Insect Pests of Potato: Global Perspectives on Biology and Management [2 ed.] 0128212373, 9780128212370

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Insect Pests of Potato

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Insect Pests of Potato

Global Perspectives on Biology and Management

SECOND EDITION

Edited by Andrei Alyokhin School of Biology and Ecology, University of Maine, Orono, ME, United States

Silvia I. Rondon Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon Integrated Pest Management Center, Oregon State University, Corvallis, OR, United States

Yulin Gao State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2022 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-821237-0 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Nikki P. Levy Acquisitions Editor: Nancy J. Maragioglio Editorial Project Manager: Veronica III Santos Production Project Manager: Kumar Anbazhagan Cover Designer: Greg Harris

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Contents List of contributors Preface

xiii xv

Part I Potato as an important staple crop 1. Potatoes and their pests: setting the stage Andrei Alyokhin, Silvia I. Rondon and Yulin Gao 1.1 History and present status 1.2 Potatoes and human civilization 1.3 Insect pests 1.4 Meeting the challenge References

3 4 4 4 5

2. Growing potatoes Lakesh K. Sharma, Ahmed Zaeen and Sukhwinder Bali 2.1 2.2 2.3 2.4 2.5 2.6

Introduction Geographic distribution Climate requirements Soil requirements Soil reaction (pH) Major inputs: nitrogen, phosphorus, potassium, sulfur, and organic matter 2.7 Irrigation requirements 2.8 Seed planting depth, spacing, and hilling 2.9 Time to maturity 2.10 Types of cultivars 2.11 Remote sensing References

7 7 7 8 8 8 9 10 10 11 11 12

15 15 17 17 17 18 18 19 19 19 19 20 20 20 20 21 21 21 21 21 22 23 23 24 24 24

Part II Biology of major pests 4. Colorado potato beetle

4.1

Gina A. Greenway and Joseph F. Guenthner Introduction

Economics of seed pricing and production 3.2.1 Pricing 3.2.2 Seed production 3.3 Frozen processed potatoes 3.3.1 Market structure 3.3.2 Frozen processed contract negotiations and complications 3.3.3 Frozen processed contract parameters 3.4 Potato chips 3.5 Fresh potatoes 3.5.1 Market structure 3.5.2 Grading and packing 3.5.3 Bargaining associations in the fresh potato industry 3.6 Storage economics 3.6.1 Fixed costs 3.6.2 Storage variable costs 3.6.3 Understanding shrinkage 3.6.4 Other storage variable costs 3.6.5 Monthly break-even points 3.7 US potato consumption trends 3.8 Potato demand 3.8.1 Population size and distribution 3.8.2 Consumer income 3.8.3 Other goods 3.8.4 Consumer tastes and preferences 3.9 Global trends and future prospects for potato demand in developing countries References

Andrei Alyokhin, Galina Benkovskaya and Maxim Udalov

3. Economic considerations in potato production 3.1

3.2

15

4.2

Taxonomy and morphological description Origins and history of spread

29 31

v

vi

Contents

4.3 4.4 4.5 4.6 4.7

Genetic variability Pest status and yield loss Seasonal life cycle and diapause Interactions with host plants Reproduction and individual development 4.8 Movement and dispersal 4.9 Management implications References

32 33 33 35 35 37 37 38

5. Aphids Andrei Alyokhin, Erik J. Wenninger and Andy Jensen 5.1

Basic biology 5.1.1 Taxonomy 5.1.2 Morphology 5.1.3 Life cycles 5.1.4 Diversity of aphids affecting potato 5.1.5 Population growth and regulation 5.1.6 Movement and dispersal 5.2 Interactions with host plants 5.2.1 Host finding, recognition, and acceptance 5.2.2 Phloem feeding 5.2.3 Overcoming plant defenses 5.2.4 Social facilitation 5.3 Virus transmission 5.4 Management approaches 5.4.1 Monitoring aphid populations 5.4.2 Aphid control versus virus control 5.4.3 Manipulation of crop borders 5.4.4 Mineral oils 5.5 Summary and future directions References

45 45 45 46 49 49 51 51 51 53 53 54 54 56 56 57 59 59 60 60

6. Psyllids Erik J. Wenninger and Arash Rashed 6.1 6.2

6.3

Introduction Potato psyllid (Bactericera cockerelli) 6.2.1 Identification 6.2.2 Geographic distribution 6.2.3 Biology and ecology 6.2.4 Damage 6.2.5 Management Other psyllids 6.3.1 Bactericera nigricornis 6.3.2 Russelliana solanicola 6.3.3 Acizzia spp.

69 69 69 71 71 74 82 87 87 88 89

6.4 Final remarks References

90 90

7. Wireworms as pests of potato Bob Vernon and Wim van Herk 7.1 7.2

Introduction Elaterid biology 7.2.1 Wireworm diversity 7.2.2 Identification 7.3 Species of economic importance in the holarctic 7.3.1 Pacific Northwest, Montana, California 7.3.2 Midwestern USA 7.3.3 Mid-Atlantic, Central Eastern USA 7.3.4 Southeastern USA 7.3.5 Northeastern USA 7.3.6 Canada, Alaska 7.3.7 Russia and Eastern Europe 7.3.8 Western and Central Europe 7.3.9 Asia 7.4 Differences within economic species 7.4.1 Mating, oviposition, and larval development 7.4.2 Larval activity 7.4.3 Preferences in soil type and soil moisture content 7.4.4 Feeding preferences 7.5 Wireworms and the potato crop 7.6 Sampling 7.6.1 Wireworm sampling and risk assessment 7.6.2 Click beetle sampling 7.7 Wireworm control 7.7.1 Cultural methods 7.7.2 Chemical methods 7.7.3 Biological controls 7.7.4 Semiochemical controls 7.8 Conclusions References

103 104 104 106 108 108 108 109 109 110 110 111 111 112 112 112 113 114 114 114 117 117 121 125 126 128 133 135 136 138

8. Potato tuberworm Silvia I. Rondon and Yulin Gao 8.1 8.2

Taxonomy of P. operculella and other “tuberworms” Phthorimaea operculella distribution around the world 8.2.1 America 8.2.2 Asia and Australasia 8.2.3 Europe

149 150 150 150 151

Contents

8.3 8.4

Host range Life cycle 8.4.1 Adults 8.4.2 Eggs 8.4.3 Larvae 8.4.4 Pupae 8.5 Life table 8.6 Damage in the field 8.7 Damage from field to storage 8.8 Developmental thresholds and temperatures 8.9 Monitoring Phthorimaea operculella 8.9.1 Pheromones 8.9.2 Trapping 8.10 Integrated pest management of P. operculella 8.10.1 Cultural control 8.10.2 Biological control 8.10.3 Chemical control 8.10.4 Control in storage 8.10.5 Plant resistance 8.11 Conclusions Acknowledgments References

151 151 151 152 152 152 153 153 154 154 155 155 156 156 156 157 158 159 159 159 160 160

9. Hemipterans, other than aphids and psyllids affecting potatoes worldwide

Introduction Leafhoppers 9.2.1 Empoasca fabae (potato leafhopper) 9.2.2 Empoasca decipiens (green leafhopper) 9.2.3 Circulifer tenellus (beet leafhopper) 9.2.4 Macrosteles quadrilineatus (aster leafhopper) 9.3 Planthoppers 9.3.1 Hyalesthes obsoletus 9.3.2 Reptalus panzeri and R. quinquecostatus 9.4 True bugs 9.4.1 Lygaeidae (seed bugs) 9.4.2 Pentatomidae (stinkbugs) 9.4.3 Miridae (plant bugs) 9.4.4 Lygus hesperus and L. elisus 9.5 Conclusion Acknowledgments References

10. Potato ladybirds Andrei Alyokhin and Yulin Gao 10.1 10.2 10.3

Underappreciated defoliator Morphology Geographic distribution, host range, and taxonomy 10.4 Damage 10.5 Biology 10.5.1 Life cycle 10.5.2 Interactions with host plants 10.5.3 Abiotic effects 10.5.4 Natural enemies 10.6 Management 10.6.1 Chemical control 10.6.2 Biological control 10.6.3 Host plant resistance 10.6.4 Other methods 10.7 Conclusions and future directions References

189 189 191 192 192 192 193 194 194 195 195 195 195 196 196 196

Part III Management approaches 11. Chemical control Thomas P. Kuhar, Christopher Philips, Anna Wallingford, John D. Aigner and Adam Wimer

Tiziana Oppedisano, Govinda Shrestha and Silvia I. Rondon 9.1 9.2

vii

167 167 168

11.1 11.2 11.3

170 171 173 175 176 176 177 177 177 178 178 181 181 181

11.4

Introduction Early history of chemical control in potatoes The pesticide treadmill 11.3.1 Chlorinated hydrocarbons 11.3.2 Organophosphates and carbamates 11.3.3 Pyrethroids 11.3.4 Neonicotinoids A plethora of chemical control options still available in the 21st century 11.4.1 Diamides 11.4.2 Cryolite 11.4.3 Avermectins 11.4.4 Novaluron 11.4.5 Cyromazine 11.4.6 Indoxacarb 11.4.7 Metaflumizone 11.4.8 Tolfenpyrad 11.4.9 Spinosyns

201 201 201 202 202 202 204 206 206 206 206 207 207 207 207 207 207

viii

Contents

11.5

Insecticide options for organic potatoes 11.5.1 Pyrethrins 11.5.2 Azadirachtin 11.5.3 Bacillus thuringiensis subspecies tenebrionis (Bt) 11.6 Chemical control of hemipteran pests 11.6.1 Pymetrozine 11.6.2 Flonicamid 11.6.3 Spirotetramat 11.7 Chemical control of wireworms 11.8 Chemical control of potato tuberworm 11.9 Final thoughts References

13.2

208 208 208 208 209 210 210 210 210 211 212 212

12. Insecticidal RNA interference (RNAi) for control of potato pests Swati Mishra and Juan Luis Jurat-Fuentes 12.1 12.2

Introduction Parameters affecting insecticidal activity of dsRNA 12.3 Delivery of dsRNA to potato pests 12.4 Safety of insecticidal dsRNA 12.5 Use of dsRNA against potato pests 12.5.1 Potato psyllid (Bactericera cockerelli) 12.5.2 The 28-spotted potato ladybird (Henosepilachna vigintioctopunctata) 12.5.3 Colorado potato beetle (Leptinotarsa decemlineata) 12.5.4 Myzus persicae (green peach aphid) 12.5.5 Potato tuber moth (Phthorimaea operculella) 12.6 Resistance to dsRNA and management in potato 12.7 Conclusions and future prospects Acknowledgments References

219 220 221 222 222 222

223 224 224 224 225 225 226 226

13. Biological and behavioral control of potato insect pests

Introduction

231 231

237 244 245 248 250 253 254 254 254 255

255

255

256 256

256 256 257 257 257 258 258 258

14. Potato resistance against insect herbivores

Donald C. Weber, Michael B. Blackburn and Stefan T. Jaronski 13.1

Natural enemies of major potato pests 13.2.1 Colorado potato beetle (Coleoptera: Chrysomelidae) 13.2.2 Potato tuber moths (tuberworms) (Lepidoptera: Gelechiidae) 13.2.3 Hadda beetle and potato lady beetle: Epilachna spp. 13.2.4 Andean potato weevil 13.2.5 Wireworms (Elateridae) 13.2.6 Potato psyllid 13.2.7 Aphids (Hemiptera: Aphididae) 13.3 Biological and behavioral control deployments 13.3.1 Conservation biocontrol 13.3.2 Augmentative and inundative biocontrol 13.3.3 Introduction biocontrol 13.3.4 Biological and behavioral control: interactions with other management methods 13.3.5 Interaction with chemical control (insecticides, fungicides) 13.3.6 Interaction with cultural controls (cultivar, tillage, rotation) 13.3.7 Interaction with crop resistance (cultivar, transgenes) 13.3.8 Interactions between microbial and arthropod biological controls 13.4 Endophytic fungi 13.5 Pheromones for monitoring and population management 13.6 Interactions of biological and behavioral control 13.7 Current and future research needs 13.8 Conclusion Acknowledgments References

Helen H. Tai and Jess Vickruck 231

14.1

Introduction

277

Contents

Natural variation in potato insect resistance 14.2.1 Glycoalkaloids 14.2.2 Trichomes 14.2.3 Other defenses 14.2.4 Potato tolerance to insect pests 14.3 Engineered resistance 14.3.1 Bacillus thuringiensis (Bt) endotoxins 14.3.2 Protease inhibitors 14.3.3 Avidins 14.3.4 Lectins 14.3.5 RNA interference (RNAi) gene silencing in insects 14.3.6 Plant gene silencing 14.4 Constraints on host plant resistance 14.5 Future directions References

278 278 279 280

Part IV Problems and solutions in major potato-producing areas of the world

280 281

16. Latin America potato production: pests and foes

14.2

281 282 284 284 285 286 286 287 287

15. Cultural control and other non-chemical methods _ Beata Gabry
s and Bozena Kordan 15.1 15.2

Introduction Management of abiotic conditions 15.2.1 Site selection, planting and harvest time 15.2.2 Soil tillage 15.2.3 Soil moisture 15.2.4 Mulches 15.2.5 Fertilizers and other soil amendments 15.2.6 Physical control methods 15.3 Management of biotic conditions 15.3.1 Intercropping 15.3.2 Trap crops and barrier crops 15.4 Examples of habitat management 15.4.1 Push-pull and trap crop strategies 15.4.2 Cover-crop residues 15.4.3 Antifeedants 15.5 Concluding remarks References Further readings

297 297 298 299 300 301 303 303 304 305 306 307 307 308 308 309 309 314

ix

Silvia I. Rondon, Carmen Castillo Carrillo, Hugo X. Cuesta, Patricia D. Navarro and Ivette Acun˜a 16.1

History of potato production in Latin America 16.2 Unintentional and intentional breeding efforts 16.3 Potato’s contribution to the national economies 16.4 Potato issues in Latin America 16.5 Integrated pest management approach to control pest problems in potatoes: common issues across diverse regions 16.6 Main pests affecting potato production in Latin America 16.6.1 Order Hemiptera 16.6.2 Order Lepidoptera 16.6.3 Order Diptera 16.6.4 Order Coleoptera 16.6.5 Order Thysanoptera 16.7 Natural enemies References

317 317 318 319

319 319 319 324 325 326 328 328 328

17. The United States of America and Canada Andrei Alyokhin 17.1 17.2

Introduction Potato farming in overall economy 17.3 Local agroclimatic conditions 17.4 Main producers and market conditions 17.5 Main insect pests 17.6 Methods of pest control 17.7 Problems and perspectives References

331 331 332 332 333 335 336 336

x Contents

18. Regional overview of potato pest problem in EU

19.4.5 Methods of pest control 19.4.6 Problems and perspectives 19.5 Summary and conclusions References

Aigi Margus and Leena Lindstro¨m 18.1

Potato has been cultivated in Europe for over 500 years 18.2 Two major pests of potato in Europe 18.3 Potato farming was worth EUR 11 billion in 2017 18.4 Biggest current pest problems 18.5 Means of mitigating pest problems 18.6 Future challenges 18.6.1 International trade 18.6.2 Warming climate 18.6.3 Agricultural policies and consumer choices References

339 339 340 341 344 344 345 345 345 346

19. Russian Federation, Belarus, and Ukraine Andrei Alyokhin, Galina Benkovskaya, Galina Sukhoruchenko, Sergei Volgarev and Ildar Mardanshin 19.1 19.2

19.3

19.4

History and local characteristics of potato production Russian Federation 19.2.1 Potato farming in overall economy 19.2.2 Local agroclimatic conditions 19.2.3 Main producers and market conditions 19.2.4 Main insect pests 19.2.5 Methods of pest control 19.2.6 Problems and perspectives Republic of Belarus 19.3.1 Potato farming in overall economy 19.3.2 Local agroclimatic conditions 19.3.3 Major potato producers 19.3.4 Main insect pests 19.3.5 Methods of pest control 19.3.6 Problems and perspectives Ukraine 19.4.1 Potato farming in overall economy 19.4.2 Local agroclimatic conditions 19.4.3 Major potato producers 19.4.4 Main insect pests

349 350 350 350 350 351 352 352 352

20. China and Central Asia Wenwu Zhou, Asim Munawar, Runzhi Zhang and Yulin Gao 20.1

Potato production in China and Central Asia 20.1.1 China 20.1.2 Central Asia 20.2 Abundance, the relative importance of potato pests in China and Central Asia 20.2.1 China 20.2.2 Central Asia 20.3 Management practices of key potato pests in China and Central Asia 20.3.1 China 20.3.2 Central Asia 20.4 Conclusions References

361 361 362

362 362 363 364 364 366 368 368

21. Insect pests of potato in India: biology and management R.S. Chandel, V.K. Chandla, K.S. Verma and Mandeep Pathania 21.1 21.2

352 353 353 353 354 354 354 354 355 355 355

355 356 356 356

21.3

Introduction Root and tuber-eating pests 21.2.1 White grubs 21.2.2 Cutworms 21.2.3 Surface cutworm, Agrotis spinifera 21.2.4 Greasy cutworm, Agrotis ipsilon 21.2.5 Common cutworm, Agrotis segetum 21.2.6 Gram cutworm, Agrotis flammatra 21.2.7 Wireworms 21.2.8 Termites and ants 21.2.9 Potato tuber moth 21.2.10. Mole cricket, Gryllotalpa africana Palisot 21.2.11. Minor pests Sap-feeding pests 21.3.1 Aphids

371 372 372 377 378 378 378 379 379 381 382 384 384 384 384

Contents

21.3.2 Leafhoppers 21.3.3 Thrips 21.3.4 White flies 21.3.5 Sap-sucking bugs 21.4 Leaf-eating and defoliating insects 21.4.1 Defoliating caterpillars 21.4.2 Oriental armyworm, Mythimna separata (Walker) 21.4.3 Bihar hairy caterpillar, Spilosoma obliqua (Walker) 21.4.4 Hairy caterpillar, Dasychira mendosa (Hubner) 21.4.5 Tobacco cutworm, Spodoptera litura (Fab.) 21.4.6 Gram pod borer, Heliothis armigera (Hubner) 21.4.7 Eggplant borer, Leucinodes orbonalis Guenee 21.4.8 Leaf-eating beetles 21.4.9 Flea beetles, Psyllodes plana Maulik 21.4.10 Blister beetle, Epicauta hirticornis Hagg 21.4.11 Gray weevil, Myllocerus subfasciatus Guerin References

386 388 389 391 391 391

392 392 393 393 394 395 395 396 397 397 398

22. Australia and New Zealand Paul Horne and Jessica Page 22.1 Overview of the industry 22.2 Main pests 22.3 Control methods Acknowledgments References

401 401 403 405 405

23. Management of potato pests and diseases in Africa Joseph E. Munyaneza and Benoit Bizimungu 23.1 23.2

23.3

Overview Potato pests and diseases 23.2.1 Insect pests 23.2.2 Plant parasitic nematodes 23.2.3 Potato diseases Pest and disease management practices 23.3.1 Chemical control 23.3.2 Biological control

407 409 409 411 412 415 416 416

23.3.3 Cultural control 23.3.4 Plant host resistance 23.4 Conclusion References

xi

416 416 421 421

Part V Basic science in potato pest management 24. Evolutionary considerations in potato pest management Andrei Alyokhin, Yolanda H. Chen, Maxim Udalov, Galina Benkovskaya and Leena Lindstro¨m 24.1 24.2 24.3 24.4 24.5

Introduction Fundamentals of evolution Applied evolution Evolution in agricultural ecosystems Evolutionary process of becoming a pest 24.6 An obscure leaf beetle turns into a major pest of potatoes 24.7 Insecticide resistance 24.7.1 Insecticide treadmill 24.7.2 Colorado potato beetle as a resistant superbug 24.7.3 Green peach aphid e resistance in a mostly parthenogenic organism 24.7.4 Resistance to nonchemical control methods 24.7.5 Resistance management 24.7.6 Epigenetic considerations 24.8 Interactions with abiotic environment 24.9 Human turn to adapt? 24.10 Conclusions References

429 429 430 431 432 432 434 434 434

438 439 440 441 441 443 443 443

25. Ecology of a potato field Andrei Alyokhin and Vadim Kryukov 25.1 “Potatoes partly made of oil” 25.2 An underappreciated challenge 25.3 Healthy soils and healthy plants 25.4 Dawn of the killer fungi 25.5 The power of connections Acknowledgments References

451 452 453 455 458 459 459

xii Contents

Part VI Current challenges and future directions

26. Ecological and evolutionary factors mitigating Colorado potato beetle adaptation to insecticides Michael S. Crossley, Zachary Cohen, Benjamin Pe´lissie´, Silvia I. Rondon, Andrei Alyokhin, Yolanda H. Chen, David J. Hawthorne and Sean D. Schoville 26.1 26.2 26.3

Introduction Genetic variation Pesticide use 26.3.1 Insecticides 26.3.2 Fungicides 26.4 Noncrop host plants 26.5 Natural enemies 26.6 Crop rotation 26.7 Climate suitability 26.7.1 Temperature 26.7.2 Water availability 26.7.3 Fitness trade-offs 26.8 Future research 26.8.1 Examining parallel patterns of evolution of insecticide resistance in Europe 26.8.2 Regulation of gene expression 26.8.3 Legacies of historic insecticide exposure 26.8.4 Prolonged dormancy 26.8.5 Linking noncrop host plant utilization with insecticide susceptibility 26.8.6 Interactions with regional potato cultivars 26.8.7 Importance of natural enemies 26.8.8 Climate suitability 26.9 Conclusion Acknowledgments References

27. Integrated Pest Management (IPM) in potatoes Paul Horne and Jessica Page 463 466 467 467 468 468 468 469 470 471 471 472 472

472 473 473 473

27.1 27.2

What is IPM? The elements of IPM 27.2.1 Biological control agents 27.2.2 Cultural controls 27.2.3 Pesticides 27.3 An IPM strategy for potatoes typical in Australia 27.4 Taught everywhere but typically slow and low rates of adoption. Why? 27.5 Changing to IPM when a crisis occurs or avoiding a crisis. Examples beyond potatoes 27.6 How to achieve rapid adoption of IPM in the absence of a crisis 27.7 Conclusion Acknowledgments References

484 485 485 486

486

486 487 489 489 489

28. Epilogue: the road to sustainability

473

Andrei Alyokhin, Silvia I. Rondon and Yulin Gao

473

References

474 474 474 475 475

483 483

Index

492

493

List of contributors Ivette Acuña, Institute of Agricultural Research, Chile John D. Aigner, Department of Entomology, Virginia Tech, Blacksburg, VA, United States Andrei Alyokhin, School of Biology and Ecology, University of Maine, Orono, ME, United States; University of Maine, School of Biology and Ecology, Orono, ME, United States Sukhwinder Bali, Department of Agronomy, University of Florida, Gainesville, FL, United States Galina Benkovskaya, Institute of Biochemistry and Genetics, Russian Academy of Science, Ufa, Russia Benoit Bizimungu, Agriculture and Agri-Food Canada, Fredericton Research and Development Centre, Fredericton, NB, Canada Michael B. Blackburn, Invasive Insect Biocontrol and Behavior Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States Carmen Castillo Carrillo, Institute of Agricultural Research, Ecuador R.S. Chandel, Department of Entomology, Himachal Pradesh Agriculture University, Palampur, Himachal Pradesh, India V.K. Chandla, Division of Plant Protection, Central Potato Research Institute, Shimla, Himachal Pradesh, India Yolanda H. Chen, University of Vermont, Department of Plant and Soil Sciences, Burlington, VT, United States Zachary Cohen, University of Wisconsin, Department of Entomology, Madison, WI, United States Michael S. Crossley, University of Georgia, Department of Entomology, Athens, GA, United States Hugo X. Cuesta, Institute of Agricultural Research, Ecuador Beata Gabry
s, Department of Botany and Ecology, University of Zielona Góra, Zielona Góra, Poland

Yulin Gao, State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, China; National Center of Excellence for Tuber and Root Crops Research, Chinese Academy of Agricultural Science, Beijing, China Gina A. Greenway, Greenway Research and Consulting, Parma, ID, United States Joseph F. Guenthner, Department of Agricultural Economics and Rural Sociology, University of Idaho, Moscow, ID, United States David J. Hawthorne, University of Maryland, Department of Entomology, College Park, MD, United States Paul Horne, IPM Technologies Pty Ltd, Hurstbridge, VIC, Australia Stefan T. Jaronski, Jaronski Mycological Consulting LLC, Virginia Polytechnic Institute and State University, Department of Entomology, Blacksburg, VA, United States Andy Jensen, Washington State Potato Commission, Moses Lake, WA, United States Juan Luis Jurat-Fuentes, Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, United States Bo_zena Kordan, Department of Entomology, Phytopathology and Molecular Diagnostics, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland Vadim Kryukov, Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia Thomas P. Kuhar, Department of Entomology, Virginia Tech, Blacksburg, VA, United States Leena Lindström, Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

xiii

xiv

List of contributors

Ildar Mardanshin, Bashkortostan Agricultural Scientific Research Institute, Russian Academy of Science, Ufa, Russia

Helen H. Tai, Agriculture and Agri-Food Canada, Fredericton Research and Development Center, Fredericton, NB, Canada

Aigi Margus, Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

Maxim Udalov, Independent Consultant, Ufa, Russia

Swati Mishra, Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, United States Asim Munawar, Institute of Insect Sciences, Zhejiang University, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Hangzhou, China Joseph E. Munyaneza, United States Department of Agriculture, Agricultural Research Service, Office of National Programs, Crop Production and Protection, Beltsville, MD, United States Patricia D. Navarro, Institute of Agricultural Research, Chile Tiziana Oppedisano, Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon State University, Hermiston, OR, United States Jessica Page, IPM Technologies Pty Ltd, Hurstbridge, VIC, Australia Mandeep Pathania, Department of Entomology, Himachal Pradesh Agriculture University, Palampur, Himachal Pradesh, India Christopher Philips, Department of Entomology, Virginia Tech, Blacksburg, VA, United States Benjamin Pélissié, University of Nebraska-Kearney, Biology Department, Kearney, NE, United States Arash Rashed, Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Moscow, ID, United States Silvia I. Rondon, Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon Integrated Pest Management Center, Oregon State University, Corvallis, OR, United States Sean D. Schoville, University of Wisconsin, Department of Entomology, Madison, WI, United States Lakesh K. Sharma, Soil and Water Sciences Department, University of Florida, Gainesville, FL, United States Govinda Shrestha, Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon State University, Hermiston, OR, United States Galina Sukhoruchenko, All-Russian Plant Protection Institute, Saint Petersburg, Russia

Wim van Herk, Agassiz Research and Development Centre, Agriculture and Agri-Food Canada, Agassiz, British Columbia, Canada K.S. Verma, Department of Entomology, Himachal Pradesh Agriculture University, Palampur, Himachal Pradesh, India Bob Vernon, Sentinel IPM Services, Chilliwack, British Columbia, Canada Jess Vickruck, Agriculture and Agri-Food Canada, Fredericton Research and Development Center, Fredericton, NB, Canada Sergei Volgarev, All-Russian Plant Protection Institute, Saint Petersburg, Russia Anna Wallingford, Department of Entomology, Virginia Tech, Blacksburg, VA, United States Donald C. Weber, Invasive Insect Biocontrol and Behavior Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States Erik J. Wenninger, Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Kimberly Research & Extension Center, Kimberly, ID, United States Adam Wimer, Department of Entomology, Virginia Tech, Blacksburg, VA, United States Ahmed Zaeen, Department of Ecology and Environmental Sciences, University of Maine, Orono, ME, United States Runzhi Zhang, Institute of Zoology, Chinese Academy of Sciences, Beijing, China Wenwu Zhou, Institute of Insect Sciences, Zhejiang University, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Hangzhou, China

Preface The potato, Solanum tuberosum L., has been cultivated by humans for over 8000 years. During that period, potatoes spread all over the world from their center of origin in the Central Andes region of South America and became an important staple food in the diets of billions of people after the Spaniards introduced potatoes to the rest of the world. Nutritionally superior to most other staple crops, rugged, and relatively easy to grow, potato has been instrumental in improving the quality of life in a variety of geographic areas throughout human history. Currently, potatoes are firmly embedded in the top five most common world crops and remain of great importance in both industrialized and developing parts of the world. Insect pests have been taking a heavy toll on potato farming throughout its history. In the absence of adequate control, they can severely reduce potato yields, sometimes all the way to the zero harvestable tubers. As a result, insect management receives considerable attention from the scientific community, which is well reflected in the number of scientific publications on this subject. Since 1981, summaries of this research have been published in the book form, on average, every 15 years. With this volume, we are hoping to continue this tradition. “Advances in Potato Pest Management” edited by Lashomb and Casagrande was published by the Hutchinson Ross Publishing Co. in 1981. That was followed by “Advances in Potato Pest Biology and Management” edited by Zehnder, Jansson, Powelson, and Raman and published by the APS Press in 1994. The First Edition of “Insect Pests of Potatoes: Biology and Management” edited by Giordanengo, Vincent, and Alyokhin was released by Academic Press/Elsevier in 2013. Considerable amount of new information became available since that time, while reader feedback revealed additional topics in need of coverage. This book attempts to address these current issues. Similar to the First Edition, this book is made of contributions written by an international team of experts working in major potato-growing areas of the world. Some of the authors are the same as for the First Edition, updating their chapters with the new information that has become available over the last 9 years. Other authors (and two of the editors) are new, bringing indispensable fresh blood to the project. As with the First Edition, we made a strong effort to include valuable, but often little known, information published in non-English language literature, including materials written in Spanish, Chinese, and Russian. In Part I, we start with introducing potato as a crop that is essential for meeting nutritional demands of the humankind and discuss agronomic and economic issues of its sustainable production. After that, we proceed to covering biology of the major potato pests in Part II of our book. Part III is dedicated to practical approaches to protecting potatoes from insect damage. Emphasis is placed on techniques allowing pest suppression in an environmentally friendly manner. Part IV is new to the Second Edition and reviews potato production and pest management in the main potato-growing areas of the world. This includes information on the insect species of local importance. Part V is also new, although it draws on some of the information from the previous edition. It discusses applications of basic ecological and evolutionary principles in developing scientifically sound foundation for pest management and provides relevant examples. Part VI concludes the book with the discussion of current challenges and future prospects in developing integrated pest management plans for potato farms. We are deeply grateful to Nancy Marogioglio, Veronica Santos, Narmatha Mohan, and Cole Newman from Elsevier for their help and guidance throughout the editorial process. We also thank Natalie “Natasha” Alyokhin for assisting with initial processing and formatting of the manuscript. Aaron Buzza kept research program at the Alyokhin laboratory from falling apart while its head was busy with the book.

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It is our hope that this book will be of use and interest to a variety of people involved in potato production. We also always welcome our readers’ feedback, including (but not limited to) constructive criticism. We dedicate this book to all past and current contributors that provide the information you are about to read. Sincerely, Andrei Alyokhin Silvia Rondon Yulin Gao

Part I

Potato as an important staple crop

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Chapter 1

Potatoes and their pests: setting the stage Andrei Alyokhina, Silvia I. Rondonb and Yulin Gaoc, d a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bDepartment of Crop and Soil Science, Hermiston Agricultural

Research and Extension Center, Oregon Integrated Pest Management Center, Oregon State University, Corvallis, OR, United States; cState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, China; d

National Center of Excellence for Tuber and Root Crops Research, Chinese Academy of Agricultural Science, Beijing, China

1.1 History and present status The cultivated potato, Solanum tuberosum L. (Solanaceae), is a currently ubiquitous and valuable tuber crop that is grown and consumed all over the world. This crop has a long history, although it did not reach its present-day prominence until 19th century. Potato was first domesticated about 8000 years ago in the Central Andes region near Lake Titicaca that is currently split between Peru and Bolivia. This area still remains an important source of biological diversity for potato crops, preserving a large proportion of their currently existing 4000 edible varieties (Zuckerman, 1999; Reader, 2009; de Haan et al., 2019). However, by volume most potatoes are currently produced in other areas, where they were introduced only several hundred years ago. Potatoes first left South America in the 16th century when conquistadors introduced them to Spain around 1570. From there, potatoes spread to Italy in 1586, to Austria in 1588, to England in 1596, and to Germany in 1601. They arrived in North America in the 1620s, when the British governor of the Bahamas presented several tubers to the governor of the colony of Virginia (Brown, 1993; Zuckerman, 1999). In China, potatoes were introduced in mid-17th century to Beijing, from where they spread throughout the country over the next 100 years (Zhai, 2001). In Russia, potatoes first appeared in the late 17th century; however, they did not enter the mainstream agriculture for another 100 years (Anonymous, 2019). Initially, newly introduced potatoes were treated as a botanical curiosity and had few uses limited to consumption by the upper classes of society. Potato flowers were used for decorations while tubers were treated as an exotic novelty food. Acceptance of this crop by the broader public was slow. In addition to general neophobia commonly surrounding the introduction of new foods, potato fruit and foliage have high content of glycoalcoloids and are unsuitable for human consumption. Occasional poisonings due to eating of aboveground parts by uneducated peasants reinforced their resistance to growing an unfamiliar crop. In Europe and Russia, the value of growing potatoes was first recognized mostly by the scientific community rather than by farmers and peasants, and then heavily promoted through government programs. Those eventually succeeded, with potatoes becoming an essential staple food (Zuckerman, 1999; Reader, 2009; Anonymous, 2019). Recently, Chinese government also undertook a serious effort to promote potato farming to improve overall food security in the country, which resulted in dramatic increase in production and consumption of this vegetable (Su and Wang, 2019). In 2019, the last year for which the data are currently available, the Food and Agriculture Organization of the United Nations (FAOSTAT, 2021) reported potato production for 156 countries that span pretty much the entire globe. The total output was 370,497,921 tons of harvested tubers. Ten largest producers were China, India, Russian Federation, Ukraine, United States of America, Germany, Bangladesh, France, Netherlands, and Poland. Overall, potato is the world’s most popular vegetable (Jansky et al., 2019) and is one of the five most important staple crops (Scott and Suarez, 2012; Devaux et al., 2014).

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1.2 Potatoes and human civilization Of all major staple crops, potato is the best in terms of human nutrition (Kolasa, 1993; Woolfe, 1987). Although it is usually eaten as a source of carbohydrates, potato also provides dietary fiber, vitamins C and B6, carotenoids, phenolic acids, potassium, magnesium, and iron (Beals, 2019; Navarre et al., 2019). In addition, several compounds naturally occurring in potato tubers contribute to maintaining gut health, including suppressing inflammatory bowel disease (Bibi et al., 2019; Reddivari et al., 2019) and colon cancer (Charepalli et al., 2015; Vanamala, 2019). Even potato glycoalcoloids, which are toxic when ingested in large amounts, may have anticarcinogenic properties at low concentrations (Yang et al., 2006; Wijesinha-Bettoni and Mouille, 2019; Jansky et al., 2019). Eating potatoes is especially appropriate for people engaging in high-intensity physical activities (Kanter and Elkin, 2019). Together with superb nutritional qualities, high caloric yields per unit of area characteristic of potato crops had a profound effect on human populations that adopted it. More abundant and better-balanced diets improved human health and likely promoted rapid population growth in a variety of nations (Zuckerman, 1999; Reader, 2009; de Jong, 2016). It is relatively well known that potato farming was an important contributing factor to the rise of the Inca Empire, a great Mesoamerican civilization that once extended from present day Columbia to Argentina (McEwan, 2006; de Jong, 2016). It is less appreciated that potatoes were also essential for accelerating economic development in Europe and North America during the Industrial Revolution by providing inexpensive and nutritious meals to factory workers flocking to the rapidly growing cities and to landless agricultural laborers on increasingly industrialized agricultural enterprises (Kolasa, 1993; Zuckerman, 1999). Presently, potato farming continues being an important source of food security in the developing world (Gatto et al., 2020), with potato production quadrupling in some areas over the last quarter-century (de Jong, 2016). In addition to providing nutrients that are absent in other staple crops, potatoes allow crop diversification that hedges against possible catastrophic losses due to pest outbreaks or unfavorable weather.

1.3 Insect pests Not surprisingly, humans are not the only species that thrive on potatoes. There is a wide array of insect species that also feed on this plant, thus competing with humans for the same valuable resource. In some cases, their impact is severe enough to result in complete crop failure. Damage occurs directly through feeding on tubers or indirectly through feeding on leaves and stems or transmitting pathogens. Necessity to control insect pests has been an important feature of potato farming for a long time. It has been argued that the need to protect potato plants from insect damage largely shaped the early development of the modern pesticide industry (Gauthier et al., 1981). While it is common to attribute the outmost significance to one’s field of study, there is considerable historical evidence supporting this claim. Search for insecticides capable of controlling Colorado potato beetles started in 1864 (Gauthier et al., 1981), and included such important developments as discovery of Paris green (copper[II]acetoarsenite), lead arsenate, DDT, cyclodiene organochlorines, organophosphates, carbamates, and neonicotinoids (Alyokhin, 2009). Application equipment evolved along with the chemical industry. Early advances included mechanical devices such as perforated tin cans, powder guns with hand-cranked gear drives, and wheel-drawn pressurized pump sprayers (Sanderson, 1912; Gauthier et al., 1981), followed by devices powered by fossil fuels. The first successful sprayer based on a steam engine appeared in 1894, quickly followed by a gasoline-powered sprayer in 1900 (Gauthier et al., 1981). While chemical control remains a predominant and successful method in managing potato pests, its shortcomings have become increasingly obvious since mid-20th century. Toxicity to non-target organisms (including humans), heavy reliance on non-renewable resources during manufacturing and application, and repeated failures due to the selection of resistant insect pest populations have led to a considerable demand for non-chemical alternatives. Substantial advances have been made in meeting this demand; however, the chemically centered crop protection paradigm still remains firmly in place.

1.4 Meeting the challenge Potato farming is likely to be an important economical activity for a long time into the future, and it is largely impossible without effective management of insect pests. Routine chemical control along the lines of “we spray e they die; and if they do not die, we spray them with something else” is increasingly unlikely to be sufficient for ensuring lasting crop protection. This is especially true in the time of rapid global change, which includes new weather patterns and rapid establishment of non-native species.

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Timely development of viable alternatives requires understanding of the biology of target pests and the ecology of their interactions. Considerable efforts are currently invested into meeting this goal in potato production. A quick search of scientific literature published since 2013 (the year when the First Edition of this book came out) using “potato insect pest” keywords in Google Scholar produced ca. 19,600 results. Systematizing and presenting this vast body of knowledge was the main goal of our book. We hope that our endeavor will facilitate sustainable management of this amazing crop.

References Alyokhin, A., 2009. Colorado potato beetle management on potatoes: current challenges and future prospects. Fruit, Veg. Cereal Sci. Biotechnol. 3, 10e19. Anonymous, 2019. History of Potato in Russia (in Russian). https://vitusltd.ru/kartofel_rossija.html. (Accessed 11 April 2021). Beals, K.A., 2019. Potatoes, nutrition and health. Am. J. Potato Res. 96, 102e110. Bibi, S., Navarre, D.A., Sun, X., Du, M., Rasco, B., Zhu, M.J., 2019. Beneficial effect of potato consumption on gut microbiota and intestinal epithelial health. Am. J. Potato Res. 96, 170e176. Brown, C.R., 1993. Origin and history of the potato. Am. Potato J. 70, 363e373. Charepalli, V., Reddivari, L., Radhakrishnan, S., Vadde, R., Agarwal, R., Vanamala, J.K., 2015. Anthocyanin-containing purple-fleshed potatoes suppress colon tumorigenesis via elimination of colon cancer stem cells. J. Nutr. Biochem. 26, 1641e1649. de Haan, S., Burgos, G., Liria, R., Rodriguez, F., Creed-Kanashiro, H.M., Bonierbale, M., 2019. The nutritional contribution of potato varietal diversity in Andean food systems: a case study. Am. J. Potato Res. 96, 151e163. De Jong, H., 2016. Impact of the potato on society. Am. J. Potato Res. 93, 415e429. Devaux, A., Kromann, P., Ortiz, O., 2014. Potatoes for sustainable global food security. Potato Res. 57, 185e199. FAOSTAT, 2021. FAO Statistical Databases. http://faostat.fao.org/. (Accessed 8 August 2021). Gatto, M., Petsakos, A., Hareau, G., 2020. Sustainable intensification of rice-based systems with potato in Eastern Indo-Gangetic plains. Am. J. Potato Res. 97, 162e174. Gauthier, N.L., Hofmaster, R.N., Semel, M., 1981. History of Colorado potato beetle control. In: Lashomb, J.H., Casagrande, R. (Eds.), Advances in Potato Pest Management. Hutchinson Ross Publishing Co., Stroudsburg, PA, USA, pp. 13e33. Jansky, S., Navarre, R., Bamberg, K., 2019. Introduction to the special issue on the nutritional value of potato. Am. J. Potato Res. 96, 95e97. Kanter, M., Elkin, C., 2019. Potato as a source of nutrition for physical performance. Am. J. Potato Res. 96, 201e205. Kolasa, K.M., 1993. The potato and human nutrition. Am. Potato J. 70, 375e384. McEwan, G.F., 2006. The Incas, New Perspectives. ABC-CLIO, Inc., Santa Barbara, CA, USA, p. 269. Navarre, D.A., Brown, C.R., Sathuvalli, V.R., 2019. Potato vitamins, minerals and phytonutrients from a plant biology perspective. Am. J. Potato Res. 96, 111e126. Reader, J., 2009. Potato: A History of the Propitious Esculent. Yale University Press, New Haven and London, p. 336. Reddivari, L., Wang, T., Wu, B., Li, S., 2019. Potato: an anti-inflammatory food. Am. J. Potato Res. 96, 164e169. Sanderson, E.D., 1912. Insect Pests of Farm, Garden, and Orchard. Wiley, New York, USA. Scott, G.J., Suarez, V., 2012. The rise of Asia as the centre of global potato production and some implications for industry. Potato J. 39, 1e22. Su, W., Wang, J., 2019. Potato and food security in China. Am. J. Potato Res. 96, 100e101. Vanamala, J.K., 2019. Potatoes for targeting colon cancer stem cells. Am. J. Potato Res. 96, 177e182. Wijesinha-Bettoni, R., Mouillé, B., 2019. The contribution of potatoes to global food security, nutrition and healthy diets. Am. J. Potato Res. 96, 139e149. Woolfe, J.A., 1987. The Potato in the Human Diet. Cambridge University Press, Cambridge, UK., p. 231 Yang, S.A., Paek, S.H., Kozukue, N., Lee, K.R., Kim, J.A., 2006. a-Chaconine, a potato glycoalkaloid, induces apoptosis of HT-29 human colon cancer cells through caspase-3 activation and inhibition of ERK 1/2 phosphorylation. Food Chem. Toxicol. 44, 839e846. Zhai, Q.X., 2001. Preliminary exploration of the introduction time of potato in China. Agric. Hist. China 20, 91e92 (in Chinese). Zuckerman, L., 1999. The Potato: How the Humble Spud Rescued the Western World. North Point Press, New York, NY, USA, p. 301.

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Chapter 2

Growing potatoes Lakesh K. Sharmaa, Ahmed Zaeenb and Sukhwinder Balic a

Soil and Water Sciences Department, University of Florida, Gainesville, FL, United States; bDepartment of Ecology and Environmental Sciences,

University of Maine, Orono, ME, United States; cDepartment of Agronomy, University of Florida, Gainesville, FL, United States

2.1 Introduction Potato (Solanum tuberosum L.) originates in the Andes Mountains, and there are hundreds of related wild species in South and Central America. Potatoes are sometimes called Irish potatoes to separate them from sweet potatoes (Nair et al., 2017). The Irish people were heavily dependent on potato for nutrition, and in 1719 Irish immigrants brought the crop from Europe to the eastern United States. The edible part of the plant is the tuber, which is an underground modification of the stem. Potatoes are produced for fresh markets and are processed into a variety of food items, including chips and French fries. Potato crop has high economic importance worldwide (FAOSTAT, 2015). Potato is the fourth most crucial crop after rice (Oryza sativa L.), wheat (Triticum aestivum L.), and maize (Zea mays L.) (FAOSTAT, 2015). These four crops currently contribute extensively to human food security throughout the world (FAOSTAT, 2015), as also discussed in Chapters 1 and 3. Potato cultivation systems face several challenges, including maintaining soil fertility, combatting plant diseases, and controlling insect pests. The effective management of nitrogen (N) fertilizers is the first challenge in potato production (Fageria and Baligar, 2005). A high N rate has a positive impact on vegetative growth, which in turn increases tuber yield (Oliveira and Alberto, 2000). On the opposite, N stress may restrict photosynthesis and negatively affects the partitioning of photosynthesis from leaves to tubers (Jin et al., 2015). Low N rates not only produce a lower yield but also decrease tuber size because of reduced leaf area and early defoliation. On the other hand, excess N promotes the growth of plant parts other than tubers (Goffart et al., 2008; Fontes et al., 2010). The goal of this chapter is to focus on the most important potato production requirements and review some techniques that can help improve yield and quality while reducing environmental contamination.

2.2 Geographic distribution Potato originates from Central and South America but is presently extensively naturalized beyond its native area in extratropical regions (Holm et al., 1979; Randall, 2012). Potato is comprised of thousands of cultivars that differ, among other characteristics, by color, size, shape, and other sensory properties of their tubers. The cultivated potato started in the PeruColombia-Chile area of the South American Andes, but has a wide-ranging center of diversity from Colombia, Venezuela, Ecuador, Bolivia, Peru, Argentina, and Chile across the Pampa and Chaco areas of Uruguay, Argentina, Paraguay, and northward into Central America, Brazil, Mexico, and the southwestern United States (Kiple and Ornelas, 2000; Wagner et al., 2014).

2.3 Climate requirements Potato is a crop principally of temperate climate, where the plants flourish best in cool conditions with long frost-free periods. Potato plants do not perform well in hot regions (Bodlaender, 1963; Hijmans, 2003). The optimal and threshold values for the growth of the aboveground portion of the potato plant (leaves and stems) and the tubers are cultivar dependent characteristics (Rykaczewska, 1993; Van Dam et al., 1996). Based on the research carried out in growth Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00025-1 Copyright © 2022 Elsevier Inc. All rights reserved.

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chambers, haulm growth is optimized in the temperature range of 20e25
C, whereas the optimum range for tuber initiation and tuber growth is between 15 and 20
C. Under high-temperature conditions, plant growth and tuber initiation are significantly inhibited, and photoassimilate partitioning to tubers is considerably decreased (Haynes et al., 1989; Lafta and Lorenzen, 1995). Heat stress due to raised temperature is a problem in several regions worldwide (Birch et al., 2012). Transitory or constant high temperatures induce a series of morphoanatomical, physiological and, biochemical modifications in plant systems, which influence plant growth and evolution. They may lead to an extreme economic reduction in yield (Wahid et al., 2007). The undesirable impacts of heat stress can be mitigated by developing potato plants with improved thermotolerance using several crossbreeding genetic strategies (Levy et al., 1991; Veilleux et al., 1997). Thus, accurate knowledge of the physiological responses of plants to high temperatures is necessary. Currently, there is not much data on the possible differences in responses to heat and drought stresses among different stages of potato development (De Temmerman et al., 2002; Levy and Veilleux, 2007). Although drought and heat stress are two separate classes of abiotic stresses, they often happen concurrently under natural conditions. However, due to the increasing use of irrigation on potato farms and periodic observations of heat stress despite good soil moisture, the influence of high temperature on potato plants is often separated from the influence of drought (Rykaczewska, 2004).

2.4 Soil requirements Potatoes grow properly in un-compactable soils, such as loams, sandy loams, sandy clay loams, and silt loams. These kinds of soils have a well-balanced capacity to hold water, form a stable structure, provide sufficient aeration, and possess the ability to maintain a moderate soil temperature. However, the more sandy or gravely soils have an increased chance of aridity, lowered nutrient holding capacities, and a higher potential for nutrient loss, including leaching to groundwater. On the other hand, clay soils tend to be easily compacted and create a crust. Therefore, they are more problematic regarding both drainage resistance and water erosion (Anonymous, 2019). Potatoes planted in loamy sand soils have significantly higher N uptake than those grown in sandy loam and coarse sand. In contrast, N uptake in plants planted in sandy loam soils did not significantly differ from the uptake of potatoes grown in coarse sand (Ahmadi et al., 2011). The soil-root contact area is an important factor in water and nutrient uptake, particularly in coarse-textured soils (Jensen et al. (1993). Potatoes grown in loamy sand soils had significantly higher root density (about two-fold increase) in the deep soil layers compared to the plants grown in other soils (Ahmadi et al., 2008). Therefore, the improved N uptake by the plant’s root in loamy sand soils can primarily be attributed to an increased soil volume searched by roots and to a larger uptake area. Under non-limiting water availability, loamy sand is the most proper soil for growing potatoes because N uptake is high, resulting in yield increases. When water is more limiting, sandy loams, loams, and clay loams are more productive.

2.5 Soil reaction (pH) Soil reaction (pH) is an important factor in any fertilizer application. For potatoes, it is also a consideration in controlling common scab, Streptomyces scabies. Raising pH close to 6.0 improves the availability of plant nutrients and decreases the activity of toxic elements, thereby optimizing growing conditions as far as nutrients are concerned. In the regions where common scab is not a major problem, the pH level should be as high as possible (up to 6.0). However, soil pH should range between 5.0 and 5.2 when common scab is an issue. In regions with high soil pH levels, scab resistant cultivars should be grown. Liming is a usual process to raise soil pH, where soil pH testing is required to calculate the lime amount that must be added. The fall season is the best time to do liming, but it can also be performed in the spring before planting time (Johnson, 2009).

2.6 Major inputs: nitrogen, phosphorus, potassium, sulfur, and organic matter Nitrogen (N) is an essential component of the chlorophyll molecule besides its function in the synthesis of proteins (Tisdale and Nelson, 1975). N makes up to 10e40 g kg1 of the plant’s dry weight; it is taken up from the soil in the form of nitrate (NO-3) or ammonium (NHþ 4 ) and combines with components of carbohydrate metabolism in the plant to produce aminoacids and proteins (FAO 1978). Proper N fertilization is significant for optimizing potato yield and quality, with a considerable impact on all growth parameters (Jatav et al., 2017; Kołodziejczyk, 2014). Inadequate available N leads to diminished growth and light interception (Millard and Marshall, 1986), early crop senescence (Kleinkopf et al., 1981), and

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decreased yields (Westermann and Kleinkopf, 1985). However, excessive available N can postpone tuber formation (Kleinkopf et al., 1981), decrease yields (Lauer, 1986), and reduce tuber dry matter content (Millard and Marshall, 1986). Furthermore, excessive N increases the potential for environmental contamination due to nitrate leaching or runoff (Westermann et al., 1988). After N, phosphorus (P) is the second most limiting mineral nutrient for potato crop production. The shortage of P in mesophyll cells impacts photosynthesis function through the availability of inorganic P in the chloroplast, ultimately causing reduced carbon assimilation (Hermans et al., 2006). However, sucrose translocation into the phloem is sometimes maintained or even increased throughout the early periods of P starvation (Hermans et al., 2006). Inorganic P is positively correlated with the less sugar concentration in the stem tissue (Nitsos and Evans, 1969). P uptake from soils is generally inefficient, therefore, potato plants need a large quantity of applied P for maximum growth and yield despite taking up much less P than N. P uptake and usability are genetically variable among cultivars (Nitsos and Evans, 1969). There are contradictory opinions regarding potassium (K) fertilization of potato plants, especially concerning its effect on the tuber initiation stage as it promotes vegetative growth. K applications usually improve the size of the tuber (Sharma and Arora, 1988; Chapman et al., 1992). Potassium increases leaf extension, especially at the early stages of growth, and increases leaf area duration by postponing leaf dropping near maturity due to an increase in the tuber bulking duration and rate. The application of K activates many enzymes required in photosynthesis, proteins, and carbohydrate metabolism and supports the translocation of carbohydrates from leaves to tubers, which increases the size of tubers but not their number (Trehan et al., 2001). Starch formation enzymes have a particular demand for K (Nitsos and Evans, 1969); thus, tubers depend on a dynamic supply of K for the optimum starch content (Lindhauer and De Fekete, 1990). The formation and accumulation of starch positively influence the plant biomass generally and the tuber bulking rate in particular. Potassium plays a vital role in this respect because it is the most effective monovalent cation that stimulates starch formation enzyme activity, catalyzing simple glucose molecules’ association into large, compound starch molecules (Moinuddin et al., 2004). The starch formation is coupled with tissue and cell growth of the tubers, as K improves the overall plant growth (Singh and Singh, 1996) and eventually promotes the translocation of assimilates to the tubers (Moinuddin et al., 2005). This could subsequently increase the tuber bulking, biomass, yield, and resistance to diseases, drought, and frost (Imas and Bansal, 1999). Sulfur (S) is a secondary nutrient that plays an important role in the plant’s biological and chemical processes (Wes Haun, 2013). Sulfur helps increase crop yields directly by serving as a plant nutrient; indirectly by improving soil, principally for calcareous and saline/alkali soils with high pH, and promoting the use efficiency of other primary plant nutrients. Sulfur deficiencies not only diminish crop yield but also negatively influence quality. The three fundamental forms of sulfur available for field applications are ammonium thiosulfate, ammonium sulfate, and elemental sulfur (Wes Haun, 2013). Soil organic matter content is an essential soil quality characteristic, which impacts the physical well-being of soils and their productivity. Soil organic matter content improves soil bulk density, air and water contents, porosity, facilitates root penetration, water and nutrient use, and microbial activities in the soil (Khaleel et al., 1981; Lampurlanés and Cantero-Martinez, 2003). For example, Barmaki et al. (2008) reported that the total yield on plots to which manure was applied increased by about 15.6% over plots that received only chemical fertilizers. Soil organic matter decomposition significantly decreases soil pH (McCauley et al., 2009). Most micronutrients [e.g., zinc (Zn), copper (Cu), iron (Fe), manganese (Mn)] are bound firmly to the surface of soil particles. At high pH, these metal ions precipitate with calcium (Ca) compounds. As a result, they are not prevalent in soil solution and are inadequately available for plant uptake. In contrast, at low pH, fewer metal ions may either stick to the soil surface or precipitate with Ca compounds, making them more accessible for plant uptake. Soil organic matter also plays a direct role in preventing micronutrient fixation to soil particles. As the soil organic matter decays, micronutrients that are present in the organic matter are released and become available to crops. Furthermore, a combination of residual soil NO3 plus the N made available through the growing season by mineralization of soil OM can afford adequate N fertility to produce potato yields within 15% of the maximum obtained by applying 196 kg ha1 of used N Zebarth et al. (2004).

2.7 Irrigation requirements The potato crop is usually considered a water-requiring crop when, in fact, many other crops have similar or higher seasonal water use demands. This misinterpretation stems from the higher potato susceptibility to water stress contrasted to most other crops. This is partially due to its comparatively shallow root system. Furthermore, potatoes are usually grown in coarse-medium textured soils, which are characterized by low to medium water holding capacities (Pereira and Shock, 2006).

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Tuber initiation and early tuber development are sensitive stages for water stress. Water shortages at this period can considerably reduce yields by increasing the proportion of irregular, misshapen tubers. Water stress at early season can also diminish tuber quality (specific gravity). During the tuber bulking stage, water stress usually influences total tuber yield more than tuber specific gravity (King and Stark, 2015); however, late-season drought stress can increase tuber specific gravity relative to well-watered conditions. A large photosynthetically active leaf surface area is essential to secure high tuber bulking rates for an extended period. Maintenance of this large active leaf surface area necessitates continued growth of new leaves to replace the less active ones. Water stress stimulates leaf senescence and prevents new leaf development, resulting in an irreversible decline of leaf area, photosynthesis, and tuber bulking. The soil moisture content at harvest time has a vital impact on mechanical damage to tubers during the harvesting operation. Tubers that are dried because of low soil moisture content at harvesting time are more susceptible to blackspot bruises. In contrast, high soil water content at harvest time can increased tuber turgidity making the tubers more vulnerable to thumbnail cracking and shatter bruises (King and Stark, 2015). Potato tuber yield and quality are sensitive to excess soil water as well. Excess soil water from frequent or intense irrigation or rainfall throughout any growth stage can lead to leaching of NO3eN below the root area (rhizosphere), resulting in N deficiency, diminished fertilizer use efficiency, and an increased risk of groundwater pollution. The soil’s saturation for more than 8e12 h can damage the roots due to a deficiency of oxygen required for the respiration process. During the planting period, excessive soil moisture encourages seed tuber decay and delays plant emergence due to diminished soil temperature. Excess soil moisture during tuber bulking and maturation increases the risk of tuber decay. Potato that is over-irrigated during vegetative growth, especially at the tuber initiation stage, has a greater potential for developing tubers with brown core and hollow heart defects and are usually more sensitive to early dying (King and Stark, 2015).

2.8 Seed planting depth, spacing, and hilling Seed tubers need to be planted consistently with a specific spacing within and between rows as well as a consistent planting depth (Baarveld et al., 2002). Modern potato planters usually allow precision in the spacing of rows, a uniform distribution of tubers within the row, and a consistent planting depth and ridge formation above the seed tubers (Haider et al., 2012). Shallow planting depth is favored in the wet and heavy soils (clay) because deep seeding of the tubers may lead to depletion of stored nutrients before the sprouts appear above the soil surface. In contrast, in light-textured soils, where there is a higher probability of drought due to moisture stress, deep seeding is beneficial. Deep seeding also has an advantage over shallow seeding, where temperatures are high (Lorenz, 1945; Baarveld et al., 2002; Chehaibi et al., 2013). Deeper seeding might reduce the tuber’s infestation by certain pests (Lambion et al., 2006). Several different row spacings are in practice for potatoes in different areas of the world. In general, 20e40 cm seed spacing depending on the cultivar and market and a 90 cm row spacing is very common among potato growing areas (University of Illinois Extension, 2020). A close spacing (90 cm between rows and 30 cm or less between plants) is suggested, especially for early potato cultivars so that the plants can shade the soil and limit the extreme soil temperature throughout the tuber development stages (University of Illinois Extension, 2020). Potato hilling a very important practice in many areas around the world, especially where soil fumigation is not a common practice. It ensures good coverage of developing tubers with soil, which prevents their greening and often elevates yields. Potato hilling is usually conducted after emergence to allow tubers to grow in number and size in soft-tilled soil. The height of the hill varies depending on the cultivar and soil type. However, it usually ranges between 30 and 40 cm in height. There are two types of hilling, single- or double-pass hilling. Single-pass hilling is now more common in largescale production as it takes less effort to hill the potatoes without affecting the total yield. Double-pass hilling is done in two passes. The first pass typically occurs after the potato plants reach 15e20 cm in height. The second hilling conducted is conducted 7e14 days later and well before the plants close the rows. Hilling when the plants are very large can severely damage both the tops and the root system. In areas where soil fumigation, seepage irrigation, and flood irrigation are common, potato beds are prepared before seed planting, the seed potatoes are planted into the pre-made beds, and either no hilling or one-pass hilling is conducted.

2.9 Time to maturity Westermann (1993) classified the growth of the potato crop into five main stages. The duration of each stage depends on the cultivar and environmental conditions.

