence of Steinernema riobravis, S. carpocapsae (All strain) and 

Heterorhabditis sp. (Egyptian isolate) against larvae and adults of RPW. They 

found that the three nematode species caused 10–100% mortality in the larvae, 

at concentrations ranging from 30 to 240 infective juveniles (IJs) per larva. The 

trial was carried out in Petri-dishes lined with filter paper. The LC 50 values were 

51, 61 and 56.6 IJs per larva for S. riobravis, S. carpocapsae and 

Heterorhabditis sp., respectively. Adults RPW were less susceptible to the 

nematode infection, as the corresponding LC 50 values for the three species were 

900, 1,100 and 1,416 IJs per adult. However, such infected adults produced 

2,000–242,000 IJs per weevil, but no correlation was found between dose and 

IJs production.


225 

Abbas et al. (2001b, 2001c) were able to isolate S. abbasi and H. indicus 

from RPW adults collected from date palm plantations at Al-Hamranyia, UAE. 

They tested the pathogenicity of these two species to larvae and adults in Petri 

dishes and found that 5th larval instar was less susceptible than the 3rd instar to 

both species, at concentrations of 100 and 200 IJs per larva. The LC 50 values for 

3rd and 5th instars were 69.2 and 97.7 IJs per larva, respectively, for S. abbasi 

while for H. indicus they were 123 and 128.8 IJs per larva. However, only 11.5 

and 8.6% of dead RPW larvae infected with S. abbasi and H. indicus, 

respectively, produced IJs. The average number of IJs produced per larva was 

33,000 (2,000–113,000) for S. abbasi and 35,000 (5,000–85,000) for H. indicus. 

Slight differences in virulence towards adult weevils were found between S. 

abbasi and H. indicus, at concentrations of 12.5 and 25 IJs/cm 2 of sand surface, 

in a trial carried out in plastic cups lined with moistened sterilized sand. No 

difference was noticed at concentrations of 50 and 100 IJs/cm 2 . The calculated 

LC 50 values were 23.2 and 25.1 IJs/cm 2 of sand for S. abbasi and H. indicus, 

respectively. Of the dead adults infected with S. abbasi and H. indicus, 93 and 

89%, respectively, produced IJs with respective averages of 983,000 (93,000– 

3,055,000) and 776,000 (145,000–2,820,000) IJs per weevil at the applied 

concentration of 100 IJs/cm 2 of sand. It should be noted that the recommended 

commercial application of EPNs as biocontrol agents was reported to be 2.5– 5⋅ 

10 9 IJs/ha (Georgis & Hague, 1991). This rate is equivalent to 25–50 IJs/cm 2 of 

soil surface. 

Saleh and Alheji (2003) compared virulence of four species of EPN to the 

3rd and 8th larval instars, as well as adults of RPW in laboratory. Such tested 

nematodes were H. indicus (from Saudi Arabia), H. bacteriophora HP88 (from 

USA), S. abbasi (from Sultanate of Oman) and S. carpocapsae (from Germany). 

A concentration of 100 IJs per larva (in 9 cm Petri dishes lined with filter paper) 

was used for the assay with larvae, whereas concentrations of 10–100 IJs/cm 2 of 

sand surface were used for adults (in 9 cm Petri-dishes lined with 50 g fine 

sand). The results indicated that 3rd instar larvae were highly susceptible as all 

tested nematode species caused 100% mortality within 2–3 days. The 8th instar 

larvae were found to be less susceptible, as percentages of mortality were 60% 

by S. abbasi, 70% by H. indicus and H. bacteriophora, and 80% by S. 

carpocapsae. RPW adults were also less susceptible to nematode infection than 

larvae. Mortality at the tested concentrations, 10–100 IJs/cm 2 of sand surface, 

ranged from 17 to 75% for H. indicus, from 25 to 83% for H. bacteriophora, 

from 33 to 75% for S. abbasi and from 33 to 92% by S. carpocapsae. The 

respective LC 50 values were 49.9, 40.2, 32.4 and 6.4 IJs/cm 2 of sand. Such LC 50 

values correspond to 3,172, 2,555, 2,060 and 406 IJs per adult RPW, 

respectively. 

Shamseldean (2002), however, reported that adult R. ferrugineus was the 

most susceptible stage to nematode infection when testing the efficiency of 13 

species and/or isolates of the Heterorhabditis and 2 isolates of Steinernema 

against larvae, pupae and adults. He stated also that the last instar larva was less 

susceptible than the pupa. Shamseldean and Atwa (2004) reported that three 

Egyptian isolates of Steinernema were highly pathogenic to RPW larvae and 

adults. High mortality rates (100%) were recorded when adults were treated with

226 

M.S.T. ABBAS 

those 3 isolates, while mortalities in last larval instar ranged between 78 and 

90%. 

5.3.2. Field trials 

5.3.2.1. Injection of Nematodes 

Nematodes injection is carried out by making 3–4 artificial tunnels (15–20 cm 

deep) using an electrical hammer drill with a 20–40 cm long screw, above and 

around the infested spot, in the palm trunk , where creamy to dark brown sap is 

noticed (a symptom of RPW infestation). Nematode suspensions are injected in 

such tunnels through perforated plastic tubes inserted into such tunnels. After 

injection, the opening of the tunnels are covered with damp soil to avoid 

reinfestation. 

Shamseldean (2002) carried out field applications of EPN against RPW 

infestation (during 1998–2001) by injecting the trees with 120 ml of the 

nematode suspension at a concentration of 3,000 IJs/ml, injected in each 

artificial tunnel with a total of 1,440,000 IJs per tree. The treated date palms 

were checked 1 month later and during the following 5 months to check the recovery 

from infestation. The numbers of treated palms were 36 (in 1998), 45 (in 1999), 30 

(in 2000), 27 (in 2001). Egyptian isolates of EPN were used: H. bacteriophora 

(strain EKB20), H. indicus (strain EGBB) and Steinernema sp. (strain EBNUE). 

The author mentioned that the treated palm trees, in all applications, were found 

healthy with no symptoms of old or new infestation. Shamseldean and Atwa 

(2004) stated that injection of three Egyptian isolates of Steinernema in infested 

date palm trees resulted in 88.9 and 91.9% recoveries when the isolate EGG4 

was used, compared to 77.7 and 77.1% when the isolate EBNE was used during 

2001 and 2002, respectively. In 2003, percentages of recoveries obtained were 

83.3 and 72.2%, by EGG4 and EIKE isolates, respectively. 

Abbas, Saleh, and Okil (2001a) applied the same technique of nematodes 

injection to seven infested date palm trees, but used another method to evaluate 

the efficiency of the injected nematodes. Two weeks after injection the leafaxils 

in the treated area was removed until reaching the open of the natural 

tunnel made by the insect larva. It was interesting that no dead larvae could be 

obtained in the treated trees and all larvae found were alive and healthy. The 

nematodes used in this trial were S. abbasi, S. riobravis, S. feltiae, S. 

carpocapsae and H. bacteriophora. El-Bishry, El-Sebaey, and Al-Elimi (2000) 

obtained almost similar results. 

Another method of injecting nematodes in the infested palm trees was tested 

by Abbas, Hanounik, Mousa, and Al-Bagham (2000). The leaf-axils were 

removed from the infested spot on the trunk (showing symptoms of infestation) 

until reaching the entrance of the larval tunnel. The tunnels were then injected 

with the nematode suspension containing 5,000 IJs/ml after which the entrances 

were plugged with damp soil. The area where the leaf-axils were removed was


227 

also covered with a thick layer of damp soil, to prevent new infestations. Thirty 

one tunnels in 25 trees were injected, each with 50–100 ml. of the S. riobravis 

suspension. Two weeks later, the injected tunnels were checked for dead and/or 

alive larvae. Out of the 31 injected tunnels, only four contained nematodeinfected 

dead larvae, while 12 tunnels contained alive healthy larvae, with a total 

25% mortality. However, no dead or alive larvae could be found in the other 15 

tunnels. The absence of larvae in the latter tunnels was interpreted as the larvae 

probably migrated through sub-tunnels inside the trunk, before or after the 

nematode injection. 

Saleh and Alheji (2003) used a third method for injecting a nematode 

suspension in the infested date palm trees, treating 30 active tunnels, in 20 trees, 

with fresh exudates and frass, by making few small holes with an electric drill at 

the site of infestation, to reach the tunnel network in the trunk. A suspension of 

H. indicus at the rate of 10,000 IJs/ml was injected through the holes at the site 

of infestation, then blocking the holes with soil. Two weeks later, the tunnels 

were inspected and numbers of dead and alive larvae or adults were recorded. 

The results indicated that percentages of mortality were 58.8% in larvae and 

43.5% in adults. 

In conclusion, the recovery of treated palm trees expressed by “no symptoms 

of old or new infestation” as mentioned by Shamseldean (2002) and 

Shamseldean and Atwa (2004) appears controversial. Injecting nematodes in 

artificial tunnels around the spot of infestation does not warrant that the infective 

juveniles reach RPW larvae inside their tunnels. The walls of the artificial 

tunnels form barriers as the IJs can not penetrate such walls and/or move 

through wood tissues. 

El-Bishry et al. (2000) attributed the poor results of injecting nematodes to 

the deleterious effect of frass in larval tunnels on the injected IJs. These authors 

mentioned that juveniles of five species of EPN were killed within 24 h when 

placed on the frass of infested and decomposed tissues of date palm. However, 

our studies (unpublished) revealed that the feces of RPW larvae and frass 

obtained from larval tunnels did not affect viability or pathogenicity of infective 

juveniles of S. riobravis or H. indicus when placed on such material for 15 days. 

The findings of El-Bishry et al. (2000) could be related to the fact that the frass 

and decomposed tissues of infested palm are subjected to fermentation by 

microorganisms which produce alcohols and other toxic materials toxic to the 

juveniles. 

Compared to nematode injection, the chemical insecticides injected in 

artificial tunnels can penetrate such tunnels, are absorbed by the wood tissues 

and may reach the larvae inside their tunnels. 

5.3.2.2. Spraying Nematodes 

Trunk Spraying 

A semi-field trial was conducted by Abbas et al. (2000) to estimate the 

efficiency of nematodes sprayed against adults of RPW. Sixteen young trees (3–5 

years old) were individually caged by 2 × 2 × 2 m cages made of wooden frame

228 

M.S.T. ABBAS 

and wire screen. The trunks of 12 trees representing three treatments were 

sprayed with one l of nematode suspension containing 2 × 10 6 IJs per tree. The 

amount of suspension was enough to wet the whole short trunk and was sprayed 

carefully so that it did not reach the soil. Two commercial antidesiccants, Liqua- 

Gel (Miller Chemicals and Fertilizer Corporation, USA) at a rate of 100 ml/l and 

Leaf-Shield (Aquatrols Corporation of America) at a rate of 2.5 g/l, were added 

to the nematode suspension in the first and second treatments, respectively. The 

last four trees were sprayed with water as control. Ten females and five males of 

RPW were released in each cage immediately after treatment. 

The palm trees were inspected daily for 10 days and the dead weevils were 

transferred to laboratory and kept individually in White-traps for extracting the 

infective juveniles (IJs) produced by the infected insects. Dead weevils which 

did not give rise to infective juveniles were dissected to check infection. The 

results indicated that mortality in RPW adults was 8.9% when the anti-desiccant 

Leaf-Shield was used with nematode suspension and 13.3% when Liqua-Gel 

was used. However, nematode suspension without anti-desiccant gave 11.7% 

mortality. 

In general anti-desiccants are utilized with the commercial formulations of 

EPN to enhance their persistence and performance in the field (Georgis, 1990; 

Kaya & Gaugler, 1993). The poor efficacy of S. riobravis sprayed on palm trees 

despite the addition of anti-desiccants could be attributed to the adverse effect of 

sun heat and UV radiation on the IJs. The leaf-axils of palm trees do not provide 

enough shade or shelter to IJs. In addition, soil, not leaf-axils, is the natural 

habitat for the nematodes. 

Hanounik et al. (2000a) carried out a similar trial using a Heterorhabditis sp. 

isolated from Saudi Arabia, alone or with Leaf-Shield (100 ml/l of water) or 

Liqua-Gel (2.5 g/l of water). The caged date palm trees were first artificially 

infested by releasing 10 RPW adults on the trunk of each tree and 1 h later the 

trees were sprayed by the nematode suspension. Each tree received an average 

of 3.75 × 10 6 IJs in 2 l of water. The trees were inspected daily starting from the 

3rd day until the 7th day post-treatment to record weevil mortality. The results 

showed that mortalities in R. ferrugineus adults were 65% (by using the 

nematode alone or with Liqua-Gel) and 87.5% (by using the nematode with Leaf 

Shield). Such results, differ from those obtained by Abbas et al. (2000) and may 

depend on the experimental procedure applied. The RPW adults in procedure of 

Hanounik et al. (2000a) were released on the trunks of the palm trees before 

spraying the EPN suspension, which means that the weevils were sprayed 

directly with the infective nematodes. 

5.4. Soil Treatments 

According to field studies and observations (Abbas et al., 2000), it was 

concluded that RPW adults sometimes inhabit soil, probably seeking shade and 

shelter. This conclusion was based on the following reasons: (i) up to 20–100% 

of RPW adults collected monthly by pheromone traps were found to be


229 

parasitized with unidentified non pathogenic nematodes, (ii) both S. abbasi and 

H. indicus were isolated from RPW adults (Abbas et al., 2001b, 2001c), (iii) 

young date palm trees (3–10 years old) were found to undergo severe infestation 

by RPW at or below soil surface, (iv) terrestrial pheromone traps were found to 

capture 2–3 fold RPW, compared to aerial traps (hung at 1–1.5 m height). 

Abraham, Shuabi, Faleira, Abuzuhairah, and Vidyasagar (1998) mentioned that 

on young growing date palms, the weevils take shelter under the splitting bark 

and lay eggs within the newly emerging roots. 

Ferry and Gomez (2002) reported that larvae of R. ferrugineus could be 

found in any place within the palm even in the very base of the trunk where the 

roots emerge. The emerged adults in this case emerge in the soil. Also, El- 

Sebaey (2004a) found that many infested trunk bases of date palm harbored 

reliable numbers of RPW surviving in these parts, just under the ground level. 

Such weevils were found alive after removing the infested collapsed palms for a 

long time and infested the growing roots in the soil. 

Table 2. Mortality (%) of Rhynchophorus ferrugineus adults released in cages 

with soil treated with Steinernema riobravis at a rate of 8 × 10 6 IJs per cage. 

Mortality 

Treated cages 

Untreated 

cages 

7 8 

1 

2 

3 

4 

5 

6 

Total 

86.7 

46.7 

80.0 

86.7 

73.0 

100 

20.0 

13.8 

Due to 

nematode 

infection 

86.7 

33.3 

60.0 

66.7 

60.0 

86.7 

– 

– 

5.5. Semi-Field Trials 

As reported by Abbas et al. (2000), eight 3–5 years old date palm trees were 

caged individually by 2 × 2 × 2 m cages made of wooden frame and wire screen. 

In six cages, the soil was sprayed with 10 l of EPN suspension with 8 × 10 6 IJs 

of S. riobravis, while in the other 2 cages the soil was sprayed with 10 l of 

water as control. Ten females and five males of RPW were released in each cage 

3 h post treatment. The cages were inspected daily and the dead weevils were 

transferred to laboratory and kept in White-traps to extract the IJs produced by 

infected weevils. Dead weevils not giving rise to IJs were dissected to check 

infection. The results of this trial (Table 2) showed that S. riobravis caused 

considerable mortalities among RPW adults in the treated cages. Average 

mortality due to nematode infection was 65.6% (range 33.3–86.7%). 

Interestingly, 40% of the dead weevils were found on the trunk at leaf-axils. 

Saleh and Alheji (2003) conducted similar trial by using S. carpocapsae and 

H. bacteriophora at a rate of 2 million IJs in 3 l of water per tree. The trial was 

carried out in Saudi Arabia in February, with daily mean temperature between 8 

and 20°C. Steinernema carpocapsae caused 77.5% mortality in RPW adults

230 

M.S.T. ABBAS 

while H. bacteriophora caused only 17.5 % mortality. The authors mentioned 

that the low effect of H. bacteriophora could be interpreted as this species was 

isolated from a tropical area, therefore it was not adapted to low prevailing 

temperatures. Such findings confirm the importance of the biological and 

ecological characteristics of the EPN applied, since soil is the natural habitat of 

EPN and most of the successful control with EPNs was achieved against soilinhabiting 

insects (Georgis, 1990). 

In conclusion, soil application of EPNs could be recommended as a 

biological tool for RPW control, within a durable IPM strategy. Persistance after 

release is a fundamental property of any biocontrol agent, in view of its practical 

exploitation. Steinernema abbasi and H. indicus, sprayed in a field study around date 

palms, survived in the treated soil for at least 1 year (Abbas & Mousa, 2003). 

REFERENCES 

Abbas, M. S. T., & Hanounik, S. B. (1999). Pathogenicity of entomopathogenic nematodes to red 

palm weevil, Rhynchophorus ferrugineus. International Journal of Nematology, 9, 84–86. 

Abbas, M. S. T., Hanounik, S. B., Mousa, S. A., & Al-Bagham, S. H. (2000). Soil application of 

entomopathogenic nematodes as a new approach for controlling Rhynchophorus ferrugineus on 

date palm. International Journal of Nematology, 10, 215–218. 

Abbas, M. S. T., Hanounik, S. B., Mousa, S. A., & Awash, S. A. (2001b). Isolation of 

entomopathogenic nematodes from Ras Al-Khaima and Al-Fugaira Emirates (UAE). Egyptian 

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10 

CONTROL OF URTICATING LEPIDOPTERA 

OUTBREAKS WITH BACILLUS THURINGIENSIS 

AERIAL TREATMENTS 

PIO FEDERICO ROVERSI, LEONARDO MARIANELLI, 

LORENZO MARZIALI, MICHELE SQUARCINI AND 

GIANPAOLO BARZANTI 


Research Centre for Agrobiology and Pedology, 

Cascine del Riccio, 


Abstract. The main species of urticating Lepidoptera are presented, together with the environmentfriendly 

methods based on biological control agents. These include the bacterium Bacillus thuringiensis 

and the technologies developed to treat large park and forest areas, in wild as well as urban environments. 

Advances in the aerial control methods developed and the effects of formulations on the treatments 

efficacy and persistence are briefly described. 


A limited number of Lepidoptera is considered as seriously harmful in forest and 

urban parks and this characteristic is linked to the possibility that massive population 

explosions may occur (Myers, 1988). From the ecological point of view, dramatic 

density changes or “outbreaks” are phenomena common to various animal species, 

including insects, and occur through cycles of increasing population density changes 

(Berryman, 1987). The capability to increase enormously in number and to attack 

trees in normal-growing conditions, acting as a prime debilitating or “early damagecausing 

biotic factor” makes the infestation of some species of defoliating 

Lepidoptera particularly dangerous. Furthermore, their attacks can predispose trees 

to infections by pathogenic agents, that exploit the reduced capability of the host to 

react. 

Among Lepidoptera there are species noted not only for the direct damage 

caused by defoliating activities, but also for their capability to interact with agro- 

235 




236 

P.F. ROVERSI ET AL. 

forestry productions and other human activities, including aspects related to 

environmental hygiene. To this instance are referred those species whose larvae, 

during specific developmental stages, bear urticating hairs, i.e. tegumentary 

appendages, connected to special glands, capable of eliciting adverse reactions in 

humans rangin from dermatitis and conjunctivitis to Ig-E mediated anaphylactic 

reactions (Wirtz, 1984; Arlian, 2002). 

In this chapter recent advance on these issues are discussed, with particular 

attention to environment-friendly methods based on biological control agents, 

including the G+ bacterium Bacillus thuringiensis and the technologies developed to 

treat large park and forest areas in wild as well as urban environments. 

2. URTICATING LEPIDOPTERA 

The larval hairs, which act as defence mechanisms, are very small (about one tenth 

of mm) and are generally harpoon-shaped. Their dissemination in the environment 

raises serious implications for the public hygiene. When hairs penetrate the skin and 

mucosal tissues of man or other warm-blooded organisms, they cause severe 

irritations due to both the physical action of penetration (favoured by their shape) 

and the chemical activity of a soluble protein released by the accidental breaking of 

the hairs. These structures are set up on the larval body in particular areas called 

“mirrors”, whose morphology and distribution are characteristic for each species. 

The “mirrors” are produced at every moult, reaching their maximum breadth in last-age 

larvae that can present from hundred–thousand to, sometimes, million urticating 

hairs (Fig. 1b, c). 

The effects produced on man by urticating hairs present a remarkable interest in 

health-care, either for epidermic reactions, more or less persistent, aroused on the 

majority of victims or for other consequences, sometimes observed in individuals 

particularly responsive or sensitized, owing to reiterated contacts. Some worthmentioning 

effects are those related to mucous tissues and sensory organs, mainly 

eyes. Inflammatory reactions can be particularly dangerous for main airways when 

massive inhalation occurs, due to unsafe operations performed during pest control 

by workers not adequately protected (Lamy, Novak, Duboscq, Ducombs, & 

Maleville, 1988). 

Thanks to their tiny size, urticating hairs are easily carried away by air currents. 

For this reason, during intense and widespread outbreaks, remarkable drawbacks 

may occur not only close or within areas stricken by the disease, but also in 

locations considerably far. In recent years, when monitoring the diffusion of this and 

other structures or arthropods parts, these phenomena were referred as “Animal 

Atmospheric Pollution”. At the same time, monitoring operations of pollen and other 

allergenic structures transported by air are performed on this kind of organic 

materials (Lamy, 1990; Werno & Lamy, 1990; Gottschling & Meyer, 2006). 

Lepidopteran larvae bearing urticating hairs with a defence function are known 

among many species of temperate and tropical regions within the following families: 

Thaumetopoeidae, Lymantriidae, Saturniidae, Nymphalidae, Lasiocampidae, 

Bombycidae, Arctiidae, Noctuidae, Anthelidae, Eupterotidae, Limacodidae and 

Megalopygidae.

AERIAL BT TREATMENTS 

237 

The main species of urticating Lepidoptera, responsible of severe infestations 

among countries around the Mediterranean see, belong to the genus Thaumetopoea 

(Fam. Thaumetopoeidae) and Euproctis (Fam. Lymantridae) (Roversi, 2006). In the 

Palaearctic region, the members of the Thaumetopoeidae family form a small group 

of species that represents a formidable menace in wide areas even because of the 

progressive expansion of their distribution range. The increase in their distribution 

area is the consequence of both general climatic trends, characterized by milder 

winter temperatures, and anomalous climatic events allowing colonization of new 

territories, either at higher altitudes as well as in areas northern than those reached 

until a few years ago. 

The two main species known for the negative effects of their infestations are the 

Pine Processionary Moth (PPM), Thaumetopoea pityocampa (Den. et Schiff.) and 

the Oak Processionary Moth (OPM), T. processioneae (L.). Proceeding towards 

northern territories other species are worth mention, such as T. pinivora (Treitschke) 

whose colonies are reported to have increased their extension in areas of North 

Europe completely undamaged until recent times. 

The individuals of the three species exhibit a sub-social behaviour, their larvae 

living in groups throughout their development. Moreover, the first two species 

sometimes build nests of remarkable dimensions, so that a huge amount of urticating 

hairs can be present inside the nests for a long time. 

PPM is a lepidopteran with a wide distribution range in the Mediterranean area 

and Middle-East Europe. It is considered the most important insect pest of pines in 

southern Europe and North Africa, affecting many indigenous and exotic pines, as 

well as other Pinaceae (in order of preference, Pinus nigra austriaca, P. sylvestris, 

P. laricio, P. pinea, P. halepensis, P. pinaster, P. canariensis, Cedrus spp. and Larix 

decidua) (OEPP/EPPO, 2004). Within its range of distribution, T. pityocampa is 

common in extremely diversified habitats, varying from coastal formations to 

mountain woods at altitudes higher than 2,000 m. Particularly severe problems are 

reported at the end of winter, when long processions of mature larvae abandon pines 

in a line, as they come down from trees to deepen themselves into the ground, where 

pupation will take place (Fig. 1a). In this last phase, contacts with people and 

animals are very frequent. 

OPM is an univoltine forest defoliator of deciduous oaks, widely distributed in 

central, western and southern Europe (Agenjo, 1941). The larvae are equipped, from 

the third instar, with urticating hairs and are active in spring–summer. They exhibit a 

gregarious behaviour throughout their life, constructing sack-shaped nests on the 

stem or axis of large branches, in which they pupate in a papery cartoon. This pest 

can completely defoliate oak stands but it is also found on isolated trees in avenues 

and parks. Since the 1990s, heavy attacks by OPM have become increasingly 

frequent throughout very large areas in various European countries (Flemming, 

1997; Tomiczek & Krehan, 2003; Lövgren & Dalsved, 2005; Wulf & Pehl, 2005), 

including Holland, where outbreaks had not been reported for a century (Bosma & 

Jans, 1998; Stigter & Romeijn, 1992; Stigter, Geraedts, & Spikers, 1996). 

In recent years, OPM became a problem even in United Kingdom (Townsend, 

2007). In southern Europe heavy and extensive infestations occurred both in Middle 

European oak environments and forests, and in sub-Mediterranean inhabited mainly

238 


by the Turkey oak Quercus cerris (Camerini, Caronni, & Roversi, 2002; Roversi, 

2002). Nest construction on oak stems not only enhances risk of accidental contacts 

in green areas but, mostly represents a considerable hazard for forest-workers 

committed to carry out coppice cut or to collect firewood. 

Figure 1. Thaumetopoea pityocampa larval procession (a), dorsum detail of a 

mature larva with a “mirror” of urticating hairs (b, white circle) and SEM 

magnified densely thickened urticating hairs of a “mirror” (c) 

Euproctis chrysorrea (L.), a moth widespread in North Africa and Europe 

including Italy, has been introduced also to North America. This species is common 

from the sea level up to the beech mountain altitude, and is also frequent in coastal 

environments on Arbutus unedo and in inland regions on oaks and various 

Rosaceae shrubs, particularly Crataegus spp. On the latter it forms permanent 

hotbeds even in urban and suburban parks. During heavy infestations it can defoliate 

entire woods, making them unfit to deploy. Since the second instar, Euproctis larvae 

bear, on their back, dense strands of tiny urticating hairs, 0.1 mm long, with tricuspidate 

tip. 

Equally important cases are reported in other geographic areas. A clear example 

is the leaf skeletonizer Uraba lugens Walker (Lepidoptera Nolidae), a serious pest of 

forestry and Eucalyptus stands, particularly in risky areas (e.g., urban zones or near 

waterways). Uraba lugens is widespread in the majority of Australian territory 

where periodic outbreaks occur which can lead to extensive defoliations. The 

species is well established also in new Zealand (Farr, 2002; Mansfield et al., 2006). 

The larvae of U. lugens bear, on their back, hairs that after being thrust into man


239 

skin inject istamine, causing irritation, sometimes severe, and wide itching rash 

(Southcott, 1978). 

Lepidoptera families including urticating species are present and spread in almost 

every continent except the most cold regions. Among them the Limantriidae is the most 

important one, due to the genus Euproctis. In addition to the two species E. chrysorrhoea 

(Fig. 2) and E. similis (Fuessly), worth mention are also E. edwardsii (Newman) in 

Australia on Eucalyptus spp., E. lunata Walker on Acacia trees in the Indian region, 

E. scintillans (Walker) on Robinia pseudoacacia L., E. bipunctapex Hampson in 

Singapore and E. pseuconspersa (Strand) in Japan (Ooi, Goh, Loe, & Goh, 1991; Dunlop 

& Freeman, 1997; Ohtaki & Takino, 1998; Balit, Ptolemy, Geary, Russel, & Isbistes, 

2001; Subramanian & Krishnamurthy, 2002; Kalia & Pandey, 2004). 

Figure 2. Euproctis chrysorrhoea: detail of a tuft of urticating hairs with tri-cuspidate tips. 

Many authors reported reactions of “tussockosis” to irritating setae of the 

Douglas Fir Tussock Moth larvae, Orgyia pesudotugata (McDunnough) in the US 

Northwest (Perlman, Press, Googins, Malley, & Poareo, 1976; Press et al., 1977). 

Moreover, in some species, adult females rather than larvae exhibit urticating hairs 

such as in African and South American species belonging to the genus Anaphe 

(Family Notodontidae) and to the genus Hylesia (Family Saturniidae), like A. panda 

(Boisduval), H. urticans Floch & Abonnenc, H. iola Dyar and H. lineata (Druce) 

(Lamy, Pastureaud, Novak, & Ducombs, 1984). The reactions caused by adult moths 

or butterflies are called “Lepidopterism”. Damages to people and animals are caused 

in this case by barbed setae in the anal tuft (Fig. 2), the tips of which show glands 

secreting a toxin, normally released by female on egg clusters as an effective 

deterrent against egg predators and parasitoids, like i.e. the Lycenidae Eumaeus 

atala florida Rueber (Rotschild, Reichstein, Von Euw, Aplin, & Harman, 1970) and 

the Thaumetopoeidae Ochrogaster lunifer Herrich-Schäffer (Floater, 1998).

240 


3. AERIAL CONTROL 

In the last decades, the increasing need to carry out direct monitoring interventions 

as a consequence of diffused infestations of urticating species, showed the limit of 

control means deployed only after damages was already assessed. It is important to 

underline that the use of biocides to reduce large phytophagous populations cannot 

solve, in the short term, public health and hygiene problems. In fact, the mass of 

urticating hairs can remain for a long time in the environment rendering the areas hit 

by infestations unfit for any use, even for many years. 

From this overall picture of serious issues raised by lepidopteran infestations 

and given that, in general, the interventions are set up in forest ecosystems in which 

wide range pesticides are not allowed because of their negative environmental 

fallout, new adequate strategies must be promoted. Among them, it is necessary to 

combine the set up and maintaining of efficient monitoring task forces, to forecast 

the beginning of new attacks, with the improvement of methods and means for the 

timely deploy of biopesticides with a low environment impact. 

Formulations of B. thuringiensis var. kurstaki (Btk), a naturally sporulating soil 

bacteria, have been used for years in North America and Europe against lepidopteran 

defoliators, in coniferous and broad-leaved woods (Martin & Bonneau, 2006; Van 

Frankenhuyzen & Payne, 1993; Van Frankenhuyzen, 2000; Roversi, 2008). The 

formulations are chosen on account of their effectiveness and specificity, as well as 

of the rapidity with which the spores are killed by the UV radiation (Wilson & 

Benoit, 1993; Leong, Cabo, & Kubinski, 1980). 

In Canada and USA, most of the treatments are applied with airplanes. In Italy, 

as well in other European countries like France and Germany, helicopters are 

preferred for control of defoliator lepidopterans, because of their small size and the 

more or less irregular borders of the areas to be treated. Further reasons are the close 

association of the treated surfaces with cultivated areas or the general morphology of 

their environments, which rarely present uniform landscapes over large surfaces 

(Lentini & Luciano, 1995; Luciano & Lentini, 1999; Martin & Bonneau, 2006). 

For aerial spreading of Btk formulations, helicopters have proved more useful 

when wind speed is less than 16 kmh, to reduce drift. The best equipment is the 

electrically operated rotary nozzle, mounted on bars to wet at ultra-low swath 

intervals of about 30 m at each flight. GPS equipments proved also useful to record 

both the flight and the complete treatment coverage. 

Btk spraying experiments carried out in New Zealand against the Tussock Moth 

Uraba lugens Walker, proved the reliability of an ULVA-8 spinning disc operating at 

12,500 rpm and mounted above a track conveyor belt to obtain very small droplets, 

with a median volume diameter of 150 μm, varying the dosis applied by changing the 

belt speed and the flow rates (Mansfield et al., 2006). In Spain, Pascual, Robredo, and 

Galante (1990) showed that aerial treatments using a plane distributing soluble 

powders of Btk at the dose of 5 l/ha 1 (1,500 cc of commercial product with 8,500 

u.i./mg 1 and 3.5 l of water), resulted in high mortality of OPM larvae, in colonies 

artificially transferred to areas that were then experimentally treated. 

Unlike standard protocols today available for other harmful defoliators of 

mesophilous forests, i.e. Lymantria dispar (L.), noxious also to cork oak in North


241 

Africa, or Choristoneura fumiferana (Clem.), which is often very dangerous to many 

nearctic conifer stands (Lentini & Luciano, 1995; Bauce, Carisey, Dupont, & Van 

Frankenhuyzen, 2004), no standard protocols are available thus far in Italy for Btk 

products aimed to control main urticating lepidopteran defoliators. Data are now 

available only on T. pityocampa, based on experiments proceeding from other 

countries. In Italy, observations began in the 1960s (De Bellis & Cavalcaselle, 

1969; Triggiani & Sidor, 1982; Currado & Brussino, 1985; Niccoli & Tiberi, 1985; 

Ambrosi, Salvatori, & Zanotelli, 1993; Battisti, Longo, Tiberi, & Triggiani, 1998). 

Further investigations on the capability of aerial treatments by means of 

biopesticides against PPM were carried out also in other European countries, 

especially in France where this species is often noxious mostly in tourist areas, i.e. in 

the Maritime Alps (Demolin, Martin, & Lavanceau, 1993; Demolin & Martin, 1998; 

Martin & Bonneau, 2006). 

Very few data are available for the Brown Tail Moth (BTM) E. chrysorrhoea as 

well as for OPM. The latter species, has spread recently northwards in Europe 

convincing some EU Member States to introduce national or regional control 

programmes for public health reasons (EFSA, 2009). However, only in 2008 an 

experimental protocol has been issued by means of aerial spreading of Btk over 

large areas. Employ doses were stated at 2.5 l/ha 1 of 12.7 BIU (Billion International 

Units)/l of commercial formulation and were distributed at ultra-low volume at the 

time of bud opening, against 1st and 2nd instar larvae (Roversi, 2008). 

Before aerial Btk treatments are deployed, it is also useful to know the exact 

time of presence of larvae, which varies normally according to the different 

urticating. For instance, OPM and BTM have different larval presence. In Italy, for 

the former species it is necessary to treat by the end of April or at the beginning of 

May, when buds are opening and leaves growing. However, it is important to treat 

larvae before they reach the third instar, when they become urticating. Early 

treatments in spring are also capable to better wet the crowns inside. In fact, to reach 

a good biopesticide spraying all over the new foliage it is necessary to avoid some 

larval groups to escape. 

For BTM, the different life cycle patterns lead to treatments in the late summer 

or autumn, just before the larvae hide themselves inside winter nests. However, in 

mild Mediterranean climates with mild winters where BTM can feed and survive on 

mixed scrubs, treatments can be delayed to the end of autumn. As to PPM, 

treatments can be performed by the end of summer, when the newly hatched larvae 

start to feed on needles. The winter control of PPM is possible by means of Btk 

formulations applied on third instar larvae or more (L4–L5) (Martin & Mazet, 

2001). Furthermore, it is worth to remark that PPM can show different life cycle 

patterns, according to the different seasonal conditions and climates. In fact, PPM 

eggs can be laid sometimes also at the beginning of autumn (Battisti, 1989). 

Numbers of researches have been carried out in the recent years also on the Btk 

impact on non-target species, as well as on the persistence of the microbial products 

in the treated environment (i.e., spores-crystal complex), or the host plant effects 

(Cooke & Régnière, 1999; Appel & Schultz, 1994; Kouassi, Lorenzetti, Guertin, 

Cabana, & Mauffette, 2001; Bauce, Bidon, & Berthiaume, 2002; Carisey, Bauce, 

Dupont, & Miron, 2004), so that the Btk residual activity is now a key-factor in

242 


operational forestry and urban programs (Gindin, Navon, Protasov, Saphis, & 

Mendel, 2007). 

Figure 3. Petri dish with Btk colonies developing from already died 2nd instar larvae 

collected in the field after an aerial treatment. 

In experimental assays carried out in spring 2004 on Turkey oak woods in 

Tuscany (Central Italy), coinciding with the early phase of a new T. processionea 

outbreak, a wide aerial Btk treatment was carried out, followed by a 1-month 

evaluation of its effect on non-target lepidopterans. The control area was checked 

daily with traps placed underneath the crowns (Roversi, Rumine, & Barzanti, 2006). 

These trials showed a low effect of the treatment against OPM, with a small number 

of dead larvae of other species (Roversi et al., 2006). 

Figure 4. Numbers of Btk colonies developed from 1 ml water washings of Turkey Oak leaves 

collected from the upper part of the tree crowns, after treatment with 31.75 Btk BIU/ha, at 

Berignone Forest (Tuscany, Central Italy). Leaves were collected in a period of about months 

(Bars show standard deviation) (Roversi et al., unpublished).


243 

Further laboratory analyses of both the insects midgut and leaves revealed the 

presence of bacterial spores inside the whole crown, together with the development 

of colonies from 100% of the OPM larval cultures. These were obtained from larvae 

died within the first 9 days after the treatment (Fig. 3). Further controls of Btk 

persistence using agar cultures of water washings from leaves, collected at both high 

and medium crown levels, revealed a marked reduction of the living spores 10 days 

after the treatments (Fig. 4). In some cases, on the contrary, colonies of Btk spore 

were obtained from leaves collected 2 months or more, after treatments (Roversi et 

al., unpublished data). 

Other field experiments confirmed the persistance of Btk applications based on 

milk formulations, used successfully against T. wilkinsonii Tams in Israel. Data 

showed that the formulation has a rain-fasting effect, resulting in the retaining of 

more than half of the Btk activity after 8 days (Gindin et al., 2007). 

In conclusion, the exploitation of biopesticides based on Btk is likely to be 

strongly increased in the future, owing to both the scientific evolution and the 

government policies, encouraging the use of alternative pest control products. 

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Section 3 

MITES BIOLOGICAL CONTROL AND IPM

11 

IPM POTENTIALS OF MICROBIAL PATHOGENS 

AND DISEASES OF MITES 

LEO P. S. VAN DER GEEST 

IBED, Section Population Biology 

University of Amsterdam, 

1098SM 

Amsterdam, The Netherlands 

Abstract. An overview is given of diseases in mites, caused by infectious microorganisms. Many 

pathogens play an important role in the regulation of natural populations of mite populations and are for 

this reason subject of research on the feasibility to develop such pathogens to biological control agents. 

Several examples are given of successful application of pathogens for the control of mite pests, but also 

failures are discussed. Most studies concern fungal pathogens of tetranychids and eriophyids; some of 

these fungi are possible candidates for biological control agent of species of noxious mites. An interesting 

group of pathogens form the intracellular symbionts: bacteria that may cause unusual effects in their 

hosts, such as parthenogenesis, feminization, male killing and incompatibilities. This group of bacteria is 

present in many invertebrates species and are presently widely studied as new molecular techniques have 

become available that make detection of such symbionts possible. Attention is also given to quality 

control of beneficial mites that are being used in integrated control programs. Beneficial mites, as e.g. 

predatory mites, may also be infected by microorganisms (bacteria, viruses, microsporidia), resulting in 

poor performance of the predator. Prospects for the application of pathogens in IPM systems are 

discussed. 


As other organisms, Acari may also be subject to disease, usually caused by 

pathogenic microorganisms. Our knowledge on pathogens of mites, however, is still 

fragmentary, in contrast to what we know about pathogens of insects. The rapid 

development of invertebrate pathology in the second half of the twentieth century 

has largely been due to the study of insect pathogens. Relatively few mite pathogens 

are known, despite the large number of mite species. Approximately 48,000 species 

have hitherto been described and it is estimated that this number represents only 

10% of the total number of mite species. 

That mite pathogens have been studied less comprehensively is not surprising: 

their frequently small size renders disease diagnosis often difficult and 

pathophysiogical studies almost impossible. From the other hand, the often large 

249 




250 

L.P.S. VAN DER GEEST 

reproductive potential of mites makes many acarine species ideal model organisms 

for detailed epidemiological investigations. 

Pathogens in populations of mite species often play a major role in the 

regulation of population size and population density in natural habitats. In several 

instances, we see that populations of pest species in agricultural systems are kept 

below the economic threshold level by the occurrence of a disease. Such 

observations often provide impetus for further studies on the pathogen involved that 

may eventually lead to the successful application of a pathogen for the biological 

control of a mite pest. In addition, the occurrence of disease may be undesirable, e.g. 

in the case of cultures of beneficial mites: several cases have been reported on the 

occurrence of disease in mass cultures of predatory mites. In many instances, such 

observations have led to comprehensive studies on the mite pathogen involved. 