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Stage I is the sprout development stage that occurs within the first 30 days after planting. At this stage, the seed tuber is the primary source of nutrients and energy for the developing shoot, while soil N uptake is minimal. Growth stage II, occurring between 30 and 55 days after planting, is the vegetative growth period. During this stage, roots start to provide nutrients for the vines, and photosynthesis occurs in the leaves to produce energy for growth. Tuber initiation and setting occur at growth stage III. It usually occurs between 50 and 70 days after planting, although this maybe earlier, especially in early-maturing varieties. Vegetative growth and N uptake increase fast through this growth stage. As presented above, environmental conditions, such as temperature, soil moisture, N nutrition, and disease infections, as well as the physiological age of the seed at planting, can affect tuber initiation. Growth stage IV is the tuber bulking stage. The rates of vegetative growth and N uptake are decreased during this stage and can cease in the early-maturing varieties, while carbohydrates and other nutrients are translocated to the tubers. This stage occurs between 60 and 90 days after planting for the early-maturing varieties and 70e150 days after planting for the late-maturing varieties. Growth stage V is the tuber maturation stage. Vines start to senesce and nutrients are solubilized in the leaves and roots and then transported to the tubers. There is insignificant or no N uptake during this growth stage.

2.10 Types of cultivars Potatoes have different skin and flesh colors, specific gravity, sugar content, and processing characteristics. They can be classified into six major classes based on the characteristics of their tubers: russet, yellow, round-white, red, fingerling, and specialty. Russets are usually more desirable for frying and baking due to their high starch and low sugar content. Yellows have yellow skin and yellow to cream flesh. They are often used for baking, mashing, and boiling. Reds have red skin, but the flesh is typically cream or white in color. Due to their higher sugar content and low specific gravity, reds are not recommended for baking but are good for boiling and use in salads. Fingerlings are thin, finger-sized potatoes used for boiling or roasting. They are considerably less common compared to the other types and usually have a higher price. Specialty potatoes are also relatively rare and include a variety of colors and shapes, including rose, blue, and purple varieties. They can have purple skin and flesh as well, or rose flesh, and a range of other features (Nair et al., 2017).

2.11 Remote sensing Many types of research (Reynolds et al., 2000; Haverkort and MacKerron, 2012) confirmed that traditional practices of crop yield estimation could lead to inadequate crop yield assessment and inaccurate crop area appraisal. Besides, these methods typically depend on rigorous field data collection of crop and yield, which is a costly and time-consuming process. These strategies are time-consuming and heavily dependent on soil and plant analyses in the laboratory. Because of the restrictions of traditional yield prediction techniques, developing a non-destructive, rapid, and convenient approach to estimate yields timely would help facilitate management decisions and control fertilizer application. Remote sensing technologies have been utilized extensively in agriculture for precise management, nutrition investigation, and in-season yield prediction (Caturegli et al., 2016). Remote sensing technology can be utilized to estimate the temporal variation in crop dynamics, including crop yield and its spatial variability (Taylor, 1997). Visible (blue, green, and red) and near-infrared (NIR) parts of the electromagnetic spectrum can provide information on crop type, crop health, soil moisture, N stress, and crop yield (Magri et al., 2005; Hassaballa and Matori, 2011; Abdalla Hassaballa et al., 2013; Hassaballa et al., 2014). Numerous studies have found a good association between vegetation indices provided by remote sensing techniques, crop yield, and biomass (Rasmussen, 1997; Liu and Kogan, 2002). Numerous plant indices based on multispectral sensors, ratio vegetation index (RVI), perpendicular vegetation index (PVI), the simple ratio (SR), etc., have been used to distinguish plant physiological indexes, such as leaf area accurately, plant N response, and biomass (Broge and Leblanc, 2001; Aparicio et al., 2002; Hansen and Schjoerring, 2003). Several experiments (Taylor et al., 1997; Baez-Gonzalez et al., 2002, 2005; Funk and Budde, 2009) have focused on crop growth analysis using normalized difference vegetation index (NDVI) to improve precision agriculture. A study in plant life monitoring has confirmed that NDVI is linked with the leaf area index and the photosynthetic activity of crops. The NDVI is an indirect method of estimating primary productivity and crop yield using the portion of absorbed photosynthetically active radiation (Prince, 1990; Los, 1998). Among these indices, NDVI estimated with an optical sensor has shown to be efficient in predicting the in-season yield of many crops (Raun et al., 2001; Prasad et al., 2007). NDVI measurements can be utilized for identifying the N condition or biomass development of plants and can sometimes be employed for obtaining nutritional monitoring in field crops of elements like phosphorus (P) and potassium (K) (Samborski et al., 2009; Pimstein et al., 2011).

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References Abdalla Hassaballa, A., Matori, A.N., Shafri, M., Zulhaidi, H., 2013. Surface moisture content retrieval from visible/thermal infrared images and field measurements. Casp. J. Appl. Sci. Res. 2, 182e189. Ahmadi, S.H., Andersen, M.N., Plauborg, F., 2008. Potato root growth and distribution under three soil types and full, deficit and partial root zone drying irrigations. Plant Soil 206, 123e136. Ahmadi, S., Andersen, M.N., Lærke, P.E., Plauborg, F., Sepaskhah, A., Jensen, C.R., Hansen, S., 2011. Interaction of different irrigation strategies and soil textures on the nitrogen uptake of field grown potatoes. Int. J. Plant Product. 5, 263e274. Anonymous, 2019. Soil Management-Field Selection for Potato Production. https://www2.gnb.ca/content/gnb/en/departments/10/agriculture/content/ land_development/field_selection.html. (Accessed 22 July 2021). Aparicio, N., Villegas, D., Araus, J., Casadesus, J., Royo, C., 2002. Relationship between growth traits and spectral vegetation indices in durum wheat. Crop Sci. 42, 1547e1555. Baarveld, H., Peeten, H., Sterk, T., 2002. Culture Professionnelle de Pomme de Terre. In: NIVAA, nstitut Néerlandais pour la promotion des débouchés des produits agricoles., Pays-Bas, p. 20. Baez-Gonzalez, A.D., Chen, P.-Y., Tiscareño-López, M., Srinivasan, R., 2002. Using satellite and field data with crop growth modeling to monitor and estimate corn yield in Mexico. Crop Sci. 42, 1943e1949. Baez-Gonzalez, A.D., Kiniry, J.R., Maas, S.J., Tiscareno, M.L., Macias, C., Mendoza, J.L., Manjarrez, J.R., 2005. Large-area maize yield forecasting using leaf area index based yield model. Agronomy 97, 418e425. Barmaki, M., Rahimzadeh Khoei, F., Zehtab Salmasi, S., Moghaddam, M., Nouri Ganbalani, G., 2008. Effect of organic farming on yield and quality of potato tubers in Ardabil. J. Food Agric. Environ. 6, 106e109. 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Potassium nutrition of Kennebec and Russet Burbank potatoes in Tasmania: effect of soil and fertiliser potassium on yield, petiole and tuber potassium concentrations, and tuber quality. Aust. J. Exp. Agric. 32, 521e527. Chehaibi, S., Hamdi, W., Abroug, K., 2013. Effects of planting depth on agronomic performance of two potato varieties grown in the Sahel region of Tunisia. J. Dev. Agric. Econ. 5, 272e276. De Temmerman, L., Hacour, A., Guns, M., 2002. Changing climate and potential impacts on potato yield and quality ‘CHIP’: introduction, aims and methodology. Eur. J. Agron. 17, 233e242. Fageria, N.K., Baligar, V.C., 2005. Enhancing nitrogen use efficiency in crop plants. Adv. Agron. 88, 97e185. FAO, 1978. Food and Agriculture Organization. Fertilizer and Their Use. A Pocket Guide for Extension Officers, third ed. (Rome, Italy). FAOSTAT, 2015. Food and Agriculture Organization of the United Nations. Data Base of Agricultural Production. Food and Agriculture Organization, Rome, Italy. Fontes, P.C.R., Braun, H., Busato, C., Cecon, P.R., 2010. Economic optimum nitrogen fertilization rates and nitrogen fertilization rate effects on tuber characteristics of potato cultivars. Potato Res. 53, 167e179. Funk, C., Budde, M.E., 2009. Phenologically-tuned MODIS NDVI-based production anomaly estimates for Zimbabwe. Remote Sens. Environ. 113, 115e125. Goffart, J.P., Olivier, M., Frankinet, M., 2008. Potato crop nitrogen status assessment to improve N fertilization management and efficiency: paste presentefuture. Potato Res. 51, 355e383. Haider, M.W., Ayyub, C.M., Pervez, M.A., Asad, H.U., Manan, A., Raza, S.A., Ashraf, I., 2012. Impact of foliar application of seaweed extract on growth, yield and quality of potato (Solanum tuberosum L.). Soil Environ. 31, 157e162. Hansen, P., Schjoerring, J., 2003. Reflectance measurement of canopy biomass and nitrogen status in wheat crops using normalized difference vegetation indices and partial least squares regression. Remote Sens. Environ. 86, 542e553. Hassaballa, A., Matori, A., 2011. The estimation of air temperature from NOAA/AVHRR images and the study of NDVI-Ts impact: case study: the application of split-window algorithms over (Perak Tengah & Manjong) area, Malaysia. In: Proceeding of the 2011 IEEE International Conference on Space Science and Communication (IconSpace), 2011, pp. 20e24. Hassaballa, A.A., Althuwaynee, O.F., Pradhan, B., 2014. Extraction of soil moisture from RADARSAT-1 and its role in the formation of the 6 December 2008 landslide at Bukit Antarabangsa, Kuala Lumpur. Arabian J. Geosci. 7, 2831e2840. Haun, W., 2013. Optimizing Production with Sulfur: Fine-tuning Potato Nutrient Management. Potato Grower Magazine. https://www.potatogrower.com/ 2013/01/optimizing-production-with-sulfur. (Accessed 22 July 2021). Haverkort, A.J., MacKerron, D.K., 2012. Potato Ecology and modelling of crops under conditions limiting growth. In: Proceedings of the Second International Potato Modeling Conference, Held in Wageningen 17e19 May, 1994, vol. 3. Springer, Amsterdam, p. 379. Haynes, K., Haynes, F., Henderson, W., 1989. Heritability of specific gravity of diploid potato under high temperature growing conditions. Crop Sci. 29, 622e625.

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Hermans, C., Hammond, J.P., White, P.J., Verbruggen, N., 2006. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11, 610e617. Hijmans, R.J., 2003. The effect of climate change on global potato production. Am. J. Potato Res. 80, 271e279. Holm, L., Pancho, J.V., Herberger, J.P., Plucknett, D.L., 1979. A Geographical Atlas of World Weeds. John Wiley and Sons. Imas, P., Bansal, S., 1999. Integrated nutrition management in potato. In: Paper Presented at the Global Conference on Potato, December 1999, New Delhi, India. Jatav, A., Kushwah, S., Naruka, I., 2017. Performance of potato varieties for growth, yield, quality and economics under different levels of nitrogen. Adv. Res. 9, 1e9. Jensen, C., Svendsen, H., Andersen, M.N., Lösch, R., 1993. Use of the root contact concept, an empirical leaf conductance model and pressure-volume curves in simulating crop water relations. Plant Soil 149, 1e26. Jin, V.L., Schmer, M.R., Wienhold, B.J., Stewart, C.E., Varvel, G.E., Sindelar, A.J., Vogel, K.P., 2015. Twelve years of stover removal increases soil erosion potential without impacting yield. Soil Sci. Soc. Am. J. 79, 1169e1178. Johnson, S.B., 2009. Potato Facts: Growing Potatoes in the Home Garden. (Bulletin #2077). University of Maine. Khaleel, R., Reddy, K.R., Overcash, M.R., 1981. Changes in soil physical properties due to organic waste applications: a review. J. Environ. Qual. 10, 133e141. King, B.A., Stark, J.C., 2015. Potato Irrigation Management. (BUL 789, 800, 1-97). University of Idaho Extension Bulletin No. 800, Moscow, ID, p. 997. Kiple, K.F., Ornelas, K.C., 2000. Cambridge World History of Food. Cambridge University Press, Cambridge, UK, p. 1251. Kleinkopf, G., Westermann, D., Dwelle, R., 1981. Dry matter production and nitrogen utilization by six potato cultivars. Agronomy 73, 799e802. Kołodziejczyk, M., 2014. Effect of nitrogen fertilization and microbial preparations on potato yielding. Plant Soil Environ. 60, 379e386. Lafta, A.M., Lorenzen, J.H., 1995. Effect of high temperature on plant growth and carbohydrate metabolism in potato. Plant Physiol. 109, 637e643. Lambion, J., Toulet, A., Traente, M., 2006. Plant protection cultivation of organic potato, Fact 2: the fight against pests. Tech. Inst. Org. Agric. ParisFrance 4. Lampurlanés, J., Cantero-Martinez, C., 2003. Soil bulk density and penetration resistance under different tillage and crop management systems and their relationship with barley root growth. Agronomy 95, 526e536. Lauer, D., 1986. Russet Burbank yield response to sprinkler-applied nitrogen fertilizer. Am. Potato J. 63, 61e69. Levy, D., Veilleux, R.E., 2007. Adaptation of potato to high temperatures and salinity-a review. Am. J. Potato Res. 84, 487e506. Levy, D., Kastenbaum, E., Itzhak, Y., 1991. Evaluation of parents and selection for heat tolerance in the early generations of a potato (Solanum tuberosum L.) breeding program. Theor. Appl. Genet. 82, 130e136. Lindhauer, M., De Fekete, M., 1990. Starch synthesis in potato (Solanum tuberosum) tubers: activity of selected enzymes in dependence of potassium content in storage tissue. Plant Soil 124, 291e295. Liu, W., Kogan, F., 2002. Monitoring Brazilian soybean production using NOAA/AVHRR based vegetation condition indices. Int. J. Rem. Sens. 23, 1161e1179. Lorenz, O.A., 1945. Effect of planting depth on yield and tuber set of potatoes. Am. Potato J. 22, 343e349. https://doi.org/10.1007/BF02861893. Los, S.O., 1998. Linkages between Global Vegetation and Climate: An Analysis Based on NOAA Advanced Very High Resolution Radiometer Data: Available from NASA Center for AeroSpace Information. Magri, A., Van Es, H.M., Glos, M.A., Cox, W.J., 2005. Soil test, aerial image and yield data as inputs for site-specific fertility and hybrid management under maize. Precis. Agric. 6, 87e110. McCauley, A., Jones, C., Jacobsen, J., 2009. Soil pH and organic matter. Nutr. Manag. Mod. 8, 1e12. Millard, P., Marshall, B., 1986. Growth, nitrogen uptake and partitioning within the potato (Solanum tuberosum L.) crop, in relation to nitrogen application. J. Agric. Sci. 107, 421e429. Moinuddin, Singh, K., Bansal, S., Pasricha, N., 2004. Influence of graded levels of potassium fertilizer on growth, yield, and economic parameters of potato. J. Plant Nutr. 27, 239e259. Moinuddin, Singh, K., Bansal, S., 2005. Growth, yield, and economics of potato in relation to progressive application of potassium fertilizer. J. Plant Nutr. 28, 183e200. Nair, A., Vince, L., Donald, L., Laura, J., Lina, R.S., 2017. Iowa State University Extension and Outreach-Commercial Potato Production Guide. www. extension.iastate.edu/vegetablelab. (Accessed 22 July 2021). Nitsos, R.E., Evans, H.J., 1969. Effects of univalent cations on the activity of particulate starch synthetase. Plant Physiol. 44, 1260e1266. Oliveira, C., Alberto, D.A.S., 2000. Potato crop growth as affected by nitrogen and plant density. Pesqui. Agropecuária Bras. 35, 940e950. Pereira, A., Shock, C., 2006. Development of Irrigation Best Management Practices for Potato from a Research Perspective in the United States, vol. 1. Sakia.org e-publish, pp. 1e20. Pimstein, A., Karnieli, A., Bansal, S.K., Bonfil, D.J., 2011. Exploring remotely sensed technologies for monitoring wheat potassium and phosphorus using field spectroscopy. Field Crop. Res. 121, 125e135. Prasad, B., Carver, B.F., Stone, M.L., Babar, M., Raun, W.R., Klatt, A.R., 2007. Potential use of spectral reflectance indices as a selection tool for grain yield in winter wheat under great plains conditions. Crop Sci. 47, 1426e1440. Prince, S., 1990. High temporal frequency remote sensing of primary production using NOAA AVHRR. Appl. Remote Sens. Agric. 4, 169e183. Randall, R., 2012. A Global Compendium of Weeds. Department of Agriculture and Food of Western Australia, Perth, Australia, p. 1124. Rasmussen, M.S., 1997. Operational yield forecast using AVHRR NDVI data: reduction of environmental and inter-annual variability. Int. J. Rem. Sens. 18, 1059e1077.

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Raun, W.R., Solie, J.B., Johnson, G.V., Stone, M.L., Lukina, E.V., Thomason, W.E., Schepers, J.S., 2001. In-season prediction of potential grain yield in winter wheat using canopy reflectance. Agronomy 93, 131e138. Reynolds, C., Yitayew, M., Slack, D., Hutchinson, C., Huete, A., Petersen, M., 2000. Estimating crop yields and production by integrating the FAO Crop Specific Water Balance model with real-time satellite data and ground-based ancillary data. Int. J. Rem. Sens. 21, 3487e3508. Rykaczewska, K., 1993. Effect of temperature during growing season and physiological age of minitubers on potato plant development and yield. Bull. Potato Inst. 42, 39e46. Rykaczewska, K., 2004. Effect of high temperature during vegetation on potato (Solanum tuberosum L.) yield, period of tuber dormancy and seed tuber yielding ability. Part III. Value of seed tuber yielding. Zesz. Probl. Postepow Nauk. Rol. 496, 207e216. Samborski, S.M., Tremblay, N., Fallon, E., 2009. Strategies to make use of plant sensors-based diagnostic information for nitrogen recommendations. Agronomy 101, 800e816. Sharma, U., Arora, B., 1988. Effect of applied nutrients on the starch, proteins and sugars in potatoes. Food Chem. 30, 313e317. Singh, V.N., Singh, S.P., Thomas, G., 1996. Influence of split application of potato. J. Indian Potato Association 23, 72e74. Taylor, J.C., Wood, G.A., Thomas, G., 1997. Mapping yield potential with remote sensing. Precis. Agric. 1, 713e720. Tisdale, S.L., Nelson, W.L., 1975. Chapter 5: soil and fertilizer nitrogen. In: Soil Fertility and Fertilizers, third ed. Macmillan, New York, pp. 122e188. Soil Fertility and Fertilizer. Trehan, S., Roy, S., Sharma, R., 2001. Potato variety differences in nutrient deficiency symptoms and responses to NPK. Better Crops Int. 15, 18. University of Illinois Extension, 2020. Potatoes, Illinois Vegetable Garden Guide. https://web.extension.illinois.edu/vegguide/grow_potato.cfm. (Accessed 22 July 2021). USDA-NASS, 2019. https://spudman.com/news/usda-estimate-2019-potato-crop-down-6/. (Accessed 22 July 2021). Van Dam, J., Kooman, P.L., Struik, P., 1996. Effects of temperature and photoperiod on early growth and final number of tubers in potato (Solanum tuberosum L.). Potato Res. 39, 51e62. Veilleux, R.E., Paz, M.M., Levy, D., 1997. Potato germplasm development for warm climates: genetic enhancement of tolerance to heat stress. Euphytica 98, 83e92. Wagner, W., Herbst, D., Lorence, D., 2014. Flora of the Hawaiian Islands Website. Smithsonian Institution, Washington, DC, USA. https:// naturalhistory2.si.edu/botany/hawaiianflora/. (Accessed 22 July 2021). Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199e223. Westermann, D.T., Kleinkopf, G., 1985. Nitrogen requirements of potatoes. Agronomy 77, 616e621. Westermann, D.T., Kleinkopf, G.E., Porter, L., 1988. Nitrogen fertilizer efficiencies on potatoes. Am. Potato J. 65, 377e386. Westermann, D., 1993. Fertility management. In: Rowe, R.C. (Ed.), Potato Health Management. APS Press, St. Paul, MN, pp. 77e86. Zebarth, B., Leclerc, Y., Moreau, G., 2004. Rate and timing of nitrogen fertilization of Russet Burbank potato: Nitrogen use efficiency. Can. J. Plant Sci. 84 (3), 845e854.

Chapter 3

Economic considerations in potato production Gina A. Greenwaya and Joseph F. Guenthnerb a

Greenway Research and Consulting, Parma, ID, United States; bDepartment of Agricultural Economics and Rural Sociology, University of Idaho,

Moscow, ID, United States

3.1 Introduction Potato production systems are characterized by a series of interconnected links in a supply chain designed to meet the demands of consumers. Producers, processors, and packers are faced with the common challenge of optimizing resource allocation in ways that minimize input costs while maximizing the quality of output. Large capital investment in fixed assets and uncertain threats from weather and pests contribute to the level of risk incurred by potato growers. Potato processors and packers who form intermediate links in the supply chain face the risk of ensuring an ample supply of highquality raw product is available to meet evolving consumer demands. Economic issues related to pricing and production will be unique to the market potatoes are grown for. Resource requirements and quality standards will differ for seed, fresh, frozen processed, and chipping markets. Factors impacting consumer demand for potatoes and potato products require careful consideration to ensure production of raw and processed product is tailored to meet the tastes and preferences of final purchasers.

3.2 Economics of seed pricing and production 3.2.1 Pricing The reputation of individual seed potato producers is one attribute that has served as a signal of value across global seed potato production systems throughout time (Peppin, 1926; Hane, 1969; Gildemacher, 2009; Forbes et al., 2020). The single opportunity growers have each year to prove the quality of their product creates a unique level of risk, and a strong economic incentive to engage in careful and thorough management practices. Seed potato tubers are priced similar to other farm products in a two-stage process. Supply and demand forces form the basis for determining a market clearing price. A specific price is then “discovered” by combining the market clearing price with buyer/seller interactions. These include consideration of product attributes such as location, grades, quality, discounts, and buyer and seller services (Kohls and Uhl, 2002). One bad year can be enough to negatively impact the reputation of a grower or seed growing region for many years (Guenthner, 1976). As a result, producers with a reputation for disease presence or other issues relating to quality can suffer from the problem of excess supply. Buyers will bid down the price of seed until equilibrium is reached. A supply and demand model in disequilibrium (Fig. 3.1) forms the foundation for graphical analysis (Norwood and Lusk, 2008). In Fig. 3.1, 4000 cwt (181,437 kg; cwt is an abbreviation for hundredweight, which is a measure traditionally used in potato trading and equal to 100 pounds or 45.36 kg) of seed potatoes are available, but buyers are only willing to purchase 2000 cwt at the $16 per cwt price. Seed growers must lower their price to get rid of the excess supply. The lower price encourages producers to reduce production the following year. A consistent reputation for producing seed that is low in disease incidence and high in quality can have the opposite effect creating excess demand for seed from specific producers or regions. Buyers will bid up the price until equilibrium is reached. Fig. 3.2 provides graphical illustration of the theory of

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00028-7 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 3.1 Excess supply.

FIG. 3.2 Excess demand.

excess demand. At a price of $8 per cwt, buyers will want to purchase 4000 cwt of seed when only 2000 cwt of seed are available. Buyers will bid up the price of high-quality seed enticing producers to expand production the following year. A historical example from the burgeoning seed potato industry in Prince Edward Island, Canada illustrates the concept of excess demand for high quality seed potatoes. In 1919, Prince Edward Island seed producers shipped a train carload of seed potatoes to Long Island. The results from the seed were so favorable that every bushel produced the next year was purchased by Long Island seed dealers. The subsequent number of seed potato acres planted on PEI increased every year for the next 5 years (Peppin, 1926). One way that the reputation of seed growers and seed growing regions can be enhanced is through strict seed certification systems. Formal seed certification systems maintain a common goal of providing seed potato purchasers with independent third-party verification of low incidence of pathogens, varietal purity, and physiological age (Forbes et al., 2020). Specific criteria for obtaining certification vary by state, province, region, and country. Failure to meet these criteria results in a grower’s inability to sell harvested potatoes on the seed market and receive an appropriate price premium over processing or table stock potatoes. Infection with aphid-borne viruses, which is discussed in detail in Chapter 5, is a common cause for the tubers not being certified as seed.

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Informal seed systems represent another important way of marketing seed potatoes. Informal systems are often characterized by farmer-to-farmer trade or the purchase of unregulated seed at local markets (Forbes et al., 2020). In Kenya, researchers found three components of the seed potato system: Formal, Semi-formal and Farmer. The Farmer segment made up 96% of production but was considered the poorest quality, pointing out the need for seed improvement (Kaguongo et al., 2014). Whether a formal or informal system is used, the reputation of the producer is an important determinant of value in the price discovery process for seed potatoes.

3.2.2 Seed production In the US, the process of seed potato production begins with disease-free plantlets produced in tissue culture labs. The plantlets can be planted directly in the field but are typically used to produce minitubers. Soilless systems such as hydroponics or aeroponics are one way of producing minitubers; they can also be grown in soil by potting plantlets in greenhouses or screenhouses. Once produced, minitubers are harvested, stored, and planted the next year for production of the first field generation of seed. Minituber production and the subsequent early field generations of seed represent significant costs and risks. Minituber production costs will depend on yield and variety but have been estimated to range between $0.41 to $0.57 per minituber when produced by state university minituber production programs (Guenthner et al., 2013). When producing the first field generation of seed, specialized equipment will be needed to plant the minitubers. Some producers will use a modern-belt type planter designed to drop the mini tubers one by one with a high level of depth and spacing precision. Other producers will rely on older technology using an iron age style planter to seed the minitubers. Wider spacing will be required of early generations of seed for reduction of disease spread. Typical seeding rates in the US range from about 19,360 minitubers per acre (47,839 per ha) to 14,520 minitubers per acre, (35,879 per ha) depending on spacing. The resulting per acre costs from seed alone vary from about $5953 per acre ($14,704 per ha) to $11,035 per acre ($27,257 per ha) depending on variety and source of minitubers. Smaller multiplication rates should be expected from the first field generation of seed. Significant expenses for testing, management, and labor for roguing also require careful consideration. Additional risk will be incurred from seed grown in a commercial setting for the first time from newly released varieties because of a lack of previous history of commercial scale field performance. After the first field generation of seed is harvested, it is stored, and planted the next year for multiplication. This process is then repeated a limited number of times in the field to reduce the probability of disease infection.

3.3 Frozen processed potatoes 3.3.1 Market structure Frozen processed potato markets in the US are best characterized within the oligopsony market structure because of the concentration of a limited number of potato processors and many potato growers (Patterson and Bolotova, 2011). The levels of concentration of potato processors reflect economies of scale. Utilizing large facilities allows firms to capture efficiencies that reduce the per unit costs of processing. Potato processors are similar to many different types of food manufacturers in their ability to influence the price of inputs they purchase. Incentive adjusted contracts are the main pricing mechanism used for procuring raw product. The contracting system is designed to be mutually beneficial for growers and processors. Pre-season contracts provide processors access to a stable supply of high-quality raw product while helping growers reduce open market risk by securing placement for their crop in advance of planting. In an attempt to countervail some of the market power exerted by processors, frozen processed potato contracts are typically negotiated through grower formed cooperative bargaining associations. The degree to which market concentration in the potato industry impacts growers and consumers is not fully known. Research by Katchova et al. (2005) indicates oligopsony power in frozen French fry and chipping markets may be limited. In contrast, Richards et al. (2001) found grower losses due to oligopsony power could amount to as much as 1.6% of revenue. Research from other food industries characterized by market concentration suggest a simple perfect and imperfect competition model can provide an adequate basis for evaluating the impacts market concentration (Norwood and Lusk, 2008). A hypothetical market in perfect competition is shown in the left panel of Fig. 3.3. As the processing industry becomes more consolidated, buyers possess increased market power to negotiate prices below the intersection of supply and demand

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PART | I Potato as an important staple crop

FIG. 3.3 Producer and consumer surplus under perfect competition and oligopsony.

as shown in the right panel of Fig. 3.3. The ability of the few large firms to process potatoes at a lower cost than a perfectly competitive market increases the value of raw product causing the marginal value curve to rise. The demand curve for raw product shifts out. The increase in demand offsets the gain in market power achieved by processors. The result is no change in price, or producer surplus. Consumers would be made better off under this scenario. However, in cases where the shift in demand is smaller, consumers and producers would both be worse off.

3.3.2 Frozen processed contract negotiations and complications Each buyer negotiates specific contractual terms separately, but a primary goal of bargaining associations is to maintain a level of equivalency among the different contracts (Patterson and Bolotova, 2011). Price tends to be the focal point of the annual negotiations but revisions to other elements of the contract such as rejection clauses, quality incentives or penalties, and volume may also be discussed. Force majeure, or “Act of God” contractual provisions will be particularly noteworthy in the years 2020 and 2021. The provision, rooted in French law is literally translated as superior force, and allows buyers to modify contractual agreements with growers in the event of highly unexpected extenuating circumstances. The decline in food service demand for frozen potato products as a result of the COVID-19 pandemic resulted in uncertainty over raw product needs and use of the “Act of God” clause to revise agreements with growers in some potato producing regions in the US. Many production factors also contribute to uncertainty in contractual arrangements. Since contracts are negotiated in advance of planting, predicting input costs at the time of negotiation can be difficult. Insect pest pressure or unexpected disease pressure may also impact the profitability of contracts negotiated in advance of production. Weather is one of the largest factors affecting contract risk for growers. In recent years, air pollution resulting from wildfire smoke has also become an emerging issue for potato producers in the Pacific Northwest. The impact of prolonged periods of haze on direct sunlight may jeopardize grower’s ability to meet quality requirements.

3.3.3 Frozen processed contract parameters Potatoes will be contracted either for direct delivery to the processor at harvest, or for delivery from a grower storage facility at a specified date. Both direct delivery and grower storage contracts include some compensation for hauling the potatoes to their destination. Potatoes contracted for grower storage will include extra compensation to cover a portion of the fixed and variable costs of storage. Storage economics are discussed in detail in later section of the chapter.

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Incentive adjustments specified in the contracts are designed to reward potato attributes that improve processed quality and reduce waste. Maximizing the recovery rate, which is the finished product as a percent of raw product usage, is key for processor profitability (Bolotova and Patterson, 2009). Common contract incentives and penalties of particular importance to the frozen processing industry include consideration of potato size, specific gravity, bruise, and color (Curtis and McClusky, 2003; Bolotova and Patterson, 2009). Size and shape of the tuber are incentivized by processors to increase uniformity of the final product. Specific gravity measured as the ratio of weight in air to weight in water is a highly incentivized quality attribute because of the relationship of solids content of potatoes to the recovery rate of finished product (Kleinkopf et al., 1987). Color incentives are important for reducing acrylamide formation and meeting consumer preferences for golden colored potato products (FDA, 2016). Bruise is an important consideration because of its impact on disease and shrinkage in storage, recovery of raw product at the plant, and quality of final product (Thornton and Bohl, 1998).

3.4 Potato chips Potato snack foods, known as chips in the US and crisps in the UK, are an important market channel for many growers. The market structure consists of one dominant processor e Frito Lay e and dozens of smaller processors with mostly regional distribution. Growers are scattered, with many operating far from traditional potato growing regions. Potato snack transport is expensive due to the low density of the final product. Shipping containers reach a physical capacity long before a weight capacity. As a result, potato snack processing facilities are located close to population centers. Growing raw product for the snack market requires expertise and varieties that are different from those in fresh and frozen market channels. As a result, most potato snack growers specialize in production of chipper potato varieties. Some growers operate in multiple locations, including warm-weather states where winter and spring crops can be produced, to provide a reliable supply of raw product year-round. To minimize peel and trim loss, many chip processors prefer to buy freshly harvested potatoes rather than long-term storage product. Since chipstock potatoes are stored at higher temperatures, storage shrinkage is higher than that for fresh and frozen markets. Price discovery in the snack market is similar to the frozen processing market. Both rely on pre-season contracts, but some raw product also comes from the open market. One difference is that there are fewer quality incentives in the snack market, which traditionally operated on an accept/reject method of evaluating loads of raw product. Another difference is a lack of collective bargaining in the snack market. One reason for that is that the snack growers are scattered across the entire continent rather than located in a few adjacent counties.

3.5 Fresh potatoes 3.5.1 Market structure The majority of fresh potato production in the US is dedicated to russet-skinned varieties, followed by white, red, and yellow potatoes (USDA, 2019). Potatoes grown for the fresh market will either be sold off-the-field at harvest or stored for marketing later in the season. The fresh potato industry in the US is becoming increasingly vertically integrated, with many grower-owned packing operations or cooperative relationships with growers and packers. In addition to supplying restaurants and grocery stores with high quality product in a variety of packages, the fresh potato sector typically plays an important role in the dehydrated potato supply chain. A large portion of the raw product needed by dehydrators is procured from fresh pack potatoes that do not meet fresh-pack grade standards due to irregularities such as size, shape, and blemish.

3.5.2 Grading and packing Potatoes sold to the fresh market are subject to strict size and quality standards. In the US, minimum size requirements are specified by the USDA, but individual states or growing regions can use federal marketing orders to impose size standards that exceed USDA criteria. Smaller potatoes grading number one, with a diameter greater than one and 7/8 inches (5.4 cm), typically weighing between 4 and 8 ounces (113e226 g) are packed in five- or 10-pound (2.27e4.54 kg) bags and marketed for retail in grocery stores. The potatoes are shipped from the packer in bales containing either 10 five-pound bags, or five ten-pound bags. Larger potatoes meeting number one quality standards will be sorted by size and packaged in 50-pound (22.68 kg) cartons for sale to both retail and food service markets. The “count” cartons contain a specific number of potatoes, the

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smaller the count the larger the potato. The largest potatoes are purchased in a 40-count carton, with an average tuber weight of 20 ounces (567 g; 800-ounce carton divided by 40 tubers). The carton counts increase in increments of 10 up to a maximum count of 100 potatoes per carton. A 100-count carton corresponds with the smallest potato size profile available in a carton pack, with an average tuber weight of 8 ounces (226 g: 800/100). Number two potatoes can be sold in a variety of packages but are commonly marketed in fifty-pound sacks.

3.5.3 Bargaining associations in the fresh potato industry Fresh potato markets are often characterized by a high degree of price volatility. Adoption of new varieties and technology have contributed to improvements in production practices leading to steady increases in supply. At the same time, rising incomes and shifting consumer tastes and preferences for eating food away from home in affluent economies are contributing to a decline in fresh potato consumption in many countries throughout the world (USDA-ERS, 2019; Thorne, 2012). The imbalance between production and consumption can create prolonged periods of depressed prices, forcing some producers out of the industry while increasing levels of consolidation among remaining market participants. In the US, Idaho potato growers set the course for a change in fresh potato price patterns through formation of a marketing cooperative, United Potato Growers of Idaho (UPGI). The organization, established in 2004, was able to legally coordinate activities through anti-trust exemption provisions for agricultural cooperatives provided under the Capper Volstead Act of 1922. However, many cooperatives fail for reasons of inadequate capital, lack of memberships support, or ineffective management (Kohls and Uhl, 2002). United’s goals of managing potato supplies in ways that would make fresh potato production profitable, and facilitating coordinated marketing were communicated clearly. Since individualized, decentralized negotiations tend to produce the widest variation in pricing (Kohls and Uhl, 2002) providing improved access to market information was a critical managerial element that would impact the success of the cooperative. The cooperative was successful in achieving high membership, capturing 85% of potatoes destined for the fresh market at inception (Guenthner, 2012). Following Idaho’s lead, many other states formed regional cooperatives. In 2005, the regional cooperatives pooled to form United Potato Growers of America (UPGA). The cooperatives reach expanded across North America, when United Potato Growers of Canada, a sister organization, was formed. United was successful in improving price for fresh potato growers during the period of 2005 through 2010. However, during the 2011 to 2016 period, pricing was similar to the pre-cooperative period of 1993e2004 (Bolotova, 2017). One reason the impact of the cooperative was less pronounced during the 2011 timeframe could be due to modifications of United’s supply management program resulting from settlement of a lawsuit.

3.6 Storage economics Whether potatoes are used for seed, fresh market consumption, or for processing into chips or French fries, potato storage presents a number of considerations to be analyzed. Storage decision making requires consideration of the value of the potato, the fixed ownership costs of the storage facility, and the variable costs of operating the storage facility.

3.6.1 Fixed costs Fixed costs are: 1. Fixed only after the expense has been incurred 2. A function of time, not output 3. Not relevant for determining optimal level of input use The DIRTI five are the most common category of fixed costs which include Depreciation, Interest, Repairs, Taxes, and Insurance. Fixed costs categories for potato storage include consideration of the DIRTI five for the storage building, the ventilation or refrigeration system, and the storage handling equipment such as potato pilers and conveyors.

3.6.2 Storage variable costs Variable (Operating) costs are: (1) Incurred on an annual basis (2) Only incurred if the crop is stored (3) Vary with the amount of potatoes stored

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The variable cost categories for storage include shrinkage, operating interest, labor, power, sprout inhibitor (for all uses except seed), and insurance.

3.6.3 Understanding shrinkage The costs of shrinkage and quality loss as a function of time represent a unique and important variable cost category in potato storage. Since potato tubers are a living organism they will respire, losing moisture each month that they are stored. At higher temperatures potatoes will respire more, which is why the highest weight loss typically occurs upon entry to storage when the heat from the field is “sweat” from the potatoes as they prepare for dormancy. Following the initial “sweating” phase the amount of moisture loss will stabilize until the potatoes break dormancy. Once dormancy is broken late in the storage season the potatoes will lose greater amounts of moisture. The amount of shrink depends on storage temperature, relative humidity, variety, condition of potatoes upon entry, type of storage and air system, and management expertise. The dollar value of shrinkage is typically calculated by multiplying the percent of weight loss in each month of storage by the value of the potatoes. The value used for potatoes entering storage can either be based on the cost of production, or the market value, depending on the analysis being conducted.

3.6.4 Other storage variable costs An interest charge to the value of potatoes should be included to capture the accruing cost of capital as a result of storage. The cost of insurance may also require consideration and should be based on the value of the crop. Labor required to fill the storage will represent another important consideration. Electricity charges will depend on regional temperature variations, electricity rates, and type of storage, but some allocation should be made to estimate the costs of running air or refrigeration systems. Sprout inhibitor costs will depend on the number of applications and type of product being used.

3.6.5 Monthly break-even points All storage variable costs, including the cost of shrinkage, will accumulate month over month. As a result, the price required to break even will increase as a function of time. Accurate and detailed estimated monthly break-even point analysis is desirable for making informed and profitable storage decisions.

3.7 US potato consumption trends Trends in US per capita potato consumption from 1960 to 2019 are presented in Figs. 4 and 5 (USDA ERS, 2019). Total per capita consumption of potatoes in all forms, including fresh, frozen, chips, dehydrated, and canned increased at an average rate of 0.71 pound (322 g) per capita from 1960 to 1996 but declined by an average of 1.42 pounds (644 g) per capita from 1996 to 2019 (Fig. 3.4). Trends by individual potato category (Fig. 3.5) highlight relatively stable per capita consumption of potato chips over the 1960 to 2019 timeframe. Potato chip consumption averaged 16.4 pounds per person over 59 years. Dehydrated potato product consumption showed steady growth in all but 1 year from about 1960 to 1976. From 1977 to 2019, per capita consumption of dehydrated potato products has remained stable. Consumption of fresh potatoes has decreased at an average annual rate of 0.63 pounds (286 g) per capita over 59 years. Frozen potato consumption has increased at an average annual rate of 0.68 pounds (308 g) per capita since 1960.

3.8 Potato demand Tomek and Robinson (1990) group major factors influencing demand into four categories: population size and distribution, consumer income and its distribution, prices and availability of other commodities and services, and consumer tastes and preferences. These factors provide important framework for analyzing the historical context and evolution of demand for potatoes and potato products over time and for projecting future domestic and global demand for potatoes and potato products.

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PART | I Potato as an important staple crop

FIG. 3.4 Per capita US potato consumption, all potato products, 1960e2019.

FIG. 3.5 US per capita potato consumption by category, 1960e2019.

3.8.1 Population size and distribution The US population has increased at an average rate of about 1% each year over the last 60 years. Since 2002, growth in population has been increasing at a rate of less than 1% per year (US Census, 2019b). Trends in fertility rates suggest the number of children per woman is lower than what is needed to replace the population (US Census, 2019a). As a result, population growth will not have a large impact on demand for potatoes in the US in coming years. It is likely to remain a consideration in other parts of the world, such as Africa and India (see below).

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Age distribution of the population also influences demand and highlights some important considerations. Millennials and baby boomers make up the largest age groups in the US population, each require unique considerations. Millennials have a particular interest in eco-friendly and fair-trade products creating more opportunity for potato growing regions like Wisconsin to capture millennial market share with products like Healthy Grown . An estimated 73 million Americans are part of the baby boomer generation, and by the year 2030 all baby boomers will reach age 65 or older (US Census, 2019a). The “gray tsunami” demographic shift may play an important role in driving future demand for a wider variety of single serving potato products that are easily prepared.

3.8.2 Consumer income Understanding America’s changing eating habits will be important for forecasting future demand for potato products. Food away from home (FAFH), also known as the foodservice market, captures the category of food that is prepared outside of the home. Food at home (FAH), also known as the retail market, captures the category of food typically purchased for preparation in the home (USDA ERS, 2018). The FAFH category has seen steady increases in the share of household food budgets. In 2010, FAFH spending surpassed spending on food purchased for at home preparation from the retail market for the first time (USDA ERS, 2018). Higher income households have also been found to make FAFH purchases more frequently and to spend more on FAFH. Insights from the past can provide important context for understanding the impact of income on future demand for potatoes and potato products. Research from the 1990s found per capita disposable income to have a positive impact on demand for frozen potato products in both retail and foodservice markets (Guenthner et al., 1991a,b). Income has been found to have a positive impact on demand for a variety of other value-added potato products, including potato chips, and dehydrated potato products purchased for FAH consumption (Guenthner et al., 1991a,b). The positive relationship of income to demand suggests the value-added potato products mentioned above are normal goods. When goods are normal, an increase in income results in an increase in demand. The impact of income on the fresh potato category may be dependent on the specific variety of potato, packaging, and time. Research from the 1980s and 1990s found income to have a negative impact on fresh potato demand as a whole (Cardwell and Davis, 1980; Guenthner et al., 1991). The inverse relationship suggests fresh potatoes were inferior goods during the 1980s and 1990s. As income increased demand for fresh potatoes decreased. More recent research suggests the fresh russet, the fresh red, and fresh organic category may be normal goods. As income increases demand for fresh red, russet, and organic potatoes increases (Greenway et al., 2010; Chen et al., 2019).

3.8.3 Other goods 3.8.3.1 Substitutes The price and availability of other goods are important concepts within the context of potato demand. Goods are substitutes when an increase in the price of one leads to an increase in demand for the other. Previous research would suggest that the closest substitute for a potato is another type of potato. As fresh potato prices increase, frozen potatoes tend to be the substitute. The substitute for rising frozen potato prices is use of dehydrated potatoes (Guenthner et al., 1991). Other substitutes for potatoes include starchy foods such as rice.

3.8.3.2 Complements Goods that tend to be used together are complements. Complement goods are characterized by an inverse relationship between the price of one good and demand for the other. The diets of many international and domestic consumers throughout time have been characterized by the unique complementary relationship of potatoes to many different foods. The fish and chips industry represents an important complementary relationship in potato demand theory. It also represents a historical example of innovation for improvement of the quality of early day “take out.” Around 1910, Hancock Collis and Co, was selling a special “chip potato” paper bag that was designed to alleviate some of the problems of England’s vibrant fish frying sector (Walton, 1989). The bags filled important needs in the early day Quick Service Restaurant (QSR) marketplace by removing the negative connotations of serving fish and chips wrapped in old newspaper, providing an easy way to serve uniform portions in greaseproof paper, and proving customers the ability to put vinegar on their chips more readily (Walton, 1989). The “American” mainstay of hamburgers and French fries represents another important complementary relationship in potato demand theory that is often associated with QSR’s. White Castle was said to have taken emergency measures amidst

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PART | I Potato as an important staple crop

World War II when they began pairing French fries alongside their burgers for the first time (Kosalko, 2020). However, McDonald’s is perhaps more often associated with the “burger and fry” relationship, famously branding the Mac Fry as the gold standard for quality. The quintessential complementary relationship of meat and potatoes extends beyond foods typically associated with QSR0 like fish and chips or hamburgers and French fries to food at home fare. One example is steak, which has been found to be a complement to red and russet potatoes (Greenway et al., 2010) As the retail price of steak decreases, demand for red and russet potatoes increases. Chicken represents another complementary relationship found in food purchased for preparation at home. As the retail price of chicken decreases, demand for organic and yellow potatoes increases (Greenway et al., 2010).

3.8.4 Consumer tastes and preferences Changes in consumer tastes and preferences are often difficult to isolate from other demand shifters. Age, education, advertising, and experience are all factors that can contribute to the consumer’s decision-making process. Busy lifestyles have driven demand for products that are conveniently packaged and can be quickly and easily prepared. The number of women in the labor force has been found to have a positive impact on demand for frozen potato products because of their ease of preparation (Guenthner et al., 1991a,b). Other innovations that have eased preparation of food at home such as the microwave have also played a role in demand for potatoes. Research documents the positive impact of microwave oven ownership on demand for fresh potatoes during the period of 1970 through 1988 (Guenthner et al., 1991a,b). Diet fads are another taste and preference variable that has impacted demand for potatoes throughout time. The Atkins diet developed in the 1960s and popularized in the early 2000s influenced consumer attitudes toward carbohydrates, including potatoes. More recently, the carbohydrate restrictive ketogenic diet has attracted consumer attention. Other popular diet trends such as gluten free, vegan, and vegetarian support potato consumption. One of the most interesting trends on the horizon that could fuel potato demand is replacement of grain beer with potato brewed beer (Bamberg and Greenway, 2019). Potato beer is not only lower in gluten but could afford consumers nutritional advantages with its high potassium and vitamin C content (Bamberg and Greenway, 2019).

3.9 Global trends and future prospects for potato demand in developing countries The size and distribution of the population requires careful consideration in forecasting future demand for potatoes worldwide. Projections by the United Nations suggest India will gain status as the world’s most populous country by the year 2030. Researchers forecasted a corresponding 20 to 30 million ton increase in demand for potatoes over the same timeframe (Scott et al., 2019). Increased urbanization in the country could also contribute to shifts in consumer preference for processed, and value-added potato products. The vegetarian culture in India represents another important consideration. As income in India increases with economic growth and development, consumers are less likely to allocate additional income to meat products, creating more opportunity for expenditure on vegetables like potatoes (Pingali, 2006). Growth in global demand for potatoes is not limited to Asia. Accelerated economic development, rising consumer incomes, and growing urbanization in many developing countries have led to important shifts in eating habits (Scott et al., 2019). Expanded future prospects for potato demand in Africa, and South America are worthy of consideration. Within the South American region, Brazil shows a high potential for increasing demand for potatoes in the coming decade. The country has shown shifts away from traditional staples in favor of diversification of diets. Shifts in consumer tastes and preferences toward processed potatoes in the form of snacks and French fries represent another noteworthy development in Brazil (Scott and Kleinwechter, 2017).

References Bamberg, J., Greenway, G., 2019. Nutritional and economic prospects for expanded potato outlets. Am. J. Potato Res. 96, 206e215. Bolotova, Y., 2017. Recent price developments in the United States potato industry. Am. J. Potato Res. 94, 567e571. Bolotova, Y., Patterson, P.E., 2009. An analysis of contracts in the Idaho processing potato industry. J. Food Distrib. Res. 40, 32e38. Cardwell, H.T., Davis, B., 1980. A Seasonal Analysis of the U.S. Potato Market. College of Agricultural Science Publication No. T-l-192, Texas Tech University, Lubbock, Texas. Chen, I.C., Mitchell, P.M., Du, X., 2019. Price premium for geographically labelled food: the case of fresh potatoes. In: Proceedings of the Agricultural and Applied Economics Association Annual Meeting July 21e23, Atlanta, GA.

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Curtis, K., Mccluskey, J.J., 2003. Contract Incentives in the Processed Potato Industry. http://citeseerx.ist.psu.edu/viewdoc/download?doi¼10.1.1.200. 6071&rep¼rep1&type¼pdf (Accessed on 21 July 2021). Forbes, G.A., Charkowski, A., Andrade-Piedra, J., Parker, M.L., Schulte-Geldermann, E., 2020. Potato seed systems. In: Campos, H., H., Ortiz, O. (Eds.), The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind. Springer, Cham, Switzerland, pp. 431e447. Gildemacher, P.R., 2009. Innovations in Seed Potato Systems in East Africa. https://library.wur.nl/WebQuery/wurpubs/fulltext/212110 (Accessed on 21 July 2021). Greenway, G., Guenthner, J., Makus, L., Pavek, M., 2010. Fresh potato and meat preferences by US region. J. Food Distrib. Res. 41, 12e25. Guenthner, J., 2012. The development of United potato growers cooperatives. J. Coop. 26, 1e16. Guenthner, J., Lin, B., Levi, A., 1991. The influence of microwave ovens o the demand for fresh and frozen potatoes. J. Food Distrib. Res. 22, 45e52. Guenthner, J.F., 1976. An Economic Analysis of an Elite Seed Potato Farm in Montana. https://scholarworks.montana.edu/xmlui/bitstream/handle/1/5276/ 31762100141538.pdf?sequence¼1 (Accessed on 21 July 2021). Guenthner, J.F., Charkowsi, A., Genger, R., Greenway, G., 2013. Varietal differences in minituber production costs. Am. J. Potato Res. 91, 376e379. Guenthner, J.F., Levi, A.E., Lin, B., 1991. Factors that affect the demand for potato products in the United States. Am. Potato J. 68, 569e579. Hanes, J.K., 1969. Organization and Structure of the Red River Valley Potato Industry. Economic Study Report No. S68-3. Department of Agricultural Economics, Institute of Agriculture, University of Minnesota, Minneapolis Minnesota, in Cooperation with the U.S. Department of Agriculture. Kaguongo, W., Maingi, G., Barker, I., Nganga, N., Guenthner, J., 2014. The value of seed potatoes from four systems in Kenya. Am. J. Potato Res. 91, 109e118. Katchova, A.L., Sheldon, I.M., Miranda, M.J., 2005. A dynamic model of oligopoly and oligopsony in the U.S. potato-processing industry. Agribusiness 21, 409e428. Kleinkopf, G.E., Westermann, D.T., Wille, M.J., Kleinschmidt, G.D., 1987. Specific gravity of russet Burbank potatoes. Am. Potato J. 64, 579e587. Kohls, R.L., Uhl, J.N., 2002. Marketing of Agricultural Products. Prentice-Hall, Inc, New Jersey. Kosalko, G.F., 2020. The History of White Castle. Whiting-Robertsdale Historical Society. https://www.wrhistoricalsociety.com/white-castle (Accessed on 21 July 2021). Norwood, F.B., Lusk, J.L., 2008. Agricultural Marketing and Price Analysis. Pearson Education, Inc, New Jersey. Patterson, P.E., Bolotova, Y., 2011. Have processing potato contract prices kept pace with cost of production? An empirical analysis from Idaho. Am. J. Potato Res. 88, 135e142. Peppin, S.G., 1926. The seed potato situation in Prince Edward Island. Am. Potato J. 3, 62e64. Pingali, P., 2006. Westernization of Asian diets and the transformation of food systems: implications for research and policy. Food Pol. 32, 281e229. Richards, T.J., Patterson, P.M., Acharya, R.N., 2001. Price behavior in a dynamic oligopsony: Washington processing potatoes. Am. J. Agric. Econ. 83, 259e271. Scott, G., Kleinwechter, U., 2017. Future scenarios for potato demand, supply and trade in South America to 2030. Potato Res. 60, 23e45. Scott, G.J., Petsakos, A., Suarez, V., 2019. Not by bread alone: estimating potato demand in India in 2030. Potato Res. 62, 281e304. Thorne, F., 2012. Potato prices as affected by supply and demand factors: an Irish case study. In: Proceedings of the European Agricultural and Applied Economics Association Annual Seminar February 23-24, Dublin, Ireland. Thornton, M.K., Bohl, W.H., 1998. Preventing Potato Bruise. University of Idaho Cooperative Extension System Agricultural Experiment Station Bul 725. University of Idaho, Moscow, Idaho. https://www.extension.uidaho.edu/publishing/pdf/bul/bul0725.pdf (Accessed on 21 July 2021). Tomek, W., Robinson, K., 1990. Agricultural Product Prices. Cornell University Press, New York. United States Census Bureau, 2019a. Census Will Help Prepare for the Incoming Wave of Aging Baby Boomers. https://www.census.gov/library/stories/ 2019/12/by-2030-all-baby-boomers-will-be-age-65-or-older.html (Accessed on 21 July 2021). United States Census Bureau, 2019b. New Estimates Show US Population Growth Continues to Slow. https://www.census.gov/newsroom/press-releases/ 2019/popest-nation.html (Accessed on 21 July 2021). United States Department of Agriculture Economic Research Service, 2018. Americas Eating Habits: Food Away from Home. https://www.ers.usda.gov/ webdocs/publications/90228/eib-196_ch3.pdf?v¼2267.5 (Accessed on 21 July 2021). United States Department of Agriculture Economic Research Service Food Availability Per Capita Data System, 2019. https://www.ers.usda.gov/dataproducts/food-availability-per-capita-data-system/ (Accessed on 21 July 2021). United States Department of Agriculture, 2019. Potatoes Annual Summary. https://downloads.usda.library.cornell.edu/usda-esmis/files/fx719m44h/ 7p88cv74d/b5645489z/pots0919.pdf (Accessed on 21 July 2021). United States Department of Health and Human Services Food and Drug Administration Center for Food Safety and Applied Nutrition, 2016. Guidance for Industry Acrylamide in Foods. https://www.fda.gov/media/87150/download (accessed on July 21, 2021). Walton, J.K., 1989. Fish and chips and the British working class, 1870-1930. J. Soc. Hist. 23, 243e266.

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Part II

Biology of major pests

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Chapter 4

Colorado potato beetle Andrei Alyokhina, Galina Benkovskayab and Maxim Udalovc a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bInstitute of Biochemistry and Genetics, Russian Academy of

Science, Ufa, Russia; cIndependent Consultant, Ufa, Russia

The Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), is one of the most notorious insect pests of potatoes. Since becoming a problem in the mid-19th century, the beetle remains a formidable threat to the potato industry, and it continues to expand its geographic range into new regions of the world. A diverse and flexible life history, combined with a remarkable adaptability to a variety of stressors, makes the Colorado potato beetle a very challenging pest to control.

4.1 Taxonomy and morphological description The Colorado potato beetle belongs to the family Chrysomelidae, or leaf beetles. With 35,000 species described worldwide, it is the third largest family in the order Coleoptera. Members of this family feed on plants, both as larvae and as adults, with both life stages consuming the same or related plant species. Many species of Chrysomelidae are host-specific (Arnett, 2000). The Colorado potato beetle was first described by Thomas Say in 1824 as a member of the genus Chrysomela (Say, 1824). Based on morphological characteristics, it was then moved to the genus Doryphora (Suffrain, 1858). Finally, Stål (1865) included this species into a newly described genus, Leptinotarsa, as it stands today. Jacques (1988) listed a total of 41 species in this genus, of which nine occur in the United States, nine in Central and South America, and 27 in Mexico. However, Bechyne (1952) argued that L. porosa Baly and L. paraguensis Jacoby belong to the genus Cryptostetha. Leptinotarsa is considered to be an evolutionarily recent genus that is still in the process of active speciation in North America, with Southern Mexico most likely being its center of origin (Tower, 1906; Medvedev, 1981). The 20 Leptinotarsa species that live on known host plants are specialized feeders (Hsiao and Hsiao, 1983). Ten of these (including the Colorado potato beetle) feed on plants in the family Solanaceae, nine in the family Compositae, and one in the family Zygophyllaceae. The Colorado potato beetle is the most notorious member of Leptinotarsa. The adult beetles are oval in shape and are approximately 10 mm long by 7 mm wide. They are pale yellow in color, with five black stripes along the entire length of each elytron and black spots on the head and pronotum. The eggs are about 1.5 mm long, and their color changes from yellow right after oviposition to orange for mature eggs that are ready to hatch. The larvae are eruciform (an entomological term that means resembling caterpillars in shape and capable of moving freely using legs attached to the thorax; the bodies may be long or short and humped), red to orange in color, with black head and legs and two rows of black dots on each side. Four instars are completed before pupation. Based on morphological characteristics, in particular on spot patterns and coloration of the head, pronotum, and elytra, Tower (1906) originally subdivided what is currently known as L. decemlineata into four species. However, later experiments showed that all of those were fully capable of interbreeding (Tower, 1918; Hsiao, 1985). Furthermore, analysis of male genitalia did not reveal any noticeable differences. As a result, Jacques (1972) merged them into a single species, an approach currently followed by most scientists. However, Jacobson and Hsiao (1983) found distinct difference in isozyme frequencies in the Colorado potato beetle population from southern Mexico and populations from the United States, Canada, and Europe. The difference was large enough to regard the two as separate subspecies. Their finding is supported by more recent work done using modern molecular techniques, where Piiroinen et al. (2013) found significant

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(A)

(B) 1

2

4

5

7

8

3

6

9

FIG. 4.1 Spot patterns on the Colorado potato beetle pronotum.

divergence among haplotypes of nuclear genes between Colorado potato beetle populations collected from wild hosts on the central plains of the United States and pest populations on one side, and Mexican populations on the other side. Similarly, Izzo et al. (2018) reported that mtDNA haplotype difference between United States and Mexico beetles was sufficient to justify placing them into two distinct species. Furthermore, beetles from these two geographic areas responded differently to the onset of winter conditions and had different overwintering behaviors (Izzo et al., 2014a,b). Morphological analyses of spot patterns on the adult pronotae (Fasulati, 1985, 1993, 2002, 2007) (Fig. 4.1) also supported the existence of several (American, EuropeaneSiberian, and Central Asian) subspecies of the Colorado potato beetle. Interestingly, there were considerable changes in spot patterns within the same populations over several decades (Zeleev, 2002; Kalinina, 2007; Benkovskaya et al., 2004). Those may indicate active microevolutionary processes within the species. Alternatively, they could be attributed to genetic bottlenecks due to insecticide applications (see Chapter 24 for more details). Several morphotypes that can be distinguished from each other by degree of their melanization may exist within the same Colorado potato beetle populations. Tower (1906) in the United States and Boiteau (1980) in Canada collected beetles that were almost completely white in color. Hsiao and Hsiao (1982) later discovered that some of the Boiteau’s (1980) white-colored beetles also had pearl-colored eyes. They determined that white-body and pearl-eye morphotypes were caused by mutations in single autosomal recessive genes that segregated independently from each other. Boiteau et al. (1994) also found a beige mutant in Canada that had no black stripes on its elytra, which are otherwise characteristic for this species and even inspired its Latin name. The inheritance of the beige mutation was controlled by two dominant genes, both of which were required for the expression of this trait. On the other side of the spectrum, Kaplaneck (1953) and Faber (1957) in Austria and Boiteau (1985) in Canada observed entirely black adult beetles. In both Austrian and Canadian cases, the black color was inherited recessively (Faber, 1957; Boiteau, 1985). Along the same lines, Benkovskaya and Nikonorov (2016) identified three morphological types that differed by the degree of integument melanization and were simultaneously present in the populations of beetles from Southern Urals region in Russian Federation. They described those as light-colored achromists, dark-colored melanists, and normal-colored intermediates. In addition to color, Colorado potato beetle morphotypes may also differ in other biological characteristics. For example, black (Faber, 1957; Boiteau, 1985; Benkovskaya and Nikonorov, 2016) and beige (Boiteau et al., 1994) morphotypes had lower reproductive output compared to the normally-colored beetles, although for the beetles observed by Benkovskaya and Nikonorov (2016) that was compensated by the lower survival of their offspring. To the contrary, white beetles did not suffer any reduction in fitness (Boiteau, 1980). Overall, it appears that current evidence is supportive of Tower’s (1906) idea that modern L. decemlineata consists of several species, and that merging them into a single species by Jacques (1972) was not justified by their evolutionary history. Therefore, it may be appropriate to at least describe Mexican Colorado potato beetles as a new species. However, as discussed in Chapter 24, it is still debatable what constitutes a distinct species, and how much different species should differ from each other. For practical reasons, separating Mexican populations is probably not important because most of the research has been done over the years on pest populations, which will still belong to L. decemlineata.