Interest in pathogens of mites is increasing. This is apparent from literature 

reviews that have been published in recent years. We refer to reviews by Van der 

Geest (1985), McCoy (1996), Poinar and Poinar (1998), Samish and Řeháček 

(1999), Chandler et al. (2000) and Van der Geest, Elliot, Breeuwer, and Beerling 

(2000). A survey of pathogenic fungi infecting plant-inhabiting mites can be found 

in Van der Geest (2004). The student is referred to these reviews if more detailed 

information is required than is given in the underlying chapter. 

Mites obtain their food in general by inserting their mouth parts into their 

vertebrate host or plant tissue. It is therefore unlikely that mites would contract 

disease through the alimentary tract unless the vertebrate host or food plant is 

infected by a pathogen. As penetration through the mouth parts is hampered, the 

pathogen should follow other infection routes. A plausible infection route is through 

the integument. Fungi are in general capable to penetrate a mite (or other arthropod 

species) through the integument. It is therefore not surprising that most mite 

pathogens are found among the fungi. 

In this chapter, the different groups of microorganisms that may cause diseases 

in Acari will be treated. 

2. VIRUS DISEASES 

Relatively few viruses are known from mites, in strong contrast to what is observed 

in insects, from which more than 1,600 viruses have been described in about 1,100 

species. Insect viruses are often embedded in larger inclusion bodies, as is the case 

for nuclear polyhedrosis viruses. The rod-shaped virus particles are situated in 

proteinaceous bodies that protect the virus against unfavorable conditions when 

released from the insect cadaver. Such structures are not found for viruses that are 

known from mites. Well-studied viruses in mites are found in two spider mite 

species: the citrus red mite, Panonychus citri, and the European red mite, P. ulmi. 

The first record on a virus disease in a spider mite is by Muma (1955), who 

noted diseased mites in a natural population of the citrus red mite (CRM) in Florida, 

USA. Affected mites showed signs of diarrhea and the cadavers were adhered to the 

leaf surface by a black resinous material that was excreted from the anus. The 

disease has later also been reported in California by Smith, Hill, Munger, and

MITE PATHOGENS IN IPM 

251 

Gilmore (1959). They observed spherical particles inside diseased mites and 

assumed that these were virus particles. Later, it could be demonstrated that a rodshaped, 

non-inclusion virus is the cause of the disease (Reed & Hall, 1972). The 

virus particles are approximately 194 × 58 nm in size and enclosed in an envelope of 

circa. 266 × 111 nm. The virus is formed inside the nuclei of epithelial cells of the 

midgut, but later it moves out of the nucleus, into the cytoplasm. The pathogen is 

transmitted when healthy mites ingest the feces of infected mites. 

The spherical particles were studied in more detail by Reed and Desjardins 

(1978). These authors found spherical particles of three different sizes, but only in 

laboratory reared mites. The particles were apparently acquired by the mites from 

the green lemons on which they were grown. No detrimental effects of the particles 

on the mites were observed, although the spheres did multiply inside the mites. In 

diseased mites, birefringent bodies of irregular shape were found. The size of these 

bodies may vary from a few micrometers up to 50 μm in diameter (Smith & 

Cressman, 1962). The function of these bodies is not known, but they seem to be 

associated with the formation of the so-called fecal pellets, that probably contain 

guanine as excretion product. Similar bodies have been found in mites showing poor 

physiological condition (see Section 6.1). 

The virus disease is common in citrus groves in California and Arizona and 

causes a considerable reduction in the population density of the CRM (Reed, 1981). 

In the 1960s, efforts were made to use the virus as a biological acaricide in order to 

control the CRM. A drawback in the use of viruses for biological control is that 

multiplication is only possible in living cells. Control experiments were carried out 

by spraying aqueous suspensions of macerated diseased mites (Shaw, Chambers, & 

Tashiro, 1968). For this purpose, mites were grown on green lemons and harvested 

after infection. This is a very laborious method and can only be done for small field 

experiments. Another more efficient method was the collection of infected mites in 

the field by means of a vacuum-suction devise. The mites were subsequently kept on 

lemons for an additional 6–7 days in order to increase the level of infection. 

Application of field collected material usually rendered better results than virus 

suspensions obtained from laboratory cultured mites. The results in small field trials 

were promising, but large field applications were less satisfactory. Reasons are that 

the virus is easily inactivated by sunlight when applied as an aqueous suspension 

and that high temperatures have a negative effect on the virulence of the pathogen. 

An advantage of using viruses as biological control agent is that they have a narrow 

host spectrum: they are able to infect only a few species of spider mite and show no 

effect on other organisms, e.g. phytoseiids (Shaw, Moffitt, & Sciven, 1967). 

Steinhaus (1959) studied a virus disease of the European red mite (ERM) in 

California. He observed spherical particles with a size of 40–60 nm inside affected 

mites and assumed that these were virus particles. A virus disease was also observed 

in P. ulmi in fruit orchards in Ontario (Putman & Herne, 1966). This disease was 

caused by a rod-shaped virus that developed inside the nuclei of fat body cells. 

There is no conclusive evidence that we are dealing with the same virus as the one 

that described from California. Affected mites can be recognized by a darker color 

of the immature stages, but diseased adults show no difference in color. The most 

conspicuous symptoms, however, is the presence of birefringent bodies inside the

252 


midgut of the mites. These crystal-like structures probably contain guanine. The virus 

may cause epizootics in natural populations, but only at high densities of the spider 

mite. Field experiments were carried out by Putman (1970) by introducing infected 

immature mites into a peach orchard. In this way, a considerable reduction of the mite 

population could be obtained. Sprays of aqueous suspensions of the virus were less 

successful. It was assumed that the leaves release virus inhibitors that inactivate the 

virus. Recent studies on virus diseases in tetranychids have not been conducted. 

Transmission electron microscopy (TEM) has revealed virus-like particles in 

diseased females of the predatory mite Metaseiulus occidentalis (Poinar & Poinar, 

1998). Diseased females in laboratory colonies showed a reduced oviposition and 

often died suddenly with a paralyzed appearance (Hoy & Jeyaprakash, 2008). Three 

types of icosahedral virus particles were detected by TEM analysis. One type was 

situated in epithelial cells, 47 nm in diameter with an electron dense core of 35 nm. 

Poinar and Poinar (1998) assumed that these particles were similar to those reported 

earlier in the citrus red mite and also similar to those found in epithelial cells of 

diseased and healthy twospotted spider mites (see above). It might be possible that 

the predatory mites obtained these particles from their prey, T. urticae. A second 

type of virus particles in M. occidentalis was approximately 38 nm in diameter with 

an electron dense core of 20 nm. These particles were located in large numbers in 

the nuclei of midgut cells, but free virions were also observed in the cytoplasm and 

lumen of the midgut. A third type of virus particles was 45 nm in diameter with a 35 

nm dense core. These particles were only observed in tissue of the alimentary tract. 

We know little about the etiology of the disease and whether these observed 

particles are the cause of the disease and whether the predator becomes infected by 

feeding on infected prey. The predatory mites studied belonged to crowded 

laboratory colonies, no field material had been included in the study. 

Virus-like particles have been observed in the yolk of eggs developing inside gravid 

Neoseiulus cucumeris by Steiner (1993) and inside Phytoseiulus persimilis females by 

Bjørnson, Steiner, & Keddie (1997). In adults of these species, also birefringent crystals 

were observed, but there may be no relation between the presence of the virus-like 

particles and these crystals.Virus infections in cultures of predatory mites are undesirable 

as such conditions may affect the efficacy of the predator as biological control agent. 

Several phytophagous species are known to transmit plant viruses. For example, the 

dry bulb mite Aceria tulipae has been reported as vector of two viruses of Allium sp. 

(Van Dijk & Van der Vlugt, 1994) and Brevipalpus spp. are known as vector of, among 

others, citrus leprosis virus in citrus in Latin America (Rodrigues, Kitajima, Childers, & 

Chagas, 2003), of orchid fleck virus in many orchid species world-wide (Kondo, Maeda, 

& Tamada, 2003) and of coffee ringspot virus in coffee in Brazil and Costa Rica 

(Chagas, Kitajima, & Rodrigues, 2003). It is doubtful whether these vector mites suffer 

from the presence of viruses inside their body, although the high plain virus and Pigeon 

Pea Mosaic virus seem to replicate in their respective vectors (Kumar, Duncan, Robert, 

Jones, & Reddy, 2002). The Brome Mosaic Virus, usually transmitted by a beetle, is 

capable to multiply in the eriophyid Aceria tulipae. It may cause severe cytopathological 

effects in the midgut cells of the mite (Paliwal, 1972). Similarly, mites e.g. 

Dermanyssoidea play a role in the transmission of viruses to vertebrates (e.g. equine 

encephalitis viruses, West Nile virus, fowl pox virus) (Valiente Moro, Chauve, &


253 

Zenner, 2005). It is not within the scope of this article to describe these viruses 

comprehensively, as they are considered to be plant, resp. vertebrate viruses. 

Several viruses are known from the honeybee (Apis mellifera), some of which 

are associated with the varroa mite Varroa jacobsoni and the honeybee tracheal mite 

(HBTM) Acarapis woodi (Sammataro, Gerson, & Needham 2000). These viruses 

may always be present in the bee, either in a latent or in an unapparent form. 

Wounds inflicted by the mites may activate the viruses in the bee. These viruses are 

probably not capable to infect the varroa mite or the HBTM, but the presence of 

these mites affects the incidence of virus disease in honey bees. The varroa mite may 

also play a role in the transmission of Bee Kashmir Virus (KBV), although the virus 

was already known from bee colonies before Apis mellifera colonies were infested 

by V. destructor. The presence of the virus in the mite has been demonstrated by 

several authors (e.g. Chen, Pettis, Evans, Kramer, & Feldlaufer, 2004). Virus-free 

mites may become infected by coinhabiting in the same cell as virus-infected mites. 

Whether transmission to honey bees occurs mechanically or biologically is a 

question that has not yet been conclusively solved. Shen, Yang, Cox-Foster, and Cui 

(2005) suggested that varroa mites cause suppression of the immune system of the 

honey been which leads to activation of latent virus infections. 

Liu (1991) found virus-like particles in a sample of HBTM that originated from 

Scotland, but no such particles were found in HBTM samples from California. 

Tissues of affected mites showed extensive lysis, while most cells were tightly 

packed with virus-like particles. The virions are 27–30 nm in size and are arranged 

in paracrystalline arrays forming hexagonal patterns. The ultrastructural morphology 

of the particles indicates that we may be dealing with a picorna-like virus. Such 

viruses resemble picornaviruses that are found in vertebrates. Picorna-like viruses 

are also known from honeybees, but on the basis of histopathological studies it was 

assumed that the virus found in HBTM is not derived from honeybees, but actually 

multiplies inside the mite. 

Kleespies, Radtke, and Bienefield (2000) performed a search for diseases in 

varroa mites in parasitized bee colonies. They found mites with characteristic 

internal black-colored changes of the gut and the fat body. On living adult bees, 

3.6% of the mites showed this anomaly, in brood cells, even 8% of the juvenile 

mites were affected. Disease incidence and intensity of the symptoms can be 

enhanced by changes in environmental conditions, such as deficiency of bee brood, 

deficiency of pollen, abnormal brood temperature and death of the host. The authors 

found that longevity of black-colored mites was reduced by 43%. Cytopathological 

studies showed the presence of a large number of spherical virus-like particles, 

especially in the nuclei of fatbody and muscle tissue. The particles measure 

approximately 27–60 nm in diameter and were very similar to the particles found by 

Liu (1991) in HBTM. Per os infection experiments with extracts of fatbody tissue 

derived from symptomatic mites were unsuccessful. 

Ongus et al. (2004) detected virus-like particles in varroa mites that were 

collected in bee hives in The Netherlands. The virions were mainly present in the 

cytoplasm of mite tissue and resemble the virus-like particles found by Kleespies 

et al. (2000). Immunochemical studies revealed that the virus was localized in the 

abdominal part of the alimentary tract and in the gastric caeca, but not in the salivary

254 


glands (Ongus, 2006). It was possible to isolate the virus and to determine the base 

sequence of the virus genome. The virus (Varroa destructor virus 1) is a single 

stranded RNA genome and, based on the base sequence, it was decided that it belongs 

to the genus Iflavirus (Ongus et al., 2004). Viruses in this genus belong also to the 

picorna-like viruses. The virus is closely related to deformed wing virus, known from 

honey bees. The latter virus causes morphological anomalies in wings of bees. 

3. DISEASES CAUSED BY BACTERIA 

The most widely studied bacterium in invertebrate pathology is Bacillus 

thuringiensis. It was first described in 1915 by Berliner, who isolated it from soil 

samples in the Thuringian Forest in Germany. Simultaneously with spore formation, 

a crystalline body is formed in the bacterium. Upon ingestion by an insect, this 

crystal (δ-endotoxin) falls apart into toxic subunits that may cause paralysis of the 

alimentary tract, resulting in the death of the insect. Most varieties (serotypes) of B. 

thuringiensis show an effect on larvae of Lepidoptera, but some also on other groups 

of insects, e.g. Coleoptera and Diptera. 

Very comprehensive research has been carried out on B. thuringiensis that has 

resulted in the development of several commercial preparations that are mainly used 

against lepidopterous pests. Also, the gene encoding for the crystalline toxic body 

has been isolated and transferred into crop plants, e.g. corn and cotton, making these 

crops resistant towards a number of lepidopterous pests. Several serotypes of B. 

thuringiensis produce in addition an exotoxin, the β-exotoxin, named thuringiensin. 

This exotoxin is excreted by the bacterium into the culture medium. It has a 

nucleotide-like structure and inhibits DNA-dependent RNA polymerase. This results 

in a blockage of mitosis. When thuringiensin is applied to young holometabolous 

insects, morphological deformations may occur in the adult stage. 

Field applications of thuringiensin were successful against the citrus red mite P. 

citri (Hall, Hunter, & Arakawa, 1971) and Tetranychus pacificus (Hoy & Ouyang, 

1987). Later, Royalty, Hall, and Taylor (1990) conducted experiments by testing two 

different formulations of thuringiensin against the twospotted spider mite T. urticae. 

The results indicated that thuringiensin might be a potential acaricide. In particular 

young instars are susceptible, since these have a high growth rate. Various 

physiological processes in young organisms require higher RNA synthesis than in 

the older slower growing stages. A major drawback is that thuringiensin is toxic for 

a wide range of organisms. Not only are spider mites affected, but also beneficial 

mites, such as Phytoseiulus persimilis: oviposition starts to decline after 2 days and 

ceases completely after 3–4 days in both predator and spider mite T. urticae (Guo, 

Zuo, Zhao, Wang, & Jiang, 1993). The chemical is apparently a nonselective 

acaricide that should not be used in combination with predatory mites. 

The spore-crystal complex of B. thuringiensis has been tested on spider mites 

by Krieg (1972), but no mortality was observed. However, Chapman and Hoy 

(1991) conducted experiments in which T. urticae and Metaseiulus occidentalis 

were treated with a commercial preparation of B. thuringiensis var. tenebrionis. This 

variety of B. thuringiensis shows an effect on beetles and is recommended for use 

against the Colorado Potato Beetle, Leptinotarsa decemlineata. No effect was noted


255 

on the twospotted spider mite, but the preparation did show a toxic effect on M. 

occidentalis. Eggs were not affected, but if juveniles were treated, only 65% reached 

the adult stage. This toxic effect could be enhanced by starving the mites: the 

authors assumed that starvation may lead to a higher uptake of the material, or that 

the mites were more exposed to the preparation as starving mites tend to move 

faster. It is also possible that starvation acts as a stress factor. The authors have no 

explanation for the toxic effect on the predatory mite: the preparation did not contain 

the β-exotoxin (thuringiensin) known to be toxic for mites. 

In more recent years, isolates of B. thuringiensis have been found that do show 

toxicity towards spider mites and house dust mites (Payne, Cannon, & Bagley, 1993; 

Payne, Cannon, & Ralph, 1994). It has been suggested to isolate the δ-endotoxin of these 

isolates and to formulate it as an acaricide. One may also transfer the gene, encoding for 

this specific δ-endotoxin into a crop plant in order to protect the crop against spider mite 

infestations. 

An interesting discovery is the isolation of a B. thuringiensis strain from dead 

twospotted spider mites, T. urticae (Jung, Mizuki, Akao, & Côte, 2007). In 

sporulating cultures of the bacterium, roughly spherical parasporal inclusion bodies 

are formed. This crystalline body is composed of at least two polypeptides of 86 and 

79 KDa. The crystal is not toxic to the twospotted spider mite, but after cleavage 

with trypsin, it is cytocidal to some human cancer cells. 

In Table 1, a list is given of bacteria that have been isolated from mites. We realize 

that this list may not be complete, but we have tried to limit the list to bacteria that show 

pathogenicity towards mites. Many species of bacteria may be isolated from mites (and 

other organisms): in many instances, these may not appear to be pathogenic. 

Aksoy, Ozman-Sullival, Ocal, Celik, and Sullivan (2008) studied the effect of 

Pseudomonas putida biotype B on the twospotted spider mite T. urticae. The 

bacterium had been isolated from greenhouse soil in Turkey and was tested on newly 

emerged, copulated females. The authors observed a strongly reduced egg production 

and no hatching of the eggs was noted. The results showed that the bacterium may be 

very effective in causing mortality in T. urticae populations. Further research is 

required to find out whether this organism may be developed to a microbial miticide. 

The predatory mite Phytoseiulus persimilis has been mass cultured for several 

decades for the biological control of spider mites in various field and glasshouse crops. 

This predator species is very important in integrated pest control programs and has 

stimulated research on predator-prey interactions and foraging behavior. It has been 

shown in several instances that adult female predatory mites are attracted to volatiles that 

are emitted by plants infested by prey. This emission of volatiles by the plant after 

herbivore attack is apparently a defense mechanism against herbivorous mites. Schütte 

(2006) noticed a change in response to prey-induced plant volatiles in a laboratory 

colony of P. persimilis. This population showed a lower attraction to these volatiles than 

other populations of the predator. It could be demonstrated that the change in behavior is 

caused by the involvement of a bacterium. Transmission of the bacterium occurs through 

feces and debris. There is no evidence that vertical transmission (from one generation to 

the next) occurs. The bacterium could be isolated and was described as Acaricomes 

phytoseiuli (Pukall, Schumann, Schütte, Gols, & Dicke, 2006). Comparative analysis of 

the 16S rDNA sequence revealed that it belongs to the Micrococcaceae, and that it is

256 


related to the soil bacterium Arthrobacter globiformis, to A. rissicus, a bacterium 

originally isolated from air in the Russian space laboratory and to Renibacterium 

salmoninarum, the causal agent of kidney disease in salmon. The bacterium clearly 

affects the effectiveness of P. persimilis as biological control agent as infected mites 

show a lower response to the volatiles emitted by the plant after herbivorous attack. At 

this moment, there are no signs that the disease is present in commercial populations of 

P. persimilis, nor is it widespread in laboratory populations of this predator. 

Table 1. Bacterial infections in mites. 

Species Mite host Mite family References 

Bacillus 

thuringiensis 

Spider mites 

House dust mites 

Tetranychidae 

Pyroglyphidae 

Payne et al. (1993, 1994) 

B. thuringiensis Tetranychus urticae Tetranychidae Jung et al. (2007) 

B. thuringiensis 

var. israelensis 

Dermatophagoides 

pteronyssinus 

Pyroglyphidae Saleh et al. (1991) 

B. thuringiensis 

var. tenebrionis 

Metaseiulus occidentalis Phytoseiidae Chapman and Hoy (1991) 

B. sphaericus Dermatophagoides 

pteronyssinus 

Pyroglyphidae 

Saleh, Kelada and Shader 

(1991) 

Bacteroidetes Metaseiulus occidentalis Phytoseiidae Hoy and Jeyaprakash (2008) 

Enterobacter Metaseiulus occidentalis Phytoseiidae Hoy and Jeyaprakash (2008) 

Pseudomonas 

putida 

Acaricomes 

phytoseiuli 

Tetranychus urticae Tetranychidae Aksoy et al. (2008) 

Phytoseiulus persimilis Phytoseiidae Pukall et al. (2006). 

Rickettsia sp. Metaseiulus occidentalis Phytoseiidae Hess and Hoy (1982) 

Vatacarus ipoides Trombiculidae Thomas and Poinar (1973) 

Rickettsiella 

phytoseiuli 

Phytoseiulus persimilis Phytoseiidae Šut’áková (1988) 

Wolbachia Bryobia sp. Tetranychidae Weeks (personal 

communication) 

Eutetranychus orientalis Tetranychidae Breeuwer and Jacobs (1996) 

Oligonychus biharensis Tetranychidae Breeuwer and Jacobs (1996) 

Tetranychus yusti Tetranychidae Breeuwer and Jacobs (1996) 

Tetranychus kanzawai Tetranychidae Breeuwer and Jacobs (1996) 

Gomi, Gotoh, and Noda (1997)


257 

Table 1 Continued 

Tetranychus 

neocaledonicus 

Tetranychidae Breeuwer and Jacobs (1996) 

Tetranychus turkestani Tetranychidae Breeuwer and Jacobs (1996) 

Tetranychus quercivorus Tetranychidae Gotoh, Abe, Kurihara, and 

Suzuki (1995) 

Tetranychus urticae Tetranychidae Breeuwer and Jacobs (1996) 

Tsagkarakou, Guillemaud, 

Rousset, and Navajas (1996) 

Metaseiulus occidentalis Phytoseiidae Johanowicz and Hoy (1966) 

Breeuwer and Jacobs (1996) 

Neoseiulus barkeri Phytoseiidae Breeuwer and Jacobs (1996) 

Neoseiulus bibens Phytoseiidae Breeuwer and Jacobs (1996) 

Phytoseiulus persimilis Phytoseiidae Steiner (1993) and Breeuwer 

and Jacobs (1996) 

Cardinium sp. 

Brevipalpus phoenici 

Brevipalpus californicus 

Euseius finlandicus 

Neoseiulus californicus 

Metaseiulus occidentalis 

Tenuipalpidae 

Tenuipalpidae 

Phytoseiidae 

Groot and Breeuwer (2006) 

Chigira and Miura (2005) 

Enigi and Schausberger 

(2007) Hoy and Jeyaprakash 

(2008) 

Spiroplasma 


Dermanyssus gallinae 

Tetranychidae 

Dermanyssidae 

Enigi and Schausberger (2007), 

De Luna, Valente Moro, Guy, 

Zenner, and Sparagano (2009) 

Serratia 

marcescens 

Metaseiulus occidentalis Phytoseiidae Lighthart, Sewall, and 

Thomas (1988) 

Mite and also tick species are frequently infected with intra-cellular 

microorganisms (Šut’áková, 1988, 1994; Steiner, 1993; Munderloh & Kurtti, 1995; 

Bjørnson et al., 1997) These microorganisms have been placed into the family 

Rickettsiaceae within the class α-Proteobacteria. The family Rickettsiaceae (or 

Rickettsia-like organisms) consists of three tribes: Rickettsieae, Ehrlichieae and 

Wolbachieae (Weiss & Moulder, 1984). Representatives of these tribes have a number 

of features in common: they are obligate intracellular gram-negative bacteria naturally 

found in arthropod hosts, they multiply inside eukaryotic cells and are often 

surrounded by multiple membranes. Some are also capable of infecting humans and 

other vertebrates and are frequently pathogenic in these secondary hosts They often 

cause severe diseases such as spotted fever, typhus and scrub typhus (Hayes & 

Burgdorfer, 1989). A good classification of these organisms has been hampered by the 

fact that classical microbiological identification tools cannot be used because of their

258 


obligate intracellular lifestyle. Since a number of years, tools have become available to 

sequence DNA of organisms. Sequence information on 16S rDNA genes has revealed 

interesting aspects of the order Rickettsiales, including their phylogeny. For additional 

information see Van der Geest et al. (2000). 

The best studied group of rickettsia are those that are vectored by ticks, as they 

often cause disease in vertebrates and are therefore of great medical and veterinary 

importance. In plant-inhabiting mites, rickettsia-like infections have mainly been 

observed in microscopic surveys (Šut’áková, 1988, 1994; Hess & Hoy, 1982; 

Steiner, 1993; Munderloh & Kurtti, 1995; Bjørnson et al., 1997). They are described 

as intracellular microbes often localized in the reproductive tissue of their host, but 

no data are available on their possible effect on mites. 

Hess and Hoy (1982) studied diseased laboratory colonies of the predatory mite 

Metaseiulus occidentalis more comprehensively, as these colonies produced only 

few eggs and often died out. Two different pathologies could be discerned. Some 

adult females were plump in appearance and had cream- to pink-colored plugs 

excreting from their rectum. Such females rarely produced eggs, although they 

appeared gravid. Immatures and males seldom showed this plug. The second 

condition affected both females and juveniles. These females failed to lay eggs and 

immatures often died, in particular during molting. Two forms of Rickettsia-like 

organisms were described, based on structure of the cell wall and the presence of 

cytoplasmic inclusions. Type A was observed in all mites examined, while type B 

was present in approximately two-thirds of the mites investigated. The Type A 

organisms were small, ovoid and 0.75 μm in length and 0.5 μm in width, with a 

trilaminar membrane of 7 nm thick, while Type B was rod-shaped, and measured 0.5 

μm in width and 2 μm in length. The Type A organisms were located intracellularly, 

singly or in groups of two or three in all tissues except ovarian and nervous tissue. 

The Type B organisms were both inter-and extracellular within membrane-bound 

vacuoles of cells that are similar in structure to mycetomes in insects. For a more 

detailed description is referred to Hoy and Jeyaprakash (2008). 

Since the mid-1990s, molecular screening for intracellular microorganisms is 

possible. This has resulted in the discovery of Wolbachia in tetranychid and 

phytoseiid mites (e.g. Gotoh et al. 1995; Gotoh, Gomi, & Nagata, 1999; Gotoh, 

Sugasawa, & Nagata, 1999; Breeuwer & Jacobs, 1996; Johanowicz & Hoy, 1996; 

Tsagkarakou et al., 1996). Probably all Rickettsia-like organisms that have been 

reported in the early microscopic surveys are members of the genus Wolbachia 

belonging to the family Rickettsiaceae. These bacteria are parasites of the 

reproductive system of mites and insects and cause many unusual effects in their 

hosts, such as parthenogenesis (infected females produce only females), male killing 

(male embryos die while female embryos develop into adults), feminization 

(infected male embryo’s develop into females) and cytoplasmic incompatibility. 

Wolbachia is a bacterium that is vertically transmitted to the next generation 

through the females. It modifies host reproduction in several ways in order to 

enhance its own spread (Weeks & Breeuwer, 2001). It induces parthenogenesis in 

the spider mite Bryobia praetiosa, causing males not to be produced. This is to the 

advantage of the bacterium, as only females are able to transmit the pathogen to the


259 

next generation. Probably over 1 million species of insects are infected, and 

infection rates in other taxa of arthropods may be similar. 

Van Opijnen and Breeuwer (1999) showed that Wolbachia can induce 

cytoplasmic incompatibility in the arrhenotokous 1 twospotted spider mite 

Tetranychus urticae between uninfected females and infected males. 

Cytoplasmic incompatibility is expressed through a male-biased sex ratio and 

low hatchability of eggs. It could be suppressed by removing Wolbachia from 

spider mites reared on a diet with antibiotics. The authors also demonstrated that 

heat treatment (32° C.) can eliminate Wolbachia from infected mites. It was 

shown that 71% of the mites were “cured” after being reared for four 

generations at 32°C. The infection could be completely eliminated by keeping 

the mites for 6 generations at 32°C. 

In a recent study Hoy and Jeyaprakash (2008) studied M. occidentalis females 

with large anal plugs. These females were collected from crowded laboratory 

colonies. The authors used 16S PCR primers to amplify the bacterial DNA and 

subsequently cloned and sequenced the products. It was remarkable that only 

bacteria were found that could also be detected in “healthy” females, viz. Wolbachia, 

Cardinium, an undescribed species of Bacteroidetes and an Enterobacter species. 

The authors assumed that stress could increase the titer of one or more 

endosymbionts which may lead to “disease”. The authors cite the statement of Dale 

and Moran (2006) that “as more cases of chronic bacterial infection are 

characterized, the distinction between pathogenesis and mutualism has become 

increasingly blurred. Infection by a particular bacterium may be beneficial to a host 

under circumstances but harmful in other hosts or environments” Another 

interpretation for the occurrence of the disease in M. occidentalis is that the predator 

obtains Rickettsia-like organisms from its food. Rickettsia-like organisms have been 

detected in twospotted spider mites. However, there is no conclusive evidence that 

the predator obtains the endosymbionts from its prey (Hoy & Jeyaprakash, 2008). 

Groot and Breeuwer (2006) showed the presence of the symbiont Cardinium in 

the thelytokous 2 mite species Brevipalpus phoenici. Cardinium spp. belong to the 

Flexibacteraceae (Phylum: Bacteroidetes; Class: Sphingobacteria). It was 

demonstrated that Cardinium induces thelytoky by feminizing unfertilized haploid 

eggs. Isofemale lines were set up and in some of these lines, males were produced 

by only very young daughters, while older females produce daughters exclusively. 

That a bacterium was involved was apparent from the fact that a treatment with 

antibiotics resulted in an increased number of male progeny. The presence of 

Cardinium was also shown in B. californicus (Chigira & Miura, 2005). Tetracyclinetreated 

females produced many male progeny while untreated females produced 

only female progeny. This is an indication that B. californicus is feminized by 

Cardinium. Comparison of infected females with uninfected males and other closely 

related species, revealed that Cardinium does not have a negative effect on the 

fitness of B. californicus. The bacterium has also been found in a population of 

1 Arrhenotokous: capable of producing male offspring only. 

2 Thelytokous: capable of producing female offspring only.

260 


Eotetranychus suginamensis in Japan (Gotoh, Noda, & Ito, 2006). One species of 

spider mite, Eotetranychus pueraricola harbored both Cardinium and Wolbachia, 

but these symbionts seemed to have no effect on the reproduction of the host. 

Cardinium has also been found to play a role in insect species, e.g. Encarsia sp. 

Cardinium is also present in field populations of the predatory mites Euseius 

finlandicus and Neoseiulus californicus and the spider mite Eotetranychus uncatus 

(Enigi & Schausberger, 2007). The endosymbionts has also been detected in the 

poultry red mite Dermanyssus gallinae (De Luna et al., 2009). 

Another genus of endosymbionts is the genus Spiroplasma. This genus belongs 

to the family Spiroplasmataceae, class Mollicutes, phylum Firmicutes. These 

bacteria are fastidious organisms which means that they can only been grown on rich 

nutrient media. Spiroplasma has been shown to kill males of Danaus chrysippus 

(Lepidoptera) and also of other insect species. Interspecific transmission of 

Spiroplasma poulsonii, a male-killing symbiont has been demonstrated between 

Drosophila sp. and Macrocheles sp., an ectoparasitic mite that feeds on the 

hemolymph of Drosophila (Jaeniki, Polak, Fiskin, Helou, & Minhas, 2007). Enigi 

and Schausberger (2007) showed the presence of Spiroplasma in the twospotted 

spider mite, but its effect on reproduction and other biological parameters is not yet 

known. Spiroplasma has also been detected in the poultry red mite Dermanyssus 

gallinae (De Luna et al., 2009). 

The ecological implications of modification of reproduction in herbivorous and 

predatory mites by intracellular symbionts is an interesting field of study. It will be 

clear that such modifications will have a great impact on the development of mite 

populations. 

4. DISEASES CAUSED BY FUNGI 

The Kingdom Fungi is a monophyletic assemblage which comprises at present four 

phyla: Chytridiomycota, Zygomycota, Basidiomycota and Ascomycota. In addition, 

there is a group called the Deuteromycetes (or Fungi Imperfecti), fungi of which no 

sexual stage is known. In the past, many parasitic fungi were classified in this group, 

but were reclassified after the sexual stage had been discovered. Most of these 

“reclassified” fungi belong to the Ascomycota. Nucleotide sequence analysis also 

suggests that the majority of these fungi belong to the Ascomycota. A large number 

of fungi capable to infect arthropods are found in the Deuteromycetes. 

Chytridiomycota and Zygomycota share common features, in particular the 

absence of cross walls (septa) in their hyphae. The Chytridiomycota (chytrids) 

represent a primitive group of aquatic fungi. Chytrids have gametes that are mobile 

by means of flagella. No chytrids are known that infect mites. 

Zygomycota are characterized by the formation of zygospores. These sexual 

spores are not contained within a specialized fruiting body or sac, but are unenclosed 

(or naked) between their parental hyphae. The haploid nuclei at the end of two 

hyphae fuse to a diploid zygote. This zygote undergoes immediately meiosis to form 

haploid cells that develop into zygospores. 

Ascomycota are also called “sac fungi” as their sexual spores (ascospores) are 

enclosed in tube-like sacs, known as asci. The formation of ascospores is similar to


261 

that of zygospores, but the spores are not naked but contained within asci. 

Ascomycota have cross walls in their hyphae. 

Basidiomycota are also known as the “club fungi”. Their sexual spores are 

formed on often very complex fruiting bodies called basidia. This group of fungi 

possesses also septa inside their hyphae. 

4.1. Zygomycota 

In this phylum, only the order Entomomophthorales (meaning insect destroyers) 

(class Zygomycetes) contains species that are pathogenic for Arthropoda. These 

fungi are mainly obligatory pathogens of insects and other arthropods, often with a 

restricted host spectrum. However, some species are parasitic on desmids (green 

algae) or fern prothalli while other species may be saprophytic on plant debris 

(Moore-Landecker, 1996). Hosts that are infected by fungi of this group are usually 

not killed before all available nutrients have been utilized, in contrast to, e.g. 

Deuteromycetes infections where mycotoxins often cause the death of the host prior 

to the complete utilization of food reserves. Hajek (1997) assumed that the complete 

utilization of the live host by the fungus seems to be consistent with the obligate 

nature of this group of fungi. 

As mentioned above, Zygomycetes are characterized by their sexual 

reproduction, the so-called zygospore formation, usually inside the parasitized host. 

Zygospores bud laterally from conjugation bridges between gametangia 3 (hyphal 

bodies). These thick-walled, dark-colored spores are also called resting spores and 

may germinate to produce conidiophores with conidia attached. Other types of 

resting spores are chlamydospores, thick-walled, nonsexual spores originating from 

transformed hyphal cells, and azygospores that may arise from parthenogenetic 

development of hyphal bodies (short segments of mycelium inside the host). 

Azygospores may also be the result of budding of chlamydospores, or they may be 

formed at the tip of hyphae that arise from chlamydospores or hyphal bodies. 

Resting spores (Fig. 1) seem to aid the fungus in surviving unfavorable conditions, 

e.g. periods of drought. Conditions under which resting spores germinate are not 

well-understood. 

More common is the formation of sporangiospores or ballistospores. These 

asexual spores are nonmotile and are formed within a sac-like structure, the 

sporangiole. Under nearly saturated conditions, these spores (by most mycologists 

called: primary conidia) are forcibly discharged from the spore bearing structure 

(sporangiophore, conidiophore). Primary conidia are often sticky due to the presence 

of a mucous substance causing them to adhere to a substrate after they have been 

released. The conidia may either form hyphae directly that may infect a new host or 

form secondary conidia. 

Six families are recognized within the Entomomophthorales; pathogens of 

arthropods are mainly found in the Entomophthoraceae, Neozygitaceae and 

Ancylistaceae. These families are recognized on the basis of nuclear characters (size, 

3 A single-celled structure producing gametes (sex cells) or gametic nuclei.

262 


number, stainability), mode of formation of resting spores, and mechanism of 

discharge of primary conidia. 

Figure 1. Resting spores of Neozygites tanajoae in the cassava green mite 

Mononychellus tanajoa. Photograph courtesy of Dr. Fabien C.C. Hountondji. 

Entomophthoraceae are obligate pathogens of arthropods. In this family, primary 

conidia are released in a cannon-like manner when the conidiophore ruptures at the apex. 

The conidium is actually a bud at the apex of the conidiophore that is filled with 

protoplasm from the conidiophore. When the conidium is fully developed, both 

conidium and conidiophore absorb water quickly under humid conditions. The osmotic 

pressure is larger in the conidium than in the conidiophore and this fact results in the 

forcible discharge of the conidium. When the spore lands on a suitable host, it may infect 

the host after germination. These primary conidia may form secondary conidia if landed 

on a non suitable substrate. A well-known example is Entomophthora muscae, a species 

capable to infect flies. Mites infecting species are known in the genus Tarichium. Of 

species of this genus, only resting spores are known and species determination is largely 

based on the shape and size of the resting spores. Tarichium spp. have been isolated in 

soil samples from several species of mites, in many cases Oribatidae (e.g. Bałazy & 

Wiśniewski, 1982, 1984). 

Neozygitaceae are obligate pathogens of insects (mainly Homoptera) and mites. They 

release primary conidia that germinate to form smaller secondary conidia with an adhesive 

haptor on long, thin conidiophores. The resting spores are often dark-colored and 

ornamented on the outside wall. They possess two pores and are formed inside the hosts. 

Ancylistaceae contains a number of representatives that may not only infect 

arthropods, but also vertebrates. For example, Conidiobolus coronatus causes 

serious infectious of mucous membranes of humans and other vertebrates (Maiti et 

al., 2004). Other species in this family are found in the soil and are often 

saprophytic. Primary conidia are forcibly discharged towards a light source and 

germinate to form secondary conidia that usually have the same shape as the primary 

conidia. The secondary conidia are either forcibly discharged or discharged 

passively from long slender conidiophores.


263 

4.1.1. Course of Infection 

Entomophthoralean fungi usually penetrate their host through the cuticle by means 

of a germ tube that is formed by the conidium. Mite infecting species are mainly 

found in the Neozygitaceae. The primary conidium is released from the 

conidiophore and forms on top of a slender tube a much smaller secondary 

conidium, called capilliconidium. The capilliconidium is considered to be the 

infectious propagule. When landed on a suitable host, it penetrates through the 

cuticle by means of a newly formed germ tube (Fig. 2). After penetration, mycelium 

is formed within the body cavity of the host that fragments into a number of smaller 

segments, the hyphal bodies. Hyphal bodies are the propagative units and multiply 

by budding and by undergoing fission. In addition, rhizoids may be formed: sterile 

hyphae, often branched, that perforate the ventral side of the host and attach the host 

to the substrate. The infected host becomes in this way fixed to the substrate, also 

after its death. Favorable conditions (high relative humidity) allow the formation of 

conidiophores that grow through the cuticle of the host. On top of these structures, 

conidia are formed that form a halo around the dead host after discharge from the 

conidiophores. The spores have a mucous substance on the outside and stick to the 

substrate on which they have landed. They may be picked up by new, uninfected 

hosts. A high relative humidity (near saturation point) is required at two points in the 

course of the disease: germination of the spores needs a high relative humidity, but 

also sporulation requires humid conditions. 

Figure 2. Capilliconidium of a Neozygites sp. on a leg of a spider mite 

Photograph: Leo P.S. van der Geest.

264 


The presence of rhizoids is an important property of the fungus for a successful 

transmission of the disease to a new host: the dead host (mummy) remains fixed to 

the plant surface and does not fall on the soil. In this way, chances for a successful 

transmission are increased. 

The formation of resting spores is an interesting phenomenon. Sometimes, 

resting spores are present in large numbers. It is assumed that they may assist the 

fungus to overcome poor favorable conditions, such as extreme periods of drought. 

However, we still know very little about the role of resting spores and the conditions 

under which they germinate are poorly understood. The fungus may also survive 

unfavorable conditions in other manners. Klingen, Wærsted, and Westrum (2008) 

showed that Neozygites floridana may survive cold winter periods in the form of 

hyphal bodies inside hibernating females of T.urticae. 

Most entomophthoralean fungi are difficult to culture in artificial culture media. 