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4.2 Origins and history of spread Wild Colorado potato beetles feed mostly on buffalobur, Solanum rostratum, which is considered to be their original ancestral host (Tower, 1906; Hsiao, 1981; Casagrande, 1987; Izzo et al., 2018). The Colorado potato beetle was first collected in the United States in 1811 by Thomas Nuttall. Subsequently, additional collections were made in 1819e20 near the IowaeNebraska border by Thomas Say (Casagrande, 1985; Jacques, 1988). It has been long thought that both buffalobur and the beetles might have been brought into the southern and central plains of the United States by early Spanish settlers moving northwards from the central highlands of Mexico (Gauthier et al., 1981; Casagrande, 1987; Hare, 1990), the point of view advocated in the first edition of this book. However, Piiroinen et al. (2013) and Izzo et al. (2018) presented convincing molecular evidence that Colorado potato beetle actually expanded onto potato from buffalobur on the central plains of the United States, while Mexican beetles belong to a separate species that is not even adapted to feeding on potatoes (see Chapter 24). The host expansion occurred without a noticeable genetic bottleneck, suggesting considerable gene flow between beetles on potato and buffalobur, at least early in the invasion process. The first major Colorado potato beetle outbreak in cultivated potatoes in the United States was reported in 1859, when severe damage was observed on fields about 100 miles west of Omaha, Nebraska (Jacques, 1988). Feeding on potatoes represented a host range expansion for this species, which is described in detail in Chapter 24. Following the initial outbreak, eastward expansion of the beetles’ geographic range was very rapid, with beetles reaching the Atlantic coast of the United States and Canada in 15 years (Casagrande, 1987). The beetles crossed the Mississippi river in 1865, reached Ohio in 1869, and reached Maine in 1872 (Jacques, 1988). They then proceeded to the southern provinces of Canada, which were colonized by 1901 (Ivanschik and Izhevsky, 1981). Westward expansion was somewhat slower, limited in part by scarcity of potatoes (Riley, 1877). The first serious damage to potatoes in Colorado was reported in 1874 (Riley, 1875). However, 10 years earlier, Walsh (1865) reported a considerable beetle population feeding on S. rostratum in Colorado. That observation eventually resulted in the name of that state being incorporated into the generally accepted common name of this species (Jacques, 1988). As discussed here, however, this name is somewhat misleading. Calling this species a Nebraska potato beetle or an Omaha potato beetle would have been more appropriate given its geographic origin and the history of spread. All in all, the beetle’s range between 1860 and 1880 expanded by more than 4 million km2 (Trouvelot, 1936). Colonization of North America was completed in 1919, when the beetles were found in British Columbia (Ivanschik and Izhevsky, 1981). The first European population of Colorado potato beetles was discovered in England in 1875; the beetle then invaded continental Europe via Germany in 1877. Another infestation was discovered 1 year later in Poland. All those populations were successfully eradicated soon after being discovered (Feytaud, 1950; Wegorek, 1955; Jacques, 1988). Quarantine measures and eradication campaigns were largely successful in keeping the pest out of Europe until 1922, when selfpropagating populations were finally established in France (Feytaud, 1950). After 1922, the beetle steadily spread throughout Western and Central Europe, reaching the border of Poland by the mid-1940’s (Ivanschik and Izhevsky, 1981). Beetle dispersal was greatly facilitated by relaxed quarantine regulations and large-scale movements of military cargo during World War II. In 1949, Colorado potato beetles crossed the border of the Soviet Union but were quickly eradicated. Strict quarantine, combined with field monitoring and eradication programs, kept beetles away for the following 9 years. However, in 1958, warm spring temperatures and strong western winds resulted in massive invasions ranging from the Carpathian Mountains to the Baltic Sea. This led to the establishment of reproducing populations, which have continued their eastward spread ever since (Ivanschik and Izhevsky, 1981). Presently, the Colorado potato beetle damages potato crops all over Europe, Asia Minor, Iran, Central Asia, western China, and Russian Far East (Jolivet, 1991; Weber, 2003; Bienkowski and Orlova-Bienkowskaja, 2018). Its current range covers over 16 million km2 in North America, Europe, and Asia and continues to expand (Weber, 2003). Potentially, the beetle could spread to temperate areas of East Asia, the Indian subcontinent, South America, Africa, New Zealand, and Australia (Vlasova, 1978; Worner, 1988; Jolivet, 1991; Weber, 2003). Although the Colorado potato beetle is a highly mobile species that is capable of flying over long distances, especially with prevailing winds (Boiteau et al., 2003), its rapid dispersal had been greatly facilitated by human movement. Potato is a common and ubiquitous crop, which is often moved over considerable distances after harvest. Furthermore, there is often a considerable amount of traffic of material through potato-growing areas. Because of their small size, the beetles can easily hitch a ride with a variety of different cargoes. The rapid spread of the Colorado potato beetle during World War II and at the onset of the Cold War has been sometimes attributed to its use as a biological weapon. In particular, East German authorities initiated an aggressive propaganda campaign that accused the United States in dropping the beetles on their crops. Similar rumors circulated in the

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Soviet Union, although the propaganda pitch was much more subdued. There was indeed some research into the possibilities of weaponizing this species conducted in France, Germany, and possibly Great Britain right before or during World War II (Garrett, 1996; Lockwood, 2009). However, there is no evidence that the Colorado potato beetle has ever been released for the purpose of sabotaging enemy crops. On the contrary, the timing and geography of the spread indicate that the spread was attributed to natural range expansion from previously colonized areas. Interestingly, during the recent war between NATO and Taliban in Afghanistan, local farmers blamed the recent beetle arrival on United States aid workers bringing the pest in with contaminated shipments of seed potatoes (Arnoldy, 2010). Again, in this case, it can be speculated that the beetles most likely arrived on their own from neighboring Tajikistan.

4.3 Genetic variability Populations invading new areas are usually subject to the founder effect during the colonization event (Sakai et al., 2001). As a result, they are often genetically depauperate compared to their geographic centers of origin. Grapputo et al. (2005) used the analysis of mitochondrial DNA (mtDNA) and amplified fragment length polymorphism (AFLPs) markers to examine the genetic diversity of Colorado potato beetle populations in North America and Europe. They found high levels of both mitochondrial and nuclear variability in North American beetle populations, with the highest genetic diversity detected in populations from the central United States. Crossley et al. (2019) obtained allele frequency data from 7408 single-nucleotide polymorphism loci and detected no evidence of severe bottlenecks associated with colonization history. There was also a strong genetic differentiation between populations in North America and Europe. European populations showed a significant reduction at nuclear markers (AFLPs) and were fixed for one mitochondrial haplotype. That finding suggested the possibility of a single successful founder event. However, European populations have maintained genetic variability at the nuclear level. When the populations from the two continents were analyzed separately, the level of population differentiation was similar among North American populations and among European populations. Thus, it is probably more likely that the Colorado potato beetle invasion of Europe resulted from multiple introductions of the same haplotype. The extent of the gene flow between the geographically distinct Colorado potato beetle populations remains somewhat unclear. Colorado potato beetles are capable of long-distance flights, particularly when assisted by wind (Boiteau et al., 2003). However, the frequency of such dispersal, and the resulting gene flow, may be relatively low (Grafius, 1995). Zehnder et al. (1992) found no evidence of significant separation within North American populations based on the mtDNA data, which they attributed to the rapid range expansion of this species across the continent. However, other studies on North American beetles using mtDNA markers (Azeredo-Espin et al., 1996; Grapputo et al., 2005) and AFLPs (Grapputo et al., 2005) detected a strong separation among the studied populations. Furthermore, genetic data were consistent with differences in host plant affinity, photoperiodic response (Jacobson and Hsiao, 1983), and insecticide resistance (Hare, 1990). In addition, chromosomal studies suggested the existence of three different races within the species (Hsiao and Hsiao, 1983). Analysis of phenotypic variations in different geographic populations seems to confirm the populations’ relative isolation from each other. Based on nine variations of the spot patterns on the pronotae of adults, at least five distinct population complexes of the Colorado potato beetle were identified in Eastern Europe. Additional two complexes were described from North Kazakhstan and Central Asia (Fasulati, 1993). The taxonomic statuses of these seven population complexes have not yet been determined. According to Fasulati (1993), they are “probably close to geographic races.” Similarly, Eremina and Denisova (1987) reported differences in frequencies of pronotal patterns between different populations collected in the Saratov region of the Russian Federation. In the Lipetsk region, western and eastern groups of populations were identified on the basis of color pattern studies; the boundary between the ranges of these groups coincided with that between the agro-climatic regions (Ovchinnikova and Markelov, 1982). Two large population complexes were isolated on the territory of Bashkortostan in the Russian Federation based on the spot patterns and coloration of heads, pronotae, and elytra. The first complex included populations from the central part of the area, and the second complex included populations from the peripheral parts of the range (Udalov et al., 2010). Chen et al. (2014) reported different intrinsic rates of population growth in four beetle populations collected from different locations in the United States. Chen et al. (2014) and Baker et al. (2014) also detected geographic differences in the sizes of egg masses laid by females. Those led to the differences in the rates of egg cannibalism by newly hatched larvae, with more cannibalistic larvae hatching from eggs laid in larger clutches (Baker et al., 2014). Patterns of insecticide resistance in Colorado potato beetle populations provide additional insights into the extent of their interconnectedness. On a large geographic scale, beetles from the eastern United States have lower baseline susceptibility to insecticides the beetles from the northwestern United States (Alyokhin et al., 2015; Crossley et al., 2018;

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Dively et al., 2020). Eastern beetles have a constitutively elevated expression of an array of detoxification genes compared to the western beetles (Dively et al., 2020). Although the reported differences are related to the intensity of prior insecticide exposure and to crop management practices (Alyokhin et al., 2015; Dively et al., 2020), they did not appear to result from immediate selection by specific chemicals (Dively et al., 2020). On a smaller geographic scale, considerable differences in the levels and mechanisms of insecticide resistance in adjacent Colorado potato beetle populations (Boiteau et al., 1987; Heim et al., 1990; Ioannides et al., 1991; Grafius, 1995) also imply low gene flow at the time of resistance development. De Wilde and Hsiao (1981) and Hsiao (1981) observed significant differentiation in photoperiodic responses and host plant adaptation among geographically isolated Colorado potato beetle populations. Subsequent crosses confirmed the genetic nature of those differences. Lehmann et al. (2015) also detected a clear latitudinal pattern in diapause incidence and burrowing age for diapause among European beetle populations (Lehmann et al., 2015). Along the same lines, less heatshock protein Hsp70 was induced by cold temperature in the northernmost beetle populations than in the southernmost beetle populations. The level of constitutive Hsp70 was similar among the populations regardless of their geographic origins (Lyytinen et al., 2012). Heat tolerance, on the other hand, was similar among geographically isolated populations collected from different regions of the United States (Chen et al., 2014). Crossley et al. (2019) investigated the effects of historic and contemporary connectivity between potato fields on genetic differentiation of Colorado potato beetle populations in Wisconsin and in the Columbia Basin of Oregon and Washington using single-nucleotide polymorphism loci. They found significant, but weak, overall associations between landscape structure and genetic differentiation, with contemporary landscape features being considerably more important than historic features. There was no indication that the extent of potato land cover surrounding sampling sites affected genetic diversity; therefore, the observed relationship was not likely to be driven by the size of suitable habitat or the intensity of pest management.

4.4 Pest status and yield loss Wherever present, the Colorado potato beetle is considered to be the most important insect defoliator of potatoes. Indeed, ca. 40 cm2 of potato leaves per day are consumed by a single beetle during the larval stage (Logan et al., 1985; Ferro et al., 1985), and close to 10 cm2 of foliage are consumed per day during the adult stage (Ferro et al., 1985). After removing all foliage from colonized plants, beetles can feed on stems and exposed tubers. However, these constitute a suboptimal diet compared to leaves, and lead to poor larval growth and cessation of oviposition by adults (Alyokhin, unpubl. data). The Colorado potato beetle is very prolific, with one female laying 300e800 eggs (Harcourt, 1971), usually in clutches (masses) of 20e60 eggs each (Alyokhin, unpublished). It is not unusual for the beetles to completely destroy potato crops in the absence of control measures. Nevertheless, potato plants can withstand a considerable amount of defoliation without any reduction in tuber yield, particularly when damage is done before or after the tuber bulking period (Dripps and Smilowitz, 1989). For example, Hare (1980) found little effect of beetle feeding except during the middle four to 6 weeks of the season, when 70% defoliation resulted in a ca. 20% reduction in yield, while complete defoliation resulted in a ca. 64% reduction in yield. Similarly, in the study by Cranshaw and Radcliffe (1980), plants completely recovered from up to 33% defoliation inflicted early in the season and suffered only minor yield reduction from 67% defoliation. Wellik et al. (1981) also found that losing 29% of the leaf area did not affect potato yield. Zehnder et al. (1995) developed the action thresholds of 20% defoliation from plant emergence to early bloom, 30% from early bloom to late bloom, and 60% from late bloom to harvest. Ferro et al. (1983) and Zehnder and Evanylo (1989) did not find any effects of up to 100% defoliation during the 2 weeks immediately preceding vine kill. Stieha and Poveda (2015) conducted meta-analysis of the existing literature and derived damage thresholds greater than 60% defoliation at potato emergence and post-bloom and less than 40% defoliation pre-bloom and during bloom when potato stems stayed intact. If the stems were damaged, emergence and post-bloom damage thresholds were reduced to 35% and 52% defoliation, respectively, while the damage thresholds during bloom were reduced to 20% defoliation. Unfortunately, yield loss data are commonly highly variable, and its analysis is often a challenge (Nault and Kennedy, 1998). Furthermore, commercial farmers are very risk-averse and are generally not willing to tolerate beetle infestations in their crops. Therefore, even non-damaging levels of Colorado potato beetle infestations trigger control measures, usually in the form of insecticidal sprays.

4.5 Seasonal life cycle and diapause Diapause plays a very important role in Colorado potato beetle adaptation to the surrounding environment and greatly contributes to its success as a pest of cultivated potatoes. In particular, it allows for the colonization of territories with much

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colder climates compared to that of the beetle’s center of origin (Biever and Chauvin, 1990). Furthermore, diapausing individuals escape certain catastrophic events, such as insecticide applications, and then restore population sizes once conditions become favorable. Colorado potato beetles have a facultative overwintering diapause that takes place during the adult stage. It is induced by a short-day photoperiod and modulated by temperature and food condition and availability (de Wilde and Hsiao, 1981; de Kort, 1990). The exact ratio of light-to-dark hours differs among the populations. For example, beetles from Utah (41
440 N) entered diapause in response to a 15-hour photophase, while beetles from Arizona (31
580 N) responded to a 12-hour photophase. Beetles from Texas (26
240 N) did not enter diapause, regardless of photoperiod (Hsiao, 1981). A temperature of 31
C has been shown to shorten the critical photophase by three to 5 hours (de Wilde and Hsiao, 1981). Being a complex phenomenon, diapause is regulated by a number of different genes, including those coding for the juvenile hormone esterase (Vermunt et al., 1999), vitellogenin (de Kort et al., 1997), and a number of specialized diapause proteins (de Kort et al., 1997; Yocum, 2003). Beetle diapause is also affected by photoperiodic response of its host plants. Potato plants grown under short day conditions accumulated significantly more nitrogen in their leaves compared to the plants grown under long day conditions. Feeding on short-day plants more than tripled the number of Colorado potato entering the diapause (Izzo et al., 2014b). Diapause phenotypes may also vary within beetle populations. Yocum et al. (2011) developed a multiplex PCR protocol using five diapause-regulated genes to monitor diapause development of the Colorado potato beetle under field conditions. They found that some beetles were already in the diapause initiation phase in June when the day length was greater than 17 h. There was also noticeable inter-seasonal variation in the timing of diapause development, with the greatest differences being observed before the day length decreased to less than 15 h. After diapause initiation, some beetles burrow into the soil in the field. Other beetles move toward field edges by flight and by walking, presumably navigating toward tall silhouettes of trees and shrubs commonly found in hedgerows (Voss and Ferro, 1990a; Weber and Ferro, 1993; French et al., 1993). Upon arrival to overwintering sites, the beetles seek concealment by burrowing into the soil (Voss and Ferro, 1990b). The majority of the beetles dig down to between 10 and 25 cm (Lashomb et al., 1984; Weber and Ferro, 1993; Hunt and Tan, 2000). Overwintering survivorship increases with increasing depth (Lashomb and Ng, 1984; Weber and Ferro, 1993; Hunt and Tan, 2000). Lashomb et al. (1984) calculated that a 10-cm in soil depth decreased winter mortality in loam soils in New Jersey, USA by ca. 32%. However, additional digging requires the expenditure of extra energy, which can be in short supply during diapause. To channel additional resources used to survive unfavorable winter conditions, the flight muscles of diapausing beetles undergo significant degeneration (Stegwee et al., 1963). Diapause is terminated by temperatures >10
C (de Kort, 1990). However, there is usually a refractory phase of approximately 3 months, during which the beetles do not react to changes in environmental conditions. The post-diapause beetles usually accumulate 50-250
-days (DD > 10
C) before they appear on the soil surface (Ferro et al., 1999). Males and females exit their diapause simultaneously and start mating before re-colonizing the host plants (Ferro et al., 1999). There is considerable intra-population variation in the times of beetle emergence from the soil. Ferro et al. (1999) reported that beetles overwintering within a woody hedgerow adjacent to a potato field in western Massachusetts, USA emerged over a 3-month period. A certain number of overwintering beetles may remain in an extended diapause for two or more years (Isely, 1935; Trouvelot, 1936; Wegorek, 1957a,b; Ushatinskaya, 1962, 1966). Their exact proportion varies among beetle populations and may depend in part on environmental conditions. Ushatinskaya (1962, 1966) reported that, in western Ukraine, 0.4% e6.5% of beetles overwintering in sandy soils remained dormant for 2 years, but all beetles overwintering in clay soils emerged after the first winter. In Washington State, 16%e21% of overwintering adults emerged after two winters, and up to 2% emerged after three winters (Biever and Chauvin, 1990). Tauber and Tauber (2002) found extended diapause in 0% e7.2% of the beetles overwintering in upstate New York. However, prolonged diapause resulted in lower female fertility and lower larvae-to-adult survival. No such effects were observed for male beetles. Females exiting prolonged diapause produced quicker-developing offspring, but the opposite was true for males (Margus and Lindström, 2020). Up to 25% of the overwintered population may enter a second diapause (Isely, 1935; de Wilde, 1962; Jermy and Saringer, 1955; Minder and Petrova, 1966). However, they usually suffer very high mortality rates (Isely, 1935; Minder and Petrova, 1966), and probably do not play a significant role in the overall dynamics of beetle populations. In addition to overwintering diapause, Colorado potato beetles may also enter summer diapause, or aestivation. It is particularly common in arid areas (Tower, 1906; Faber, 1949), but has also been reported in other locations (Grison, 1939; Jermy, 1953; Minder and Petrova, 1966). Physiologically, summer diapause is similar to overwintering diapause, although its duration is usually shorter (Ushatinskaya, 1961, 1966; Minder and Petrova, 1966). From an ecological standpoint, it serves as an adaptation to excessive heat and desiccation.

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4.6 Interactions with host plants The Colorado potato beetle is an oligophagous herbivore that infests about 10 species of solanaceous plants. Of those, potato, Solanum tuberosum, tomato, S. lycopersicum, and eggplant, S. melongena, are important cultivated hosts. Feeding on potatoes represents a host range expansion for the Colorado potato beetle. There is also some host specialization among geographically-isolated Colorado potato beetle populations. Host-plant associations and the evolution of feeding preferences are discussed in detail in Chapter 24. To find and colonize potatoes and other host plants, Colorado potato beetles use both visual (de Wilde et al., 1976; Zehnder and Speese, 1987) and olfactory (Visser and Nielsen, 1977; Visser and Ave, 1978; Thiery and Visser, 1986; Landolt et al., 1999; Dickens, 2000) cues. Beetle attraction to potato odor in a laboratory olfactometer was first tested by McIndoo (1926) and was then repeatedly confirmed by a number of other authors (e.g., de Wilde et al., 1969; Visser, 1976; Thiery and Visser, 1986; Landolt et al., 1999). Not surprisingly, the attraction is stronger in hungry beetles (Thiery and Visser, 1995). In the same time, prior feeding experience enhances the beetle’s responses to host plant odor, probably due to associative or non-associative learning (Visser and Thiery, 1986). The beetles are capable of distinguishing between the odors of different host plant species. In an olfactometer study by Hitchner et al. (2008), they chose potato over eggplant or tomato, and eggplant over tomato. Also, damaged plants were more attractive to adult beetles compared to intact plants (Bolter et al., 1997; Landolt et al., 1999), but no such difference was detected for larvae (Dickens, 2002). Potato odor is comprised of a number of general leaf volatiles, all of which are emitted by most species of flowering plants (Visser et al., 1979). When tested individually or in combination, they did not elicit any response in the exposed Colorado potato beetles (Visser and Ave, 1978; Visser et al., 1979). Therefore, it is thought that beetles distinguish host plants based on the ratios of individual green leaf volatiles in the odor blend (Visser and Ave, 1978). Indeed, Dickens (2000, 2002) identified a three-component mixture consisting of common green leaf volatiles (z)-3-hexenyl acetate, (þ/) linalool, and methyl salicilate that was attractive to Colorado potato beetle adults. Despite strong olfactory responses displayed by the Colorado potato beetles under laboratory conditions, their ability to actively search and find hosts over long distances in the field is somewhat uncertain (Boiteau et al., 2003). It is likely that chance encounters play a significant role in the colonization of new habitats (Jermy et al., 1988), although beetle dispersal is definitely not a completely random process. Once Colorado potato beetles arrive onto host plants, they use their sense of taste for final host acceptance. Hsiao and Fraenkel (1968) and Hsiao (1969) identified several carbohydrates, amino acids, phospholipids, and chlorogenic acid that act as phagostimulants. Szafranek et al. (2006) found two additional phytochemicals, the alcohols present in the leaf surfaces of potatoes. Other secondary plant compounds are toxic to the beetles and/or serve as feeding deterrents. They might be responsible for plant resistance to beetle herbivory and therefore would be of interest to plant breeders, as discussed in Chapter 14 of this book. Adult oviposition preferences do not necessarily correlate with larval performance on chosen plants. Hufnagel et al. (2017) found that adults laid more eggs on S. immite Dunal plants compared to S. tuberosum, S. chacoense Bitter, and S. pinnatisectum Dunal. Larval development, feeding, and survival, however, were lower on S. immite than on the other three Solanum species. Similarly, Hsiao and Fraenkel (1968) and Sinden et al. (1980) also observed higher numbers of eggs on plant species that did not support larval or adult feeding. Such a mismatch may be an evolutionary strategy for widening the host range (Wiklund, 1974) because larvae surviving on a low-quality host plant will be relieved from intraspecic competition. It may also be responsible for the Colorado potato beetle’s switch onto cultivated potatoes that is discussed in detail in Chapter 24. There is also mounting evidence that interactions between phytophagous insects and their host plants are affected by microbial communities associated with both plants and insects (Wielkopolan and ObrepalskaSteplowska, 2016; Chung et al., 2017; Sorocan et al., 2020a,b), which we discuss in Chapter 25.

4.7 Reproduction and individual development Reproductive behavior in the Colorado potato beetle is strongly directed toward maximizing the genetic diversity of its offspring, and might be largely responsible for the evolutionary plasticity and adaptability of this species (see Chapter 24 for more details). The Colorado potato beetle is a highly promiscuous species, with both males and females performing multiple copulations with different partners (Szentesi, 1985). Although males guard females following copulation and display aggressive behavior toward other males (Szentesi, 1985), duration of such guarding is not sufficient to prevent subsequent mating (Alyokhin, unpublished). Instead of trying to protect their parental investment in a single female, mated summer-generation males increase their flight activity, probably to maximize the number of copulations with different mates (Alyokhin and Ferro, 1999b).

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However, there is some evidence of assortative mating among different beetle morphotypes. As discussed above, Benkovskaya and Nikonorov (2016) identified three beetle morphs that differed by the degree of integument melanization: light-colored achromists, dark-colored melanists, and normal-colored intermediates. The frequency of copulations among representatives of the three morphs was statistically different from what could have been expected in the case of random pairings. In particular, no mating was detected between achromist males and melanist females. Sexually mature females produce an airborne sex pheromone which acts as a long-range attractant for males (Edwards and Seabrook, 1997). Male beetles spend significantly more time on female-exposed potato foliage than on male-exposed or unexposed foliage. They also engage in a characteristic searching behavior that includes exploring more leaves per plant and moving more rapidly between leaves (Weber et al., 2020). In addition, there is a difference between the sexes in the composition of cuticular hydrocarbons (Dubis et al., 1987), which might be perceived by contact chemoreception and may play an important role in sex recognition (Jermy and Butt, 1991). Boiteau (1988) determined that at least three copulations are required to completely fill the female’s spermatheca. Moreover, between 5% and 20% of all copulations do not result in sperm transfer (Thibout, 1982). Therefore, repeated copulations appear to be necessary for the females to realize their full reproductive potentials. However, Orsetti and Rutowski (2003) did not find any correlation between the number of matings and the number of transferred sperm or female fecundity. On the contrary, there was a significant decrease in hatch rate with an increase in the number of copulations. When a summer generation female mates with two different males, their sperm mixes, and the first male still fertilizes 28%e48% of the eggs (Boiteau, 1988; Alyokhin and Ferro, 1999a; Roderick et al., 2003). Flight mill experiments conducted by Ferro et al. (1999) and Alyokhin and Ferro (1999b) revealed that gravid Colorado potato beetle females engage in a considerable amount of flight activity, allowing them to distribute eggs within and between host habitats. However, they fly significantly less than unmated females (Alyokhin and Ferro, 1999b), probably because of the weight and energy demands of maturing eggs. Alternatively, a higher flight propensity of unmated females may be related to their attempts to find a mate. Post-diapause females can lay eggs by utilizing sperm from pre-diapause mating from the previous fall, but at a significant fertility cost compared to spring-mated females (Ferro et al., 1991; Baker et al., 2005). Spring mating encourages vitellogenesis and oviposition (Peferoen et al., 1981; Benkovskaya, 2009). Therefore, beetles usually mate after diapause termination in the spring (Ferro et al., 1999). Experiments using radiation-sterilized Colorado potato beetle males revealed that sperm from spring mating takes complete precedence over overwintered sperm from the previous year’s mating (Baker et al., 2005). Unlike flight of summer-generation beetles, flight of post-diapause beetles is not affected by their mating status (Ferro et al., 1999). Summer-generation females do not usually start ovipositing until they accumulate at least 51
-days since emergence from pupae (Alyokhin and Ferro, 1999b). The effective developmental threshold for the Colorado potato beetle is 10
C. Development from egg to adult takes between 14 and 56 days (de Wilde, 1948; Ferro et al., 1985; Logan et al., 1985). The fastest development occurs between 25 and 32
C and appears to differ among populations of different geographic origins. Growth rates follow a curve typical of poikilothermic organisms, including insects (Logan et al., 1976). This curve initially ascends from threshold temperature to optimum temperature, and then rapidly descends from optimum to lethally high temperature. Colorado potato beetle larvae frequently cannibalize each other, especially soon after eclosion from eggs. In most cases, cannibalistic larvae and adults consume conspecific eggs. Harcourt (1971) found that cannibalism accounted for over 10% of total beetle mortality. It also accelerates development and increases the size of growing Colorado potato beetle larvae (Collie et al., 2013; Tigreros et al., 2017), with some indications that females produce trophic eggs to support neonate larvae (Tigreros et al., 2017). In addition to egg cannibalism, adult Colorado potato beetles also attack and consume each other, especially under conditions of starvation or feeding on unpreferred host plants, lack of water, and crowding (Booth et al., 2017; Alyokhin and Baron, 2021). Not surprisingly, small and injured beetles are most vulnerable to predation (Booth et al., 2017). Pupation takes place in soil near plants where the larvae have completed their development. Average pupation depth is 5e12 cm (Feytaud, 1938). Both Colorado potato beetle larvae and adults are capable of behavioral thermoregulation, which allows them to maintain body temperatures that are more optimal for physiological development than ambient temperatures (May, 1981). The beetles usually rest and feed on the upper surface of leaves when air temperatures are low, thus increasing their exposures to solar radiation (May, 1981). As a result, their body temperatures are often elevated to several degrees above air temperature (May, 1981). When ambient temperatures increase, larvae tend to move under leaves (Lactin and Holliday, 1994) or to the inner part of the potato canopy (May, 1981).

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4.8 Movement and dispersal Dispersal and migration are important adaptive strategies in the Colorado potato beetle (Boiteau et al., 2003; Boiteau and Heikkila, 2013). Similar to diapause, migration in this species is facultative. When environmental conditions are benign, the beetles often spend their entire lives in the general vicinity of the place of their larval development (Grafius, 1995). However, when the need arises, they are also capable of traveling over considerable distances. For example, the beetles repeatedly invaded Jersey Island, located 20 km off the French coast, arriving both by flight and by being carried by sea currents (Small, 1948; Small and Thomas, 1954). Incursions across the Baltic Sea to Scandinavia imply that, given favorable wind speed and direction, Colorado potato beetles can fly more than 100 km (Wiktelius, 1981). Also, a group of beetles was recorded landing on the deck of a ship 110 km away from the nearest shore (van Poeteren, 1939). The Colorado potato beetle has three distinct types of flight that play different ecological roles in its life history (Voss and Ferro, 1990a). A low-altitude flight with frequent turning within the host habitat serves to distribute eggs within a field, to find mates, or to move onto less defoliated host plants. A straight, often downwind flight over a distance of several hundred meters or more is used for colonization of new areas; it is a true migratory flight that is not interrupted by the presence of suitable habitats in the vicinity of the beetle’s place of origin (Caprio and Grafius, 1990). Diapause flight is a low altitude, directed flight toward tall vegetation bordering potato fields. The flying beetles arrive in wooded hedgerows, where they immediately burrow into the soil to diapause (Voss and Ferro, 1990a). Both male and female beetles engage in flights of all three types (Weber and Ferro, 1994a). As discussed above, gender and reproductive status may affect their propensity to fly. However, studying beetle flight under field conditions is difficult, and there was considerable variation in the collected data. Voss and Ferro (1990b) showed that significantly more males than females engaged in local flight activity, possibly in search of mates. Hough-Goldstein and Whalen (1996) reported that almost twice as many overwintered males immigrated into fields by flight compared to overwintered females, although a portion of their data probably reflected local flight activity, especially later in the season (Voss and Ferro, 1990a; HoughGoldstein and Whalen, 1996). Also, Weber and Ferro (1994b) found that overwintered males departed from a non-host habitat more readily than females, but were more likely to remain in a potato field than females. On the contrary, Zehnder and Speese (1987) reported a 50:50 sex ratio of beetles caught in windowpane traps throughout the growing season. Movement by flight is instrumental for the Colorado potato beetle to be able to colonize new habitats and escape from hostile environments. It also ensures gene flow between isolated populations. Walking is relatively less important because beetles are able to walk only several hundred meters at a relatively low speed (Ng and Lashomb, 1983). However, it plays a role in beetle dispersal within already-colonized host habitats and for movement between host habitats and overwintering sites. Colorado potato beetles are a terrestrial species. Therefore, they normally avoid bodies of water (Boiteau and MacKinley, 2017). Nevertheless, they can float on water surface and even actively swim, although at a slow speed. Floating beetles survive for up to 10 days (Dunn, 1949; Boiteau and MacKinley, 2017), although their survivorship is significantly higher in fresh water than in salt water (Boiteau and MacKinley, 2017). The beetles can also survive submergence for up to 16.5 h and can walk under water (Boiteau and MacKinley, 2017). As a result, while water bodies serve as barriers to beetle dispersal, this barrier is not unsurmountable.

4.9 Management implications Different approaches to Colorado potato beetle control are discussed in Part III (Chapters 11e15). However, it is extremely important to realize that no single technique will ever provide a lasting solution for managing this insect. A complex and diverse life history makes the Colorado potato beetle a challenging pest to suppress. The beetles integrate diapause, dispersal, feeding, and reproduction into an ecological “bet-hedging” strategy, distributing their offspring in both space (within and between host plants and host habitats) and time (within and between seasons). They are also extremely adaptable to adverse conditions, including human attempts of their control (Chapter 24). Yet, humans historically rely on a very rigid and simplistic set of techniques, which is largely limited to spraying insecticides. Thirty-five years ago, Casagrande (1987) described the long history of Colorado potato beetle control as “135 years of mismanagement.” Unfortunately, the situation is no different at present. Even replacing insecticides with non-chemical methods described later in this book will never provide sustainable means for controlling this pest. In order to succeed, we need to become as flexible and adaptable as the Colorado potato beetle itself. The only option for the economically sound and environmentally friendly protection of potato crops is the science-based integration of multiple control techniques into a comprehensive and dynamic pest management approach.

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Crossley, M.S., Rondon, S.I., Schoville, S.D., 2019. Patterns of genetic differentiation in Colorado potato beetle correlate with contemporary, not historic, potato land cover. Evol. Appl. 12, 804e814. Crossley, M.S., Rondon, S.I., Schoville, S.D., 2018. A comparison of resistance to imidacloprid in Colorado potato beetle (Leptinotarsa decemlineata Say) populations collected in the Northwest and Midwest U.S. Am. J. Potato Res. 95, 495e503. de Kort, C.A.D., 1990. Thirty-five years of diapause research with the Colorado potato beetle. Entomol. Exp. Appl. 56, 1e13. de Kort, C.A.D., Koopmanschap, A.B., Vermunt, A.M.W., 1997. Influence of pyriproxifen on the expression of haemolymph protein genes in Colorado potato beetle, Leptinotarsa decemlineata. J. Insect Physiol. 43, 363e371. de Wilde, J., 1948. Developpement embryonnaire et postembryonnaire dy doryphore (Leptinotarsa decemlineata Say) en function de la temperature. 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Izzo, V.M., Hawthorne, D.J., Chen, Y.H., 2014a. Geographic variation in winter hardiness of a common agricultural pest, Leptinotarsa decemlineata, the Colorado potato beetle. Evol. Ecol. 28, 505e520. Izzo, V.M., Armstrong, J., Hawthorne, D., Chen, Y., 2014b. Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore, Leptinotarsa decemlineata. Ecol. Entomol. 39, 75e82. Izzo, V.M., Chen, Y.H., Schoville, S.D., Wang, C., Hawthorne, D.J., 2018. Origin of pest lineages of the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 111, 868e878. Jacobson, J.W., Hsiao, T.H., 1983. Isozyme variation between geographic populations of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 76, 162e166. Jacques, R.L., 1972. Taxonomic Revision of the Genus Leptinotarsa (Coleoptera: Chrysomelidae) of North America. Ph.D. dissertation. Purdue University, West Lafayette, Indiana. Jacques, R.L., 1988. The Potato Beetles. E. J. Brill, Leiden, Netherlands. Jermy, T., 1953. Egyszerü módszer a burgonyabogár lárvák fejdlödése fikozatainak megkülönböztetésére. Növényvéd. Idösz. Kérd. 2, 17e18. Jermy, T., Saringer, G., 1955. A Burgonyabogár (Leptinotarsa decemlineata Say). Mezögazd Kiadó, Budapest, Hungary. Jermy, T., Butt, B.A., 1991. Method for screening female sex pheromone extracts of the Colorado potato beetle. Entomol. Exp. Appl. 59, 75e78. Jermy, T., Szentesi, A., Horvath, J., 1988. Host plant finding in phytophagous insects - the case of the Colorado potato beetle. Entomol. Exp. Appl. 49, 83e98. Jolivet, P., 1991. The Colorado beetle menaces Asia (Leptinotarsa decemlineata Say 1824)(Col. Chrysomelidae). L’Entomologiste 47, 29e48. Kalinina, K.V., Nikolaeva, Z.V., 2007. Evaluation of potato varieties for resistance to Colorado potato beetle in North-West Russia. Kartofel and Ovoshchi 8, 16e18 (In Russian). Kaplaneck, P., 1953. Beobachtungen uber melanismus beim kartoffelkafer (Leptinotarsa decemlineata say). Nachrichtenbl. Dtsch. Pflanzenschutzdienst 7, 56e58. Lactin, D.J., Holliday, N.J., 1994. Behavioral responses of Colorado potato beetle larvae to combinations of temperature and insolation, under field conditions. Entomol. Exp. Appl. 72, 255e263.

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Landolt, P.J., Tumlinson, J.H., Alborn, D.H., 1999. Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environ. Entomol. 28, 973e978. Lashomb, J.H., Ng, Y.S., 1984. Colonization by the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) in rotated and non-rotated potato fields. Environ. Entomol. 13, 1352e1356. Lehmann, P., Lyytinen, A., Piiroinen, S., Lindström, L., 2015. Latitudinal differences in diapause related photoperiodic responses of European Colorado potato beetles (Leptinotarsa decemlineata). Evol. Ecol. 29, 269e282. Lockwood, J.A., 2009. Six-Legged Soldiers. Oxford University Press, New York. Logan, J.A., Wollkind, D.T., Hoyt, J.C., Tanigoshi, L.K., 1976. An analytic model for description of temperature dependent rate phenomena in arthropods. Environ. Entomol. 5, 1130e1140. Logan, P.A., Casagrande, R.A., Faubert, H.H., Drummond, F.A., 1985. Temperature-dependent development and feeding of immature Colorado potato beetles, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Environ. Entomol. 14, 275e283. Lyytinen, A., Mappes, J., Lindström, L., 2012. Variation in Hsp70 levels after cold shock: signs of evolutionary responses to thermal selection among Leptinotarsa decemlineata populations. PLoS One 7 (2) e31446. Margus, A., Lindström, L., 2020. Prolonged diapause has sex-specific fertility and fitness costs. Evol. Ecol. 34, 41e57. May, M.L., 1981. Role of body temperature and thermoregulation in the biology of the Colorado potato beetle. In: Lashomb, J., Casagrande, R. (Eds.), Advances in Potato Pest Management. Dowden, Hutchinson & Ross, New York, pp. 86e104. McIndoo, N.E., 1926. An insect olfactometer. J. Econ. Entomol. 19, 545e571. Medvedev, L.N., 1981. Systematic status of Leptinotarsa decemlineata Say within the family Crysomelidae, phylogeny, evolution of the species. In: Ushatinskaya, R.S. (Ed.), The Colorado Potato Beetle, Leptinotarsa decemlineata Say. Nauka Publishers, Moscow, Russia, pp. 27e34 (In Russian). Minder, I.F., Petrova, D.V., 1966. Ecological and physiological characteristics of the summer rest of the Colorado beetle. In: Arnoldi, K.V. (Ed.), Ecology and Physiology of Diapause in the Colorado Beetle. Nauka, Moscow, Russia, pp. 257e279. Nault, B.A., Kennedy, G.G., 1998. Limitations of using regression and mean separation analyses for describing the response of crop yield to defoliation: a case study of the Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 91, 7e20. Ng, Y.S., Lashomb, J.H., 1983. Orientation by the Colorado potato beetle (Leptinotarsa decemlineata Say). Anim. Behav. 31, 617e618. Orsetti, D.M., Rutowski, R.L., 2003. No material benefits, and a fertilization cost, for multiple mating by female leaf beetles. Anim. Behav. 66, 477e484. Ovchinnikova, N.A., Markelov, G.V., 1982. 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Colorado potato beetle microsymbionts Enterobacter BC-8 inhibits defense mechanisms of potato plants using crosstalk between jasmonate- and salicylate-mediated signaling pathways. Arthropod. Plant Interact. 14, 161e168. Sorokan, A., Cherepanova, E., Burkhanova, G., Veselova, S., Rumyantsev, S., Alekseev, V., Mardanshin, I., Sarvarova, E., Khairullin, R., Benkovskaya, G., Maksimov, I., 2020b. Endophytic Bacillus spp. as a prospective biological tool for control of viral diseases and non-vector Leptinotarsa decemlineata Say in Solanum tuberosum L. Front. Microbiol. 11, 2433. Stål, C., 1865. Till kannedomen om Amerikas chrysomeliner. Ofv. Svenska Vet.-Akad. Forh. 15, 469e478. Stegwee, D., Kimmel, E.C., de Boer, J.A., Henstra, S., 1963. Hormonal control of reversible degeneration of flight muscle in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera). J. Cell Biol. 19, 519e527. Stieha, C., Poveda, K., 2015. Tolerance responses to herbivory: implications for future management strategies in potato. Ann. Appl. Biol. 166, 208e217. Suffrian, E., 1858. Ubersicht der in den Verein. Staaten von Nord-Amerika einheimischen Chrysomelen. Stettiner Ent. Zeitung 19, 237e278. Szafranek, B., Chrapkowska, K., Waligora, D., Palavinskas, R., Banach, A., Szafranek, J., 2006. Leaf surface sesquiterpene alcohols of the potato (Solanum tuberosum) and their influence on Colorado beetle (Leptinotarsa decemlineata Say) feeding. J. Agric. Food Chem. 54, 7729e7734. Szentesi, A., 1985. Behavioral aspects of female guarding and inter-male conflict in the Colorado potato beetle. In: Ferro, D.N., Voss, R.H. (Eds.), Proceedings, Symposium on the Colorado Potato Beetle. XVIIth International Congress of Entomology, Research Bulletin 704, pp. 127e137. Tauber, M.J., Tauber, C.A., 2002. Prolonged dormancy in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): a ten-year field study with implications for crop rotation. 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Thibout, E., 1982. Le comportement sexuel du doryphore, Leptinotarsa decemlineata say et son possible controle par l’hormone juvenile et les corps allates. Behaviour 80, 199e217. Thiery, D., Visser, J.H., 1986. Masking of host plant odour in the olfactory orientation of the Colorado potato beetle. Entomol. Exp. Appl. 41, 165e172. Thiery, D., Visser, J.H., 1995. Satiation effects on olfactory orientations patterns of Colorado potato beetle females. Comptes Rendus Academ. Sci. Ser. Life Sci. 318, 105e111. Tigreros, N., Norris, R.H., Wang, E.H., Thaler, J.S., 2017. Maternally induced intraclutch cannibalism: an adaptive response to predation risk? Ecol. Lett. 20, 487e494. Tower, W.L., 1906. An investigation in evolution in Chrysomelid beetle of the genus Leptinotarsa. Publ. Carnegie Inst. Wash. 48, 1e320. Tower, W.L., 1918. The Mechanism of Evolution in Leptinotarsa. Carnegie Institution of Washington, Washington, DC, p. 384. Trouvelot, B., 1936. Remarques sur l’ecologie du doryphore en 1935 dans le massif central et le centre de la France. Rev. Zool. Agr. Appl. 25, 33e37. Udalov, M.B., Benkovskaya, G.V., Khusnutdinova, E.K., 2010. Population structure of the Colorado potato beetle in the southern Urals. Russ. J. Ecol. 2, 126e133. Ushatinskaya, R.S., 1961. Summer diapause and second winter diapause in the Colorado potato beetle in Transcarpathia. Dokl. AN USSR 5, 1189e1191 (In Russian). Ushatinskaya, R.S., 1962. Colorado potato beetle diapause and development of its multi-year infestations. Zashchita Rastenii (Mosc.) 6, 53e54 (In Russian). Ushatinskaya, R.S., 1966. Prolonged diapause in the Colorado beetle and conditions of its development. In: Arnoldi, K.V. (Ed.), Ecology and Physiology of Diapause in the Colorado Beetle. Nauka, Moscow, Russia, pp. 120e143 (In Russian). van Poeteren, N., 1939. Die Entwicklung der Kartoffelkafer. Frage in Niederlanden. In: Verh. VII Intern. Kongr. Entomol. Berlin, 1938, pp. 2701e2703. 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Isolation and identification of volatiles in the foliage of potato, Solanum tuberosum, a host plant of the Colorado beetle, Leptinotarsa decemlineata. J. Chem. Ecol. 5, 13e25. Vlasova, V.A., 1978. A prediction of the distribution of Colorado beetle in the Asiatic territory of the USSR. Zashchita Rastenii (Mosc.) 6, 44e45. Voss, R.H., Ferro, D.N., 1990a. Phenology of flight and walking by Colorado potato beetle (Coleoptera: Chrysomelidae) adults in western Massachusetts. Environ. Entomol. 19, 117e122. Voss, R.H., Ferro, D.N., 1990b. Ecology of migrating Colorado potato beetles (Coleoptera: Chrysomelidae) in western Massachusetts. Environ. Entomol. 19, 123e129. Walsh, B.D., 1865. The new potato bug and its natural history. Pract. Entomol. 1, 1e4. Weber, D.C., Duan, J.J., Haber, A.I., 2020. Male Colorado potato beetles alter search behavior in response to prior female presence on potato plants. J. Pest. Sci. 93, 595e604. Weber, D.C., Ferro, D.N., 1993. Distribution of overwintering Colorado potato beetle in and near Massachusetts potato fields. Entomol. Exp. Appl. 66, 191e196. Weber, D.C., Ferro, D.N., 1994a. Colorado potato beetle: diverse life history poses challenge to management. In: Zehnder, G.W., Jansson, R.K., Powelson, M.L., Raman, K.V. (Eds.), Advances in Potato Pest Biology and Management. APS Press, St. Paul, MN, pp. 54e70. Weber, D.C., Ferro, D.N., 1994b. Movement of overwintered Colorado potato beetles in the field. J. Agric. Entomol. 11, 17e27. Weber, D., 2003. Colorado beetle: pest on the move. Pestic. Outlook 14, 256e259. Wegorek, W., 1955. Investigation on spring migration of the Colorado beetle (Leptinotarsa decemlineata Say) and possibilities of combating the insect. Ecol. pol. Ser. A 3, 217e271. Wegorek, W., 1957a. Badania nad biologia i ekologia stonki ziemniaczanej (Leptinotarsa decemlineata Say). Rocz. Nauk Roln. 74, 135e185. Wegorek, W., 1957b. 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Yocum, G.D., Rinehart, J.P., Larson, M.L., 2011. Monitoring diapause development in the Colorado potato beetle, Leptinotarsa decemlineata, under field conditions using molecular biomarkers. J. Insect Physiol. 57, 645e652. Zehnder, G., Speese III, J., 1987. Assessment of color response and flight activity of Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) using window flight traps. Environ. Entomol. 16, 1199e1202. Zehnder, G.W., Evanylo, G.K., 1989. Influence of Colorado potato beetle sample counts and plant defoliation on potato tuber production. Am. Potato J. 65, 725e736. Zehnder, G.W., Sandall, L., Tisler, A.M., Powers, T.O., 1992. Mitochondrial DNA diversity among 17 geographic populations of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 85, 234e240. Zehnder, G., Vencill, A.M., Speese III, J., 1995. Action thresholds based on plant defoliation for management of Colorado potato beetle (Coleoptera: Chrysomelidae) in potato. J. Econ. Entomol. 88, 155e161. Zeleev, R.M., 2002. Evaluation of polymorphism of pronotum and elytra patterns of the Colorado potato beetle, Leptinotarsa decemlineata, in the vicinity of Kazan. Zool. J. 3, 316e322 (in Russian).

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Chapter 5

Aphids Andrei Alyokhina, Erik J. Wenningerb and Andy Jensenc a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bDepartment of Entomology, Plant Pathology, and Nematology,

University of Idaho, Kimberly Research & Extension Center, Kimberly, ID, United States; cWashington State Potato Commission, Moses Lake, WA, United States

5.1 Basic biology 5.1.1 Taxonomy The aphids belong to the order Hemiptera, which is a large and diverse group of hemimetabolous insects that have unique piercing-sucking mouthparts (Triplehorn and Johnson, 2005). The order is subdivided into three suborders: Heteroptera (true bugs), Auchenorrhyncha (cicadas, leafhoppers, and planthoppers), and Sternorrhyncha. Aphids belong to the suborder Sternorrhyncha, which they share with the psyllids (Psylloidea), whiteflies (Aleyrodoidea), and scale insects (Coccoidea) (Blackman and Eastop, 2000). There are currently over 5100 recognized species of aphids (Aphididae) (Favret, 2020).

5.1.2 Morphology Aphids are small, mostly soft bodied insects, with adults of most species ranging in length from about 0.5 to 7 mm and some tree-feeding species nearing 10 mm. They specialize on phloem-feeding, with a small number of species specializing on non-vascular plants such as mosses (Blackman and Eastop, 2000). A key and easily seen morphological feature shared by most aphids is a pair of variously shaped siphunculi (a.k.a. cornicles) on the abdomen; these can be long and cylindrical, short and trunk-shaped, simple flat pores, and other shapes. Almost all winged aphids, when at rest, hold their wings over the body in a roof-like position (as opposed to laid flat as in many other insects). Two common potato-infesting species shown in Fig. 5.1 illustrate these and other features of aphids. Because of their small size and soft bodies, aphids are cleared and mounted on microscope slides for morphological study. Fig. 5.2 shows a typical slide preparation of an Aphis fabae Scopoli (the black bean aphid) and illustrates key features of aphid morphology. Among the thousands of aphid species, there are many ways of life that relate to diverse morphology. Most aphids are host-specific, able to feed and reproduce on only one or a handful of plant species (Blackman and Eastop, 2000). Many familiar pest aphids, however, are examples of “polyphagous” feeding biology, that is, they can develop on many plant species (e.g., Macrosiphum). Most aphids are free-living on their host plants, some living above-ground on stems, petioles, and/or leaves, whereas others live on below-ground parts including crowns, rhizomes, and roots. Some aphids can induce their host plants to create various growth deformities inside which the aphids live. These include curled single leaves, groups of leaves bunching together, and stems, leaves, or petioles developing into specialized cavities called galls. Freeliving, above ground species tend to have longer legs and antennae and readily walk or run, but a few specialized groups are almost sedentary, strongly resembling whitefly nymphs or scale insects (e.g., Aleurodaphis and Cerataphis). The many gall-feeding aphids (such as in the subfamily Eriosomatinae) tend to have short legs and antennae with large globose bodies and limited mobility.

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00012-3 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 5.1 Aphids. (A) Myzus persicae apterous viviparous female; (B) Macrosiphum euphorbiae apterous viviparous female; (C) Macrosiphum euphorbiae alate viviparous female.

5.1.3 Life cycles Aphids have several unusual or unique biological features that are adaptive to their environments and often allow an extremely rapid build-up in their numbers. More specifically, they are all parthenogenetic and viviparous, with telescoping generations and seasonal polyphenism (for more details, see Blackman, 1974 and Dixon, 1997). Terms describing their rather complicated life cycles are defined in Table 5.1. Parthenogenesis is the reproductive strategy wherein females produce offspring that are genetic copies of themselves without mating with males. As a result, assemblages of aphids in the field are usually comprised of genetically identical clones that consist of the progeny of single mothers. As discussed in Chapter 24, this has important evolutionary implications, in particular in relation to insecticide resistance development in agricultural fields. All aphids display parthenogenesis, but most also have one generation per year of sexual reproduction (see below for description and Fig. 5.3 for graphical representation).

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FIG. 5.2 Cleared and slide-mounted apterous viviparous female of Aphis fabae, with morphological features important in species recognition labeled. These features and important aspects of them in aphid taxonomy: (A) Antennae: number of segments, lengths, and pigmentation; (B) Front of the head: shape, prominence of the “antennal tubercles” on which the antennae are mounted; (C) Rostrum (mouthparts): shape and length; (D) Leg: length of segments, pigmentation; (E) Siphunculus: length, pigmentation, ornamentation; (F) Cauda: length, pigmentation, hairs; (G) Pigmentation: color, size, and distribution of markings on the body.

TABLE 5.1 Glossary of terms used to describe aphid morphs and life cycles. Term

Definition

Parthenogenesis

Reproductive strategy wherein females produce offspring from unfertilized eggs without mating with males

Viviparity

Practice of giving birth to live offspring

Oviparity

Practice of laying eggs

Seasonal polyphenism

Ability to produce throughout the season multiple types of adults that differ in morphology, physiology, and behavior

Apterous

Wingless

Alate

Winged

Ovipara

Egg-laying female aphid

Fundatrix

Viviparous female aphid that hatches from the egg in spring

Virginopara

Parthenogenetic viviparous female aphid that produces more parthenogenetic females

Gynopara

Parthenogenetic viviparous female aphid that produces the sexual generation comprised of males and females

Heteroecious life cycle

Overwintering host plant species are different from summer host plant species

Autoecious life cycle

Overwintering and summer host plant species are the same

Anholocyclic life cycle

Sexually reproducing stage is absent; populations consist only of virginoparae

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FIG. 5.3 Heteroecious life cycle of the green peach aphid, Myzus persicae (Sulzer). For most of an annual life cycle, green peach aphids are present as parthenogenic females. In areas with seasonal climates, this aphid species overwinters as eggs on trees in the Prunus genus. Wingless aphids hatch from these eggs in the spring and go through several generations on the same trees where they spent winter. As their densities increase, winged forms are produced, which then move to summer, usually herbaceous, hosts. Their offspring are mostly wingless, although winged forms may be again produced, especially when aphid density increases or plant condition deteriorates. Multiple generations are produced during the summer. In the fall, short day length and lower temperatures induce production of winged males and females. These move back to the Prunus overwintering hosts. Females arrive first and give birth to wingless females, which then mate with the subsequently arriving males and lay overwintering eggs, thus completing the life cycle.

Viviparity is the practice of giving birth to live young. It contrasts with oviparity, which is the practice of laying eggs that is by far more common among insects. All aphids (family Aphididae) display at least one generation per year of viviparity, but most also have one generation per year of oviparity (egg-laying; see below). Telescoping generations is a phenomenon in which viviparous female aphids contain developing young from an early age. In fact, most aphids are pregnant when they are born. Female aphids often begin to deposit offspring within a few hours after molting to the adult stage. Seasonal polyphenism refers to aphids’ ability to produceddepending on environmental conditionsdmultiple types of adults through the season. Most aphids are without wings, or “apterous,” though almost all aphid species can also produce winged, or “alate,” females. A single female aphid can produce offspring that are genetically identical but are a mix of wingless and winged individuals. Other specialized forms include the viviparous female that hatches from the egg in spring, known as the fundatrix; the fundatrix can resemble others of her species or have distinct morphology and extreme reproductive capacity. Finally, most aphid species can produce males and egg-laying females; males can be either winged or wingless depending on the species, and egg-laying females are almost always wingless. A parthenogenetic viviparous aphid that produces the sexual generation is known as gynopara, an egg-producing female is known as ovipara, while a parthenogenetic female that produces more parthenogenetic females is known as virginopara. As described in the next paragraph, these types of adults alternate in a more-or-less orderly manner throughout a season, completing an aphid life cycle. Aphid species are generally divided into three life cycle strategies known as heteroecious, autoecious, and anholocyclic. Heteroecious aphids are also known as migratory or host-alternating. These species overwinter as eggs on a woody shrub, vine, or tree. Eggs hatch and two or a few generations develop on that host. Then, a generation will form that is mostly or entirely winged, and those females migrate to completely unrelated species of plants and reproduce on them throughout a growing season. The majority of the offspring produced by the spring migrants is wingless, but a few winged individuals are produced throughout the summer. The production of winged summer migrants is encouraged by overcrowding and poor quality of host plants (Sutherland and Mittler, 1971; Hodjat and Bishop, 1978; Radcliffe et al., 1993; Muller et al., 2001). Finally, a special kind of winged female and winged males are produced, usually in response to changes in photoperiod, often also modulated by temperature (MacGillivray and Anderson, 1964; Lamb and MacKay, 1997). These migrate back to the woody host, where the males mate with egg-laying females that were given birth by the migrating alate

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females. Such a complicated life cycle allows combining a propensity for rapid population growth through parthenogenic reproduction and telescoping generations with maintaining genetic diversity through sexual reproduction. Autoecious aphids lack this alternation between unrelated host plants. However, they still have a similar biology of overwintering eggs, wingless and winged females throughout the growing season, and then males and egg-laying females in the fall. Anholocyclic aphids survive completely without sexual reproduction, having only wingless and winged females. Species with this strategy live in warm climates or indoors. Some aphids can be facultatively anholocyclic when living in warm places.

5.1.4 Diversity of aphids affecting potato Aphids are a ubiquitous and cosmopolitan group of insects with many interesting morphological and physiological characteristics, as well as a large economic importance. Most crops, including potatoes, have at least one or more associated aphid species that are considered to be pests. Aphids can damage their host plants through direct feeding on the phloem sap of the plant, by transmitting viruses to plants, or by contaminating the harvested product with their excrement known as honeydew. Potato is affected by aphids in the first two of these ways, with spreading viral diseases being the more important of the two. The vast majority of aphid species are restricted to Northern Hemisphere temperate environments, in contrast to other insect groups, which are more diverse in the tropics (Dixon, 1997). In cool-climate potato producing regions in the North, there are hundreds of aphid species living in the landscape around most potato fields. As an example, in just several days of collecting, 90 aphid species were found in the areas surrounding potato fields in two potato-producing counties of Washington State, USA (Jensen, unpublished); many more species could have been found with additional collecting effort. Almost all these species are host-specific on plants other than potato and cannot successfully colonize and reproduce on potato. In fact, many aphid species feed only on trees and shrubs and are rarely seen in or near agricultural landscapes. The subfamily Aphidinae, however, is diverse and abundant, feeding on both woody and herbaceous plants in and around agricultural systems. Blackman and Eastop (2000) list 14 colonizing species that are known to feed and reproduce on potato, 12 of which are members of Aphidinae and two of Eriosomatinae (Table 5.2). Many other species can still be important to potato as vectors of viruses as described later in this chapter. However, they do not colonize potato plants because they are not suitable for them as hosts, possibly because of the high contents of glycoalcoloids in their foliage (see Chapter 14 for more information on host plant resistance). All the important pest aphids of potato (both colonizing and non-colonizing) belong to the Aphidinae. Any given production area will usually have one or two aphids commonly colonizing potato, a few others capable of colonizing, and dozens of possible virus vector species that cannot colonize potato but that commonly visit potato fields in search of proper hosts (e.g., DiFonzo et al., 1997). In the United States and Canada, for example, potato aphid, Macrosiphum euphorbiae (Thomas); green peach aphid, Myzus persicae (Sulzer); and buckthorn aphid, Aphis nasturtii Kaltenbach, are the most usual colonizers of potato plants. Foxglove aphid, Aulacorthum solani (Kaltenbach), is also capable of developing on potato, but it is by far less common than the other three species (Radcliffe et al., 1993).