For mass production, it is often necessary to use live host. Species that can be 

cultured in artificial media have usually a broad host spectrum. On the other hand, 

species with a restricted host range can hardly be grown outside their host, although 

some progress have been made with very complex culture media. Entomophthorales 

observed in mites are given in Table 2. 

Table 2. Entomophthoralean fungi infecting mites and their hosts. 

Fungus species Mite species Mite family References 

Not identified 

Entomophthoralean 

species 

Arctoseius sp. 

Macrocheles 

peregrinus 

Pergamasus 

crassipes 

Tetranychus 

desertorum 

Arctoseiinae 

Macrochelidae 

Parasitidae 

Tetranychidae 

Bałazy and Wiśniewski 

(1989) 

Milner (1985) 

Milner (1985) 

Walter (1999) 

Resting spores of 

Entomophtoralean 

species 

Agistemus 

Asca sp. 

Amblyseius 

igarassuensis 

Stigmaeidae 

Ascidae 

Phytoseiidae 

Van der Geest, De Moraes, 

Navia, and Tanzini (2002) 

Basidiobolus sp. Tetranychus urticae Tetranychidae See: Chandler et al. (2000) 

Conidiobolus sp. Bryobia sp. Tetranychidae Bałazy, Mietkiewski, 

Tkaczuk, Wegensteiner, 

and Wrzosek (2008) 

Conidiobolus 

brefeldionis 

Tyrophagus 

perniciosus 

Acaridae See: Chandler et al. (2000) 

Conidiobolus 

chapowski 

Pergamasus Parasitidae See: Chandler et al. (2000)


265 


Conidiobolus 

coronatus 

Dendrolaelaps sp. Digamasellidae Bałazy et al. (2008) 

Conidiobolus 

obscurus 

Phytoseiulus 

persimilis 

Mononychellus 

tanajoa 

Tetranychus 

bimaculatus 


Phytoseiidae 

Tetranychidae 

See: Chandler et al. (2000) 

Nyiira (1982) 


Conidiobolus 

thromboides 


Eotetranychus 

sexmaculaturs 

Mononychellus sp. 

Mononychellus 

tanajoa 


Tetranychus evansi 

Tetranychus 

pacificus 

Tetranychus 

tumidus 

Tetranychus 

turkestani 

Vatacarus sp. 

Tetranychidae 

Trombiculidae 


Selhime and Muma (1966) 

Bartkowski Odindo, and 

Otieno (1988) 

Delalibera, Sosa Gomez, 

De Moraes, De Alencar, 

and Farias Araujo (1992) 

Fisher (1951) 

Humber, De Moraes, and 

Dos Santos (1981) 

Steinhaus and Marsh (1962) 


Carner and Canerday 

(1968) 


Erynia 

phalangicidae 

Pergamasus sp. Parasitidae Bałazy and Wiśniewski 

(1984) 

Zoophthora radicans Tetranychus urtcae Tetranychidae See Chandler et al. (2000) 

Neozygites sp. 

Euseius citrifolius 

Alaskozetes 

antarcticus 

Phytoseiidae 

Ameronothridae 

Furtado, De Moraes, and 

Keller (1996) 

Bridge and Worland (2004, 

2008) 

Neozygites 

abacaridis 

Abacarus hystrix 

Aculodes mckenziei 

Aculodes sp. 

Aculus fockeui 

Eriophyidae 

Miętkiewski and Bałazy 

(2003) 

Bałazy, Mietkiewski, 

Tkaczuk, Wegensteiner, 

and Wrzosek (2008)

266 



Neozygites acaricida 

Halotydeus 

destructor 

Penthaleus major 

Eupodidae 

Penthaleidae 

See Chandler et al. (2000) 

Neozygites acaridis 

Halotydeus 

destructor 

Penthaleus major 

Eupodidae 

Penthaleidae 

James (1994) 

Neozygites 

floridana 

Bryobia sp. 

Eotetranychus 

banksi 

Tetranychidae 

Miętkiewski, Balazy, and Van 

der Geest (1993) 

Weiser and Muma (1966) 

Oligonychus 

gossypii 

Yaninek, Saizonou, Onzo, 

Zannou, and Gnanvossou (1996) 

Oligonychus 

hondoensis 

Nemoto and Aoki (1974) 

Dick, Buschman, and Ramoska 

(1992) 

Fisher (1951) 

Rameseshiah (1971) 

Oligonychus 

pratensis 


Saba (1971) 

Smith and Furr (1975) 

Tetranychus ludeni 

Tetranychus tumidus 


Neozygites 

tanajoae 

Mononychellus 

tanajoa 

Tetranychidae 

Delalibera, Hajek, and Humber 

(2004) 

Oligonychus gossypii 

Neozygites 

tetranychid 

Tarichium 

acaricolum 

Tarichium 

azygosporicum 

Tarichium 

distinctum 

Tetranychus urticae Tetranychidae Weiser (1968) 

Pergamasus sp. Parasitidae Bałazy and Wiśniewski (1984) 

Pergamasus sp. Parasitidae Bałazy, Wiśniewski, and 

Kaczmarek (1987) 

Pergamasus sp. Parasitidae Bałazy et al. (1987) 

Tarichium 

hyalinum 

Tarichium 

monokaryoticum 

Tectocepheus 

velatus 

Tricouropoda 

szczecinensis 

Parasitidae Bałazy et al. (1987) 

Uropodidae Bałazy et al. (1987)


267 


Tarichium 

svalbardense 

Dinychus carinatus 

Pergamasus sp. 

Veigaia sp. 

Prodinychidae 

Parasitidae 

Veigaiidae 

Bałazy et al. (1987) 


(1984) 

Bałazy et al., 1987 

Tarichium 

obtusoangulatum 

Uropoda minima Uropodidae Bałazy and Wiśniewski 

(1984) 

Tarichium pusillum Pergamasus sp. Parasitidae Bałazy and Wiśniewski 

(1984) 

Tarichium 

sphaericum 

Trachyuropoda 

coccinea 

Trachyuropodidae 


(1984) 

Tarichium 

subglobosum 

Pergamasus sp. 

Uropoda minima 

Parasitidae 

Uropodidae 


(1984) 


(1984) 

Tarichium 

tenuisculpturatum 

Pergamasus sp. Parasitidae Bałazy and Wiśniewski 

(1984) 

Tarichium 

uropodinis 

Trachyuropoda 

coccinea 

Trachyuropodidae 


(1982) 

Tarichium 

verruculosum 

Celaenopsis sp. 

Unidentified 

Celaenopsidae 

Galumnidae 

Bałazy et al. (1987) 

4.1.2. Natural Entomophthoraceous Infections 

The first record of an entomophthoralean fungus infection in spider mites was 

observed by Fisher (1951) who noted adult mortality from 32 to 95% in populations 

of the citrus red mite Panonychus citri. The fungus was in particular prevalent 

during late summer and early autumn throughout the Florida peninsula. Weiser and 

Muma (1966) isolated the fungus later from the Texas citrus mite Eutetranychus 

banksi and described it as Entomophthora floridana. The fungus has since been 

reported from several other spider mites species: For example, it was observed in 

Tetranychus tumidis on cotton in the humid subtropical regions of Florida (Saba, 

1971), in T. evansi on tomato crops in Brazil (Humber et al., 1981), in T. ludeni 

on bean in India (Ramaseshiah, 1971), in Oligonychus hondoensis on cedar in 

Japan (Nemoto & Aoki, 1975) and in T. urticae on field corn in North Carolina, 

USA (Brandenburg & Kennedy, 1982). The fungus has also been reported in 

Poland on the twospotted spider mite T. urticae and on Bryobia sp. (Mieţkiewski 

et al., 1993). 

Keller and Wuest (1983) noted infections by Neozygites adjarica in T. urticae 

on bean in Switzerland, but later investigations showed that this fungus is identical 

to N. floridana; N. tetranychi, described by Weiser (1968) as a pathogen of the

268 


twospotted spider mite from a fruit orchard in Southern Bohemia, Czech Republic, is 

also considered to be a synonym of N. floridana (Keller, 1997). 

Bridge and Worland (2008) observed a Neozygites infection in the 

cryprostigmatic mite Alaskozetes antarcticus (Ameronothridae). This mite was 

collected at Rip Point, Nelson Island off the West coast of the Antarctic peninsula. A 

few specimens appeared to be infected by a fungus that was provisionally described 

as Neozygites cf. acaridis. The mite survives the harsh climatic conditions by 

lowering the freezing point by the accumulation of low molecular weight 

cryoprotective compounds such as glycerol, together with the removal or masking of 

ice-nucleating substances from its body. 

The introduction of the cassava green mite Mononychellus tanajoa into the 

cassava growing regions on the African continent has led to a comprehensive search 

for natural enemies of this pest. This has resulted in the isolation of a Neozygites sp. 

that is very specific for the cassava green mite in Venezuela by Agudela-Silva (1986) 

and later also in Brazil by Delalibera et al. (1992). The fungus is also known from the 

African continent. Originally, the fungus was considered to be identical to N. 

floridana, although it did show differences in, among others, its very restricted host 

spectrum and in the size of the conidia. Recently, the fungus has been described as N. 

tanajoae (Delalibera et al., 2004). It can be distinguished from N. floridana on the 

basis of 18S ribosomal DNA (rDNA) sequences, host range, nutritional requirement 

for growth in vitro, tolerances to low temperatures (4° C) and ability to withstand 

specific cryopreservation techniques. N. tanajoae isolates from Brazil and Africa have 

identical 18S rDNA sequences but they presented 5.7 and 9.94% pair wise distance 

from N. floridana isolates. N. tanajoae proved to differ sufficiently from other mitepathogenic 

fungi referred to as N. floridana to justify the description as a new species. 

4.1.3. Role of Neozygites floridana in the Field 

The role of Neozygites spp. in the field has been studied in a number of instances. 

Numerous examples show that Neozygites sp. may have a major impact on 

populations of spider mites in agricultural crops. Saba (1971) observed Neozygites 

floridana in populations of T. tumidus in cotton field in the humid subtropical part of 

Florida. A reduction of 220 spider mites per cotton leaf down to less than 1 spider 

mite was noted during a period of warm humid weather with heavy rainfall. This 

reduction could be mainly attributed to the presence of the fungus disease. Similar 

observations were made by others, e.g. Smith and Furr (1975) who established that 

Neozygites in the main factor that limits late-season population increases of T. 

urticae on cotton in the delta of the Mississippi and Carner (1976) who found the 

fungus throughout the states Georgia, South Carolina and Alabama. He considered 

Neozygites a very important factor in regulating spider mite populations in cotton. 

Treatment of crops with fungicides may affect the incidence of fungus disease 

in populations of spider mite: Brandenburg and Kennedy (1983) observed a lower 

proportion of spider mites infected by Neozygites in lima beans when the fungicide 

benomyl was applied. The fungicide did not affect sporulation of the pathogen, but 

seemed to have an effect on conidial germination and growth of the fungus.


269 

Immature stages of T. urticae are more susceptible to N. floridana than adult 

mites, while adult females are more susceptible to infection than adult males (Susilo 

Nordin, & Brown, 1994). The authors suggest than the thinner cuticle of the 

immature mites could be the cause that immature stages are more vulnerable to the 

fungus disease. That males are less susceptible to infection is probably due to the 

stronger cuticle of this sex compared to that of females. Males have to compete with 

other males for females which may have resulted in a tougher cuticle. On the other 

hand, females have a more elastic opisthosomal cuticle, needed for ovarial 

development and oviposition. The authors speculate that the cuticle of females might 

be thinner, or somewhat different in chemical composition. 

Infection by entomogenous fungi results from penetration of the fungus through 

the cuticle of the host by a combination of enzymatic and mechanical processes. 

Successful infection by a fungus depends largely on the effectiveness of various 

antifungal substances present in the host cuticle. The authors claim that differential 

susceptibility of different stages and sexes of mites can be attributed partially to the 

presence or absence of antifungal substances. This finding is in contrast with 

observations by Elliot (1998) on an epizootic of Neozygites tanajoae in the cassava 

green mite M. tanajoa in Brazil. Far fewer capilliconidia of the fungus were found 

on field-collected juveniles than on adult females, while the vast majority of killed 

mycosed mites were adult females. Elliot (1998) assumed that the limited movement 

of immature stages makes them less likely to pick up capilliconidia from the leaf 

surface. For additional information on the role of N. floridana in natural populations 

of spider mites is referred to Van der Geest et al. (2000). 

4.1.4. The Cassava Green Mite and Neozygites tanajoae 

The unfortunate introduction of the cassava green mite (GCM), M. tanajoa, from 

Latin America into East Africa during the 1970s led to a comprehensive search for 

natural enemies of this pest. The mite dispersed within 10 years across the cassava 

belt in Africa, threatening cassava production in vast areas of the continent 

(Yaninek, 1988). It was already clear from the beginning that chemical control of the 

CGM would be no option. Cassava is a marginal crop in Africa and the farmers 

would not be able to afford the cost of chemical control. Moreover, chemical control 

would result in an unacceptable environmental pollution in large parts of the 

continent. It was clearly understood that classical biological control would be the 

most desirable solution for the problem. Several predatory mites of the family 

Phytoseiidae were collected in various locations in Latin America and introduced 

into Africa. 

During the search for natural enemies, also a species of Neozygites was found, 

first in Venezuela (Agudela-Silva, 1986), later also in Brazil by Delalibera et al. 

(1992). The fungus has a very narrow host spectrum and does not infect other spider 

mites or predatory mites. The fungus, initially considered to be N. floridana, but 

later described by Delalibera et al., (2004) as Neozygites tanajoae, is considered a 

good candidate as biological control agent for the CGM in Africa, because of its 

high specificity (De Moraes & Delalibera, 1992). A drawback, however, is the fact

270 


that the fungus cannot successfully be grown on artificial media (Leite, Smith, De 

Moraes, & Roberts, 2000), which means that it should be released in the field in the 

form of fungus infected dead mites. A detailed study was therefore performed in 

order to gain information on the suitability of the fungus as biocontrol agent. In a 

series of experiments, Oduor, De Moraes, Yaninek, and Van der Geest (1995a), 

Oduor, Yaninek, Van der Geest, and De Moraes (1995b), Oduor (1995c), Oduor, De 

Moraes, Van der Geest, and Yaninek (1996a), Oduor, Yaninek, Van der Geest, and 

De Moraes (1996b), Oduor, De Moraes, Van der Geest, and Yaninek (1997a) and 

Oduor, Sabelis, Lingeman, De Moraes, and Yaninek (1997b) studied the biology of 

N. tanajoae and its effect on the CGM. They demonstrated that the production of 

primary conidia is affected by ambient humidity, temperature and photoperiod: 

production of conidia increased with higher temperatures between 13°C and 23°C, 

but no conidia production was obtained above 28°C. Also, germination of 

capilliconidia on cassava green mites is affected by exposure time, temperatures, 

ambient humidity and photoperiod. 

Infectivity of capilliconidia is lost after several days: only 3.5% of the spores 

germinate after a storage period of 10 days. It was also found that germination 

occurred at all temperatures studied (13–33°C), even at 13°C, more than 15% of the 

capilliconidia germinated. This is an indication that the minimum temperature for 

germination may still be lower. An interesting observation is also that more 

capilliconidia germinate at 18°C than at higher temperatures. Germination in the 

dark is considerably higher than in light, while this process is also greatly affected 

by ambient humidity. The fungus apparently sporulates under natural conditions 

early in the morning before sunrise when the temperature is still low and the relative 

humidity high. Primary conidia can then disperse and produce capilliconidia that 

wait on the leaf surface to be picked up by a suitable host. 

N. tanajoae cannot be mass produced in artificial culture media. Propagation 

needs to be performed in live mites, which is a laborious, and also expensive 

process. Storage of dead, non-sporulating infected mites (also called mummies) 

appears to be possible over prolonged periods of time in well-sealed plastic 

containers with cotton wool partially soaked in glycerol to establish a low humidity. 

In this manner, the fungus remains viable for periods of 6–7 months. 

The fungus causes significant reductions in cassava green mite populations in 

cassava fields in the State of Bahia, Brazil (Delalibera, De Moraes, & Sosa Gomez, 

1999), reaching infection levels up to 75% during the wet season. Elliot et al. (2000) 

conducted a 4-year study in cassava fields in a semi-arid region in northeastern 

Brazil. The authors found that the fungus had a significant effect on CGM 

populations, but results were not very consistent for the different years. The fungus 

was not found in live mites during dry periods and for that reason it was assumed 

that resting spores were the most feasible mechanism to survive these periods of 

drought. Resting spores were found in great numbers during an epizootic in 1995, but 

they were not found in epizootics in early and mid 1998. Elliot (1998) considered 

perennial survival in the field of the fungus in mummies highly improbable as 

experiments had demonstrated that no viable fungus could be detected in dead mites 

after 2 month of hot and dry storage, both in the field and in the laboratory. In a later 

report, Elliot, De Moraes and Mumford (2008) discussed results of an experiment in


271 

which they monitored a population of the CGM and its natural enemies in central 

Bahia. Despite the presence of very high levels of the predatory mite Neoseiulus 

idaeus, there was an overexploitation of the cassava plants by the cassava green 

mite, which led to a total leaf loss. A simple regression model predicted a potential 

epizootic by N. tanajoae, but at that time, no inoculum of the fungus was present. 

There could have been an epizootic after the CGM population crashed, but then 

there were no hosts present to infect. The study showed the ineffectiveness of the 

predator and the importance of a correct timing of the pathogen. The authors 

concluded that the fungus may be a useful addition to biological control in this 

system with another predator than N. idaeus. 

Yaninek et al. (1996) carried out a survey of fungi occurring in mites in the 

Republic of Benin, West Africa and found N. tanajoae in CGM and in 

Oligonychus gossypii. The fungus was present during the entire year, although 

the incidence of the disease was considerably greater in the wet season. 

Infection levels reached by the Benin strain were never as high as those of the 

Brazilian isolates where infection levels close to 100% may sometimes be 

reached. However, disease incidences in O. gossypii were about twice as high as 

in CGM. This species of mite is indigenous to Africa, in contrast to the cassava 

green mite. The N. tanajoae strains native to Africa are thought to be weakly 

pathogenic towards the CGM as they cause only low levels of mortality in CGM 

populations. 

Based on these studies, N. tanajoae pathotypes from Latin America were 

being considered as a biological control agent of the CGM in Africa. An 

international collaboration between the International Institute for Tropical 

Agriculture (IITA, Cotonou, Benin), Empresa Brasileira de Pesquisa 

Agropecuária (EMBRAPA, Brazil) and the University of Amsterdam (The 

Netherlands) was set up in order to guide the introduction and release of the 

fungus into Africa. An in vivo release procedure has been developed at the 

(IITA) as it is not yet possible to culture the fungus in artificial culture media. 

Field experimental releases were performed in order to test the possibility to 

induce the development of epizootics in the field (Hountondji, 2005). The in 

vivo release method consisted of the release of 1-day old infected mites on 

young leaves of with CGM infested cassava fields Two different Brazilian 

strains were released in Southeastern Benin, resulting in disease incidence levels 

of 34 and 26.5% respectively, while the maximum prevalence for a Beninese 

isolate was only 4.5%. The fungus is in the first site endemically present, but 

had never been found in northeastern Benin. Post-release monitoring in 

Southeastern Benin showed after 10 months the presence of the fungus in 3 out 

of 20 cassava field where the fungus had been released. In Northeastern Benin, 

epizootics were also observed with infection levels between 15 and 70%. An 

interesting observation is that infection levels were consistently higher in fields 

inoculated with Brazilian isolates compared to those inoculated with the 

Beninese isolates. 

The epizootics were especially observed during periods of hot days and cool 

nights with high relative humidity. The establishment of the Brazilian isolates at the 

release site could be confirmed. However, resting spores, believed to be essential for

272 


the survival of the fungus during dry periods were hardly found. Further studies will 

be needed to determine the suitability of the fungus as biocontrol agent of the CGM 

in Africa. 

Hountondji (2008) discussed the interactions within the cassava green mite- 

Neozygites tanajoae system. He states that most fungal pathogens lack the 

capacity to search for their hosts but that they have rather developed a sit-and-wait 

strategy. Field applications of N. tanajoae against the CRM has resulted in only 

limited success and for that reason, studies were conducted on the tritrophic 

interactions in the system. An interesting finding is that herbivores trigger the 

release of volatile chemicals (HIPV) that promotes sporulation of the fungal 

pathogen, whereas the host mites avoid the haloes of conidia. However, the mite 

does not avoid the pathogen when the fungus is inside the mummified cadaver. 

Mechanically damaged leaves produce also volatile, but these “green leaf 

volatiles” seem to delay sporulation. Hountondji (2005) speculates that a delay in 

the formation of conidia until the HIPV’s are produced is to the advantage of the 

fungus. The production of HIPV’s is a signal for the fungus that herbivores (hosts 

for the fungus) are present. 

4.2. Deuteromycetes 

The Deuteromycetes, also mitosporic or anamorphic fungi, and formerly called the 

Fungi Imperfecti, is a group of fungi of which no sexual stage is known. It is 

difficult to place these fungi in the fungus classification system, since this 

classification is mainly based on the mode of sexual reproduction. The majority of 

Deuteromycetes are probably the asexual stages of Ascomycota and Basidiomycota, 

with the largest number belonging to the Ascomycota. The approximately 20,000 

species (2,600 genera) of Deuteromycetes (or Deuteromycota) lack any common 

phylogenetic origin or relationship and have only been grouped together for the sake 

of convenience. Classification of Deuteromycetes is mainly based on morphological 

similarities. The criteria typically used are color, shape, size and septation of the 

conidia (whether the spores are unicellular, or made up of multiple cells). The effect 

of this classification is that unrelated fungi have been “lumped” together while 

possibly related fungi have been classified into different form-classes because of 

differences in the visual appearance of the spores. When the sexual stage 

(teleomorph) is discovered, the correct name of the fungus will be that of the 

teleomorph. 

A group in the Deuteromycetes is the form-class Hyphomycetes. These fungi 

have a mycelium but lack a sporocarp (structure in which spores are formed). The 

spores are borne on separate or aggregated conidiophores (stroma). We speak of a 

synnema when the conidiophores are united at the base and of a sporodochium when 

the hyphae are aggregated to a cushion-line structure on which the conidiophores are 

formed. Many of the spores of the Deuteromycetes have morphologically distinct 

features so that the spores of this group are some of the most easily identified. These 

fungi are also easily cultured so that more research has been conducted on this group 

of fungi than on many others.


273 

4.2.1. Hirsutella Infections in Mites 

A well-known genus in the Hyphomycetes is Hirsutella. Approximately 80 species 

have been described in this genus; most species are pathogenic to tropical 

invertebrates, some are pathogens of Acari, in particular of eriophyids. Teleomorphs 

of Hirsutella have been reported as Cordyceps and Torrubiella spp. (cf. Chandler 

et al., 2000). Hirsutella species observed in mites are given in Table 3. 

The first published report of a Hirsutella infection in an eriophyid goes back to 

1924: Speare and Yothers (1924) observed a sudden decimation of a large 

population of the citrus red mite (CRM) (Phyllocoptruta oleivora) on grapefruit in 

Florida. The population density of CRM was in June sometimes extremely high with 

5,000 mites on a single grapefruit, but soon after the maximum density had been 

reached, populations went down to almost zero. The authors were able to discern 

fungal hyphae in mite cadavers and also noted that disease incidence was much 

lower after application of a fungicidal copper spray. Fisher (1950) described this 

fungus later as Hirsutella thompsonii (Fig. 3). 

Figure 3. Epitremerus goniathrix (Eriophyidae), infected by Hirsutella sp. 

Photograph: Leo P.S. van der Geest. 

The conidia are the infective propagules of the fungus. They are formed on 

phialides (flask-like conidiophores) that taper into a long narrow neck, and produce 

usually only 1–3 conidia in a dense terminal sphere of slime. This gives the 

impression that only one spore on each phialide is produced (Fig. 4). The mucous 

coat facilitates adhesion of the spores to the host cuticle. Penetration of the fungus is 

usually through all parts of the host’s body, but in case of spider mites, it is usually 

through the legs. The fungi enter the host through the cuticle which is composed of 

about 30% chitin embedded in a protein matrix. Entomogenous fungi often produce 

proteases that may play a role in the early stages of penetration by exposing the 

chitin fibrils. Subsequently, chitinolytic enzymes are excreted that causes 

degradation of the fibrils into chains of glucose-N-acetyl of variable length.

274 


Table 3. Hirsutella species infecting mites and their hosts. 

Fungus species Mite species Mite family Reference 

Hirsutella sp. 

Amrineus cocofolius 

Epitremerus goniathrix 

Eriophyoidea Van der Geest et al. (2002) 

Mononychellus sp. 

Notostrix attenuata 

Tetranychidae 

Eriophyoidea 

Bartkowski et al. (1988) 

Van der Geest et al. (2002) 

Pronematus sp. Tydeidae Cabrera and McCoy (1984) 

Propilus syagris 

Retracus jonhstoni 

Eriophyoidea Van der Geest et al. (2002) 

Tarsonemus sp. Tarsonemidae Van der Geest et al. (2002) 

H. brownorum Mites in soil Humber (1992) 

H. gregis Abacarus hystrix Eriophyoidea Minter, Brady, and Hall 

(1983) 

Unidentified sp. Acaridae Miętkiewski, Bałazy, 

and 

Tkaczuk (2000) 

H. danubiensis Tetranychus urticae Tetranychidae Bałazy et al. (2008) 

H. haptospora Uropodina sp. Uropodoidea Humber (1992) 

Urobovella sp. Uropodoidea Miętkiewski et al. (2000) 

Unidentified species Parasitiformes Miętkiewski et al. (2000) 

H. kirchneri Abacarus hystrix Eriophyoidea Minter et al. (1983) 

Eutetranychus 

orientalis 

Tetranychidae 

Sztejnberg, Doron-Shloush, 

and Gerson (1997) 

Hemisarcoptes 

coccophagus 

Hemisarcoptidae Sztejnberg et al. (1997) 

Panonychus citri Tetranychidae Sztejnberg et al. (1997) 

Phyllocoptruta oleivora Eriophyoidea Cabrera and Dominguez 

(1987a) and Sztejnberg 

et al. (1997) 

H. necatrix Abacarus hystrix Eriophyoidea Minter et al. (1983) 

Tetranychus 

cinnabarinus 

Tetranychidae Sztejnberg et al. (1997)


275 


Dendrolaelaps cornutus Digamasellidae Miętkiewski et al. (2000) 

H. nodulosa Aceria guerreronis Eriophyoidea Cabrera and Dominguez 

(1987b) 

Phyllocoptruta oleivora Eriophyoidea Cabrera and Dominguez 

(1987a) 


latus 

Tarsonemidae 

Peña, Osborne, and Duncan 

(1996) 

Steneotarsonemus 

fragariae = 

Phytonemus pallidus 

Tarsonemidae Miętkiewski et al. (2000) 

H. rostrata Dendrolaelaps 

tetraspinosus 

Digamasellidae 


(1989) 

Proctolaelaps sp. Ascidae Bałazy and Wiśniewski 

(1989) 

H. thompsonii Abacarus hystrix Eriophyoidea Lewis, Heard, Brady, and 

Minter (1981) 

Acalitus vaccinii Eriophyoidea Baker and Neunzig (1968) 

Aceria cynodoniensis Eriophyoidea McCoy (1996) 

Aceria guerreronis Eriophyoidea Humber (1992) 

Aceria sheldonii Eriophyoidea McCoy (1996) and Sosa 

Gomez and Moscardi (1991) 

Aceria sp. Eriophyoidea McCoy and Selhime (1977) 

Aculops lycopersici Eriophyoidea In: Chandler et al. (2000) 

Calacarus heveae Eriophyoidea Tanzini, Alves, Tamai, De 

Moraes, and Ferla (2000) 

Colomerus 

novahebridensis 

Eriophyoidea 

Hall, Hussey, and Mariau 

(1980) 

Epitremerus goniathrix Eriophyoidea Van der Geest et al. (2002) 

Notostrix formosae Eriophyoidea Van der Geest et al. (2002) 

Phyllocoptruta oleivora Eriophyoidea Fisher (1950) 

Retracus elaeis Eriophyoidea Urueta (1980) 

Rhynacus sp. Eriophyoidea Cabrera, Caceras, and 

Dominguez (1987) 

Vasates destructor Eriophyoidea McCoy (1996)

276 




latus 

Tarsonemidae Peña et al. (1996) 

Vasates mckenzie Tarsonemidae Miętkiewski et al. (2000) 

Dolichotetranychus 

floridanus 

Tenuipalpidae Humber (1992) 

Eutetranychus banksi Tetranychidae McCoy and Selhime (1977) 

Eotetranychus 

sexmaculatus 

Tetranychidae McCoy and Selhime (1977) 

Eutetranychus 

orientalis 

Tetranychidae 

Gerson, Kenneth, and 

Muttath (1979) 

Mononychellus tanajoa Tetranychidae Yaninek et al. (1996) 

Panonychus citri Tetranychidae McCoy and Selhime (1977) 

Oligonychus gossypii Tetranychidae Yaninek et al. (1996) 

Tetranychus 

cinnabarinus 

Tetranychidae 

Cehrnin, Gafni, Mozes- 

Koch, Gerson, and 

Sztejnberg (1997) 

Oligonychus ilicis Tetranychidae Gardner, Oetting, and 

Storey (1982) 

Tetranychus urticae Tetranychidae Gardner et al. (1982) 

Tetranychus turkestani Tetranychidae In: Chandler et al. (2000) 

Trachyuropoda 

coccinea 

Trachyuropodidae Bałazy and Wiśniewski 

(1982) 

H. tydeicola Lorryia formosa Tydeidae Cabrera, see: Samson and 

McCoy (1982) 

Tydeus californicus Tydeidae Cabrera, see: Samson and 

McCoy (1982) 

Tydeus gloveri Tydeidae Samson and McCoy (1982) 

H. vandergeesti Amblyseius sp. 

Neoseiulus sp. 

Seiulus sp. 

Typhlodromus sp. 

Tarsonemus lacustris 

Phytoseiidae 

Tarsonemidae 

Bałazy et al. (2008)


277 

When grown in artificial cultures, a toxic protein is produced with a molecular 

weight of 15–16 kDa (Vey, Quiot, Mazet, & McCoy, 1993). This protein, hirsutellin 

A (HtA) is a heat stable, non-glycosylated protein with properties similar to 

ribosome-inhibiting proteins. It is a single chain polypeptide that is composed of 130 

amino acids (Herrero-Galán et al., 2008). HtA shows ribotoxin activity and interacts 

with phospholipid membranes. When administered orally or by injection, it causes 

strong cytotoxic effects against several insect species (pycnosis of the nucleus and 

lesions in the midgut, malpighian tubules, hypodermis, fatbody, hemocytes, muscles 

and silk glands of larvae). The toxin affects a wide range of arthropods, including 

mites. It was tested against the citrus rust mite Phyllocoptruta oleivora, the natural 

host of the fungus, where it caused considerable mortality among adult mites, while 

oviposition of females was lowered prior to their death (Omoto & McCoy, 1998). 

Maimala, Tarter, Bouciar, and Chandrapatya (2002) studied 162 strains of H. 

thompsonii and found that more than half of these strains produced the toxin. They 

were able to characterize the gene encoding for the toxin, but the presence of the 

gene could not be associated with enhanced insecticidal properties of the fungus. 

Other toxins have also been reported to be produced by Hirsutella sp., such as 

hirsutellin B and phomalactone. It is not within the scope of this manuscript to 

discuss these products further. 

H. thompsonii regularly causes epizootics in populations of P. oleivora under natural 

conditions in Florida and affects both nymph and adult stages. The asexual spores are 

produced outside the host body on the plant surface. Conidia germinate under favorable 

conditions (high relative humidity) and enter the body by means of a germ tube. After 

penetration, a ramifying growth of the fungus can be discerned. The fungus erupts after 

Figure 4. Phialid of Hirsutella thompsonii with conidia. The globular structure on 

top of the phialid may hold several conidia which are contained in a slimy sheath. 

Photograph courtesy of Dr. Marcel R. Tanzini.

278 


death of the mite through the cuticle and forms new spores. It takes about 4 h for a spore to 

penetrate the cuticle of the host, while time from infection to formation of new spores is 

around 4 days at 25–30°C (Fig. 4). 

The fungus can easily be grown on artificial media and this property together with its 

high infective potential towards the citrus rust mite (CRM) has led to research aimed at the 

development of the fungus as biological control agent. Large-scale laboratory and industrial 

production methods have been developed for the production of mycelial and conidial 

preparations (McCoy, Hills, & Kanavel, 1975; McCoy, 1981). It was planned to introduce 

the fungus early in the season as a prophylactic to reduce outbreaks of the CRM. 

Commercial production of conidial preparation in the USA was developed in 1975–1976 

by Abbott Laboratories and full registration was received for a mycoacaricide for the 

control of eriophyids on citrus under the name Mycar TM . Several hundreds of kilograms 

were sold of the product but commercial production was discontinued in 1985 as too many 

factors affected the stability and reliability of the acaricide. 

Interest in the production of H. thompsonii based acaricides for use against eriophyids 

continued in other countries even after the production of Mycar TM in the USA was 

discontinued. Experiments have been conducted in several countries, e.g. Brazil, Argentina, 

Mexico and Sri Lanka, but these studies have yet not led to a commercial biological control 

product. More successful were studies in India where the coconut mite, Aceria (Eriophyes) 

guerreronis, is a major constraint to coconut farming in India, the third largest producer of 

coconuts in the world. Biological control has been considered for a long time, despite the 

availability of other control methods, including chemical and botanical pesticides and 

nutrition-based cultural methods (Sreerama Kumar & Singh, 2001; Sreerama Kumar, 

2006). Research has resulted in the identification of the most infective mite pathogen, 

H. thompsonii, as important regulator of the coconut mite (Fig. 5). Further research had led 

to the production of a biological acaricide, Mycohit TM , with a mixture of mycelium 

Figure 5. Aceria (Eriophyes) guerreronis infected by Hirsutella thompsonii. 

Photograph courtesy of Dr. P. Sreerama Kumar.


279 

and conidia as active ingredients. In a series of field experiments, it was shown that 

Mycohit TM is a very effective acaricide that brings down the population to over 90%. For 

the application of the product, youngsters are hired that climb into the trees in order to 

carry out the applications (Figs. 6 and 7). 

Further research has led to the development of Mycohit-M TM , a preparation that 

contains only mycelium (Sreerama Kumar & Singh, 2008). The authors also studied 

the effect of several adjuvants (glycerol, yeast extract powder and dehydrated malt 

extract) on the growth and spore forming of the latter preparation. In the presence of 

these adjuvants H. thompsonii biomass produced under laboratory conditions more 

colonies and a higher number of conidia. These products also showed protection 

against sun irradiation under field conditions. Studies are presently also conducted in 

Brazil on the control of the coconut mite by use of H. thompsonii (cf. Van der Geest 

et. al., 2000). Various isolates of the fungus were introduced from Mexico into Brazil 

and were mass produced on rice and corn grids, but the mortality due to the fungus was 

too low (about 35%). However, it was possible to increase the virulence of the fungus by 

passage through the host. The fungus has been established in the field, although damage 

due to A. guerreronis is still too high. 

Figure 6. Spraying of coconut trees with Mycohit. Photograph courtesy of 

Dr. P. Sreerama Kumar.

280 


Several attempts have been made to use the fungus also for the control of other 

mite pests. However, most of these attempts were unsuccessful, as e.g. the control of 

spider mites (T. cinnabarinus, Eotetranychus orientalis and T. urticae in 

greenhouses (Rombach & Gillespie, 1988). Hirsutella kirchneri has also been 

considered a good candidate for the control of plant-inhabiting mites. Its 

pathogenicity was tested by Sztejnberg et al. (1997) against a number of different 

mites. It was shown to be effective against the eriophyid P. oleivora, and against the 

spider mites Eutetranychus orientalis, Panonychus citri, T. cinnabarinus and in 

some degree against Hemisarcoptes coccophagus (Hemisarcoptidae). However, no 

infectivity was found towards the broad mite Polyphagotarsonemus latus 

(Tarsonemidae), Rhizoglyphus robini, Tyrophagus putrescentiae (Acaridae) and 

Typhlodromus athiasae (Phytoseiidae). No infectivity was noted towards a number 

of beneficial arthropods. 

Figure 7. Spraying of coconut trees with Mycohit. Photograph courtesy 

of Dr. P. Sreerama Kumar. 

A few reports deal with the occurrence of the H. thompsonii on the cassava 

green mite M. tanajoa in the cassava belt in Africa. Yaninek et al. (1996) observed


281 

the fungus on CGM and on Oligonychus gossypii during an inventory in Benin, and 

Odongo, Odindo, Brownbridge, and Kumar (1998) carried out experiments in which 

CGM infected plants were treated with suspensions of H. thompsonii. In the treated 

plots, 76.6% disease incidence was obtained, but rainfall caused a reduction in 

disease prevalence in the mites. The authors concluded that the application of the 

fungus has promise for controlling the CGM, but that the fungus should be applied 

in harmony with other natural mortality factors such as rainfall. 

The fungus has also been recorded in Calacarus heveae (Eriophyidae) an 

important pest in rubber plantations in Brazil (Tanzini et al., 2000). This mite is a 

major pest in the Michelin rubber plantation in Itiquira, Mato Grosso, where it 

causes considerable economic damage. Calacarus heveae feeds on the upper side of 

the leaves, in contract to most other rust mites (Figs. 8 and 9). Populations of several 

hundreds of mites per rubber tree leave are no exception. However, the mite 

populations are usually decimated after a few weeks by the action of Hirsutella 

thompsonii (Figs. 9 and 10). These epidemics are usually too late to avoid damage to 

the plantation (defoliation of the trees). 

Figure 8. Calacarus heveae, killed by Hirsutella thompsonii. Photograph: 

Leo P.S. van der Geest. 

Hirsutella thompsonii is normally associated with prostigmatic mites 

(Eriophyidae and Tetranychidae), although it has also been observed to infect 

mesostigmatic mites (McCoy & Selhime, 1977; Bałazy & Wiśniewski, 1982). 

Gerson, Gafni, Paz, and Sztejnberg (2008) tested Hirsutella thompsonii, H. 

kirchneri and H. necatrix with respect to their effect on several mite species: spider 

mites, rust mites, broad mites, but also scavengers and predatory mites were 

included in the study. The results of these experiments led to the conclusion that 

none of these fungus species gave satisfactory control of mite pests, neither in 

greenhouses, nor outdoors.

282 


Figure 9. Rubber tree leaves with numerous cadavers of Calacarus heveae. The 

mites have been killed by the fungus Hirsutella thompsonii. However, the 

disease cannot prevent substantial economic damage to the rubber 

plantations in Itiquira, MG, Brazil, as the epidemics come too late in the 

season. Photograph courtesy of Dr. Marcel R. Tanzini. 

Figure 10. Calacarus heveae (Eriophyidae), killed by Hirsutella thompsonii. Photograph 

courtesy of Dr. Marcel R. Tanzini. 

4.2.2. Other Deuteromycetes Infecting Mites 

Some of the other Deuteromycetes are probably the most comprehensively studied 

entomopathogenic fungi. However, of these fungi, only few records have been made 

of natural infections in mites. Leatherdale (1965) observed a mycosis of the 

blackcurrant mite Cecidophyopsis ribis by Paecilomyces eriophytis, later also found


283 

in Italy on Phytoptus avellanae, a mite causing big bud disease in ornamental and 

fruiting hazel (Corylus avellana). Experiments were carried out with the fungus 

isolate from C. ribis to infect the European red mite Panonychus ulmi and the 

eriophyids Aceria hippocastani (from horse chestnut) and Cecidophyes galii (from 

goosegrass). The fungus proved to be pathogenic for the first two species, but no 

infection was obtained in C. galii. The fungus has also been reported by Baker and 

Neunzig (1968): high infection rates were noted in the blueberry bud mite Aceria 

vaccinii (Eriophyidae) in North Carolina, USA, when high temperatures coincided 

with heavy rainfall and high relative humidity. Disease incidence declined from 

August onwards, when conditions were less favorable for the fungus. The population 

density of the blueberry mites then increased. 

One of the earliest experiments in which a fungus was tested against a 

phytophagous mite was a field application of B. bassiana spores for the control of 

the twospotted spider mite T. urticae (Dresner, 1949). Mites were treated with a dust 

containing 0.5% spores of the fungus, resulting in a mortality of 71%. However, 

these experiments did not lead to the development of a microbial acaricide. 

Deuteromycetes have widely been studied for the control of insect (and in a few 

instances mite) pests. A number of these fungi (e.g. Metarhizium, Beauveria) have a 

broad host spectrum and can easily be mass produced on relatively simple culture 

media. In Brazil, research is being conducted to evaluate several Deuteromycetes as 

possible control agent of the twospotted spider mite (Tamai, Alves, Lopes & Neves 

1998). They tested 152 different isolates for the fungi B. bassiana, B. brongniartii, 

Beauveria sp., Metarhizium sp., Paecilomyces lilacinus and P. farinosus. Only 

isolates of Beauveria spp. caused mortality between 35 and 95%. The pathogenicity 

of some isolates was further tested: one isolate gave even better control than 

obtained with chemical pesticides. The fungus was also effective against other pests 

in chrysanthemum, such as thrips and aphids (Alves, Tamai, & Lopes, 1998). 

Three different fungus species were investigated by Peña et al. (1996) with 

respect to their potential as biological control agent of the broad mite 

Polyphagotarsonemus latus (Tarsonemidae). This very polyphagous pest species 

thrives under warm and humid conditions, and this seemed to be a good reason to 

study the feasibility of using fungi as control agents. Three fungi were tested: B. 

bassiana, H. thompsonii and Paecilomyces fumosoroseus under controlled 

temperature and humidity conditions in the laboratory and in the greenhouse. All 

fungi were capable to infect the mites: higher doses resulted in a faster death of the 

mites, while density of the mites also affected disease incidence. The authors 

concluded from their experiments that the fungus selected should cause epizootics 

within 2–3 days following application. Promising results for the control of the broad 

mite on mulberry have been obtained with M. anisopliae by Maketon, Orosz- 

Coghlan, and Sinprasert (2008). The fungus is effective against larvae and adults, 

but no ovicidal effect was noted. The broad mite has also been found in association 

with Hirsutella nodulosa (Peña et al., 1996). No other associations of this mite with 

fungi have been reported. 

Shi, Feng, and Liu (2008) noted an ovicidal effect of sprays of an emulsifiable 

B. bassiana formulation against the twospotted spider mite T. urticae. The fungal 

isolate was obtained from mycosed aphids and has been formulated for the control

284 


of whiteflies in greenhouses. The dried conidial powder was suspended in a mixture 

of 95% industrial paraffin as oil carrier and 5% fatty alcohol polyethylene glycol 

ether as emulsifier. The authors are of the opinion that the formulation has greatly 

enhanced egg mortality, also at lower relative humidities. Oily formulations may 

give a better attachment of the conidia to the target pest and a better protection of the 

conidia against desiccation. The formulation has also provided significant control of 

the citrus rust mite in orchards in East China and of T. truncates and T. turkestani in 

cotton in the Tarim Basin of northwest China. 

Isolates of fungi may show large differences in virulence to their hosts. For 

example, Bugeme, Maniania, Knapp, and Boga (2008) studied 23 isolates of 

Metarhizium anisopliae and 3 isolates of B. bassiana with respect to their 

pathogenicity versus the spider mite T. evansi. Temperature greatly affected 

observed mortality of the spider mites, but also germination of the spores and 

growth were affected and varied with isolate. 

The fungi M. anisopliae and H. thompsonii are being investigated as control 

agents of Varroa jacobsoni (Kanga, James, & Boucias, 2002). They are pathogenic 

for the varroa mite and the conditions under which they can infect mites are similar 

to those found in bee colonies. Meikle, Mercadier, Holst, and Girod (2008) studied 

the impact of formulations of B. bassiana on varroa mites and on the honey bees. 

They formulated conidial preparations of two strains of the fungus with either 

carnauba or candelilla wax powder and studied the effect on colony health and mite 

fall (mortality). Bees were nof affected by the fungal preparations, but mite fall was 

consistently higher than the control. Results were encouraging, but more knowledge 

should be acquired on conidia dosage, number of applications and conditions within 

the bee hives. 

Eken and Hayat (2008) conducted an inventory for natural enemies of the 

twospotted spider mite Tetranychus urticae in Turkey. They found several isolates 

of Cladosporium cladosporioides (Moniliaceae), that were subsequently tested in 

the laboratory with respect to their pathogenicity towards T. urticae. The fungus 

caused mortality levels of 51–75% when sprayed on leaflets infested with 

twospotted spider mites. These results are encouraging and additional experiments 

should be conducted. Cladosporium infections were also found by Van der Geest et 

al. (2002) in Retracus johnstoni, an eriophyid feeding on the palm tree Syagrus 

romanzoffiana in Brazil. The fungus has been isolated on potato-dextrose agar, but 

no further experiments have been carried out with this isolate. 

Interesting experiments were performed by Sanassi and Amirthavalli (1970) 

with the velvet mite Trombidium gigas (Trombidiidae). Mite were infected with 

spores of the fungus Aspergillus flavus, a fungus also capable of infecting humans 

and problematic in foods as it produces the very toxic aflatoxin. Three different 

methods were applied: injection of spore suspensions into the body cavity, spraying 

of spore’s suspensions on the integument of the mite and dusting of spores on the 

integument. In all cases infection of the mites was obtained. Changes in the structure 

of the integument were noted (Sanassi & Oliver, 1971). The first sign of the disease 

is the loss of the scarlet-red plumose cuticular setae of the mites. Each seta consists 

of a main central stem from where minor secondary branches arise. The base of the


285 

central stem is normally slightly enlarged and is buried in sockets present in the epiand 

procuticle. 

The fungus apparently digests the lipoproteinaceous epicuticular layer that 

attaches the base to the cuticular sockets. Subsequently, the process is followed by 

additional chemical changes in the composition of the cuticle. Epidermal cells 

display interesting pathological symptoms. In uninfected mites, epidermal cells form 

a syncytium, but after infection a remarkable reaction occur in these cells. The cells 

line up in almost a single row just below the outer limiting border of the epidermis. 

Vacuoles appear in the cytoplasm of the epidermal cells, while organelles such as 

mitochondria and Golgi apparatus are not anymore discernable. 

In a search for control agents of the citrus red mites (CRM) in Israel, field 

collected mite cadavers were examined for the presence of pathogens. This has 

resulted in the finding of three species of fungi that were found to be associated with 

mites. The fungi were described by Boekhout et al. (2003) as novel species 

belonging to the Ustilagomycetes, a class that is also called the smut fungi. It is a 

large taxon with over 1,400 species in 70 genera that are almost exclusively plant 

pathogens. The three fungi are anamorphic (they have no sexual state) and belong 

therefore to the Deuterymycetes. However, morphologically they are similar to 

yeast-like fungi which have been classified in the Ustilaginales. Based on molecular 

properties, they should be considered to belong to two different lineages within the 

Exobasidiomycetidae of the Ustilaginomycetes (Basidiomycota). These fungi, 

described as Meira geulakonigii, M. argovae and Acaromyces ingoldii, are hard to 

isolate from field-collected material: they are slow-growing fungi and for their 

identification physiological and molecular methods are needed. This probably 

explains the fact that they have only recently been discovered. 

The three fungi were further studied with respect to their potential as biological 

control agents of phytophagous mites. Laboratory investigations showed that all 

three fungi affected mites, although M. argovae showed no effect towards T. urticae. 

(Gerson et al., 2008). Meira geulakonigii caused considerable mortality of spider 

mites and citrus red mite. An interesting observation was that none of the fungi 

invaded the mites, although the fungi did grow on the mite’s cadavers. It is assumed 

that mortality among the mites was caused by the action of fungal toxins. 

Further tests showed that the fungus was endophytically present within the 

sealed grapefruit flowers and in the flavedo (the tough outer skin) of grapefruit. 

There was no evidence that the fungus caused any damage to the plants, which led 

the authors to the assumption that M. geulakonigii serves as a “body guard” of 

grapefruits. Also, M. geulakonigii had only minimal fungicidal effect on some 

predatory mites. This property, together with its tolerance to many insecticides and 

acaricides, suggests that this fungus has possibilities for integrated control programs. 

4.3. Ascomycota 

The Ascomycota is a large taxon of fungi with approximately 2,000 genera and over 

30,000 species. Members of the Ascomycota bear the sexual spores within an ascus, 

originally a cell that at first contains a diploid nucleus resulting from karyogamy (the

286 


fusion of nuclei or nuclear material that occurs during sexual reproduction). The 

nucleus undergoes subsequently meiosis, resulting in the formation of haploid 

ascospores inside the asci. These asci are often borne in or on top of a sporocarp. 

Very few Ascomycota have been isolated from mites. These isolations concern 

mainly Laboulbeniales infections in a number of mite species. Laboulbeniales is an 

order of fungi with more than 2,000 species. They are small, often minute fungi that 

have an obligate association with arthropods, mainly insects, and they lack 

mycelium. On their host, they appear as scattered or densely crowded bristles or 

bushy hairs which may form furry or velvety patches on certain part of the host’ 

integument. These plume-like structures and triggers help in ascospore release when 

the arthropod comes into contact with a mature thallus. 

The site of attachment is usually limited to definite regions on the integument of 

each host. The entire thallus (body) is derived from enlargement and subsequent cell 

division of the two-celled ascospore. Below the surface of the arthropod cuticle 

absorption through a peg- or root-like haustorium provides a nutrition source for the 

fungus; however, the fungal parasites of this group do not appear to cause much 

damage to the host. A few species have been found on mites, including a Rickia sp. 

and an unknown species on Hirstionyssus (Demanyssidae) (Steinhaus & Marsh, 1962). 

5. DISEASES CAUSED BY EUKARYOTIC MICROPARASITES 

Traditionally, the animal kingdom has been divided into two subkingdoms: the 

Protozoa (unicellular eukaryotes) and the Metazoa (multicellular animals). In 

modern taxonomy, a kingdom Protista is considered of which the members are either 

unicellular, colonial or multicellualar. All these organisms are eukaryotes, 

The Protista are divided into three major groups: the Protozoa, the Algae and 

the Fungus-like protists. Protozoa are defined as single-celled eukaryotic organisms, 

that feed heterotrophically (feeding both on both organic and inorganic raw 

materials) and exhibit diverse motility mechanisms. Traditionally, four divisions are 

discerned, based on their mode of mobility: 

- Flagellata (Mastigophora) are protozoa that move by means of flagellar 

action. Some flagellates have their flagella attached in a structure called an 

undulating membrane. They often have symbiotic relationships with 

multicellular organisms. 

- Rhizopoda (Amoebozoa) Rhizopoda are protozoa that move by employing 

pseudopodia, which are covered by membranes. These pseudopodia are 

cytoplasmic extensions that are not only used for locomotion but also to 

engulf food. Amoebae live in moist terrestrial and aquatic environment. 

- Apicomplexa (or Sporozoa). The Sporozoa are parasitic spore formers that 

do not move by their own power. Plasmodium vivax, the cause of malaria, 

is a sporozoan. 

- Ciliata (Ciliophora) Ciliata are protozoa that move by means of cilia action. 

Cilia are small and numerous; flagella are large and few. Because of the 

tremendous variety in ciliary arrangements and functions, ciliates are 

among the most diverse cells in the biological world.

MITE PATHOGENS IN IPM 287 

Table 4. Protozoan infections in mites. 

Species Mite host Mite family References 

Apicomplexa 

Acarogregarina 

corolla 

Scutovertex minutus Scutoverticidae Erhardová (1955) 

Asterophora 

caloglyphi 

Erhardovina 

bisphaera 

Caloglyphus moniezi Acaridae Geus (1969) 

Damaeus clavipes Damaeidae Purrini and Ormieres 

(1981) 

Damaeus onustus Damaeidae Purrini and Ormieres 

(1981) 

Eupelops hirtus Eupelopidae Purrini and Ormieres 

(1981) 

E. carabodesi Carabodes coriaceus Carabodidae Purrini and Ormieres 

(1981) 

E. euzeti Euzetes seminulum Euzetidae Lipa (1982) 

E. fuscozetesi Fuscozetes setosus Ceratozetidae Purrini, Bukva, and 

Bäumler (1979) 

E. fuscozetesi Euzetes globulus Euzetidae Purrini and Ormieres 

(1981) 

E. oribatarum Mite see Lipa (1971) 

E. phtiracari Phthiracarus globosus Phthiracaroidea Purrini and Ormieres 

(1981) 

Phthiracarus piger Phthiracaroidea Purrini and Ormieres 

(1981) 

E. platynothri Platynothrus peltifer Nothroidea Purrini and Ormieres 

(1981) 

E. postneri Hermannia gibba Hermannioidea Purrini et al. (1979) 

E. scutovertexi Scutovertex minutus Scutoverticidae Erhardová (1955) 

Erhardovina sp. Limnochares aquatica Hydrachnellae Issi and Lipa (1968) 

Gregarina sp. Eupelops subuliger Eupelopidae Purrini et al. (1979) 

Eupelops torulosus Eupelopidae Purrini et al. (1979) 

Rhysotritia ardua Phthiracaroidea Purrini et al. (1979) 

Erhardovina sp. Damaeus geniculatus Damaeidae see Lipa (1971)

288 



Erhardovina sp. Damaeus oblongus Damaeidae see Lipa (1971) 

Gurleya sokolovii Limnochares aquatica Hydrachnellae Issi and Lipa (1968) 

Unidentified 

gregarine 

Tyrophagus 

putrescentiae 

Acaridae Steiner (1993) 

Adelina acarinae Nothrus silvestris Nothroidea Purrini (1984) 

Microspora 

Intexta acarivora 

Tyrophagus 

putrescentiae 

Tyroglyphidae 

Larsson, Steiner, and 

Bjørnson, (1997) 

Microsporidium 

phytoseiuli 

Phytoseiulus persimilis Phytoseiidae Bjørnson, Steiner, 

and Keddie (1996) 

Microsporidium sp. Amblyseius barkeri Phytoseiidae Beerling and Van der 

Geest (1991a, 1991b) 

Neoseiulus 

cucumeris 

Phytoseiidae 

Beerling and Van der 

Geest (1991a; 1991b) 

Napamichum 

aequifolium 

Limnochares aquatica Hydrachnellae Larsson (1990) 

Nosema acari Damaeus onustus Damaeidae Purrini and Weiser 

(1981) 

Damaeus clavipes Damaeidae Purrini and Weiser 

(1981) 

N. euzeti Euzetes seminulum Euzetidae Lipa (1982) 

N. führeri Phthiracarus globosus Phthiracaroidea Purrini & Weiser 

(1981) 

N. helminthorum Ceratoppia sp. Liacaroidea Moniez (1887) 

Ceratoppia bipilis Liacaroidea Dissanaike (1958) 

Xenillus tegeocranus Liacaroidea Dissanaike (1958) 

N. hermanniae Hermannia gibba Hermannioidea Purrini et al. (1979) 

N. ptyctimae Rhysotritia ardua Phthiracaroidea Purrini and Bäumler 

(1976) 

N. sperchoni Sperchon sp. Sperchontidae Lipa (1962) 

N. steganacari Steganacarus striculus Phthiracaroidea Purrini and Weiser 

(1981)


289 


N. steinhausi Tyrophagus putrescentiae Tyroglyphidae Weiser (1956) 

Oligosporidium 

occidentalis 

Metaseiulus occidentalis Phytoseiidae Becnel, Jeyaprakash, 

Hoy, and Shapiro 

(2002) 

Pleistophora cephei Cepheus dentatus Cepheoidea Purrini and Weiser 

(1981) 

P. dindali Carabodes coriaceus Carabodidae Purrini and Weiser 

(1981) 

P. platynothri Platynothrus peltifer Nothroidea Purrini and Weiser 

(1981) 

P. oribatei Carabodes femoralis Carabodidae Purrini and Weiser 

(1981) 

Damaeus clavipes Damaeidae Purrini and Weiser 

(1981) 

Microtritia minima Euphthiracaroidea Purrini and Weiser 

(1981) 

Phthiracarus piger Phthiracaroidea Purrini and Weiser 

(1981) 

Phthiracarus sp. Phthiracaroidea Purrini and Weiser 

(1981) 

Physotritia duplicata Phthiracaroidea Purrini and Weiser 

(1981) 

Thelohania 

microtritiae 

Microtritia minima Euphthiracaroidea Purrini and Weiser 

(1981) 

The above classification is still being used, but we know now on the basis of 

ribosomal RNA gene sequencing that various groups in the Flagellata and Rhizopoda 

are not closely related. There may be greater genetic difference between two groups of 

Flagellata than between flowering plants and vertebrates. In modern classification, the 

following seven phyla are distinguished: Apicomplexa, Sarcomastigophora, 

Microspora, Ciliophora, Acetosphora, Myxospora and Labyrinthomorpha. It is not 

within the scope of this chapter to go into details about this classification. 

Two phyla of the subkingdom Protozoa, the Apicomplexa and the Microspora, 

have members that are found in arthropods. Some of these are also pathogens of 

vertebrates, while others are commensals or weak pathogens; sometimes, they are 

highly virulent and pathogenic organisms (cf. Tanada & Kaya, 1993). 

Protozoa associated with mites are mainly found in the Apicomplexa, with the 

classes Gregarina and Coccidia, and in the phylum Microspora. The class Gregarina 

is divided into the orders Eugregarinida and Neogregarinida. Several members of the 

former order have been detected in mites.

290 


The phylum Microspora also contains several pathogens of mites. Table 4 lists 

protozoan species that have hitherto been isolated from mites. There is little 

information available on the population dynamical effects of these organisms on 

natural mite populations. 

5.1. Apicomplexa Infections in Mites 

Apicomplexans have very complex life cycles, with much variation among the 

different apicomplexan groups. Both asexual and sexual reproduction is involved, 

although some Apicomplexa skip one or the other stage. The life cycle starts when 

an infective stage, the sporozoite, enters a host cell, and then divides repeatedly to 

form numerous merozoites. Some of the merozoites transform into sexually 

reproductive cells, or gamonts. These gamonts join together in pairs and form a 

gamontocyst. Within the gamontocyst, the gamonts divide to form numerous 

gametes. Pairs of gametes then fuse to form zygotes, which give rise by meiosis to 

new sporozoites, and the cycle starts all over again. 

Apicomplexa are transmitted to new hosts in various ways; some, like the 

malaria parasite, are transmitted by infected mosquitoes, while others may be 

transmitted in the feces of an infected host, or when a predator eats infected prey. 

Gregarinia, or gregarines have mature gamonts (trophozoites) that are large and 

extracellular. The gamonts are found in the digestive tract and body cavities of 

invertebrates and they possess organelles (see Tanada & Kaya, 1993). They have 

usually similar gametes (isogametes) and undergo syzygy: mature gamonts detach 

themselves from the midgut and line themselves end to end in pairs or in large 

numbers to form a prenuptial association. The zygotes form oocysts within 

gametocysts. Eugregarines have a life cycle that consists only of gametogony and 

sporogony, but the neogregarines, considered more primitive, have an additional 

schizogony (a multiple fission process). This schizogony (or merogony) occurs 

intra- or extracellularly and causes the presence of larger numbers of the pathogen 

than in case of the eugregarines. These higher numbers result in a more virulent 

infection. 

As early as 1885, the eugregarine Gregarina oribataram was reported in an 

unidentified mite (see Lipa, 1971). Unidentified gregarine infections were observed 

in the oribatids Damaeus oblongus and D. geniculatus (Damaeidae) by Michael in 

1884 and Wellmer in 1911 (see Lipa, 1971). Gregarina scutovertexi was described 

by Erhardová in 1955 from Scutovertex minutus, an oribatid mite that serves as 

vector of the tape worm Monieza expansa. Several other eugregarine species were 

described by Purrini et al. (1979) and Purrini and Ormiers (1981). For more details 

is referred to Table 4. 

An interesting eugregarine infection was also noted in the intestinal wall of the 

water mite Limnochares aquatica (Hydrachnellidae) (see Issi & Lipa, 1968), while 

Gregarina euzeti was detected in the oribatid Euzetes seminulum (Lipa, 1982). 

Despite all these reports on gregarines, no data are available on the impact of these 

infections on the host. It is generally believed that gregarines are of low virulence.


291 

Coccidia differ from the gregarines in their gamogony: female gamonts of 

gregarines give rise to a number of gamonts whereas those of Coccidea only to 

single gamonts. One coccidian species has been described from an oribatid (Purrini, 

1984). 

5.2. Microspora Infections in Mites 

Microspora (or Microsporidia) are obligate intracellular parasites with a broad host 

range including all animal groups. They rank among the smallest eukaryotes (1–40 μm) 

with the shortest eukaryotic genome and are generally considered to be a separate 

phylum within the subkingdom Protozoa. However, recent molecular studies 

indicate that they may be considered to be extremely reduced fungi. Replication 

takes place within the host's cells, which are infected by means of unicellular spores. 

Microsporidia are unusual in lacking mitochondria and in having mitosomes. 4 

They also lack motile structures such as flagella. The spores are protected by a 

layered wall made of proteins and chitin. Their interior is dominated by a unique 

coiled structure called the polar filament. Spores, the infective stage, are ingested by 

the host and, in the midgut, their polar filament is instantaneously emitted as turning 

a garden hose inside out. The polar tube penetrates the host cell and the contents of 

the spore are pumped through it without destruction of the host cell. Within the host 

cell, an increase in numbers followed by the development into new spores takes 

place. In this way, the infection spreads throughout the host. Many different tissues 

may be affected. The spores may be released into the environment during the life of 

the host or after its death. The spores are the only stages that can survive outside the 

host. Many microsporidia have very complex life cycles with several spore types 

and host involved. Microsporidiosis is often transmitted vertically (from mother to 

offspring), usually without spores as intermediary. Vertical transmission may be 

transovarial, by passage though the ovary, or transovum, a form of transovarial 

transmission in which the pathogen enters the egg while it is still in the ovary. 

Taxonomy was in the past mainly based on spore size and shape. These 

characters are, however, unsatisfactory and for that reason, ultrastructural 

characteristics have been used. This has caused a considerable revision in this group 

of pathogenic organisms (Sprague, Becnel, & Hazard, 1992). Recently, several 

research groups have started to integrate molecular techniques for phylogenetic 

studies of Microsporidia. This will undoubtedly result in a new revision of these 

taxa. 

The first microsporidium described in mites was Nosema steinhausi (Weiser, 

1956) from the stored product mite Tyrophagus putrescentiae (Tyroglyphidae). The 

disease affects both adults and nymphs. Experiments in a colony of the mite showed 

that the disease progressed from about 10% infection at the start of the experiment to 

4 A mitosome is an organelle found in some unicellular eukaryotic organisms. The 

mitosome has only recently been found and named, but its function has not yet been 

well characterized. It is sometimes termed a crypton.

292 


75% after 2 months. The colony was completely eradicated after a further 2 weeks. 

Several other authors have described microporidia from various species of mites. 

For more details refer to Table 4. 

In the late 1980s poor performance was noted of phytoseiids used as biological 

control agent for thrips and spider mites in greenhouse crops and this observation 

has led to studies on the possible involvement of pathogens in predator colonies. 

Beerling and Van der Geest (1991a, 1991b) studied a microsporidosis in mass 

cultures of the predators Amblyseius barkeri and Neoseiulus cucumeris 

(Phytoseiidae) that are being used for the control of the thrips pests Frankliniella 

occidentalis and Thrips tabaci (Thripidae) on vegetable and ornamental crops in 

greenhouses. Diseased predators show a low reproduction and predation capacity of 

the mites unsatisfactory. Predatory mites were sluggish in their movement and had a 

swollen and whitish appearance (Beerling & Van der Geest, 1991a). 

The presence of numerous spores could be detected in squash preparations of 

the mites and it was assumed, that the pathogen involved belonged to the 

Pleistophoridae (Microspora). Also infected stored product mites were observed. 

Further work showed that three different spore types are found in the predator 

cultures. It is difficult to say that three species of Microsporidia are involved, since 

some species have several spore types during their life cycle. Recently, a new 

species of a microsporidium parasite, Intexta acarivora, was observed in the gut 

epithelium of the forage mite T. putrescentiae (Larsson et al., 1997), obtained from a 

commercial culture in The Netherlands. Mites of this culture are used as prey for a 

commercial rearing of N. cucumeris. 

Beerling and Van der Geest (1991a, 1991b) also studied infected mite strains 

from a commercial rearing in The Netherlands, but it is not known whether this has 

the same origin as the samples studied by Larsson et al. (1997). The spore size 

values of this microsporidium do not correspond with any of the values of the spores 

in Beerling, Rouppe van der Voort, and Kwakman (1993). 

Bjørnson et al. (1996) studied colonies of P. persimilis that were obtained from 

suppliers of biological control agents. On the basis of spore morphology, three 

distinct microsporidia could be observed in strains of P. persimilis, obtained from 

three different suppliers. The ultrastructure of the pathogen and the course of the 

disease of a colony obtained from Europe were studied in more detail. Schizonts 

were observed inside the nuclei of the digestive cells of the ventriculus and within 

the protoplasm of cells that line the caecal wall and the muscle tissue underlying it. 

The properties of the pathogen made it difficult to assign it to an existing genus. For 

that reason, it was placed in the collective group Microsporidium. Vertical 

transmission for this microsporidium was proven, as mature spores were observed in 

developing eggs inside gravid females (Fig. 11). The performance of an infected 

colony was greatly affected (Bjørnson & Keddie, 1999): mean fecundity and prey 

consumption of infected mites were significantly reduced. Short-term survivability 

was variable and was not a good measure of predator quality. However, uninfected 

females lived longer than infected females.


293 

Figure 11. Cross section of a microsporidian spore and a crystal of Phytoseiulus 

persimilis. The polar filament of the spore is not visible. Photograph by Dr. Susan 

Bjørnson. 

Poor performance of the predators, due to the presence of pathogens in the mass 

cultures is a threat to integrated pest management in especially glasshouse crops 

(e.g. Steiner, 1993). It is clear that more attention should be paid to a good 

monitoring system. The presence of pathogens should be established early in the 

manufacturing process, which requires a fast and reliable detection method. In the 

past, visual inspection with the aid of a binocular or compound microscope was the 

only way to establish the presence of these pathogens. A polarizing filter is needed 

to avoid confusion with the birefringent crystals that are commonly present inside 

adult phytoseiids (see Section 6.1). 

The availability of a method to detect the disease at an early stage is of great 

importance for the commercial production of natural enemies. Beerling et al. (1993) 

developed an ELISA to detect the presence of microsporidiosis in predator massrearings. 

Monoclonal antibodies were produced against one spore type (oblong), that 

was present in both prey and predator species. A next step would be the use of more 

sensitive molecular techniques which makes the detection of microsporidiosis 

possible regardless of spore type, and even before spores are formed (Malone & 

McIvor, 1996). 

Recently, a new species of microsporidia was described by Becnel, Jeyaprakash, 

Hoy, and Shapiro (2002) from the predatory mite Metaseiulus occidentalis. Mites 

infected with Oligosporidium occidentalis do not show any external or gross signs 

of infection, but electronmicroscopical analysis reveales that the pathogen develops 

in eggs, larvae, nymphs and adults of the predator. Mature cells of O. occidentalis can 

be found in cecal cells, lyrate organ cells, ganglia, epithelial cells, muscle, inside the 

ovary and in developing and mature eggs. Female predators have in general a shorter

294 


life span, a low oviposition rate and fewer female progeny. No effect could be 

shown on longevity of males or on male progeny survival to larval and adult stages. 

The infection may affect the performance of the predator. Heat treatments of 

infected colonies had some success: eggs placed for 7 days in a chamber at 33°C and 

subsequently at 27°C showed a reduced infection rate, but the disease was still not 

completely eliminated. Mites emerging from these eggs still showed spores inside 

their body, but it was assumed that most of these spore were dead as the majority of 

the mites survived. After a number of weeks, infection rates were again high, 

indicating that the heat treatment was only partially effective. However, when eggs 

were placed at 33°C. and when their progeny was also kept at this temperature, 

disease-free mites were obtained. It was also shown that the disease may be 

horizontally transmitted, probably by cannibalism. 

At this moment, no other cure exists for microsporidiosis in predatory mite 

mass rearings. Anti-microsporidial compounds, such as albendazole, fumagillin, 

metronidazole and nifedipine were not successful in eliminating microsporidiosis in 

mass cultures of P. persimilis (Bjørnson, 1998). Therefore, efforts should be made to 

keep the starting cultures of predatory mites disease-free. Heat treatment of infected 

eggs, or rearing infected individuals at elevated temperatures, has been shown to 

reduce disease prevalence in some cases; however, the most effective and practical 

means for rearing microsporidian free predatory mites is to start a new rearing with 

progeny from uninfected females. 

6. OTHER DISEASES 

6.1. Symptoms Ascribed to Poor Condition 

In this chapter, we discuss a condition in mites that cannot be ascribed to the action 

of a pathogen. In a number of instances, rectal plugs, usually in combination with 

abdominal discoloration have been observed in phytoseiids (Tanigoshi, Fagerlund, 

& Nishio-Wong, 1981; Bjørnson et al., 1997). This discoloration is usually 

manifested as two white stripes along the dorsal sides of the body within the 

Malpighian tubules. The condition is frequently found in laboratory colonies of 

predatory mites and it may be a sign of poor condition of the predator. Tanigoshi 

(1982), for example, considered the condition a sign of senescence. Affected mites 

are often lethargic and have frequently numerous densely packed, birefringent 

dumbbell-shaped bodies, mainly in the Malpighian tubules, rectum and anal atrium. 

In Cheyletus eruditus, abdominal discoloration is also associated with the 

occurrence of birefringent crystals in the excretory organs, especially when reared 

under crowded conditions. These crystals are considered to be the normal excretory 

products (Hughes, 1950) and probably consist of guanine and uric acid (McEnroe, 

1961). These compounds are insoluble and are probably stored in the malpighian 

tubes prior to excretion. The crystals observed in P. persimilis, however, contain 

high levels of potassium, low levels of phosphorous and sulphur and traces of 

chlorine, very unlike the common waste products mentioned above (Bjørnson, 

1998). Large numbers of crystals in mites are especially found in laboratory mites,


295 

reared under crowded condition (Fig. 12), and it is assumed that they are an 

indication of a poor condition of the mites. 

Figure 12. Crystals in tissue of Phytoseiulus persimilis. Such crystals are often an 

indication of a poor condition of the mite. Photograph of Dr. Susan Bjørnson. 

6.2. Identification of Pathogens 

Recognition of an organism causing disease in noxious mites will aid in the process 

of implementing control strategies against such mites, while it will also be of great 

importance to know disease causing organisms in mites that are mass reared for 

biological control purposes. However, identification of pathogens is not in all 

instances easy: for example, virus recognition in diseased mites may require very 

comprehensive research before one may decide that a virus is the disease causing 

agent. In contrast to insects, very few viruses have been isolated from mites and the 

viruses known to cause disease in mites are not as readily identifiable as some of the 

insect viruses. A large number of insect viruses belong to the baculoviruses, rodshaped 

viruses that may form large inclusion bodies (polyhedra) in the cell nuclei 

(nuclear polyhedrosis viruses), or smaller so-called granula (granulosis viruses). 

Other viruses, the cytoplasmic polyhedrosis viruses are icosahedra and are also 

included in large inclusion bodies of irregular form. Identification of such viruses 

can partially be done by light-microscopic means, in combination with more 

sophisticated molecular techniques. Such viruses are not known from Acari. 

Hitherto, only few viruses have been identified as pathogen of mites. 

Bacteria causing disease are often obligate intracellular organisms. Classical 

identification based on characters such as nutrient requirement and structure of 

colonies on artificial media is not possible as these bacteria cannot be grown outside 

it host’s cell. However, the availability of molecular techniques has made

296 


identification of such intracellular bacteria possible by, among others, analysis of 

16S rDNA gene sequences. The best-known species of such intracellular bacteria 

belong to the genus Wolbachia, probably the most widely-spread parasitic bacterium 

known. Abnormal sex ratios, incompatibilities between strains of mites and absence 

of male offspring may point to the presence of Wolbachia sp. or other symbionts. 

Feeding infected mites with antibiotics may remove these parasitic bacteria and will 

result in “normal” offspring. Molecular analysis of 16S rDNA will finally prove the 

presence of Wolbachia or other intracellular bacteria. 

The largest number of pathogens of mites is found in the fungi. Pathogens of 

mites are mainly found in the Zygomycota and Deuteromycota (or Fungi 

Imperfecti). For a proper identification, it is usually necessary to study sporulating 

fungi. This can be accomplished by incubating the infected mites under conditions 

of a high relative humidity. 

Zygomycota are characterized by the absence of cross walls (septa) in their 

hyphae and the presence of tick-walled, sexual spores (zygospores). However, the 

primary taxonomic emphasis is on asexual reproductive structures. The asexual 

spores (conidia) are released from the conidiophores by force and form often a halo 

around the host’s cadaver. Species infecting mites form secondary conidia upon 

germination of these conidia. The secondary conidium is much smaller in size and is 

called capilliconidium. Identification to the species is often difficult and requires the 

aid of specialists. Of some species, only zygospores (or resting spores) are known. 

Taxonomy of these species is mainly based on the properties of these spores. These 

species have been lumped together in the genus Tarichium. 

Several Deuteromycetes have been isolated from Acari, belonging to the 

following genera: Aspergillus, Beauveria, Cephalosporium, Hirsutella, 

Paecilomyces, Sporothrix, Tolypocladium and Lecanicillium (Verticillium). A key to 

the genera of Deuteromycetes infecting insects and mites can be found in Samson 

(1981). Identification requires examination of conidium ontogeny which is the 

primary character for typifying the different genera. There are two modes of blastic 

conidiogenesis: phialidic and sympodal. A succession of conidia is produced by a 

phialidic conidiogenous cell. The shape of the phialide is dependent on the genus: 

flask-like in Paecilomyces and Hirsutella, awl-like in Lecanicillium and cylindrical 

in Metarhizium. The conidia are produced in chains (Paecilomyces, Metarhizium), or 

they are contained in slimy heads or droplets (Lecanicillium, Fusarium). Phialides of 

Hirsutella form conidia that are held together in a slimy sheath. This gives the 

impression that only one conidium is being produced. Sympodial development is 

observed in species of the genera Beauveria and Sporothrix. Conidia are formed 

singly on a laterally proliferating conidiogenous cell that often shows a geniculate or 

zigzag type of elongation. For more details is referred to Samson (1981). 

7. PROSPECTS OF ACAROPATHOGENS FOR INTEGRATED PEST 

MANAGEMENT 

Comprehensive research has been conducted to study the possibilities to use 

pathogens for the control of insects and other invertebrate pests. There are several 

cases known how pathogens may decimate populations of phytophagous mites under


297 

natural conditions. An early example is a virus disease of the citrus red mite in citrus 

groves throughout California and Arizona (Reed, 1981). However, successful 

application of the virus failed for a variety of reasons. Mass production of the virus 

is difficult as the virus can only be grown in living mites. This fact makes mass 

production very laborious and expensive. Furthermore, the virus becomes rapidly 

inactivated by sunlight when applied in aqueous formulations, while high 

temperatures, common in citrus orchards in California and Arizona, also have a 

negative effect on the virulence of the virus. Inactivation of the virus by sunlight 

may be overcome by the addition of ultraviolet protecting substances. The main 

reason that this virus, although very host specific, has never been successful are the 

difficulties encountered during mass production. Biological acaricides with viruses 

as active ingredient are not foreseen for the near future, as few viruses of 

phytophagous mites are known. The situation with respect to the varroa mite Varroa 

jacobsoni may be completely different. Several viruses have been isolated from this 

parasitic mite and more research may lead to the discovery of viruses that could be 

used for the control of the varroa mite. A point to worry about is that the varroa mite 

may act as vector of honey bee viruses. Host specificity experiments are for that 

reason of great importance. 

Many fungal pathogens show a high pathogenicity towards phytophagous mites. 

There are several examples showing how fungi are able to cause large epidemics in 

natural populations of tetranychids and eriophyids. One of the main obstacles for a 

successful application of fungal pathogens for the control of invertebrate pests in 

agricultural crops is the ambient condition within the vegetation. Almost all fungi 

require a relative humidity near the saturation point for both spore germination and 

spore formation. Entomophthorales epidemics have frequently been observed in 

insect and mite populations: Neozygites floridana is a fungal pathogen that may 

cause large reductions in population sizes of several species of spider mite. Such 

epidemics usually occur later in the season, when population sizes of spider mites 

are large and when relative humidity is near the saturation point. Damage to the crop 

has then already been inflicted. 

Experiments have been conducted to advance epidemics by inundative releases 

of the pathogen. The high virulence against certain target pests and their high 

specificity make these fungi attractive for inundative releases. However, 

entomophthoralean species are very fastidious: culturing and sporulation in artificial 

media is hardly possible which makes mass production of these fungi very 

expensive and laborious, as they should be grown in living mites. In addition, the 

infective stages of these fungi are rather short-lived and this characteristic makes 

their application difficult. It has been suggested that the use of these fungi in 

greenhouses may show good prospects (Maniania, Bugeme, Wekesa, Delalibera, & 

Knapp, 2008). 

In many greenhouses, high value horticultural crops are grown where 

environmental coniditions that normally favor the efficacy of these fungi can easier 

be manipulated than in outdoor crops. In addition, horizontal transmission of the 

fungus may be more efficient when spider mites densities are sufficiently high, 

making repeated inundative releases unnecessary. However, low spider mite 

densities would be an disadvantage for successful control of the pest concerned.

298 


From the other hand, classical biological control with these fungi seems to be 

attractive in certain circumstances. Efforts have been made to use Neozygites 

tanajoae as a control agent for the cassava green mite in Africa by releasing the 

fungus in cassava fields in Benin as a classical biological control agent. The fungus 

has later been isolated from the release areas where it caused a higher mortality 

among cassava mites than the local strains of N. tanajoae did. However, more 

knowledge is required. We know too little how the fungus overcomes unfavorable 

periods, about the role of resting spores and under which conditions may resting 

spores sporulates. Interesting observations were made by Elliot et al. (2008) in a 

cassava field in the state on Bahia, Brazil. Epidemics of the fungus were virtually 

absent when cassava green mite populations reached high densities, as not sufficient 

fungus inoculum was present. Later in the season, sufficient fungus inoculum was 

observed, but at that time no mites were present due to defoliation of the cassava 

plants. It is very hard to manipulate such a system, as mass production, followed by 

inundative releases is impossible at a large scale. 

The fungus does not seem to be the solution for the cassava green mite problem 

in Africa, although it is promising that the fungus seems to become established in 

the release areas. The fungus may be an important factor in the control of the 

cassava mite, when applied in combination with predatory mites. A point of concern 

is also the use of chemical pesticides: it is known that, in particular fungicides may 

have a detrimental effect on the fungal pathogen. Careful selection of chemicals 

used in a crop system is of utmost importance. 

Figure 13. Brevipalpus phoenicis infected by Lecanicillium (Verticillium) lecanii. 

Photograph courtesy of Dr. Marcel Tanzini. 

Several Deuteromycota are known with a high virulence towards mites and 

other invertebrates. This group of fungi can in general be grown in artificial media 

and mass production is therefore no problem. The first attempt to control an


299 

invertebrate pest with a fungus of this group was already conducted in Russia in 

1888, when Krassilstschik sprayed a suspension of spores of Metarhizium anisopliae 

in the field for the control of the sugar beet curculio Cleonis punctiventris (cf. 

Steinhaus, 1949). Since then, many attempts have been made to formulate 

mycopesticides, mainly for the control of insect pests (De Faria & Wraight, 2007). 

Until now, 171 products have been developed worldwide with entomo- and 

acaropathogens as active ingredients. Of these, 129 products are still available. The 

number of products that have been developed for use against mites is small: only 17 

products are recommended for use against Acari. The main part of these pesticides 

contains B. bassiana as active ingredient, but four preparations are based on 

Lecanicillium sp. (formerly Verticillium lecanii) (Fig. 13). Many of these species 

have a broad host spectrum, like Beauveria bassiana and Metarhizium anisopliae. 