5.1.5 Population growth and regulation Populations of many aphid species, including potato-colonizing species, have a high intrinsic propensity for growth, which is greatly aided by parthenogenic reproduction and telescoping generations. Furthermore, aphids have short generation times. Under optimal temperatures, newborn Myzus persicae Sulzer, the green peach aphids, reach adulthood in 6e7 days (Liu and Meng, 1999), while newborn buckthorn aphids mature in 6e8 days (Wang et al., 1997). Population growth rates in aphids are driven more by the rates of their development than by their fecundity. Also, the number of offspring produced early in aphid life is more important for realizing its full reproductive potential than total reproductive capability (Dixon, 1997). Growth of aphid populations follows a near-exponential trajectory in the beginning of a season, usually followed by an abrupt crash (Dixon, 1994). Aphids are highly vulnerable to a variety of external factors, such as unfavorable weather conditions, predation, and parasitism. Alyokhin et al. (2005) found strong evidence of density-dependent regulation for the populations of buckthorn aphid, potato aphid, and green peach aphid on potatoes in northern Maine, USA. There was also evidence of regular population cycles for buckthorn aphids and green peach aphids, but not for potato aphids. Further investigations (Alyokhin et al., 2011) suggested that potato aphids were negatively affected by both fungal disease and predators, while buckthorn aphids were negatively affected by predators only. Parasitoids did not have a noticeable effect

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TABLE 5.2 Aphids considered to be able to colonize potato, including their life cycles (Blackman and Eastop 2020). All these aphids are distributed almost worldwide, some affecting potato in most of the world, others affecting potato rarely or only in certain regions. Species: Scientific name and common name(s)

Life cycle; Primary host(s)

Aphis fabae Scopolia Black bean aphid

Heteroecious or anholocyclic; Euonymus, Philadelphus, Viburnum

Aphis frangulae Kaltenbacha

Heteroecious or anholocyclic; Rhamnus

Aphis nasturtii Kaltenbacha Buckthorn-potato aphid

Heteroecious or anholocyclic; Rhamnus

Aphis spiraecola Patcha Spiraea aphid; green citrus aphid

Heteroecious or anholocyclic; Spiraea, Citrus

Aulacorthum solani (Kaltenbach)a Foxglove aphid

Autoecious or anholocyclic

Macrosiphum euphorbiae (Thomas)a Potato aphid

Heteroecious or anholocyclic; Rosa

Myzus ascalonicus Doncastera Shallot aphid

Anholocyclic

Myzus ornatus Lainga Violet aphid

Anholocyclic

Myzus persicae (Sulzer)a Green peach aphid; peach potato aphid

Heteroecious or anholocyclic; Prunus

Neomyzus circumflexus (Buckton)a Mottled arum aphid

Anholocyclic

Pemphigus sp.b; secondary host forms, not identifiable to species

Heteroecious or anholocyclic; Populus

Rhopalosiphoninus latysiphon (Davidson)a Bulb-and-potato aphid

Apparently anholocyclic

Rhopalosiphum rufiabdominalis (Sasaki)a Rice root aphid

Heteroecious or anholocyclic; Prunus

Smynthurodes betae Westwoodb Bean root aphid

Heteroecious or anholocyclic; Pistacea

a

Aphidinae Eriosomatinae From: Blackman, R.L., Eastop, V.F., 2000. Aphids on the World’s Crops. John Wiley & Sons, Ltd., West Sussex, U.K. 466 pp. b

on the growth of any of the three aphid species. Growth of green peach aphid populations was negatively influenced by interspecific interactions with the other two aphid species. Density-independent weather factors, such as temperature and precipitation, also affected population growth, either directly or through natural enemies. However, their effects were less pronounced compared to the effects of predators and diseases (Alyokhin et al., 2011). During the last 30 years, populations of buckthorn aphid and green peach aphid experienced a significant reduction in both density and annual oscillations compared to their historic averages. No such trend was noticeable for the populations of potato aphids (Alyokhin et al., 2005). The observed decline was likely caused, at least in part, by the establishment of an exotic Asian lady beetle, Harmonia axyridis (Pallas), which is a more voracious aphid predator compared to the native lady beetle species (Alyokhin and Sewell, 2004; Finlayson et al., 2010; Leppanen et al., 2012). Aphid populations currently remain low, while the Asian lady beetle is still a dominant species (Alyokhin, unpublished).

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5.1.6 Movement and dispersal Migration and dispersal have important ecological implications for living organisms. In the case of aphids, these factors also have large economic significance because of the ability of aphids to transmit plant viruses. Under certain conditions, winged aphids can fly up to several hundreds of kilometers via air currents (Dickson, 1959; Close and Tomlinson, 1975; Hardy and Cheng, 1986). However, the frequency of such long-distance movement appears to be fairly low, and most movement is likely to happen on a much more limited spatial scale (Garrett and McLean, 1983; Loxdale et al., 1993). Migration is a costly strategy, both in terms of uncertainty and energy expense (Rankin et al., 1986; Loxdale et al., 1993; Ward et al., 1998). Therefore, it can be argued that the progeny of migrating aphids that land on potato plants should remain on the same plants as long as they are provided with an adequate food supply. By using radiolabeled green peach aphids, Harrewijn et al. (1981) determined that a considerable percentage of winged summer migrants performed only short-distance flights (1e100 m) that did not remove them from the field of origin. However, yellow cards used in their experiment tend to overestimate landing rates because they are highly attractive to aphids (Irwin, 1980). Other studies have shown that a certain proportion of potato-colonizing aphids disperse even under generally favorable conditions. Hodgson (1978) described frequent intraplant movement of green peach aphids, presumably to find more suitable feeding sites on rapidly growing plants. Boiteau (1997) completed a series of laboratory experiments comparing propensity for dispersal of winged and wingless morphs of potato, buckthorn, and green peach aphids. Both winged and wingless individuals of all three species were fairly mobile, with up to 47% of monitored individuals moving over a 24-h period from an excised potato leaflet to another leaflet located 17.5 cm away. Alyokhin and Sewell (2003) reported that wingless aphids of these three species did not voluntarily leave potato plants and, when forcibly removed and released on the soil surface, re-colonized plants within 1 hour. However, in the absence of other choices, a significant proportion of aphids was capable of walking over bare ground for up to 180 cm between the point of release and the nearest host plant. Potato aphid, which is the largest of the three species, was the most mobile. Narayandas and Alyokhin (2006a) also showed that wingless potato aphids moved between potato plants even when canopies did not overlap. In that study, aphids preferentially moved within the rows of potato plants, but there was also considerable movement over bare soil between the rows. Aphid dispersal is likely to be influenced by many biotic and abiotic factors. For example, it has been shown that wind, herbicide applications, coccinellid predators, crowding, mechanical disturbance, drought, and virus infection affect movement of bird cherry oat aphid, Rhopalosiphum padi (L.), and spread of barley yellow dwarf virus in oats (Bailey et al., 1995). Similarly, for wingless potato aphids simulated rain encouraged movement between plants with non-overlapping canopies, while simulated wind, simulated rain, and mechanical raking significantly enhanced movement between plants with overlapping canopies in greenhouse arenas (Narayandas and Alyokhin, 2006a).

5.2 Interactions with host plants 5.2.1 Host finding, recognition, and acceptance Aphids face considerable challenges in finding suitable host plants (Powell et al., 2006). For example, most aphids feed on one or a few closely related species, and the suitable host range differs considerably for gynoparae seeking primary hosts and virginoparae seeking secondary hosts. Moreover, the small size and soft cuticles of aphids severely constrains the duration that they can survive off a host, and, as relatively weak flyers, aphids may have limited ability to take directed flight in wind speeds of more than 1 ms 1 (Hardie et al., 1996). These challenges are underscored by the estimation of Ward et al. (1998) that about 99% of winged dispersing bird cherry oat aphids fail to find a host. Aphids use different sensory modalities to find host plants, including olfaction, vision, and gustation. The complex stages involved in aphid host-finding behavior were modeled by Moericke (1955) and Kennedy (1966) following extensive experiments on green peach aphid and on black bean aphid, Aphis fabae Scopoli, respectively. Some early researchers expressed skepticism of the role of olfaction in host finding behavior (e.g., Kennedy et al., 1959a,b), despite some evidence of orientation to host odors by black bean aphids (Jones, 1944). However, a considerable body of evidence has since emerged demonstrating the use of olfactory cues (Pickett et al., 1992; Webster, 2012; Döring, 2014). Host recognition by herbivores may occur before (“pre-alighting”) and/or after (“post-alighting”) coming into physical contact with a host or prospective host (Bukovinszky et al., 2005). Although much of the information that aphids perceive from prospective hosts is gathered after landing on a plant (Powell et al., 2006), aphids generally are able to acquire some pre-alighting olfactory information on host suitability during flight (Gibson and Pickett, 1983; Döring, 2014). Such olfactory cues may serve as attractants, arrestants, or repellants. Olfactory cues used to distinguish hosts from non-hosts may include either volatiles

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that are characteristic of a host or species-specific blends of more ubiquitous plant volatiles (Visser, 1986; Webster, 2012; Döring, 2014). For example, certain isothiocyanate compoundsda signature of the Brassicaceaedhave been found to attract or arrest aphids that feed on brassicas (e.g., green peach aphid; Kan et al., 2002) and to repel aphids that do not (e.g., black bean aphid; Nottingham et al., 1991; Isaacs et al., 1993). Black bean aphid responses also demonstrate how blends of ubiquitous plant volatiles can be used in host orientation. Several such compounds identified from one of its hosts, broad bean (Vicia faba), were found to be repellant when presented individually at certain doses, but to exhibit attraction or arrestment when presented as a blend at those same doses (Webster et al., 2010). In some cases, aphids respond to certain concentrations of individual compounds and in other cases to the relative concentrations of a blend of compounds (Döring, 2014). Although the importance of volatile cues in host orientation has been clearly demonstrated in some species, the relatively narrow taxonomic coverage of such studies underscores the need for more investigations across species. In contrast with olfactory cues, the importance of visual cues in aphid host location has been long established. The first suggestive evidence of aphid response to color in green peach aphid (Moore, 1937) was later clearly demonstrated by Moericke (1950). Attractiveness to certain colors may be measured by behaviors including flying, landing, walking, or probing. Most aphids studied to date have shown attraction to yellow over green and red (Döring and Chittka, 2007; Döring, 2014), with some notable exceptions, including a stronger attraction in bird cherry oat aphid to green over yellow (Kieckhefer et al., 1976). However, given the different perception of colors between human observers and insects as well as the potentially confounding roles of light intensity and reflectance on relative color preferences, caution must be used in interpreting any responses to qualitatively described colors that do not include spectrometric measurements (Chittka and Döring, 2007). The perception of colors by aphids can be modeled as a function of the spectrum of the illumination source (i.e., sunlight), the reflectance spectrum of the object (e.g., a leaf), and the sensitivity of different photoreceptors in the aphid’s eyes (Chittka, 1992; Döring and Chittka, 2007). If the taxonomic coverage of olfaction studies in aphids has been limited, then the studies of aphid photoreceptors has been even more taxonomically narrow. Photoreceptor sensitivities have been characterized for a handful of species, including green peach aphid (Kirchner et al., 2005), the cabbage aphid Brevicoryne brassicae (Döring and Kirchner, 2007), and black bean aphid (Döring et al., 2011). Improved understanding of the perception of color by aphids should contribute to quantitative investigations into the influence of color on aphid behavior (Döring, 2014). Of course, host plants may be observed against a background of other color cues from the plant’s surroundings, including adjacent plants and the soil, and successive exposure to different colors has been shown to affect aphid responses (Moericke, 1950; Kirchner et al., 2005). Indeed, it has been thought that the contrast in color between a green target plant and a background of brown soil is an important factor in host detectability in agroecosystems (e.g., Moericke, 1955; Müller, 1964; Finch and Collier, 2003). Consistent with this hypothesis, Potato virus Y (PVY) incidence in potato has been reported to occur in higher incidence adjacent to larger stand gaps in potato fields (Davis et al., 2009), but the mechanisms that may underpin color contrast perception and behavioral responses in aphids warrant more rigorous experimentation (Döring, 2014). In addition, more studies are needed to clarify aphid responses to shape (e.g., Hodgson and Elbakhiet, 1985), which might also be used in conjunction with color and other cues in host orientation (Bruce et al., 2005; Reeves, 2011). Narayandas and Alyokhin (2006b) investigated circadian rhythmicity of potato aphid’s movement toward host plant odor in a series of laboratory experiments. Their results showed that both daytime and illumination facilitated host finding by the released aphids. The effect of illumination was smaller during the day than during the night. They concluded that potato aphid is a diurnal species regarding its movement toward host plants, and that the circadian rhythm in its hostfinding behavior is regulated by both exogenous and endogenous mechanisms. The effect of light also implies possible importance of visual cues in locating the hosts. However, a considerable proportion of tested aphids moved toward plant odor even in complete darkness. Finch and Collier (2000) hypothesized that insect pests of cruciferous crops are stimulated to land on green objects only after detection of appropriate volatiles from plants, with contact chemoreception then used to accept or reject the plant. This hypothesis might underestimate the importance of pre-alighting olfactory and visual cues in host assessment in some cases, though it is apparent that such signals from plants often are insufficient to fully assess host suitability (Prokopy and Owens, 1983; Powell et al., 2006). Following contact, but before stylet penetration, aphids may perceive cues from the leaf substrate that encourage or discourage settlingdincluding epicuticular waxes and trichomes as well as contact chemosensory and gustatory cuesdin addition to further assessing color and volatile chemical cues (Miller and Strickler, 1984; Goffreda et al., 1989; Smith and Severson, 1992; Powell et al., 1995, 1999, 2006). Aphids may even secrete and re-imbibe saliva on the leaf surface, allowing them to evaluate dissolved surface molecules with proboscis chemoreceptors before stylet penetration (Miles, 1999). It is unclear how important such pre-probing cues are for host selection.

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Despite the myriad mechanisms by which aphids may access host suitability before inserting their stylets into plant tissue, aphids may readily probedas a tarsal contact reflexd hosts, non-hosts, and even solid non-plant surfaces. Such probes may be mediated in part by various other factors, including olfactory cues, substrate topology, light exposure, and proximity to conspecifics (Ibbotson and Kennedy, 1959; Phelan and Miller, 1982; Powell et al., 1999, 2006). The first few stylet probes are typically brief, penetrating no further than the epidermis, from which aphids can ingest plant sap that can contact a gustatory organ on the interior of the stylet (Wensler and Filshie, 1969). These probes may be followed by aphid dispersal (host rejection) or continued probing, with aphids often then moving to the lower leaf surface (Calabrese and Edwards, 1976; Powell and Hardie, 2000). Longer probes (ca. 30e60 s) that follow are associated with penetration beyond the epidermis and into the mesophyll and parenchyma tissues (Bradley, 1952; Nault and Gyrisco, 1966). Electrical penetration graph (EPG) studies have revealed that further ingestion of plant sap, salivation, and gustatory discrimination may occur during probing and subsequent feeding behaviors (Powell et al., 2006). As the stylet moves into the plant tissue, cells are punctured, allowing for host quality assessment as well as perception of cues that orient the aphid within the different types of tissue that are encountered (Hewer et al., 2010). Different types of saliva are secreted at different stages of the feeding process (Miles, 1999; Prado and Tjallingii, 2007). For example, within the intercellular stylet pathway, a thick, congealing “sheath saliva” is secreted that encases the stylet bundle (Prado and Tjallingii, 2007). As cells are penetrated and phloem feeding begins, aphids alternate between secreting a watery saliva and ingesting plant sap (Prado and Tjallingii, 2007). A watery saliva is also secreted during stylet penetration of the sieve tube of the phloem and is thought to be involved in suppressing plant wound healing that would otherwise inhibit aphid feeding (Prado and Tjallingii, 1994; Will et al., 2007). Stylet probes that resulted in phloem acceptance and sustained ingestion were reported to take an average of 45 min for A. fabae, though this was after several probing attempts; thus, the total duration from initial encounter with a plant to sustained feeding may be ca. 4e5 h (Tjallingii, 1994). For potato aphid and green peach aphid on potato, time from initial encounter with a potato plant to initiation of phloem feeding was ca. 50e80 min (Boquel et al., 2011).

5.2.2 Phloem feeding Aphids feed nearly exclusively on phloem sap (Auclair, 1963), which presents challenges regarding osmotic pressure regulation, water balance, and assimilation of essential nutrients for growth and reproduction. With a high sugar concentration, primarily sucrose in many plants, phloem has an osmotic pressure approximately three times higher than that of an aphid’s body fluids; this should result in shriveling of an aphid’s body from water moving to the gut as the aphid ingests sap (Douglas, 2006). However, transformation of ingested sucrose to high concentrations of oligosaccharides reduces the osmotic pressure of the gut contents (Walters and Mullin, 1988; Rhodes et al., 1997; Ashford et al., 2000), thereby restoring osmotic balance in the aphid body. When sucrose molecules are separated into glucose and fructose, the former product typically is used in oligosaccharide production and the latter serves as a respiratory substrate and carbon source to produce lipids and proteins (Febvay et al., 1999; Ashford et al., 2000). Although phloem feeders, occasional ingestion of water-rich xylem sap may also aid in regulation of water balance in aphids (Boquel et al., 2011; Pompon et al., 2011). The nitrogen found in phloem is predominantly in the form of free amino acids, with many, and at times, all of the 20 amino acids found in phloem (Douglas, 2003). However, phloem typically contains a high ratio of non-essential to essential amino acids (Douglas, 2006). Aphids can overcome this shortfall of essential amino acid content in their diet from symbiotic bacteria, Buchnera aphidicola, that synthesize and provide these nutrients (Douglas, 2003; Gil et al., 2004; Hansen et al., 2020). Accounting for 90% or more of the total number of microbial cells in an aphid (Douglas, 2003), B. aphidicola are located in the hemocele within the mycetocyte (also called the bacteriocyte), a type of cell with the apparent sole function of maintaining the bacteria (Whitehead and Douglas, 1993a). This mutualistic association is obligatory for both partners (Mittler, 1971; Douglas, 1992; Whitehead and Douglas, 1993b), and B. aphidicola are transmitted vertically from the mother aphid to her offspring (Hinde, 1971).

5.2.3 Overcoming plant defenses Relative to chewing herbivores, the direct damage to plants from aphid feeding is comparatively small. Nevertheless, plants may respond to aphid feeding by upregulating genes associated with defense (Moran and Thompson, 2001) and mobilizing callose and proteins to plug the sieve pores that are punctured during phloem feeding (Will et al., 2013). As discussed above, watery salivary secretions by aphids appear to suppress this wound healing response. Moreover, the salivary sheath formed from gelling saliva may inhibit induction of at least some plant defense responses, thereby functioning to insulate the stylets from defenses inside the sieve tubes of the phloem (Miles, 1999; Will and van Bel, 2006; Will et al., 2013). However, the salivary sheath may actually induce defense responses in other plant tissues (Will and van Bel, 2008; Louis

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and Shah, 2013; Will et al., 2013). Thus, the protection offered by the salivary sheath does not allow an aphid to completely overcome plant defenses. Plant defense responses to herbivory are mediated by phytohormones, including jasmonic acid and salicylic acid, the former being more commonly mobilized in association with leaf-chewing herbivores and some phloem feeders and the latter more commonly induced by aphid feeding (Züst and Agrawal, 2016a). Reciprocal antagonism between jasmonic and salicylic acids is thought to function to fine-tune plant defense (Thaler et al., 2012). By inducing the latter response in plants rather than the former, aphids may be able to avoid jasmonic acid-mediated defenses which appear to be more detrimental to aphid feeding and population growth (Walling, 2008; Züst and Agrawal, 2016a). Interestingly, previous aphid infestation generally appears to systemically induce plant resistance at the plant scale but to suppress induction of defense and phloem sealing at the local scale (e.g., on the same leaf) (Züst and Agrawal, 2016a). Secondary metabolites are important defense compounds in plant resistance to chewing herbivores; however, their role in defense against aphids is less evident, in part because of the reduced exposure to such compounds by phloem feeders. For example, aphids may limit uptake of plant secondary metabolites since they are less prevalent in phloem than in plant cells (Molyneux et al., 1990). Moreover, some plant secondary metabolites (e.g., glucosinolates and benzoxazinoids) are enzymatically activated in response to cell damage or ingestion; thus, by causing limited damage to plant cells while feeding, aphids to some extent reduce activation of these compounds (Cambier et al., 2001; Kim and Jander, 2007). Other plant secondary metabolites that do not require enzymatic activation (e.g., alkaloids and cardenolides) may be excreted in the honeydew if such compounds are polar or passively sequestered in the aphid’s body if apolar (Wink and Römer, 1986; Züst and Agrawal, 2016b). Apolar alkaloids in plants can be exploited by aphids as acquired toxins for their own defense (Wink and Römer, 1986; Wink and Witte, 1991) and are, therefore, beneficial at relatively low concentrations; however, both alkaloids and cardenolides appear to be toxic to aphids at (naturally) high concentrations (Dugravot et al., 2007; Brunissen et al., 2009; Züst and Agrawal, 2016a).

5.2.4 Social facilitation By manipulating their host plants, aphids can promote the development and reproduction of conspecifics (Takemoto et al., 2013). Potato aphids have been shown to prefer plants previously infested by conspecifics over undamaged plants (Ameline et al., 2007). A similar situation has been reported for cowpea aphid, Aphis craccivora (Koch) (Pettersson et al., 1998), and the damson-hop aphid, Phorodon humuli (Schrank) (Campbell et al., 1993). Along the same lines, green peach aphids had longer periods of phloem ingestion on plants previously infested by conspecifics (Civolani et al., 2010; Dugravot et al., 2007). The modulation of aphid attraction may happen in a density-dependent manner (Pettersson et al., 1998). Insinga et al. (2021) observed that individual green peach aphids preferred to settle on potato leaflets obtained from plants infected with soft rot pectolytic bacterium Dickeya dianthicola (Samson), while green peach aphids released in groups of 10 were more likely to settle on leaflets from uninfected plants. The authors speculated that a host with physiological defenses compromised by a bacterial infection may be more suitable for aphids in the absence of host manipulation by conspecifics. At the same time, aphid-manipulated uninfected hosts may be preferable when conspecifics are present because aphids do not have such a negative impact on nutritional properties of the host plant as D. dianthicola, which metabolizes its nutrients and reduces phloem flow by destroying vascular tissues (Effantin et al., 2011; Toth et al., 2003).

5.3 Virus transmission Potato leafroll virus (PLRV) and Potato virus Y (PVY) are the two most important potato-infecting viruses, severely diminishing potato yield and quality in most potato-growing areas. Both are single-stranded RNA viruses. PLRV is a phloem-limited luteovirus that infects about 20 plant species in five families, including potato and tomato (Brunt and Loebenstein, 2001). Symptoms of PLRV in potato include characteristic rolling or cupping of foliage, foliar discoloration, stunted growth, and phloem necrosis in stems. The yield reduction in infected plants may exceed 50% (Beemster and de Bokx, 1987), and even reach the point of a complete crop failure (Rahman et al., 2010). Furthermore, the tubers of some cultivars react to PLRV infection with an internal necrosis, known as net necrosis, which can be seen with the naked eye when a tuber is cut (Beemster and de Bokx, 1987). PVY is the type member of the virus family Potyviridae. It is generally considered to have a wide host range and has been reported to naturally infect plants in more than nine families, including 14 genera of the Solanaceae (Gray et al., 2010; Karasev and Gray 2013). However, not all non-potato isolates infect potatoes (Karasev and Gray, 2013). Furthermore, it is possible that some of the earlier reports of PVY infection of non-potato hosts may have been based on false positive ELISA

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results (Chatzivassiliou et al., 2004; Kaliciak and Syller, 2009). Confirmed hosts of agronomic importance include pepper, tomato, tobacco, nightshade, and potato. PVY exists as a complex of strains differing molecularly and in their reactions among potato cultivars (Karasev and Gray, 2013; Green et al., 2018). Symptoms of PVY infection in potato include mottling, crinkling, and yellowing of leaves, with secondarily infected plants stunted and having brittle foliage. Some recombinant strains of PVY can cause Potato Tuber Necrotic Ringspot Disease (PTNRD) or other defects in the tubers of susceptible potato cultivars, making them completely unmarketable (Karasev and Gray, 2013). Yield reduction in potato crops in response to the PVY infection depends on variety and may be as high as 70%e86% (Beemster and de Bokx, 1987; Mondjana et al., 1993; Rahman et al., 2010), although smaller yield penalties are more common (Karasev and Gray, 2013). Nolte et al. (2004) estimated that for each percentage of increase in PVY infection rate, yield declines by about 0.18 t/ha. Both PLRV and PVY are transmitted by aphids. However, there are significant differences in the transmission mechanism between these viruses. PLRV is a persistent virus transmitted exclusively by potato-colonizing aphid species, with green peach aphid being the most efficient vector (MacGillivray, 1981). Aphids need to reach the phloem tissue and feed for 20e30 min in order to become infective. There is a latent period of 12e48 h between acquisition and inoculation, during which virus particles cross the gut wall into the aphid hemolymph, and then enter the salivary gland. After the latent period, an infective aphid can transmit PLRV effectively for its entire life (Radcliffe et al., 1993; DiFonzo et al., 1996a). Unlike PLRV, PVY is transmitted by at least 65 different aphid species (Lacomme et al., 2014), although transmission efficiency varies greatly among aphid species and virus strains and isolates (Al-Mrabeh et al., 2010; Shrestha et al., 2014; Mondal et al., 2016b, 2017a). Similar to PLRV, potato-colonizing green peach aphid is the most efficient vector of PVY. However, the majority of vector species are non-colonizing aphids. PVY transmission is non-persistent, i.e., the mouthparts of the aphid may get contaminated with viral inoculum in the brief process of probing the epidermal tissues of infected plants. There is no latent period between acquisition and inoculation, and the entire transmission process can take just seconds to minutes. Also, infectivity is lost after several probes (Bradley and Rideout, 1953). Viruses can induce physiological changes in plants that they infect by affecting both their immune responses and the availability of plant nutrients (Culver and Padmanabhan, 2007; Belliure et al., 2010; Carr et al., 2019). These changes, in turn, influence the frequency and nature of interactions between hosts and vectors, probably due to altered visual cues or volatiles released from the plant (Hodge and Powell, 2008). Green peach aphids and potato aphids grew faster, survived better, and produced more offspring on potatoes infected by PLRV compared to uninfected plants (Castle and Berger, 1993; Castle et al., 1998; Srinivasan et al., 2008). However, little to no such effect was observed in case of potatoes infected by PVY (Castle and Berger, 1993; Castle et al., 1998; Srinivasan and Alvarez, 2007). Not surprisingly, both aphid species also demonstrated a preferential attraction and longer feeding arrestment on PLRV-infected plants and attraction, but shorter feeding arrestment on PVY-infected plants (Castle and Berger, 1993; Castle et al., 1998; Eigenbrode et al., 2002; Srinivasan et al., 2006; Alvarez et al., 2009). Such a change in behavior directly benefits the virus since PLRV is transmitted in a persistent manner favoring the longer latent and acquisition period, as opposed to the non-persistently transmitted PVY which does not require long feeding durations (Eigenbrode et al., 2002; Mauck et al., 2018). These behavioral responses to infected plants may also affect the dynamics of virus spread within potato fields. Vector movement has a great influence on spatial and temporal patterns of viral infections (Peters, 1987; Irwin and Thresh, 1990). Primary virus inoculum can arrive with winged aphids immigrating from outside of a given field. Once initial inoculum is established, whether by immigrating aphids or infected seed, further virus transmission throughout a potato field will likely depend on local within-field aphid movement from infected to uninfected plants. Short-distance movement of infective aphids may be responsible both for enlarging existing disease concentrations, as well as for creating new foci within the same field (Irwin and Thresh, 1990). Using the continuous-time, deterministic, and compartmental mathematical model, Jeger et al. (1998) and Madden et al. (2000) also showed that local aphid dispersal was a potentially crucial component of the plant-aphid-virus system, especially for the non-persistent plant viruses. The relative importance of colonizing versus non-colonizing aphids in driving PVY outbreaks in potato fields is uncertain and difficult to study. While the former can build up large populations within potato fields and have high transmission efficiencies (Al-Mrabeh et al., 2010), the latter are likely to probe more plants within a potato field, creating more opportunities to move the virus from one plant to another (Boquel et al., 2014). Moreover, at times the sheer numbers of non-colonizing individuals can compensate for their lower transmission efficiencies. Van Hoof (1979) found a significant correlation between the abundance of green peach aphids and local PVY spread in the Netherlands. Similarly, Harrewijn et al. (1981) suggested that short hovering flights performed by the green peach aphid summer migrants might be responsible for a considerable amount of PVY transmission. Also, most winged aphids captured near potato fields by Sano et al. (2019) that tested positive for PVY using RT-PCR belonged to potato-colonizing species. On the other hand, DiFonzo et al. (1996a) reported that winged non-colonizing aphids coming from outside the crop were responsible for the

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majority of PVY infection in Minnesota potato fields. Kirchner et al. (2011) observed high levels of field PVY incidence despite a lack of colonizing aphids, while Steinger et al. (2015) did not find any link between PVY spread and the green peach aphid abundance. Furthermore, Mondal et al. (2016a) saw a significant correlation between PVY infection rate and captures of non-colonizing aphids. In contrast, the relationship between abundance of colonizing species and PLRV prevalence should be expected to be more straightforward. Indeed, Mondal et al. (2017b) found a correlation between abundance of green peach aphids on plants and prevalence of PLRV infection across three potato cultivars, though the correlation between viruliferous green peach aphid abundance and PLRV infection was observed only in two of the three cultivars studied. Galimberti et al. (2020) used a spatially explicit agent-based mathematical model based on the existing empirical information on aphid biology and their interactions with potato plants to simulating PVY spread in a potato field. They determined that non-colonizing aphids are likely to be more important for PVY spread compared to colonizing aphids, particularly at high densities. An early-season peak in their numbers produced a spike in the number of infected plants in the end of the season. Mid- and late-season peaks caused relatively little virus spread. A field study by MacKenzie et al. (2016) confirmed that PVY infection significantly increased when aphid populations were high early in the season, but not when they were high late in the season. At the same time, PVY incidence reported in that study increased when mid-season aphid populations were high. An overall current consensus is that PVY spread in potato fields is primarily determined by abundance and activity of non-colonizing aphids. However, relative contribution of colonizing and non-colonizing species is likely to vary among locations and cropping seasons because of differences in their abundance and species composition. Therefore, importance of the former should not be automatically discounted, and their good control must remain an important consideration in potato pest management.

5.4 Management approaches 5.4.1 Monitoring aphid populations Taking control measures only when justified by the threat posed by the existing pest populations is the very foundation of integrated pest management (see Chapter 27 for further discussion of this approach). Therefore, reliable methods for pest detection are very important. Abundance of colonizing aphids on potato plants is often determined by visual counts. Shands et al. (1954) demonstrated that counting the number of aphids on one top, one middle, and one bottom leaf of a randomly selected potato plant accurately estimated the number of aphids inhabiting the whole plant. Another commonly used approach is the beat bucket method. It is a modification of beat sheet sampling that relies on disturbing of potato plants, catching falling aphids in a bucket, and then counting them (Wohleb et al., 2021). Both methods reveal the abundance of mostly wingless aphids. However, because of their potential role in virus transmission winged aphids belonging to both colonizing and non-colonizing species are usually more of a concern to potato growers. Their abundance is determined using a variety of traps. Suction traps have been used extensively in several countries for monitoring activity of flying insects, including aphids. While details of their design may vary from place to place, a typical suction trap consists of a vertical tube two to several meters high and 20e30 cm in diameter that is open on top, a suction fan pulling air through the tube, and a collection container filled with a mixture of ethanol and propylene glycol (Allison and Pike, 1988; Quinn et al., 1991). These traps are usually arranged in regional networks that are maintained by government agencies or universities, often in collaboration with grower organizations (Quinn et al., 1991; Wohleb et al., 2021). Suction traps are designed to sample insects flying above canopy level (Quinn et al., 1991). Therefore, they are well-suited for quantifying long-distance migrations, but not necessarily for measuring insect abundance and activity within potato fields. Lure-and-kill traps deployed at the canopy level within or in the immediate vicinity of potato fields provide a better option for monitoring activity of flying aphids in relation to virus transmission within these fields. These traps use color that mimics the color of host vegetation for attracting the aphids. Aphids captured by water pan traps containing a mixture of water and propylene glycol can be further analyzed for the presence of PVY using RT-PCR (Pelletier et al., 2012; Sano et al., 2019). Three commonly used trap types are yellow sticky traps, yellow water pan traps, and green tile water pan traps (Radcliffe and Ragsdale, 2002). For most aphid species, yellow traps capture more aphids compared to green tile traps (Eastop and Raccah, 1988). However, attractiveness of yellow color may vary for different aphid species (Baldy and Rabasse, 1983). In a study of aphid vectors of soybean viruses, green tile traps provided a less biased estimate of landing rates than did yellow traps (Irwin, 1980). In potato, however, these same green tiles provided a biased estimate of landing rates compared to similarly designed traps using potato foliage (Boiteau, 1990).

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Both colonizing and non-colonizing aphids may be found in traps and foliage samples. It is important, therefore, to be able to recognize the winged females of colonizing aphid species, to appreciate how their relative incidence among all the aphids that might be found visiting potato, and to understand the diversity of non-colonizing aphids that might be found while sampling insects in potato. Complete coverage of this issue is beyond the scope of this book, and the details of species present and relative abundance of them will vary by location and year; however, a few illustrative examples of common species pairs in western North American cropping systems illustrate this point (Fig. 5.4). Fig. 5.4A and B show alate females of Aphis frangulae Kaltenbach and Aphis spiraecola Patch, respectively, one or both are common in many potato-growing regions of the world, but with different hostplant biology. Fig. 5.4C is an alate female of the potato aphid Macrosiphum euphorbiae, a common potato pest, while Fig. 5.4D is Macrosiphum mentzeliae (Wilson), a common species in some parts of western North America that lives only on Mentzelia sp. (Loasaceae). Fig. 5.4E and F are two common pest species, the green peach aphid Myzus persicae and Myzus cerasi (F.), respectively; of these two similar species, only one is of serious concern for potato production. Identification of captured aphids and distinguishing among morphologically similar species requires considerable expertise, which is often lacking in pest management practitioners. DNA barcoding may provide a valuable alternative to visual identification (Foottit et al., 2008; Sano et al., 2019). However, it requires specialized molecular equipment and knowledge, which are much more common than training in classical aphid taxonomy, but still very far from universal among farmers and crop consultants.

5.4.2 Aphid control versus virus control Most crop damage caused by aphids in potatoes is due to virus transmission. Yield reduction due to direct feeding is usually small and does not warrant control measures by itself. While virus infection can significantly reduce yields of potatoes harvested for human consumption, the biggest concern is production of seed tubers for sale to other potato growers. Regulations existing in many places limit percentage of virus-infected tubers in potato lots that can be legally sold as seed (Gray et al., 2010). This presents a considerable problem for potato growers because seed potatoes command a significantly higher price compared to potatoes sold for other purposes. Furthermore, finding alternative market for rejected seed potatoes may be challenging because of their smaller size, and because contracts between growers and processors are usually signed well in advance of harvest. For nuances on potato production and marketing, please refer to Chapters 2 and 3. Similar to other insect pests, in large-scale commercial production potato-colonizing aphids are suppressed mostly by insecticides (Chapter 11). At this point, chemical control works reasonably well. As a result, PLRV, which is vectored by the colonizing species, has become a considerably smaller problem than it was in the past. However, the two major problems associated with insecticides, resistance and pest resurgence, are very applicable to aphid management. Green peach aphid, which is the most effective virus vector, is also notorious for its ability to evolve resistance to wide variety of chemicals (Chapter 24). Furthermore, natural enemies are important in regulating population growth of potato-colonizing aphids (Alyokhin et al., 2011; Leppanen et al., 2012; see also Chapter 13). After natural controls are gone due to the use of broad-spectrum pesticides, high intrinsic rates of growth typical for aphid populations make them very capable of rapidly bouncing back (Fig. 5.5). Dealing with non-colonizing aphids, which may be very important for transmission of PVY, presents additional challenges. Despite occasional reports of lower PVY incidence in insecticide-treated potatoes (Alyokhin et al., 2002), insecticides are usually inefficient in preventing transmission of non-persistent viruses by non-colonizing aphids (Shanks and Chapman, 1965; Loebenstein and Raccah, 1980; Irwin, 1999). Rejection of non-host plants often does not take place until aphids probe them using their mouthparts (Kennedy, 1950; Swenson, 1968). As a result, dispersing winged adults of non-colonizing species commonly land on potato plants, insert their stylets into plant tissue, and then leave in search of a more appropriate host. Direct damage caused by probing is negligible. However, probing may also result in the transmission of PVY to healthy plants. Since the whole process takes minutes, time of exposure to insecticides is not sufficient for acquisition of a lethal dose. To the contrary, exposure to sublethal doses of many insecticides can induce restless behavior and encourage aphid movement (Lowery and Boiteau, 1988; Nauen, 1995). Cultural control methods directed toward suppression of potato-colonizing aphids are described in Chapter 15. There are also several effective cultural approaches that are specifically directed toward suppressing potato viruses rather than their aphid vectors. Probably the most important one is reducing the amount of inoculum that arrives at a field by planting virus-free tubers. This is achieved by testing the tubers that are destined for planting and allowing only seed lots that contain less than a certain proportion of infected tubers. Many jurisdictions have extensive bodies of regulation on what can be considered seed tubers and authorized organizations responsible for certifying them as such (Gray et al., 2010; Frost

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FIG. 5.4 Slide-mounted specimens of some aphid species that can be common in and near potato fields, illustrating the similarity in appearance of common congeneric aphids. These specimens are all 2e3 mm long from head to tip of cauda. (A) Aphis frangulae; (B) Aphis spiraecola. These and many Aphis share short antennae, short cylindrical siphunculi, and abdomen without extensive dorsal markings. (C) Macrosiphum euphorbiae; (D) Macrosiphum mentzeliae. Among other features, members of this genus share long antennae, long cylindrical siphunculi, and abdomen without extensive dorsal markings. (E) Myzus persicae; (F) Myzus cerasi. Myzus species illustrate features common in this and other genera including prominent converging frontal tubercles, slightly swollen siphunculi, and dorsum of abdomen with dark markings.

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FIG. 5.5 Resurgence of green peach aphids and potato aphids on potato plots treated with a broad-spectrum insecticide (Alyokhin, unpublished). Ambush (permethrin) is a broad-spectrum foliar insecticide that is toxic to aphid natural enemies. Admire (imidacloprid) and Platinum (thiamethoxam) were applied in furrow at planting, thus minimizing their contact with non-target insects. Plots were four rows wide and 15.24 m long. Aphids were counted on one top, one middle, and one bottom leaf of 20 plants haphazardly selected from each plot.

et al., 2013; Karasev and Gray, 2013). Another method is removing plants that show visible signs of viral infections, commonly referred to as rogueing (Boquel et al., 2017). Yet another method is suppressing solanaceous weeds that can serve as a reservoir for both PLRV and PVY (Srinivasan et al., 2013). Also, whenever possible seed potato fields should be isolated from other potato fields that may serve as sources of virus inoculum (Harrington et al., 1986; Halbert et al., 1990). However, all these approaches are often unpractical for seed growers to fully implement.

5.4.3 Manipulation of crop borders As discussed above, aphids usually tend to land on the edges of fields (DiFonzo et al., 1996a,b) where the contrast between green plants and dark soil is greatest (Moericke, 1955; Müller, 1964; Finch and Collier, 2003) and where swirls in wind currents are favorable for aphid landing (Broadbent et al., 1951; Johnson, 1950). Because of this, a significant proportion of them alight on the border plants. Since PVY is a non-persistent virus that is lost after several probes, PVY-carrying aphids are likely to lose their infectivity within the border, or not move into the main crop at all. Therefore, surrounding a potato field with plants that are not PVY hosts is likely to reduce PVY spread within that field. Indeed, DiFonso et al. (1996b) successfully reduced PVY infection on potato plots bordered by soybean (Glycine max [L.]), sorghum (Sorghum bicolor [L.] Moench), and winter wheat (Triticum aestivum L.). Boiteau et al. (2009) achieved a similar result by deploying borders of seeded grass or green tarps. Rondon (personal communication) also used Sudan grass (Sorghum bicolor ssp. drummondii (Nees ex Steud.) de Wet & Harlan) with success. These border crops still need to be treated with insecticides to prevent them from becoming a breeding ground for aphids that may later move into the area planted with potatoes.

5.4.4 Mineral oils Mineral oil is a blend of various petroleum-derived hydrocarbons, primarily paraffins. Its commercial formulations often also include a surfactant (Davidson et al., 1991). It has insecticidal properties primarily against small, soft-bodied pests including aphids (Herron et al., 1995; Martín-López et al., 2006; Galimberti and Alyokhin, 2018). The mechanism behind the insecticidal activity of oil is not completely understood and may include suffocation caused by blocking the insect’s spiracles (Davidson et al., 1991) and cellular damage following penetration through insect cuticle (Najar-Rodríguez et al., 2008). Mineral oil also interferes with plant colonization by aphids (Ameline et al., 2009; Galimberti and Alyokhin, 2018), in part due to its masking of foliage odor (Ameline et al., 2009). Furthermore, treating plants with oil may reduce the release of volatiles involved in host plant location (Mensah et al., 2005). Mineral oil also interferes both with acquisition of non-persistently transmitted viruses, including PVY, by aphids, as well as with infection of plants probed by viruliferous vectors (Bradley et al., 1962; Wróbel, 2007; Margaritopoulos et al., 2010). As in the case of insecticidal properties, its mode of action against viruses is not completely clear. Most likely, it involves reduction of the ability of a virus particle to attach itself to an aphid stylet (Wang and Pirone, 1996; Boquel et al.,

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2013). Mineral oil also may induce expression of plant defense genes against virus infection (Khelifa, 2017) and/or restrict virus movement within the plant tissue (Al-Daoud et al., 2014; Boquel and Nie, 2017). Though the mechanisms remain unclear, the efficacy of mineral oil in reducing PVY spread in the field is well-demonstrated (Bradley et al., 1966; Boiteau and Singh, 1982; Kirchner et al., 2014; Rolot et al., 2021). However, mineral oil may not always reduce PVY to acceptable levels (Hansen and Nielsen, 2012). Mineral oil is a good fit in pest management programs. It is relatively safe compared to many synthetic insecticides due to its low environmental persistence (Davidson et al., 1991) and low toxicity to important natural enemies of aphids such as lady beetles (Kraiss and Cullen, 2008). Moreover, integrating oil applications with other methods may be necessary in some cases for obtaining the best results. MacKenzie et al. (2017) reported that oil sprays lowered PVY below the control levels, but only in one of the 2 years of the study. At the same time, they saw no reduction in PVY incidence relative to the untreated control after spraying several different insecticides, but no oil. However, oil and insecticides used in combination were able to consistently suppress the spread of PVY, regardless of the oil dose and frequency of insecticide sprays. Similarly, in the study by Rolot et al. (2021) systemic insecticides provided additional protection against PVY in a mix with mineral oil when activity of winged aphids was high. Boiteau et al. (2009) showed that combining mineral oil applications with non-potato crop border was almost twice as effective in reducing PVY incidence as either method used alone. Furthermore, oil effects were similar whether it was applied to the border, the center seed plot, or both. Rolot et al. (2021) reported that straw mulching, a technique described in detail in Chapter 15, enhanced the effects of mineral oil and reduced the number of sprays required for successful protection of potato crops. As a bonus, Galimberti and Alyokhin (2018) found synergism between mineral oil and the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Clavicipitaceae) against the Colorado potato beetle, Leptinotarsa decemlineata (Say). Beetle larvae died quicker when sprayed with both products, possibly because the oil facilitated cuticle penetration by the fungus.

5.5 Summary and future directions Aphids are important pests of potatoes. While their direct damage is usually small, the viruses they transmit among potato plants may lead to significant economic damage. Currently, potato-colonizing aphids can be successfully controlled by insecticides, thus curtailing the spread of persistently transmitted PLRV. However, insecticides do not prevent nonpersistent transmission of PVY by non-colonizing aphids, which remains a serious problem. PVY epidemiology is rather complex; therefore, finding simple solutions for preventing its outbreaks is unlikely. Successful PVY management depends on effective integration of different control methods. Although controlling aphid vectors remains an important task, solving PVY problems largely depends on the measures taken directly against the virus, such as reducing the amounts of its inoculum, interfering with its transmission by spraying mineral oil, and breeding virus-resistant plants. Synergistic integration of different techniques for PVY management is an important task that requires interdisciplinary cooperation among entomologists, plant pathologists, agronomists, and plant breeders.

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Campbell, C.A.M., Pettersson, J., Pickett, J.A., Wadhams, L.J., Woodcock, C.M., 1993. Spring migration of damson-hop aphid, Phorodon humuli (Homoptera: Aphididae), and summer host plant-derived semiochemicals released on feeding. J. Chem. Ecol. 19, 1569e1576. Carr, J.P., Murphy, A.M., Tungadi, T., Yoon, J.Y., 2019. Plant defense signals: players and pawns in plant-virus-vector interactions. Plant Sci. 279, 87e95. Castle, S.J., Berger, P.H., 1993. Rates of growth and increase of Myzus persicae on virus-infected potatoes according to type of virus- vector relationship. Entomol. Exp. Appl. 69, 51e60. Castle, S.J., Mowry, T.M., Berger, P.H., 1998. Differential settling by Myzus persicae (Homoptera : Aphididae) on various virus infected host plants. Ann. Entomol. Soc. Am. 91, 661e667. Chatzivassiliou, E.K., Efthimiou, K., Drossos, E., Papadopoulou, A., Poimenidis, G., Katis, N.I., 2004. A survey of tobacco viruses in tobacco crops and native flora in Greece. Eur. J. 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Rhodes, J.D., Croghan, P.C., Dixon, A.F.G., 1997. Dietary sucrose and oligosaccharide synthesis in relation to osmoregulation in the pea aphid, Acyrthosiphon pisum. Physiol. Entomol. 22, 373e379. Rolot, J.L., Seutin, H., Deveux, L., 2021. Assessment of treatments to control the spread of PVY in seed potato crops: results obtained in Belgium through a multi-year trial. Potato Res. 2021. https://doi.org/10.1007/s11540-020-09485-7. Sano, M., Ohki, T., Takashino, K., Toyoshima, S., Maoka, T., 2019. Species composition of alate aphids (Hemiptera: Aphididae) harboring Potato virus Y and the harbored virus strains in Hokkaido, northern Japan. J. Econ. Entomol. 112, 85e90. Shands, W.A., Simpson, G.W., Reed, L.B., 1954. Subunits for estimating aphid abundance on potatoes. J. Econ. Entomol. 47, 1024e1027. Shanks, C.H., Chapman, P.K., 1965. The effects of insecticides on the behavior of Myzus persicae Sulzer and its transmission of Potato virus Y. J. Econ. Entomol. 58, 79e83. Shrestha, D., Wenninger, E.J., Hutchinson, P.J.S., Whitworth, J.L., Mondal, S., Eigenbrode, S.D., Bosque-Pérez, N.A., 2014. Interactions among potato genotypes, virus strains, and inoculation timing and methods in the Potato virus Y and green peach aphid pathosystem. Environ. Entomol. 43, 662e671. Smith, M.T., Severson, R.F., 1992. Host recognition by the blackmargined aphid (Homoptera: Aphididae) on pecan. J. Entomol. Sci. 27, 93e112. Srinivasan, R., Alvarez, J.M., 2007. Effect of mixed viral infections (Potato virus Y-Potato leafroll virus) on biology and preference of vectors Myzus persicae and Macrosiphum euphorbiae (Hemiptera: Aphididae). J. Econ. Entomol. 100, 646e655. Srinivasan, R., Alvarez, J.M., Eigenbrode, S.D., Bosque-Perez, N.A., 2006. Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae: Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ. Entomol. 35, 546e553. Srinivasan, R., Alvarez, J.M., Eigenbrode, S.D., Bosque-Pérez, N.A., Novy, R., 2008. Effect of an alternate weed host, hairy nightshade, Solanum sarrachoides (Sendtner), on the biology of the two important Potato leafroll virus (Luteoviridae: Polerovirus) vectors, Myzus persicae (Sulzer) and Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae). Environ. Entomol. 37, 592e600. Srinivasan, R., Cervantes, F.A., Alvarez, J.M., 2013. Aphid-borne virus dynamics in the potato-weed pathosystem. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Oxford, UK, pp. 311e337. Steinger, T., Goy, G., Gilliand, H., Hebeisen, T., Derron, J., 2015. Forecasting virus disease in seed potatoes using flight activity data of aphid vectors. Ann. Appl. Biol. 166, 410e419. Sutherland, O.R.W., Mittler, T.E., 1971. Influence of diet composition and crowding on wing production by the aphid Myzus persicae. J. Insect Physiol. 17, 321e328. Swenson, K.G., 1968. Role of aphids in the ecology of plant viruses. Annu. Rev. Phytopathol. 6, 351e374. Takemoto, H., Uefune, M., Ozawa, R., Arimura, G.-I., Takabayashi, J., 2013. Previous infestation of pea aphids Acyrthosiphon pisum on broad bean plants results in the increased performance of conspecific nymphs on the plants. J. Plant Interact. 8, 370e374. Thaler, J.S., Humphrey, P.T., Whiteman, N.K., 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260e270. Tjallingii, W.F., 1994. Sieve element acceptance by aphids. Eur. J. Entomol. 91, 47e52. Toth, I.K., Bell, K.S., Holeva, M.C., Birch, P.R.J., 2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4, 17e30. Triplehorn, C.A., Johnson, N.F., 2005. Borror and DeLong’s Introduction to the Study of Insects. Thomson Brooks/Cole, Belmont, CA, p. 864. van Hoof, H.A., 1979. Spread of potato virus YN to and from potato fields. Meded. Fac. Landb. Wet. Gent. 44, 645e651. Visser, J.H., 1986. Host odor perception in phytophagous insects. Annu. Rev. Entomol. 31, 121e144. Walling, L.L., 2008. Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146, 859e866. Walters, F.S., Mullin, C.A., 1988. Sucrose-dependent increase in oligosaccharide production and associated glycosidase activities in the potato aphid Macrosiphum euphorbiae (Thomas). Arch. Insect Biochem. Physiol. 9, 35e46. Wang, K.J., Tsai, H., Harrison, N.A., 1997. Influence of temperature on development, survivorship, and reproduction of buckthorn aphid (Homoptera: Aphididae). Ann. Entomol. Soc. Am. 90, 63e68. Wang, R.Y., Pirone, T.P., 1996. Mineral oil interferes with retention of tobacco etch potyvirus in the stylets of Myzus persicae. Phytopathology 86, 820e823. Ward, S.A., Leather, S.R., Pickup, J., Harrington, R., 1998. Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? J. Anim. Ecol. 67, 763e773. Webster, B., Bruce, T., Pickett, J., Hardie, J., 2010. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 79, 451e457. Webster, B., 2012. The role of olfaction in aphid host location. Physiol. Entomol. 37, 10e18. Wensler, R.J., Filshie, B.K., 1969. Gustatory sense organs in the food canal of aphids. J. Morphol. 129, 473e491. Whitehead, L.F., Douglas, A.E., 1993a. A metabolic study of Buchnera, the intracellular bacterial symbionts of the pea aphid Acyrthosiphon pisum. J. Gen. Microbiol. 139, 821e826. Whitehead, L.F., Douglas, A.E., 1993b. Populations of symbiotic bacteria in the parthenogenetic pea aphid (Acyrthosiphon pisum) symbiosis. Proc. Royal Soc. B 254, 29e32. Will, T., van Bel, A.J.E., 2006. Physical and chemical interactions between aphids and plants. J. Exp. Bot. 57, 729e737. Will, T., Tjallingii, W.F., Thonnessen, A., van Bel, A.J.E., 2007. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. Unit. States Am. 104, 10536e10541.

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Will, T., van Bel, A.J.E., 2008. Induction as well as suppression: how aphid saliva may exert opposite effects on plant defense. Plant Signal. Behav. 3, 427e430. Will, T., Furch, A.C.U., Zimmermann, M.R., 2013. How phloem-feeding insects face the challenge of phloem-located defenses. Front. Plant Sci. 4, 336. Wink, M., Römer, P., 1986. Acquired toxicity - the advantages of specializing on alkaloid-rich lupins to Macrosiphon albifrons (Aphidae). Naturwissenschaften 73, 210e212. Wink, M., Witte, L., 1991. Storage of quinolizidine alkaloids in Macrosiphum albifrons and Aphis genistae (Homoptera, Aphididae). Entomol. Gen. 15, 237e254. Wohleb, C.H., Waters, T.D., Crowder, D.W., 2021. Decision support for potato growers using a pest monitoring network. Am. J. Potato Res. 98, 5e11. Wróbel, S., 2007. Effect of a mineral oil on Myzus persicae capability to spread of PVY and PVM to successive potato plants. J. Plant Protect. Res. 47, 383e390. Züst, T., Agrawal, A.A., 2016a. Mechanisms and evolution of plant resistance to aphids. Native Plants 2, 16206. Züst, T., Agrawal, A.A., 2016b. Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca. Funct. Ecol. 30, 547e556.

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Chapter 6

Psyllids Erik J. Wenningera and Arash Rashedb Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Kimberly Research & Extension Center, Kimberly, ID, United

a

States; bDepartment of Entomology, Plant Pathology, and Nematology, University of Idaho, Moscow, ID, United States

6.1 Introduction Few species of psyllids have been reported to cause damage to potato: the potato psyllid Bactericera cockerelli, Bactericera nigricornis, and Russelliana solanicola among them. In addition, four species in the genus Acizzia have recently been described from solanaceous hosts in Australia, but their ability to feed on potato is unknown. Of these species, the potato psyllid has received the most attention by far largely due to its role in transmission of “Candidatus Liberibacter solanacearum” (Lso) (also known as “Candidatus Liberibacter psyllaurous”), the pathogen associated with zebra chip disease (ZC). ZC is an emerging disease of potato that has reduced yields, increased production costs, and complicated integrated pest management programs in parts of the USA, Mexico, several Central American countries, and New Zealand. ZC was recently reported from Ecuador and poses a potential threat to many other potato-growing regions around the world where either the pathogen or the psyllid vector is currently present or might be unintentionally introduced. Therefore, the bulk of this chapter is focused on the potato psyllid, followed by a brief discussion of the other psyllids known to damage potato and related solanaceous crops.

6.2 Potato psyllid (Bactericera cockerelli) 6.2.1 Identification Adult potato psyllids (Fig. 6.1) are small insects (body length ca. 1.8 mm; length to wing tips ca. 2.75 mm) with a body shape resembling cicadas in the adult stage. This is in part because their wings are held roof-like over the body at rest (Pletsch, 1947; Wallis, 1955). Adults have two pairs of clear wings; the forewings are larger than the hindwings and have more pronounced venation. Newly emerged adults are pale green to light brown and become darker over the next 1e5 days (Knowlton and Janes, 1931), with considerable variation among individuals in color intensity. Adult body color is light brown to dark brown to black with prominent white to whitish lines on the head and thorax. Characters that are distinctive to the potato psyllid include a white band on the dorsum of the first abdominal segment as well as a V-shaped white mark on the dorsum of the last abdominal segment (Fig. 6.1). A white or whitish stripe is also often visible on the dorsum of the abdomen extending from the V-shaped mark toward the thorax. White markings on the head and thorax are more variable, but characteristically feature a white margin along the top, front of the head (Fig. 6.1). Adult psyllids have legs adapted for jumping and fly readily when disturbed. Hence, another common name for psyllids: jumping plantlice. Potato psyllid eggs are yellow to orange, oval, and about 0.3 mm long (Pletsch, 1947, Fig. 6.2). Each egg is attached to the leaf via a short (ca. 0.2 mm) stalk on one end, the length of which may aid in distinguishing potato psyllids from other psyllids. Eggs are often laid along leaf margins and undersides of leaves (Pletsch, 1947), but may be found on the upper surfaces, especially when psyllid density is high. Nymphs develop through five instars, and their body color is variable. Early instars are pale yellow to orange, becoming yellow to green as they mature (Fig. 6.3). Their bodies are flat and broadly oval, with a fringe of “hairs” around the margins of the body. Nymphs hold their bodies close to the leaf surface, usually on the leaf undersides; unlike adults, they generally do not move readily unless physically disturbed. Psyllid nymphs resemble whitefly nymphs which do not move when disturbed. Wing pads are evident in the third instar and become more prominent with subsequent molts. Nymphs produce Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00004-4 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 6.1 Adult potato psyllid. Photo: E.J. Wenninger.

FIG. 6.2 Potato psyllid eggs. Photo: E.J. Wenninger.

FIG. 6.3 Late-instar potato psyllid nymph and two first-instar nymphs. Photo: E.J. Wenninger.

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large amounts of white, waxy, honeydew excretions while feeding. This honeydew may adhere to the foliage and promote fungal growth on the leaf surface. Although both adults and nymphs produce honeydew, it is perhaps more apparent near nymphs because they are more sedentary than adults.

6.2.2 Geographic distribution The potato psyllid is native to western North America (Essig, 1917) and is currently present throughout the Central to Western USA (Pletsch, 1947; Wallis, 1955; Cranshaw, 1994; Munyaneza et al., 2009; Wenninger et al., 2017, 2019), Mexico, and the Central American countries of Guatemala, Honduras, El Salvador, and Nicaragua (Pletsch, 1947; Wallis, 1955; Rubio-Covarrubias et al., 2006; Crosslin et al., 2010; Munyaneza, 2010; Bextine et al., 2013a,b, Fig. 6.4). In addition, the potato psyllid has been introduced to New Zealand (Gill, 2006; Thomas et al., 2011), Australia (IPPC, 2017), and Ecuador (Castillo-Carrillo et al., 2019). Likely introduced to New Zealand during the early 2000s, potato psyllids are now established in all potato growing regions of the country, on both the north and south islands (Vereijssen, 2020). Potato psyllids were first reported on the Australian territory of Norfolk Island in 2014 (Maynard et al., 2018) and near Perth in the state of Western Australia in 2017 (DAFWA, 2017). Potato psyllids have also been reported from most Canadian provinces bordering the USA (EPPO, 2020), but few details on these observations are available. Such observations are thought to be the result of seasonal migration from the USA without successful overwintering (EPPO, 2020), though a similar longstanding hypothesis regarding potato psyllid populations in the Pacific Northwest of the USA has recently been corrected (see Section 6.2.3.4, below). Recent introductions of potato psyllids to other countries are concerning, especially given that climate models indicate that nearly 80% of the global potato acreage is suitable for potato psyllids, with at least 96% of the potato acreage at risk in South America, Eurasia, and Australia (Wan et al., 2020).

6.2.3 Biology and ecology 6.2.3.1 Host range Potato psyllids feed and develop primarily on plants within the family Solanaceae, including many cultivated and weedy species (Essig, 1917; Knowlton and Thomas, 1934; Pletsch, 1947; Wallis, 1955; Cooper et al., 2019a). Solanaceous crop hosts include potato (Solanum tuberosum), tomato (Solanum lycopersicum), pepper (Capsicum spp.), and eggplant/ aubergine (Solanum melongena). Solanaceous non-crop hosts in North America and New Zealand include various species of nightshade (Solanum spp.), groundcherry (Physallis spp.), matrimony vine/boxthorn (Lycium spp.), and other

FIG. 6.4 Map showing distributions of potato psyllids by country or state (red) and approximate distributions of the different haplotypes of “Candidatus Liberibacter solanacearum” (Lso). Lso haplotypes F and G are known only from one potato tuber sample in Oregon and a Solanum umbelliferum herbarium sample in California, respectively. Genetically distinct Lso haplotypes were both named H (one in Apiaceae and Polygonaceae in Finland and one in Colvolvulaceae in Mexico) due to concurrent publication. Potato psyllids and haplotype A are present on Norfolk Island, Australia, which is barely visible on the map north of New Zealand. Lso has not been reported from mainland Australia.

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solanaceous weeds and ornamentals, including jimsonweed (Datura stramonium), henbane (Hyoscyamus niger), coyote tobacco (Nicotiana attenuata), apple of Peru (Nicandra physalodes), and poroporo (Solanum aviculare) (Martin, 2008; Cooper et al., 2019a). In addition, potato psyllids are known to feed and develop on several species within the family Convolvulaceae, including sweet potato (Ipomea batatas), and field bindweed (Convolvulus arvensis). Potato psyllids have been observed on many other species across numerous plant families; however, they do not appear to reproduce and develop on these hosts (Knowlton and Thomas, 1934; Pletsch, 1947; Wallis, 1955). Rather, adults may be able to use a wide diversity of plants as transient hosts or shelter hosts (Knowlton, 1933c, 1934b; Knowlton and Thomas, 1934) that do not support complete development of immature stages.

6.2.3.2 Haplotypes Liu et al. (2006) reported on genetic variation between potato psyllids collected from Western North America (California and Baja, Mexico) versus psyllids from central USA (Colorado and Nebraska) and eastern Mexico (Coahuila), suggesting different geographically based biotypes. Subsequently, four genetically distinct haplotypes of potato psyllids were described in the USA and named after regions with which they exhibit geographic associations: Western, Northwestern, Central, and Southwestern (Swisher et al., 2012, 2014a). These haplotypes are distinguished based on high resolution melt curve analysis of the mitochondrial CO1 gene (Swisher et al., 2012, 2014a). Some differences in biology among haplotypes have been observed, particularly with respect to host plant associations (Swisher et al., 2013c; Dahan et al., 2017; Thinakaran et al., 2017; Wenninger et al., 2019) and life history traits (Liu and Trumble, 2007; Mustafa et al., 2015b). In addition, breeding incompatibility has been observed between certain haplotypes (Mustafa et al., 2015b), apparently as a result of Wolbachia-related cytoplasmic incompatibilities (Cooper et al., 2015b; Fu et al., 2020). Despite some notable differences in psyllid biology among haplotypes, differences have not been observed with respect to transmission efficiency of Lso (Swisher Grimm et al., 2018). The Central potato psyllid haplotype occurs in the Central and Midwestern USA as well as in Mexico, Central America, and Ecuador (Swisher et al., 2012, 2013a, 2014b; Castillo-Carrillo et al., 2019). In addition, the Central haplotype exhibits relatively low but consistent incidence in Idaho (Dahan et al., 2017). The Western haplotype is mainly found west of the Rocky Mountains, including the Pacific Northwest states of Idaho, Washington, and Oregon (Swisher et al., 2013b, 2013c, 2014b; Dahan et al., 2017) as well as in Baja Mexico, Southern California, New Mexico, Texas, and New Zealand (Liu et al., 2006; Swisher et al., 2012, 2014b; Workneh et al., 2018). Thus far, the Northwestern haplotype has only been observed in the Pacific Northwest (Swisher et al., 2012, 2014b; Dahan et al., 2017). The Southwestern haplotype has been observed in New Mexico and Colorado (Swisher et al., 2014a,b; Workneh et al., 2018) and in relatively low numbers in Texas (Workneh et al., 2018) and Idaho (Dahan et al., 2017; Wenninger et al., 2019). Idaho is unique among geographic localities studied to date in that all four potato psyllid haplotypes have been observed there, though the reason for this is not entirely clear (Dahan et al., 2017).

6.2.3.3 Lifecycle and reproductive biology Numerous studies have examined the life history traits and reproductive biology of potato psyllids on different hosts with considerable variation in results that may be attributed largely to temperature and host plant. Adult longevity of mating and actively feeding potato psyllids under laboratory conditions has been reported to average from ca. 15 to well over 100 days (Knowlton and Janes, 1931; Pletsch, 1947; Yang and Liu, 2009; Mustafa et al., 2015b) when held on solanaceous hosts. Potato psyllids may also survive for considerable durations even when held on nonhosts. For example, Knowlton (1933c) reported that adult longevity ranged from 17 to 96 days when held on various nonhost plants. Females generally live longer than males (Knowlton and Janes, 1931; Yang and Liu, 2009). Longevity varies on different host plants (Yang and Liu, 2009; Yang et al., 2010; Mustafa et al., 2015b) and among different potato psyllid haplotypes (Mustafa et al., 2015b). Females reach reproductive maturity on the day of adult eclosion and males at 1 day posteclosion (Guédot et al., 2012). Previous reports suggested a longer premating period of ca. 2e5 days (Knowlton and Janes, 1931; Pletsch, 1947; Abdullah, 2008). Following mating, oviposition begins within 1e5 days, with older females beginning oviposition relatively quickly (Guédot et al., 2012). Fecundity has been reported by several authors, with considerable variation among studies, ranging from ca. 200 eggs to over 1000 eggs during a female’s life (e.g., Pletsch, 1947; Abdullah, 2008; Mustafa et al., 2015b). This variation reflects differences in host plant (Pletsch, 1947; Yang and Liu, 2009; Cooper et al., 2019a; Mustafa et al., 2015b,c), haplotype (Prager et al., 2014a; Mustafa et al., 2015b), insecticide exposure (Cerna-Chávez et al., 2018), and the experimental conditions used. Moreover, at least some of the variation among these studies might also be attributed to reduced reproductive output when potato psyllids are assayed on hosts that differ from their natal host (Prager et al., 2014a). Not surprisingly, both fecundity and longevity of potato psyllids are generally greater under laboratory conditions than in the field (Yang et al., 2010, 2013).

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Eggs hatch after ca. 4e6 days at ca. 27
C (Yang and Liu, 2009; Yang et al., 2010). Lifetable studies at this temperature show that each of the five instars develops over ca. 2e6 days, with potato psyllids on tomato (Yang et al., 2013) and potato (Yang et al., 2010) apparently tending to develop faster than those on eggplant and pepper (Yang and Liu, 2009). Under such optimal conditions, potato psyllids may complete one generation in under 3 weeks or slightly longer than 3 weeks under field conditions (Yang et al., 2010, 2013). Development time from egg to adult may be similar or considerably longer on various weed hosts, depending upon their apparent suitability as host plants (Cooper et al., 2019a). The sex ratio of newly eclosed adults has been reported to be ca. 1:1 (Knowlton and Janes, 1931; Pletsch, 1947; Yang and Liu, 2009; Yang et al., 2010). Guédot et al. (2010) demonstrated evidence of sex attractants in potato psyllids, with males attracted to odors from both sexes and females repelled by odors from both sexes. Following mating, a refractory period of diminished attraction was observed (Guédot et al., 2013). Further clarification on the role of olfactory cues in reproductive behavior of potato psyllids remains to be studied. Vibrational cues are also involved in communication between the sexes (Avosani et al., 2020). The combination of sensory modalities used in orientation of males to females likely will complicate any efforts to develop applied tools using olfactory or vibrational communication.

6.2.3.4 Phenology Temperature is an important factor in the biology and ecology of potato psyllids, which appear to be adapted to warm temperatures and are limited by extremely hot temperatures. Under laboratory conditions, the optimum temperature for survival and development was ca. 24e27
C, depending on life stage, host plant, and statistical model (List, 1939; Pletsch, 1947; Tran et al., 2012; Lewis et al., 2015). The lower developmental threshold ranged from ca. 4e8
C (Tran et al., 2012; Lewis et al., 2015). For temperatures at or above 30
C, oviposition, egg hatching, and survival begin to decrease substantively, with some variation among studies in the intensity of effects (List, 1939; Pletsch, 1947; Tran et al., 2012; Lewis et al., 2015). Henne et al. (2010a) reported that nymphs and at least some adults survive 24-h exposure at least to 15 and 10
C, respectively. Nymphs appear to be more cold-tolerant than adults, though both life stages may survive short durations of exposure to temperatures as low as 20
C (Whipple et al., 2012). Cruzado (2019) showed that infection with Lso increased survival during exposure to temperatures as low as 4
C and that Northwest psyllids showed lower mortality rates than did Western and Central psyllids. Thus, although more work is needed to clarify the cold tolerances of potato psyllids, they appear to survive at temperatures lower than previously considered (Pletsch, 1947; Wallis, 1955). The seasonal phenology of potato psyllids in potato has been investigated primarily within its native geographic range in North America, especially in Texas (Goolsby et al., 2007a,b, 2012; Henne et al., 2012; Workneh et al., 2014), as well as in Washington (Munyaneza et al., 2009; Cohen et al., 2020), Oregon (Cohen et al., 2020), and Idaho (Wenninger et al., 2017, 2019). In South Texas, potato psyllids may be found in potato at crop emergence in January, with populations peaking during March, shortly before harvest. Similar gradual increases in abundance over the potato-growing season (ca. May to September) were observed in Washington and Idaho, though psyllids were first detected in Washington potato during late July and in Idaho potato during late May to early June. Phenologies of psyllids in New Zealand (Cameron et al., 2009; Walker et al., 2011b) and New Mexico (Djaman et al., 2020) potato followed a similar pattern as well. In all cases, potato psyllid abundance in potato declines toward the end of the growing season. Extensive monitoring of potato psyllid populations in potato across the Pacific Northwest over several years has allowed for the development of species distribution models that show that potato psyllids were more abundant in landscapes with high connectivity, low crop diversity, and large natural areas as well as in areas or years with higher levels of winter moisture (Gutiérrez Illán et al., 2020). For decades the conventional wisdom had been that potato psyllids migrated annually from the southwestern US and northern Mexico to US states and Canadian provinces along and near the Rocky Mountains (Romney, 1939; Wallis, 1946, 1955; Pletsch, 1947; Jensen, 1954; Strand, 2006; Nelson et al., 2014). Several factors contributed to this perception, including the sense that potato psyllids could not tolerate severe cold (Pletsch, 1947; Wallis, 1955), the inability to find overwintering populations in northern latitudes, and the thought that a suitable “green bridge” host was not available between overwintering and emergence of potato crops (Horton et al., 2015). Wallis (1946, 1955) provided several lines of circumstantial evidence in support of the migration model, but experimental evidence is still lacking (Nelson et al., 2014; Horton et al., 2015). In New Zealand, seasonal migration has not been observed, and all life stages may be found on noncrop hosts year-round, even in areas with frost and snow (Vereijssen et al., 2018). This is consistent with evidence from the US Pacific Northwest where potato psyllids overwinter in a temperature-controlled quiescence rather than in a true diapause (Horton et al., 2014).

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Potato psyllids in the Pacific Northwest have been observed to overwinter on bittersweet nightshade (Solanum dulcamara) (Jensen et al., 2012; Murphy et al., 2013; Wenninger et al., 2019) and matrimony vine (Lycium spp.) (Thinakaran et al., 2017). Adults have been the primary overwintering stage observed, though eggs, nymphs, and adults reportedly may overwinter (Hodkinson, 2009; Murphy et al., 2013; Vereijssen et al., 2018). The seasonal distribution and abundance patterns of potato psyllids across southern Idaho potato fields also are consistent with the idea that at least a portion of the potato psyllids found in potato come from local overwintering sources (Wenninger et al., 2017). However, these observations cannot fully account for the potato psyllids found in the region given the incongruity in haplotype distributions between potato and overwintering hosts. Potato psyllids collected from bittersweet nightshade in Idaho (Swisher et al., 2013c; Wenninger et al., 2019), Washington (Swisher et al., 2013c; Castillo Carrillo et al., 2016), and Oregon (Swisher et al., 2013c) were almost exclusively of the Northwestern haplotype, with a handful of Western haplotype psyllids and, in Idaho (Wenninger et al., 2019), a few Central and Southwestern psyllids. Fu et al. (2017, 2020) showed that potato psyllids collected from potato crops throughout the Pacific Northwest region were genetically similar to those found on matrimony vine, but dissimilar from those found on bittersweet nightshade. Although matrimony vine is an overwintering host of both Northwestern and Western potato psyllids (Thinakaran et al., 2017), this plant does not appear to be as prevalent in Idaho as in Washington or Oregon (Wenninger et al., 2019). Thus, the current evidence on overwintering biology in the Pacific Northwest cannot explain the dominance of Western psyllids in Idaho potato and the abundance of Central psyllids during some years (Swisher et al., 2014b; Dahan et al., 2017). Whether there are additional overwintering hosts in Idaho and other parts of North America that harbor other haplotypes remains to be clarified. It also may be that successful overwintering does not require a true host and might readily occur on various transient or shelter hosts (Essig, 1917; Knowlton, 1933c, 1934b; Knowlton and Thomas, 1934). Pletsch (1947) reported that potato psyllids held without a plant at 100% relative humidity and 4
C may live up to 92 days, demonstrating the considerable longevity of potato psyllids in the absence of a host provided temperatures are low and humidity is high. Indeed, Cooper et al. (2019c) confirmed through gut content analysis that autumn-dispersing psyllids feed extensively on a diversity of nonreproductive transitory plants; thus, it is possible that some potato psyllids that do not find a reproductive host on which to overwinter might do so on a nonreproductive host. Potato psyllid phenology in areas other than the northwestern USA has not been studied as extensively. For regions that do not feature major seasonal changes during the winter and in which suitable host plants are consistently available (e.g., parts of Mexico and Central America), potato psyllids are able to reproduce and develop year-round (Munyaneza and Henne, 2013).

6.2.4 Damage The potato psyllid has been among the most damaging potato pests in North America. In the species description of  Paratrioza cockerelli (the original species name for the potato psyllid) Sulc (1909)din reference to the large numbers of nymphs found on pepper plantsdstated that “we may infer that the insect can become very destructive” (translation from Pletsch, 1947). Similarly, other early accounts of potato psyllids noted explosive population growth and/or severe plant injury (Crawford, 1914; Compere, 1915, 1916; Essig, 1917) that presaged the frequent outbreaks of this pest that would plague potato growers.

6.2.4.1 Psyllid yellows Richards et al. (1927) described a 1927 outbreak of a new disease of potato in Utah associated with potato psyllids originally termed “yellows” (Richards, 1928) and later “psyllid yellows” (Richards, 1931; Richards and Blood, 1933). The symptoms are characterized initially by upward curling of the basal portions of the leaflets near the top of the plant, followed by chlorosis or purpling of the leaves and shoots, stunted growth, aerial tubers, shortened and thickened internodes, extensive setting of small tubers, premature sprouting of daughter tubers, premature senescence, and eventually plant death (Richards, 1928; Richards and Blood, 1933; Pletsch, 1947; Wallis, 1955; Sengoda et al., 2010). Following the description of psyllid yellows and its association with potato psyllids, the disease was putatively attributed to previous outbreaks in potato dating back as early as 1911 (Pletsch, 1947) and to outbreaks in tomato as early as 1898 (List, 1939). These sporadic outbreaks over the early 1900s occurred in states and provinces along the Rocky Mountains, with Utah, Wyoming, Colorado, and Nebraska experiencing the most frequent and severe damage (Pletsch, 1947; Wallis, 1955). By the 1930s psyllid yellows was widely considered to be the most destructive of all potato diseases in these growing areas (Richards and Blood, 1933; Pletsch, 1947), with reported losses as high as 75% in affected states (Butler and Trumble, 2012c).

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Much of our knowledge of psyllid yellows derives from studies conducted before the advent of molecular diagnostic tools. Psyllid yellows has long been thought to be caused by toxins transmitted through the feeding activity of potato psyllids (Eyer and Crawford, 1933; Richards and Blood, 1933; Carter, 1939). Interestingly, psyllid yellows was reported to be associated with feeding only by nymphs, with infestations of up to 1000 adults per plant failing to elicit symptoms (Richards, 1931); however, this observation would be worth reevaluating. Symptoms of psyllid yellows and zebra chip disease are remarkably similar, with both diseases systemically affecting the entire plant; however, following removal of psyllids, plants affected by psyllid yellows show alleviation of symptoms and may even recover (Richards, 1928; Carter, 1939; Sengoda et al., 2010). Plant recovery seems to only occur with shorter feeding durations (under ca. 30 days) (Richards, 1928) and if the plant is not close to maturity (Eyer, 1937). It appears that potato psyllid nymphs need not to have fed previously on symptomatic plants in order to elicit symptoms in healthy plants (Richard and Blood, 1933; Eyer, 1937). Early reports suggesting that nymphal feeding on diseased plants was a prerequisite to producing psyllid yellows in a healthy plant (Binkley, 1929; Eyer and Crawford, 1933) were later called into question (Eyer, 1937; Carter, 1939) by the likelihood that experimental conditions used in these studies (especially light intensity) may not have been conducive to symptom expression (McKay et al., 1933). On the other hand, early reports of transmission through tubers (Shapovalov, 1929) and grafting (Daniels, 1954) suggest that direct psyllid feeding activity may not be necessary to induce psyllid yellows symptoms. However, successive grafts resulted in gradual recovery of affected plants (Daniels, 1954), and tuber transmission was not observed in subsequent investigations (Schaal, 1938). It should be noted that all evidence that psyllid yellows is caused by a salivary toxin has been circumstantial; the suspected toxin has yet to be identified despite several attempts to do so (Carter, 1954; Daniels, 1954; Abernathy, 1991). Sengoda et al. (2010) did not detect Lso in plants with psyllid yellows symptoms, but this does not rule out the possible role of another liberibacter or another pathogen altogether, or the possibility of false negatives with PCR (Arp et al., 2013). Clearly more work is needed to understand the pathology of psyllid yellows. However, recent decades have shifted attention to a different disorder associated with potato psyllids: zebra chip disease.

6.2.4.2 Zebra chip disease 6.2.4.2.1 Symptoms Zebra chip disease (ZC) was first officially identified in commercial potato fields near Saltillo, Mexico in 1994 (Gudmestad and Secor, 2007). Aboveground symptoms are similar to those of psyllid yellows and include chlorosis and purpling of foliage, twisted stems, swollen nodes, aerial tubers, vascular discoloration, and leaf scorching and wilting (Secor et al., 2006, 2009; Munyaneza et al., 2007b; Sengoda et al., 2010, Figs. 6.5 and 6.6). Affected tubers show distinctive belowground symptoms as well, including enlarged lenticels and collapsed stolons (Gudmestad and Secor, 2007). However, the primary tuber symptoms are manifested as brown discoloration of the vascular ring and medullary rays that are initially expressed at the stolon attachment end but eventually extend through the tuber (Secor et al., 2006, 2009; Munyaneza et al., 2007b; Sengoda et al., 2010, Figs. 6.7 and 6.8). This discoloration is observed as striped necrotic patterns through the

FIG. 6.5 Chlorosis of foliage in potato with zebra chip disease. Photo: E.J. Wenninger.

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FIG. 6.6 Chlorosis, purpling, and curling of foliage in potato with zebra chip disease. Photo: E.J. Wenninger.

FIG. 6.7 Tuber symptoms of zebra chip disease in potato include brown discoloration through the entire length of the tuber (infected tuber above; healthy tuber below). Photo: E.J. Wenninger.

FIG. 6.8 Sliced tuber with zebra chip disease. Photo: E.J. Wenninger.

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length of tubers, a diagnostic symptom that separates ZC from other potato diseases (Secor et al., 2009) and led to the name “zebra chip.” The disease is referred to as “papa manchada” (stained potato) in Mexico and “papa rayada” (striped potato) in Guatemala and other Latin American countries (Gudmestad and Secor, 2007). Tuber symptoms are more pronounced in fried products (e.g., French fries and potato chips or crisps), rendering them unmarketable due to burnt appearance and unpleasant taste (Figs. 6.9 and 6.10).

FIG. 6.9 Fresh (left) and fried (right) chips processed from tubers with zebra chip disease. Photo: E.J. Wenninger.

FIG. 6.10 Fries processed from tubers with zebra chip disease. Photo: E.J. Wenninger.

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6.2.4.2.2 Liberibacter, the putative causal agent of ZC The identity of the bacterium associated with ZC was first reported in 2008 (Hansen et al., 2008; Liefting et al., 2008). Hansen et al. (2008) designated the bacterium “Candidatus Liberibacter psyllaurous” shortly before Liefting et al. (2008) identified the same bacterium (Wen et al., 2009) and proposed the name “Candidatus Liberibacter solanacearum” (Lso) (Liefting et al., 2009b). Of these two synonyms, the latter name has been used more widely in the literature, perhaps because the authors argued that the bacterium is the causal agent of zebra chip disease (Liefting et al., 2008, 2009a,b) rather than psyllid yellows (Hansen et al., 2008). “Ca. Liberibacter” species are gram-negative a-proteobacteria that have not been cultured; thus, Koch’s postulates cannot yet be fully validated. Potato psyllids were implicated in transmission of the putative causal agent of ZC as early as 2006e07 (Goolsby et al., 2007a; Munyaneza et al., 2007a,b) and confirmed as the vector of Lso shortly thereafter (Secor et al., 2009; Sengoda et al., 2010). 6.2.4.2.3 Lso haplotypes Ten different haplotypes of Lso have been described to date: haplotypes A, B, C, D, E, F, G, H (Apiaceae and Polygonaceae), H (Convolvulaceae), and U (Nelson et al., 2011, 2013; Teresani et al., 2014; Haapalainen et al., 2018b; Mauck et al., 2019; Swisher Grimm and Garczynski, 2019; Contreras-Rendón et al., 2020; Haapalainen et al., 2020) by SNPs on the 16s rRNA, 16s/23s ISR and 50s rplJ, and rplL ribosomal protein genes. Four of these haplotypes are associated with solanaceous species: A, B, F, and G. Haplotypes A and B are known to be vectored by potato psyllids and infect solanaceous crops, including potato, tomato, pepper, eggplant, tomatillo, tamarillo, and tobacco (Munyaneza, 2015). Recent reports show that haplotype B can cause more severe symptoms in its solanaceous hosts when compared to haplotype A (Mendoza-Herrera et al., 2018; Swisher Grimm et al., 2018; Harrison et al., 2019, 2020). Numerous weeds, primarily in the Solanaceae, have been found to harbor Lso and/or to be infected with Lso by potato psyllids, though the haplotype has not been identified in all studies (Wen et al., 2009; Murphy et al., 2014; Thinakaran et al., 2015a; Torres et al., 2015; Vereijssen et al., 2015; Cooper et al., 2019a; Contreras-Rendón et al., 2020). Haplotype F was identified from one potato tuber sample from southern Oregon (Swisher Grimm and Garczynski, 2019); it is presumably vectored by potato psyllids as well, though this has not been tested. Haplotype G was identified from an herbarium sample of a host of the potato psyllid, Solanum umbelliferum, so details on its transmission also are not known (Mauck et al., 2019). The available evidence suggests that the other haplotypes of Lso are of limited importance in the epidemiology of ZC. Haplotypes C, D, and E infect various apiaceous plants (notably carrot, Daucus carota, and celery, Apium graveolens) in several countries in Europe, the Mediterranean region, and in the United Kingdom (Munyaneza et al., 2010a,b; AlfaroFernández et al., 2012a,b; Nelson et al., 2013; Nissinen et al., 2014; Tahzima et al., 2014; Teresani et al., 2014). Haplotype C occurs in northern Europe and is vectored by Trioza apicalis (Nissinen et al., 2014). Haplotypes D and E occur in the Mediterranean region to southern Europe and are vectored by Bactericera trigonica (Nelson et al., 2013; Teresani et al., 2014; Antolinez et al., 2017). There is some geographical overlap in the distribution of the two vectors (EPPO, 2020). In greenhouse experiments, B. trigonica was reported to transmit Lso haplotype E to potato at low rates, but showed very limited settling, oviposition, and feeding rates on potato (Antolinez et al., 2017). Another psyllid, B. nigricornis, can reproduce on carrot and is the only known psyllid species in Europe that can reproduce on potato (Antolinez et al., 2019), so there exists potential for movement of Lso between these two crops by this species. Teresani et al. (2015) reported that B. nigricornis collected from carrot crops in Spain tested positive for Lso (presumably haplotype E). Moreover, Antolinez et al. (2019) reported preliminary evidence that B. nigricornis can indeed transmit Lso haplotype E to both carrot and potato and produce typical disease symptoms; however, the details of this work are still forthcoming and the importance of such transmission in the epidemiology of ZC in potato remains to be explored. Greenhouse experiments with T. apicalis showed no transmission of haplotype C to potato, though this haplotype was observed in fieldcollected potato and successful transmission was achieved through dodder and grafting; nevertheless, potato plants harboring Lso haplotype C exhibited no symptoms characteristic of ZC (Haapalainen et al., 2018a). Thus, although at least haplotypes C and E may be found in potato, the risk of natural infection appears to be limited. There is a report of haplotype C associated with ZC-like symptoms in commercial potato in Spain, but few details have been published (EPPO, 2017). The low risk currently posed to potato by Lso haplotypes associated with apiaceous species may be due to limited effects of those haplotypes on potato and/or the lack of an efficient psyllid vector that feeds on both solanaceous and apiaceous hosts. Two recently discovered Lso haplotypes, both named haplotype H due to concurrent publication (Contreras-Rendón et al., 2020; Haapalainen et al., 2020), might similarly pose little risk to potato given their observations in plants in the Apiaceae, Polygonaceae, and Convolvulaceae, but too little is known about these haplotypes to be certain. The last Lso haplotype considered here, haplotype U, was found in stinging nettle, Urtica dioica, and in the psyllid Trioza

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urticae (Haapalainen et al., 2018b), but transmission by this psyllid to stinging nettle or other hosts has not been investigated nor has pathogenicity to potato been studied. It is likely that the host range of T. urticae similarly limits any risk of this haplotype to potato. 6.2.4.2.4 Geographic distribution Following the first report of ZC in 1994, the disease was not reported in the US until 2000, after it was found in commercial potato fields in the Pearsall and Lower Rio Grande Valley areas of Texas (Secor and Rivera-Varas, 2004; Gudmestad and Secor, 2007; Crosslin et al., 2010). By 2004, ZC incidence was as high as 80% in some fields in northeastern Mexico (Gudmestad and Secor, 2007) and was causing considerable economic damage in southwestern Texas (CNAS, 2009). Following its discovery in Texas, observation of ZC spread throughout the Central and Western US. By 2007, symptomatic potatoes were reported from Nebraska, Colorado, Kansas, New Mexico, Arizona, Nevada, and California (Munyaneza et al., 2007a). ZC was identified in Idaho, Washington, and Oregon at the end of the 2011 growing season (Hamm et al., 2011; Nolte et al., 2011; Crosslin et al., 2012a,b). The disease was also reportedly found in Wyoming (Munyaneza et al., 2011) and Utah (Nischwitz et al., 2015) and was reported from Alberta, Canada in 2017 (Henrickson et al., 2019). Lso haplotypes A and B have been observed in North America (Fig. 6.4). Similar to the spread across the US, reports of ZC symptoms and/or Lso in potato were reported in several Central American countries following the initial observation in Mexico (Fig. 6.4). The disease had been previously reported from Guatemala (Secor and Rivera-Varas, 2004) and was subsequently reported from Honduras as early as 2006 (Rehman et al., 2010), Nicaragua in 2011 (Bextine et al., 2013b), and El Salvador in 2012 (Bextine et al., 2013a). Lso haplotypes A and B have been observed in Mexico, whereas haplotype A has been observed in Central America. At least three countries outside of the native range of the potato psyllid have reported introductions of both the potato psyllid and Lso damaging solanaceous hosts (Fig. 6.4). Lso was reported in potato in New Zealand (Liefting et al., 2008) not long after the initial detection of the potato psyllid (Gill, 2006) and soon was widely observed across the country (Teulon et al., 2009). During 2013, Lso haplotype A was collected from tomato plants on Norfolk Island, Australia (Thomas et al., 2018), and the next year potato psyllids were collected from potato and tomato plants (Maynard et al., 2018). Recently, potato psyllids and ZC-infected potato were reported in potato for the first time in South America (Ecuador) (Castillo Carrillo et al., 2019). In all of these introductions, only Lso haplotype A has been reported. 6.2.4.2.5 Epidemiology Although Lso is primarily recognized as a vector-borne plant pathogen, it can also be transmitted through grafting (Secor et al., 2009) or through propagated seed pieces (Pitman et al., 2011) at least in potato. Grafting is not a common practice in solanaceous crops, so this means of transmission plays no practical role in ZC epidemiology. However, potato is a vegetatively propagated crop, which has raised some serious concerns, especially regarding ZC spread into other potato growing regions via infected seed pieces through commercial trading. Early studies on tuber transmission showed conflicting results, with Pitman et al. (2011) reporting high incidence of Lso in plants grown from ZC-infected seed pieces and Henne et al. (2010c) reporting low incidence of Lso in such plants. The potential for ZC spread through seed pieces became more concerning as later studies revealed that the pathogen and ZC symptoms continue to develop in affected potato tubers after harvest (Rashed et al., 2015) and during cold storage (Wallis et al., 2017; Rashed et al., 2018; Wenninger et al., 2020). More recent studies on tuber transmission, however, have concluded that ZC spread, and introduction into new regions through seed potato is unlikely to occur (Rashed et al., 2015; Harrison et al., 2020; Swisher Grimm et al., 2020). This conclusion, consistent with Henne et al. (2010c), was based on the findings that most Lsoinfected tubers fail to germinate, and those that do germinate produce “hair sprouts” that lead to stunted, nonvigorous plants that usually die soon after emergence and rarely harbor Lso (Rashed et al., 2015; Harrison et al., 2020; Swisher Grimm et al., 2020). Thus, from an epidemiological standpoint, the likelihood of disease introduction and spread through seed pieces is low (Henne et al., 2010c; Rashed et al., 2015; Harrison et al., 2020; Swisher Grimm et al., 2020). Therefore, the primary epidemiological factors that predict patterns of ZC distribution and pathogen spread include the presence of potato psyllids and their interactions with Lso and their host plants within the environment. Knowledge of vector/plant pathogen interactions in the ZC pathosystem at different ecological scales continues to expand, which will improve our understanding of Lso spread and ZC epidemiology. At the same time, discoveries of additional haplotypes of both Liberibacter and potato psyllids have revealed greater complexity of this system just as epidemiological studies have only begun to gain traction among researchers. Potato psyllids can transmit Lso as both adults and nymphs, but adults are more efficient vectors of the pathogen (Buchman et al., 2011), and adults have higher titers of Lso (Casteel et al., 2012; Cooper et al., 2014). There have been

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limited studies demonstrating transovarial transmission of Lso to offspring at relatively high rates (Hansen et al., 2008; Casteel et al., 2012). Such transmission may contribute to spread of the pathogen within and among fields, depending on how far females disperse while actively ovipositing. Provided their vector efficiency and mobility, adult psyllids are the major life stage of concern for disease spread, especially among fields and across regions. Lso spread is influenced by various abiotic and biotic environmental variables, with ambient temperature being among the most studied. Temperature can greatly impact both Lso development (Munyaneza et al., 2012b) and potato psyllid life history, thus heavily influencing interactions among the three biotic elements of the ZC disease triangle: the psyllid vector, the solanaceous host, and Lso. For instance, Lso development slows considerably in temperatures below 17
C and stops when temperatures exceed 32
C (Munyaneza et al., 2012b). Temperatures that approach or exceed 32
C also negatively affect potato psyllids, severely constraining oviposition and survival (List, 1939; Pletsch, 1947; Wallis, 1955; Abdullah, 2008; Tran et al., 2012; Lewis et al., 2015). Therefore, fluctuations in temperature can affect the nature of Lso/plant interactions as well as vector life history traits, influencing the likelihood of Lso persistence in the environment, which will ultimately drive patterns of Lso spread. Lso transmission success by its potato psyllid vector relies on effective acquisition of the pathogen from an infected host and inoculation of a healthy plant after a latent period. The potato psyllid is a persistent vector of Lso (Hansen et al., 2008; Pearson et al., 2010; Cooper et al., 2014; Sengoda et al., 2014). After acquiring Lso, the pathogen continues to multiply and circulate throughout the insect body, eventually translocating to the salivary glands (Sengoda et al., 2014). This process takes about 2 weeks (Sengoda et al., 2014) and coincides with a plateauing of Lso titer increase in psyllids (Sengoda et al., 2013). Thus, potato psyllids acquiring Lso from potato experience a latent period of about 2 weeks before they become “infective.” Tang et al. (2020) reported a slightly longer latent period of at least 17 days for psyllids on tomato. Lso can be inoculated into a new host plant as an infective potato psyllid salivates during the process of feeding on the plant sap (Pearson et al., 2010). Infective adult potato psyllids can inoculate a host plant within an hour of feeding, but inoculation success increases with feeding time (Buchman et al., 2011; Sengoda et al., 2013). An inoculation efficiency of 21% has been reported for a single adult potato psyllid within 24 h (Buchman et al., 2011), with the potential of exceeding 70% within 48 h of feeding (Rashed et al., 2012). Transmission rates of up to 100% have been reported where multiple psyllids feed on the potato host for extended periods (Buchman et al., 2011; Rashed et al., 2012). Although the number of infective potato psyllids does not seem to strongly affect ZC progress or symptom severity (Gao et al., 2016; Wenninger et al., 2020), feeding by multiple Lso-positive vectors could result in a shorter disease incubation time (Rashed et al., 2012). In the field, the onset of foliar symptoms of ZC is generally between three to 4 weeks after successful inoculation; tuber symptoms, on the other hand, may appear within 2 weeks of infection (Rashed et al., 2014). In potatoes, it has also been demonstrated that Lso is heterogeneously distributed among leaflets and other tissue types within the host plant (Wen et al., 2009; Lévy et al., 2011; Cooper et al., 2015a), a variability which can potentially influence potato psyllid exposure to Lso and its efficiency in acquiring the pathogen (Rashed et al., 2012; Vereijssen et al., 2018). Potato psyllids can feed on any aboveground tissues of their solanaceous host; however, in potatoes they tend to concentrate on top and middle parts of their host (Butler and Trumble, 2012b; Martini et al., 2012; Walker et al., 2013). Acquisition rates are relatively high when psyllids are restricted to stems or leaf petioles, though highest when psyllids have unrestricted access to the whole plant (Rashed et al., 2012). In addition to acquisition success and transmission efficiency, spatiotemporal movement of potato psyllids is a crucial component in predicting pathogen spread given that psyllid and ZC distribution patterns across fields are typically clustered (Henne et al., 2012; Henne and Thinakaran, 2020). Early season buildup of potato psyllid populations in natural vegetation around fields (Workneh et al., 2012) as well as in volunteer potatoes (Hill, 1947; Wallis, 1955) likely contributes to the initially greater abundance of psyllids on the edges of fields (Jensen, 1939; Wallis, 1955; Cranshaw, 1994; Butler and Trumble, 2012b). This “edge effect” has not been observed for psyllid densities in New Zealand (Vereijssen et al., 2018), though at least initially higher prevalence of ZC has been observed on field edges in both the US (Workneh et al., 2012) and New Zealand (Vereijssen et al., 2018), with ZC later spreading into inner parts of fields (Workneh et al., 2012). Another factor that may contribute to the uneven distribution or patchiness of the disease within a field is that once psyllids find a suitable host, they typically do not actively search for another host plant (Rashed et al., 2014) as long as environmental conditions are suitable. Nevertheless, adults psyllids are capable of dispersing considerable distances within potato fields over relatively short time periods (Henne et al., 2010b). Potato psyllid dispersal and biology can also be influenced by the presence or absence of Lso within psyllids and hosts. Lso infection can manipulate host plant physiology, mediated by qualitative and quantitative changes in volatile organic compounds (Davis et al., 2012; Mas et al., 2014). Lso-infected host plants are shown to be more attractive to noninfective (“healthy”) potato psyllids; however, upon Lso acquisition, potato psyllids shift their preference toward Lso-negative

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plants (Davis et al., 2012; Mas et al., 2014). Changes in volatiles emitted by hosts in response to Lso infection are plantspecific but critical in host selection by potato psyllids (Davis et al., 2012; Mas et al., 2014). This Lso-manipulated behavioral response of psyllids should facilitate a higher rate of pathogen spread within a field. This may on balance be beneficial for Lso, but there are fitness costs to the vector carrying the pathogen (Nachappa et al., 2012; Thinakaran et al., 2015b; Yao et al., 2016). Lso has been shown to negatively impact potato psyllid reproductive output and survival (Nachappa et al., 2012, 2014; Thinakaran et al., 2015b), with haplotype B of Lso having a greater impact on psyllid fitness than haplotype A. Recent studies have begun to delineate differences in replication, transmissibility, and virulence between Lso haplotypes A and B. For example, Tang et al. (2020) reported faster replication in the psyllid gut, a shorter latent period, and higher transmission rates for Lso haplotype B relative to haplotype A. In addition, Lso haplotype B has been shown to be more virulent than haplotype A, producing greater disease incidence in tubers, more severe symptoms, and greater reduction in tuber yield (Swisher Grimm et al., 2018; Harrison et al., 2019, 2020). Moreover, plants propagated from Lso B-infected tubers generally show poorer emergence and produce lower daughter tuber yields than those from Lso Ainfected tubers (Swisher Grimm et al., 2020). Despite greater fitness costs to the vector from Lso haplotype B and reduced tuber yields, greater virulence and transmissibility of Lso B might be contributing factors in the increased prevalence of this haplotype over time in southern Idaho (Dahan et al., 2017, 2019). More work will be needed to understand how the epidemiologies of ZC associated with these Lso haplotypes compare and whether such changes in relative prevalence of haplotypes has occurred elsewhere. Another component of ZC epidemiology in need of further research is the role of alternative host plants that may serve as reservoirs of Lso. Many noncrop solanaceous hosts have been found to harbor Lso (Wen et al., 2009; Murphy et al., 2014; Thinakaran et al., 2015a; Vereijssen et al., 2015; Cooper et al., 2019a). Such hosts likely contribute to spread of the pathogen and, in the case of perennials, to overwintering of Lso and carryover of the pathogen from season to season. The association of Lso of various haplotypes with other species of psyllids further complicates the epidemiological picture, especially when overlaps in host plant use by different psyllid species creates the possibility of “cross-transmission” of the pathogen. For example, Lso can be transmitted between Bactericera maculipennis and potato psyllids when both are feeding on plants within the Convolvulaceae, despite the lack of host suitability of potato to B. maculipennis (Borges et al., 2017). Similar cross-transmission scenarios between potato psyllids and other psyllid species via shared hosts (see “Section 6.3” below) require further exploration to clarify their roles in ZC epidemiology. 6.2.4.2.6 Economic impact Damage from ZC was initially of sporadic importance following its discovery (Munyaneza and Henne, 2013). First reported in the US in 2000 (Secor and Rivera-Varas, 2004), by the mid-2000s ZC was causing millions of dollars in losses to potato growers in the US, Mexico, and Central America (Munyaneza et al., 2007a,b; Crosslin et al., 2010). ZC has been estimated to reduce the value of Texas potato production by ca. 33 million USD annually (CNAS, 2009). During 2009e11, growers in Texas were spending an average of 740 USD per hectare annually on insecticide applications for potato psyllid control and those in Kansas and Nebraska were spending ca. 700 USD per hectare (Guenthner et al., 2012). During 2014, growers in Idaho and the Columbia Basin of Washington and Oregon were estimated to have spent a total of 11 million USD on additional insecticide applications targeting ZC management (Greenway and Rondon, 2018). Studies on the detailed economic effects of ZC in other countries are lacking, but likely have also been substantial given the similar increases in insecticide applications reported (Secor et al., 2009; Munyaneza, 2012). During just the first 4 years after the introduction of potato psyllids to New Zealand, millions of dollars had been lost to increased management costs, crop losses, and loss of export markets (Teulon et al., 2009). Despite multiple insecticide applications aimed at ZC management, producer revenues may still be affected by yield losses, quality losses, and rejections of potatoes by processors (Guenthner et al., 2012). The tuber defect resulting from ZC reduces tuber quality, limiting the market value or even rendering some products unmarketable (CNAS, 2009; Munyaneza et al., 2007a, 2008). In addition to quality losses, yield reductions can be severe as well, especially if infection occurs early in the season, at or before the tuber initiation stage (Rashed et al., 2014). In some cases, the prevalence and severity of ZC infection has led to the abandonment of entire fields (Munyaneza et al., 2007a,b; Crosslin et al., 2010), though for less severe cases a lower market class may be pursued. Management of ZC in potato is heavily dependent on insecticides to reduce vector numbers, and increased costs associated with insecticide applications targeting potato psyllids have contributed substantively to the economic effects of ZC (Patterson, 2012, 2014; Greenway, 2014; Greenway and Rondon, 2018).

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6.2.5 Management 6.2.5.1 Monitoring Management of ZC in potato currently relies largely upon insecticides to suppress potato psyllid numbers. Because infestations can be unpredictable in space and time, considerable effort has been aimed at monitoring potato psyllids to determine the need for and timing of insecticide applications. Monitoring tools have included sweep nets, colored sticky traps, beat sheets, vacuum samplers, suction traps, and direct examination of plants; the latter has been the most common approach for monitoring immature stages. Sweep nets were used extensively in early studies to sample adult potato psyllids from potato and other hosts (e.g., Knowlton and Janes, 1931; Pletsch, 1947; Wallis, 1948). Suction traps have been used successfully for areawide monitoring of alate aphids but have been reported to capture few potato psyllids even when local populations are high (Cranshaw, 1994). Suction traps were among the tools used to detect potato psyllid distributions across New Zealand (Teulon et al., 2009), though they would not be practical for monitoring at a local farm level. Recent studies have often featured yellow sticky traps for monitoring adult potato psyllids (Al-Jabr and Cranshaw, 2007; Goolsby et al., 2007a,b; Teulon et al., 2009; Walker et al., 2011b; Echegaray and Rondon, 2017; Wenninger et al., 2017; Djaman et al., 2020). Yellow sticky traps have been shown to be more attractive than several other colors in trials in potato (Taylor et al., 2014) and in greenhouse-grown tomato (Al-Jabr and Cranshaw, 2007). Also in greenhouse tomato, Hodge et al. (2019) reported that adding ultraviolet illumination increased captures for all colors tested. In potato, Yen et al. (2013) showed that yellow sticky traps and yellow pan traps captured more psyllids and were more efficient than sweep net samples, vacuum samples, and direct searching. Goolsby et al. (2007b) and Wenninger et al. (2017) also found vacuum sampling in potato to often capture fewer psyllids than yellow sticky traps. Although sticky traps appear to outperform sweep net and vacuum samples, sticky trap captures in a crop likely primarily reflect dispersal into that crop, whereas vacuum samples are thought to reflect colonization of psyllids within the crop (Goolsby et al., 2007b; Wenninger et al., 2017). Thus, the relative efficacy of different trapping tools is partly related to the phenology of the psyllid assemblages within a given sampling target. Vacuum and beat sheet sampling can be useful approaches for sampling adults on alternative host plants where active dispersal may be less prevalent than in potato (Thinakaran et al., 2017; Wenninger et al., 2019). However, sticky traps have an advantage over many other tools in that they are “passive” traps, requiring little time to deploy and retrieve, but capturing psyllids over several days in the interim. Recently, a trap was developed using a three-dimensional printer, designed to collect psyllids directly into a preservative fluid (Horton et al., 2019). Although Lso detection rates were improved with higher quality and quantity of DNA (Wentz et al., 2020), the current design of the trap was not as effective as yellow sticky traps at capturing psyllids (Horton et al., 2019). While various sampling tools have been used to monitor adult psyllids, the primary approach to monitor eggs and nymphs has been direct observation of plants. Early efforts to elucidate noncrop breeding hosts of potato psyllids featured extensive examinations of plants for immature stages (e.g., Richards and Blood, 1933; Janes, 1937; Wallis, 1955). Although a leaf-washing method was developed for counting nymphs in potato (Martini et al., 2012), direct inspection of leaf samples continues to be the standard approach to monitor immature stages of potato psyllids (Goolsby et al., 2007a; Cameron et al., 2009; Munyaneza et al., 2009; Workneh et al., 2014; Echegaray et al., 2015; Wenninger et al., 2017). Nymphs are typically found on the lower surface of the leaf (Binkley, 1929; Lehman, 1930; Butler and Trumble, 2012b), but may be found on the upper surface as well, especially if the leaf is shaded. Eggs are also typically found on the lower leaf surface or on leaf margins (Pletsch, 1947). Martini et al. (2012) reported that nymphs tended to be more prevalent within the middle third of the canopy, whereas Butler and Trumble (2012b) observed psyllids primarily within the top and middle of the canopy. Walker et al. (2013) reported that counting nymphs within the top half of the plant or, failing that, a middle leaf, gave reliable estimates of densities on the entire plant. Ultimately, the aim of sampling potato psyllids in potato is to determine whether and when to apply insecticides or take other management steps to mitigate risk of damage. Therefore, the key to any sampling approach is whether it provides an accurate assessment of psyllid densities and risk of damage. Pletsch (1947) found that psyllid densities from sweep net samples correlated with prevalence of psyllid yellows. However, ZC risk may be less strongly tied to psyllid densities partly due to the high temporal and spatial variability in Lso incidence among psyllids (Goolsby et al., 2012; Dahan et al., 2017, 2019; Wenninger et al., 2017, 2019). Indeed, Workneh et al. (2013) found that environmental factorsdnot densities of psyllids or even densities of Lso-positive psyllidsdwere the strongest predictors of ZC occurrence across Texas, Kansas, and Nebraska. In a study in Oregon, Echegaray et al. (2015) reported a correlation between Lso-positive psyllid abundance and ZC incidence in only one of 2 years. Nevertheless, lower densities of potato psyllids have generally been associated with lower incidences of ZC (Goolsby et al., 2007a; Wenninger et al., 2017). Studies in New Zealand showed a

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correlation between adult abundance on yellow sticky cards and the presence or absence of nymphs, though not with abundance of nymphs (Cameron et al., 2009). Walker et al. (2015) showed a correlation between potato psyllid densities and ZC prevalence and proposed an action threshold of >3 adult potato psyllids per yellow sticky to maintain ZC incidence around 1%. Thresholds based on nymph counts showed that an average of one or more nymphs per leaf resulted in commercially unacceptable levels of damage (4%e9%). Butler and Trumble (2012b) developed binomial sequential sampling plans for psyllid nymphs in potato, suggesting that a hypothetical threshold of 0.5 or one nymph per leaf could be a reliable sampling approach. However, thresholds have yet to be worked out for potato psyllids in the USA. In order to more accurately account for risk of ZC, any action threshold ideally would consider both potato psyllid numbers and incidence of Lso within psyllids, which would require a rapid diagnostic assay. Monitoring protocols focused on plant samples should consider the aggregated distribution of psyllids and ZC infection within fields (Butler and Trumble, 2012b; Henne et al., 2012; Henne and Thinakaran, 2020), including potentially greater densities on field edges (Jensen, 1939; Wallis, 1955; Cranshaw, 1994; Butler and Trumble, 2012b). Walker et al. (2015) also evaluated the utility of the degree-day model developed from New Zealand populations of potato psyllids (Tran et al., 2012) to predict risk. They found the model to be unreliable as a stand-alone tool, perhaps related to the difficulty of using a biofix date in a region in which potato psyllids are actively breeding all year. Similarly, the degree-day model developed using a Texas population of potato psyllids (Lewis et al., 2015) could not predict first occurrence of psyllids in the crop given that they are present at emergence; however, the model could contribute to population assessments when integrated with standard monitoring protocols. Degree-day models for potato psyllids remain to be validated in other, more temperate growing regions. Earlier attempts to predict expected population densities of potato psyllids involved preseason sampling of matrimony vine (Wallis, 1955). More recently, Cooper et al. (2019b) confirmed the dispersal of potato psyllids from matrimony vine in association with onset of summer dormancy of this host. However, the value of this approach to predict potato psyllid infestations in potato may be limited by the complicated phenology and wide alternative host range of potato psyllids. Moreover, matrimony vine has been eradicated in some areas to reduce potato psyllid harborages; therefore, other plants may have to be used for such preseason population forecasting (Cranshaw, 1994).

6.2.5.2 Insecticides Both psyllid yellows and ZC have been managed primarily through application of insecticides to suppress populations of the psyllid itself. The first used chemical control, lime-sulfur (List, 1917) and later sulfur dust (List, 1935), became widely used by the 1930s and 1940s, but its utility was limited somewhat by its apparent phytotoxicity (Cranshaw, 1994). Other effective chemical controls that emerged later for management of psyllid yellows have included many organophosphates (e.g., diazinon, acephate, phorate) and pyrethroids, the carbamate aldicarb, and the organochlorine endosulfan (reviewed by Butler and Trumble, 2012c). Applications of many of these broad-spectrum chemistries have diminished over the years in favor of alternative chemistries with improved worker safety and lesser effects on beneficial insects. As the association between potato psyllids and ZC was becoming clear, at-plant application of a neonicotinoid insecticide had begun to be the standard practice as part of psyllid insecticide programs (Goolsby et al., 2007a). The neonicotinoids imidacloprid anddto a lesser extentdthiamethoxam have continued to be among the most used insecticides for management of psyllids and other insects in potato throughout the US (Guenthner et al., 2012; Greenway and Rondon, 2018). Typically, these insecticides are applied at planting, though they are labeled for multiple uses, including foliar applications (Prager et al., 2013b). In addition to killing the insects, psyllids on imidacloprid-treated plants alter their settling and feeding behaviors and show reduced pathogen transmission (Butler et al., 2011a, 2012). Efficacy of at-plant applications is sensitive to both application method and irrigation rates (Prager et al., 2013b). Moreover, at-plant neonicotinoid applications are expected to diminish in efficacy over the season, which may be problematic in areas such as the Pacific Northwest USA where potato psyllids arrive in greater abundance late season. Abamectin and spirotetramat are also widely used insecticides for potato psyllid management (Guenthner et al., 2012; Greenway and Rondon, 2018). Although its residual activity may be relatively short-lived in the field (Gharalari et al., 2009), abamectin is among the most efficacious knockdown chemistries (Berry et al., 2009; Gharalari et al., 2009) and reduces both oviposition and feeding activity (Gardner-Gee et al., 2012; Mustafa et al., 2015a). Spirotetramat has shown long residual activity against nymphs, at least on pepper plants in the greenhouse (Page-Weir et al., 2011), and some reduction in oviposition on potato (Gardner-Gee et al., 2012). However, spirotetramat showed little or no effects on adult mortality (Page-Weir et al., 2011; Gardner-Gee et al., 2012), took some time to show efficacy against nymphs (Page-Weir

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et al., 2011), and showed no significant effect on Lso transmission in potato (Barnes et al., 2014). This underscores the importance of considering the life stages present in the crop when selecting an insecticide. Other products that have shown efficacy and considerable use against potato psyllids in recent years in potato include pymetrozine, flonicamid, and spiromesifen. Pymetrozine may not readily kill psyllids (Berry et al., 2009; Prager et al., 2016); however, its antifeedant and repellant activity (Butler et al., 2011a) is expected to negatively affect Lso transmission. Little has been published in the primary literature on effects of flonicamid on potato psyllids, but effects might be similar to those of pymetrozine given the similar modes of action. Similarly, the efficacy of spiromesifen is presumably not unlike that of spirotetramat given that they have identical modes of action; spiromesifen has been reported to show residual activity against nymphs up to 1 week after application, though no strong knockdown effect (Berry et al., 2009). Some relatively new insecticidesdcyantraniliprole, spinetoram, and sulfoxaflordshowed knockdown and residual activity against adults in greenhouse trials, and the former also reduced survival of nymphs (Gardner-Gee et al., 2012; Echegaray et al., 2017); however, in another study cyantraniliprole did not show a reduction in Lso transmission (Barnes et al., 2014). Cyantraniliprole, sulfoxaflor, and tolfenpyrad have all shown reductions in settling, feeding, and/or oviposition behavior (Gardner-Gee et al., 2012; Mustafa et al., 2015a; Echegaray et al., 2017). Pyrethroid insecticides also have been widely used for potato psyllid management in potato, and certain carbamates have been effective as well (Cranshaw, 1994; Butler and Trumble, 2012c; Echegaray et al., 2017); however, both insecticide groups may also flare potato psyllid populations. Cranshaw (1985) reported that the carbamate methomyl lead to increased densities of potato psyllids, and more recently Prager et al. (2016) showed similar increases with weekly sprays of a combination of methomyl and the pyrethroid permethrin. The association of higher potato psyllid densities with broad-spectrum insecticide applications may be related to the negative effects of such applications on natural enemies of potato psyllids (Cranshaw, 1985; Rojas et al., 2015; Prager et al., 2016). In addition to the synthetic insecticides described above, several alternative chemical controls have been studied for potato psyllid management. For example, kaolin particle film negatively affected settling and probing behavior of psyllids (Butler et al., 2011a; but see Prager et al., 2013a) and showed modest reductions in oviposition on potato (Prager et al., 2013a) and reductions in all life stages on tomato under field conditions (Peng et al., 2011). However, kaolin did not reduce Lso transmission in the lab (Butler et al., 2011a), nor did it reduce psyllid populations or ZC incidence in a field trial (Wright et al., 2013). In the lab, horticultural oils and mineral oils have been shown to reduce settling and probing behavior (Butler et al., 2011a), reduce survival of nymphs (Jorgensen et al., 2013), and slightly reduce Lso transmission (Barnes et al., 2014). Incorporation of a crop oil into an insecticide program reduced potato psyllid densities and ZC incidence relative to an insecticide-only program with more sprays (Wright et al., 2017). Numerous plant essential oils have been shown to repel females and deter oviposition in laboratory trials (Walker et al., 2011a; Diaz-Montano and Trumble, 2013) and even reduce field populations, but trials evaluating effects of plant essential oils on ZC prevalence in the field remain to be further explored. Many of the alternatives to broad-spectrum insecticides are unlikely to provide standalone control of ZC but show promise in incorporation with other integrated pest management (IPM) tools. Indeed, the development of resistance in potato psyllids to several insecticide modes of action underscores the need to explore alternative management strategies. Potato psyllids collected from fields in Mexico during 2006, shortly after the major onset of ZC outbreaks in Mexico and Texas, were still highly susceptible to abamectin, neonicotinoids, and numerous pyrethroids (Vega-Gutiérrez et al., 2008). However, studies conducted on potato psyllids collected during 2005 showed that California populations had lower susceptibility to imidacloprid and spinosad (but not spiromesifen) relative to Texas populations (Liu and Trumble, 2007). By 2012, potato psyllids collected from Texas fields were more than 3 times less susceptible to imidacloprid than a laboratory colony initiated from 2006 collections (Prager et al., 2013b), demonstrating clear evidence of resistance. Cerna et al. (2013) and Cerna Chávez et al. (2015) reported resistance to abamectin with more than 10-fold lower susceptibility in some Mexican populations of potato psyllids, but much more modest reductions in susceptibility to endosulfan and imidacloprid. More recently, Szczepaniec et al. (2019) reported that potato psyllids collected during 2016e17 from Colorado, New Mexico, and Texas all showed resistance to imidacloprid, with susceptibility ranging from ca. 5 to 30 times lower than the control population. Resistance to the less widely used neonicotinoid, thiamethoxam, was evident as well, but less pronounced (Szczepaniec et al., 2019). The heavy reliance on insecticides for ZC management coupled with increasing occurrences of insecticide resistance is not sustainable. In addition to rotation of modes of action and incorporation of alternatives to broad-spectrum insecticides into IPM programs, optimization of application timing and coverage can improve the efficacy of available tools (Cranshaw, 1994; Nansen et al., 2011). More information on the relationships among potato psyllid densities, Lso incidence, and ZC prevalence will be needed to develop decision support tools to ensure that insecticides are applied only when justified by risk. New insecticides, including those based on RNAi (Wuriyanghan et al., 2011), will likely be developed to aid in improving efficacy against the target pest. However, the particular insecticide program used might be less important for

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reducing ZC than the need to continue the program for the duration of the season (Goolsby et al., 2007a; Echegaray and Rondon, 2017). Thus, the need for development of alternatives to insecticides in ZC IPM programs will remain.

6.2.5.3 Cultural and physical control Limited options exist for controlling potato psyllids using cultural management, i.e., changing how the crop is grown to make the crop less suitable for the pest or to enhance the ability of the crop to withstand pest attack (Norris et al., 2003). Early reports showed lower psyllid yellows incidence or severity in later potato plantings (Hartman, 1937; Schaal, 1938; Eyer and Enzie, 1939; Starr, 1939). However, Eyer and Enzie (1939) observed that, at least in southern New Mexico, this effect was likely related to higher temperatures later during the growing season being detrimental to psyllid survival. Wallis (1955) reported that in Nebraska by July, temperatures in the foliage of the larger plants in early planted fields were more moderate than in the smaller plants of later planted fields, which likely contributed to the differences in psyllid densities. Interestingly, Goolsby et al. (2007b) and Munyaneza et al. (2012a) also reported lower incidence of ZC in later planted fields in Texas. Whether late planting would be an effective cultural control for potato psyllids may depend upon how local weather conditions affect potato psyllid phenologies. Although this approach would be worth investigating for management of ZC, it may often be impractical given that many other factors often dictate planting dates. Other possible cultural practices include adjusted fertility regimes, elimination of early breeding hosts, and colored plastic mulches, but these approaches would need more study to fully clarify their potential roles in psyllid management. Schaal (1938) observed that susceptibility of plants to psyllid yellows was greater on poor quality, highly alkaline soils. Eyer and Enzie (1939) suggested the possible benefits of supplemental fertilizers to correct alkaline conditions as well as to compensate for nutrient deficits in plants affected by psyllid yellows, but these possible approaches remain to be further studied. Elimination of spring and early summer breeding hosts, including matrimony vine (Cranshaw, 1994), early potato plantings, and volunteer potatoes in cull piles (Hill, 1947) have been promoted, but the value of these practices in reducing potato psyllid infestations into potato are not fully known. Aluminum and white plastic mulches significantly reduce potato psyllid densities, at least in garden tomato plots (Demirel and Cranshaw, 2006), warranting further investigation of this approach in potato. However, white and other colored sprays on potato foliage did not affect psyllid densities in potato (Cranshaw and Liewehr, 1990). In another study that investigated manipulating visual stimuli on potato plants, Merfield et al. (2019) showed that potted potatoes grown under plastic screens that blocked ultraviolet (UV) radiation tended to support fewer potato psyllids than those under screens that did not block UV radiation. Physical control options for potato psyllid management have also been very limited. Mesh crop covers have been shown to physically exclude potato psyllids (Merfield et al., 2015a) and reduce psyllid densities in potato and increase yield and tuber size (Merfield et al., 2015b, 2019). Though this technique is effective, whether it can be economical on a large scale remains to be seen.