The genus Hirsutella contains several members with a high specificity towards 

mites. The best studied species is H. thompsonii, originally described from the citrus 

rust mite Phyllocoptruta oleivora. Acaricidal preparations with H. thompsonii as 

active ingredient were developed in the 1980s for the control of the citrus rust mite, 

but the production was discontinued because of instability of the product. It is 

hopeful to notice that the interest in the production of H. thompsonii based 

acaricides has recently been renewed in India, and in some Latin American 

countries, but now for the control of rust mites in coconut. This renewed interest has 

led in India to the production of a successful bio-acaricide. 

In Colombia, biopesticides have been developed that contain a mixture of 

invertebrate pathogens, e.g. Microbiol Completo contains B. bassiana, M. 

anisopliae, Nomuraea rileyi, Isaria fumosorosea and B. thuringiensis. It is 

recommended for the control of a variety of insect species and Acari. It is 

remarkable that in particular in Latin American countries, many bioinsecticides are 

being developed with fungal pathogens as active ingredients. The climatic 

conditions may be more suitable for the applications of such pesticides than, e.g. in 

Europe. As mentioned earlier, a major drawback in the use of fungi is their 

dependence on a high relative humidity during spores germination. Oily 

formulations seem to be a solution to this problem. Oily substances protect the 

spores against desiccation and allow sporulation at a somewhat lower relative 

humidity. 

Hirsutella thompsonii var. synnematosa has been introduced from Zimbabwe 

and H. thompsonii var. vinacea from North Carolina as classical biological control 

agents for the control of Eriophyes sheldoni and Phyllocoptruta oleivora in 

Argentina. Infection levels after release were high, but no information is available 

about their persistence. The project has been discontinued (cf. Maniania et al., 2008). 

A point of major concern in integrated control programs is the quality of 

biological control agents. Predatory mites have been used for several decades for the 

control of spider mites in horticultural and agricultural crops. Low performance of 

predators has revealed the presence of pathogens. For reviews is referred to Schütte 

and Dicke (2008), Bjørnson (2008) and Hoy and Jeyaprakash (2008). Microspora 

species have been causing problems in mass cultures of several species of 

Phytoseiidae, in particular Amblyseius barkeri and A. cucumeris, but they are also 

known to occur in Phytoseiulus persimilis and Metaseiulus occidentalis. Sanitary

300 


measures and careful selection of uninfected lines of predatory mites are still the 

only solution to these problems. Acaricomes phytoseiuli is a bacterium that affects 

the behavior and predacious capacity of P. persimilis. This bacterium has not yet 

been encountered in mass rearings for the predator, but it will be clear that screening 

for such pathogens is necessary. Another group of bacteria that can cause 

considerable damage in mass cultures of beneficial mites and insects are Wolbachia 

sp., Cardinium sp., Spiroplasma sp. and other bacteria that affect sex ratios and that 

may cause incompatibilities between strains of the same species. This type of 

bacteria is widespread in mites and other vertebrates 

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12 

IPM STRATEGIES THROUGH SPECIALIST AND 

GENERALIST PHYTOSEIIDS (ACARI, 

MESOSTIGMATA) 

SAURO SIMONI AND MARISA CASTAGNOLI 


Research Centre for Agrobiology and Pedology 

via di Lanciola 12/A, Cascine del Riccio, 


Abstract. The exploitation of natural enemies, especially the predaceous mites phytoseiids, has become a 

fundamental factor for IPM in integrated crop production in Europe and worldwide. In controlling 

harmful insect and mite species, various species/strains from this group of predators are commonly used 

and marketed. Intrinsic biological traits of phytoseiids allow their ranking in different life style types. 

These factors, together with their quick adaptability to face new emergencies (i.e. phytophagous and 

exotic pests outbreaks and new environment or climatic conditions) confirm their role as a significant and 

sustainable tool in biological control. In this chapter the foundations for a more intensive adoption of 

phytoseiids are underlined, including the enhancement and introduction of new strategies aiming at a long 

term and efficient pest control. 


The need to increase food availability hardly couples with better chances to limit 

plant pests in modern agriculture, and several actions aim worldwide at increasing 

crop production and facilitating food and commodities trade. These efforts include 

lengthening of the plant/crops seasonal life or strategies increasing the consistent 

uniformity of varieties and cultivars used which represent, in fact, useful factors for 

business at small time scale. However, these actions are not always suitable to 

prevent a multitude of pest infestations on a regional scale. Since pests are also 

persistently poised for plant invasion, preventive and early remedial pest 

management strategies and treatments are needed at regular time intervals, in almost 

any cropping system (Sparks, 1999; Jarvis, Mar., & Sears, 2006; Gerson & 

Weintraub, 2007). 

311 




312 

S. SIMONI & M. CASTAGNOLI 

Given the worldwide trend towards crops with high genetic uniformity, much of 

the biodiversity found in the context of agroecosystems is sustained and maintained 

by means of the marginal environments surrounding productive areas. Any loss of 

such diversity due to crop management choices reduces farmers capacities to cope 

with plant stress factors. These include biotic factors like extreme temperatures, 

drought and salinity (Wang, Vinocur, & Altman, 2003). Consequently, due to the 

synergies occurring among biotic and abiotic stress factors, the problems that much 

of the world population practicing subsistence agriculture has to face are also 

emphasized. Furthermore, and typically in plants that regularly shut down, periodic 

inspections by specialists involved in integrated pest management (IPM) are needed 

for monitoring (with related costs). On the other hand, in more intensive agricultural 

systems, crop production in field or under protected conditions, whether in climatecontrolled 

greenhouses and glasshouses or tunnels with little or no climate control, is 

increasing worldwide, due to market demand, demographic pressure and/or 

unavailability of suitable environments. Although these last cropping systems are 

closed and relatively protected, they still remain vulnerable to known or invasive pests. 

The general and pressing consumers demand for healthy products, the increasing 

legal restrictions on pesticides, along with the increase in resistance to pesticides, is 

driving the greenhouse industry to apply as many non-chemical solutions as possible, 

so that different kinds of control strategies have to interact (Hussey & Scopes, 1985; 

Tanigoshi, Martin, Osborne, & Peña, 2004; Gillespie & Raworth, 2004). In addition, 

during the last decade there has been a consistent and widespread increase in market of 

foodstuffs and other “biological” products. These are associated with natural and 

healthy processes even if this association is frequently far from to be ascertained. 

Many countries, i.e. United Kingdom, have adopted strategies to reduce reliance on 

pesticides and encourage, or in some instances force, growers to consider other 

strategies in managing pests. This aim was pursued in 2006 by i.e. lowering 

registration fees associated with the development of biopesticides, in an effort to 

increase availability of reduced-risk pesticides to growers (ESRC, 2008). 

Campaigns against the use of pesticides in agriculture in the EU led to an increase 

of the production area and market size of the greenhouse industry, introducing 

biological control in many agricultural systems. Frequently and realistically, in spite of 

the great emphasis on the use of “natural” techniques concerning control and 

production requiring the exclusion of artificial products, biological/organic agriculture 

do not appear so different from most modern “conventional” regimes: these processes 

can be indeed largely based on the use of active ingredients, natural but still toxic that, 

on a different scale, could yield problems similar to those already known for pesticides 

(i.e. residues on foodstuffs, side effects on non-target organisms). 

The global situation of pests control and the increasing efforts, both in biological 

and IPM agriculture, related to the adoptions of sustainable ways can be affected by 

the lack of whole efficacy of these products, more than by a loss of strategic trust in 

pesticides. Given this context and perspectives, the control of pests matches frequently 

and unavoidably with the release and/or enforcing of natural enemies and antagonists 

already present on a crop (Bale, Van Lenteren, & Bigler, 2008).

PREDATORY MITES IN IPM 

313 

Among natural enemies of arthropod pests, predaceous mites Phytoseiids 

(Acari: Mesostigmata), became in the recent years a fundamental tool for IPM in 

integrated crop production in Europe as well as worldwide. Various species or 

strains belonging to this group of predators are commonly used and marketed to 

control harmful insect and mite species. The phytoseiids ranking in different life 

style types, together with their quick adaptability to face new emergencies confirm 

their role as a significant and sustainable tool in biological control. In this chapter 

we review the basic concepts related to and the possible use of phytoseiids, 

including the enhancement and introduction of new strategies for efficient pest 

control, durable in time. 

2. CONCEPTS ON NATURAL ENEMIES AND/OR ANTAGONISTS IN IPM 

The role of natural enemies and/or antagonists in IPM and the degree at which 

biological control agents (BCAs) can be exploited vary from crop to crop and from 

area to area. Some questions need consideration and precise answers, before 

deciding on effectiveness of natural enemies against major pests on a crop system 

and defining the guidelines for their application or safeguard. One the most 

important issues concerns the occurrence of effective natural enemy on the 

considered pest and if, from an economic and ecologic point of view, it is more 

convenient to introduce mass reared enemies or to facilitate the colonization of the 

crop by local populations, from the surrounding areas. The crops or vegetation types 

adjacent to the targeted crop are important, since some plants can act as possible 

refuge for natural enemies, while others can harbour unwanted pests. 

Crops grown under "organic" or "conventional" regimes obviously need 

different approaches for pest management. If the crop is "organic" it can provide 

added incentives to the use of biocontrol methods. However, a crop does not have to 

be grown organically to benefit by the use of biocontrol methods. "Soft" chemical 

options must be found for use in conjunction with natural enemies. Furthermore, 

crop life span and environment have to be suitable enough for harboring natural 

enemies. Generally, it can be difficult to establish BCAs in short lived crops. Also, 

the knowledge about plant life stages suitable for natural enemies is important, since 

BCAs may be most appropriate at a particular stage of the growing cycle. 

In addition to these questions, there are those related to the cost, practicality and 

degree of difficulty encountered when controlling key pests with chemical means 

alone and/or natural enemies, and when assuming which strategy is more demanding 

in terms of cost, efficiency or healthy status returns. Furthermore, difficulties are 

encountered when switching from a conventional towards an IPM or organic system. 

Practices and routines need to be modified continuously as new information must be 

gained during this process. Regular monitoring is necessary to identify pest 

outbreaks and their location within a crop. Also, "soft" controls methods should be 

checked and tested, since they may be available for some pests, but not for others. 

When an antagonists-based strategy is adopted, some damage induced by pests 

must be tolerated, since a minimum number of individuals may be required to 

support a useful population of its natural enemy. Deciding whether or not spraying

314 


(and when) can represent a further difficulty. However, if "soft" options are 

available for the pest in question, this is not such an issue. The identification of the 

most appropriate release timing is necessary when introducing natural enemies and 

to get them established quickly and maintained along. The introduction of 

appropriate numbers of mass reared BCAs is another condition necessary to 

facilitate quick establishment. 

Another aspect to be considered is providing a suitable environment. Very hot 

dry conditions are not conducive to some BCA's and research programs were 

recently developed (Palevsky et al., 2006). Adjustments may need to make to favour 

BCA's, e.g. shade, windbreaks, overhead watering. Having an expectation that one 

cannot spray chemicals at all could be incorrect and may result in failure of the IPM 

system. BCA's usually recover from occasional sprays of moderately toxic products 

and can remain at useful levels. 

Actually, by referring to the state of knowledge on animal organisms and to the 

complex represented by phytophagous-natural and/or commercial enemies, 

consolidated strategies (and not only theoretical approaches) are available for 

farmers. They aim, among the several factors involved, to the reconstitution of the 

populations balance and to the improvement of the action against enemies. This 

objective is pursued by: (i) the diffusion of antagonists, (ii) the elimination of 

sources of perturbance and (iii) the adoption of environmental and cultural 

management measures. 

This chapter deals with the phytoseiid mites, which have a significant role on 

control of crop pests in greenhouse and field conditions, worldwide. By focusing on 

the definition of DeBach (1964), biological control is: the study and uses of 

parasites, predators and pathogens for the regulation of host (pest) densities. Two 

main principles are included in this review: (1) most organisms are consumed by 

other organisms and this can be exploited by the man as “natural control”, (2) this 

natural/biological control reduces, rather than eradicates, the pest. As a consequence, 

a number of important pests can be kept at a low population density by biological 

control agents over long time periods or, differently, populations of pests are 

reduced but further releases, or additional methods are needed to achieve an 

adequate level of control. Among BCAs, phytoseiids are, for their traits, highly 

capable to efficiently interface with rapidly changing contexts, as crop and 

environment turn over. At the same time, the great versatility of some species seems 

to guarantee long lasting control expectancy of pests and a presidium of the area 

with an acceptable level of related costs. 

3.1. Mass Rearing 

3. WHY PHYTOSEIIDS? 

The breeding of auxiliaries is a very complex task, requiring the development of 

refined and very reliable techniques. The high cost involved, together with the need 

to be supported by a sure market, has sometimes considerably limited the use of 

natural enemies. However, the environments to be protected usually hosts intensive 

or expensive cultures and, on the other hand, do not facilitate the dispersion of the


315 

antagonists. For this reason, processes optimising their efficacy and persistence are 

needed. 

A combination of control efficiency with low production costs and receptive 

markets is needed to support the development of effective mass rearing technologies 

for selected antagonists, including importation and cultures of appropriate natural 

enemies on alternative food, automated productions, testing of technologies for 

production and quality of predators, processing, storage, packaging, distribution and 

release of natural enemies of insect and/or weed pests. Recently, more and more 

effective augmentative and classical biological control strategies for key pests have 

been developed. 

Phytoseiids satisfactorily match all the needs of the production pathway and 

their production and marketing sensibly increased in the last years (Van Lenteren, 

2003). Some species i.e. Phytoseiulus persimilis and Neoseiulus californicus (Fig. 1) 

are worldwide employed in control strategies. They have been widely and 

successfully used in the biological control of tetranychids phytophagous mites, for 

over half a century and more recently for thrips and aleurodids (Gerson & 

Weintraub, 2007; Messelink, Van Steenpaal, & Ramakers, 2006; Messelink, 

Maanen, Van Steenpaal, & Janssen, 2008). For many phytoseiids species the rearing 

can be conducted on a number of alternative preys, which lowered considerably the 

costs. 

Figure 1. Phytoseiulus persimilis preying on Tetranychus urticae on strawberry leaf (A), and 

Neoseiulus californicus preying astigmatid mite on rearing unit (B). 

The large number of studies on biological traits of phytoseiids allowed 

producers to determine and/or automate the best mass rearing techniques and to 

establish their potential for control. At the same time research from bioindustries 

contributed to increase the bulk of knowledge, not only in terms of production 

standards and/or protocols to evaluate the quality and efficiency of reared predators, 

but also in terms of benefits for the theoretical study of predator-prey interactions.

316 


3.2. Fitness and Adaptation Characters 

Phytoseiids have a short life span and are relatively easy to rear in the laboratory. 

For these reasons they are frequently chosen as a subject for basic studies on the 

mechanisms regulating the herbivores-predators-plants relationships. Some effective 

phytoseiids proved to retain high developmental and population increase rates on 

prey (Table 1), as well as good numerical and functional responses on prey density 

(Nachman, 1981; Sabelis, 1986; Castagnoli & Simoni, 1999). Data are available also 

on population dynamics and density changes in both seasonal and spatial 

distribution studies (Sabelis & Bakker, 1992; Sabelis & Janssen, 1994), as well as on 

mechanism and cues which determine the search of prey and infested plants (Sabelis 

& Van der Baan, 1983; Takabayashi, Dicke, & Posthumus, 1991). Data on the 

characteristics and occurrence of diapause and on the abiotic factors involved in its 

induction, maintenance and termination (i.e. photoperiod, temperature and food 

availability), are available for phytoseiid mites, as well as knowledge about the 

physiological mechanisms and related applied aspects (Veerman, 1992). 

Table 1. Intrinsic rate of increase (r m ) and population doubling time at about 25°C 

of phytoseiid species, largely utilized in biological control. 

Phytoseiid species 

Prey 

r m 

(day –1 ) 

Doubling time 

(days) 

References 

Phytoseiulus 

persimilis 

Neoseiulus 

californicus 

Tetranychids 0.317 2.19 


Takafuji and Chant 

(1976) 

Castagnoli and 

Simoni (1991) 

Neoseiulus cucumeris 

Tetranychids 

Thrips 

0.174 

0.178 

3.98 

3.89 

Castagnoli and 

Simoni (1990) 

Amblyseius swirkii Whitefly 0.213 3.25 

Nomikou, Janssen, 

Schraag, and Sabelis 

(2001) 

Galendromus 

occidentalis 


Tanigoshi, Hoyt, 

Browne, and Logan 

(1975) 

However, the phytoseiids reproductive strategy is the trait which perhaps makes 

these predators quite peculiar. In arrhenotokous arthropods males arise from 

unfertilized eggs and, by controlling the fertilization process, mothers can adjust the 

sex ratio in their offspring. In pseudo-arrhenotokous phytoseiid mites, males are 

haploid, even if arising from fertilized eggs. The haploid state is achieved through 

elimination of a chromosome set during the embryonic development. Phytoseiid 

females can control the sex ratio in their offspring and this control seems extremely 

flexible (Nagelkerke & Sabelis, 1998). As predicted by current evolutionary theory


317 

of sex allocation, sex ratios approached half males, half females under random 

mating, whereas a female bias was observed under sib-mating. It is suggested that 

arrhenotoky is selected for when there is a substantial risk of high portion of 

unmated females in the population: pseudo-arrhenotoky may evolve by 

external/environmental pressure, since it retains the possibility to reinstall lost genetic 

information in the maternally derived chromosome, by using the paternal chromosome 

as a template for DNA-repair. This precise control of sex allocation in phytoseiids is 

probably the significant mechanism by which these predators can regulate their 

density, depending on both phytoseiid female and prey densities. They can in fact 

adjust offspring sex ratio in response to the presence of conspecifics or their cues and 

also to synchronize their population with that of prey (Nagelkerke & Sabelis, 1996). 

The prediction of optimal sex ratio by means of modeling is selectively advantageous 

when local mating groups vary in size and are usually small, as in the case of 

experimental laboratory studies on phytoseiids. At a larger spatial scale than the local 

mating group, the prediction appears to be less precise, may be due to operating and 

interfering selection levels (Nagelkerke & Sabelis, 1998). 

3.3. Life Style Types 

The characterization and ranking of phytoseiid mites is a helpful and significant tool 

(McMurtry & Croft, 1997), allowing a rating of species based on some 

morphological, reproductive and developmental aspects. Furthermore, traits like 

feeding and diet needs (McMurtry & Rodriguez, 1987; Schausberger & Croft, 1999) 

and adaptation to certain foods (Castagnoli, Simoni, & Liguori, 2003), were 

considered to ascribe the predators to the different life styles. McMurtry and Croft 

(1997) considered that a four-types classification may be efficient to rank the 

different species of phytoseiids and gave emphasis to the biological control of spider 

mite pests (Table 2). However, new life style types might be identified. 

Recent studies aimed at estimating/identifying the more significant traits 

involved in phytoseiids rating and to possibly generate more stable classifications 

(Croft, Blackwood, & McMurtry, 2004). The mainly and first exploited traits/factors 

to rate phytoseiids were: (i) Feeding: the ability to prey and to feed on various prey 

and other food types (McMurtry & Rodriguez, 1987; McMurtry, 1992), a primary 

criterion considered for classification; (ii) External morphology: apparently, no 

strong correlation was found between body size and generalist–specialist phytoseiids 

(Schuster & Pritchard, 1963; Chant & Hansell, 1971) and more evidence is needed 

to establish the association between body size and different life styles (Croft et al., 

2004); more correspondence was found in the evaluation of the adult dorsal shield 

setal length, in association with the feeding specialization (Sabelis & Bakker, 1992). 

Also, the mouthpart apparatus may be different between specialists and generalists 

(Flechtmann & McMurtry, 1992), but it is not clear to what extent this could work 

for a clear attribution to a life style; (iii) Biological parameters: research focused on 

reproduction, development and mortality; the specialist phytoseiids generally show 

intrinsic rates (Sabelis & Janssen, 1994) and sex ratio values higher than generalist 

(Nagelkerke & Sabelis, 1996) as well as shorter developmental times (Luh & Croft,

318 


1999, 2001). Concerning mortality, studies characterized more exactly the 

dependence on prey density and the rate by which this changes. Through mortality, 

species differently adapt to varying prey or food levels, in the different life style 

types: the specialist species shows a tendence towards fast response to higher prey 

densities than a generalist, whereas a generalist tends to persist for a longer time, at 

limited or scarce prey density (Walzer & Schausberger, 2005; Simoni, Castagnoli, & 

Liguori, 2005). 

Table 2. Categorization of phytoseiids life style types by McMurtry and Croft (1997). 

Type Strategy a Crop b 

Type I spp. 

Phytoseiulus persimilis 1, 2, 3 L, G 

P. macropilis 2 L 

P. longipes 2 L, G 

Type II spp. 

Galendromus annectes 1, 2 T 

G. helveolus 1, 2 T 

G. occidentalis 1, 2, 3 T, L, V 

Typhlodromus (T.) rickeri 

T 

Neoseiulus bibens 1 L, Sh 

N. californicus 1, 2 T, L, V 

N. fallacis 1, 2, 3 T, Sh, L 

N. idaeus 1, 3 Sh, L 

N. longispinosus 1, 2 T, Sh, L 

N. tiki 1 Sh, L 

Type III spp. 

Typhlodromus (T.) pyri 1, 2 T, V, Sh 

T. (T.) exhilaratus 1 T 

T. (Anthoseius) caudiglans 1 T 

T. (A.) doreenae 1 V 

Metaseiulus arboreus 1 T 

M. citri 1 T 

M. pomi 1 T 

Paraseiulus soleiger 1 T


319 


Type III spp. (continued) 

Phytoseius macropilis 1 T 

P. spoofi 1 T 

Amblyseius andersoni 1, 2 T 

A. eharai 1 T 

A. swirskii 1 T 

Neoseiulus barkeri 2 G 

N. cucumeris 1, 2 L, G 

N. umbraticus L, T 

Kampimodromus aberrans 1,2 T, V 

Typhlodromalus aripo 1, 3 Sh 

T. limonicus 1 T, Sh 

T. manihoti 1, 3 Sh 

Typhlodromips sessor 

T. newsami 1, 2 T 

Iphiseius degenerans 1, 2 T, Sh, G 

Type IV spp. 

Euseius addoensis 1 T 

E. elinae 1 T 

E. finlandicus 1 T 

E. fructicolus 1 T 

E. sojaensis 1 T 

E. tularensis 1 T 

E. stipulatus 1,3 T 

E. victoriensis 1 T 

a Strategies: 1 = conservation; 2 = augmentation; 3 = importation and establishment. 

b Crops: L = low-growing; G = greenhouse; T = tree; Sh = shrub; V = grapevine. 

A considerable amount of studies has been recently added concerning the 

evaluation of the different degree of responses by generalists and specialists 

predators, as a consequence of their different physiology and behaviour. Even if a 

build up in basic physiological studies is still necessary, physiological and 

behavioural responses were analysed frequently and in different contexts. 

Preliminary studies indicate appreciable differences among life styles. One of the 

most remarkable concerns the response to odours produced by preys, other foods, 

competitors, host plants and other habitat-related elements (Blackwood, Luh, & 

T

320 


Croft 2004; Gnanvossou, Hanna, & Dicke, 2003; Schausberger & Croft, 2001). In 

particular, host–plant relationships seem to be especially affected by the intrinsic 

physiological traits, and generalists have closer associations with host plants than 

specialist phytoseiids do (Kreiter, Tixier, Croft, Auger, & Barret, 2002; Tixier, 

Kreiter, Croft, & Auger, 2002). Specialists also tend to aggregate mostly in 

proximity of preys, by suffering sometimes higher mortalities (McMurtry & Croft, 

1997; Faraji, Janssen, & Sabelis, 2002), whereas the perception of the prey cues can 

lead to different inter and/or within plant dispersal. 

It should be considered that the phytoseiids life style categorization is not a 

dogma, although it can be represent a dynamic underlying support in setting control 

strategies of different pests. To determine the value of each definition, a sort of 

holistic approach would be advisable, by considering more factors and criteria in the 

grouping. Future studies are needed to estimate both the optimal numbers of traits 

and numbers of life styles type, simultaneously. Such fitting problems, or more 

robust classifications, probably will require the use of a multi-sample classification 

methods. By this point of view, significant trials were performed by Luh and Croft 

(1999, 2001) by a computer-based genetic algorithm, and by Blackwood et al. 

(2004), by a discriminant analysis model. The results obtained by Luh and Croft 

(2001) were in full agreement with the ranking of McMurtry and Croft (1997): just 

one, Neoseiulus longispinosus, out the 20 species considered in the two 

categorizations shifted by one style type level. The selection of subsets of variables 

optimizing the classification and reducing the chance of misclassification of traits 

included for best fit, shows to be effective as identifying potential useful indicators 

of life style type. 

3.4. Single or Multiple Antagonists Release 

Several herbivores can be usually attacked by numerous predator species but, 

historically, studies concerning single prey-single predator interactions were mainly 

performed (Holling, 1966; Hassell, 1978; Kareiva, 1994). A controversial issue was 

the use of a natural enemy complex, as opposed to a single enemy strategy, to 

achieve the best biological control (Ehler, 1990; Riechert & Lawrence, 1997; Losey 

& Denno, 1998). As concerns mite pests management, control in different 

agricultural systems was generally performed by adopting the release of a single 

phytoseiid species. More sporadic were evaluations about the release of two or more 

species. The interaction and dynamics of different phytoseiids spp. with, evenly, 

different life styles, may return different responses in comparison with the expected 

outcome (Helle & Sabelis, 1985; McMurtry & Croft, 1997; Schausberger & Walzer, 

2001; Castagnoli, Simoni, & Nachman, 2001). 

Walzer and Schausberger (2005) evidenced that the combination of a specialist 

predator as Phytoseiulus persimilis and a diet-generalist as Neoseiulus californicus 

in a sustainable way, might control spider mite, with higher efficiency in perennial 

crops. Control on eggplant and pepper was achieved by single N. californicus 

release (Castagnoli, Liguori, & Simoni, 2005). Simoni et al. (2005) evaluated the 

same phytoseiids and P. persimilis alone, by means of single and combined releases, 

on the same infested solanaceae as well as on tomato, in order to evaluate if their


321 

effect was additive, multiplicative or detrimental in the action of predators. The notoverlapping 

degree of specialization, narrow in P. persimilis, wider in N. 

californicus, and the consequent asymmetry in the response guaranteed, for some 

weeks, fast (mainly due to P. persimilis) and longer (mainly due to N. californicus) 

term equilibrium of the prey-predator system and of biological control, especially on 

eggplant and pepper. 

As concerns the ascertained intrinsic traits and versatility of some phytoseiid, N. 

californicus appears able to adapt to different food and climatic conditions 

(Castagnoli & Simoni, 2004), and it may be considered feasible and convenient if 

combined to or in light shifts of phytoseiid releases, or in application with some 

other kind of biocontrol agents (i.e. other mites, insects or the fungus Beauveria 

bassiana). Obviously, the adoption of such a tactic needs an intensive monitoring, a 

full evaluation of the possible effect of the microrganism on the predator and an 

assessment concerning the possibility that the phytoseiid is able to recognize the 

treated substrate (Simoni, Guidi, & Tarchi, 2009). 

3.5. Cannibalism and Intraguild Predation 

The coexistence and interaction of two different phytoseiids species sharing a 

common prey resource can undoubtedly determine new functional-trophic relations 

(Rudolf, 2008). Intraguild predation and cannibalism are, in cases of combined 

release of predators, variables to be included in current models aiming at 

overcoming the discrepancy between theory and empirical data. 

Although cannibalism may often represent a weak, unuseful interaction in 

nature, it may have significant consequences at the population level (McCann, 

Hastings, & Huxel, 1998). Cannibalism can be a crucial factor contributing to 

population structure, dynamics and control in a given habitat (McCann et al., 1998), 

affecting the quantity and quality of food for the remaining individuals. Predatorpredator 

interactions such as competition, intraguild predation (IGP), and 

cannibalism affect the development and coexistence of predator populations, and 

can have significance in the biological control of commonly exploited pest 

organisms (Castagnoli, Liguori, & Simoni, 2002; Schausberger & Croft, 2000). 

Furthermore, phytoseiids are suitable models for studying cannibalism and related 

phenomena, due to their diversity and variability, small size and ease of rearing in 

the laboratory. In future research and in the frame of tactics and strategies of control, 

most fields are to be exploited, i.e. kin the link of cannibalism with discrimination 

and disease transmission, the interplay between cannibalism and dispersal, and the 

effects of cannibalism on population dynamics and species communities. 

4. CONCLUSIONS 

Given the number and complexity of factors involved in the wide pattern of natural 

enemies and antagonists, phytoseiid mites appear able to significantly interact in the 

dynamic equilibria of different prey-crop contexts. The modality of agricultural 

pests control by these predators can range from classical biological control, with 

introduction and establishment of foreign species, to safeguard and augmentation of

322 


indigenous species. Perspectively, it appears convenient to stress further the search 

for appropriate control strategies and tactics, on which phytoseiids have a dominant 

role. Phytoseiids proved to be able to quickly adapt to new environmental conditions 

(Helle & Sabelis, 1985). Laboratory selection of phytoseiids produced several 

strains with different traits as no-diapausing strains, strains adapted to live on 

unsuitable hosts or more resistant to adverse climate or pesticides (Castagnoli, 

Liguori, Simoni, & Guidi, 1998; Castagnoli, Liguori, & Simoni, 1999; Castagnoli 

et al., 2003; Drukker, Janssen, Ravensberg, & Sabelis, 1997; Fournier, Pralavorio, 

Berge, & Cuany, 1985). Frequently, these adapted strains have been mass reared and 

released for pest management programs in glasshouses and agricultural cropping 

systems. The majority of researches on the argument show that the release of 

phytoseiids for augmentation or classical biological control programs involves 

minimal risk for the environment and indigenous predators, with great benefits 

(Pilkington, Messelink, Van Lenteren, & Le Mottee, 2009). 

The development of recombinant DNA techniques for the genetic manipulation 

of crops and microorganisms may be successfully applied also to phytoseiids, and 

much debated opinions concern risks of transgenic phytoseiids release. Great 

attention and punctual researches still need to address the real impact in the 

environment of phytoseiids that have been manipulated with genetic techniques. 

These studies, further to answer to the question, could again provide opportunities to 

expand our understanding of the ecological impact of phytoseiids in agricultural and 

natural environments, and lead to improved pest management tactics (Hoy, 1992). 