6.2.5.4 Biological control Information mostly from laboratory and greenhouse studies indicate that many generalist predators, pathogens, and even specialist parasitoids have long been known to attack potato psyllids. A few studies have shed some light on the role of these natural enemies in the field. Early work in the US, especially by Knowlton and colleagues in the 1930s, began to catalog the generalist predators collected from potato that fed upon potato psyllids at least in laboratory settings, which included various species within the Chrysopidae, Coccinellidae, Anthocoridae, Geocoridae, Nabidae, Miridae, and Syrphidae (Knowlton, 1933a,b, 1934a; Knowlton and Allen, 1936). Numerous recent laboratory and greenhouse studies in North America and New Zealand also have focused on suitability of potato psyllids as prey for various predators, including the lacewings Chrysopera carnea (Ail-Catzim et al., 2012, 2018) and Micromus tasmaniae (MacDonald et al., 2016), five lady beetle species (O’Connell et al., 2012; Pugh et al., 2015; MacDonald et al., 2016), the mirid zoophytophagous predators Dicyphus hesperus (de Lourdes Ramírez-Ahuja et al., 2017; Calvo et al., 2018a,b) and Engytatus varians (Pérez-Aguilar et al., 2019), the hover fly Melanostoma fasciatum (MacDonald et al., 2016), the damsel bug Nabis kinbergii (MacDonald et al., 2016), and at least three species of predatory mites (Xu and Zhang, 2015; Geary et al., 2016; Patel and Zhang, 2017; Kean et al., 2019). Many of these studies demonstrate the potential for generalist predators as biocontrol agents against potato psyllids in the laboratory or on greenhouse tomato or pepper, but their importance in reducing potato psyllid populations in the field is less clear. Romney (1939) reported that coccinellid and chrysopid predators can reduce potato psyllid populations on matrimony vine in Arizona during some years, and more detailed observations of predator activity in the field were undertaken later by Pletsch (1947), who observed high densities of the lacewing Chrysopa plorabunda in association with potato psyllids over the season and heavy egg predation in complementary laboratory studies. Unfortunately, augmentative release in potato of

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another lacewing predator, Chrysoperla carnea, did not reduce potato psyllid numbers (Al-Jabr, 1999). More recently, based on natural enemy correlations with potato psyllid densities and effects on survival in exclusion cage experiments, Butler and Trumble (2012a) observed three predators to be most important in potato, tomato, and peppers in California: the minute pirate bug Orius tristicolor, the big-eyed bug Geocoris pallens, and the lady beetle Hippodamia convergens. Although many generalist predators are known to feed on potato psyllids in controlled conditions, more studies are needed to clarify the roles of these natural enemies in managing potato psyllids under field conditions. Parasitoids typically may be expected to exert stronger control on their hosts than can be relied upon by generalist predators, though this has generally not been the case for the few parasitoids known for potato psyllids. Parasitism of potato psyllids was noted by several earlier researchers (e.g., Richards and Blood, 1933; Schaal, 1938; Romney, 1939; Compere, 1943). Pletsch (1947) described the life history of the tetrastichid wasp Tetrastichus triozae on potato psyllids but observed that its inconsistent abundance among years and locations likely precluded its reliance for control of psyllid populations. Factors that might limit this parasitoid’s effects on psyllid numbers include relatively low parasitism rates (ca. 20%; Pletsch, 1947; Johnson, 1971; Butler and Trumble, 2012a), high pupal mortality (Johnson, 1971), hyperparasitism (Butler and Trumble, 2011), poor synchronization with potato psyllid populations (Johnson, 1971), and high susceptibility to insecticides (Liu et al., 2012; Luna-Cruz et al., 2015; Morales et al., 2018). Jensen (1957) also reported that T. triozae parasitizes at least nine other psyllid species, so its less than complete specificity on potato psyllids might also be expected to influence its reliability in biocontrol. However, studies in Mexico show higher rates of parasitism (ca. 70%e80%), especially in fields with lower insecticide use (Rojas et al., 2015). Despite inconsistent evidence of the parasitoid’s biocontrol potential in North America, T. triozae was released in New Zealand following assessment in quarantine (Barnes, 2017). The contribution of T. triozae to biocontrol of potato psyllids in New Zealand remains to be fully evaluated. Another parasitoid of potato psyllids, the encyrtid Metaphycus psyllidus, has been observed in Southern California (Compere, 1943), but only at very low parasitism rates ( 1400). Both report that egg laying typically follows an interrupted pattern of several days of laying followed by several days of not laying, repeated several times. In comparison, the average fecundity of A. mancus in New York was calculated to be 100 eggs (Rawlins, 1940), that of A. litigiosus in Russia 200 eggs (up to 370, Kosmatshevsky, 1960), and that of M. caudex in Japan only 17 (Yoshida, 1961). Not surprisingly, there are also differences in where females oviposit. Gibson et al. (1958) reports that L. canus prefers to oviposit in bare soil while L. californicus prefers soils covered by vegetation. The number of larval instars and duration of development also differ considerably among and within species. Lacon variabilis Candèze, an Australian species, develops through 6e8 instars (Zacharuk, 1962a), while in the southern USA Conoderus rudis develops through 3e4 instars (Seal and Chalfant, 1994) and C. scissus through 7e10 (Chalfant and Seal, 1991). Agriotes sputator larvae pass through 10e12 instars in Russia and 7e9 instars in England (Zacharuk, 1962a). Larvae of Glyphonyx recticollis complete development in 1 year, while larvae of M. communis and C. lividus occurring in the same field require 4 and 2 years, respectively (Kulash and Monroe, 1955). In China, Melanotus cribricollis and S. latus have a life cycle of 4e5 years, but M. caudex, P. canaliculatus and A. fuscicollis 3 years (Liu et al., 1988; Wu and Li, 2005; Zhou et al., 2008). In Japan, M. okinawensis has a 2e3 year life cycle (Arakaki, 2010), and in Korea S. puncticollis has a 3e4 year life cycle (Kwon et al., 2004). The variation of life cycles is perhaps most notable in the genus Conoderus. Of the pest species frequently found together in southern USA, C. scissus has a 2-year life cycle (Seal et al., 1992); C. lividus and C. amplicollis complete their larval development in 1 or 2 years (Cockerham and Deen, 1936; Jewett, 1946; Seal et al., 1992); and C. vespertinus and C. bellus have a 1-year life cycle. Of the latter, C. vespertinus is a larva for 300e350 days (Eagerton, 1914; Rabb, 1963) and C. bellus for approx. 30 days (Jewett, 1945). Conoderus rudis and C. falli complete larval development in 2e3 months (Seal et al., 1992) and have at least two generations per year (Norris, 1957; Chalfant et al., 1979). Unfortunately, the life cycle of many pest species remains unknown, and that of others can vary considerably based on latitude and diet. The larval stage of S. a. destructor can vary from 4 to 11 or more years during which the larvae may reduce in size despite the availability of food (Strickland, 1942). This delayed development and “regressive moulting” has also been observed for L. canus and A. obscurus larvae (van Herk, unpubl. data).

7.4.2 Larval activity Pest wireworm species do not always cause damage when present, as the larvae appear to spend a relatively small amount of time of each instar actively feeding. In his studies of A. ustulatus and A. sordidus development, Furlan (1998, 2004) reports the amount of time these larvae spend per instar on (consecutively) mandible hardening (10 d, 8%, respectively), feeding (19 d, 24%), and pre-moulting (71 d, 68%). Similarly, Kosmatshevsky (1960) describes A. litigiosus as undergoing four phases of activity in each instar: moulting, intensive feeding, intensive burrowing with little feeding, and quiescence in earthen cells. Zacharuk (1962a) observed these phases in S. a. destructor, but does not report on intensive burrowing phase. As conspecific larvae in a field appear to undergo these phases in synchrony (e.g., moult at approximately the same time; van Herk, unpubl. data), there are periods of peak wireworm activity. The number of such peak activity periods will depend on numerous factors (e.g., species, latitude, weather), and the time of activity periods may vary from year to year for a particular species in a particular field (Vernon, unpubl. data). Doane (1981) reports that on the Canadian prairies S. a. destructor and H. bicolor have a period of peak activity in June, followed by a sharp decline in activity, and a second, less intense period of activity in AugusteSeptember; similar periods of activity have been observed for A. obscurus in Agassiz, BC (Vernon, unpubl. data). For these species the periods of reduced activity generally coincide with the periods of warmest and driest soil temperatures, which are avoided by vertical migration downward in the soil (Falconer, 1945). As periods of

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activity vary with species and location, it is critical for effective management that they be assessed on a local level, as has been done for M. communis in Florida (Cherry, 2007) and various Limonius species in the Pacific Northwest (Jones and Shirck, 1942; Stone and Foley, 1955).

7.4.3 Preferences in soil type and soil moisture content Economic wireworms differ considerably in soil type and soil moisture preferences. Some genera (e.g., Limonius) prefer moist soils, while others are obligate dryland species that diminish in importance when fields are brought under irrigation (e.g., those previously listed as Ctenicera, with the notable exception of Sylvanelater cylindriformis; Fox, 1961). For a review of wireworm soil moisture preferences we refer to Thomas (1940) and Chalfant and Seal (1991). Little research has been done on this in recent years, and some of the key studies were conducted by Zacharuk (1962b), Lees (1943), and Schaerffenberg (1942). Wireworm soil preferences likewise can be quite specific. In a comparison of the distributions of S. a. aeripennis and S. a. destructor in Canada, Zacharuk (1962a) found S. a. destructor in brown and black soil zones and S. a. aeripennis in the more northern gray soils, with virtually no overlap of the two subspecies. The degree of specificity is species-dependent: MacLeod and Rawlins (1935) found both A. mancus and L. agonus prefer low-lying parts of New York fields, but this was considerably more pronounced in A. mancus. Such preferences help explain why the species composition can vary between nearby fields.

7.4.4 Feeding preferences Most elaterid larvae do not feed on crops (Zacharuk, 1963; Turnock, 1968), and there can be considerable variability in the feeding preferences among larvae of a pest species. In their study of the feeding ecology of A. obscurus in Austria, Germany, and Italy, Traugott et al. (2008) measured carbon (12C/13C) and nitrogen (14N/15N) isotope ratios to determine their trophic level and the importance of soil organic matter and weeds within their diet and observed that 10% of the A. obscurus larvae fed primarily on animal prey. Interestingly, A. obscurus larvae show a clear preference for the roots of some types of grass over others (Hemerik et al., 2003), but will remain with a particular food source as long as its supply is sufficient (Schallhart et al., 2011). Not surprisingly, a wireworm’s food source will affect its growth, as has been demonstrated for L. dibutans and M. depressus (Keaster et al., 1975). Wireworm feeding preferences have been reported for various species (e.g., A. sputator; Fox, 1973), and help explain the differences in tuber damage when different potato cultivars are planted in the same fields, as reported from studies conducted in Sweden, Iran, Korea, and the UK (Jonasson and Olsson, 1994; Kwon et al., 1999; Bagheri and Nematollahi, 2007; Johnson et al., 2008). It is interesting to note that different species may also cause different types of damage to a crop. For example, Willis et al. (2010) report that C. amplicollis appears to cause more extensive surface scarring of sweet potato than other Conoderus species.

7.5 Wireworms and the potato crop Typically, common above-ground insect pests of potato arrive as immigrants to the already established potato crop. The opposite is true with wireworms, where potatoes are planted into fields that have already been occupied by one or more species in various instars for one to several years, depending on the species and cropping history of the field. There is absolutely no question that wireworm populations can build up to enormous numbers in grassland or pasture, especially where these fields have been in this state for several years (Thomas, 1940; Parker and Howard, 2001; Traugott et al., 2015), and this seems to be a generality worldwide. A mature field of pasture may contain cohorts of more than one species of wireworm from adult oviposition events occurring over a number of consecutive years, and populations can be distributed in various spatial patterns throughout a field depending on species and the various habitat variables (e.g., soil moisture) mentioned above. When pasture is removed, generally by ploughing, wireworm populations remain in place in the soil and, depending on the length of their life cycle, can feed on subsequent crops for years until all cohorts have left the soil as adults. It is generally when potatoes are planted following the removal of pasture that damage from wireworms can be severe, and this damage can be as or even more severe if potatoes are grown in the second year (Miles and Cohen, 1938). The severity of wireworm damage to a potato crop in the first or second year is likely related to how the preceding pasture is removed from the field. Pasture that is ploughed green just before planting potatoes will delay and reduce damage to daughter tubers in the first year, since wireworm populations will occupy and feed on the slowly decomposing green manure that typically lies about 20e30 cm below ground (Miles and Cohen, 1938). This principal has also been demonstrated in fields of maize, where damage was significantly reduced by deep-ploughing green pasture just before planting (Furlan et al., 2020). When green manure has fully decayed, usually by late summer, wireworms will then

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gradually move to other food sources such as daughter potato tubers, and cause damage commensurate with population size and the amount of time they spend feeding. If potatoes are planted the following year, the only food source throughout the growing season is generally the potato crop, and a higher amount of daughter tuber damage can occur. In fields where the pasture is killed with herbicide in fall or early spring, and subsequently disked rather than ploughed prior to planting potatoes, wireworm populations will feed primarily on the potato crop throughout the initial growing season, and damage will be highest in the initial year of planting (Vernon, unpubl. data). This principle also has a direct bearing on the success or failure of various wireworm monitoring and management strategies, which will be discussed later. In addition to pasture, significant oviposition will also occur in cereal crops, and high wireworm populations can arise in these fields in a single year (Thomas, 1940; Salt and Hollick, 1944; Andrews et al., 2008; Vernon et al., 2013a). This is of particular relevance to potatoes, especially in Canada, in that the majority of potatoes grown have 1 or more years of a cereal crop in their rotations (Noronha, 2011; Vernon et al., 2013a). On the Canadian prairies, where an increasing amount of wireworm damage is occurring to wheat each year (van Herk et al., 2018), growers routinely apply the organophosphate phorate (Thimet 20G) in rotated potato fields to prevent cosmetic damage to tubers destined mostly for the processing industry. In Prince Edward Island (PEI), growers typically plant barley or wheat undersown with clover in 3-year rotations with potatoes (Noronha, 2011). This practice, which is known to give rise to damaging wireworm populations in fields (Landis and Onsager, 1966), has also resulted in the requirement for prophylactic phorate use on an increasing scale, and despite this severe damage is occurring on many farms. The potato crop itself has not been reported to be a favored site for oviposition by click beetles, although our work has shown that some oviposition and production of a small cohort of wireworms (A. obscurus) will occur in well-weeded potato fields (Vernon et al., 2013a). During a typical growing season in the northern hemisphere, many species of wireworms manifest two distinct periods of feeding activity in potatoes (e.g., Doane, 1981; Gratwick, 1989; Parker and Howard, 2001), but this can vary between species and between species between years (Doane 1977, 1981) as discussed above. Typically, the first activity period occurs in spring (between April and June), which usually coincides with the planting of mother tubers and the development of roots and stems. As will be discussed later, it is believed that wireworms in the soil respond to carbon dioxide (CO2) (Doane et al., 1975) produced by the sprouting mother tubers and follow these cues to the planted rows. Damage to the tuber or roots appears as holes of about the same diameter as the wireworms that made them, and they can often be seen partially or wholly inside mother tubers at that time. Some mortality to mother tubers may occur in fields with extremely high populations, but typically crops will establish normally even in the presence of high populations. This period of feeding in spring is followed in the hot, dry summer months of July and August by a quiescent period where little feeding or damage occurs. The second period of feeding generally occurs from late August through to the end of potato harvest, during which time daughter tubers are developing and two types of characteristic damage may occur. Wireworms feed on daughter tubers in much the same way as on mother tubers, making wireworm-sized holes into the tuber flesh. However, feeding on smaller daughter tubers produces holes that expand and suberize as the tuber matures, often giving rise to misshapen and unmarketable tubers (Fig. 7.2). Entry holes made to larger tubers are the most common form of damage, however, and these can be quite numerous under high wireworm pressure (Fig. 7.2). As would be expected, the higher the population of potato-feeding wireworms, the higher the number of holes generally made in tubers (Menusan and Butcher, 1936; Thomas, 1940), although the number of holes per tuber is not necessarily in direct proportion to the population, and damage to tubers may be clumped (Gui, 1935). Potato varieties with a lower number of tubers per hill have also been shown to have more damage per tuber than varieties with larger numbers per hill (MacLeod, 1936). In addition, the longer the tubers are left in the ground before harvest, the higher the amount of damage that will occur, as we have found in several years of potato trials (Fig. 7.3) and which has also been reported elsewhere (Anonymous, 1948; Parker and Howard, 2001; Kuhar and Alvarez, 2008). This increase in holes with time is likely due to continued feeding by individuals, by increasing numbers of wireworms feeding with time, or both, although this has not been thoroughly researched (Parker and Howard, 2001; Kuhar and Alvarez, 2008). The impact of wireworm feeding on the marketability of a potato crop is a function of the amount of visible wireworm damage and all other defects on tubers, and tolerance for tuber blemishes varies according to various industry standards and the final destination of the crop. Organic and seed potatoes, for example, may have a higher tolerance for blemishes than ware or processing potatoes, but even these rules of thumb may vary depending on the collective type(s) of blemishes involved, the client, product abundance, competition, and so on. In our work to develop management approaches for wireworms, we have established a tolerance of only one obvious wireworm hole per tuber, with two or more holes or wireworm-caused deformities constituting a “cull.” In addition, we aim for less than 5% overall cullage caused by wireworm feeding as being a threshold that would generally meet most industry standards. The relationship of the percentage of culls due to wireworm damage (2 blemishes/tuber) versus the mean number of holes per tuber is shown in

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FIG. 7.2 Damage done to potatoes by wireworm feeding. (A) Left, undamaged potatoes; Right, potatoes damaged early in the growing season, causing misshaping. (B) Extensive (bottom) and slight (top) damage to tubers late in the growing season.

FIG. 7.3 Wireworm damage increases when tubers are kept longer in the soil. Mean number of wireworm blemishes per market-sized tuber in samples taken approximately 20 days apart from control treatments in insecticide efficacy studies conducted by the authors from 2004e10.

Fig. 7.4 for feeding by A. obscurus on Chieftain potatoes in British Columbia, Canada, and a virtually identical relationship has been found for wireworm damage (Melanotus spp. and Limonius agonus) on potatoes in Ontario, Canada (Vernon, unpubl. data). Such a relationship, however, would be expected to change depending on whether feeding by other species is more or less aggregated, or whether various soil amendments (e.g., repellent insecticides) steer wireworm feeding activities to more limited regions of a hill. Although wireworm damage to potatoes is fairly obvious once seen, there are other types of damage that might cause some confusion. In Europe and the UK, injury by small slugs, for example, resembles entrance holes made by wireworms, although slugs will hollow out cavities within tubers, which is not a characteristic of wireworm damage (Gratwick, 1989; Parker and Howard, 2001). Subterranean larvae of the tuber flea beetle (Epitrix tuberis Gentner), a pest of potatoes in the Pacific Northwest region of North America, also make holes in the flesh of potatoes, but these holes are generally smaller in diameter than those of wireworms (Vernon and van Herk, 2017). Millipedes are often found in association with wireworms and damage (Parker and Howard, 2001), especially in former fields of sod or pasture, but direct damage by millipedes to tubers, although suspected, has not been confirmed.

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FIG. 7.4 The proportion of tubers culled per sample is significantly correlated to the number of mean blemishes per tuber. Shown are data from control treatments of insecticide efficacy studies conducted from 2003e10; n ¼ 104 independent samples.

7.6 Sampling 7.6.1 Wireworm sampling and risk assessment Threshold-based monitoring programs have been developed and implemented for many potato insect pests, including Colorado potato beetles (Leptinotarsa decemlineata (Say)), aphids (e.g., Myzus persicae (Sulzer)) and flea beetles (e.g., Epitrix cucumeris (Harris), Anonymous, 2010; E. tuberis, Vernon and van Herk, 2017). The development of efficient, accurate and consistent monitoring programs and risk assessment methods for use in management strategies for wireworms, however, has proven to be somewhat elusive. The fact that wireworms occupy a subterranean habitat has greatly impeded the development of accurate sampling methods. Not only are wireworms underground, but they may also be anywhere from near the soil surface to 1.5 m deep (Andrews et al., 2008) depending on the species, instar, geography, temperature and moisture, cycles of feeding and moulting, presence or absence of ground cover (e.g., grass vs. fallow) and location of food (e.g., Zacharuk, 1962b; Doane et al., 1975; Toba and Turner, 1983; Parker, 1996). Thus, the timing and protocols selected for sampling are absolutely critical to the success of any sampling objective, be it simple detection, species census/survey, population estimation, or threshold-based monitoring. Since the results of various sampling approaches will vary quite radically both spatially and temporally (Parker, 1996; Simmons et al., 1998; Horton, 2006), the realities and limitations of wireworm sampling need to be considered at the very outset of developing such programs. This is particularly true if the sampling approach is to provide information to growers regarding the need to “apply” or, more importantly, “not apply” pre-emptive wireworm controls (i.e., field avoidance or insecticide use). Sampling for wireworms can be segregated into “absolute” versus “relative” population sampling methods (Southwood, 1978). Absolute sampling methods, such as soil coring to extract wireworms in situ from their soil habitat, typically involve a higher level of expertise, time, infrastructure, and associated expense to conduct, and as such are generally relegated to more research than extension programs. Relative sampling methods, including the use of attractive baits or traps to draw wireworms from variable distances in the soil are also used for research purposes, but have mostly been developed with the intention of providing indications of wireworm presence and relative abundance for use in management programs.

7.6.1.1 Absolute sampling methods The main objective of absolute sampling for wireworms has historically been to estimate the population size, spatial distribution (horizontal and vertical), and temporal activities of wireworms in a field. This has typically involved removing field soil in layers (e.g., Gibson, 1939; Salt and Hollick, 1944) or by soil coring (e.g., Yates and Finney, 1942;

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Anonymous, 1948) at various depths and at enough locations in a field over time that wireworm population estimates can be made with reasonable precision. Probably the best example of an absolute sampling program is from the UK during World War II in the early 1940s, where core samples were taken in pasture to estimate wireworm populations (Agriotes spp.) prior to conversion to cultivated crops, including potato. Sample sizes of 20 cores (10 cm diameter  15 cm deep) per field (4e10 ha) were taken, and hundreds of fields were surveyed annually (Yates and Finney, 1942). Although providing acceptable population estimates where wireworm levels were high, sampling error increased at lower population levels, with the lower limit of detection being about 62,500 wireworms/ha (Yates and Finney, 1942; Parker and Howard, 2001). In determining the suitability of a field (i.e., currently under cultivation or in pasture) for eventual potato production, however, higher levels of accuracy are required at lower population levels, since significant cosmetic damage can occur at levels even below 62,500 wireworms/ha (French and White, 1965; Parker and Howard, 2001). Up to 5% of tubers have been observed to have some wireworm damage at populations of 25,000 wireworms/ha, and the number of tubers with nine or more blemishes was well above tolerance at 75,000 wireworms/ha (Hawkins, 1936). In order to detect such low economic levels in a field with acceptable precision, a larger number of core samples would be required, along with a proportionately higher amount of labor and associated sampling costs. It is interesting to note that increasing the number of soil samples from 20 to 40 cores per field did not reduce wireworm sampling variability in cultivated and grass pasture fields in Iowa (Simmons et al., 1998), suggesting that a much higher number of cores per field would be required to reduce sampling variability and better meet the minimum detection level of 62,500 wireworms/ha. With soil sampling methods, a major drawback has always been the difficulty in extracting wireworms of all instars from soil samples in a timely, cost-effective manner. Although methods have been designed to remove wireworms from soil or turf by flotation (Salt and Hollick, 1944), mechanical methods (Smith et al., 1981; Lafrance and Tremblay, 1964), or extraction using various funnel systems (i.e., Tullgren or Berleze Funnels, Vernon et al., 2009; Furlan, 2014), these approaches still require considerable labor and laboratory processing, and by modern standards are expensive and/or inconvenient. Where abundant labor and extraction infrastructure are available, however, soil coring with a sample size sufficient to detect low population levels of potentially damaging wireworm populations would provide an accurate means of sampling in fields destined for potatoes. As has been amply covered in the previous section on wireworm biology, soil sampling programs to guide management decisions would have to be customized for specific agricultural regions, and would have to consider the species complex involved, their field distribution(s), the optimal times and conditions for sampling each species, and the development of conservative action thresholds (e.g., Robinson, 1976). The level of expertize required to establish and interpret these sampling programs would be commensurate with the complexity of the wireworm complex involved, and the risk of making economic errors.

7.6.1.2 Relative sampling methods The time required to examine soil samples, and the large number of samples required to accurately estimate wireworm populations in fields, has led to the development of several attractant-based sampling methods in North America and Europe, and a number of these are cited in Chalfant and Seal (1991) and Parker and Howard (2001). Essentially, wireworms are attracted in soil to sources of CO2 production (Doane et al., 1975), which in the field would include germinating seeds, respiring plants, decomposing plant material and so on. Of the large number of CO2-producing baits tested, including fruits and vegetables (i.e., melons, carrot, potato) and processed cereals (i.e., bran, rolled oats, flour), baits containing germinating cereal seed (e.g., wheat, barley) and/or other seeds (e.g., corn, sorghum) have been found most effective and are now most commonly used (Bynum and Archer, 1987; Jansson and Lecrone, 1989; Chabert and Blot, 1992; Parker, 1994, 1996; Simmons et al., 1998; Parker and Howard, 2001; Horton and Landolt, 2002; Vernon et al., 2003, Furlan et al., 2014). Among the more important characteristics of wireworm trapping systems for use in research and especially in management programs include the following: consistency among traps; some control over CO2 production; ease of trap assembly and deployment; and rapid, accurate methods of wireworm extraction. Of the methods developed, traps similar to those described by Chabert and Blot (1992), consisting of 450-mL plastic pots filled with medium-grade vermiculite, and with 100 mL each of untreated corn and hard red spring wheat spread in layers in the middle of the pots, adequately meet these criteria (Vernon et al., 2009; Furlan, 2014) (Fig. 7.5A). In our studies, traps are soaked with warm water to runoff twice, placed the same day in 15-cm deep holes, sealed with soil on all sides, and a 20-cm diameter inverted tray is positioned 5 cm above the trap and level with the ground. Traps are generally left for 12e14 d, are removed without surrounding soil, and the trap contents (vermiculite and germinated wheat and corn seed) are sorted by hand to find larger wireworms (>1 cm), and/or are placed in Tullgren funnels which effectively extracts the majority of all instars (Vernon et al., 2009). Traps such as this have been shown to be as or more efficient than other “relative” methods in terms of ease of

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FIG. 7.5 Traps used for sampling wireworms or click beetles. (A) Left, bait trap for sampling wireworms in soil, showing germinated wheat seed after 14 days. (B) “Yatlorf”pheromone trap used for trapping male click beetles in Europe. (C) “Noronha Elaterid Light Trap (NELT),” used for tapping male and female click beetles in Prince Edward Island, Canada.

deployment (i.e., placement, retrieval, and sorting), consistency and quantity of wireworm catch and cost (e.g., Simmons et al., 1998). Other bait trapping systems, including the various food baits mentioned, are likely to be inconsistent in CO2 production among baits, and wireworm counts are prone to greater variability since variable amounts of soil surrounding the baits is often sampled as well. Various methods of improving the efficacy of bait traps have been developed, such as covering the baits at the soil surface with black plastic (Ward and Keaster, 1977; Chabert and Blot, 1992; Simmons et al., 1998) or charcoal dust (Ward and Keaster, 1977; Bynum and Archer, 1987). Essentially these approaches raise soil temperature, which provides better conditions for the germination of living baits (e.g., wheat and corn seed) or microbial respiration in non-living baits (e.g., bran, rolled oats, flour), all of which increase CO2 production. These methods have facilitated earlier trapping and higher catches for some species (Ward and Keaster, 1977; Bynum and Archer, 1987), but they also increase the time and cost of sampling, which may not be practical or necessary for all monitoring purposes. Baits or baited traps draw wireworms in the soil from distances as far away as wireworms can detect distinct CO2 gradients. Doane et al. (1975) found that wireworms (e.g., Selatosomus aeripennis destructor) can detect and orient to CO2 sources from as far away as 20 cm (the limit of their soil bioassay arena), and Vernon et al. (2000) showed that the majority (83%) of wireworms (A. obscurus) in field plots will orient to trap crops of wheat spaced 1 m apart. It has also been found that bait stations with untreated wheat (11 cultivars), barley, oats, or fall rye seed will increase in attractiveness to wireworms (A. obscurus) as the density of seed increases, but will reach plateaus of catch at seeding densities specific to each variety (Vernon et al., 2003). The draw of any CO2-producing bait or trap to wireworms, therefore, will reach well beyond the physical boundaries of the trap, but this distance will vary with the type of trap, the trap bait, the temperature and moisture of soil, competing CO2 sources (i.e., ploughed pasture, various living weeds and grasses), the soil texture, and the species, instar, and feeding status of wireworms in the field (Parker, 1996; Vernon et al., 2003; Horton, 2006; Furlan, 2014). In our experience, we have found that bait traps are much less effective at soil temperatures below 10 C, in freshly ploughed fields of pasture with high levels of green manure (Parker, 1996), and at various times of the growing season when wireworms are not feeding (Furlan, 1998, 2004, 2014). Where we have found bait trapping to be relatively successful and consistent is when the area surrounding a bait trap (1 m radius) has been cleared of all living plant material or other potential sources of competing CO2 production. Trapping is also done only when soil reaches a fairly stable temperature of greater than 10 C, which is typically when wireworms become more consistently active, germination of seed in traps is high, and seedling growth in baits is about 1 cm/d, which is ideal for a 12- to 14-day trap placement (Fig. 7.5A). Lower temperatures reduce wireworm activity, seed germination, and growth, and higher temperatures result in rapid seedling growth and increased biomass for sorting, all of which alter the effectiveness and consistency of trapping (Vernon, unpubl. data). In the development of any bait trap sampling program for wireworms, therefore, especially where consistency in trapping is important, the field conditions most suitable for sampling all economic species present should be identified concurrent with determining the most appropriate baits and sampling protocols. Unfortunately, other than studies involving A. obscurus and A. lineatus (Vernon, 2005), and A. ustulatus, A. sordidus and A. brevis (Furlan, 2014), little information on optimal sampling conditions for other species is available.

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7.6.1.3 Absolute versus relative sampling Bait trapping, which draws in wireworms from areas outside of the trap, would be expected to collect higher numbers of wireworms than direct soil sampling techniques, and this has been verified in a number of studies (e.g., Parker, 1994, 1996; Simmons et al., 1998). Of these studies, that of Simmons et al. (1998) is of particular note in that they compared the “absolute” soil sampling method developed in the UK (Yates and Finney, 1942; Salt and Hollick, 1944; Anonymous, 1948) with a number of candidate “relative” sampling methods to develop farmer- or consultant-run sampling programs in the USA. Of the relative methods tested, wheat/corn baits (placed in holes in the ground) had consistently higher wireworm counts (collective counts of Melanotus pilosus, Conoderus auritus, Hadromorphus inflatus, Hypnoidus abbreviatus, and M. similis) and a lower variability index (Buntin, 1994) than core samples. They also determined that a high positive correlation existed between the wheat/corn baits and core samples in fields with higher population pressure. Their data further indicated that wheat/corn bait catch could be calibrated to estimate field populations, and that sample sizes of 50, 25, or 10 baits/ha would be needed to achieve 10, 15, or 25% levels of precision, respectively. Although only a single study, the methodologies used by Simmons et al. (1998) to determine sample size and efficiency (trap effectiveness and cost) for various “relative” wireworm sampling methods versus “absolute” sampling methods can be considered for other regions and species. Attempts at using relative sampling methods to consistently predict wireworm damage to potato have met with discouraging results. Using cereal-baited traps in the UK, Parker (1996) found that high levels of damage occurred (>60% tubers with blemishes) in plots where no wireworms (Agriotes spp.) were detected. This was also observed in trials conducted in the USA, where plots baited with rolled oats had between 3.3% and 6.8% damaged tubers despite no wireworms (L. canus) being caught over a 7-week period (Horton, 2006). Horton’s work also found that damage predictions based on wireworm counts could vary dramatically from week to week, indicating the variability in efficacy over time that can be expected with relative sampling methods. Both authors concluded that using baits to predict damage to tubers would be difficult to implement with a great deal of confidence (Parker, 1996; Horton, 2006). This is not to say that the use of baits or bait traps has no value in wireworm management programs. Parker (1996) further concluded that bait traps are more effective than core samples at indicating the presence or absence of wireworm infestations, and would be of value in fields where wireworm populations are below the limit of detection using soil cores (62,500 wireworms/ha), and bait trapping and/or soil core sampling has been recommended alongside pheromone trapping programs in the UK for improving risk assessments in fields (Anonymous, 2011).

7.6.1.4 Timing of sampling in potato fields What should be obvious from the above discussion is that the optimum conditions for sampling wireworms to determine the risk of damage to potato crops often occur when growers intend to plant potatoes, and this is a major impediment to the implementation of pre-planting wireworm monitoring (Horton, 2006). Optimal conditions for deploying absolute sampling methods such as soil coring also occur at this time, since populations are predominantly in the upper regions of the soil and within coring depth (Simmons et al., 1998; Horton, 2006). The selection of any sampling system, therefore, must consider the time it takes to complete the sampling procedure and provide timely input to the grower prior to planting. Because of these current-season time constraints, wireworm sampling can also be conducted the year prior to planting potatoes. Fields at greatest risk of damage by wireworms will often have been in pasture the year previously, and sampling of pasture using absolute or relative sampling techniques can be timed to coincide with wireworm feeding activity periods nearest the soil surface. Although bait trapping techniques are less effective in pasture due to competition with grassy hosts (Parker and Howard, 2001), the strategic removal of sections or strips of pasture with herbicide and/or shallow cultivation well in advance of trapping would enhance the competitiveness of baits. Such considerations also apply to the use of bait traps deployed in cultivated fields the year prior to potato planting.

7.6.1.5 Habitat and risk to potatoes Attempts to correlate field-specific characteristics, including soil type, moisture, topography, cropping history, grower activities, etc., on the distribution, abundance, and risk of economic injury from a species complex of wireworms has met with limited success (Thomas, 1940; Parker and Howard, 2001). Nevertheless, abiotic factors such as soil moisture content have been used to model the likelihood of wireworms occurring in “Conservation Reserve Program” grass fields in Iowa (Lefko et al., 1998), and soil sampling for wireworms has been stratified within fields according to soil moisture characteristics (MacLeod and Rawlins, 1935). Biotic factors, such as the presence and duration of grassland in a field, are obvious but not guaranteed indicators of wireworm presence or absence, indicating that other abiotic or biotic factors

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would need to be considered to improve predictions (Parker and Seeney, 1997; Parker and Howard, 2001; Barsics et al., 2013). In a more recent study, the risk of wireworm damage to maize fields in Italy increased depending on one or more of the following: the species of wireworms present and their relative damage potential; soil organic matter >5%; previous field rotations favoring adult oviposition and wireworm survival (i.e., pastures, double crops); and surrounding landscapes with permanent pasture, uncultivated grass and double crops (Furlan et al., 2017). This study was quite comprehensive, and although geographically isolated with distinctive climate, habitat and wireworm species characteristics, could be used as a model approach for determining the risk of wireworm damage to fields in potato production regions elsewhere. As a simplified general rule, the authors consider any field that has had a history of grassland, cereals, or grassy cover crops (present during adult oviposition periods) within the past 4e5 years to be at higher risk for wireworm damage to potatoes and other crops in Canada. Although there are uncertainties associated with using field variables and cropping history to consistently predict the risk of wireworm damage in fields (Parker and Howard, 2001), improved knowledge of the species complex present in specific agricultural areas, their preferred habitats, oviposition and feeding preferences, and the cropping history of individual fields would improve the accuracy of field-specific risk assessments. In addition, the development of more efficient methods for sampling wireworms (described above), and species-specific pheromone traps for adult click beetles (described below), will improve wireworm risk predictability that can ultimately be conducted at the field scale by growers and consultants (Vernon and van Herk, 2017).

7.6.2 Click beetle sampling 7.6.2.1 Pheromone traps As mentioned earlier (Identification: Pheromone-based approaches), female-produced sex pheromones have been discovered for 22 key economic elaterid species in Europe and Russia (mostly Agriotes species, Yatsinin and Lebedeva, 1984; Tóth, 2013), Japan (three Melanotus species, Tamaki et al., 1986, 1990), and more recently in North America (e.g., Selatosomus aeripennis destructor, Limonius californicus, Melanotus communis, Agriotes mancus, A. ferrugineipennis (LeConte); Williams et al., 2019; Gries et al., 2021, 2022, van Herk unpubl. data). A number of pheromone trap designs have also been developed or adopted for use in monitoring Agriotes spp. (e.g., Tóth et al., 2003; Ester and van Rozen, 2005; Vernon and Tóth, 2007; van Herk et al., 2018) and Melanotus spp. (Kawamura et al., 2002). Of these, the Yatlor Funnel Trap (Yatlorf, Csalomon, Budapest, Hungary; Furlan and Toth, 2007) (Fig. 7.5B) is the most commonly used in various elaterid surveys and IPM programs throughout Europe, and the newly developed Vernon Pitfall Trap (Intko Supply Ltd., Chilliwack, BC, Canada; van Herk et al., 2018) (Fig. 7.6) is commonly used for invasive Agriotes

A.

B.

C.

D .

E.

F.

FIG. 7.6 Vernon Pitfall TrapÒ, designed to function as a pheromone trap for elaterids or as an unbaited pitfall trap for elaterids and other ground beetles. (A) The bottom, pitfall component. (B) The underside of the cover with inserted pheromone lure and vertebrate exclusion fence. (C) The assembled trap. (D) The trap installed in soil with collected male Agriotes sputator click beetles. (E) Optional cover for winterizing traps left in field. (F) The assembled trap with winterizing cover.

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spp. surveys and general elaterid research and IPM program development in North America. Both of these trap designs will accept commercial pheromone lures (Csalomon, Budapest, Hungary) for the majority of pest elaterids occurring in Europe, and for the invasive Agriotes species A. obscurus, A. lineatus and A. sputator in North America (Intko Supply Ltd., Chilliwack, BC, Canada). Elaterid pheromone traps provide a highly effective tool to study the occurrence of click beetle populations spatially and temporally in fields or in larger agricultural landscapes during single or multiple seasons, which would otherwise have required considerable alternative resources, and which promises to enrich our understanding and even management of this previously ignored, but critical elaterid life stage. Pheromone traps, assuming species specificity, are particularly useful in rapidly determining the presence, absence, and relative abundance of various pest species in agricultural areas. This is particularly true of the Agriotes genera, where aggressive surveys of eight key species (A. ustulatus, A. litigiosus, A. sputator, A. obscurus, A. lineatus, A. rufipalpis, A. sordidus, and A. brevis) have been carried out for years in Europe (Furlan et al., 2001; Furlan and Tóth, 2007), and delimitation surveys of A. sputator, A. obscurus, and A. lineatus, introduced from Europe to the western and eastern coasts of North America, have been conducted in Canada and the USA since 2000 (Vernon et al., 2001; LaGasa et al., 2006). Since the starting point in developing pest management strategies for wireworms in any agricultural region is to know the key species present, pheromone trapping, if available for the key species involved, is the most efficient and inexpensive method available, and in contrast to wireworm sampling procedures does not require a high level of expertize to conduct and rapidly identify the species captured. In addition, pheromone traps are effective at detecting species at very low population levels, which cannot generally be achieved with soil sampling or bait trapping (Furlan and Tóth, 2007). An important consideration in the practical use of pheromone traps for regional, farm or field-specific surveys, monitoring and risk-determination in IPM programs, or various control options (i.e., mass trapping and mating disruption), is where they should be deployed in agricultural ecosystems to best achieve these goals. Strictly speaking, intensively farmed agricultural areas are typically divided into arable fields surrounded by non-farmed headland areas. Actively farmed fields in potato production areas are characterized by a variety of crop rotations which are annually punctuated by various crop-specific mechanical (i.e., ploughing, disking, harvesting), chemical (i.e., fertilizers, pesticides) and irrigation interventions, many of which favor or disfavour the successful establishment and survival of various species of wireworms. The headland areas surrounding these arable fields on the other hand, are generally more permanent and typically contain undisturbed narrow strips of wild vegetation and grasses which are highly suitable for the stable and long-term establishment of wireworm populations (reservoir populations). Therefore, the advantages, drawbacks, and implications of placing pheromone traps directly within farmed fields versus the surrounding headlands will often differ in achieving specific goals, and these need to be considered at the outset of any trapping program.

7.6.2.2 In-field click beetle monitoring There are a number of important considerations when developing and implementing in-field pheromone trapping as a survey, monitoring or control tool for use in scientific or management programs (e.g., Blackshaw et al., 2009). A major concern is the period of time traps need to be deployed in a field (which may span months or even years), which for many species coincides with various early season farming activities. Trapping efforts also become amplified as the number of species, traps and fields increases, and whether periodic unsynchronized trap removal and replacement is required. In-field sampling is also hampered or prevented where large-scale production of potatoes by individual growers (>1000 ha in Canada) occurs on a combination of personal and leased land, the latter of which are not available for in-field monitoring during non-lease years. The interpretation of in-field pheromone trap data in estimating the presence and severity of wireworms in particular fields is also complicated and is currently in its infancy. So far, it has had limited success as a stand-alone predictive criteria for a number of reasons. Fundamentally, the number of male click beetles captured in field traps is the result of an oviposition event that occurred in the field and/or surrounding areas (wireworm reservoirs) several years previously (e.g., 4e5 years for various Agriotes spp.). In the case of fields in permanent grassy pasture, where oviposition occurs annually and populations of one or more species are relatively stable, it is likely that wireworm populations of various yearly cohorts will be present in the soil during the year of pheromone trapping, and trap catch will usually correlate well with wireworm presence and risk of damage to a subsequent crop. On the other hand, in fields that have been out of pasture for 1 or more years, and where favorable crops for oviposition have been planted on one or more occasion during the past 4e5 years, wireworm populations may be much more variable in abundance and age structure. For example, a field that was converted from pasture to arable crops 4e5 years ago may have high numbers of adults in pheromone traps 4e5 years later (from oviposition occurring during the last year of pasture) but have correspondingly low numbers of wireworms in

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the field due to unfavorable crops for oviposition after the pasture is removed. Conversely, levels of adults in pheromone traps might be low due to an unfavorable crop for oviposition 4e5 years previous, but one or more large wireworm cohorts could still be present in the field due to the planting of favorable oviposition crops thereafter (e.g., cereal crops). In addition, if pheromone traps are placed too close to grassy headland areas or adjacent fields harboring reservoir populations of wireworms/click beetles, trap catch can simply reflect immigrants arriving at traps from outside of the field, and the movement of large populations of A. obscurus and A. lineatus into fields from grassy verges has been demonstrated (Blackshaw et al., 2017). Hicks and Blackshaw (2008) also estimated the effective in-field sampling areas for A. obscurus, A. lineatus, and A. sputator pheromone traps (Yatlorf traps, Fig. 7.5B) after a 15-day deployment period to be 2580 m2, 2588 m2, and 1698 m2, respectively. To reduce immigrants from surrounding wireworm reservoir areas entering pheromone traps inside fields, therefore, the surrounding areas should lie well outside of the effective trapping areas of the traps, which is not possible with smaller or narrow fields. In addition, the means of immigration (flight and/or walking) and the relative mobility of various species are considerations that present additional problems of in-field data interpretation where several species are involved. For example, Hicks and Blackshaw (2008) reported the relative speed of the three primary UK species to be of the order A. lineatus > A. obscurus > A. sputator, which suggests that the rate of pheromone trap catch will vary between species, and therefore risk cannot be accurately estimated by simply adding catches of these traps together. The confounding effect of immigrant adults on in-field pheromone trap interpretation, however, can be mitigated somewhat by early beetle emergence trapping for shorter periods of time, even in smaller fields. In the UK, the possibility of placing pheromone traps in fields in the morning and removing them in the afternoon has being explored (Anonymous, 2011), and has been used to collect adults over smaller, more localized areas in various field studies (Blackshaw, unpubl. data). If this is done early enough during adult emergence, it would more accurately reflect populations arising from “within” as opposed to “outside” of a field. Despite the concerns discussed above, some examples of in-field monitoring to estimate the risk of wireworm damage to various crops are worthy of discussion. Pheromone traps have been used by growers to estimate the risk of wireworm damage (i.e., A. lineatus, A. obscurus, and A. sputator) to potatoes in the UK (www.syngenta-crop.co.uk) by placing traps for each species in fields the year prior to planting potatoes. The total number of Agriotes beetles caught over the course of the season is then used to determine appropriate risk-aversion measures for the following growing season, including avoidance of planting, growing an early potato crop and/or harvesting earlier to reduce damage, selecting a more damagetolerant variety, or using an insecticide at planting (Anonymous, 2011). According to this system, collective beetle captures of 0, 1e49, 50e150, and >150 correspond to wireworm population estimates and risk of damage of, respectively, 0 wireworms (little or no damage); 25,000e150,000 wireworms (some damage); 150,000e250,000 wireworms (significant damage), and >250,000 wireworms (severe damage) (Anonymous, 2011). Unfortunately, corroborative data linking the above trap catch to wireworm numbers and crop risk has not been published, and many of the concerns expressed above with in-field sampling (i.e., 4e5 year field history of wireworm-favouring or disfavouring crops; elevated trap catches due to immigrating populations from surrounding verges; and unequal damage potential of the various species trapped) have not been addressed with this system. In-field elaterid monitoring with pheromone traps has recently developed traction in helping determine the risk of wireworm damage in maize crops in northern Italy (Furlan et al., 2020). Taking into account the various concerns expressed above with in-field trapping, pheromone traps for three key wireworm species (A. sordidus, A. brevis and A. ustulatus) placed in the center of fields (0.2e1.0 ha) over two consecutive years prior to maize, produced good speciesspecific correlations with wireworm populations and damage estimates (Furlan et al., 2020). The success of this system, however, would be more challenging to develop and implement in potato production areas where: wireworm species (i.e., A. obscurus, A. lineatus and A. sputator) have longer life cycles concurrent with more diverse crop rotations (4e5 years); field size is typically large (>5 ha); and the tolerance for damage to tubers is very low which increases the likelihood of economic errors occurring.

7.6.2.3 Field headland click beetle monitoring Elaterid pheromone traps set in non-farmed grassy headlands provide a number of advantages over in-field trapping. Since headland areas are relatively untouched during a growing season, traps are more isolated and relatively protected, are easily accessible, and do not interfere with in-field grower activities. As mentioned earlier, wireworm populations in grassy headland areas are generally stable (Blackshaw and Vernon, 2006, 2008) relative to in-field populations and are typically the reservoir sources of annually emerging click beetles that re-invade adjacent fields when crop rotations are favourable for oviposition and wireworm survival (e.g., cereal crops). As such, although headland sampling may not accurately predict wireworm populations in adjacent fields, it does provide a relative species-specific estimate of “wireworm risk potential” at

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the field, farm, or regional scales. For general delimitation surveys, elaterid pheromone traps are typically placed in headland areas, where they are more protected from farming activities or vandalism (e.g., LaGasa et al., 2006), and where well established populations of the target species are most likely to reside. In determining the “wireworm risk potential” of the exotic European wireworm species occurring in PEI (A. lineatus, A. obscurus, and A. sputator), Vernon Pitfall Traps (Fig. 7.6) have been placed in multiple headland regions occurring between two or more contiguous fields destined for eventual potato crops. These traps, termed “Sentinel Traps’, have been able to determine regions of PEI where these exotic species have not yet colonized, versus regions where one or more species have become well established and crop threatening (Vernon and van Herk, 2017) (Fig. 7.7). These surveys have been used by some growers to determine fields at low risk that require minimal wireworm mitigative actions and even where organic potato production can be undertaken, and conversely, determine those fields with high wireworm risk potential where heightened wireworm measures are required. In addition, we have also determined that these pheromone traps, when placed about 1e2 m into headland regions surrounding arable fields in PEI (two traps per field edge, termed “IPM Traps”) can indicate headland regions where reservoir populations of A. sputator are highest, and where mitigative control actions can be taken to reduce populations in those areas (van Herk, unpubl. data). Where “Sentinel Trapping” and “IPM Trapping” intersect with in-field damage predictions is in an Agriotes risk rating system that combines: (a) the cropping history of a field over the past 4e5 years, (b) the presence of recent wireworm damage to potato crops at various proximities to the field, (c) optional wireworm sampling results and (d) the previous year’s Agriotes species pheromone trapping results (using regional “sentinel traps” and/or field-specific “IPM traps”). This risk rating system is currently under evaluation in BC and PEI concurrent with ongoing research to determine the relative favourability of common rotational crops in promoting or disfavouring wireworm population growth in fields (Vernon and van Herk, 2017, van Herk unpubl. data).

FIG. 7.7 Map of farming regions in Prince Edward Island showing locations of Vernon Pitfall Traps in grassy headland areas between fields (termed “Sentinel Traps”) and relative numbers of Agriotes sputator click beetles captured. Trap catches indicate regions where populations of A. sputator are high and aggressive mitigative control actions are required in potatoes, and regions where populations are low and require less aggressive control actions.

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7.6.2.4 Other click beetle trapping systems Non-baited pitfall traps have been used to collect elaterid adults primarily for species survey purposes in Canada (i.e., A. lineatus, A. obscurus, A. sputator, A. mancus, Aeolus mellillus, Hypnoidus abbreviatus, H. bicolor, Limonius californicus, L. canus, L. infuscatus, Melanotus communis, and Selatosomus destructor; Vernon and Päts, 1997; van Herk et al., 2018) or in research programs to assess adult activity and dispersal (e.g., Melanotus depressus and M. verberans; Brown and Keaster, 1986; A. obscurus and A. lineatus, Vernon et al., 2014a,b). In contrast to pheromone traps, which primarily collect male beetles of only a single species, unbaited pitfall traps will simultaneously collect both sexes of several species. Pitfall traps are typically a variety of in-house designs, the most common of which consists of plastic cups (e.g., standard beer cups) dug into the ground such that the top lip of the cup is flush with the soil surface. Another identical cup with the top 1e2 cm removed can be inserted into the base cup to collect the trapped specimens, which can be removed and replaced without disturbing the base cup. To prevent rain and other debris from falling into the trap, a covering can be used such as a plywood square with 1 cm pegs at each corner to elevate the cover from the trap and surrounding soil. An improvement to these devices is the Vernon Pitfall Trap (Intko Supply, Ltd., Chilliwack, BC, Canada, Fig. 7.6), which has been designed to function both as a pheromone-baited trap or as an unbaited pitfall trap. These traps can be rapidly and consistently installed in soil with standard bulb planters, have removable cups for rapid specimen removal, have an elevated entry ramp and exclusion cage to reduce water and rodent entry, and a surface lid to exclude rain and other debris. Their advantage over in-house traps is that they are much simpler to assemble, install and inspect, less prone to flooding, are consistent in shape and function, easily transported in and out of the field and are highly durable (Vernon and van Herk, 2017; van Herk et al., 2018). Another recently developed design for trapping elaterid beetles in potato fields is the Noronha Elaterid Light Trap (NELTÔ , Fig. 7.5C), which combines a pitfall trap with a light source. The trap consists of three components, including: a 20-cm diameter plastic base with a white pitfall trap holder that is dug into the ground; an elevated solar-powered spotlight adjusted to shine light in and around the cup; and a poultry wire cage cylinder surrounding the trap to prevent rodents and beneficial insects from falling into the trap (Fig. 7.6). The light has been shown to increase catch of A. sputator in NELT traps threefold relative to NELT traps without light, and the ratio of male to female beetles taken is about 6:4 (Noronha, unpubl. data). These traps are now in use in PEI for monitoring a number of elaterid species and are being evaluated for mass trapping. Pitfall traps provide a “relative” rather than “absolute” measure of click beetle abundance, since they capture click beetles during their trivial movements within a habitat, and trap catch typically increases with time as new beetles enter the trapping area. As was the case with “in situ” soil sampling methods for wireworms, which catch few wireworms relative to bait traps, unbaited pitfall traps catch far fewer male click beetles per sample than attractant-based methods. Pheromonebaited Vernon Pitfall Traps (Fig. 7.6) for A. obscurus, A. lineatus and A. sputator, for example, captured 96, 214 and 108 times more males than unbaited pitfall traps, respectively (van Herk et al., 2018). Despite catching lower numbers than pheromone traps, pitfall traps in general catch adequate numbers of several elaterid pest species (males and females) for surveys and for use in various scientific studies (van Herk, unpubl. data). Another useful adult elaterid sampling method is the use of what has been generally termed “forage traps” (L. Furlan, pers. comm.). These traps include a clear sheet of plastic (about 60 cm  90 cm), secured flat to the ground (usually bare ground) with soil covering the edges, and with a good handful (5 cm diameter) of wild grasses about 40e60 cm long placed along the middle of the sheet. The grass can be held in place by a wire hoop through the sheet into the ground. These traps appear to act as harborage or as food sites for both sexes of click beetles, and hundreds can be collected in this manner overnight. We have used this method for collecting both sexes of A. obscurus and A. lineatus in non-pasture fallowed fields for various markereleaseerecapture studies. Since these traps collect more beetles than pitfall traps (Vernon, unpubl. data), it appears that there may be some level of attraction occurring, possibly to the grass component. The use of these traps for monitoring click beetles for management approaches has not been explored.

7.7 Wireworm control The availability and efficacy of management tools and approaches for the prevention of economic injury to potato crops from wireworms has varied considerably over the past century, and the reader is directed to review articles by Thomas (1940), Parker and Howard (2001), Ritter and Richter (2013) and Traugott et al. (2015) for listings of some of the early and more contemporary control options, respectively. The review of Thomas (1940) essentially pre-dates the inception of the synthetic insecticide era (e.g., organochlorines, organophosphates, carbamates, etc.), and the management options at that time included cultural methods such as cultivation, fallowing, crop rotation, fertilization, mulching; time of potato harvest;

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physical methods such as attractants and repellents; and insecticidal methods such as fumigants (e.g., carbon disulfide, chloropicrin, cyanides, paradichlorobenzene), seed treatments, and soil amendments (e.g., arsenicals, mercury compounds, pyrethrum, rotenone). It is interesting to note that although the management options available for wireworms pre-1940 would likely have been more expensive and much less effective than the synthetic insecticides which came later, the tolerance of consumers for wireworm damage to potatoes was also higher, and the availability of potato products was quite limited in contrast to todays’ higher quality standards and diverse product selection. Whereas primarily ware potatoes were produced pre-1940, modern-day production markets for potatoes include regular table grade; pre-packed specialty varieties; numerous processed products (such as French fries, potato chips, hash browns, instant potatoes); seed potatoes; and versions of these products as conventional or organically produced. In many of these modern products there is essentially a zero tolerance for wireworm blemishes (e.g., Anonymous, 2011), and the evolution in diversity and quality of the potato industry over the past century has somewhat paralleled our ability to effectively control wireworm damage. However, since our arsenal of effective wireworm insecticides is dwindling in many countries, and reports of growing populations and damage are occurring in many key crops, our ability to sustain the quality and abundance of our current potato industries will be challenged in the future. The availability of various contemporary methods for wireworm management in potatoes has been reviewed by Parker and Howard (2001), and covered research relating to cultural, biological, physical, and insecticidal controls. In recent years, however, additional scientific research has expanded our knowledge into these and other management approaches that warrant discussion in this chapter. Since our ability to manage wireworms as a whole has virtually vanished with the loss of the persistent organochlorines, our discussion of management options will also focus on the need for more regionand species-specific strategies, and the opportunities and considerations involved in researching and developing these strategies for the future.

7.7.1 Cultural methods The potential economic importance of wireworms in a field is a function of the quantity of eggs deposited over several years, and the survivorship of these eggs and wireworms on the hosts available in the field throughout their life history. As such, wireworm populations can be managed by a number of cultural methods that either prevent or reduce oviposition, or decrease the survivorship of wireworms at all stages in the field. These techniques, as they apply to the production of potatoes, include field avoidance, crop rotation, cultivation, and other modifications to field conditions that reduce the economic impact of wireworms.

7.7.1.1 Crop avoidance and rotation Since wireworm populations generally build up to economic levels in fields with a recent history (e.g., within the past 4e5 years) of pasture, cereals, or grass seed (Thomas, 1940; Andrews et al., 2008; Huiting and Ester, 2009), an obvious cultural control method is to avoid planting potatoes immediately into these fields (Parker and Howard, 2001; Ritter and Richter, 2013). After grassland has been removed, and crops favoring oviposition by click beetles (such as cereal crops, certain forages, grassy cover crops, etc.) are not included in subsequent crop rotations, populations of wireworms will typically decline to sub-economic levels as resident wireworms gradually complete their life cycles (Fox, 1961). In general, the presence of any preferred wireworm crop coincident with click beetle oviposition can give rise to economic wireworm populations in a single year (Landis and Onsager, 1966; Jansson and Lecrone, 1991; Keiser et al., 2012). It is important, therefore, to know the economic species involved, the oviposition activity periods of the adults and their preferred oviposition hosts in order to avoid recurring wireworm problems in a field. This strategy, especially in the absence of effective insecticidal control options (e.g., organic production systems), requires land availability, long-term planning and patience in planting potatoes until wireworm populations have dropped to sub-economic levels. Conventional potato production in many countries, however, often involves land that is leased during the year of planting and/or is often pasture, and prophylactic insecticidal control measures are generally required to avoid economic damage (Ester and Huiting, 2007). Considerable work has been done to determine the positive or negative effects of various crop rotations on wireworm populations, and this topic is extensively covered in the reviews of Thomas (1940), Miles (1942), Parker and Howard (2001) and Ritter and Richter (2013). Studies have focused on crops tolerant to or damaged by wireworms, or that favor or disfavor wireworm population survivorship. The findings often vary considerably between and even within areas worldwide, however, and generalities outside of the general preference of wireworms for pasture, cereals or other grassy crops are tenuous. For example, leguminous plants such as alfalfa and clover (several varieties) were found by many

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researchers in the 1930s to be rotational crops unfavorable for increase of wireworm populations (19 publications cited in Thomas, 1940); however, increases in wireworm populations have been found in these same crops in other research (12 publications cited in Thomas, 1940). These contradictions may be due to differences in species, geographic regions, soil types, soil moisture, methods of evaluation used, etc., but underpin the need for contemporary, region- and species-specific research into this subject that follow harmonized assessment methodologies. In recent work, brown mustard (Brassica juncea L.) or buckwheat (Fagopyrum esculentum Moench) planted in 3-year rotations with potatoes was found to reduce wireworm (Agriotes sputator) damage to daughter tubers relative to high levels of damage observed in rotations of barley (undersown to clover) or alfalfa in Prince Edward Island, Canada (Noronha, 2011). This work was significant in that it demonstrated to growers in PEI (who were incurring increasing wireworm damage to potatoes) that wireworm populations and damage to potatoes were exacerbated by the common practice of rotating cereal crops (barley or wheat) undersown to clover (Landis and Onsager, 1966), and further demonstrated that damage could be reduced by planting rotational crops unfavourable to oviposition and wireworm establishment and/or exhibiting allelopathic properties (discussed below).

7.7.1.2 Cultivation Mechanical methods of disturbing the soil, such as ploughing, harrowing, disking, and rotovating are known to reduce various stages of wireworms (Thomas, 1940; Parker and Howard, 2001; Ritter and Richter, 2013), and although not a primary control method can sometimes be considered part of an IPM program. The objective of cultivation is to directly destroy eggs, larvae, pupae, and adults in the soil, or indirectly kill them by bringing them to the surface and exposing them to heat or to natural enemies such as birds and arthropod predators (Thomas, 1940; Seal et al., 1992). Pupae of many wireworm species, which are very soft-bodied and generally found in the upper 38 cm of soil during July and August, are particularly vulnerable to shallow ploughing, and up to 90% mortality has been reported (Andrews et al., 2008). Cultivation at that time might also expose eggs and small larvae to desiccation and mechanical injury (Thomas, 1940). Some reductions in larger wireworms by cultivation have been reported, and a 91% drop in wireworms caught in traps occurred when soil was ploughed three times during the summer (Seal et al., 1992). The aforementioned studies, however, were conducted in fallowed fields during summer months, which are not typical field conditions available to most growers. In the UK, where summer cultivation is not possible, cultivation practices are thought to be most effective in reducing wireworm populations if done in the autumn when wireworms are active near the soil surface (Gratwick, 1989).