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α-copaene, 92 

α Proteobacteria, 257 

α-ylangene, 92 

β-exotoxin, 254 

δ-endotoxin, 254, 255 

(1R-CIS)-3-isopropenyl-2.2- 

dimethylcyclobutyl-methyl acetate, 

14 

(3Z, 6R)-3-methyl-6-isopropenyl-3.9- 

decadien-l-yl acetate, 14 

1,4 diaminobutane, 32 

16S rDNA, 255, 258, 296 

18S ribosomal DNA, 268 

18S, 118 

4,8-dimethylnona-1, 3, 3-triene, 200 

4-methyl-5-nonanol, 218 

4-methyl-5-nonanone, 218 

5.8S, 118 

5.8S rRNA gene, 118 

A 

Abacarus hystrix, 265, 274, 275 

Abamectin, 21, 24, 25, 44, 68 

ABC, 17, 19 

Abdomen, 75, 87, 89 

Abdominal segments, 80 

Abundance, 107, 109, 111, 112, 113, 

115, 123, 137, 140, 195, 199, 204 

Acacia, 76, 79 

Acalitus vaccinii, 275 

Acalyptris minimella, 83 

Acarapis woodi, 253 

Acari, 61, 66, 67–68, 77, 249, 250, 

273, 295, 299–300 

Acaricidal preparations, 299 

Acaricides, 5, 21, 23, 51, 53, 251, 254, 

255, 278, 279, 283, 285, 297, 299 

Acaridae, 264, 274, 280, 287, 288 

Acariformes, 11 

Acariformis phytoseiuli, 300 

Acarofauna, 69 

Acarogregarina corolla, 287 

Acaromyces ingoldii, 285 

Accidental introduction, 74 

INDEX 

Accuracy, 117, 119 

Aceratoneuromyia indica 

(= Syntomosphyrum indicum), 20 

Aceria (Eriophyes) guerreronis, 278 

Aceria cynodoniensis, 275 

Aceria guerreronis, 275, 279 

Aceria sheldoni, 29, 30, 50, 51, 275 

Aceria tulipae, 252, 306 

Aceria vaccinii, 283 

Aceria, 252, 275, 278, 283, 306, 308 

Acetamiprid, 21–24, 45, 68 

Acetosphora, 289 

Acetylated derivatives, 200, 208 

Achaia, 30, 31, 48 

Acrididae, 7 

Acrinathrin, 21, 23, 24 

Acrobasis nuxvorella, 138 

Acrosternum hilare, 155 

Active compounds, 22 

Active ingredient, 22–24, 26, 66–68, 

279, 299 

Active substances, 35, 39, 41, 44, 47, 

49, 50, 53 

Activity, 214, 233 

Aculodes, 265 

Aculops lycopersici, 275 

Aculops pelekassi, 11, 29, 30, 50, 51 

Aculus fockeui, 265 

Adalia bipunctata, 46 

Adalia decempunctata, 46 

Adaptation, 190, 192, 196, 205 

Adelina acarinae, 288 

Adhesive knobs, 115 

Administrative boundaries, 165 

Adulticides, 104 

Adults, 13, 14 

Aegina, 31 

Aerial control, 240 

Aerial platforms, 167, 172 

Aerial treatment, 240–241 

Afghanistan, 83 

Aflatoxin, 284 

Africa, 83, 87, 89, 164, 165, 170, 

172, 173, 181, 182, 184, 185, 187, 

327 



DOI 10.1007/978-90-481-8606-8, © Springer Science+Business Media B.V. 2010

328 

INDEX 

237, 238, 241, 268, 269, 271, 280, 

298, 305, 309 

African citrus psylla, 6 

Aganaspis (Trybliographa) daci, 34 

Ageniaspis citricola, 43, 54, 63, 81, 

82 

Aggregation Pheromone Traps, 209, 

218, 223, 231 

Aggregation pheromone, 209, 211, 

218, 219, 222, 223, 231–233 

Agistemus, 264 

Agricultural systems, 312, 320 

Agriculture, 22 

Agrobacterium tumefaciens, 137, 141 

Agrochemicals, 5 

Agroecosystem, 47, 312, 324 

Agromyza hiemalis, 84, 97 

Agromyzidae, 84, 97 

Agronomic management, 94 

Agronomist, 31 

Air currents, 236 

Airways, 236 

Alaskozetes antarcticus, 265, 268, 301 

Albendazole, 294 

Alder, 76 

Aleurocanthus spiniferus, 74, 98 

Aleurocanthus woglumi, 74 

Aleuroclava jasmini, 74 

Aleurodicus dispersus, 74 

Aleurothrixus floccosus, 8, 23, 29–31, 

40–42, 55, 57, 62–64, 74, 93, 97, 98 

Aleyrodidae, 8, 23, 29, 30, 40, 41, 

54–58, 63, 64 

Alfamethrin, 21 

Algae, 286 

Algeria, 4, 82 

Alimentary tract, 250, 252, 253, 254 

Allergenic structures, 236 

Allium canadense, 196 

Allium, 252 

Alloxysta, 46 

Almond, 76 

Alnus rubra, 193, 208 

ALOS, 168 

alpha-cypermethrin, 21, 23, 24 

Alternate prey, 153 

Alternative host plants, 140 

Alternative hosts, 61, 67, 84, 86 

Alternative prey, 68 

Aluminum phosphide, 217, 218 

Amaranthus, 143 

Amblyseius andersoni, 51, 319 

Amblyseius barkeri, 299 

Amblyseius cucumeris, 299 

Amblyseius eharai, 319 

Amblyseius igarassuensis, 264 

Amblyseius swirskii, 319 

Amblyseius, 264, 276, 288, 292, 300, 

308 

America, 135, 159, 160, 162 

Ameronothridae, 265, 268 

Amitus spiniferus, 63, 93 

AML, 177 

Ammonia, 35 

Ammonium acetate, 32 

Ammonium, 92 

Amoebae, 286 

Amoebozoa, 286 

Amrineus cocofolius, 274 

Amsterdam, 249, 300, 303, 305, 308 

Amudarya River, 178, 186, 187 

Anacridium aegyptium, 7 

Anagyrus pseudococci, 38, 65, 66, 

71, 87, 88 

Anal atrium, 294 

Anal tuft, 239 

Anaphe panda, 239 

Anaphe, 239, 244 

Anaphylactic reactions, 236 

Ancylistaceae, 261, 262 

Angelica archangelica, 92 

Animal manure, 106, 111, 114 

Animals, 237, 239 

Anisolabis maritima, 215 

Annual broadleaf weeds, 146 

Anoplophora chinensis, 74 

Antarctica, 163 

Antennae, 80, 87 

Anthelidae, 236 

Anthracnose, 141 

Antibiotics, 259, 296 

Antidesiccants, 228, 232

INDEX 

329 

Ants, 13, 46, 47, 78, 81, 87, 88, 93, 

95, 96 

Aonidiella aurantii, 6, 9, 14, 23, 29–31, 

36, 37, 39, 63, 65, 74–76, 78, 94, 

97, 99, 100 

Aonidiella citrina, 74 

Apex, 50, 75, 262 

Aphelinidae, 37, 40, 54, 55, 58, 77, 

79, 93, 97, 98, 99 

Aphid colonies, 47 

Aphid parasitoids, 69 

Aphid populations, 69, 153, 154, 155 

Aphid predators, 46 

Aphid species, 139, 162 

Aphid vector, 94 

Aphid, 14, 53 

Aphidae, 67 

Aphidicides, 139 

Aphididae, 8, 23 

Aphidius colemani, 69 

Aphidius matricariae, 46 

Aphidius urticae, 46 

Aphidophaga, 153, 154, 157 

Aphidophagous coccinellid, 46 

Aphidophagous insects, 48, 133, 154 

Aphids, 13, 14, 22, 23, 29–31, 42, 

45–48, 53, 55, 68, 69, 134, 139, 

140, 142, 148, 152, 153, 154, 156, 

157, 159, 161, 193, 194, 200 

Aphis craccivora, 8, 45 

Aphis fabae, 8 

Aphis gossypii, 8, 23, 29, 45, 56, 62, 

63, 65, 67, 75, 94, 99 

Aphis nerii, 67 

Aphis spiraecola, 8, 23, 29, 45, 65, 

67, 74, 94 

Aphytis chilensis, 38 

Aphytis chrysomphali, 38, 77 

Aphytis coheni, 37 

Aphytis lepidosaphes, 30, 37, 63 

Aphytis lingnanensis, 37, 63, 77 

Aphytis melinus, 37, 63, 65, 77, 78, 

97, 98, 99, 100 

Aphytis proclia, 77 

Aphytis yanonensis, 10 

Apical twigs, 13 

Apicomplexa, 286, 287, 289 

Apis mellifera, 253 

Apotetrastichus postmarginalis, 86 

Apotetrastichus sericothorax, 86 

Apples, 31 

Application threshold, 36 

Application, 35, 50, 51, 226, 233, 

249, 250, 273, 279, 281, 283, 284, 

297, 299, 308 

Aprostocetus, 86 

Aqueous suspension, 251 

Arabidopsis thaliana, 200, 202 

Arabidopsis, 197, 198, 207, 208 

Arachnida, 70 

Aralia, 76 

Araneae, 70 

Araucaria, 76 

Arbutus unedo, 238 

Archery equipment, 134 

Archips rosanus, 10, 75, 94 

Arctiidae, 134, 236 

Arctoseiinae, 264 

Arctoseius, 264 

Argentina, 82, 278, 299, 307 

Argentine ants, 154, 161 

Argolis, 30, 31, 42, 43, 54 

Arizona, 135, 251, 297 

Armoured scale, 14, 37, 38, 75, 94, 99 

Arrhenotokous, 50, 259 

Arrhenotoky, 317 

Arrowleaf sida, 143 

Artemisia, 181 

Arthrobacter globiformis, 256 

Arthrobotrys oligospora, 115 

Arthropod densities, 151 

Arthropod hosts, 257 

Arthropod pest, 23, 29–31, 73, 313 

Arthropoda, 261 

Arthropodofauna, 69 

Arthropods, 6, 53, 67, 106, 112, 123, 

125, 126, 236, 246, 259–262, 277, 

286, 289 

Artificial habitat, 116 

Artificial media, 264, 270, 278, 295, 

297 

Artificially wounded leaves, 191, 200

330 

INDEX 

Asaphes vulgaris, 46 

Asaphes, 46 

Asca, 264 

Asci, 260, 286 

Ascidae, 275 

Ascomycota, 260, 272, 285 

Ascospores, 260, 286 

Asecodes delucchii, 86 

Asian Citrus Psyllid, 102 

Asparagus, 79 

Aspergillus flavus, 284, 307 

Aspergillus, 284, 296, 307 

Aspidiotus nerii, 9, 23, 39, 68, 74, 79 

Asterophora caloglyphi, 287 

Astigmatid mite, 315 

Astipalea, 42 

Asynonychus godmani, 11 

ATP synthase-subunit, 199 

Attack, 79, 81, 212, 235, 237, 240 

Attica, 31, 42, 44, 47, 58 

Attractants, 14, 21–23, 92 

Augmentation, 40, 55, 62, 101–103, 

105, 106, 111, 124, 129 

Augmentative biological control, 3, 

7, 21, 70 

Augmentative release, 53 

Aulacorthum solani, 8, 45 

Australasia, 64 

Australia, 43, 54, 57, 64, 66, 72, 82, 

83, 84, 89, 92, 96, 98, 170, 172, 

179–184, 239, 243, 244 

Australian plague locust, 179, 180, 

182, 184 

Authorization, 22 

Autogenous defensive secretions, 196 

Autumn, 13, 14, 104, 241, 267 

Avocado, 76 

Azadirachtin, 21–25, 41, 44, 47, 68 

Azobacter, 150 

Azocyclotin, 53 

Azores, 6, 12 

B 

Bacillus sphaericus, 256 

Bacillus thurigiensis var. aizawai, 21, 

22, 24, 49 

Bacillus thuringiensis var. kurstaki, 

21, 22, 24, 49, 240 

Bacillus thuringiensis, 67, 68, 107, 

134, 235, 236, 243–244, 254–256, 

299, 301, 303–304, 306 

Bacteria symbiosis, 123 

Bacteria, 105, 112, 116, 119, 123, 

147, 150, 151, 157, 209, 249, 255, 

259–260, 295, 300, 302 

Bacterial cells, 216 

Bacterial disease, 102 

Bacterial leaf scorch, 141 

Bacterial spores, 243 

Bacterium, 102, 113, 215, 235, 236, 

254, 255, 258, 259, 296, 300 

Bacteroidetes, 256, 259 

Bactrocera oleae, 35 

Baculoviruses, 295 

Baermann funnel, 121, 122 

Bahamas, 82 

Bahiagrass, 143, 146 

Bahrain, 209, 232 

Bait spraying, 34 

Balkans, 89 

Ballistospores, 261 

Banker plants, 67 

Baryscapus, 86 

Baseball bats, 134 

Basidiobolus, 264 

Basidiomycota, 260, 261, 272, 285 

Basque Country, 6 

Basudin, 217 

BC programs, 61, 64, 65 

BCAs, 313, 314 

Beauveria bassiana, 21, 22, 24, 216, 

231, 283, 284, 299, 321, 325 

Beauveria brongniartii, 283 

Beauveria, 283, 296, 299, 300, 305, 

307 

Bee Kashmir Virus, 253 

Bee, 148, 253, 284, 297, 302, 304, 

305, 307 

Beet army worm, 199, 201 

Beetle, 211, 232 

Behavior, 255, 300 

Beijing-1, 168

INDEX 

331 

Belgium, 175 

Belt, 240 

Bemisia hancocki, 8 

Bemisia tabaci, 8 

Beneficial arthropods, 5, 21, 25, 151, 

280 

Beneficial insects, 133, 139, 148 

Beneficial mites, 133, 249 

Beneficial organisms, 26, 102 

Benfuracarb, 21, 23–25, 68 

Benin, 271, 281, 298, 309 

Bergamot, 4, 22, 29, 73 

Bermudagrass, 143 

Bifentrin, 21, 23, 24, 25 

Big bud disease, 283 

Bigarade orange, 3 

Binodoxys acalephae, 46 

Binodoxys angelicae, 46 

Bioactivity, 218 

Biocides, 240 

Biocontrol agent, 215, 230 

Biocontrol methods, 313 

Biocontrol, 101, 103, 107, 110, 114 

Biodiversity, 192 

Bio-ecological equilibrium, 73 

Bioindustries, 315 

Biological control agents, 36, 235, 

236, 249, 251, 256, 285, 292, 298, 

299, 303, 308, 314 

Biological control programs, 74, 78, 

81, 89, 92, 93 

Biological control, 3, 6, 7, 21, 26, 27, 

33, 36–38, 40–43, 45–48, 51, 53, 

54–55, 58, 64, 70, 71, 74, 77, 78, 

82, 85–88, 92–96, 100–103, 106, 

110, 111, 113, 120, 123, 124–129, 

134, 139, 152, 154, 204, 205, 218, 

224, 231–233, 249–252, 255, 

269–271, 278, 283, 285, 292, 295, 

298, 299, 301, 302, 307–308, 

311–317, 320, 321, 323, 324 

Biological parameters, 260, 317 

Biomass consumption, 192 

Biomass transfer, 203 

Biopesticide, 106, 123, 240, 241, 243 

Biorational insecticides, 138 

Biosynthetic pathways, 200 

Biotechnical methods, 34 

Biotic environment, 203 

Bird peck damage, 134 

Bird, 134, 135, 151, 157, 160 

Birefringent bodies, 251 

Birefringent crystals, 252, 293, 294 

Bitter orange, 29, 34, 36, 39, 45 

Black pecan aphid, 136, 138, 139, 

153 

Blackmargined aphid, 138, 139 

Blastic conidiogenesis, 296 

Blue lupine, 148 

Blueberry mites, 283 

Body cavity, 263, 284, 290 

Bohemia, 268 

Bombix mori, 197 

Bombycidae, 236 

Borax, 32, 33 

Borers, 64 

Botanical pesticides, 278 

Bougainvillea, 76 

Bovine serum albumin, 120 

Boxwood, 76 

Brachycaudus helichrysi, 45 

Braconidae, 16, 20, 64, 65, 81, 92 

Bradysia impatiens, 198 

Branches, 14, 76, 79, 87, 88, 93, 237, 

284 

Brassica napus, 197, 207 

Brazil, 82, 168, 252, 267–271, 278, 

279, 281, 282, 283, 284, 298, 300, 

302–330, 307, 308 

Breeding programs, 143 

Breeding, 173, 179, 186 

Brevipalpus californicus, 12, 259 

Brevipalpus phoenicis, 12 

Bristles, 286 

Broad spectrum insecticides, 42, 138, 

139 

Brome Mosaic Virus, 252 

Brown citrus aphid, 6, 74 

Brown stink bug, 155 

Brown Tail Moth, 241 

Bryobia praetiosa, 258 

Bryobia, 256, 264, 266, 267

332 

INDEX 

Btk spore, 243 

Btk, 240–243 

BTM, 241 

Bugs, 81 

Bulb, 68 

Buprofezin, 21–25, 68, 77, 79, 89 

Bursaphelenchus mucronatus, 130 

Bursaphelenchus xylophilus, 130 

Buzzing, 214 

C 

Cabbage white butterfly, 196 

Cabinetry, 134 

Cacoecimorpha pronubana, 10 

Cadavers, 250, 273, 282, 285 

Calabria, 82 

Calacarus heveae, 275, 281–282, 308 

Calcium polysulfur, 21 

Calcium, 200 

Cales noacki, 15, 25, 40, 54, 63, 64, 

67, 68, 93, 94 

California red scale, 6, 29, 30, 36, 37, 

39, 74, 75, 77, 78, 95, 96, 98, 99 

California, 64, 66, 72, 74, 75, 77, 78, 

89, 94, 95–99, 104, 125, 135, 157, 

250, 251, 253, 297, 308 

Calliptamus italicus, 181, 187 

Calocoris trivialis, 7, 13, 75 

Caloglyphus moniezi, 287 

Calyx, 50 

Cambium layer, 134 

Camellia, 76 

Cameras, 166 

Camponotus nylanderi, 11, 89 

Campsis radicans, 143 

Canada, 240 

Canary Islands, 6, 19, 20, 63, 64 

Candelilla wax powder, 284 

Candidatus Liberibacter asiaticus, 

102 

Candidatus Liberobacter, 6 

Cannibalism, 294, 321, 322, 323, 324 

Cannon, 262 

Canopy, 14, 104, 108, 116, 134, 154 

Capilliconidia, 269, 270, 306 

Capilliconidium, 263, 296 

Capture, 77, 78, 88, 219–223, 229 

Carabodes coriaceus, 287, 289 

Carabodes femoralis, 289 

Carabodidae, 287, 289 

Carbaryl, 138, 158, 216 

Carbofuran, 218 

Carbosulfan, 21, 23–25 

Cardinium, 257, 259, 300, 302, 303 

Carfentrazone, 144 

Caribbean, 104, 110, 125 

Carnauba, 284 

Carob, 76, 79 

Carya illinoinensis, 133, 159 

Cassava belt, 269, 280 

Cassava green mite, 262, 268–271, 

280, 298, 302–303, 306, 309 

Cassava mites, 298 

Cassava, 262, 268–271, 280, 298, 

300, 302–303, 306, 309 

Caterpillar, 134, 191, 196, 197, 201, 

206 

Caterpillars dieting, 197 

CBC, 15–20 

CBERS-2, 168 

Cecidomyidae, 77 

Cecidomyids, 67 

Cecidophyes galii, 283 

Cecidophyopsis ribis, 283 

Cecropia insignis, 194 

Cecropia, 194 

Cedrus, 237 

Cells, 251, 252, 253, 255, 258, 261, 

272, 285, 286, 290, 291, 292, 293, 

304 

Celphos, 217 

Cement, 217 

Central America, 88, 89 

Central Asia, 177, 181, 185 

Cephalosporium, 296, 300 

Cepheoidea, 289 

Cepheus dentatus, 289 

Ceratitis capitata, 6, 11, 13, 14, 20, 

24, 31–33, 34–35, 55, 57–59, 

62–64, 69, 72, 74–75, 89–92, 95 

Ceratoppia bipilis, 288 

Ceratoppia, 288

INDEX 

333 

Ceratozetidae, 287 

Cereal crops, 179 

Ceroplastes floridensis, 9, 38, 74 

Ceroplastes japonicus, 9 

Ceroplastes rusci, 9, 29, 30, 31, 36, 

38, 75, 94 

Ceroplastes sinensis, 9, 23, 62 

Certification, 5 

Cetonia carthami, 11 

CGM, 269, 270, 271, 281 

Chaff scale, 75 

Chalcididae, 20 

Chania, 43, 47, 49, 50, 54, 57, 59 

Charaxes jasius, 11 

Charcoal, 134 

Chelisoches morio, 215, 231 

Chemical activity, 236 

Chemical and biological controls, 

137 

Chemical arsenals, 189 

Chemical compounds, 76 

Chemical contaminants, 120 

Chemical control methods, 140 

Chemical control, 21, 34, 39, 41, 44, 

47, 49–51, 209, 269 

Chemical insecticides, 211, 217 

Chemical options, 313 

Chemical pesticides, 106, 283, 298 

Chemical treatments, 14, 74, 78, 79, 

86, 88, 93 

Chemicals, 39, 42, 49, 77, 216, 228 

Chemo-receptors, 224 

Cheyletus eruditus, 294 

Chilocorus kuwanae, 77 

Chilocorus bipustulatus, 38, 77, 79 

Chilocorus nigritus, 19, 77 

China, 43, 75, 83, 95, 168, 177, 178, 

284 

Chinese bitter orange, 3 

Chinotto, 4, 73 

Chios, 16, 18, 34, 37, 42, 44, 47, 55, 

57 

Chitin, 273, 291 

Chitinolytic enzymes, 273 

Chlorfenapyr, 44 

Chlorine, 294 

Chlorpyrifos, 21–25, 39, 47, 49, 50, 

67, 68, 77, 89, 97 

Chlorpyrifos-ethyl, 217 

Chlorpyrifos-methyl, 21–23, 25, 39, 

47 

Chorion, 80 

Choristoneura fumiferana, 241, 243, 

244, 245 

Choroedocus illustris, 193, 201, 202, 

203 

Chortoicetes terminifera, 179, 185 

Chromatomyia horticola, 84 

Chromosome, 316 

Chromotropic, 6 

Chronic bacterial infection, 259 

Chrysocharis pentheus, 86 

Chrysomphalus aonidum, 9, 74 

Chrysomphalus dictyospermi, 9, 19, 

23, 37, 62, 63 

Chrysomphalus pinnulifer, 10 

Chrysoperla carnea, 47 

Chrysopidae, 47 

Chytridiomycota, 260 

Chytrids, 260 

Cicadellidae, 7 

Cicindelidae, 70, 72 

Cidial, 217 

Cihexatin, 21 

Cilia, 286 

Ciliary arrangements, 286 

Ciliata, 286 

Ciliophora, 286 

Cirrospilus nr. lyncus, 86 

Cirrospilus diallus, 86 

Cirrospilus ingenuus (=Cirrospilus 

quadristriatus), 20 

Cirrospilus ingenuus, 20, 63 

Cirrospilus pictus, 43 

Cirrospilus quadristriatus, 43 

Cirrospilus vittatus, 86 

Cirrospilus, 43, 44 

Citron, 3, 29, 39, 47–50, 73 

Citrostichus phyllocnistoides, 20, 43, 

44, 63, 71, 81, 83–86, 98, 99 

Citrus aphids, 46, 67 

Citrus arthropod pest, 30

334 

INDEX 

Citrus aurantifolia, 3 

Citrus aurantium, 3, 29 

Citrus bergamia, 4, 29 

Citrus decumana, 4 

Citrus deliciosa, 3 

Citrus flower moth, 30 

Citrus flowers, 48 

Citrus grandis, 3 

Citrus greening, 102, 103 

Citrus leafminer, 6, 29, 30, 42, 43, 

45, 58, 74, 80, 81, 85, 95, 96, 98 

Citrus limon, 3 

Citrus maxima, 3, 29 

Citrus mealybug, 6, 29, 36, 37, 38, 

39, 74, 87, 88 

Citrus medica, 3, 29 

Citrus myrtifolia, 4 

Citrus orchards, 61, 64–69, 72, 78, 

89, 101, 102, 107, 110, 114, 123, 

124 

Citrus paradisi, 3, 29 

Citrus pest management, 21, 27, 61 

Citrus pests, 15, 61–63, 69, 71 

Citrus red mite, 250, 252, 254, 267, 

273, 285, 297, 302, 307 

Citrus reticulata, 3, 29 

Citrus sinensis, 3, 29 

Citrus snow scale, 6 

Citrus Tristeza Virus, 74, 94 

Citrus whitefly, 29, 30 

Citrus, 3, 4, 6, 7, 12–14, 17, 21–23, 

25–51, 53–74, 76, 78–83, 85–99 

Cladosporium cladosporioides, 284, 

302 

Cladosporium, 284, 302 

Classical biological control programs, 

322 

Classical biological control, 15, 37, 

42, 61, 81, 106, 321 

Classification algorithms, 169 

Classification methods, 320 

Classification, 272 

Clay loam soils, 109 

Clays, 92, 95 

Clementine, 22, 73 

Cleonis punctiventris, 299 

Cleora fortunata, 10 

Clethodim, 144 

Climate, 74, 87, 312, 322 

Climatic conditions, 78, 81, 88, 93, 

311, 321 

Climatic events, 237 

Clofentezine, 21, 22, 24, 25, 53, 68 

Clover cover crops, 133 

Clover, 146, 147, 149, 151, 152 

Coccidae, 9, 17, 23, 29, 38, 55, 58 

Coccidea, 291 

Coccidia, 291, 306 

Coccidoxenoides perminutus 

(= Pauridia peregrina), 17 

Coccidoxenoides perminutus, 88 

Coccinella septempunctata, 46 

Coccinellid predator, 37, 38 

Coccinellid, 13, 14, 67 

Coccinellidae, 15–19, 38, 46, 47, 55, 

56, 61, 65, 77, 79, 87, 88, 134, 

153, 157, 160, 161 

Coccobius fulvus, 19 

Coccoidea, 36, 64, 68 

Coccophagus ceroplastae 

(= Aneristus ceroplastae), 17 

Coccus hesperidum, 9, 17, 23, 62 

Coccus pseudomagnoliarum, 9, 17, 

38, 74 

Coccus viridis, 9 

Coconut mite, 278, 279, 303, 308 

Coconut palm, 209 

Coconut trees, 279 

Coconut, 209, 210, 217, 232, 233 

Cocoon, 80, 211 

COII, 200, 205 

Coleoptera, 11, 61, 65, 70, 77, 79, 87, 

88, 92, 134, 157, 160, 161 

Collembola, 111 

Colloid surfaces, 114 

Colombia, 82 

Colomerus novahebridensis, 275 

Colonization, 237 

Colony health, 284, 305 

Colony, 75, 78, 87–89, 93, 237, 240, 

242, 243, 255, 284, 291, 292, 305 

Colorado Potato Beetle, 254

INDEX 

335 

Colour, 13 

Columbia University, 175, 176 

Commercial compounds, 23 

Commercial damage, 76 

Commercial production, 278, 293 

Commercially formulated EPNs, 107 

Commodities, 311 

Comperiella bifasciata, 19, 37, 63, 

77, 78, 98 

Computer simulations, 143 

Concentration, 217, 225, 226 

Confidor, 216 

Conidia, 141, 158, 261–263, 268, 

270–273, 277, 278, 284, 296, 305 

Conidial preparations, 278 

Conidiobolus brefeldionis, 264 

Conidiobolus coronatus, 262, 265 

Conidiobolus obscurus, 265 

Conidiobolus thromboides, 265 

Conidiobolus, 262, 264 

Conidiophore, 261–263, 272, 273, 

296 

Conidium, 262, 263, 296 

Conifer, 76 

Conjunctivitis, 236 

Conservation BC, 67, 70 

Conservation biocontrol strategies, 61 

Conservation biological control, 102, 

106 

Conservation, 62, 65, 70 

Constricting rings, 112, 115 

Consultants, 30, 42 

Control measures, 29, 30, 39, 47 

Control strategies, 312, 315, 320, 322 

Control tactic, 101, 103 

Control techniques, 5 

Control, 15–20, 29, 30, 32, 34–42, 

44, 45, 47–51, 53–57, 73, 74, 76, 

78, 79, 81, 86–89, 91–100, 133, 

134, 136–146, 149, 152–161, 249, 

251, 255, 269, 278–279, 281–285, 

292, 295, 296–299, 301–308 

Conveyor belt, 240 

Conyza canadensis, 143 

Cool season legumes, 137, 146, 147, 

149, 152 

Copper oxychloride, 217 

Copper sprays, 102 

Copper, 92, 95 

Cordyceps, 273 

Coreidae, 155 

Corfu, 15, 40, 58 

Coriander, 92 

Corn, 254, 267, 279, 301, 301 

Cornuaspis beckii, 62, 63 

Corsica, 4, 15, 18, 19 

Cortical lesions, 76 

Corylus avellana, 283 

Cos, 42 

Cosmopterigidae, 84 

Cosmopterix pulchrimella, 84 

Cotesia robecula, 200, 201 

Cotton aphid, 75 

Cotton rolls, 33 

Cotton, 254, 267, 268, 270, 284, 

307 

Cottony egg masses, 13 

Cottony-cushion scale, 36, 38 

Cotyledons, 198, 203 

Cover crop management, 69 

Cover spaying, 34, 35 

Cowpea curculio, 154, 160 

Cowpea, 155, 199 

CPV, 216 

CPWC, 144 

Crabgrass, 143 

Crapemyrtle aphid, 153, 159 

Crataegus, 238 

Crawlers, 75, 79, 87, 99 

Crematogaster scutellaris, 11 

Crematogaster, 92 

Crete, 15–20, 30, 31, 32, 34, 37, 40, 

42, 43, 47, 49, 50, 54, 56, 57, 58 

Crimson clover, 146–152 

Cristulariella pyrimidalis, 141 

Criteria, 5, 21 

Critical period of weed control, 144 

CRM, 250, 251, 272, 273, 278, 285 

Crop cultivars, 107 

Crop protection practices, 70 

Crop, 13, 134–136, 141, 144, 146–150, 

152, 155–157, 158, 192, 193, 207,

336 

INDEX 

254, 255, 267–269, 292, 293, 297, 

298, 299, 305, 307 

Cropping systems, 312, 322 

Cropping, 113–115 

Crossvine, 76 

Crown gall, 141 

Crown, 210, 215, 241, 242 

Cryoprotective compounds, 268 

Cryptic habitats, 224 

Cryptoblabes gnidiella, 10 

Cryptochaetum iceryae, 63 

Cryptolaemus montrouzieri, 17, 25, 

37, 38, 63, 65, 67, 68, 88 

Crystal complex, 241 

Crystalline body, 254, 255 

Crystalline toxic body, 254 

Crystals, 252, 294, 301, 307 

CTV, 6 

Cultivar susceptibiltiy, 133 

Cultivars, 135, 137, 141–143, 154–156, 

158, 159 

Cultural control, 44 

Cultural practices, 4, 34, 36, 38, 40, 

41, 44, 48, 51, 108, 113, 114 

Cultural techiques, 39 

Culture media, 264, 270, 271, 283 

Curculio caryae, 138, 160 

Curculionidae, 11 

Cuticle, 112, 113, 129, 217, 263, 269, 

273, 278, 285, 286 

Cybocephalidae, 77 

Cybocephalus fodori, 38 

Cycle, 81, 82, 83, 84, 90 

Cyclopentanones, 200 

Cydia caryana, 138 

Cynodon dactylon, 143 

Cypermethrin, 21–26, 36, 39, 47, 49, 

138 

Cyperus, 143 

Cyprus, 43, 82, 83, 84 

Cystein protease, 196 

Cytopathological effects, 252 

Cytopathological studies, 253 

Cytoplasm, 251, 252, 253, 286 

Cytoplasmic incompatibility, 258, 

259, 303, 309 

Cytoplasmic polyhedrosis virus, 216 

Cytotoxic effects, 277 

Czech Republic, 268 

D 

Dactylellina dactyloides, 115 

Dactylellina haptotyla, 115, 126 

Dacus bait, 33 

Dagang, 178 

Damaeidae, 287–290 

Damaeus clavipes, 287, 288, 289 

Damaeus geniculatus, 287, 290 

Damaeus oblongus, 288, 290 

Damaeus onustus, 287, 288 

Damage categories, 178 

Damage, 48, 50, 239 

Damsel bugs, 148 

Danaus chrysippus, 260 

Darfur, 174 

Database, 67 

Datana integerrima, 134 

Date palm plantations, 220, 221 

Date palm, 210, 214, 215, 219–232 

Death, 253, 254, 261, 263, 277, 283, 

291 

Decomposition, 148, 149, 150 

Defense genes, 190, 191, 199, 200, 

204, 205 

Defense patterns, 202 

Defensive proteins, 199 

Defoliating Lepidoptera, 235 

Defoliation, 87, 134, 136, 155, 238 

Deformed wing virus, 254, 307 

Delphastus pusillus, 15 

Deltamethrin, 21–25, 92 

Demanyssidae, 286 

Demethylation inhibitors, 141 

Dendrocerus, 46 

Dendrolaelaps cornutus, 275 

Dendrolaelaps tetraspinosus, 275 

Dendrolaelaps, 265 

Density changes, 235, 316 

Density dependent pattern, 193 

Density, 5, 14, 220, 273, 283 

Dephosphorylation, 200 

Dermanyssoidea, 252, 308

INDEX 

337 

Dermanyssus gallinae, 257, 260, 302 

Dermaptera, 70, 215, 231 

Dermatitis, 236, 243, 244, 245 

Dermatophagoides pteronyssinus, 

256 

Desert locust habitats, 174, 175 

Desert locust, 164, 165, 170, 173–176, 

179, 182–187 

Desiccation, 284, 299 

Desmids, 261 

Detection, 13, 33, 36, 37, 39, 46, 53, 

249, 292, 293, 300 

Detergent, 14, 46 

Deterrent, 239 

Deuteromycetes, 260, 261, 272, 282, 

296, 307 

Deuteromycota, 272, 296, 298, 305 

Developing conservation biological, 

106 

Development, 6, 13, 76, 83, 84, 90, 

96, 312, 314, 315, 316, 317, 321, 

322, 324 

Developmental stages, 217 

Diachasma fullawayi, 20, 63 

Diachasmimorpha longicaudata, 20, 

63 

Diachasmimorpha tryoni, 20, 63 

Diaeretiella rapae, 46 

Diagnostic services, 119 

Dialectica scalariella, 84 

Dialeurodes citri, 8, 15, 23, 29–31, 

40, 54, 58, 74, 93, 99 

Dialeurodes citrifolii, 8 

Diameter, 14 

Diammonium phosphate, 92 

Diamond-back moth, 197 

Diapause, 177, 316 

Diaphorina citri, 74, 102 

Diaprepes abbreviatus, 101, 103–107, 

109, 110, 123–125, 127–130 

Diaprepes, 101, 103–105, 107, 109, 

110, 123–130 

Diarrhea, 250 

Diaspidid scales, 13 

Diaspididae, 9, 18, 23, 29, 30, 37, 62, 

63, 68, 75, 79, 96–99 

Diaspidids, 14 

Diaspidiotus perniciosus, 10 

Diazinon, 21, 22, 24, 25 

Diazinone, 217 

Dichlorvos, 21, 24 

Dicofol, 21, 22, 24, 25, 53, 68 

Dicrodiplosis, 87 

Dieback, 76 

Diflubenzuron, 21, 22, 24, 25, 139, 

161 

Digamasellidae, 265, 275 

Digital data, 167 

Digitaria, 143 

Diglyphus isaea, 86 

Dimethoate, 21–25 

Dinychus carinatus, 267 

Diospyros melanoxylon, 83, 95 

Diptera, 11, 29, 54–58, 62, 77, 84, 

87, 97 

Directive, 22, 26 

Dirhinus giffardii, 20, 33 

Discoloration, 294, 301 

Disease losses, 141 

Disease transmission, 321 

Disease, 5, 6, 102–104, 236, 244, 

249, 250, 251, 252, 253, 256, 258, 

259, 263, 264, 268, 271, 273, 281, 

283, 284, 291–295, 307, 308, 311 

Dispenser, 14 

Dispersal, 320, 321, 325 

Disruption, 12 

Distribution maps, 178 

Distribution, 108, 119, 124–127, 130, 

236, 237 

Dithiocarbamate, 5 

Ditylenchus dipsaci, 122 

Diurnal caterpillars, 191 

Diurnal insects, 192 

Diuron, 144 

Diversinervus elegans, 17, 37 

DMNT, 200 

DNA markers, 143 

DNA, 116, 118, 119, 120, 124, 125, 

127–130 

DNA-dependent RNA polymerase, 254 

Dociostaurus maroccanus, 181

338 

INDEX 

Dodine, 141, 142 

Dorsal ducts, 79 

Doses, 241 

Douglas Fir Tussock Moth, 239 

Downy Spot, 141, 142 

Dracaena, 76 

Droplets, 240 

Drosophila, 260 

Drought stressed plants, 194, 202 

Drought, 194, 202, 206, 261, 264, 

270 

Dryinidae, 15 

Dumbbell-shaped bodies, 294 

Dursban, 217 

Dusky stink bug, 155 

E 

Early detection, 163 

Earth surface, 164–167, 169 

Earth, 163, 185, 186 

Earwigs, 70, 215 

Ecesis, 83 

Echium, 84 

Ecological impact, 322 

Ecology, 101, 103, 123, 126 

Economic crop losses, 193 

Economic damage, 12, 281, 282 

Economic importance, 43, 93 

Economic injury level, 36, 38, 51 

Economic threshold, 5, 65, 66, 79, 

88, 250 

Ecosystem components, 189 

Ecosystem functioning, 189, 196 

Ecosystem processes, 190 

Ecosystem, 73, 86, 189, 193 

Ectomyelois ceratoniae, 10 

Ectoparasitic wasp, 84 

Ectoparasitoid, 77, 214 

Edaphic conditions, 106 

Egg predators, 239 

Egg sterilants, 104 

Egg, 75, 79–81, 83, 84, 87, 89–91, 

94, 104, 108, 109, 123, 209, 211, 

212, 214, 215, 229, 231, 239, 243, 

244, 252, 255, 258, 259, 292, 293 

Eggplant, 320, 325 

Egypt, 4, 27, 84, 96, 209, 210, 

215–217, 224, 231, 233 

Ehrlichieae, 257 

Elasmus flabellatus, 48 

Electromagnetic radiation, 165, 166, 

167 

Electromagnetic spectrum, 166, 167, 

172 

Eleusine indica, 143 

Elicitor defence genes, 200 

Elicitors, 189, 190, 191, 204 

Elutriation, 121 

Empoasca decedens, 7 

Empoasca, 7, 14 

Empresa Brasileira de Pesquisa 

Agropecuária, 271 

Encarsia (= Aspidiotiphagus) 