7.7.1.3 Soil amendments Plant tissues or tissue extracts from a variety of cruciferous plants have been shown to have insecticidal properties in soil (Lichtenstein et al., 1964; Kirkegaard et al., 1993). This allelochemical activity has been linked to the presence of high levels of glucosinolates found in certain crops (e.g., Brassica oleracea L., B. juncea L., B. carinata L., and B. nigra (L.) Koch and B. napus L.) (Williams et al., 1993). Although the biological activity of glucosinolates is limited, they break down to more toxic molecules when tissues are damaged, especially upon incorporation into soil (Williams et al., 1993; Borek et al., 1994). Among the more notable of these breakdown products, allyl isothiocyanate has been shown to have toxic as well as antifeedant effects on wireworms (L. californicus) in the lab (Williams et al., 1993). Rapeseed meal (from B. napus) incorporated into soil was found to be repulsive (Brown et al., 1991) as well as toxic (Elberson et al., 1996) to L. californicus in the lab, but it took almost a 1:1 mixture of meal/soil to produce a high level of mortality (90%). It was concluded from these studies that plant material with higher levels of glucosinolates would be required to effectively and more economically control wireworms in the field (Elberson et al., 1996). The need for a plant variety with higher levels of glucosinolates appears to have been met with defatted seed meal (DSM) from a particular variety of Ethiopian mustard (B. carinata sel. ISCI 7) (Patane and Tringali, 2010; Furlan, 2007; Furlan et al., 2010). In a number of laboratory studies, B. carinata DSM was shown to protect maize and lettuce seedlings from wireworm damage (one or more of A. sordidus, A. ustulatus, and A. brevis), and killed 100% of larvae at some dosages (Furlan et al., 2010). In field trials conducted in Italy, B. carinata DSM applied to the soil surface and worked homogeneously into the top 20 cm of soil provided stand protection in maize equivalent to and sometimes better than the insecticide standard (fipronil). In a potato trial, B. carinata DSM provided significant protection of young daughter tubers, but inconclusive protection of mature tubers at harvest (Furlan et al., 2010). It was noted in these trials that wireworms were sometimes found in a moribund or dead state at the soil surface in B. carinata DSM plots, which has also been observed in laboratory and field trials with neonicotinoid (e.g., Vernon et al., 2008) and pyrethroid insecticides (e.g., van Herk et al., 2013).

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It was concluded in the work of Furlan et al. (2010) that for B. carinata DSM to be practical in the field certain conditions had to be fulfilled concurrently, including a suitable dosage of glucosinolates in the DSM (at least 160 mmol of glucosinolates per liter of soil), a homogeneous broadcast application of DSM, effective and prompt soil incorporation to 20 cm, suitable soil and humidity conditions, and presence of wireworms predominantly in the upper 20 cm of soil. Given that the persistence of the toxic metabolites of glucosinolates is short (less than 48 h), it is vital that all of these conditions are met within the first 2 days of application for this approach to be fully effective. Once again, a thorough knowledge of all species present and their temporal and spatial behavior in the soil is required to determine the practicality and potential effectiveness of this technique or modified versions thereof in other areas. Nevertheless, the preliminary success of Furlan et al. (2010) suggests that further work on biofumigants such as B. carinata DSM is warranted, especially for organic production.

7.7.1.4 Potato varietal tolerance The tolerance of certain potato cultivars to wireworm damage can be an important component of management strategies, particularly in organic production systems, and most of the relevant scientific research has been reviewed by Parker and Howard (2001) and Andrews et al. (2008). Among the more notable research in recent years is that of Kwon et al. (1999) in Korea, Johnson et al. (2008) in Scotland, Langdon and Abney (2017) in the U.S.A. and Fasulati et al. (2019) in Russia, who found significant differences in wireworm damage between various cultivars in the lab or field. The relative susceptibility of various potato cultivars to feeding by wireworms has been shown to be related to the total glycoalkaloid (TGA) content present in daughter tubers (Jonasson and Olsson, 1994; Olsson and Jonasson, 1995). Unfortunately, glycoalkaloids are also toxic to humans, and there are regulatory limits to the amounts of these TGAs allowed in new potato varieties. It has not been until recently that breeding of potatoes for resistance specifically to wireworms has taken place (Novy et al., 2006). Germplasm from wild relatives of potato from South America, Solanum berthaultii Hawkes and S. etuberosum Lindley, crossed with a cultivated potato variety has produced a number of resistant clones with wireworm damage reductions as good as observed with insecticide-treated crops (Suszkiw, 2011). Some of these resistant clones contain levels of TGAs suitable for human consumption, which opens the door to their use in the development of wireworm-resistant commercial varieties for the future.

7.7.1.5 Early harvest As has been mentioned, damage to daughter tubers typically increases as the growing season progresses, and the longer potatoes are left in the ground, the greater the amount of damage that will occur (Fig. 7.4) (Anonymous, 1948; Parker and Howard, 2001; Kuhar and Alvarez, 2008, Vernon, unpubl. data). Therefore, if potatoes must be planted in infested fields, varieties should be grown that can be lifted before wireworms begin to actively feed on tubers, or later season varieties should be harvested as soon as possible (Parker and Howard, 2001; Andrews et al., 2008). In Germany, Schepl and Paffrath (2005) found less wireworm damage on tubers harvested in late July to early August (8%e50% tubers damaged) than in September (72%e77% damage), and an increase in damage with later harvest dates was observed by Neuhoff et al. (2007).

7.7.2 Chemical methods 7.7.2.1 Wireworm controls Chemical controls to manage wireworm damage to potatoes have historically involved prophylactic treatments applied before, at, or after planting to control the wireworm stage in soil. In addition to soil fumigation, pre-planting treatments have included insecticides either broadcasted on the soil surface and worked into the ground, or as insecticide-laced fertilizers (Parker and Howard, 2001), with the intent of intercepting and killing wireworms in their movements near the soil surface in spring. At the time of planting, insecticides have also been applied in-furrow either as granular or spray formulations, or more recently as seed treatments applied to mother tubers just prior to planting. Post-planting applications include side-band applications intended to kill wireworms near the surface of potato plants at the start of daughter tuber formation. The effectiveness of these various application methods has varied considerably (Parker and Howard, 2001; Kuhar and Alvarez, 2008), but in general, at-planting in-furrow applications of insecticides appear to be the most widely used methods worldwide. There have been a large number of insecticides registered for use on potatoes globally. In the U.S.A. there are over 30 insecticides in 15 classes currently registered for Colorado potato beetle control alone (Alyokhin et al., 2008), some of which are also registered for use against wireworms. The general histories of use in potatoes and chemical properties of some of these insecticidal classes, including: chlorinated hydrocarbons, organophosphates and

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carbamates, pyrethroids, neonicotinoids, and phenylpyrazoles, are covered in Chapter 11. The following describes the history and relative efficacies of various representatives of the aforementioned classes in managing wireworms, focusing on what is now known about their ability to not only reduce cosmetic damage to daughter tubers at harvest, but also to reduce wireworm populations. In addition, a new class of insecticides, the “meta diamides” is described, that will have profound impacts on wireworm management in potatoes and key rotational crops (e.g., cereals) in the future.

7.7.2.2 Organochlorines The fact that wireworms became a pest of low worldwide importance following World War II can be attributed almost certainly to the introduction and widespread use of the organochlorine insecticides in the 1950s. At that time, insecticides such as DDT and aldrin applied as pre-planting broadcast sprays or as “aldrinated” fertilizers to the soil became standard treatments for wireworms in many parts of the world (Merrill, 1952; Strickland et al., 1962; Parker and Howard, 2001; Kuhar and Alvarez, 2008). One characteristic of these and other organochlorines (e.g., heptachlor, dieldrin, chlordane, etc.) that made them particularly effective was their persistence in soil for years following application. In the case of aldrin and heptachlor, one application to soil was reported to kill wireworms (A. obscurus) for 13 years (Wilkinson et al., 1964, 1976). Multiple applications to fields during the tenure of these insecticides would have been very effective in preventing population build-ups even well beyond their global de-registrations (due primarily to their long persistence) in the 1970s and 1980s. It is thought by some that the present upsurge of wireworm populations is due in part to the gradual decline of these persistent organochlorine residues in fields to levels non-toxic to neonate wireworms (Jansson and Seal, 1994; Parker and Howard, 2001; Horton and Landolt, 2002). In addition to the persistent soil-applied organochlorines, it is relevant to this discussion that lindane, an organochlorine with shorter persistence, became a standard seed treatment for control of wireworms in cereal crops and corn in many countries as early as the 1940s. These seed treatments reportedly reduced field populations of wireworms (e.g., Selatosomus destructor and Hypnoidus bicolor) by about 70% (Arnason and Fox, 1948), and in Canada wireworm damage in the prairies declined gradually from 1954 to 1961, coincident with the increasing use of lindane seed treatments (Burrage, 1964). With the eventual de-registration of lindane in most countries by 2007, however, it was expected that wireworm populations would increase, since cereal crops are preferred oviposition hosts for many species, and no contemporary cereal seed treatments significantly kill wireworms (Vernon et al., 2009; 2013b; van Herk et al., 2018, 2021a). A dramatic increase in wireworm populations has in fact been observed over the past 2 decades in many major cereal production areas of Canada (Vernon et al., 2013b, van Herk et al., 2021a), and this has had direct implications for wireworm control in potato crops now typically grown in rotation with cereals.

7.7.2.3 Organophosphates and carbamates With the gradual demise of the persistent organochlorines, a number of organophosphate and carbamate insecticides were registered for wireworm control in potatoes on a global scale, and some of these insecticides remain the first line of defense in many countries (Edwards and Thompson, 1971; Parker and Howard, 2001; Kuhar and Alvarez, 2008). Research in Europe and North America, however, generally found that the organophosphates and carbamates were not as effective as organochlorines such as aldrin (Caldicott and Isherwood, 1967; Hancock et al., 1986; Parker et al., 1990; Parker and Howard, 2001), and organophosphates have generally proved more effective than carbamates (Arnoux et al., 1974; Finlayson et al., 1979; Toba, 1987; Parker et al., 1990). Nevertheless, control of wireworm damage with these insecticides in various countries (i.e., the organophosphates phorate, fonofos, chlorpyrifos, ethoprop, and the carbamate carbofuran) has generally been acceptable, although the efficacy of these products could be somewhat inconsistent or even fail (Hancock et al., 1986; Parker and Howard, 2001; Kuhar and Alvarez, 2008). The reasons for inconsistency in efficacy of organophosphates and carbamates for wireworm control in potatoes and other crops has not been adequately explained, although an understanding of these factors would likely lead to methods for improving the consistency and efficacy of controls. A common belief is that since most wireworm damage to potatoes occurs late in the growing season, an insecticide applied at or before planting must be residual at levels adequate to kill wireworms up to the time of harvest (Parker and Howard, 2001). Although this was likely the case with the persistent organochlorines, there is currently no evidence that organophosphate or carbamate insecticides will provide significant residual control late into the potato-growing season. In fact, the degradation curves of certain formerly used wireworm insecticides in soil (e.g., fonofos and carbofuran) indicated that less than 10% of the parent compounds remained after 70 days (Onsager and Rusk, 1969). Late season control with organophosphates and carbamates also assumes that wireworms feeding near harvest would not have contacted or fed upon the crop within the treated area up to that time. It is the understanding of the authors, however, that most if not all wireworms in a field will feed at some time in the spring, which

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generally coincides with the planting of potatoes. If the primary source of food at that time is the planted potato crop (i.e., there is no green-ploughed pasture or weeds, etc., in the field), then most wireworms will orient to and feed on mother tubers located within the insecticide-treated furrow. Also, maturing daughter tubers near harvest often lie outside the initial treatment area, which would further reduce exposure of wireworms to any residual insecticides left at that time. It is likely, therefore, that the effective control of wireworms by organophosphate and carbamate insecticides in potatoes is primarily through high early-season mortality or prolonged morbidity, rather than mortality occurring later in the season. Following this line of reasoning further, if potatoes are planted in fields with no competing sources of CO2 in soil at a time when wireworms are fully active in spring, this would ensure that the majority of wireworms would be attracted to the mother tubers (primary source of CO2), and encounter in-furrow insecticides at a time when insecticide titer was highest. In situations where these conditions are not met e for example, if planting occurs outside of the spring wireworm feeding period, or if alternative sources of CO2 are present in soil (e.g., green ploughed pasture or sod) e it is likely that part of the population would not encounter the in-furrow treatment in spring, and therefore survive to feed on maturing tubers later on. In efficacy work by the authors over a 19-year period, trials were always conducted under the optimum field conditions described above, and efficacy of various standard organophosphates (i.e., phorate and chlorpyrifos) has always been consistently high (Vernon et al., 2007, 2013a). When failures of phorate to control wireworm damage have been reported to the authors, they were generally associated with situations where the field has been in pasture and was ploughed green just prior to planting potatoes. Research to validate this line of reasoning is currently underway by the authors and others, but it might be taken into account when conducting or interpreting efficacy trials, or in developing IPM programs for growers. Just as the organochlorines were banned globally due largely to their persistence in soil, the relatively high toxicity of the organophosphates and carbamates to humans and the environment has resulted in the loss of many of these wireworm insecticides over the past decade, and this attrition is expected to continue. In Canada, for example, the organophosphate phorate (Thimet 15G, and more recently Thimet 20G) is the primary organophosphate insecticide remaining for wireworm control in potatoes. This highly toxic insecticide has already been withdrawn from use in British Columbia due to raptor poisonings coincident with increased usage in potatoes for wireworm control in the 1990s (Elliott et al., 1996; Wilson et al., 2002), and elsewhere in Canada can only be applied with specialized application equipment that reduces occupational exposure and ensures accurate placement and rate of material at planting. With the ongoing global decline of organophosphates and carbamates coincident with the re-establishment of wireworms as key pests of potato, there has been the pressing need to identify alternative insecticide candidates with more favourable toxicity and environmental profiles (Parker and Howard, 2001; Kuhar and Alvarez, 2008). In response to this need, most of the more recent research attention has focused around five contemporary classes of insecticides: the neonicotinoids, the pyrethroids, the phenylpyrazoles, the diamides, and most recently the meta diamides.

7.7.2.4 Neonicotinoids Neonicotinoids (e.g., imidacloprid, clothianidin, and thiamethoxam) applied as seed treatments to cereal crops have been shown to provide good stand and yield protection from wireworm feeding (e.g., Vernon et al., 2009), and registrations exist for cereal crops in a number of countries. Initially, at least in Canada, it was hoped that these insecticides might replace the de-registered organochlorine lindane in providing both yield protection and wireworm reduction in cereal crops, and thus reduce populations leading up to potato rotations. However, several years of field data by the authors have shown that wireworm populations are not significantly reduced by any of these neonicotinoids at the field rates registered, and damage protection in cereals is likely due to wireworms becoming reversibly intoxicated or moribund, rather than dying during the crop establishment phase (Vernon et al., 2007, 2009, 2013b; van Herk et al., 2018, 2021a). Laboratory studies have also shown that contact exposure of several economic species of wireworms (A. obscurus, A. sputator, L. canus, S. destructor, and S. pruininus) to chloronicotinoid (imidacloprid, acetamiprid) and thianicotinoid (clothianidin, thiamethoxam) insecticides causes rapid and prolonged periods of morbidity (>150 days), during which feeding ceases and after which wireworms make a full recovery (van Herk et al. 2007, 2008; Vernon et al. 2008). It was also found that toxicities of these neonicotinoids differed among species (van Herk et al., 2007, 2008). The conclusion from these laboratory and field studies is that although neonicotinoid-treated cereal crops are protected from early season feeding through wireworm intoxication, populations eventually recover to full health and can thereafter continue their life cycle in subsequent crops (i.e., potato). In addition, neonicotinoid seed treatments have no effect on neonate wireworms arising in the field later in the summer, and this cohort of wireworms will also carry over to subsequent rotational crops (Vernon et al., 2009, 2013b, van Herk et al. 2021a).

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In potatoes, a number of neonicotinoids have been registered as seed piece treatments, or as in-furrow sprays for the systemic control of various aboveground pests (e.g., Colorado potato beetles and leafhoppers; Kuhar et al., 2007) and are listed on some labels as providing wireworm damage suppression (e.g., clothianidin in Canada). The reduction of wireworm blemishes by these treatments, however, has been very inconsistent in the field, with reports of acceptable and consistent levels of control in British Columbia, Canada (A. obscurus; Vernon et al., 2007, 2013a) and Virginia, USA (Melanotus communis; Kuhar and Alvarez, 2008), and reports of unacceptable control in Ontario (Melanotus spp.; Tolman et al., 2005) and Prince Edward Island, Canada (A. sputator; Noronha et al., 2007). It is interesting to note that potato seed piece treatments with clothianidin and thiamethoxam provided excellent blemish control in 1 year in a 2006 PEI trial (Noronha et al., 2006), but no control in the years following (e.g., Noronha et al., 2007). It is thought that wireworms become intoxicated initially upon contact with neonicotinoids on potato seed or in treated furrows, and that blemish control is dependent on whether or not wireworms remain intoxicated throughout tuber maturation and harvest. The duration of intoxication, and thus damage to tubers, is likely to vary according to soil type, climate, or species (Vernon et al., 2007). As was observed with neonicotinoid-treated cereal crops, there was no significant mortality of wireworms in plots of potatoes treated with neonicotinoids when plots were sampled the following spring in several years of study by the authors (Vernon et al., 2007, 2013a).

7.7.2.5 Synthetic pyrethroids Pyrethroids, although generally formulated as above-ground foliage sprays, have also shown varying degrees of promise as in-furrow applications for wireworm control. Tefluthrin, for example, although providing acceptable protection from wireworm damage in corn as an at-planting granular application, has not provided acceptable blemish control in potatoes (Vernon, unpubl. data). As an experimental seed treatment on wheat, tefluthrin provided good crop stand and yield protection under heavy wireworm pressure (A. obscurus), but similar to neonicotinoid treatments, did not reduce resident or neonate wireworm populations (Vernon et al., 2009). In laboratory studies, tefluthrin applied to wheat seed was found to be repulsive and non-lethal to wireworms, and it is hypothesized that repulsion, rather than mortality of wireworms, accounts for the stand protection observed in wheat and corn (van Herk and Vernon, 2007). Bifenthrin, a pyrethroid with long persistence in the soil (half-life of 122e345 days; Fecko, 1999), is registered on potatoes as an in-furrow spray for wireworm control in the USA and has been shown to reduce wireworm damage similar to the commonly used organophosphate, phorate (Kuhar and Alvarez, 2008; Vernon, unpubl. data). It is interesting to note, however, that bifenthrin at field application rates was also found to be repulsive but not lethal to wireworms (A. obscurus) in the laboratory, and that soil from bifenthrin-treated potato trials was repulsive to wireworms 1 year after application (van Herk and Vernon, 2013; van Herk et al., 2013). This suggests that an in-furrow application of bifenthrin at planting will establish a repellent zone along seeded potato rows that prevents wireworms from approaching the mother and daughter tubers through the harvest period. In several field studies, we have also shown that bifenthrin applied to the sides and bottom of widely opened furrows at planting provided superior damage protection to tubers than if applied only to the furrow bottom (Vernon, unpubl. data). Although further research is needed to determine the ultimate fate of various economic wireworm species in bifenthrin-treated fields, the available data suggest that blemish protection to tubers can be significant and offers a viable alternative to existing OP insecticides.

7.7.2.6 Phenylpyrazols The phenylpyrazole fipronil, is the most effective wireworm insecticide developed since the organochlorines and has been registered for wireworm control in corn and potatoes in the USA. What makes fipronil unique relative to the neonicotinoids and pyrethroids is that it rapidly kills wireworms of all species upon contact at registered rates, and even at much lower rates will immobilize and gradually kill wireworms several months after exposure (van Herk et al., 2007; Vernon et al., 2008). This latent toxicity has presented a number of options for effective, lower-risk management of wireworms that will be discussed below. In potatoes, fipronil applied as an in-furrow spray at planting has been shown to provide blemish control comparable to the OP phorate (Sewell and Alyokhin, 2004; Vernon et al., 2007, 2013a; Kuhar and Alvarez, 2008), and high mortality of resident and neonate wireworms (96%e100%) has also been observed (Vernon et al., 2007, 2013a). In cereal crops, fipronil applied to seed at rates 10 times lower than the formerly used OC lindane was shown to provide excellent wheat stand protection, and significantly reduce resident and neonate wireworm populations in lab and field trials (Vernon et al., 2007, 2009, 2013b). Stand protection and wireworm reduction with fipronil at those low rates were actually superior to the formerly registered organchlorine lindane (Vernon et al., 2013b), suggesting that the general reductions in

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wireworm economic importance coincident with increasing lindane use in the past (Burrage, 1964) could again be achieved with fipronil seed treatments. However, due to various environmental concerns associated with the existing domestic and agricultural usage of fipronil, expanded registrations into crops such as cereals will not likely occur globally.

7.7.2.7 Diamides Diamides (e.g., cyantraniliprole), a relatively new class of insecticides, although providing early season wheat stand protection from wireworms when applied to seed, had no effect in reducing high populations of wireworms in field trials in Alberta (e.g., L. californicus, van Herk et al., 2018) and British Columbia, Canada (e.g., A. obscurus, van Herk et al., 2021a). When tested on potatoes as in-furrow sprays, neither cyantraniliprole nor chlorantraniliprole provided significant reductions in tuber damage, nor did they reduce wireworm populations (Vernon et al., 2013a). In trials conducted over 7 years in Virginia, wireworm injury to daughter tubers in cyantraniliprole plots was reduced by an average of only 38%, relative to 78% reduction in phorate plots (Kuhar and Doughty, 2015). Laboratory studies showed that cyantraniliprole was not repulsive to wireworms (A. obscurus), but rather induced reversible morbidity upon contact with treated wheat seed, much like the neonicotinoids (van Herk et al., 2015b). What appears to be occurring in potato trials, is that any wireworms encountering a diamide such as cyantraniliprole or chlorantraniliprole likely will become intoxicated, but will subsequently recover in time to cause significant feeding damage to tubers by harvest.

7.7.2.8 Meta diamides Meta diamides are a recently developed insecticidal class of GABA-gated Cl channel allosteric modulators (Nakao, 2015) that bind to a unique site in the GABA receptor (Group 30 MOA). The first meta diamide insecticide to be developed and registered, broflanilide, has shown extraordinary results in controlling wireworms in wheat and potatoes. When evaluated in wheat trials over 7 years at various rates, broflanilide was as effective at protecting wheat stand from wireworm (A. obscurus) injury as the neonicotinoid industry standard thiamethoxam (van Herk et al., 2021a). In addition, broflanilide reduced neonate and resident wireworms in research plots by 79.8%, relative to only a 6.9% wireworm reduction in thiamethoxam plots (van Herk et al., 2021a). This rate of wireworm reduction is comparable to the 70% reduction reported for the formerly widely used and highly effective organochlorine lindane (Arnason and Fox, 1948). In earlier wheat studies, the highly effective phenylpyrazole fipronil, applied at the same rate as broflanilide (5.0 g active ingredient/100 kg wheat seed), reduced A. obscurus wireworms by 85.5% (mean of four studies, Vernon et al., 2013b), suggesting these insecticides (both of which target insect GABA-gated Cl channels) would have similar efficacy in reducing wireworm populations in cereal crop rotations. When evaluated as an in-furrow spray in potato trials from 2017 to 19, broflanilide reduced damage to daughter tubers at harvest by an average 94.7%, relative to a 92.0% reduction in phorate plots (Vernon, unpubl. data). Post-harvest sampling in these trials indicated that wireworm populations in broflanilide and phorate plots were reduced by 97.7% and 88.3%, respectively, suggesting these two insecticides are roughly equivalent in efficacy, at least against A. obscurus. In laboratory studies, broflanilide on germinating wheat seed was not repulsive, and following contact, wireworms rapidly entered a morbid state and eventually died (van Herk, unpubl. data), exhibiting non-reversible toxicity symptoms similar to fipronil (van Herk et al., 2015b). In the field, the high mortality of wireworms observed in our wheat and potato studies is likely through contact with in-furrow treated soil (potatoes) and feeding and/or contact with germinating seed (wheat). Broflanilide was granted registration on wheat (Teraxxa and Teraxxa F4) and potatoes (Cimegra) in Canada (2020) and the USA (2021), and has been submitted for registration in other countries. Where registered, wireworm damage to cereal and potato crops as well as reductions in wireworm populations can be economically achieved with much lower field application rates than any currently registered insecticides. This is particularly true in production areas where cereal crops are commonly rotated with potatoes, and where both crops can be treated consecutively.

7.7.2.9 Insecticide combinations Combinations of various insecticides have been shown to enhance the scope and efficacy of management of wireworms and other pest species of potatoes beyond the effects of the individual insecticides alone (Kuhar and Alvarez, 2008; Tolman et al., 2008; Tolman and Vernon, 2009; Vernon et al., 2013a; Kuhar and Doughty, 2015). For example, combining the nonsystemic organophosphate chlorpyrifos applied as an in-furrow spray with a systemic neonicotinoid (e.g., clothianidin, thiamethoxam) applied either as seed piece treatments or in-furrow sprays, provided excellent blemish control as well as enhanced reductions in wireworm populations (Tolman and Vernon, 2009; Vernon et al., 2013a). Applied alone,

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chlorpyrifos (not systemic) will provide acceptable control of wireworms but will not control above-ground insect pests (e.g., Colorado potato beetles), and clothianidin or thiamethoxam will provide some wireworm control as well as systemic control of above-ground pests. Together, these insecticides match the broad-spectrum efficacy of the commonly used systemic organophosphate phorate, but with reduced environmental risk. Similarly, neonicotinoids applied as potato seed piece treatments or as in-furrow sprays (e.g., clothianidin, thiamethoxam) in combination with in-furrow sprays of a pyrethroid (non-systemic) such as bifenthrin have also been shown to provide slight improvements to wireworm blemish control and will also control above-ground pests (Kuhar and Alvarez, 2008; Tolman et al., 2008, 2009). Combinations of insecticides are also being investigated to control wireworm populations in rotational crops such as wheat. The organochlorine lindane, formerly registered in Canada and elsewhere as cereal and corn seed treatments, reduced resident wireworm populations in fields of wheat by 70% (Arnason and Fox, 1948; Vernon et al., 2009). It was also found that the residual action of lindane was sufficient to kill about 85% of newly formed neonate wireworms (A. obscurus) (Vernon et al., 2009, 2013b). This clean-up of existing and neonate populations of wireworms meant that the field would have low numbers of wireworms for at least 2 years, during which time potatoes could be planted with lower economic risk of wireworm damage (Vernon et al., 2009, 2013b). As discussed above, neonicotinoids (e.g., imidacloprid, clothianidin, and thiamethoxam) applied as seed treatments to cereals, although providing excellent stand protection and yield, did not significantly reduce wireworm populations (Vernon et al., 2009, 2013b). The phenylpyrazole fipronil, on the other hand, provided excellent reduction of both resident and neonate wireworms, but had reduced stand protection when applied at low rates to cereal seed (Vernon et al., 2013b). To circumvent these problems, neonicotinoids (e.g., thiamethoxam) at lower registered rates (about 10 g a.i./100 kg wheat seed), blended with low rates of fipronil (1e5 g a.i./100 kg seed) have been shown to preserve crop stand and yield, as well as reduce resident and neonate populations even more effectively than lindane applied at 60 g a.i./100 kg seed (Vernon et al., 2013b). Similar results have also been achieved with the novel meta diamide insecticide broflanilide (2.5 g a.i./100 kg wheat seed) blended with thiamethoxam (10 g a.i./100 kg wheat seed), which is expected to be used in cereal crop rotations to reduce wireworm populations in fields destined for potatoes (van Herk et al., 2021a). In addition, fipronil or broflanilide treated wheat seed, with or without thiamethoxam, has been incorporated into potato seed furrows for control of wireworms in experimental trials (Vernon et al., 2016, unpubl. data). The principle of this method is to attract the majority of wireworms to the lethal wheat seed, which germinates before the mother tubers. Such treatments have been shown to reduce wireworm damage to daughter tubers as effectively as phorate (Tolman and Vernon, 2009; Vernon et al., 2016), and significantly reduce wireworm populations with very low amounts of insecticide per ha.

7.7.2.10 Click beetle controls Click beetles set the stage for wireworm problems by ovipositing in fields of their preferred crops (i.e., pasture, cereals). By preventing oviposition in these fields, wireworm populations will not reach economic levels, and this approach has been explored in The Netherlands (Ester et al., 2004; van Rozen et al., 2007). With the use of pheromone traps for the three primary species (A. obscurus, A. lineatus, and A. sputator), peak activity of male click beetles was determined, and fields were sprayed once or twice with foliar applications of a pyrethroid (i.e., deltamethrin or lambda cyhalothrin). These sprays were very effective in killing both male and female click beetles, which in theory would reduce wireworm populations in fields through reduced oviposition (A. Ester, pers. comm.). This strategy would be applied each time a preferred oviposition crop was grown in the field, and reduced oviposition would be required for a number of years equivalent to the life cycle of the wireworms involved (i.e., 4e5 years for Agriotes spp.). Such a strategy is somewhat more limited in scope than soil-applied insecticides for wireworm control, in that management activities required are heavier and protracted over several years (i.e., routine pheromone trapping for multiple species, trap interpretation, field spraying); simple adult monitoring tools such as pheromone traps must be available for all key species; the fields must be under the control of one grower, and not leased land (as is common in many potato growing areas worldwide); and insecticides need to be registered specifically for click beetle control in each country using this technique. It is expected, however, that this approach will grow in popularity as effective soil-applied wireworm control options dwindle, and as pheromones become available for more species worldwide.

7.7.3 Biological controls 7.7.3.1 Predators A number of arthropod predators of wireworms have been recorded, including several genera of carabids, staphylinids, and therevids (Thomas, 1940; Fox and MacLellan, 1956; van Herk et al., 2015a), but there have been no records of significant

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population reductions occurring due to these species. Birds, especially crows, are commonly cited as feeding on wireworms concurrent with cultivation activities (Thomas, 1940; Gratwick, 1989), and they have been observed uprooting cabbage (Thomas, 1940) and transplanted strawberry seedlings (Vernon, unpubl. data) to feed on wireworms assembled at the roots. Although crows can eat numerous wireworms (e.g., 72 wireworms; Kalmbach, 1920), their impact on field populations is not considered significant because populations can be in the millions per ha (Miles and Cohen, 1939), and only a small portion of a population is exposed during cultivation. A more comprehensive listing of the known parasites and predators of wireworms can be found in Thomas (1940).

7.7.3.2 Microbial pathogens Microbial control agents attacking wireworms and click beetles have been commonly observed in nature or in outbreaks occurring in laboratory colonies, and the reader is referred to reviews by Thomas (1940), Parker and Howard (2001), Wraight et al. (2009) and Ritter and Richter (2013) that list the early and more contemporary literature on this subject. Historically, most of the attention has focused on the fungal pathogen Metarhizium anisopliae (Metschn.) Sorokin (now Metarhizium brunneum (Metschn.) Sorokin), which has been observed to infect, for example, Melanotus spp. (Hyslop, 1915); Agriotes mancus (Gorham, 1923); Limonius californicus (Rockwood, 1950); and A. obscurus, A. lineatus, A. sputator, and L. canus (Fox and Jaques, 1958; Kabaluk et al., 2005). Early attempts at controlling wireworm populations with inundative releases of endemic strains of M. brunneum in soil were unsuccessful (Hyslop, 1915; Fox and Jaques, 1958); however, with the development of improved methods of producing and formulating M. brunneum (Jackson and Jaronski, 2012; Eckard et al., 2014), there has been a renewed interest in evaluating various isolates for wireworm biocontrol (Wraight et al., 2009). The results thus far suggest that although wireworms of a number of species can be infected and killed under defined laboratory conditions (e.g., Ericsson et al., 2007; Kabaluk et al., 2007a), attempts to control wireworms with inundative releases in the field are typically variable due to a number of biotic and abiotic factors (e.g., Kabaluk et al., 2005; Tharp et al., 2007; Kuhar and Doughty, 2008; Ritter and Richter, 2013; Kabaluk and Ericsson, 2014; Ensafi et al., 2018). Among the more optimistic of these field trials, Kabaluk et al. (2005, 2007a) reported a 33.3% reduction in wireworm blemishes to daughter tubers with a pre-plant broadcast application of M. brunneum, and in another trial, infected A. obscurus cadavers were retrieved from treated field soil, confirming some in-field mortality was achievable with this approach (Kabaluk et al., 2007b). Opportunities for enhancing the efficacy of M. brunneum have also been explored. Ericsson et al. (2007) found that the natural insecticide spinosyn synergized efficacy against wireworms (A. lineatus) in the lab, and novel application techniques to draw wireworms to living and non-living baits in association with M. brunneum have been shown to reduce wireworm damage to tubers from 37% to 75% (e.g., Brandl et al., 2017). Although the wireworm stage is generally the main target, Kabaluk et al. (2005) reported that adult click beetles (A. obscurus) were as susceptible as wireworms to M. brunneum infections in the laboratory, and various strategies for the biological control of click beetles in the field have been proposed (Kabaluk, 2014; Kabaluk et al., 2015). The fungal pathogen Beauveria bassiana has also been evaluated with some success as a biocontrol agent for wireworms attacking potatoes (e.g., Ester and Huiting, 2007; Ladurner, 2007; Ritter and Richter, 2013, Bariselli et al., 2018), and liquid formulations of B. bassiana conidia have been approved for wireworm control in potatoes in Europe (e.g., Naturalis-LÒ, B. bassiana strain ATCC 74040; www.intrachem.com), primarily against several species of Agriotes. It should be noted, however, that the effectiveness of fungal pathogens observed against one or more wireworm species cannot be assumed to apply to all species (Wraight et al., 2009), and differential susceptibility of various wireworm species to M. brunneum or B. bassiana has been observed in the laboratory (Tinline and Zacharuk, 1960; Zacharuk and Tinline, 1968; Kabaluk et al., 2007a). Present and future areas of research identified for microbial control of wireworms include the search for superior species and isolates (in virulence, productivity and persistence; genetic modification; blending entomopathogens or entomopathogens with other agents (e.g., insecticides); and optimization of delivery at the field level (Wraight et al., 2009).

7.7.3.3 Nematodes Entomopathogenic nematodes have shown limited success in controlling wireworms at the commercial level. Toba et al. (1983), although documenting reductions in Limonius californicus populations of 29% with Steinernema feltiae (Filipjev) in the field, concluded that the lethal dose required to achieve higher levels of control would be cost-prohibitive. In addition, residual control of wireworms was not observed within months of S. feltiae application (Toba et al., 1983). In more recent work, Ester and Huiting (2007) did not find S. feltiae to be effective in the field against Agriotes spp. Between 24% and 39% mortality has been reported under laboratory conditions with S. carpocapsae, H. bacteriophora, and S. riobrave against small to medium-sized L. canus wireworms (Wraight et al., 2009). When used in combination with

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resistant cultivars and/or insecticide, S. carpocapsae reduced damage by wireworms (Conoderus spp.) to sweet potatoes by up to 25% (Schalk et al., 1993). With any living biological control agent targeted for use in soil, however, careful consideration must be given to determine the conditions required for optimal efficacy to occur (e.g., soil variables including texture, temperature, and moisture). Under abnormally wet conditions, for example, S. carpocapsae was leached from the rhizosphere of sweet potatoes and provided no wireworm control (Schalk et al., 1993).

7.7.4 Semiochemical controls Where pheromones have been developed for key wireworm species, their potential for reducing click beetle populations or disrupting mating in order to reduce oviposition and the ensuing build-up of wireworm populations has been investigated. In Russia, pheromones applied to fields at the rate of 120 g pheromone/ha caused the “disorientation” (confusion) of male Agriotes (species not disclosed), resulting in over 70% of females remaining unmated (Ivashchenko and Chernova, 1995). This abstract also alluded to mass trapping, but this technique was not discussed except to state that it was less effective than disorientation. Balkov and Ismailov (1991) found that effective direct control of A. sputator and A. gurgistanus was achieved with the intensive use of pheromone traps over 3e4 years. In other work, Balkov (1991) found that 30 A. sputator pheromone traps/ha reduced larvae by 86% after 4 years of mass trapping in a field with medium wireworm infestation (up to 5 individuals/m2). At high levels of infestation (>10 individuals/m2), 120 traps/ha were required. In the UK, Hicks and Blackshaw (2008) determined that mass trapping within fields to reduce mating of A. lineatus, A. obscurus and A. sputator would cost, respectively, 165, 247 and 2343 Euros/ha/year, which of course would be additive where 2 or three of these species occur in the same field. In Germany, Sufyan et al. (2011) determined that mass trapping for A. obscurus would require 25 traps/ha to reduce male populations below 50%. In Japan, Kishita et al. (2003) used markereleaseerecapture studies with pheromone traps to estimate the population density of Melanotus okinawensis on Ikei Island, and Yamamura et al. (2003) used the same method to estimate its average dispersal distance (144 m in 4 days). From those studies, Arakaki et al. (2008a) reduced the population of M. okinawensis on Ikei Island (158.3 ha) by about 90% over 6 years of mass trapping (10 pheromone traps/ha), but observed no reduction in population in a similar study with M. sakishimensis on Kurima Island (Arakaki et al., 2008b). In a long-term mating disruption study on Minami-Daito Island (3057 ha), using one, 80-m long pheromone dispenser roll/ha, numbers of adult M. okinawensis captured by hand had decreased by 89.3% after 7 years, and mating rates were significantly lower (range 14.3%e71.4%) than in untreated areas (96.9%e100%) (Arakaki et al., 2008c). In those studies, however, there were no surveys taken to determine if the number of wireworms in soil were proportionately reduced. The large-scale removal of adults will not necessarily reduce larval populations, as demonstrated by Campbell and Stone (1939) in California with L. californicus. This is particularly of concern if the adults can fly or repopulate a field quickly from refuge areas, in which case mass trapping may be a more effective strategy when combined with topical applications of insecticides in areas where the beetles are known to be concentrated, provided this is done prior to mating and oviposition (Ester and Rozen, 2005). The limited interest in mass trapping or disorientation of click beetles as an indirect wireworm control method can be attributed to several factors. A major obstacle is the cost and inconvenience of deploying and maintaining from 30 to 120 pheromone traps/ha annually in large fields during a mixed 4-year crop rotation (using Balkov’s, 1991 study as an example). Also, since multiple species of wireworms (e.g., Agriotes spp. and Melanotus spp.) are often present in fields, the cost of trapping increases proportionately with the number of economic species present. The use of semiochemicals for disruption or mass trapping to pre-emptively reduce click beetle oviposition has historically targeted cultivated or soon-to-be cultivated agricultural land. These fields can be considered non-permanent wireworm population reservoirs, however, in that they are subjected to a wide variety of wireworm populationdisrupting or -enhancing activities, including favorable or unfavorable crop rotations, field cultivation practices, and various field/crop amendments (e.g., irrigation, insecticide treatments, etc.). Another approach to reduce click beetle oviposition would be to target the more permanent wireworm population reservoirs that often surround cultivated fields in the general agricultural landscape. These permanent reservoirs may include grassy headlands, ditch banks, dykes, etc., which generally contain most stages of various key economic wireworm species, and which often produce the adult beetles that chronically invade adjacent fields (i.e., cereals, pasture) to oviposit. Also, these permanent reservoirs tend to occupy only a very small fraction of land in intensively farmed areas, making higher cost-control methods (such as mass trapping, mating disruption, etc.) potentially more affordable. In addition, once wireworm populations are removed from permanent reservoirs, control efforts in those areas could be abandoned for several years until new click beetle population build-ups warrant renewed control efforts.

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Management of click beetle populations by mass trapping with pheromone traps in reservoir areas has been explored in Canada by the authors. In British Columbia, A. obscurus and A. lineatus traps placed in parallel transects of 2 rows of 15 traps (3 m between traps and rows) along a 10 m wide dense grassy headland area, collected, respectively, 85.6% and 77.8% of mark-released beetles, mostly within the first week of release (Vernon et al., 2014a,b). In subsequent studies, 82%, 79% and 77% of marked A. obscurus were recaptured after 1 week in trap arrays spaced, respectively, 2.5, 5.0 and 7.5 m apart in a grassy habitat, dropping to 65% recapture at trap spacings of 10 m (Vernon, unpubl. data). This suggests that significant reductions (approx. 75%e80%) of male A. obscurus and probably A. lineatus can be achieved in grassy headlands surrounding arable fields with trap arrays spaced between 5.0 and 7.5 m apart. Although further work is needed to determine the proportion of unmated females resulting in these mass trap arrays, it is expected to be high, both from removal of males early in the beetle emergence period and mating disruption or interference in the remaining males due to pheromone saturation in the trapping area. Paired trap arrays for A. obscurus and/or A. lineatus along 10 m wide headland strips surrounding arable fields would require from 266 to 400 traps per km at 7.5 and 5.0 m spacings, respectively, which would be required over a 4 year period (the typical life cycle of these species). The amortized costs of pheromone traps (e.g., Vernon Pitfall Traps, Fig. 7.6) and lures over four consecutive years of trapping for A. obscurus or A. lineatus would range from $1130 to $1700 CDN per km annually (at 7.5 and 5.0 m spacings, respectively), not including labor. The advantages of headland over in-field mass trapping are that populations of permanent reservoir wireworm populations are reduced, which reduces the threat of annual reinvasion of arable fields, and the season-long disruption of farming activities with in-field trapping does not occur. In addition, the relative number of traps required in mass trapping headlands versus in-field trapping declines as the area of the surrounded field increases. For example, the number of traps required per species in 10 m wide headlands (using 7.5 m trap spacing to reduce A. obscurus males by 75%e80%) surrounding a square 1 ha field would be, respectively, 107 versus 177 traps (using 7.5 m trap spacings in field). In a 10 ha square field, 316 traps per species would be required in headlands relative to 1770 traps required in-field. Also, since mass trapping makes sense only if implemented over a large contiguous farming area where most headland strips are typically shared between adjacent fields, the relative cost of trapping in headlands versus in-field trapping declines even further, and the complexities associated with in-field trapping over 4 years are avoided.

7.8 Conclusions In their review of the biology and management of wireworms on potato, Jansson and Seal (1994) found that wireworms were generally considered a minor pest of potato in most regions of the world at that time. Since then, wireworms have become increasingly problematic in potato crops in Europe and North America (Parker and Howard, 2001; Vernon et al., 2001; Horton, 2006; Kuhar et al., 2008; Noronha, 2011; Barsics et al., 2013; Ritter and Richter, 2013; Traugott et al., 2015), and scientific interest in this complex group of insect pests has experienced a resurgence over the past 2 decades. During the writing of the present review, a number of generalizations were revealed that have relevance to the present and future direction of wireworm research relating to potatoes. Due to the growing severity of the problem in some areas, and since the number of researchers is somewhat limited, it is hoped that the suggestions presented will help to identify the more relevant research paths. The first generalization, arising from our review of elaterid species associated with agriculture globally, is that we are dealing with an extremely complex and diverse group of insect pests and non-pests from the worldwide agricultural landscape right down to the field level. Further to this, it was shown that different species may have vastly different life histories and other biological/behavioral traits and may have differing responses to monitoring approaches and controls; moreover, several of these species may concurrently occupy the same field or fluctuate over time. A fundamental prerequisite for any contemporary management program, therefore, is to know the wireworms involved to the species level, and to preferentially have taxonomic methods available that can be used by researchers and extension professionals at the regional or even local levels. Due to the difficulties and errors inherent with identification using morphological characteristics (e.g., Melanotus spp.), there has been growing activity and success in the development of molecular diagnostics for a number of wireworm genera. Such diagnostic tools, as they are developed for wireworms, will likely become the taxonomic methods of choice, and ultimately facilitate the rapid and accurate identification of single or mixed species in the field. Following the identification of specific wireworm species in a region, subsequent studies should be directed at unknown but relevant aspects of their general biology and ecology, including life history, larval food preferences, spatial and temporal movements in soil, mortality factors, adult oviposition hosts, and so on. The knowledge and tools gained from these research activities are requisite for the development of accurate and effective monitoring and management approaches likely to occur at the regional/field level in the future.

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The second generalization relates to fact that although absolute and relative sampling methods have been developed for wireworms in many countries and for many species, none of these methods is entirely reliable. This is the view not only of the authors but also of other researchers intimately involved with the development and implementation of wireworm sampling programs in potatoes (e.g., Parker, 1996; Parker and Howard, 2001; Horton, 2006). Although absolute or relative sampling reliability is not necessarily crucial for general survey purposes, it becomes profoundly important if the intention of sampling is to provide timely, threshold-based wireworm control recommendations to growers. Typically, the intention of most monitoring programs is to determine whether or not a control action is required to prevent economic pest damage from occurring to a crop. In the case of wireworms and potatoes, the ultimate goal of monitoring would be to indicate whether or not one or more prophylactic controls (field avoidance, planting and harvesting date, insecticide, soil amendment, etc.) is required. Unfortunately, many of the absolute and relative sampling methods developed have been shown to underestimate (or even fail to detect) economic populations of wireworms (Parker and Howard, 2001), which would ensure economic damage on occasion in commercial fields. As discussed in this chapter, much of the variability associated with relative wireworm sampling approaches lies in the consistency of the bait or bait traps used, as well as in the biotic and abiotic factors surrounding their deployment in the field. The general principles, requirements, and sources of variability of the relative sampling methods themselves (such as various baits and baited traps) have been well covered in the literature, and efforts should continue toward the development of even more consistent, convenient, and cost-effective sampling tools in the future. Where there are gaps in our knowledge of sampling, however, is in the identification of species-specific biotic (e.g., competing sources of CO2 in the field) and abiotic (soil moisture, temperature) factors in soil over time that impact positively or negatively on the efficacy and accuracy of a sampling approach. If wireworm sampling for management purposes in potatoes is ever to be implemented with confidence, the physical, environmental, and temporal field conditions contributing to a consistent level of sampling efficacy for all economic species involved must be determined. Probably one of the more exciting and applicable research directions of the past decade has been in the development of species-specific pheromone trapping systems for certain genera of wireworms in Europe (Agriotes; Tóth et al., 2003), Japan (Melanotus; Tamaki et al., 1986, 1990) and more recently in North America (Selatosomus, Limonius, Melanotus, Cardiophorus, Agriotes; Serrano et al., 2018; Williams et al., 2019; Gries et al., 2021, 2022, van Herk et al. 2021d. Such systems have facilitated: (1) large-scale surveys of various species in Europe, Russia, Japan, and North America; (2) spatial and temporal distribution studies of important species at landscape and field levels; (3) monitoring of adult populations to predict wireworm risk in potato fields; (4) monitoring the time to spray adults to reduce oviposition; and (5) investigations into semiochemical-based control programs (e.g., mass trapping). Although further research is required to fully develop and interpret these tools and methods, pheromones have already become an important tool in our wireworm research and management arsenal, and should be expanded to other wireworm genera and key species worldwide. The third and final generalization relates to our belief that to maintain our present standards of quality and abundance in a diverse potato industry, we will require more regional, integrated approaches using the more effective management tools described in this review. The need for development of future management strategies at the regional level is obvious. The conditions favoring wireworm outbreaks will vary from region to region according to many factors, including species complex, agronomic practices (irrigation, tillage), rotations favoring wireworm build-up (pasture, cereal crops), and availability of effective controls (insecticides, entomopathogens, soil amendments, semiochemicals, etc.). Due to the attrition of many of the more persistent and effective synthetic insecticides used for wireworm control in potatoes and other crops (e.g., organochlorines, organophosphates, and carbamates), our ability to actually reduce wireworm populations in fields has also diminished in some countries. This is particularly true in crops often rotated with potatoes, such as cereals and forages, where contemporary insecticides now used for wireworm control (e.g., neonicotinoids or pyrethroids), although preventing stand and yield damage, do not actually kill wireworms (Vernon et al., 2009).4 Various existing (organophosphate) and novel insecticides (neonicotinoids or pyrethroids), as well as alternative methods of control (entomopathogens, soil amendments), have also been shown to vary in efficacy between certain species, and are more suited or even restricted to some regions over others. Therefore, in designing management approaches for the future, researchers will need to know the key species present at the regional level, and the effectiveness of insecticides and alternative approaches to collectively manage these species. As was discussed above for the development of monitoring approaches, research into or selection of management approaches must also consider the biotic and abiotic effects in fields 4. A recent exception to this generality is the discovery of the meta diamide class of insecticides, the first of which, broflanilide, has been shown to provide stand protection in cereals, blemish protection in potatoes, and high levels of wireworm mortality in the lab and field. Although broflanilide is now registered on these crops in Canada and the USA, registration in other countries is not a given, especially where chemical insecticide use is being increasingly de-emphasized relative to alternative methods of control.

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that favor or disfavor the efficacy of various controls. Knowledge of these factors is currently a major gap in our knowledge of wireworm control efficacy and will be especially important if management of wireworms with various integrated cultural, biological, chemical and semiochemical methods is to be optimally realized.

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Yamamura, K., Kishata, M., Arakaki, N., Kawamura, F., Sadoyama, Y., 2003. Estimation of dispersal distance by mark-recapture experiments using traps: Correction of bias caused by the artificial removal by traps. Popul. Ecol. 45, 149e155. Yaping, G., Yuemei, L., Enbo, M., Rui, W., 2000. Study on the taxonomy, distribution and biological characteristics of barley wireworm on Shanxi province. Acta Agric. Boreali Sin. 15, 53e56. Yates, F., Finney, D.J., 1942. Statistical problems in field sampling for wireworms. Ann. Appl. Biol. 29, 156e167. Yatsynin, V.G., Lebedeva, K.V., 1984. Identification of Multicomponent Pheromones in Click Beetles Agriotes lineatus L and A. ustulatus L. Khemoretseptsiya nasekomykh, vilnius, 8, pp. 52e57 (in Russian). Yatsynin, V.G., Rubanova, E.V., Okhrimenko, N.V., 1996. Identification of female-produced sex pheromones and their geographical differences in pheromone gland extract composition from click beetles (Col., Elateridae). J. Appl. Entomol. 120, 463e466. Yoshida, M., 1961. Ecological and physiological researches on the wireworm Melanotus caudex Lewis. Fac. Agr. Shizuoka Univ. Spec. Rept. 1. Zacharuk, R.Y., 1958. Note on two forms of Hypolithus bicolor Esch. (Coleoptera: Elateridae). Can. Entomol. 90, 567e568. Zacharuk, R.Y., 1962a. Distribution, habits, and development of Ctenicera destructor (Brown) in Western Canada, with notes on the related species C. aeripennis (Kby) (Coleoptera: Elateridae). Can. J. Zool. 40, 539e552. Zacharuk, R.Y., 1962b. Seasonal behaviour of larvae of Ctenicera spp. and other wireworms (Coleoptera: Elateridae), in relation to temperature, moisture, food, and gravity. Can. J. Zool. 40, 697e718. Zacharuk, R.Y., 1963. Comparative food preferences of soil-, sand-, and wood-inhabiting wireworms (Coleoptera, Elateridae). Bull. Entomol. Res. 54, 161e165. Zacharuk, R.Y., Tinline, R.D., 1968. Pathogenicity of Metarrhizium anisopliae, and other fungi to five elaterid (Coleoptera) in Saskatchewan. J. Invertebr. Pathol. 12, 294e309. Zhang, S., Liu, Y., Shu, J., Zhang, W., Zhang, Y., Wang, H., 2019. DNA barcoding identification and genetic diversity of bamboo shoot wireworms (Coleoptera: Elateridae) in South China. J. Asia Pac. Entomol. 22, 140e150. Zhao, J., Yu, Y., 2010. Overview of researches of wireworm in China. J. Agric. Sci. 3 (abstract only). Zhou, Y., Bai, H., Shu, J., 2008. Study on biological characteristics of Melanotus cribricollis. J. Zhejiang Forest. Sci. Tech. 4 (abstract only).

Chapter 8

Potato tuberworm* Silvia I. Rondona and Yulin Gaob, c a

Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon Integrated Pest Management Center, Oregon

State University, Corvallis, OR, United States; bState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, China; cNational Center of Excellence for Tuber and Root Crops Research, Chinese Academy of Agricultural Science, Beijing, China

Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae), known as the potato tuberworm, potato tuber moth, or tobacco splitworm, is a cosmopolitan pest of Solanaceous crops including potato (Solanum tuberosum L.), tomato (Lycopersicon esculentum Mill.), tobacco (Nicotana tabacum L.), eggplant (Solanum melongena L.), bell pepper (Capsium annuum L.), cape gooseberry (Physalis peruviana L.), aubergine (S. melongena L.), and sugar beet (Beta vulgaris L.). It can also be found feeding on members of the family Chenopodiaceae (Graft, 1917; Balachowsky and Real, 1966; Rondon, 2010). Other international common names of this pest include Teigne de la pomme de terre (French), Polilla de la papa (Spanish), and Kartoffelmotte (German). Rondon (2020) described the history of P. operculella and the potato crop establishing the potential link between pest and crop. This insect causes damage in both field and storage (Westedt et al., 1998). In the field, adults oviposit in leaves, stems, and tubers preferring foliage versus tubers; after hatching, larva mines leaves but most importantly, burrows into tubers (Trivedi and Rajagopal, 1992; Ferro and Boiteau, 1993; Coll et al., 2000; Sporleder et al., 2008) (Fig. 8.1). If previously infested tubers are moved into storage or storerooms, damage further increases. In general, pest management practices, especially cultural, biological, and chemical controls are effective in controlling P. operculella (Rondon, 2010). Although this chapter will focus on current information related to P. operculella, other tuberworms will be briefly introduced.

8.1 Taxonomy of P. operculella and other “tuberworms” This insect belongs to the Phylum Arthopod, Class Insecta, Order Lepidoptera, Sub-Order Glossata, Super Family Gelechioidea, Family Gelechiidae, Sub-Family Gelechiinae (Rondon and Gao, 2018). In 1873, the genus Phthorimaea was described as Bryotropha and then Gelechia (Zeller, 1873). In the early 1900s, the genus was revised in 1902 and 1931 and assigned to the genus Phthorimaea by Meyrick (1902), Povolny (1964), and Polvolny and Weismann (1958). CABI (2010) lists other synonymous: Gnorimoschema operculella, Lita operculella, Lita solanella, P. solanella, P. terrella, and more recently, Scrobipalpa operculella, S. solanivora, and S. solanivora. Two other species of Gelechiidae moths are known as “tuber worms”: Tecia solanivora (Povolny), restricted to Central and Northwest South America known as the Central American potato tuberworm or Guatemalan potato moth (EspinelCorreal et al., 2010), and Symmestrischema plaesiosema (Turner), found in South America, Southeast Australia, and Philippines (Barragan, 2005; Rondon and Gao, 2018). Tecia solanivora was first described from Costa Rica in 1973 and since then it has spread through Central America, and northern South America probably through trade of seed potatoes; this insect can be found in Mexico and the Canary Islands, and most recently in Spain, where it is under official quarantine in Galicia and Asturias (EFSA, 2018; Schrader et al., 2019). Polvony (1967) described the genus Gnorimoschema plaesiosema (melanophinta Meyrick, tuberosella Busck) as S. capsicum reported in Lambayeque Perú (Galves and Villa, 1987). Tuta absoluta is also a serious pest found in tomatoes in Europe, Africa, western Asia, South and Central America,

* This chapter is an updated version of Rondon, S.I., Gao, Y., 2018. The journey of the potato tuberworm around the world. In: Perveen, K., (Ed.) Moths: Pests of Potato, Maize and Sugar Beet. InTech Open, London, UK, pp. 17e52. Reproduced with the permission of the publisher. Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00008-1 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIGURE 8.1 Phthorimaea operculella larva. Photo credit: OSU Extension Ketchum.

and can sometimes be taxonomically confused with P. operculella (Urbaneja et al., 2007). This pest has not been found in North America yet. Tuta absoluta damages tomato plants by mining the leaves and boring into apical and flower buds and fruit. When feeding on leaves, the larvae make irregularly shaped mines that increase in size as the larva grows, eventually killing entire plants (Urbaneja et al., 2007).

8.2 Phthorimaea operculella distribution around the world There are few studies describing the population structure of P. operculella around the world that could explain P. operculella distribution. In the USA, Medina et al. (2010) suggested that geographical barriers such as the Appalachian Mountains in North America might isolate P. operculella subpopulations (e.g., western, central, eastern). Phthorimaea operculella has increased its distribution range with increasing climate variations that is causing in many areas warmer winters. Traditionally a pest in tropical areas, it is also colonizing subtropical areas (Sporleder et al., 2004). The International Potato Center (CIP, acronym in Spanish) has compiled a list of countries with confirmed reports of presence and/ or damage caused by P. operculella (https://cipotato.org/riskatlasforafrica/phthorimaea-operculella/). Reports suggest that P. operculella originated in the topical regions of South America along with its main host, potatoes, although nowadays it has become a pest with worldwide distribution reported in over 90 countries (Rondon, 2010). Currently, P. operculella can be found in all potato production areas in South, Central, and North America, Africa, Australia, and Asia (Mitchell, 1978; Flint, 1986; Rothschild, 1986; Fuglie et al., 1992; Kroschel and Koch, 1994; Visser, 2004; Rondon, 2010; Rondon and Gao, 2018).

8.2.1 America Phthorimaea operculella was first reported affecting potatoes in South America in the early 1900’s (Graft, 1917). In 1913, P. operculella was reported in the USA (Chittenden, 1913; Radcliffe, 1982; Jensen et al., 2005; Rondon, 2010). In the USA, CIP currently reports P. operculella in Alabama, Arizona, California, Colorado, Delaware, Washington, DC, Florida, Georgia, Hawaii, Idaho, Illinois, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maryland, Massachusetts, Michigan, Minnesota, Mississippi, Missouri, Nebraska, Nevada, New Jersey, New Mexico, New York, North Carolina, Ohio, Oregon, Pennsylvania, Rhode Island, South Carolina, South Dakota, Tennessee, Texas, Utah, Virginia, Washington, and Wisconsin. In Central and South America, this insect is present in Antigua and Barbuda, Argentina, Bermuda, Bolivia, Brazil, Chile, Colombia, Costa Rica, Cuba, Dominican Republic, Ecuador, Haiti, Jamaica, Mexico, Paraguay, Peru, Puerto Rico, St. Vincent, Grenadines, Uruguay, and Venezuela.

8.2.2 Asia and Australasia P. operculella is present in Tasmania, New Zealand, and Australia (Berthon, 1855). In South Central Asia, P. operculella was introduced in 1906 to Bombay, India, apparently from Italy (Lefroy, 1907); by the mid-1900’s, P. operculella became widely distributed in all potato regions in India. The first report in China took place in 1937 when P. operculella larvae was found in tobacco plants in the Liuzhou City in Guangxi province (Xu, 1985; Hu, 2008). Phthorimaea operculella has also

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be found in Bangladesh, China, Georgia, India, Indonesia, Iran, Iraq (1970), Israel, Japan, Jordan, Korea Republic, Lebanon, Myanmar, Nepal, Oman, Pakistan, Philippines, Saudi Arabia, Sri Lanka, Syria, Thailand, Turkey, Vietnam, Yemen (Al-Ali et al., 1975; Whilshire, 1957; Zagulyaev, 1982).

8.2.3 Europe From 2002, P. operculella has emerged as a problem in the Bologna providence in northern Italy (Masetti et al., 2014). Nowadays, it is present in Bulgaria, Croatia, Cyprus, France, Greece, Hungary, Italy, Portugal, Romania, Russia, Serbia, Spain, UK, and Ukraine (CABI, 2021).