lounsburyi, 19 

Encarsia (= Prospaltella) perniciosi, 

19 

Encarsia (=Prospaltella) lahorensis, 

15 

Encarsia citrina, 38 

Encarsia herndoni (= Encarsia 

elongata), 19 

Encarsia herndoni, 19, 63 

Encarsia lahorensis, 15, 63 

Encarsia perniciosi, 19, 37, 63, 77 

Encarsia strenua, 63 

Encarsia, 260 

Encyrtid, 78, 81, 82, 88 

Encyrtidae, 18–20, 37, 38, 43, 48, 

65, 66, 71, 77, 81, 87, 88, 95, 99, 

100 

Endemic EPN species, 103, 108 

Endoparasitoids, 77, 78 

Endosymbionts, 259, 260 

Enterobacter, 256, 259 

Entomogenous fungi, 273 

Entomology, 133, 158 

Entomomophthorales, 261 

Entomopathogenic bacteria, 112 

Entomopathogenic nematodes, 101, 

103, 105, 110, 115, 123–129, 209 

Entomopathogens, 138 

Entomophagous arthropods, 50

INDEX 

339 

Entomophthora floridana, 267, 305, 

307, 309 

Entomophthora muscae, 262 

Entomophthoraceae, 261, 262, 301, 

304, 305, 309 

Entomophthoraceous infections, 267 

Entomophthoralean fungus, 263, 264, 

267 

Entomophthoralean species, 264 

Entomophthorales, 263, 297, 300–304, 

305 

Environment, 235, 236, 240, 241 

Environmental conditions, 35, 45, 

253 

Environmental hygiene, 236 

Environmental pollution, 269 

Enzymatic processes, 269 

Eotetranychus banksi, 266 

Eotetranychus hicoriae, 138 

Eotetranychus orientalis, 280 

Eotetranychus pueraricola, 260 

Eotetranychus sexmaculaturs, 265, 

276 

Eotetranychus suginamensis, 260 

Eotetranychus uncatus, 260 

Ephedrus persicae, 46 

Epidemics, 281, 282, 297, 298 

Epidemiological data, 222 

Epidermic reactions, 236 

Epistrophe baiteata, 46 

Epithelial cells, 251, 252, 293 

Epitremerus goniathrix, 273, 274, 

275 

Epizootic, 252, 269, 270, 271, 277, 

283, 302, 305, 306, 308 

EPN communities, 101, 103 

EPN distributions, 101, 107, 120 

EPN population, 101, 120 

EPN prevalence, 109, 113, 114, 116 

EPN spatial patterns, 114, 115 

EPN, 101, 103, 105–107, 109–116, 

123, 216, 224–230 

EPNs population biology, 101 

EPPO list, 6 

EPPO, 74, 98 

Equine encephalitis viruses, 252 

Eradication programs, 104 

Eretmocerus debachi, 16, 63 

Erhardovina bisphaera, 287 

Erhardovina carabodesi, 287 

Erhardovina euzeti, 287 

Erhardovina fuscozetesi, 287 

Erhardovina fuscozetis, 287 

Erhardovina oribatarum, 287 

Erhardovina phtiracari, 287 

Erhardovina platynothri, 287 

Erhardovina postneri, 287 

Erhardovina scutovertexi, 287 

Erhardovina, 287 

Eriophyes sheldoni, 11, 13, 299 

Eriophyidae, 11, 50, 54, 265, 273, 

281–283, 304, 305, 308 

Eriophyids, 249, 273, 278, 282, 297 

Eriophyiidae, 29, 30 

Eriophyiids, 50, 53 

Eriophyoidea, 274, 275, 308 

Eritrea, 173, 174 

Erosion, 149 

Erynia phalangicidae, 265 

Escharosis, 49 

Esfenvalerate, 138 

Establishment, 74, 82–86, 89, 92, 96, 

99 

Ethiopia, 173, 174 

Ethoprophos, 22 

Ethylene emission, 199 

Ethylene, 199, 200, 207 

Etiology, 252 

Etofenprox, 21, 22, 23, 24, 92 

Etoxazol, 21, 22, 24, 53, 68 

EU, 4, 62, 66, 67, 74, 241, 244 

Eucalymnatus tessellates, 9 

Eucalyptus blakelyi, 193, 206 

Eucalyptus, 238, 239 

Eucalyptus, 76 

Eucoilidae, 34, 57 

Eugregarine, 290 

Eugregarines, 290 

Eugregarinida, 289 

Eukaryotes, 286, 291 

Eukaryotic cells, 257 

Eulophid, 64, 83, 84, 85

340 

INDEX 

Eulophidae, 20, 38, 43, 44, 48, 55, 

58, 71, 81, 85, 97, 98, 99 

Eumaeus atala florida, 239 

Euonymus, 76 

Eupelopidae, 287 

Eupelops hirtus, 287 

Eupelops subuliger, 287 

Eupelops torulosus, 287 

Euphorbia species, 143 

Euphthiracaroidea, 289 

Eupodidae, 266 

Euproctis chrysorrea, 238 

Euproctis chrysorrhoea, 239, 241 

Euproctis edwardsii, 239 

Euproctis lunata, 239 

Euproctis pseuconspersa, 239 

Euproctis scintillans, 239 

Euproctis similis, 239 

Euproctis, 237, 239, 243, 245 

Eupterotidae, 236 

Europe, 237, 238, 240, 241, 292, 299 

European settlers, 135 

European silvopastoral systems, 135 

Euschistus servus, 155 

Euschistus tristigmus, 155 

Euseius addoensis, 319 

Euseius citrifolius, 265, 302 

Euseius elinae, 319 

Euseius finlandicus, 257, 260, 319 

Euseius fructicolus, 319 

Euseius sojaensis, 319 

Euseius stipulatus, 25, 51, 53, 54, 61, 

65–68, 71, 319 

Euseius tularensis, 319 

Euseius victoriensis, 319 

Eutetranychus banksi, 12, 24, 267, 

276, 309 

Eutetranychus orientalis, 12, 256, 

274, 276, 280 

Euzetes globulus, 287 

Euzetes seminulum, 287, 288, 290, 304 

Euzetidae, 287, 288 

EVA Green dye, 121 

Evaluation, 64, 66, 67 

Excretory organs, 294 

Excretory products, 294 

Exochomus quadripustulatus, 38, 77, 

79 

Exotic arthropods, 74 

Exotic biological control, 61 

Exotic eulophids, 86 

Exotic IBCAs, 62, 70 

Exotic natural enemies, 81 

Exotic parasitoids, 33, 36 

Exotic pests, 74, 311 

Exotic species, 62, 74, 88 

Exotoxin, 254, 255, 303 

External morphology, 317 

Extraction, 121, 122 

Eyes, 89 

F 

Fagales, 133 

Fall armyworm, 199 

Fall webworm, 134 

Family, 256–258, 260, 262, 264, 269, 

274, 287, 301 

Far infrared, 166 

Farmed habitats, 106 

Farmers, 30, 33, 312, 314 

Farnesol, 22 

Fatbody, 253, 277 

Fatty acid potassium salt, 47, 50 

Fatty acid, 21–23 

Fecal pellets, 251 

Feces, 218, 227, 251, 255, 290 

Fecundity, 79 

Feeding sites, 79, 87 

Feeding specialization, 317 

Feeding, 77, 79–81, 83, 84, 86, 87, 

90, 93, 210, 212, 215, 224, 252, 

284, 286, 307, 317, 325 

Female mealybugs, 14 

Female, 75, 77, 79–83, 87, 90 

Feminization, 249, 258 

Fenazaquin, 21–25, 53, 68 

Fenbutatin oxide, 21, 22, 24, 25, 53, 

67, 68 

Fenitrothion, 21, 23–25 

Fenoxycarb, 21–25, 39, 44, 54 

Fenperoximate, 21–24, 53, 68 

Fermentation, 227

INDEX 

341 

Fern prothalli, 261 

Ferrugineol, 218, 232 

Ferrugineone, 218 

Fertilization process, 316 

Fertilization, 44, 73, 86, 87 

Fertilizer, 39, 45, 137, 146, 147, 149, 

153 

Festuca arundinacea, 69 

Ficus, 87 

Field experiments, 251, 279 

Field trials, 216, 218, 219, 223 

Fig wax scale, 75 

Filaments, 87 

Fire ant, 138, 154, 158–160 

Firmicutes, 260 

Fission, 263, 290 

Flagella, 260, 286, 291 

Flagellar action, 286 

Flagellata, 286 

Flagellates, 286 

Flatid planthoppers, 15 

Flatidae, 7, 15 

Flatwoods orchards, 109 

Flavedo, 285 

Flight, 13, 77 

Flooring, 134 

Florida citriculture, 102 

Florida citrus industry, 102 

Florida, 43, 54, 56, 81, 82, 84, 89, 

96–97, 101–104, 106, 107, 109, 

110, 112, 114, 115, 123–130, 250, 

267, 268, 273, 276, 300, 301, 302, 

305, 307–309 

Flower damage, 48 

Flower tissues, 48 

Flowering plants, 289 

Flowers, 13, 48, 49, 57 

Fluazifop, 144 

Fluctuation, 32, 40 

Flucythrinate, 22–25, 36, 39, 47, 49 

Flufenoxuron, 21, 22, 24, 25, 44, 45 

Flumioxazin, 144 

Fluorescence, 116 

Flushes, 13 

Flushing twigs, 13 

Fluted scales, 16 

Fluvalinate, 21, 22, 26 

Foliage, 39, 133, 136–139, 148, 155, 

161, 162, 241, 244 

Food attractant, 32, 32, 35 

Food availability, 311, 316 

Food, 6, 14, 62, 69, 250, 259, 261, 

286, 308 

Fopius arisanus, 63, 64 

Forecasting, 5 

Forest, 235, 236, 237, 238, 240, 244, 

245 

Forestry programs, 242 

Forestry, 236, 238, 245 

Forficulidae, 215, 231 

FormaSat, 168 

Formicidae, 11, 92, 95, 96 

Formothion, 217, 218 

Formulation, 134, 235, 240, 241, 243, 

244, 254, 283, 297, 299 

Fortuitous introduction, 74 

Fosalone, 25 

Fosetil-Al, 5 

Fowl pox virus, 252 

France, 4, 6, 7, 15–20, 27, 89, 93, 98, 

168, 176, 183–186, 209, 240, 241, 

244 

Frankliniella bispinosa, 7 

Frankliniella occidentalis, 7, 49, 

292 

Frass, 218, 227 

Fruit collection, 33 

Fruit flies, 20, 24 

Fruit juices, 102 

Fruit, 13, 29–36, 48–51, 54–58, 74, 

76, 79, 80, 87–92, 99, 133, 136, 

137, 143, 161 

Fruiting body, 260, 261 

Fuelwood, 134 

Fumagillin, 294 

Fumigants, 93 

Fumigation tablets, 217, 218 

Fungal diseases, 140 

Fungal pathogens, 249, 297, 298 

Fungi Imperfecti, 260, 296 

Fungi, 102, 111, 112, 114–116, 119, 

120, 125, 126, 129, 150, 161, 209,

342 

INDEX 

216, 249, 250, 260, 261, 264, 269, 

271–273, 282–285, 291, 296–298, 

299–306 

Fungicide, 5, 135–137, 141, 142, 

144, 156, 160 

Fungus, 216, 231, 261, 264, 267–271, 

277–284, 297, 299–300, 304–309, 

321 

Furniture, 134 

Fusarium, 296 

Fuscozetes setosus, 287 

Fusicladosporium effusum, 141 

G 

Galendromus annectes, 318 

Galendromus helveolus, 318 

Galendromus occidentalis, 63, 316, 

318 

Galeopsomyia fausta, 20, 63 

Galicia, 6 

Gametangia, 261 

Gametes, 260, 261, 290 

Gametogony, 290 

Gamma rays, 166 

Gamontocyst, 290 

Gamonts, 290, 291 

Gardenia, 87 

Gas, 218 

Gene, 254, 255, 296 

Genera, 272, 285, 296 

Generalist predators, 51 

Generalist, 317, 320, 323, 324 

Generations, 32, 42, 44, 45, 48, 50, 

51, 77, 79, 81, 87, 210 

Genus, 254, 258, 260, 262, 273, 292, 

296, 299–301, 304, 306, 309 

Geographic information system, 165, 

184 

Geometridae, 10 

Georeferenced data, 170 

Georgia, 4, 133, 136, 137, 141–145, 

152, 157–162 

Geospatial technologies, 163 

Germany, 240, 246 

Germination, 262, 263, 268, 270, 

284, 296, 297, 299, 306 

GIS, 163, 165, 169–171, 176, 

181–187 

Glands, 79, 236, 239 

Glass beads, 121 

Glass McPhail trap, 33 

Glasshouse, 255, 293, 312, 322 

Global Positioning Systems, 171 

Globodera artemisiae, 121 

Globodera pallida, 121 

Globodera rostochiensis, 121 

Globodera tabacum, 121 

Glomerella cingulata, 141 

Glucose-N-acetyl, 273 

Glue, 14 

Glufosinate, 144 

Glycerol, 268, 270, 279 

Glyphosate, 144, 145 

GMOs, 5 

Golgi apparatus, 285 

Goosegrass, 143, 283 

Government policies, 243 

GPS receiver, 171 

GPS, 165, 171, 176, 240 

Gracillariidae, 10, 20, 24, 60, 53, 54, 

57–58 

Grafted trees, 44 

Grafting, 135 

Granula, 295 

Granulosis viruses, 295 

Grape, 76 

Grapefruit flowers, 285 

Grapefruit, 3, 22, 29, 36, 39, 45, 47, 

49, 73, 76, 285 

Grass control, 133 

Grasshopper feeding, 172 

Grasshopper infestations, 171, 186 

Grasshopper, 171, 172, 177, 184–187, 

190, 193–195, 198, 202–204 

Gravid females, 65, 292 

Greece, 3–5, 7, 15–20, 21–23, 26–37, 

39–42, 44–51, 53–59, 82–84, 96, 97, 

209 

Green algae, 261 

Green lacewing, 46, 148 

Green leaf volatiles, 199, 200 

Green lemons, 251

INDEX 

343 

Green manures, 149 

Green stink bug, 154, 155, 159 

Green twigs, 13 

Greenhouses, 280, 281, 283, 292, 

297, 312 

Greening disease, 74 

Gregarina euzeti, 290 

Gregarina oribataram, 290 

Gregarina scutovertexi, 290 

Gregarina, 287, 289, 306 

Gregarines, 290, 291 

Gregarious behaviour, 237 

Ground cover mangement, 61, 69 

Ground cover, 61, 67, 69, 70 

Groundwater, 134, 149 

Groves, 85, 86, 92, 96, 99–104, 128, 

129, 135, 136, 155, 156 

Growers, 30, 35, 38, 40, 42, 67, 69, 

102, 133, 135–137, 139–143, 146, 

149, 152, 155 

Growing season, 13, 14, 140, 144 

Growth regulator insecticides, 139 

Guanine, 251, 294 

Guidelines, 4, 5, 6, 69 

Gulf of Aden, 173 

Gum, 76 

Gurleya sokolovii, 288 

Gut epithelium, 292 

Gymnoscelis pumilata, 10 

Gymnoscelis rufifasciata, 10 

H 

Habitat Mapping, 174, 177, 179 

Habitat, 163, 164, 171–175, 177, 

182–185, 194, 214, 222, 228, 230, 

237, 250, 319, 321 

Haemocoel, 216 

Hairs, 236, 237, 238, 239, 240, 243 

Halo, 263, 296 

Halosulfuron, 144 

Halotydeus destructor, 266 

Haploid cells, 260 

Haploid nuclei, 260 

Hardware, 164, 182 

Hardwoods, 134 

Harmful products, 67 

Harmonia axyridis, 16, 47, 55, 56, 

134, 138, 153, 161 

Harpoon, 236 

Harvest, 35, 36, 80, 92, 99 

Haustorium, 286 

Hazel, 283 

HBTM, 253 

Health hazards, 190 

Health-care, 236 

Helicopters, 240 

Helicoverpa armigera, 10 

Heliothis veriscence, 204 

Heliothrips haemorrhoidalis, 7, 29, 

49, 50, 58 

Hemiberlesia rapax, 10 

Hemiptera, 7, 29, 30, 37, 38, 40, 41, 

53, 55, 58, 62, 64, 66, 67, 75, 79, 

87, 95, 98, 99 

Hemipterans, 137, 139, 140, 155, 

156, 160 

Hemisarcoptes coccophagus, 274, 

280 

Hemisarcoptidae, 274, 280 

Hemocytes, 277 

Herbaceous plant, 68 

Herbicide runoff, 149 

Herbicides, 5, 137, 144–146 

Herbivores, 189–208, 272, 316, 320 

Herbivorous species, 191 

Herbivory, 189–191, 193–208 

Hermannia gibba, 287, 288 

Hermannioidea, 287, 288 

Heterodera glycines, 121 

Heterodera schactii, 121 

Heterorhabditidae, 224 

Heterorhabditids, 111, 112 

Heterorhabditis bacteriophora, 225, 

226, 229 

Heterorhabditis indica, 109, 112 

Heterorhabditis indicus, 225–227, 

229, 230 

Heterorhabditis zealandica, 109–112 

Heterorhabditis, 105, 110, 125, 127, 

216, 224, 225, 228, 230 

Heterotrophic organisms, 150 

Hexythiazox, 21, 23, 24, 25, 67, 68

344 

INDEX 

Hibernation, 47 

Hickory shuckworm, 138 

Hickory, 134, 138–140, 143 

High plain virus, 252 

Hippodamia convergens, 194 

Hippodamia variegate, 46 

HIPV, 272 

Hirstionyssus, 286 

Hirsutella brownorum, 274 

Hirsutella danubiensis, 274 

Hirsutella gregis, 274 

Hirsutella haptospora, 274 

Hirsutella kirchneri, 274, 280, 281 

Hirsutella necatrix, 274, 281 

Hirsutella nodulosa, 275, 283 

Hirsutella rhossiliensis, 111 

Hirsutella rostrata, 275 

Hirsutella thompsonii, 273, 275–281, 

283, 299, 300 

Hirsutella tydeicola, 276 

Hirsutella vandergeesti, 276 

Hirsutella, 273–274, 277, 278, 281, 

282, 296, 299–305, 308, 309 

Hirsutellin A, 277, 303, 304, 306 

Hirsutellin B, 277 

Historical data, 31 

Homoptera, 83, 96, 97, 98, 99, 262 

Homopteran pests, 64 

Homopteran, 64, 94 

Honduras, 82 

Honeybee tracheal mite, 253 

Honeybees, 80, 253 

Honeydew, 13, 46, 78, 87, 88, 93, 

134 

Horsenettle, 143 

Horseweed, 143 

Horticulture, 133 

Host spectrum, 251, 261, 264, 268, 

269, 283, 299 

Host, 105, 109, 127, 250, 251, 253, 

256, 258, 259, 260, 261, 262, 263, 

264, 268, 269, 270, 271, 273, 277, 

278, 283, 286, 287, 290, 291, 295, 

296, 299, 301, 302 

House fly, 215 

Hover flies, 148 

HtA, 277 

Huanglongbing, 6, 102 

Humeral bristles, 89 

Humidity, 81, 97, 263, 270, 283, 297, 

299, 306, 307 

Hungary, 89 

Hunting, 156 

Hurricanes, 164, 166 

Hydrachnellae, 287, 288, 303 

Hydrogen, 150 

Hydrolyzed protein, 33, 92 

Hylesia iola, 239 

Hylesia lineata, 239 

Hylesia urticans, 239 

Hylesia, 239, 244 

Hymenoptera, 11, 20, 27, 33, 34, 37, 

38, 40, 43, 44, 48, 54, 55, 57, 58, 

64–66, 71, 72, 77, 79, 81, 85, 87, 

88, 92, 94, 95–100 

Hyperparasitoids, 46 

Hyperspectral images, 167 

Hyphae, 260, 261, 263, 272, 273, 296 

Hyphal bodies, 261, 263, 264, 304 

Hyphantria cunea, 134 

Hyphomycetes, 272, 300, 305, 307 

Hypoaspis, 215 

Hypodermis, 277 

Hyponomeutidae, 10, 24, 30 

I 

IBCA (Invertebrate Biological 

Control Agents), 62 

Ice-nucleating substances, 268 

Icerya purchasi, 8, 13, 16, 36, 38, 62, 

63 

Icosahedral virus particles, 252 

Iflavirus, 254, 306 

Imagery, 170, 172, 174–176, 183, 

186, 187 

Imidacloprid, 21–25, 45, 67, 77 

Immature stages, 211, 215 

Immigration, 83, 85 

Immune system, 253 

Importation, 74, 92 

Inclusion bodies, 250, 255, 295 

Incompatibilities, 249, 296, 300

INDEX 

345 

Incubation period, 215 

Incubation, 215 

India, 83, 93, 168, 173, 174, 185, 

189, 209, 215, 216, 232, 233, 267, 

278, 299, 305, 307, 308 

Indigenous food webs, 62 

Indigenous parasitoids, 38, 86 

Indigenous predators, 322 

Indochinese peninsula, 75 

Indonesia, 83, 209, 210, 232 

Industrial production, 278 

Industrial repellent, 154 

Infection periods, 142 

Infection routes, 250 

Infection, 91, 104, 105, 111, 129, 

250, 251, 252, 259, 267, 268, 269, 

270, 271, 273, 278, 282, 283, 

290–291, 293, 302, 303, 306 

Infectious propagule, 263 

Infective juvenile, 105, 113 

Infective stage, 290, 291 

Infestation, 30, 32, 35, 38–44, 46, 48, 

49, 51, 53, 55, 57, 75, 76, 78, 79, 

81, 85–89, 91, 92, 99, 209, 210, 

215–217, 220, 222, 223, 226, 227, 

229, 232, 235 

Infrared photos, 167 

Inhalation, 236 

Injection, 217, 226, 227, 233, 277, 

284 

Inoculation, 65 

Inoculum, 141, 152, 157 

Insect attack, 189, 193, 201, 203, 

204, 207 

Insect cadaver, 111, 112, 250 

Insect death, 106 

Insect grazing, 194 

Insect growth regulators, 77, 86 

Insect pest, 6, 14–20, 53, 134, 139, 

146, 148, 153, 209 

Insect, 6, 14–20, 53, 64, 69, 71, 133, 

134, 136–138, 142, 146–148, 

153–156, 160–162, 189–199, 201, 

203–205, 206, 207, 211, 249, 250, 

254, 260, 261, 277, 283, 295, 297, 

299, 300, 303, 305, 307, 323, 324 

Insectary, 78 

Insecticidal soap, 138 

Insecticidal sprays, 222 

Insecticide, 5, 21, 23, 27, 33, 35, 36, 

39, 41, 42, 44, 45, 47–50, 78, 86–87, 

89, 96, 101, 102, 104–105, 133, 

136–139, 142, 154, 209, 211, 216, 

217, 227, 230, 231, 232, 285 

Insect-plant interactions, 194 

Inspections, 3, 6, 13, 46 

Instar larvae, 82, 215, 221 

Instar, 75, 76, 78, 80, 82, 83, 84, 85, 

90–91, 215, 224, 225 

Insulaspis gloverii, 62, 63 

Integrated control programs, 249, 

285, 299 

Integrated control strategies, 74, 77 

Integrated Pest Management, 4, 29, 

42, 101, 102, 296, 312 (see also: 

IPM) 

Integrated production, 4 

Integument, 250, 284, 286 

International Institute for Tropical 

Agriculture, 271 

International Pheromone Plastic 

McPhail trap, 32 

Internet, 183, 184 

Intestine, 106, 224 

Intexta acarivora, 288, 292, 304 

Intracellular bacteria, 296 

Intracellular gram-negative bacteria, 

257 

Intracellular symbionts, 249, 260 

Intraguild predation, 321 

Intrauterine, 216 

Introduced eulophids, 86 

Introduced parasitoids, 106 

Introduction, 29, 73–74, 78, 81, 92, 

94, 311, 313, 314, 321–322 

Inundative releases, 297 

Invasion, 40, 41 

Invertebrate biological control agents, 

61, 62, 70 

Invertebrate pathology, 249, 254 

Invertebrate pests, 296–297 

IP, 4–6, 26

346 

INDEX 

Iphiseius (Amblyseius) degenerans, 

50 

Iphiseius degenerans, 50, 51, 319 

IPM strategy, 53 

IPM, 3, 4, 5, 6, 29, 36, 39, 41, 45, 47, 

49, 51, 53, 57, 63, 66–69, 71, 72, 

101–102, 103, 104, 121–123, 209, 

230, 232, 233, 249, 311–314 

IPMT, 32, 33, 36 

Ipomoea, 143 

Iran, 173 

Irrigation, 39, 44, 45, 73, 86, 87, 137, 

145, 153, 159 

Irritation, 239 

IRS 1C, 168 

IRS 1D, 168 

IRS ResourceSat, 168 

Isaria fumosorosea, 299 

Ismailia governorate, 211 

Israel, 4, 5, 81–84, 94, 209, 232, 

243 

Istamine, 239 

Italy, 3–5, 7–12, 15–20, 23, 24, 27, 

50, 71, 73–74, 80–85, 87, 91–94, 

209, 235, 238, 240, 241, 242, 243, 

283 

Itching, 239 

ITS region, 118 

ITS1, 129 

ITS2, 129 

J 

JA (jasmonic acid), 197, 198, 199, 

200, 201, 202, 204 

Japan, 83, 168, 239, 260, 267, 305 

Japanese bayberry whitefly, 40, 94, 

98 

Jasmine, 87 

Jasmonate, 198, 200, 202, 203, 205 

Jasmonic acid, 197 

Jojoba, 79 

Jordan, 209, 232 

Juglandaceae, 133 

Juice processing, 102 

Jujube, 76 

Juvenile, 113, 253, 255, 269 

K 

Kairomone, 219, 222, 230 

Kampimodromus aberrans, 319, 323, 

325 

Kaolin, 21, 92 

Kazakhstan, 177, 178, 181, 182, 185, 

187 

KBV (Bee Kashmir Virus), 253, 307 

Kelly's citrus thrips, 49, 50 

Kernel spot, 155 

Kernel-feeding hemipterans, 155 

Kerosene, 217 

Kingdom Fungi, 260 

Kiwi, 79 

Korinthia, 43, 58 

Kuwait, 209, 231 

L 

Label, 68 

Laboratory colonies, 252, 258, 259, 

294 

Laboratory production, 278 

Laboratory protocols, 119–120 

Laboulbeniales, 286 

Labyrinthomorpha, 289 

Lacewing, 77, 81 

Laconia-Peloponnese, 42 

Ladder rungs, 134 

Ladybeetle, 77, 148, 153 

Lakonia, 43 

Lambda-cyhalothrin, 21–25, 92 

Landsat 168, 172 

Landsat ETM+ data, 178, 187 

Landsat Thematic Mapper data, 174, 

185 

Landscape, 134, 151, 240 

Larix decidua, 237 

Larva, 80, 81, 84, 85, 89, 211, 224, 

225, 226 

Larvae, 80–84, 90–92, 104, 105, 

108, 109, 111, 125, 128, 129, 208, 

210, 211, 214–218, 224–227, 229, 

236–243 

Larval feeding, 198 

Lasiocampidae, 236, 244 

Lasius alienus, 89

INDEX 

347 

Lasius niger, 11 

Latin America, 252, 269, 271 

Leaf cuticle, 81, 85 

Leaf miner, 64, 68 

Leaf proteins, 193 

Leaf skeletonizer, 238, 244 

Leaf wetness, 141, 156 

Leaf yellowing, 76 

Leaf-axils, 226, 228, 229 

Leaffooted bugs, 155 

Leafhoppers, 14 

Leafminer development, 81 

Leafroller, 75 

Leaves, 40, 43, 46, 51, 79, 81, 93, 

241, 243 

Lecanicillium lecanii, 298, 299 

Legs, 87, 89 

Legumes, 137, 146–152, 161 

Leguminous plants, 147 

Lemon, 12, 22, 26–27, 32, 36, 39, 45, 

47–50, 73, 74, 75, 76, 82, 91, 95, 

96, 98 

Lemons, 48, 49, 51, 61, 251 

Leonidion, 47 

Lepidoptera, 10, 30, 53–55, 58, 80, 83, 

84, 87, 95–99, 134, 196, 235–239, 

243–245, 254, 260 

Lepidopteran defoliators, 240, 241 

Lepidopteran infestations, 240 

Lepidopteran pests, 139 

Lepidopterism, 239, 245 

Lepidopterous pests, 133, 254 

Lepidosaphes beckii, 10, 19, 23, 30, 

31, 36, 37 

Lepidosaphes gloverii, 10, 19 

Leptinotarsa decemlineata, 254 

Leptoglossus oppositus, 155 

Leptoglossus phyllopus, 155 

Leptomastidea abnormis, 38, 87, 88 

Leptomastix dactylopii, 16, 25, 37, 

50, 59, 63, 65, 71, 88, 97, 99, 100 

Lestodiplosis aonidiellae, 77 

Lesvos, 42, 44 

Leucopis, 87 

Liacaroidea, 288 

LIDAR, 167 

Life cycle, 209, 211, 216, 241, 290, 

291 

Life style, 311, 313, 317–320 

Liguria, 15 

Lima bean, 199–202, 205, 206 

Limacodidae, 236 

Limantriidae, 239 

Lime, 3 

Limnochares aquatica, 287, 288, 290, 

303 

Linepithema (=Iridomyrmex) humile, 

11 

Linoleic acid, 199 

Linolenic acid, 199, 205 

Lipid, 200 

Liriomyza, 84 

Lobes, 79 

Locomotion, 214, 286 

Locust breeding areas, 163, 174, 175, 

177, 179, 187 

Locust egg-pods, 169 

Locust habitat monitoring, 163, 174, 

183, 184–186 

Locust habitat, 170, 172, 174, 175, 

179, 182, 185 

Locust nymphal development, 164 

Locust outbreaks, 163, 164, 172, 175 

Locust plagues, 164, 172, 179, 186, 

187 

Locust swarm, 164, 175 

Locusta migratoria burmana, 177 

Locusta migratoria capito, 177 

Locusta migratoria cinerescens, 177 

Locusta migratoria manilensis, 173, 

174 

Locusta migratoria migratoria, 177 

Locusta migratoria migratorioides, 

177 

Locusta migratoria, 177, 187 

Locusts, 163, 165, 170, 172, 174–177, 

179, 181–188 

Longevity, 211 

Lopholeucaspis japonica, 10 

Loquat, 76, 90 

Lorryia formosa, 276 

Lotus corniculatus, 196, 205

348 

INDEX 

Louisiana, 82 

Lufenuron, 21–25 

Lumber, 134 

Lycenidae, 239 

Lycosidae, 70 

Lymantria dispar, 240–241, 244 

Lymantriidae, 236, 243, 244 

Lyophilization, 121 

Lysiphlebus confusus, 46 

Lysiphlebus fabarum, 46 

Lysiphlebus testaceipes, 16, 25, 46, 

63, 65, 67, 68 

Lysis buffer, 120 

Lysis, 120, 253 

Lyxus algirus, 11 

M 

Macrocheles, 260, 264, 305 

Macrochelidae, 264 

Macrosiphum euphorbiae, 8, 45 

Macrosiphum mentzeliae, 194 

Madagascar, 181, 185 

Madeira Island, 6, 12, 74 

Magnesium sulphate, 119 

Magnolia, 76 

Maize, 193, 196, 199, 200, 201, 202, 

208 

Malacosoma californicum pluviale, 

194 

Malaria, 286, 290 

Malathion, 21–25 

Male killing, 249, 258 

Males, 218, 221–224, 228, 229 

Mali, 174, 187 

Malpighian tubes, 294 

Malpighian tubules, 277, 294 

Malta, 6 

Mammals, 135, 189 

Managed habitats, 106 

Management practices, 38, 44, 47 

Management regimes, 114 

Management, 101, 102, 103, 106, 

113, 123, 124, 128, 163, 164, 

170–172, 176, 178, 181–182, 183, 

184, 185, 187, 197, 199, 205, 

311–314, 320, 322, 323 

Mandarin, 3, 22, 29, 35, 36, 39, 42–43, 

47, 49, 71, 76 

Manduca sexta, 197, 204 

Mango, 76 

Maple tree, 76 

Marathon, 47 

Margarodidae, 8, 38 

Maritime Alps, 241 

Mass production, 264, 297, 298 

Mass rearing, 314 

Mass trapping, 211, 223 

Mastigophora, 286 

Mating disruption, 138 

Mato Grosso, 281 

Mature female, 75 

Maturity, 35, 79, 91, 94 

Mauritania, 174, 183, 185–187 

Mealybug, 14, 24, 29, 30, 36, 37, 87, 

88, 96 

Mechanical damage, 197, 199, 200, 

207 

Mechanical harvester, 135 

Mechanical processes, 269 

Mechanical wounding, 197 

Medfly, 6, 31–36, 59, 64, 68 

Mediterranean areas, 91 

Mediterranean basin, 6, 62, 64, 67, 

74, 79, 81, 87, 89, 92, 94, 97 

Mediterranean black scale, 30, 36 

Mediterranean climates, 241 

Mediterranean countries, 45, 64, 66, 

91, 96 

Mediterranean fruit fly, 29–31, 54, 

56–58, 62, 64, 72, 89, 90, 91 

Mediterranean region, 3, 4 

Mediterranean, 3, 4, 6, 7, 26 

Medlure, 92 

Megalopygidae, 236 

Meiosis, 260, 286, 290 

Meira argovae, 285 

Meira geulakonigii, 285, 301 

Melanocallis caryaefoliae, 134, 159 

Melanocallis caryaefoliella, 138 

Meliaceae, 194 

Meloidogyne fallax, 130 

Meloidogyne incognita, 129

INDEX 

349 

Meloidogyne javanica, 120, 124 

Melon aphid, 75 

Member states, 21, 241 

Membranes, 257, 262, 277 286 

Mentzelia punila, 194 

Merculiaris annua, 84 

Merozoites, 290 

Metabolism, 195 

Metalaxyl, 5 

Metaphycus bartletti, 37 

Metaphycus helvolus, 37, 63 

Metaphycus lounsburyi 

(= Metaphycus bartletti), 18 

Metaphycus lounsburyi, 18, 63 

Metaphycus swirskii, 18, 37 

Metarhizium anisopliae, 283, 299, 

304 

Metarhizium, 283, 296, 301, 304 

Metaseiulus arboreus, 318 

Metaseiulus citri, 318 

Metaseiulus occidentalis, 252, 254–257, 

289, 292, 299, 304 

Metaseiulus pomi, 318 

Metazoa, 286 

Metcalfa pruinosa, 7, 15 

Meteorological data, 30 

Meteorological models, 175 

Meteorological parameters, 172 

Meteosat, 172 

Methomyl, 21–25, 33, 44 

Methoxyfenozide, 21, 22, 24, 45 

Methyl anthranilate, 154 

Methyl carbitol, 154 

Methyl jasmonate, 202–203 

Methyl myristate, 154 

Methylcyclohexanecarboxylic acid, 

92 

Metronidazole, 294 

Mexico, 82, 89, 133, 135, 143, 159, 

181, 182, 278, 279 

Microbial miticide, 255 

Microbial products, 241 

Microbiological identification, 257–258 

Micrococcaceae, 255–256 

Microcosm assays, 112 

Microlysis, 121 

Microorganisms, 92, 227, 249, 250, 

257, 258, 322 

Microscopic surveys, 258 

Microsphaera penicillata, 141 

Microspora, 288, 289, 290, 291, 299, 

301, 304, 308 

Microsporidia, 249, 291–294 

Microsporidiosis, 291, 293, 300 

Microsporidium phytoseiuli, 288, 

301 

Microsporidium, 288, 291, 292, 300, 

304 

Microterys nietneri, 63 

Microtritia minima, 289 

Microwave, 166 

Mid infrared, 166 

Middle East, 74, 89, 181 

Midgut, 251, 252, 277, 290, 291 

Migratory locust, 177, 178, 179, 

182 

Millet, 155 

Mine, 80, 81 

Mineral oil, 21–25, 67, 68, 79, 89 

Mint, 92 

Minute pirate bug, 148 

Miridae, 7 

Mirrors, 236 

Mississippi, 268, 307 

Mite pest, 50, 249, 250, 280, 281 

Mite predators, 133, 156 

Mite, 13, 24, 29, 30, 50, 51, 53, 54, 56, 

57, 66, 68, 75, 102, 111, 126, 133, 

136–140, 151, 152, 154, 156–158, 

192, 199–202, 249–260, 264–267, 

269–272, 274–275, 277–285, 287, 

289–300, 311, 313, 316, 318–321, 

322, 323, 324, 325 

Miticide, 136, 137, 139 

Mitochondria, 285, 291 

Mitosis, 254 

Mitosomes, 291 

Model, 31, 142, 143, 161 

MODIS data, 178 

MODIS, 168, 172, 175, 176, 178, 

185–188 

Moericke pan-traps, 14, 46

350 

INDEX 

Moisture, 146–148, 150, 151 

Mole cricket, 106 

Molecular beacon, 121 

Molecular detection, 119 

Molecular methods, 111, 285 

Molecular techniques, 120, 249, 291, 

293, 295 

Mollicutes, 260 

Monellia caryella, 134, 138, 158, 

159, 161 

Monelliopsis pecanis, 134, 138, 159, 

161 

Monieza expansa, 290 

Moniliaceae, 284 

MONITOR-E-1, 168 

Monitoring, 6, 13, 14, 30, 32–37, 39, 

43, 45–49, 51, 55, 77, 78, 79, 96, 

139, 155–157, 163, 167, 169, 172, 

174, 175, 178, 180–183, 236, 240, 

312, 313, 321 

Monoclonal antibodies, 293 

Mononychellus tanajoa, 262, 265, 

266, 268, 276, 302, 305, 306 

Mononychellus, 262, 265, 266, 274, 

276, 300, 302, 305 

Montenegro, 4, 7 

Moraceae, 194 

Morningglories, 143 

Morocco, 4, 26, 82, 83, 84, 98 

Morphology, 236, 240 

Mortality, 139, 140, 142, 160, 216, 

217, 224–228, 240, 254, 255, 267, 

271, 277, 279, 281, 283, 284, 285, 

298, 306, 307, 317 

Mosquitoes, 290 

Moth, 20, 30, 196, 197, 206, 237, 

238, 239, 240, 241, 243, 244 

Moult, 236 

Moulting, 75 

Mouth parts, 250 

Mouth, 211, 212 

Mucosal tissues, 236 

Mucous substance, 261, 263 

Mucous tissues, 236 

Mud, 216 

Mulberry, 76, 79 

Multicolored asian ladybeetle, 134, 

139, 153 

Multiplex systems, 120 

Mummies, 270 

Mummified cadaver, 272 

Mummy, 264 

Musca domestica, 215 

Muscle tissue, 253, 292 

Muscles, 277 

Mutualism, 259 

Mutualistic bacteria, 224 

Mycelial preparations, 278 

Mycelium, 261, 263, 272, 278, 286 

Mycetaspis personata, 10 

Mycorrhizae, 150 

Mycosed aphids, 283–284 

Mycosphaerella caryigena, 141 

Mycotoxins, 261 

Myrtle-leaved orange, 4 

Myxospora, 289 

Myzus ornatus, 8 

Myzus persicae, 8, 45, 53, 55 

N 

Napamichum aequifolium, 288 

Native stands, 134, 135, 136 

Natural enemies, 5, 6, 12, 26, 37–42, 

44–48, 51, 53, 55, 57, 61, 63, 64, 66, 

67, 68, 69, 70, 72, 74, 77, 78, 81, 87, 

88, 93, 94, 97, 102, 104, 110, 111, 

115, 123, 128, 137, 153, 154, 156, 

158, 209, 212, 214, 313, 321 

Natural mortality, 281 

Natural organisms, 5 

Natural resources, 164 

Near infrared, 166 

Neem extract, 154 

Nelson Island, 268 

Nematode infection, 224, 225, 229 

Nematode suspension, 226–228 

Nematodes, 101, 105, 109, 110, 112, 

113, 115, 116, 119, 120, 123–130, 

209, 216, 224–233 

Nematophagous fungi, 111 

Neochrysocharis formosa, 43, 44, 

86

INDEX 

351 

Neodryinus typhlocybae, 15 

Neogregarines, 290 

Neogregarinida, 289 

Neomyzus circunflexum, 8 

Neonicitinoid insecticides, 138 

Neoseiulus barkeri, 257, 319 

Neoseiulus bibens, 257, 318 

Neoseiulus californicus, 65, 66, 70, 

315, 316, 318, 320–325 

Neoseiulus cucumeris, 252, 288, 292, 

316, 319 

Neoseiulus fallacis, 318 

Neoseiulus idaeus, 318 

Neoseiulus longispinosus, 318, 320 

Neoseiulus tiki, 318 

Neoseiulus umbraticus, 319 

Neoseiulus, 252, 257, 260, 271, 276, 

288, 292, 305 

Neozygitaceae, 261–263, 302, 304 

Neozygites abacaridis, 265, 305 

Neozygites acaricida, 266 

Neozygites acaridis, 266, 305 

Neozygites adjarica, 267, 302 

Neozygites cf. acaridis, 268 

Neozygites floridana, 264, 266–269, 

297, 301–302, 304, 305, 308, 309 

Neozygites tanajoae, 262, 266, 268–271, 

298, 302, 303 

Neozygites tetranychi, 266 

Neozygites tetranychid, 266 

Neozygites, 262–269, 272, 297, 298, 

301–306 

Nephus (Sidis) anomus, 17 

Nephus bisignatus, 38, 56 

Nephus includens, 38, 56 

Nephus quadrimaculatus, 17 

Nephus reunioni, 37, 88 

Nephus sidi, 37 

Nepticulidae, 83, 84 

Nerium oleander, 67 

Nerolidol, 22 

Nest, 237, 241 

Nesting sites, 134, 151 

New South Wales, 179, 184 

Newly formed fruits, 48 

Nezara viridula, 7, 155 

Nicotiana sylvestris, 197, 207 

Nicotiana tabacum, 191 

Nifedipine, 294 

Nipaecoccus nipae, 9 

Nitidulid, 38 

Nitrogen fertilizer, 52 

Nitrogen partitioning, 203 

Nitrogen, 52, 133, 136, 137, 146–149, 

152, 153, 160, 161 

NOAA-GOESS, 168 

Noctuidae, 10, 236 

Nolidae, 238, 244 

Nomadacris septemfasciata, 181 

Nomuraea rileyi, 299 

Nonselective acaricide, 254 

Nonsexual spores, 261 

Norflurazon, 144 

Normalized Difference Vegetation 

Index, 173 

North America, 238, 240 

North Carolina, 267, 283, 299 

Nosema acari, 288 

Nosema euzeti, 288 

Nosema führeri, 288 

Nosema helminthorum, 288 

Nosema hermanniae, 288 

Nosema ptyctimae, 288 

Nosema sperchoni, 288 

Nosema steganacari, 288 

Nosema steinhausi, 289 

Nothroidea, 287, 288, 289 

Nothrus silvestris, 288, 306 

Notodontidae, 134, 239, 245 

Notostrix attenuata, 274 

Notostrix formosae, 275 

Nozzle, 240 

Nuclei, 251, 252, 253, 261, 286, 292, 

295 

Nucleotide sequence, 260 

Nucleus, 251, 277, 285 

Nursery, 12, 22, 24, 43–45, 47, 61, 

65, 66, 74, 86 

Nut crop, 134, 135, 136 

Nut production, 133, 135, 136 

Nutsedge, 143 

Nymph, 41, 140, 215

352 

INDEX 

Nymphal distribution, 164 

Nymphal exuviae, 75, 79 

Nymphal habitats, 178 

Nymphalidae, 11, 236 

O 

Oak Processionary Moth, 237, 245 

Oak stands, 237 

Oak, 76, 237, 238, 240, 244 

Ocellar bristles, 89 

Ochrogaster lunifer, 239, 244 

Octadecanoid pathway, 191, 201 

Octadecanoid signal pathway, 191 

Oenopia (Synharmonia) conglobata, 

41, 46 

Oenothera laciniata, 144 

Offshoots, 210, 215, 216 

Offspring, 259, 291, 296, 316 

Ohio, 114, 115 

Oil palm, 209, 218, 223, 231, 232, 

233 

Oklahoma, 142, 148, 159, 161 

Oleander scale, 74, 79 

Oleander, 76, 79, 87 

Olfactory cues, 90 

Oligonychus biharensis, 256 

Oligonychus gossypii, 266, 271, 276, 

281 

Oligonychus hondoensis, 266, 267, 305 

Oligonychus ilicis, 276 

Oligonychus pratensis, 266, 302 

Oligosporidium occidentalis, 289, 

293 

Olive black scale, 75 

Olive, 76, 79 

Oman, 82, 83, 84 

Onion, 196 

Ontogeny, 296 

Oocysts, 290 

Oomycetes, 104 

Oozing, 217 

Opius concolor, 33 

OPM, 237, 240, 241, 242, 243 

Oral secretion, 189–191, 199, 204 

Orange spiny whitefly, 74 

Orange trees, 33, 42 

Orange, 3, 22, 29, 32–36, 39, 42–43, 

47, 49, 61 

Orbiliales, 119, 129 

Orchard fauna, 74 

Orchard, 6, 14, 22, 26, 27, 31, 33–43, 

45–47, 49–51, 54, 55, 58, 65, 67, 

68, 70, 72, 74, 77, 78, 82, 85, 86, 

88, 89, 92–97, 99, 102, 103, 105, 

107, 109, 110, 112, 115, 124, 125, 

127, 133–137, 140–158, 161, 179, 

252, 268 

Orchid fleck virus, 252 

Orchid, 252 

Organelles, 285, 290 

Organic matter, 114, 133, 137, 147, 

149, 150 

Organochlorine soil pesticides, 105 

Organochlorine, 5 

Organophosphate insecticides, 138, 139 

Organophosphates, 89, 96 

Organs, 13 

Oribatid mite, 290, 306 

Oriental migratory locust, 178 

Ornamental plants, 76 

Ornamentals, 104 

Orthezia insignis, 8 

Ortheziidae, 8 

Orthoptera, 7 

Oryctes rhinoceros, 212, 232 

Oryzalin, 144 

Oshin, 216 

Osmotic pressure, 262 

Otiorrhynchus aurifer, 11 

Outbreak, 29, 36–39, 41, 45, 47, 50–51, 

136, 139, 153, 156, 163, 164, 

171–173, 178, 179, 181, 182, 184, 

186, 188, 235, 236, 237, 238, 242, 

278 

Outdoor crops, 297 

Ovarial development, 269 

Ovary, 291, 293 

Overgraftings, 43, 48 

Overwintering, 32, 58 

Oviposition, 90–92, 195, 196, 204, 

211, 212, 252, 254, 269, 277, 

294

INDEX 

353 

Ovipositor, 89 

Ovisac, 87 

Oxalis pes-caprae, 68 

Oxamyl, 23, 24, 47, 50 

Oxydemeton-methyl, 21, 23, 24, 25 

Oxythyrea funesta, 11 

P 

Pachyneuron aphidis, 46 

Pachyneuron vindemmiae, 92 

Pachyneuron, 46 

Paecilomyces eriophytis, 282 

Paecilomyces farinosus, 283 

Paecilomyces lilacinus, 283 

Paecilomyces, 282, 283, 296 

Paenibacillus nematophilus, 112 

Paenibacillus, 112, 113, 116, 125 

Pakistan, 83, 173, 174 

Palaearctic region, 237 

Palestine, 209 

Palm stems, 218 

Palm tissues, 211, 218, 219, 222 

Palm tree, 209–211, 218–220, 222, 

224, 226–229, 231, 232 

Palm, 76, 79, 209–212, 216–219, 

222, 226, 229, 230, 232, 233 

Panonychus ulmi, 53, 250, 251 

Panonychus citri, 12, 13, 24, 29, 30, 

50, 51, 54, 56, 61, 62, 65, 66, 68, 

74, 250, 254, 265, 266, 267, 274, 

276, 280, 307 

Pantomorus cervinus, 11 

Paper envelope, 33 

Paper folded traps, 33 

Parabemisia myricae, 8, 40, 41, 56, 

74, 93, 94, 98 

Paraffin oil, 39, 41, 45, 47, 49, 53 

Paragus albifrons, 46 

Paraleyrodes bondari, 8 

Paraleyrodes citricolus, 8 

Paraleyrodes minei, 8 

Parapheromone, 32, 33, 92 

Paraquat, 144 

Parasaissetia nigra, 9 

Parasitic females, 216 

Parasitic fungi, 260 

Parasitic wasps, 191, 201, 207 

Parasitidae, 264, 265, 266, 267 

Parasitiformes, 274 

Parasitism levels, 34 

Parasitism, 13 

Parasitization, 84–86, 92–95, 99 

Parasitoid species, 37, 38, 42, 43 

Parasitoid, 7, 14, 26, 27, 33, 34, 36–46, 

48, 54–58, 64, 65, 67, 71, 78, 81–89, 

92, 93, 94–99, 209, 214, 224, 239, 

243 

Paratheresia menezesi, 214 

Paratrichodorus pachydermus, 122 

Pardosa cribata, 70, 72 

Parietaria diffusa, 84 

Parlatoria pergandii, 62, 75, 94 

Parlatoria ziziphi, 10, 23 

Paros, 42 

Parthenogenesis, 94, 249, 258, 309 

Parthenogenetic biotypes, 79 

Parthenogenetic development, 261 

Parthenolecanium persicae, 9 

Particles, 250–253, 304, 307 

Paspalum notatum, 143 

Paste, 217, 218 

Pathogen, 250, 251, 258, 267, 268, 

271, 272, 278, 290–293, 295–297, 

301–306, 307 

Pathogenesis, 259 

Pathogenic fungi, 250, 268, 302 

Pathogenicity, 142, 225, 227, 230, 

255, 283, 283, 284, 297, 306 

Pathogens, 197, 200, 202, 205, 206, 

215, 249, 250, 261, 262, 271, 272, 

285, 287, 291, 292, 295, 296, 

299–301, 303, 305–307, 309 

PCR buffer, 120 

PCR template, 120 

PCR, 120 

Peach, 76, 79, 90, 91, 252, 306 

Pear, 31, 75, 76, 79, 90 

Pecan aphids, 134, 136, 139, 140, 

148, 152, 157, 159, 162 

Pecan leaf scorch mite, 136, 138, 

139, 158 

Pecan nut casebearer, 138–140

354 

INDEX 

Pecan trees, 134, 136, 144, 146, 148, 

154, 155, 160 

Pecan weevil survival, 139 

Pecan weevil, 136, 138–140, 152, 

154, 156 

Pecan, 133–149, 151–162 

Peloponnese, 20, 30, 36, 42, 43, 47, 

48, 49 

Pendimethalin, 144 

Penetration, 236, 250, 263, 269, 273, 

277 

Pentatomidae, 7, 138, 155 

Penthaleidae, 266 

Penthaleus major, 266 

Pepper, 320, 325 

Pergamasus crassipes, 264 

Pergamasus, 264–267 

Peridroma saucia, 10 

Persimmon, 87, 90 

Perturbance, 314 

Peru, 82 

Pest control, 5, 6, 236, 243, 311, 313 

Pest infestations, 311 

Pest management practices, 102, 123 

Pest management, 137, 148, 152, 

156, 157, 158, 160 

Pest outbreaks, 136, 140 

Pest species, 250, 283 

Pest, 3, 5, 6, 7, 13, 21, 25–32, 36–42, 

44–46, 48, 49, 51, 53, 55, 56–58, 

59, 61, 62, 63, 64, 65, 67, 68, 71, 

72, 74, 76, 77, 79, 86–88, 90, 91, 

93, 94–96, 98, 101–107, 110, 

123–125, 127, 133, 136–140, 148, 

153, 154, 156, 158, 160, 189, 192, 

193, 200, 201, 203, 204, 206, 250, 

255, 268, 269, 280, 281, 292, 296, 

297, 308, 309 

Pesticide applications, 4 

Pesticide groups, 5 

Pesticide list, 39 

Pesticide treatments, 102 

Pesticide, 3, 5, 6, 21, 25, 26, 32, 36, 

61, 66, 67, 71, 101, 102, 104, 106, 

128, 133, 135–137, 155, 156, 190, 

192, 203, 204, 207, 312, 322 

Petrobia hartii, 68 

Petroleum oil, 39, 47, 49, 53, 102 

Pezothrips kellyanus, 49, 50 

Pezothrips kellyanus, 7, 29, 49, 50, 

54, 58, 74 

Phaenacoccus madeirensis, 9 

Phaenoglyphis, 46 

Phaneroptera nana, 7 

Phaseolus lunatus, 199, 206 

Phasmarhabdites hermaphrodita, 

122 

Pheidole pallidula, 89 

Phenological changes, 182 

Phenthoate, 217 

Pheromone dispensers, 77 

Pheromone trap, 77, 79, 88, 214, 

218–222, 229, 231 

Pheromone, 14, 77, 78, 81, 91, 96 

Phialid, 277 

Phialides, 273 

Phialidic conidiogenesis, 296 

Phialidic conidiogenous cell, 296 

Phloem sap, 93 

Phoenix canariensis, 211 

Phomalactone, 277 

Phosalone, 22 

Phosmet, 21–25, 36, 39, 92, 138 

Phosphonate potassium, 5 

Phosphorous, 150, 294 

Phosphorylation, 200 

Photoperiod, 316 

Photorhabdus, 105, 224 

Phthiracaroidea, 287–289 

Phthiracarus globosus, 287, 288 

Phthiracarus piger, 287, 289 

Phthiracarus, 287, 288, 289 

Phyla, 260, 289 

Phyllocnistis citrella, 6, 10, 24, 29–31, 

42, 53–54, 56–58, 62–64, 71, 72, 

74, 80–86, 94–99 

Phyllocoptruta oleivora, 11, 24, 

273–275, 277, 280, 299, 301, 306 

Phylogenetic studies, 291 

Physiological and behavioural 

responses, 319 

Physiological changes, 191

INDEX 

355 

Physiological mechanisms, 316 

Physiological processes, 254 

Physotritia duplicata, 289 

Phytohormone, 197 

Phytonemus pallidus, 275 

Phytophagous mites, 139, 315 

Phytophagous populations, 240 

Phytophthora cactorum, 141 

Phytophthora nicotianae, 104 

Phytophthora palmivora, 104 

Phytophthora, 103, 105, 107, 124, 

125 

Phytoprotection, 200, 206 

Phytopthora Shuck and Kernel Rot, 

141 

Phytoptus avellanae, 283 

Phytoregulators, 73 

Phytosanitary control, 78 

Phytoseiid mites, 5, 68 

Phytoseiid releases, 321 

Phytoseiid, 50, 53, 251, 292, 293, 

294, 304, 314, 316, 317, 320, 321, 

322, 323, 324, 325 

Phytoseiidae, 50, 54, 56, 61, 66, 69, 

71, 77, 256, 257, 264, 265, 269, 

276, 280, 288, 289, 292, 299–302, 

307, 308 

Phytoseiulus longipes, 318 

Phytoseiulus macropilis, 318 

Phytoseiulus persimilis, 65, 66, 70, 

252, 254–257, 265, 288, 292–294, 

299, 300, 301, 306–308, 315, 316, 

318, 320, 322, 323, 325 

Phytoseius macropilis, 319 

Phytoseius spoofi, 319 

Picorna-like viruses, 253 

Pieris brassicae, 191 

Pieris rapae, 196, 200 

Pigeon Pea Mosaic virus, 252 

Pigweed, 143 

Pimetrozine, 23 

Pine Processionary Moth, 237 

Pine, 202, 237 

Pinus canariensis, 237 

Pinus halepensis, 237 

Pinus laricio, 237 

Pinus nigra austriaca, 237 

Pinus pinaster, 237 

Pinus pinea, 237 

Pinus sylvestris, 237 

Piridaben, 21, 23, 25, 68 

Pirimicarb, 21–23, 25, 47, 67, 68 

Pirimiphos-methyl, 21–23, 68 

Pistacia lentiscus, 83 

Pittosporum, 87 

Planococcus citri, 6, 9, 14, 24, 29–31, 

36, 51, 56, 62, 63, 65, 66, 71, 74, 

87–89, 96, 99 

Plant biomass, 189, 193, 204 

Plant breeders, 135 

Plant composition, 32 

Plant defense genes, 200 

Plant defense, 191, 193, 194, 205, 

207 

Plant elicitor, 197 

Plant growth regulators, 5 

Plant invasion, 311 

Plant pathogens, 285 

Plant pathology, 133 

Plant protection products, 5, 21, 26, 

36, 39, 41, 45, 47, 49, 50, 53 

Plant Protection Services, 30, 31, 35, 

36 

Plant protection, 5, 21, 26, 30, 31, 54 

Plant tissue, 250 

Plant volatiles, 190, 191, 195, 204, 

205, 207, 255 

Plantation, 219–222, 230 

Planting, 5 

Plant-inhabiting mites, 250, 280 

Plasmodium vivax, 286 

Plastic buckets, 218 

Plastic McPhail trap, 32 

Platygastridae, 16 

Platynothrus peltifer, 287, 289 

Pleistophora cephei, 289 

Pleistophora dindali, 289 

Pleistophora oribatei, 289 

Pleistophora platynothri, 289 

Pleistophoridae, 292, 300 

Plugs, 258, 259, 294 

Plywood, 134

356 

INDEX 

Pnigalio agraules, 85 

Pnigalio pectinicornis, 43, 44, 55 

Pnigalio soemius, 44, 58, 86 

Poaceae, 69 

Poales, 69 

Poland, 267, 300, 305 

Polar filament, 291, 293 

Polar tube, 291 

Pollen, 236 

Pollution, 5 

Polyhedra, 295 

Polypeptide, 255, 277 

Polyphagotarsonemus latus, 12, 275, 

280, 283, 305, 306 

Pomelo, 22 

Poor condition, 294 

Population biology, 110, 123 

Population density, 14, 32, 51, 235, 

250, 251, 273, 283, 306, 314 

Population dynamics, 316, 321 

Population equilibrium, 205 

Population fluctuation, 222 

Population levels, 32, 34, 39, 46, 47 

Population size, 32, 250 

Population, 74, 77, 79, 86, 88, 92, 94, 

98 

Populations balance, 314 

Porosity, 109, 110, 113, 114 

Portugal, 4–7, 11, 15–20, 26, 74, 83, 

85, 96 

Potassium salts, 21, 23 

Potassium, 21, 22, 23, 294 

Potato-dextrose agar, 284 

Pothos, 87 

Poultry red mite, 260, 302 

Powdery mildew, 141 

PPM, 237, 241 

Praecocilenchus ferruginophorus, 216 

Praon volucre, 46 

Pratylenchs neglectus, 121 

Pratylenchs penetrans, 121 

Pratylenchs thornei, 121 

Pratylenchus zeae, 120, 124 

Prays citri, 10, 14, 24, 30, 31, 37, 38, 

48, 49 

Predaceous mites, 311, 313, 324 

Predaceous stink bugs, 148 

Predation, 110, 112, 115, 116, 119, 

123 

Predator, 7, 13–14, 37–39, 41, 45–47, 

51, 53, 56, 57, 65, 67, 77, 79, 87, 

88, 92, 95, 189–192, 194, 196, 

200–204, 207, 209, 215, 224, 231, 

249, 252, 254, 255, 259, 271, 290, 

292–294, 299, 303, 306, 307, 311, 

313–317, 319–321, 323, 324 

Predator-predator interactions, 323 

Predatory beetles, 77, 79 

Predatory insect, 189, 190 

Predatory mite, 53, 249, 250, 252, 

254, 255, 258, 260, 269, 271, 281, 

285, 292, 293, 298, 299, 300, 303, 

306, 307 

Prenuptial association, 290 

Prepollination, 141, 142 

Prepupae, 84 

Pre-pupal stage, 211 

Prevalence, 271, 281, 294, 304 

Prey densities, 317, 318 

Prey, 38, 47, 252, 255, 259, 290, 

292–293, 304, 315, 319 

Prey-predator system, 321 

Primary conidia, 261 

Primary conidium, 263 

Primary leaf, 203 

Primary productivity, 203 

Primer targets, 118 

Primers, 116, 118, 120, 124, 129 

Privet, 76 

Probe, 118 

Probes, 116, 118, 124, 129 

Procida, 16, 17 

Proctolaelaps, 275 

Prodinychidae, 267 

Product amplification, 116 

Production, 45, 48, 50, 61, 66, 133, 

135–137, 139, 140, 142, 143, 

147–149, 153, 156–158, 160, 162 

Progeny, 259, 294 

Proline, 193, 194, 202 

Pronematus, 274 

Propagation, 270

INDEX 

357 

Propargite, 21, 22, 24, 25, 68 

Propilus syagris, 274 

Propylea quatuordecimpunctata, 46 

Protease inhibitor, 199 

Protected crops, 69 

Protein hydrolysate, 32, 33, 35 

Proteinaceous bodies, 250 

Proteinase K, 120 

Proteobacteria, 137 

Protista, 286 

Protocols, 5 

Protoplasm, 262, 292 

Protopulvinaria pyriformis, 9 

Protozoa, 286, 287, 290, 306 

Pruning, 39, 44, 45, 73, 79, 89, 141 

Pseudo-arrhenotoky, 317 

Pseudococcidae, 9, 24, 29, 56, 66, 71 

Pseudococcus calceolariae, 9, 74 

Pseudococcus longispinus, 9 

Pseudococcus viburni, 9 

Pseudomonas aeruginosa, 215, 231 

Pseudomonas putida, 255, 256, 300 

Pseudomonas syringae, 197, 205 

Pseudopodia, 286 

Psyllidae, 83 

Psylliodes chrysocephala, 198 

Psyttalia concolor, 92 

Psyttalia incisi (= Opius incisi), 21 

Psyttalia incisi, 21, 63 

Pteromalidae, 38, 81, 92 

Public hygiene, 236 

Pulp, 90 

Pulvinaria floccifera, 9 

Pumelo, 3, 29, 39, 49 

Pupa, 80, 85, 90, 211, 214, 225 

Pupae, 90, 214, 215, 217, 225 

Pupal cell, 80 

Pupal stage, 81, 82, 91 

Pupation, 237 

Putrescine, 32 

Pygidium, 79 

Pymetrozine, 21–23, 47, 68 

Pymotidae, 215 

Pyralidae, 10 

Pyrethrines, 22, 23, 47 

Pyrethroid insecticides, 5 

Pyrethroid, 92 

Pyridaben, 22, 24, 53 

Pyrimiphos-methyl, 23–25 

Pyriproxifen, 21–23, 25, 68, 77 

Pyroglyphidae, 256 

Q 

qPCR, 116–120, 124, 127 

Quadrastichus citrella, 20, 63, 81, 82 

Quadrastichus, 20, 43, 44 

Quail, 151, 156 

Qualitative damage, 49 

Quantitative PCR, 116 

Quarantine pests, 6 

Quarantine, 6, 26, 41, 42, 45, 62, 64, 

74, 84, 92, 97, 104, 138 

Queensland, 179, 184 

Quercus cerris, 238 

QUIAmp DNA mini kit, 121 

R 

RADAR, 167, 180, 182 

Radiation, 165, 166, 167 

Radiometric resolution, 167 

Rainfall, 140, 141, 142, 149, 151, 

159, 164, 169, 173–176, 268, 281, 

283 

RAMSES, 176 

Rapeseed, 197 

Raphanus raphanistrum, 196 

Rating, 317 

Ratzeburgiola incompleta, 86 

rDNA, 118, 268, 296 

Real time qPCR, 118 

Real-time PCR, 116, 126, 128 

Rearing, 64, 209, 211, 292, 293, 

314–315 

Recovery, 217, 226, 227 

Rectum, 258, 294 

Red alders, 195 

Red Palm Weevil, 209, 230–232 

Red ring disease, 223, 231–233 

Red Sea, 173, 176 

Red spider mite, 74 

Reflectance, 165, 166 

Registration, 21, 139, 224

358 

INDEX 

Regression model, 271 

Regulation, 249, 250 

Regulatory measures, 42 

Relative humidity, 65, 263, 270, 271, 

277, 283, 296, 297, 299 

Release, 15–20, 62, 64–66, 214, 215, 

217, 221, 230 

Remote sensing satellites, 163, 167, 183 

Remote sensing technology, 164 

Remote sensing, 163, 164, 165, 167, 

169, 172, 174, 175, 177, 179, 181, 

182–188 

Renibacterium salmoninarum, 256 

Repellents, 154 

Replication, 291 

Reproduction, 39, 44, 50, 79, 98, 192, 

258, 260, 261, 272, 286, 290, 292, 

301, 317 

Reproductive potential, 250 

Reproductive tissue, 258 

Research programs, 314 

Reservoir plants, 67 

Residual toxicity, 67 

Resistance genes, 143 

Resistance, 6, 137, 141, 143, 156–158, 

190, 192, 196–198, 200, 206, 207 

Resolution, 167, 168, 172, 174–176, 

178, 181, 182, 186 

Resting spores, 261, 262, 264, 270, 

296, 298 

Resurgence, 138, 139, 156, 157 

Retracus elaeis, 275, 308 

Retracus johnstoni, 274, 284 

Reversed plastic cups, 33 

Revision, 22 

Rhizobia, 151 

Rhizobiaceae, 137 

Rhizobial inoculant, 151 

Rhizobiales, 137 

Rhizoglyphus robini, 280 

Rhizoids, 263, 264 

Rhizopoda, 286 

Rhodes, 42 

Rhododendron, 87 

Rhodolia cardinalis, 38, 63, 67, 68 

Rhopalosiphum maidis, 8, 45 

Rhopalosiphum padi, 69 

Rhynacus, 275 

Rhynchophorus vulneratus, 218, 223 

Rhynchophorus ferrugineus, 209, 210, 

212, 214–216, 218–220, 222–225, 

228, 229–232 

Rhysotritia ardua, 287, 288, 306 

Rhyzobius (= Lindorus) lophanthae, 

19 

Rhyzobius forestieri, 17, 37, 55 

Rhyzobius lophanthae, 38, 63, 77, 

79 

Ribosomal DNA, 118, 130 

Ribosomal RNA gene, 289 

Ribosome-inhibiting proteins, 277 

Rickettsia, 259 

Rickettsiaceae, 257, 258 

Rickettsiales, 258, 309 

Rickettsia-like infections, 258 

Rickettsia-like organisms, 257–259 

Rickettsieae, 257 

Rickettsiella phytoseiuli, 256, 308 

Rind bleaching, 50 

Ripening, 32, 35 

Risk assessment, 30, 163, 175, 182 

Risk rating, 138, 154, 159 

Rivers, 165, 177 

RNA synthesis, 254 

Roads, 165, 170 

Robinia pseudoacacia, 239, 244 

Rodolia (= Novius) cardinalis, 16 

Rodolia cardinalis, 25, 38, 61, 63 

Romalea guttata, 196 

Root weevil, 101, 104, 106, 107, 109, 

110, 124, 125, 127, 129 

Root-knot nematodes, 112 

Roots, 104, 105a, 127 

Rosaceae, 238 

Rostrum, 211, 212 

Rotenone, 22–24 

Royal palm, 209 

RPW larvae, 215, 225 

RPW, 209–212, 214–230 

Rubber plantations, 281, 282 

Rubber tree leaves, 281 

Rubber tree, 281

INDEX 

359 

Rubus ulmifolius, 83, 84 

Rural community, 135 

Ryegrass, 152 

S 

Sac, 260, 261 

Sago palm, 209 

Sahel, 173 

Saissetia coffeae, 9 

Saissetia oleae, 9, 18, 23, 29, 30, 31, 

36–39, 55, 62, 63, 75, 94 

Salicylic acid, 200 

Saliva, 76 

Salix alba, 83 

Salvinia molesta, 198, 206 

Samea multiplicalis, 198, 206 

Samos, 42 

Sample, 109, 110, 115, 117, 119–121, 

124, 126, 127 

Sampling methods, 119 

Sampling schemes, 37 

Sampling, 6, 26, 30, 31, 33, 37, 40, 

43, 46–49, 51, 53, 55 

Sand, 107–109, 112, 114, 115 

Sap exudated, 210 

Sap, 73, 76, 210, 217, 222, 226 

Saprophytes, 115 

Sapsucking insects, 89 

Sarcomastigophora, 289 

Sardinia, 15, 16–18 

Satellite images, 164, 172, 174 

Satellite-derived information, 178 

Satellites, 164, 165, 167, 168, 171, 

172, 174, 176, 178, 182, 183 

Saturation point, 263, 297 

Saturniidae, 236, 239 

Saudi Arabia, 74, 89, 173, 186, 209, 

210, 215, 216, 225, 228, 230–233 

Scab control, 141 

Scab epidemics, 142 

Scab resistance, 143 

Scaeva albomaculata, 46 

Scale insects, 30, 36–39 

Scale population, 77 

Scale, 29, 30, 36–39, 42, 62, 75–79, 

94–99 

Scanners, 166 

Scapteriscus, 106 

Scarabaeidae, 11 

Scarring, 49, 50 

Schistocerca piceifrons piceifrons, 181 

Schistocerca, 170, 173, 183, 185, 

186, 188 

Schizogony, 290 

Scolia erratica, 214 

Scutellista cyanea, 38 

Scutellum, 89 

Scutovertex minutus, 287, 290 

Scutoverticidae, 287 

Scymnus, 79, 87 

Scymus (Pullus) subvillosus, 46 

Season, 268, 270, 271, 278, 282, 297, 

298 

Secondary conidia, 261, 262, 296 

Secondary conidium, 263 

Secondary hosts, 257 

Secondary infestations, 91 

Secondary metabolic products, 191 

Secondary metabolism, 200, 205 

Seed formation, 147 

Seedling trees, 135 

Seedlings, 136 

Segments, 211 

Seiulus, 276 

Selective insecticides, 44, 48 

Semielacher petiolatus, 18, 43, 44, 

81, 83–86, 97, 98 

Semielacher silvicola, 44, 58 

Semiochemicals, 89 

Senescence, 294 

Sensor, 167, 172, 175 

Sentinel weevils, 111 

Septa, 260, 261, 296 

Sequences, 268, 296 

Serangium montazerii (=Serangium 

parcesetosum), 15 

Serratia marcescens, 257 

Services, 5 

Sesbania extract, 154 

Sesquiterpene hydrocarbons, 92 

Sesquiterpene, 199 

Setae, 239

360 

INDEX 

Sethoxydim, 137, 144, 152 

Seville orange, 3 

Sex allocation, 317, 324 

Sex pheromone, 48 

Sex pheromone-baited traps, 14 

Sex ratio, 81, 211, 220, 224, 296, 

300, 316, 317 

Sexual attractants, 6 

Shaddock, 3 

Shade tree, 133, 158 

Shelter, 222, 228 

Shield, 75, 79 

Shoot tips, 203 

Shoots, 94 

Shrubs, 238 

Shuckworm, 138, 139, 140 

Sicily, 15, 16, 18, 19, 78, 82, 84, 86, 

95, 96, 98, 99 

Sida rhombifolia, 143 

Side effects, 3, 21 

Sieving, 121 

Siglure, 92 

Signalling, 189–191, 195, 198–200, 

201–205 

Silk glands, 277 

Silk, 80, 277 

Simazine, 144 

Singapore, 239, 245 

Skin, 236, 239 

Skis, 134 

Slime, 273 

Slug, 122 

Soft scales, 13, 14, 17 

Software, 164, 169, 170, 171 

Soil bacteria, 240 

Soil chemicals, 114, 119 

Soil cylinders, 116 

Soil erosion, 147, 149, 150, 163 

Soil food webs, 101, 103, 111 

Soil microorganisms, 150 

Soil mulches, 113 

Soil particles, 149 

Soil pH, 151 

Soil properties, 110, 114 

Soil texture, 107, 109, 114, 128 

Soil Treatments, 228 

Soil, 101, 103–105, 107, 109–116, 

119–120, 123–128, 209, 211, 214, 

216, 219, 224, 225–230 

Soilborne biological control agents, 107 

Soilborne organisms, 116, 117 

Soil-inhabiting insects, 230 

Solanaceae, 320, 323 

Solanum, 143 

Solar radiation, 165 

Soldier beetles, 148 

Solenopsis invicta, 154, 161 

Solidago canadensis, 197 

Sonchus, 84 

Sooty mould, 13, 46, 87, 93 

Sorghum, 155 

Sour orange, 3, 22 

South Africa, 64, 66, 68, 71, 83 

South America, 89, 93 

South Asian Tsunami, 164 

South-Eastern Asia, 75 

Soybeans, 155 

Space shuttles, 167 

Spain, 3–7, 12, 15–21, 23, 24, 26, 27, 

61–64, 69–71, 74, 81–84, 99, 101, 

109, 114, 115, 123, 124, 209–211, 

232 

Spatial resolution, 167 

Specialist phytoseiids, 317 

Specificity, 116, 118, 129 

Spectral ranges, 166 

Spectral resolution, 167 

Spectral signature, 165 

Speed, 240 

Sperchon, 288, 304 

Sperchontidae, 288 

Sphaerophoria, 46 

Sphyrapicus varius, 134 

Spider mite, 201, 267, 268, 269, 280, 

285, 297, 299, 301, 317, 320, 324, 

325 

Spider, 62, 66, 70, 81 

Spine, 80 

Spinning disc, 240 

Spinosad, 21, 22, 24, 25, 67, 68, 92 

Spiracles, 79 

Spirodiclofen, 22, 24

INDEX 

361 

Spiroplasma poulsonii, 260 

Spiroplasma, 257, 260, 300, 303 

Spiroplasmataceae, 260 

Spodoptera eridania, 196, 205 

Spodoptera exigua, 198, 199, 207 

Spodoptera frugiperda, 199 

Spodoptera littoralis, 109 

Sporangiophore, 261 

Sporangiospores, 261 

Spore, 112, 240, 241, 246, 254, 

260–264, 270–273, 277–279, 

283–286, 291–293, 296–299 

Sporothrix, 296 

Sporozoa, 286, 306 

Sporozoites, 290 

Sporting goods, 134 

Sporulation, 263, 268, 272, 297, 

299 

Spot treatment, 138 

SPOT VEG, 168 

SPOT-2, 168 

SPOT-4, 168 

SPOT-5, 168 

SPOT-VGT, 175 

Spray applications, 35, 36 

Spray program, 35, 142 

Spray treatments, 48 

Sprayers, 34, 141, 150 

Spraying, 34–36, 52, 197, 209, 211, 

216, 223, 227, 228, 240, 241, 245, 

251, 284 

Sprays, 34, 35, 39, 133, 136–139, 

141, 142, 152, 154–156, 252, 307 

Spring, 13, 14, 237, 241, 242 

Spurges, 143 

Squirrels, 134 

Standard curve, 117 

Standards, 5, 26 

Staphylinidae, 70, 72, 92 

Starvation, 255 

Starving mites, 255 

Steganacarus striculus, 288 

Steinernema abbasi, 216, 225, 226, 

229, 230 

Steinernema affine, 122 

Steinernema arenarium, 118 

Steinernema boemarei, 118 

Steinernema carpocapsae, 106, 224, 

225, 226, 229 

Steinernema cubanum, 118 

Steinernema diaprepesi, 109, 111, 

112, 117 

Steinernema glaseri, 109, 112, 118 

Steinernema guandongense, 118 

Steinernema kraussei, 122 

Steinernema longicaudum, 118 

Steinernema riobrave, 106, 109, 110, 

112 

Steinernema riobravis, 106, 224, 

226–229 

Steinernema scapterisci, 106 

Steinernema, 105, 110, 113, 113, 

117, 123–125, 127–129, 216, 

224–226, 229, 230 

Steinernematidae, 224 

Steinernematids, 111, 112 

Steneotarsonemus fragariae, 275 

Sterile insect technique, 32, 34 

Sticky cards, 77 

Sticky tape, 79 

Stigmella aurella, 84 

Stigmella, 83 

Stimuli, 33 

Stongylida, 112 

Storage, 270 

Stress factors, 312 

Strobilurins, 141 

Subsistence agriculture, 312 

Substrate, 321 

Sucrose centrifugation, 119 

Suction traps, 14 

Sudan, 173, 174, 176, 187, 188 

Sugarcane, 104, 124, 125, 218 

Suitable environments, 312 

Sulfur ammonium, 33 

Sulphur, 136, 294 

Sultanate of Oman, 209, 224, 225, 

230, 231 

Summary maps, 165 

Summer oils, 44 

Summer, 13, 237, 241 

Sunflower, 155

362 

INDEX 

Sunlight, 39, 90, 167, 251, 297 

Sunrise, 214 

Sunset, 214 

Surface water, 5 

Surveys, 164, 165, 171, 175, 176, 

178, 179, 186 

Survivability, 292 

Sustainable control, 36 

Swaziland, 83 

Sweet orange, 34, 73 

Switzerland, 267 

Syagrus romanzoffiana, 284 

SYBR Green, 116, 127 

Symbionts, 249, 260, 296, 302, 303 

Symbiosis, 113 

Symbiotic entomopathogenic 

bacteria, 105 

Sympherobius, 87 

Sympodal conidiogenesis, 296 

Symptoms, 251, 253, 285 

Synergies, 312 

Synthetic fertilizers, 149 

Syria, 82, 84 

Syrphidae, 46 

Syrphids, 67 

Syrphophagus aphidivorus, 46 

Syrphus latefasciatus, 46 

Systemic expression, 191 

Systemic insecticides, 139 

T 

Taiwan, 82, 83, 168 

Tangerine, 3, 22 

Tape worm, 290 

Tapinoma nigerrimum, 11, 89 

Tapinoma simrothi, 11 

TaqMan, 118, 122 

Tarichium acaricolum, 266 

Tarichium azygosporicum, 266 

Tarichium distinctum, 266 

Tarichium hyalinum, 266 

Tarichium monokaryoticum, 266 

Tarichium obtusoangulatum, 267 

Tarichium pusillum, 267 

Tarichium sphaericum, 267 

Tarichium subglobosum, 267 

Tarichium svalbardense, 267 

Tarichium tenuisculpturatum, 267 

Tarichium uropodinis, 267 

Tarichium verruculosum, 267 

Tarichium, 262, 296 

Tarsonemidae, 12, 274, 275, 276, 

280, 283, 305, 306 

Tarsonemus lacustris, 276 

Tarsonemus, 274 

Tau-fluvalinate, 21, 22, 23, 26 

Taxon, 285 

Tebufenozide, 21, 22, 24, 26, 45, 139 

Tebufenpyrad, 21, 22, 24, 26, 53, 68 

Tectocepheus velatus, 266 

Tegumentary appendages, 236 

Teleomorphs, 272 

TEM, 252 

Temperature, 65, 78, 79, 81, 82, 88, 

90–91, 95, 110, 120, 140, 159, 

164, 169, 176, 209, 230, 237, 251, 

268, 270, 283, 294, 297, 306, 309, 

316, 325 

Temporal resolution, 168 

Tenuipalpidae, 12 

Tephritidae, 11, 24, 29, 62 

Terpenoid, 191, 200, 208 

TERRA/MODIS, 168 

Terrestrial traps, 219 

Tetranychidae, 12, 29–30, 50, 54, 

61, 66, 68, 70, 71, 72, 256, 257, 

264–266, 274, 276, 281, 300–305, 

307, 308 

Tetranychids, 50, 51, 53, 249, 252, 

297, 307, 316 

Tetranychus bimaculatus, 265 

Tetranychus cinnabarinus, 274, 276, 

280 

Tetranychus desertorum, 264 

Tetranychus evansi, 265, 284, 301, 305 

Tetranychus kanzawai, 256, 303 

Tetranychus ludeni, 266, 267 

Tetranychus neocaledonicus, 257 

Tetranychus pacificus, 254, 265, 303 

Tetranychus quercivorus, 257, 303 

Tetranychus truncates, 284 

Tetranychus tumidis, 267

INDEX 

363 

Tetranychus tumidus, 265, 268 

Tetranychus turkestani, 257, 265, 276 

Tetranychus urticae, 12, 13, 24, 29–30, 

50, 51, 57, 62, 63, 65, 66, 68, 69, 70, 

72, 75, 200, 201, 252, 254–257, 259, 

264–268, 274, 276, 280, 283–285, 

300, 302, 303, 305, 307, 308 

Tetranychus yusti, 256 

Tetrapolypus rhynchophori, 215 

Tetrastichus ceroplastae, 38 

Tetrastichus giffardianus, 20, 63 

Tettigonidae, 7 

Texas, 82, 104, 124, 136, 137, 140, 

156, 158, 159, 160, 267 

Thailand, 82, 83, 98 

ThaiPhat, 168 

Thaumetopoea pityocampa, 237, 238 

Thaumetopoea processioneae, 237 

Thaumetopoea wilkinsonii, 243 

Thaumetopoea, 237, 238, 243, 244, 

245, 246 

Thaumetopoeidae, 236, 237, 239, 

243–245 

The Netherlands, 249, 253, 271, 292, 

303, 306–308 

Thelohania microtritiae, 289 

Thelytokous, 259 

Thelytoky, 259, 303 

Theoretical approaches, 314 

Thiamethoxam, 22, 23, 24, 47 

Thiophanate methyl, 141 

Thorax, 89, 220 

Threshold cycle, 116 

Thrip, 49 

Thripidae, 7 

Thrips australis, 7 

Thrips flavus, 7 

Thrips major, 7 

Thrips tabaci, 7, 292 

Thrips, 7, 23, 29–31, 49, 50, 54, 57 

Thuringiensin, 254, 255, 303, 307 

Thyme, 92 

Thysanoptera, 7, 23 

Ticks, 258, 303, 305, 307 

TMA, 32, 36 

Tobacco, 191, 195, 197 

Toddy palm, 209 

Tolypocladium, 296 

Tomato, 197, 198, 199, 201, 205, 

207, 320, 323 

Tool handles, 134 

Topography, 164, 176 

TopSat, 168 

Tortricidae, 10, 30 

Toxicity, 255, 303 

Toxin, 107, 191, 199, 239 

Toxoptera aurantii, 8, 23, 29, 45, 47, 

62, 94 

Toxoptera citricida, 6, 8, 23, 45 

Toxoptera citricidus, 74, 94 (see also: 

Toxoptera citricida) 

Trachyuropoda coccinea, 267, 276, 

300 

Trachyuropodidae, 267, 276 

Trajectory Model, 176 

Transcriptional regulation, 200 

Transgenic phytoseiids, 322 

Transmission electron microscopy, 

252 

Transmission, 252, 253, 255, 260, 

264, 292, 297, 303, 304, 306, 307 

Transovarial transmission, 291 

Trap crops, 138, 155 

Trap design, 218 

Trap networks, 35 

Trapping fungi, 119 

Trapping program, 211 

Trapping, 3, 6, 14, 30–33, 48, 58, 

221, 223, 231, 232, 233 

Traps, 14, 32–37, 39, 40, 46, 48, 50, 

55–56, 58, 77, 78, 79, 88, 92, 115, 

125, 129, 211, 214, 218–222, 224, 

228–230 

Treatment, 35, 36, 41, 47, 55, 57 

Tree damage, 104 

Tree dormancy, 149 

Tree phenology, 137 

Tree, 5, 12, 13, 14, 65, 69, 74, 76, 81, 

86, 88, 92–94, 102–104, 107, 235, 

237, 239, 244, 245, 279, 280, 308 

Trials, 242 

Trichilia cipo, 194

364 

INDEX 

Trichlorfon, 21, 22, 24, 26 

Trichlorphon, 216 

Trichodorus similis, 122 

Trichomes, 194, 203, 206 

Trichoplusia ni, 197 

Tricouropoda szczecinensis, 266 

Trimedlure, 14, 32, 33, 92 

Trimethylamine, 32 

Trioza erytreae, 6, 7 

Trioza obsoleta, 83 

Triozidae, 7 

Tristeza virus, 6 

Trombiculidae, 256, 265 

Trombidiidae, 284 

Trombidium gigas, 284 

Trophic cascade, 111, 123, 125 

Tropinota hirta, 11 

Tropinota squalida, 11 

Trumpet creeper, 143 

Trunk injection, 209, 230 

Trunk treatment, 138 

Trunk, 76, 79, 87, 88, 134, 135, 137, 

154, 157, 209, 210, 216–218, 

226–230 

Tsunami, 185 

Tube-like sacs, 260 

Tunisia, 4, 26, 82, 84 

Tunnels, 210, 218, 226, 227, 312 

Turkey oak leaves, 242 

Turkey oak, 238, 242 

Turkey, 4, 5, 7, 15–20, 81, 82, 84, 99 

Tuscany, 242 

Twigs, 13, 14, 76, 79 

Twospotted spider mite, 75, 254, 255, 

259, 260, 267, 283, 284, 301 

Tydeidae, 274, 276 

Tydeus californicus, 276 

Tydeus gloveri, 276, 307 

Type A organisms, 258 

Type B organisms, 258 

Typhlodromalus aripo, 319 

Typhlodromalus limonicus, 319 

Typhlodromalus manihoti, 319 

Typhlodromips newsami, 319 

Typhlodromips sessor, 319 

Typhlodromus (A.) doreenae, 318 

Typhlodromus (Anthoseius) 

caudiglans, 318 

Typhlodromus (T.) exhilaratus, 318 

Typhlodromus (T.) pyri, 318 

Typhlodromus (T.) rickeri, 318 

Typhlodromus athenas, 51 

Typhlodromus athiasae, 280 

Typhlodromus cryptus, 77 

Tyroglyphidae, 288, 291, 309 

Tyrophagus perniciosus, 264 

Tyrophagus putrescentiae, 280, 288, 

291, 304 

U 

UAE, 209, 210, 216, 219–220, 224, 

225, 230 

Ultrastructural morphology, 253 

Ultraviolet, 166 

Unaspis citri, 6, 10, 23 

Unaspis yanonensis, 10, 19, 74 

United Arab Emirates, 209, 231, 232, 

233 

United Kingdom, 237, 312 

United States, 133, 151, 156, 159, 

160, 161 

University of Amsterdam, 271 

Uraba lugens, 238, 240, 244 

Urban environments, 235, 236 

Urban parks, 235 

Urban programs, 242 

Uric acid, 294 

Urobovella, 274 

Uropoda minima, 267 

Uropodina, 274, 300 

Uropodoidea, 274 

Urtica, 84, 97 

Urticating, 235, 236, 237, 238, 239, 

240, 241 

Uruguay, 106 

US, 48, 133, 134, 135, 140, 143, 148, 

152 

USA, 163, 168, 176, 186, 240, 250, 

267, 278, 283 

Ustilaginomycetes, 285 

Ustilagomycetes, 285, 301 

Uzbekistan, 177, 178, 182, 186, 187

INDEX 

365 

V 

Valencia, 67, 68, 72, 83 

Valine, 194, 206 

Varieties, 73, 87, 91 

Varroa destructor, 253, 254, 302, 

304, 306 

Varroa jacobsoni, 253, 284, 297, 

304 

Varroa mite, 253, 284, 297 

Vasates destructor, 275 

Vasates mckenzie, 276 

Vatacarus ipoides, 256 

Vatacarus, 256, 265 

Vector, 6, 252, 290, 297, 304 

Vegetable gardens, 179 

Vegetables, 104 

Vegetation distribution, 166 

Vegetation, 189, 190 

Vegetative period, 42 

Veigaia, 267 

Veigaiidae, 267 

Veneer, 134 

Veneto, 15 

Venezuela, 82, 268, 269, 300 

Ventral coating, 75 

Ventriculus, 292 

Verbascum thapsus, 198 

Vertebrate host, 250 

Vertebrates, 252, 253, 257, 258, 262, 

289, 300 

Vertical transmission, 255, 291 

Vertically Looking RADAR, 175 

Verticillium lecanii, 298 

Verticillium, 296, 298 

Victoria, 179 

Vigna radiata, 199 

Villages, 165 

Vines, 143 

Vineyards, 179 

Virulence, 251, 279, 284, 290, 297, 298 

Virus inhibitors, 252 

Virus like diseases, 6 

Virus particles, 250, 251 

Virus recognition, 295 

Virus suspensions, 251 

Virus vector, 122 

Virus, 6, 209, 216, 232, 249, 250, 

251, 252, 253, 254, 295, 297, 306 

Virus-infected mites, 253 

VLR, 175 

Volatile chemicals, 189, 191, 203, 

204, 272 

Volatiles, 190–192, 195, 196, 199–202, 

204, 205, 207, 208, 255, 272 

Volicitin, 191, 199, 201, 207 

W 

Wall, 258, 262, 290, 292 

Walnut caterpillar, 134 

Walnut, 76 

Warm periods, 13 

Warm-blooded organisms, 236 

Warning, 30, 33, 37 

Waste products, 294 

Water conservation mechanism, 192 

Water potential, 110, 113 

Watering, 314 

Wavelength, 172 

Webworm larvae, 194 

Weed competition, 144, 146, 147 

Weed control, 136 

Weed science, 133 

Weeding, 73 

Weeds, 69, 89 

Weevil abundance, 107 

Weevil control, 101, 103, 106 

Weevil, 101, 103–105, 109, 110, 125, 

130, 136, 139, 140, 154, 209–212, 

214, 216–219, 221, 222, 224, 225, 

228, 229, 232, 233 

West Africa, 173, 174 

West Nile virus, 252 

Western tent caterpillar, 194 

White oil, 39, 47, 53 

Whiteflies, 13, 14, 29, 30, 40, 41, 68, 74 

Whitetail deer, 151 

Wild plant, 202 

Wildfire, 164, 165, 166 

Wildlife, 146, 147, 151, 152, 156 

Wind speed, 240 

Windbreaks, 314 

Wings, 79, 80, 89

366 

INDEX 

Winter, 32, 51, 237, 241 

Wire screen, 228, 229 

Wolbachia, 256, 258, 259, 260, 296, 

300, 301, 303, 304, 308, 309 

Wolbachieae, 257 

Wood fibers, 217 

Wood, 134, 135, 217, 227, 237, 238, 

240, 242 

Wooden frame, 227, 229 

Woolly whitefly, 29, 30, 40, 41, 42 

World War II, 147 

Wounding, 191 

Wounds, 253 

Wyoming, 163, 171, 185, 186, 187 

X 

Xenillus tegeocranus, 288 

Xenorhabdus, 105, 113, 125, 224 

X-rays, 166 

Xylella fastidiosa, 141 

Xylocorus galactinus, 215, 233 

Y 

Yellow pecan aphid, 138, 139 

Yellow sticky traps, 14 

Yellow water-pan traps, 14 

Yellow-bellied sapsucker, 134 

Yemen, 173 

Yield losses, 31, 40 

Young leaves, 13 

Z 

Z-7-tetradecenal, 48 

Zeta-cypermethrin, 22, 23, 24 

Zonate leaf spot, 142 

Zoophthora radicans, 265 

Zoospore movement, 112 

Zoospores, 104, 112 

Zygomycetes, 261, 300, 302, 303, 

304, 306 

Zygomycota, 260, 261, 296 

Zygospores, 260, 296 

Zygote, 260, 290

[Edited_by_A._Ciancio,_C.N.R.,_Bari,_Italy_and_K.(Bookos.org)

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