8.3 Host range Das and Raman (1994) and Rondon and Gao (2018) reported alternate hosts representing 60 plant species, both cultivated and wild. Most of the main hosts belong to the Solanaceae family, while others belong to the following families: Scrophulariaceae, Boraginaceae, Rosaceae, Typhaceae, Compositae, Amaranthaceae, and Chenopodiaceae; there is only one unverified report of P. operculella in sugar beet (Fenemore, 1980). Interestingly, field studies have shown that P. operculella only reproduce when feeding on potato, tomato, sugar beet, and eggplant (Chittenden, 1913; Morris, 1933; Attia and Mattar, 1939; Cunningham, 1969; Broodryk, 1971a,b; Meisner et al., 1974; Gubbaiah and Thontadarya, 1977; Fenemore, 1980; Das and Raman, 1994; Kroschel, 1995; Rondon et al., 2007; Rondon, 2010). Varela and Bernays (1988) studied the behavior of newly hatched P. operculella larvae in relation to their host plants. Their study concluded that early behavior of first instars is critical for establishing in a suitable host plant, and food source availability and quality are critical in P. operculella establishment and success. Development, survival, and reproductive rates vary considerably in relationship to host quality and availability (Trivedi and Rajagopal, 1992; Rondon, 2010).

8.4 Life cycle Phthorimaea operculella has four life stages: adult, egg, larva, and pupa. Number of days between instars depends on several factors, including temperature, humidity, altitude, and rainfall.

8.4.1 Adults Adults are small moths that are approximately 0.9 cm long with a wingspan of approximately 1.3 cm. Forewings have two to three dark dots on males, while females show an “X”-shaped dark pattern (Fig. 8.2). Both pairs of wings have characteristic fringed edges (Raman, 1980; Chauhan and Verma, 1991; Rondon et al., 2007; Rondon, 2010; Rondon and Xue, 2010). Adults are considered poor fliers (Reed, 1971; Foot, 1979; Fenemore, 1988). While they have been shown to fly for over 5 h or up to 10 km nonstop, they cannot fly at wind speeds in excess of ca. 5e6 m/s (Krambias, 1976; Foley, 1985).

FIGURE 8.2 Phthorimaea operculella adult. Photo credit: OSU Extension Ketchum.

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Moths are active at temperatures between 14.4 and 15.5
C; however, at around 11.1
C they can still sneak through soil cracks or tunnel short distances through loose soil to lay their eggs. In Oregon, P. operculella was observed searching for tubers at temperatures close to 5
C (Rondon et al., 2009). Mating can take place only 16e20 h after adult emergence and the duration of copulation ranges between 85 and 200 min (Gubbaiah and Thontadarya, 1977; Chauhan and Verma, 1985; Makee and Saour, 2001). Adults are more active (e.g., flight, mating, egg laying) at night (Attia and Mattar, 1939; Broodryk, 1970, 1971; Traynier, 1975, 1983). Adults do not oviposit in the soil close to tubers if potato foliage is available (Rondon, 2010; Traynier, 1975; Cannon, 1948). According to Gill et al. (2014), adults can live for 1e2 weeks.

8.4.2 Eggs Eggs are 0.1 cm spherical, translucent when freshly laid turning white or yellowish to light brown after 1e2 h. Eggs laid and their longevity is related to the adults’ nutrition choices (Rondon, 2010; Traynier, 1983; Trehan and Bagal, 1944; Labeyrie, 1957). In insects, chemical cues are mainly responsible for host selection; olfactory detection of plant volatiles may elicit the female to find the best host for her offsprings (Van Loon, 2013). Host selection is based on chemical cues that according to Fenemore (1980) are detected only when females enter in contact with the host. Early on, Meisner et al. (1974) showed that oviposition is stimulated by ethanolic extracts and I-glutamic acid released from potato peels. In the field, females lay their eggs on foliage, soil and plant debris, or exposed tubers (Rondon et al., 2007; Rondon, 2010); however, foliage is the preferred oviposition substrate (Varela and Bernays, 1988). Traynier (1975) and Gubbaiah and Thontadarya (1977) indicated that in the field females laid eggs singly and rarely in groups of three to five eggs on either side of the leaf but close to the midrib and near the base of the plant; in contrast, in the storage (w7.2
C), eggs were laid singly or in groups of 3e15 near the eye buds (Al-Ali et al., 1975; Gill et al., 2014; Langford and Cory, 1934; Ascerno, 1991; Rondon et al., 2009). Average incubation period could range from 7 to 15 days depending on temperatures (Van der Goot, 1926; Bartoloni, 1951; Stanev and Kaitazov, 1962; Verma, 1967; Al-Ali et al., 1975; Trivedi and Rajagopal, 1992). Attia and Mattar (1939) reported 36
C as the upper critical temperature at which no eggs were laid.

8.4.3 Larvae Larvae are usually cream to light brown reddish with a characteristic brown head. Mature larvae (0.9 cm long) may have a pink or greenish color and thorax has small black points and bristles on each segment (Gill et al., 2014). No sexual dimorphism is observed until the third larval stage when initial sexual structures become visible; in the fourth larval stage, males are different from females where males have two elongated yellowish testes in the fifth and sixth abdominal segment (Chauhan and Verma, 1991). Moregan and Crumb (1914) reported 15e17 days for the larval period while Graft (1917) and Trivedi and Rajagopal (1992) reported 13e33 days, and Van der Goot (1926) 14 days. Larvae feed on leaves throughout the canopy but prefer the upper foliage; larvae mine the leaves, leaving the epidermal areas on the mid/lower leaf surface uninterrupted (Rondon, 2010). Larvae move through cracks in the soil to find tubers; thus, exposed tubers are predisposed to P. operculella damage (Rondon, 2010; Rondon et al., 2007). Close to pupation, larvae drop to the ground and burrow into the tuber to complete its life cycle making a swirl silk cocoon pupating on soil surface or in debris (Fig. 8.4). Especially in warm dry climates, larva can attack potato plants in field and storage causing great damage (Langford and Cory, 1934; Stanev and Kaitazov, 1962).

8.4.4 Pupae Occasionally, P. operculella pupae can be found on the surface of tubers, most commonly associated with tuber eyes (Rondon et al., 2007). Phthorimaea operculella pupae (0.8 cm long) are smooth and brown and often enclosed in a covering of fine residue (“cocoon”) that protects them from low temperatures and help them endure the winter (Dŏgramaci et al., 2008). There is a clear distinction between male and female pupae. Rondon and Xue (2010) evaluated the “scar” and the “width” method. Using the “scar” method, males could be recognized by the distance between the incision located between the eighth-ninth abdominal segment and the tip of the abdomen; “width” focus on the larger end of the abdomen on females (Fig. 8.3). Age of tuberworm pupae can be identified by the gradual change in color eye pigmentation. Accordingly, they are classified into newly formed pupa (yellowish in color, 1e2 day old pupae), early red (3 day old), middle red (4 day old), late red to black eye pupa (5e6 day old) (Chauhan and Verma, 1985, 1991; Rondon and Xue, 2010; Summers et al., 1982). Some studies suggest that the pupal period depends on the temperature at which the larvae grew (Whiteside, 1985). Pupal period could range from 6 to 9 days (Moregan and Crumb, 1914), 13e33 days (Graft, 1917), or 14e17 days (Van der

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FIGURE 8.3 Pupa. Left, male (long slit); right, female (short, slit). Photo credit: OSU-Extension Ketchum.

FIGURE 8.4 Phthorimaea operculella “coccons” near tuber eyes. Photo credit: OSU Extension- Rondon.

Goot, 1926) at 31, 28, and 26
C, respectively. Studies in the western USA indicated that P. operculella adults could potentially emerge from soil at depths up to 10 cm (Dŏgramaci et al., 2008). Once adults emerge, mating occurs, and within a few hours, females seek a potential host where to lay their eggs.

8.5 Life table Phthorimaea operculella can complete several generations per year. Chittenden (1912) reported two generations of P. operculella in summer and a third generation in storage in the USA. Van der Goot (1926) reported six to eight generations a year in tropical regions. French (1915) reported two generations in Australia, with one in the winter and a second one on stored tubers. Graft (1917), Trivedi and Rajagopal (1992), and Sporleder et al. (2004) reported three-four generations in Chile and the southern USA; Mukherjee (1949) 13 generations per year in India; and Al-Ali et al. (1975) 12 generations in Iraq. Recently, pheromone trapping in Bologna Italy, where researchers integrated temperature dependent developmental time models, showed that P. operculella completed two generations throughout the potato-growing season; the remaining generations developed in the noncrop season (Masetti et al., 2014). This information suggests a correlation between the number of P. operculella generations per year and geographical location, and/or presence or absence of a food source (Rondon, 2010). Sporleder et al. (2008) indicated that locations with one crop per season will have two-three generations per year (e.g., western USA) while locations with year-round crops like in India, will have several generations per year (Mukherjee, 1949).

8.6 Damage in the field Luscious, healthy, disease free plants attract more P. operculella than wilting, nonirrigated plants (Yathom, 1968). Once P. operculella reaches a field, distribution of foliar damage tends to be nonrandom (Foot, 1974a,b, 1976a,b, 1979) and

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more severe on the edges of the field facing the prevailing winds in a band parallel to the edge (Foot, 1979). Larval density in foliage and tubers is higher at the margins of the field than in the center (Coll et al., 2000), a typical characteristic of pests that move from nearby areas (Reed, 1971; Foot, 1979; Gilboa and Podoler, 1995). Drier conditions in plants on field edges caused by wind and solar radiation lead to more P. operculella (Meisner, 1969; Meisner et al., 1974; Gilboa and Podoler, 1995; Coll et al., 2000). Research shows that moths are able to forage beyond 100e250 m from the place of eclosion (Cameron et al., 2002). In the western USA, most of the potatoes are vine-killed right before harvest. As a result, when foliage is gone, P. operculella readily moves to nearby green fields or directly down to the tubers (Chen, 1937; Rondon et al., 2007; Rondon and Hervé, 2017). Foliar damage does not usually result in significant yield losses (Graft, 1917); however, reduced marketability and damage due to tuber infestation can be significant in nonrefrigerated storage conditions (Arnone et al., 1998). All instars of P. operculella can potentially survive in volunteer potatoes or in the soil (Shelton and Wyman, 1980; Rondon et al., 2007; Dŏgramaci et al., 2008; Gill et al., 2014), and have high adaptability to low temperatures, cooling rate, and heat stress (Hemmati et al., 2014).

8.7 Damage from field to storage Generally speaking, P. operculella is not a problem in the USA under controlled conditions since all potatoes are refrigerated at 7.2
C (Rondon, 2010); in the field, yield loss has been reported only in outbreak years (Dŏgramaci et al., 2008). In 2006, several potato storage controlled units were visited (n ¼ 50) and only one had severe P. operculella infestation where the infested unit stored tubers that came heavily infested from the field. That was the first time in more than 70 years that P. operculella was reported in the states of Oregon and Washington (Rondon, unpublished data). In the Middle East, P. operculella field infestation can range between 1% and 65% (Fadli et al., 1974; Al-Ali et al., 1975) while in India, P. operculella is responsible for about 1%e13% and 70%e100% yield loss in the field and storage, respectively (Lall, 1949; Nirula, 1960; Nirula and Kumar, 1964; Gubbaiah and Thontadarya, 1977; Chauhan and Verma, 1991). In Ethiopia, P. operculella is responsible for 9%e42% yield loss (Abewoy, 2017); Lagnaoui et al. (2000) indicated that yield loss in storage could be up to 100% where no temperature and/or humidity control is possible. Yield loss due to P. operculella damage fluctuates depending on many factors like intensity of infestation the previous year, uncontrolled early versus late infestations, field versus storage, etc (DeBano et al., 2010).

8.8 Developmental thresholds and temperatures The developmental response of insects to temperature is important in understanding the ecology of their life histories, geographical distributions, population dynamics, and management (Régnière et al., 2012). For instance, Langford and Cory (1934) indicated that low temperatures retard and cause temporary cessation of P. operculella development not only physiologically but also due to the destructive effect of low temperatures on the food supply. Phthorimaea operculella developmental threshold has been widely studied (Chauhan and Verma, 1991; Attia and Mattar, 1939; Broodryk, 1970; Sporleder et al., 2004, 2008; Davoud et al., 1999; DeBano et al., 2010). Developmental thresholds are necessary in order to establish the best timing of control (Ascerno, 1991; Sporleder et al., 2004; Legg et al., 2000). Differences in temperature for P. operculella development suggest the remarkable adaptation of this insect (Attia and Mattar, 1939; Broodryk, 1971a,b; Davoud et al., 1999; Sporleder et al., 2004; Dŏgramaci et al., 2008; Rondon, 2010). Temperature dependent development can be useful in forecasting occurrence and population dynamics of pests. Golizadeh and Zalucki (2012) determined that the lower temperature threshold and thermal constant of immature stage were estimated to be 11.6
C and 339 degree-days. A degree-day is a measurement of heat units over time, calculated from daily maximum and minimum temperatures; where the minimum temperature at which insects’ first start to develop is called the “lower developmental threshold,” or baseline and the maximum temperature at which insects stop developing is called the “upper developmental threshold” or cutoff (Herms, 2004). Langford and Cory (1932, 1934) and Golizadeh et al. (2012), determined the average fecundity of females ranging from 45.3 eggs (at 16
C) to 117.3 eggs (at 28
C); net reproductive rate (R 0) ranged from 12.8 (at 16
C) to 43.2 (at 28
C), mean generation time (T) decreased with increasing temperatures from 61.0 days (at 16
C) to 16.2 days (at 32
C). In addition, eggs exposed to 1.6e4.4
C for 4 months failed to hatch. Langford and Cory (1934) observed that outbreaks of P. operculella in Virginia in 1925 and 1930 coincided with hot and dry years and the intensity of infestation vary in proportion to rainfall and humidity. Early studies in Maryland and Virginia (Underhill, 1926; Langford, 1934) indicated that P. operculella pupae can survive “short” constant subfreezing temperatures. Several other authors reported that larvae and pupae could potentially survive frost (Langford and Cory 1932; Cory, 1925; Langford, 1933), but other studies indicated that all life stages of P. operculella were killed by exposure

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to 6.6
C for 24 h (Langford and Cory, 1932, 1934). Early studies by Langford in 1934 reported that P. operculella survived temperatures ranging from 11.6 to 6.6
C but lengthy exposures to low temperatures were fatal to all stages. Trivedi and Rajagopal (1992) found that pupae were extremely tolerant to low temperatures; however, Langford and Cory (1934) and Alvarez et al. (2005) indicated that full-grown larvae survived better at low temperatures. In a manipulative study to determine how growth stage (egg, larva, or pupa), and soil depth affected the potential for winter survival, Dŏgramaci et al. (2008) in eastern Oregon found that egg survival was reduced after 1 month of exposure to low temperatures; larvae were able to survive up to 30 days at 20-cm soil depth, while tubers at the surface, and buried at 6 cm were frozen; the pupal stage showed a greater tolerance to winter conditions (average -2
C) than the egg or larval stages, surviving up to 91 days of exposure. Hemmati et al. (2014) studied the effect of cold acclimation. According to their study, super cooling points from first and fifth instar larvae, prepupae and pupae were 21.8, 16.9 18.9, and 18.0
C, respectively. Cold acclimation (1week at 0 and 5
C) did not affect super cooling for 4e5th instar larvae, prepupae and pupae. Also, LT50s (lower lethal temperature to cause 50% mortality) for first and fifth instar larvae, prepupae and pupae were 15.5, 12.4, 17.9 and 16.0
C, respectively. They concluded that cold acclimation resulted in a significant decrease in mortality of all developmental stages and heat hardening also affects cold tolerance. A relatively recent study by Golizadeh et al. (2012) determined that tubeworm failed to survive at 36
C during the egg period and that adult longevity was negatively correlated with temperature, being the longest at 16
C. Golizadeth et al. (2014) then established life tables using leaves and tubers of different cultivars recording some differences. Other parameters, such as elevations and latitude, play a role in P. operculella incidence (DeBano et al., 2010). Locations with higher spring, summer, or fall temperatures were associated with increased trapping rates in most seasons. In the western USA, trapping data from spring 2004 to fall 2005 showed that P. operculella males were present every week except in midJanuary, with the greatest numbers of P. operculella per trap occurring in December at around 0.09
C (Rondon et al., 2007, 2008; DeBano et al., 2010). In addition, “warm” winters may also account for high P. operculella populations in the following season (Rondon, 2010; DeBano et al., 2010). Similar observations were recorded in other insect species (Rondon and Murphy, 2016; Klein et al., 2017). In Israel, P. operculella first generation reached its peak in May or June (late spring, early summer) (Coll et al., 2000), and overlapping generations reached high numbers close to harvest which seems to be a characteristic of nondiapausing insects that continuously have access to host plants (Coll et al., 2000; Povolny, 1964; Whiteside, 1985; Sporleder et al., 2004; Yathom, 1968, 1986; Broodryk, 1969, 1971).

8.9 Monitoring Phthorimaea operculella 8.9.1 Pheromones Phthorimaea operculella male moths are attracted to pheromones, which are concentrated chemicals of the female “scent” impregnated in a rubber septum in the center of a sticky liner placed in delta traps (Rondon, 2010). According to Herman et al. (2005), two chemicals have been identified as the main component of P. operculella sex pheromone: (E4, Z7)tridecadienyl acetate (PTM1) (Roelofs et al., 1975), and (E4, Z7, Z10)-tridecatrienyl acetate (PTM2) (Persoons et al., 1976). These compounds; chemicals have been synthesized, blended, tested, and are commercially used (Voerman and Rothschild, 1978; Raman, 1988). Some other insects, including different species of Gelechiidae moths, could be trapped in the sticky liners. Thus, the liners should be changed once a week, and lures should be changed once a month (Rondon et al., 2007). He et al. (2021) studied the mechanism used by males to recognize sex pheromone components by cloning two pheromone receptor genes PopeOR1 and PopeOR3 in P. operculella. They found that the transcripts were highly accumulated in the antennae of male adults. They demostrated that those two PR proteins responded to (E, Z)-4,7e13: OAc and (E, Z, Z)-4,7,10e13: OAc, the key sex pheromone components of P. operculella. From the practical perspective, pheromone traps are used to monitor populations in the field to help timely control measures (Herman et al., 2005). Several authors found a positive relationship between the number of trapped adults and the density of larvae in the foliage and tuber (Shelton and Wyman, 1979a,b, 1980; Lall, 1989). Larrain et al. (2009) carried out a field experiment in Valle del Elqui, Coquimbo Region Chile to evaluate the effectiveness of different pheromone trap densities, which included 10, 20, and 40 traps ha1 baited with 0.2 mg of commercial pheromone. Results of this experiment indicated that higher numbers of P. operculella male adults were correlated with higher number of traps/ha causing significant reduction in number of months and tuber damage. In the USA, growers in areas impacted by P. operculella are encouraged to monitor insect using pheromone traps. In eastern Oregon, current “live” trapping program data can be found at https://agpass.maps.arcgis.com/apps/webappviewer/index.html?id¼8f3577c883ab4ac58f262b4c d04ff569.

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8.9.2 Trapping Horne (1993) indicated that random sampling of leaves did not always give adequate estimates, as particular life stages could be overestimated or excluded from samples. Rondon et al. (2007) recommended sampling at least 10 plants per field or section of the field; individual plants should be examined for the presence or absence of P. operculella. Rondon et al. indicated that near 55% of the mines are found in the upper third of the potato plants but they are not easily to find. Therefore, they recommended adding at least one pheromone trap per 123 acres. Kennedy (1975), Bacon et al. (1976), Raman (1988), Salas et al. (1991), and Tamhankar and Hawalkar (1994) have reported results using different type of traps. In New Zealand, Herman et al. (2005) tested water traps, which caught the greatest number of P. operculella per trap as compared to “DeSIRe” delta shaped sticky traps, “A traps” (cylinder-shaped), and funnel traps. Herman et al. (2005) concluded that delta traps were the most suitable for commercial use. Coll et al. (2000) presented information regarding pheromone traps plus poison bait placed on the ground at 50 m intervals in single rows with positive results. Based on Herman et al. (2005) findings, the recommendation in the western USA has been to place at least one delta trap per potato field, beginning after canopy closure (Rondon et al., 2007). Recent recommendations include placing four traps per field (Rondon, 2010). Soil type has an effect on number of moths caught per trap; thus, in sandy soils pheromone traps caught almost twice as many moths than in loess fields (Coll et al., 2000). California recommends a capture of 15e20 moths per trap per night as a general threshold level (University-California, 2006) and 8 moths per trap per night for eastern Oregon (Rondon and Hervé, 2017). Since P. operculella numbers vary from field to field and from area to area, it is recommended to tailored management recommendations on field(s) specific information (Chen, 1937; Rondon et al., 2007); standard thresholds should be used exclusively as a reference.

8.10 Integrated pest management of P. operculella Key aspects of the biology and ecology of P. operculella are important in selecting management practices to control this pest (Keller, 2003; Rondon, 2010; Rondon and Hervé, 2017). Rondon (2020) indicated that well-defined pest management programs should be based on prevention and monitoring. Considering that most of the economic damage by this insect occurs when it infests the tubers, focus should be close to harvest (Rondon, 2010). For instance, deeper seed planting, hilling the rows, irrigation, and early harvest are a few of the methods suggested to prevent tuber infestation (Shelton and Wyman, 1979a,b; Langford and Cory, 1932; Langford, 1933; Rondon and Hervé, 2017; Clough et al., 2010). The use of chemicals is still the main foundation of P. operculella control worldwide (Rondon and Hervé, 2017; Shorey et al., 1967; Bacon et al., 1972; Hofmaster and Waterfield, 1972). It is advisable to check with local extension or government agencies to review which pesticides are allowed to use in your region. It is also always essential to read the labels and follow the manufacturers’ recommendations.

8.10.1 Cultural control Cultural methods reported to reduce P. operculella population include the elimination of cull piles and volunteers, the manipulation of timing of vine-kill, soil moisture at and after vine-kill, the selection of proper timing between desiccation and harvest, optimizing rolling and covering of the hills, and cultivar selection (Rondon et al., 2007; Rondon and Hervé, 2017; Clough et al., 2010). In Tunisia, recommended practices included deep seeding, hilling up, early harvest, irrigation until harvest, good sorting of tubers at harvest and rapid harvesting prevent tuber infestation (von Arx, 1987; BenSalah and Aalbu, 1992). In Sudan, planting date, planting depth, hilling-up, irrigation intervals and mulching on insect infestation and on the greening of tubers in the field were studied (Ali, 1993). Ali (1993) indicated that tuber shape and skin characteristics had no effect on the degree of P. operculella infestation; early planting date resulted in fewer insect damage and greater yield compared with crops planted 3 weeks later; greater depth of planting and more frequent hilling significantly lowered infestation levels; light irrigation every 4 days and mulching with neem (Azadirachta indica L.) incorporated before harvest were the most effective treatments.

8.10.1.1 Elimination of volunteer potatoes and cull piles The growth of volunteer potatoes is a serious problem not only because of the competition with current season crops but also for sanitary reasons (Rahman, 1980). For instance, Aarts and Sijtsma (1978) indicated that volunteer potatoes can overgrow crops such as maize or sugar beets at planting. In South Africa, P. operculella is described as a significant pest before harvest and during storage; and since eggs, larvae, or pupae can survive on volunteer potatoes, they represent a source of infestation for the following season (Watmough et al., 1973; Allemann and Allemann, 2013) Besides volunteer

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potato elimination, cull piles should be removed to reduce overwintering stages which are a source of next years’ populations (Shelton and Wyman, 1980). Certainly, in western USA states, volunteer potatoes can serve as a “green bridge” for numerous insect pests.

8.10.1.2 Rolling potatoes Research has found that rolling of potato hills in sandy soil caused soil to slough off the hill, which resulted in increased P. operculella damage; obviously, this is not recommended in areas with sandy soils (Rondon et al., 2007; Clough et al., 2010). Covering hills with 3e5 cm of soil immediately after vine-kill, which can be accomplished with a rotary corrigator, has been shown to significantly reduce tuber infestation (Rondon et al., 2007; Clough et al., 2008, 2010); however it is not a common practice in the region. Others have shown that exposed tubers are more prone to P. operculella infestation (Foot, 1979; von Arx et al., 1987). He indicated that tuber infestation occurred 2e4 weeks before harvest and all infested tubers were covered with no more than 3 cm of soil (Clough et al., 2010).

8.10.1.3 Vine killing Tubers naturally mature as the potato plant senescens, but tuber maturation can be artificially induced by killing the potato vines mechanically, chemically, or with a combination of both (Rondon, 2010). Empirical observations suggest that all these activities have an impact on the level of P. operculella infestation (Rondon, 2010). Field observations support the principle that P. operculella prefer green foliage to tubers for oviposition and feeding. Thus, when foliage starts to decline, tubers are exposed, and infestations naturally increase. As a result, the time between desiccation and harvest is crucial. The longer tubers are left in the field after desiccation, the greater is the likelihood of tuber infestation (Rondon, 2010; Rondon et al., 2007; Chen, 1937). Intuitively, tubers exposed or close to the soil surface, are at high risk for P. operculella injury. In the Columbia Basin of Oregon, our recommendation includes to maintain more than 5 cm of soil over the tubers especially at the end of the season or after vine-killed (Rondon et al., 2007).

8.10.1.4 Soil moisture Phthorimaea operculela female moths favor dry soil for oviposition (Meisner et al., 1969, 1974). Larval survivorship increased with decreasing soil moisture (Meisner et al., 1969). Consequently, keeping the soil moist to avoid cracks in the soil, particularly at the end of the season when vines are drying, reduces P. operculella tuber infestation. Rondon et al. (2007), Clough et al. (2008), and Rondon and Hèrve (2017) research has shown that irrigating daily with 0.25 cm through a center pivot irrigation system from vine kill until harvest decreased P. operculella tuber damage without increase fungal or bacterial diseases. Since water closes soil cracks, reducing tuber access, P. operculella possibly perish from lack of oxygen in the soil due to water saturation, and/or their mobility is reduced by wet soil decreasing their ability to move and find a tuber.

8.10.2 Biological control The tuberworm complex is a relatively minor pest of potatoes in South America, probably due to the existence of a diverse array of natural enemies attacking this pest (Lloyd, 1972). Biological control, which is the use of living organisms to control pest populations, is considered to be a safer alternative to chemical control. However, it can also have an environmental impact while controlling pest populations (Howarth, 1991) worldwide (Cruickshank and Ahmed, 1973). There are several organisms including parasitoids, and pathogens such as fungi or viruses, that have been used successfully to control P. operculella. Some examples listed below.

8.10.2.1 Parasitoids In general, Callan (1974) and others have indicated that the “newcomers” normally achieved better control than the “‘native” natural enemies, possibly caused by the long-term coevolution or adaptation between the relevant species at different trophic levels in South America. Thus, exploration for more parasitoids in the large parts of South America, Central America, and Mexico could be a promising way to improve the parasitoid based biocontrol elsewhere. Many parasitoids have been introduced mainly from South America, the area for the origin of P. operculella (Watmough et al., 1973; Meabed et al., 2011). In 1918, biological control efforts attempted to introduce Bracon gelichiae L. to France from the Americas (CABI, 2010). Trichogramma and Copidosoma species are among the most widely used parasitoids used to control P. operculella

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but with mixed results (Broodryk, 1969, 1971; Harwalkar et al., 1987; Baggen and Gurr, 1998; Morales et al., 2007; Mandour et al., 2008). Copidosoma koehleri Blanchard and Bracon gelechiae Ashmead have been used successfully in South America and Australia, respectively (Alvarez et al., 2005). However, in Israel C. koehleri, an encyrtid polyembrionic wasp did not reduce P. operculella populations, accounting only for 4%e5% decline in larval numbers. Similar results were found by Berlinger and Lebiush-Mordechi (Berlinger, 1992; Berlinger and Lebiush-Mordechi, 1997) in Israel. In Italy, Pucci et al. (2003) also observed only modest level of control. While several biotic and abiotic conditions in the eco-niche determine the population establishment and effectiveness of parasitoids (Briese, 1986), the decrease in human interference through reducing insecticide use is crucial for the parasitoid(s) establishment and performance (Watmough et al., 1973). Availability of alternative resources, such as nectar produced by flowering plants, is also important for parasitoid establishment (Baggen and Gurr, 1998). In a laboratory study, when C. koehleri females were deprived of hosts for the first 5 days of their adult lives, neither the number of eggs laid nor longevity were significant affected (Baggen and Gurr, 1998). Kfir (1981, 2003) studied the fertility of C. koheleri compared to Apanteles subandinus L. under the effect of humidity in South Africa, concluding that low humidity is detrimental for the survivorship of this species. Choi et al. (2013) and Aryal and Jung (2015) reported that Diadegma fenestrale L. was found for the first time in Korea and accounted for 20%e30% parasitism. In Sardinia, Diadegma turcator Aubert, Bracon nigricans L., B. properhebetor L., and Apanteles spp. were also found attacking P. operculella. Labeyrie (1959), Rao and Nagaraja (1968), Leong and Oatman (1968); Divakar and Pawar (1979); Ortu and Flores (1989); Odebiyi and Oatman (1972); Lloyd and Guido (1963), Franzmann (1980), Choudhary et al. (1983), Powers and Oatman (1984), Flanders and Oatman (1982, 1987), Keasar and Steinberg (2008), and Rondon and Gao (2018) studied and reported several additional species of biological control agents like Campoplex haywardi, Chelonus contratus, or Chelonus kellieae and Chelonus phthorimaeae.

8.10.2.2 Predators The potential role of generalist predators often present in potato ecosystems, such as Orius spp. (Zaki, 1989), several species of Hymenoptera (Montllor et al., 1991), Dicranolaius spp. (Horne, 2000), phytoseiid mites (El-Sawi and Momen, 2005), Chrysoperla spp. (Abd El-Gawad et al., 2010), Agistemus (Momen et al., 2006) and a few others have been acknowledged, but not widely studied (Coll et al., 2000). Geocoris sp. (Hemiptera: Miridae) was also seen as a potential P. operculella predator in Nepal (NARC, 1995).

8.10.2.3 Nematodes Other potential biological control agents include nematodes and entomopathogens. The nematode of the genus Hexamermis, Steinernema, and Heterorhaboditis are suggested to exert significant control on P. operculella (Rusniarsyah et al., 2015; Salam et al., 1995). Steinernema feltiae, S. bibionis, S. carpocapsae and Heterorhabditis heliothidis were used in laboratory experiments in Russia with promising results (Ivanova et al., 1994). Kakhki et al. (Kakhki et al., 2013) found that the higher the concentration (0, 75, 150, 250, 375, and 500 js/mL) of S. carpocapsae and H. bacteriophora, the higher mortality in both larval and prepupal stages.

8.10.2.4 Pathogens Fungal entomopathogens such as Beauveria bassiana and Metarhizium anisopliae, have been isolated from P. operculella larvae, extracted, and used as bio-insecticides causing P. operculella death at a rate higher than 80% (Yuan et al., 2009, 2017, 2018; Gao, 2018; Sewify et al., 2000). Back in 1967, a granulovirus was found and reported as a new record (Steinhaus and Marsh, 1967); the following years the granulovirus was isolated and collectively named Phthorimaea operculella granulovirus (PhopGNV). They are well known for efficiently controlling and preventing P. operculella in storage (Espinel-Correal et al., 2010). Since first reported, GNV has been tested for pest control in the fields in South America and Australia (Espinel-Correal et al., 2010). Arthurs et al. (2008) evaluated PoGV and Bacillus thuringiensis subsp kurstaki for control of P. operculella in stored tubers with limited efficacy.

8.10.3 Chemical control Traditional chemical control targeting mainly larvae and adults is well documented (Bacon, 1960; Foot, 1976c). Back in the 1970’s, azinphos ethyl and endosulfan were effective against foliage mining (Foot, 1974a). Others reported good results using thiacloprid, quinalphos, and difluvenzuron (Chandramonhan and Nanjan, 1993; Saour, 2008). Rondon et al. (2007) provided more recent information related to pesticide use in the USA. However, potential strategies to improve

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chemical control are also being investigated. Mahdavi et al. (2017) studied the insecticidal activity of plant essential oils including the insecticidal and residual effects of nanofiber oil and pure essential oil of Cinnamomum zeylanicum L. under laboratory conditions; fumigant toxicity was evaluated on different growth stages (egg, male and female adults) of P. operculella with encouraging results. Similarly, Mahdavi et al. (2018) tested Zingiber officinalle Roscoe demonstrating the relative effectiveness of additional means of control. Tanaskovic et al. (2016) revised the effect of several plants as bioinsecticides to suppress P. operculella.

8.10.4 Control in storage In the USA, P. operculella is not a problem during storage since storage occurs under controlled conditions of temperature and humidity (Rondon, 2010). However, in other parts of the world, P. operculella can cause significant damage during storage. Moawad and Ami (2007) and Abewoy (2017) reported that P. operculella causes serious damage to stored potato through its larval tunneling and feeding which can lead to secondary infection by fungi or bacteria. During storage, the damaged tubers become unsuitable for human consumption, moreover, the adult moth flies from the infested tubers in the storage and from neglected warehouses or farms back to the fields where it causes preharvest infestation. Granulovirus was found to efficiently control P. operculella in Colombia and was used as a biopesticide in storage conditions [205]. Early on, Raman and Booth (1984), Raman et al. (1987), and Lal (1987,1988) indicated that P. operculella could be reduced by covering tubers with Lantana camara L., L. aculeate L. or Eucalyptus globulus Labill foliage. Niroula and Vaidya (2004) reported good control using Minthostahys spp., Baccharis spp., L. neesiana and Artemisi calamus L.; Sharaby et al. (Sharaby et al., 2009) tested peppermint oils, camphor, eugenol, and camphene in Egypt.

8.10.5 Plant resistance Host plant resistance enables plants to avoid, tolerate, or recover from pest infestations (Tingey, 1986; Panda and Khush, 1995). Genome diversity of tuber-bearing potato presents a complex evolutionary history that complicates domestication in the cultivated potato (Hardigan et al., 2017). Currently, plant resistance is extensively used in other insect-plant interactions systems, especially utilizing defensive plant chemicals. In contrast, the amount of information to improve potato genotypes against P. operculella in still lacking (Horgan et al., 2013). Cultivated potatoes have more than 100 tuber-bearing relatives native to the Andes of southern Peru; among them, Solanum chiquidenum L. and Solanum sandemanii L. for instance, which are highly resistant to P. operculella damage in tubers (Horgan et al., 2007). The nutritional value of the host is an important resistance factor limiting normal growth and development of P. operculella (Das et al., 1993). Moreover, some potato hybrids can inhibit oviposition, while surviving larvae have been shown to have higher mortality and slower feeding rates than those larvae reared on foliage of cultivated potatoes (Malakar and Tingey, 1999). An improved investigation of the mechanisms for the traits associated with the tuber and foliage resistance and the introduction of these traits into commercial varieties may be an effective way to enhance the plant resistance against P. operculella. Golizadeh et al. (2010) tested the resistance of six potato cultivars; also, Rondon et al. (2009) studied potato lines, some of which exhibited promising results for suppressing mines and the number of larvae in potato tubers (Gill et al., 2014). An earlier study by Rondon et al. (2009) confirmed that tubers of the transgenic clone Spunta G2 were resistant to P. operculella damage. Spunta G2 was developed in the early 2000s (Douches et al., 2002, 2004). In recent years, plants have received genes that encode toxic proteins to resist against insects (Gatehouse et al., 1999; Franco et al., 2002). Thus, researchers like Fatehi et al. (2016) evaluated the effect of wheat extracts against digestive alpha-amylase and protease activities against P. operculella; those enzymes are important digestive enzymes used during the feeding process. Inhibition of enzymes could potentially help us reduce or stop P. operculella feeding. Also, radiation to induce sterility of P. operculella males has also been studied (Makee and Saour, 1999; Saour and Makee, 1997, 2002, 2004).

8.11 Conclusions Phthorimaea operculella is one of the most important cosmopolitan pest of Solanaceous crops. Biological and ecological qualities of P. operculella plus its intrinsic adaptation capability makes this pest a challenging pest to control. Up to date, research keeps providing us the tools needed to keep this pest under checked. Future climate variations will add to the challenges to deal with this and other pests.

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Acknowledgments The author thanks Mr. N. Simarad for literature organization.

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Biology and temperature responses of Chelonus kellieae and Chelonus-phthorimaeae (Hymenoptera: Braconidae) and their host, the potato tuberworm, Phthorimaea operculella (Lepidoptera: Gelechiidae). Hilgardia 52, 1e32. Pucci, C., Franco-Spanedda, A., Minutoli, E., 2003. Field study of parasitism caused by endemic parasitoids and by the exotic parasitoid Copidosoma koehleri on Phthorimaea operculella in central Italy. Bull. Insectol. 56, 221e224. Radcliffe, E.B., 1982. Insect pest of potato. Annu. Rev. Entomol. 27, 173e204. Rahman, A., 1980. Biology and control of volunteer potatoes: a review. N. Z. J. Exp. Agric. 8, 313e319. Raman, K.V., 1980. The Potato Tuber Moth. Technical Information Bulletin 3. International Potato Center Lima, Peru. (Revised Edition 1980). Raman, K.V., Booth, R.H., 1984. Integrated control of potato moth in rustic potato storage. In: Proc. Sixth Symp. Inter. Sot. Trap. Root Crops International Potato Center, Lima, Peru, pp. 509e515. Raman, K.V., Booth, R.H., Palacios, M., 1987. Control of potato tuber moth Phthorimaea operculella (Zeller) in rustic potato stores. Trop. Sci. 27, 175e194.

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Comparison of a dry and a water trap for monitoring potato tubermoth, Phthorimaea operculella Zeller. Entomology 19, 163e165. Tanaskovic, S., Djurovic, V., Popovic, B., Knezevic, D., Gvozdenac, S., Prvulovic, D., 2016. Plants as bio-insecticides in the service of the suppression of potato tuber moth in storage. Savetovanje o Biotehncologijo, Zbornik radova 21, 453e458. Tingey, W.M., 1986. Techniques for evaluating plant resistance to insects. In: Miller, J.R., Miller, T.A., Berenbaum, M. (Eds.), Insect Plant Interactions. Springer, New York, NY, USA, pp. 251e284. Traynier, R.M., 1975. Field and laboratory experiments on the site of oviposition by the potato moth. Bull. Entomol. Res. 65, 391e398. Traynier, R.M., 1983. Influence of plant and adult food and fecundity of potato tuber moth, Phthorimaea operculella. Entomol. Exp. Appl. 33, 145e154. Trehan, K.N., Bagal, S.R., 1944. Life history and bionomics of potato tuber moth Phthorimaea operculella Zell. (Lepidoptera: Gelechiidae). Proc. Indian Acad. Sci. 19, 176e187. Trivedi, T.P., Rajagopal, D., 1992. Distribution, biology, ecology and management of potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae): a review. Trop. Pest Manag. 38, 279e285. Underhill, G.W., 1926. Studies on the Potato Tuber Moth during the Winter of 1925-26, vol. 251. Virginia Exp. Station Bull., Blacksburg, VA, USA. University of California, 2006. Integrated Pest Management for Potatoes in the Western United States. Statewide Integrated Pest Management Program. Ag. and Nat. Res. Pub. 3316, Western Regional Publication 011, p. 167. Urbaneja, A., Vercher, R., Navarro, V., Garcia, M.F., Porcuna, J.L., 2007. La polilla del tomate, Tuta absoluta. Phytoma Esspana 194, 16e23. Van der Goot, P., 1926. Brestrisding Van de aardappel-Knolrups in Goedangs. Korte Meded. Inst. Piziektenziekten 1, 17. Van Loon, J.J.A., 2013. Insect-host Integrations: Signals, Sense, and Selection Behavior. 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Chapter 9

Hemipterans, other than aphids and psyllids affecting potatoes worldwide Tiziana Oppedisanoa, Govinda Shresthaa and Silvia I. Rondonb a

Department of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon State University, Hermiston, OR,

United States; bDepartment of Crop and Soil Science, Hermiston Agricultural Research and Extension Center, Oregon Integrated Pest Management Center, Oregon State University, Corvallis, OR, United States

9.1 Introduction Hemiptera is an order of insects divided into three suborders: Auchenorrhyncha (leafhoppers, planthoppers, cicadas, treehoppers, spittlebugs), Sternorrhyncha (scales, aphids, whiteflies, psyllids), and Heteroptera (true bugs). Leafhoppers, other than aphids and psyllids, represent the most important hemipteran pests present in potatoes, Solanum tuberosum L. Some Auchenorrhyncha and Sternorrhyncha can cause serious damage to potatoes due to their direct feeding, but may also transmit pathogens, including viruses, bacteria, and phytoplasmas. Heteroptera are secondary or occasional pests, and their damage is mainly caused by direct feeding. Herein, we describe the role of hemipterans present in diverse geographical potato-growing regions worldwide. Emphasis is given to leafhoppers (Auchenorrhyncha: Cicadellidae), planthoppers (Auchenorrhyncha: Cixiidae), and true bugs (Heteroptera: Lygaeidae, Pentatomidae, and Miridae).

9.2 Leafhoppers The leafhoppers (Cicadellidae) comprise by far the largest hemipteran group, with approximately 25,000 described species and over 3200 genera (Dietrich, 2005; McKamey, 2007). Worldwide, leafhoppers occur in terrestrial habitats wherever vascular plants are found (Dietrich, 2005). These small insects are plant feeders that suck plant sap causing discoloration and some species can vector pathogens. Leafhopper adults are small to medium-sized, ranging from 2 to 30 mm in length but rarely exceeding 12 mm. They usually have somewhat cylindrical or wedge-shaped bodies (Dietrich, 2005; Munyaneza et al., 2012). Leafhoppers are very active insects and use both wings and legs for locomotion. Leafhopper adults can jump and/or fly, while immature leafhoppers, since they do not have developed wings, mostly jump or run sideways (Shah and Zhang, 2018). They have brochosomes, a unique feature of the group, which are microscopic granules on their body surface that release droplets that protect leafhoppers against parasitoids and predators (Rakitov and Gorb, 2013). Identification of leafhoppers at species level is not always easy, and often requires dissection and examination of genitalia and the use of identification keys, if available, or the use of molecular techniques (e.g., DNA barcoding) (Zhang et al., 2019). With their highly adapted piercing-sucking mouthparts, leafhopper adults and nymphs display a range of feeding strategies (Weintraub et al., 2019). One characteristic that makes them efficient vectors of pathogens is that they feed specifically and selectively on certain plant tissues such as phloem and xylem. Furthermore, their feeding is nondestructive, promoting successful inoculation of pathogens without damaging conductive tissues and/or eliciting plant defensive responses (Weintraub and Beanland, 2006). Some species feed on the sap circulating in the phloem system (e.g., Deltocephalinae), some other species feed on sap in the xylem system (e.g., Cicadellinae) and others feed on the mesophyll tissue (e.g., Typhlocybinae) (Wilson and Weintraub, 2007). Interestingly, these feeding strategies are not rigid. For instance, members of the Typhlocybinae subfamily may also feed interchangeably on sap circulating in either xylem or phloem (Weintraub et al., 2019). This is the

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reason members of the Typhlocybinae group are well known in agriculture for being destructive feeders causing “hopperburn”, but they are also known for vectoring pathogens such as phytoplasmas (Galetto et al., 2011; Weintraub et al., 2019). In potatoes, species of importance from the Typhlocybinae group include Empoasca fabae Harris and E. decipiens Paoli; from the Deltocephalinae, Circulifer tenellus Baker and Macrosteles quadrilineatus Forbes. A discussion of each species below will include biological and ecological features as well as pest status and management.

9.2.1 Empoasca fabae (potato leafhopper) The genus Empoasca contains a number of leafhoppers of economic importance (Poos and Wheeler, 1943). The potato leafhopper Empoasca fabae is undoubtedly one of the most important pests of potato. It is native to North America and commonly found throughout the USA, and in some parts of India where they cause severe damage especially in early planted potatoes (Verma, 1994). Empoasca fabae feeds and completes its life cycle on a large number of wild and cultivated host plants including potato, alfalfa, bean, eggplant, clover, and rhubarb but also tree fruits like apple, citrus, and ornamentals like dahlia (Lamp, 1991). In the USA, infestations of the potato leafhopper can reduce yields up to 80% in crops such as alfalfa if left uncontrolled (Tingey and Muka, 1983). Potato leafhoppers often go unnoticed until later in the growing season when economic injury levels have already occurred.

9.2.1.1 Biology and ecology Each spring E. fabae migrates north from southern states where they overwinter. Weather has a strong impact on time of emergence and subsequent arrivals to crops (Pienkowski and Medler, 1964; Deckfr and Cunningham, 1968). Adults of E. fabae are around 3.5 mm long and present a yellowish to bright green color (Fig. 9.1). They usually present a row of six or more white spots on the anterior margin of the pronotum. They may also present a variable pale or dark-green distinctive mark on the vertex (Capinera, 2008). The body is wedge-like with a broad head and a tapered abdomen. The head has short antennae and is characterized by a bluntly angled vertex (Capinera, 2008). Females lay translucent cylindrical eggs in stems and leaf veins, and eggs are less than 1 mm long and hatch in 6e9 days in the summer under warmer temperatures (DeLong, 1938; Hutchins, 1987). Poos and Smith (1931) reported potato as a preferred reproductive host for E. fabae. Nymphs are similar to adults in appearance, but are smaller, yellowish green to fluorescent green without fully developed

FIG. 9.1 Empoasca fabae (potato leafhopper) life stages: nymph (left); and adult (right). Photos: John Schneider (nymph) and Tiziana Oppedisano (Oregon State University).

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wings and genitalia (Fig. 9.1). Wing pads develop during the third to fifth nymphal instar. The average developmental time for all nymphal stages is typically 15 days (DeLong, 1938). Each generation takes approximately 30e35 days depending on the region, therefore E. fabae can complete two to four generations per year (DeLong, 1938; Hogg and Hoffman, 1989).

9.2.1.2 Damage and pest status Ball (1918) described the “hopperburn” as the typical injury due to the direct feeding of adults or nymphs. Hopperburn is characterized by distortion of the leaf veins and a consequent yellowing of the tissue around the margin and at the tip of the leaf; also rolling or curling rapidly spreads until the whole leaf is dry and dead (Backus et al., 2005) (Fig. 9.2). Radcliffe (1982) reported that the last nymphal stage is the most detrimental stage since they repeatedly probe the plant tissue lacerating cells. While feeding, potato leafhoppers inject a watery saliva that includes an enzyme that reduces plant photosynthetic capability (Ecale and Backus, 1995). Feeding of E. fabae causes green tissue to turn yellow because of physiological changes including increased respiration and decreased photosynthesis in the plant. Consequently, occlusions of the conductive tissues occur thus reducing tuber development (Ladd Jr and Rawlins, 1965; Munyaneza et al., 2012). When insect infestation is heavy, the entire plant is usually killed in a short period of time. Prolonged feeding can also cause stunting and dwarfing. Interestingly enough, E. fabae feeding injury can be misdiagnosed as herbicide injury or nutritional deficiencies (Hodgson, 2017), confirming the importance of a correct diagnosis. Radcliffe and Johnson (1994) indicated that the relationship between yield loss and leafhopper numbers is linear; thus, the more leafhoppers per plant, the greater the yield penalty. Yield loss due to E. fabae infestation can reach up to 75% in severely infested fields (De Medeiros et al., 2004). In potatoes in south western Ontario (Canada), average losses are up to 85% (Tolman et al., 1986), while Noetzel (1985) estimated an annual loss of $7 million USD on potato production in Minnesota (USA) due to E. fabae.

9.2.1.3 Pest management Potato leafhopper management is based on monitoring, cultural control, and the use of insecticides when economic thresholds are reached (Cancelado and Radcliffe, 1979; Sexson, 2005; Kroschel et al., 2020). The recommended economic threshold in potato is 10 or more nymphs per 100 leaves, or 10% of the leaves infested with nymphs (IPC, 1996; Kroschel et al., 2020). Visual inspections and deployment of yellow sticky cards are common practices used to monitor potato leafhoppers. Both adult and immature E. fabae prefer the underside of leaves. Since they move fast and jump readily if disturbed, visual inspections are executed by turning the leaves over and quickly counting leafhoppers. If using yellow sticky cards, they should be placed close to the crop canopy and changed weekly. Efficacy of biological control is limited although a diversity of natural enemies have been reported (De Medeiros et al., 2004). According to Kroschel et al. (2020), natural enemies such as predators and parasitoids play a very minor role in potato leafhopper control in potato fields. Weiser Erlandson and Obrycki (2010) tested the predatory effect of Coleomegilla

FIG. 9.2 Empoasca fabae feeding damage on potato (hopperburn). Symptoms are characterized by distortion of the leaf veins, and consequent yellowing of the tissue around the margin and at the tip of the leaf until the whole leaf is dry and dead. Photo: John Obermeyer (Purdue Extension Entomology).

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maculate Degeer (Coleoptera: Coccinellidae), Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), and Orius insidiosus Say (Hemiptera: Anthocoridae) on E. fabae, finding out that C. carnea larvae exhibited a higher attack rates than C. maculata and O. insidiosus adults. Among parasitoids, potato leafhopper has been reported as a host of Anagrus nigriventris (Hymenoptera: Mymaridae) (Albarracin et al., 2006). A recommended cultural control practice is to avoid planting potatoes near preferred crops such as beans or alfalfa. This practice can reduce the migration of E. fabae into the potatoes. Optimizing nutrients and proper irrigation practices can help the potato crop withstand insect damage. Current control recommendations include the use of chemical treatments when leafhoppers (both nymphs and adults) reach 10 to 15 per leaf. Various active ingredients are known to control leafhoppers; however, regulations and availability of products may differ among different states and countries. In general, systemic and contact products will be more successful than broad-spectrum insecticides. In highly affected regions, resistant or tolerant potato varieties when available, should be considered (Backus et al., 2005). Seaman et al. (2004) found the varieties “Red Norland”, “Carola” and “All Blu” as highly susceptible to hopperburn, while “Prince Hairy”, “Yukon Gold”, “Elba”, “Russian Banana”, and “All Red” were found relatively tolerant.

9.2.2 Empoasca decipiens (green leafhopper) The green leafhopper E. decipiens is an extremely polyphagous insect found on many woody, herbaceous, and wild plants and on a wide variety of agricultural crops (Poos and Wheeler, 1943; Nickel, 2003; Arzone et al., 2008). Empoasca decipiens is one of the most important insect pests found on beet, eggplant, potato, tomato, kidney bean, oak, barley, clover, cotton, lentil, maize, sugarcane, sweet potato, and wheat (Poos and Wheeler, 1943; Rassoulian et al., 2005; Naseri et al., 2007; Demirel and Yõldõrõm, 2008; Fathi et al., 2009). This leafhopper is widely distributed in central and southern Europe, North Africa (Egypt), Middle East (Turkey and Iran), and Central Asia (Ossiannilsson, 1981; Ebadah, 2002; Agboka et al., 2003; Demirel and Yõldõrõm, 2008; Fathi et al., 2009).

9.2.2.1 Biology and ecology Empoasca decipiens is commonly referred to as the “green leafhopper” because of its coloration. From a morphological point of view, it is not easy to distinguish E. decipiens from E. fabae but it is important to note that those two species are actually present in potatoes but in two different geographical regions. Like E. fabae, adults of E. decipiens are small insects, 3e4 mm long and are homogenously greenish looking with whitish markings on its pronotum and vertex (Biedermann and Niedringhaus, 2009). Females lay small eggs (less than 1.5 mm) inside the meristematic tissue or the stem of a host plant (Müller, 1956). After hatching, they develop into five nymphal stages, developing wings during their fourth instar. Development takes 10e37 days depending on temperature and host plant, with an optimal temperature for egg development and larvae emergence around 24
C. Research indicated that a four-degree increase in temperature will shorten nymphal development by 2 days (Raupach et al., 2002). In Europe, E. decipiens completes two to three generations per year while in warmer climates like North Africa it can complete up to four generations (Ebadah, 2002). Fathi et al. (2009) reported that this leafhopper prefers plants whose leaves lack trichomes, have soft tissues, and are of large size. The same authors evaluated the resistance of four potato cultivars (“Diamant”, “Casmos”, “Omidbakhsh”, and “Agria”) to E. decipiens by evaluating some life cycle parameters such as incubation period, larval development time, larval survival, female and male life span, and adult longevity. They found that the incubation period in earlier instars is not affected by variety, while fourth and fifth instar larvae life span decreased (Fathi et al., 2009). Naseri et al. (2009) described an interesting behavior on leafhoppers of this species where they aggregate in close groups when population density is high, while occurring randomly distributed in the landscape when populations are small.

9.2.2.2 Damage and pest status The green leafhopper is known to feed on both phloem and mesophyll of several hosts (Nickel, 2003). Empoasca decipiens also causes hopperburn by puncturing the phloem and xylem tissues of the plants. The injection of toxins by nymphs and adults causes curling of leaf edges, and a progression of yellowish or brownish discolorations, and necrosis of plant tissue (Nielson, 1985; El-Gindy, 2002; Raupach et al., 2002; Backus et al., 2005). This species of leafhopper also causes indirect damage by transmitting pathogenic organisms such as viruses, phytoplasma, spiroplasma, and bacteria (Nault and Ammar, 1989; Orenstein et al., 2003; Beanland et al., 2006). Indeed, the green leafhopper has been found to acquire and transmit two phytoplasmas, “Ca. Phytoplasma aurantifolia” (16SrII group), and “Ca. Phytoplasma asteris” (16SrIeB group) in cool

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season ranunculus flowers (Parella et al., 2008; Alhudaib et al., 2009). According to Galetto et al. (2011), the transmission efficiency still needs to be further investigated. There are no reports of E. decipiens vectoring phytoplasmas to potatoes thus far.

9.2.2.3 Pest management The high mobility of green leafhopper adults and nymphs makes it difficult for biological control programs to be effective. Predators such as the minute pirate bug (Hemiptera: Anthocoridae) (Helyer and Talbalaghi, 1994; Agboka et al., 2003), and the lady beetle Coccinella undecimpunctata L. (Coleoptera: Coccinellidae) (Mahmoud et al., 2011) have been moderately successful. In contrast, parasitoids such as the egg parasitoid Anagrus atomus L. (Hymenoptera: Mymaridae) was reported to reduce the fitness of green leafhoppers (Cerutti et al., 1991; Agboka et al., 2003). The dryinid Lonchodryinus ruficornis Dalman (Hymenoptera: Dryinidae) was reported as a moderately efficient parasitoid (Demichelis and Manino, 1995). Several species of entomopathogenic fungi are known to affect green leafhopper populations (Tounou et al., 2003), including Beauveria bassiana Vuill., Metarhizium anisopliae Sorokin, and Paecilomyces fumosoroseus Wize. Under laboratory conditions, first instar nymphs showed more susceptibility to pathogens compared to older instars (Kodjo et al., 2011). Kodjo et al. (2011) recommends the use of biological control in combination with other control strategies such as chemical control. Empoasca decipiens can be controlled in the field and greenhouse through application of synthetic systemic insecticides (Agboka et al., 2003).

9.2.3 Circulifer tenellus (beet leafhopper) The beet leafhopper Circulifer tenellus is a generalist leafhopper (Hudson et al., 2010). It feeds and reproduces on many different plants including sugar beet, tomato, cucurbits, and spinach, and wild hosts such as tumble mustard, pigweed, lambsquarters, groundsel, wild radish, redstem filaree, and various species of thistles (Golino et al., 1989; Rondon and Oppedisano, 2020). Circulifer tenellus may have originated from the eastern Mediterranean region (Oman, 1948), showing now a wide worldwide distribution including North America, Europe, Africa, and Asia (EPPO, 2021). This leafhopper is associated with three important pathogens: the beet curly top virus (BCTV) (Chen and Gilbertson, 2016), the phytoplasma known as beet leafhopper-transmitted virescence agent (BLTVA) (Munyaneza et al., 2006), and the spiroplasma Spiroplasma citri (Liu et al., 1983). Due to C. tenellus “super” vector powers, C. tenellus can cause economic losses in potatoes, beans, pepper, tomato, spinach, sugar beets, melons and members of the squash family (Hills, 1937; Cook, 1941; Capinera, 2001). Recently, this species is being investigated as an emergent pest on hemp (Giladi et al., 2020).

9.2.3.1 Biology and ecology Classification and distribution of C. tenellus in the Old and New world have been revised by Oman (1970), while traits of its biology and ecology have been reported by Harries and Douglass (1948). Identification of C. tenellus is not easy. Adults of C. tenellus are small insects that measure about 3.4e3.7 mm in length (Hudson et al., 2010) (Fig. 9.3). Two forms (light and dark) are found over the year; lighter coloration (whitish or yellowish) is associated with higher temperatures, while darker ones showing dorsally small dark spots, are associated with colder temperature in the fall/winter. The overwintering females are fertilized in the fall, and most of the males perish during the winter (Severin, 1919; Harries and Douglass, 1948; Douglass, 1954). Circulifer tenellus is able to cover long distances during migration (Dorst and Davis, 1937; Cook, 1967). In spring, females leave the overwintering sites to reach reproduction sites where they deposit eggs individually in the green tissue of the leaves and stems. The eggs are elongated and slightly curved, changing from whitish to yellowish in color during development (Fig. 9.3). With optimal temperature conditions of 30
C, each female may deposit 300e400 eggs during its life spam that hatch 5e7 days later (Harries and Douglass, 1948; Munyaneza et al., 2012). Newly emerged nymphs are transparent to white but become yellowish in color within a few hours. There are five nymphal instars, and the later instar is typically spotted with black, red and brown on the thorax and abdomen (Fig. 9.3). Depending on the geographical area, the number of generations is two up to five, with more generations in warmer regions (Severin, 1930; Dorst and Davis, 1937).

9.2.3.2 Damage and pest status Direct feeding by C. tenellus causes relatively minor damage on potatoes. However, its pest status derives from the ability to transmit pathogens that can cause diseases like potato purple top disease in North America. Purple top was first

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FIG. 9.3 Circulifer tenellus (beet leafhopper) life stages: eggs are elongated and slightly curved, and are laid individually on leaves and stems (A); young stages develop into five instars, third instar nymph is represented (B); and adult (C). Photos: Tiziana Oppedisano (Oregon State University).

documented in Canada in 1933, and a year later, it was cited as a limiting factor in potato production in several areas of Canada and USA, since the majority of the varieties cultivated at that time were susceptible to the disease (Cadena-Hinojosa, 1996; Leyva-López et al., 2002). In Central America (Mexico and Guatemala), potato purple top is considered the second most important disease of potato after late blight (Cadena-Hinojosa, 1996). Potato purple top disease is associated with several phytoplasmas including the BLTVA, which belongs to the clover proliferation phytoplasma group 16SrVI-A (‘Ca. Phytoplasma trifolii’) (Munyaneza et al., 2006). Circulifer tenellus was proved to be the vector responsible of the transmission of BLTVA that causes purple top in the Columbia Basin in the USA Pacific Northwest (Crosslin et al., 2005; Munyaneza et al., 2006). In other potato growing regions other phytoplasmas and other vectors are responsible for the disease. This disease is known to cause serious economic damage to potatoes affecting quality and yield (Hamm et al., 2003). Symptoms of BLTVA infection include rolling upward of the top leaves with yellowish, reddish or purplish discoloration, moderate proliferation of buds, shortened internodes, swollen nodes, aerial tubers, and early plant decline (Munyaneza, 2005; Munyaneza and Upton, 2005; Munyaneza et al., 2007) (Fig. 9.4). Population density of C. tenellus varies during the growing season (Rondon and Oppedisano, 2020). Munyaneza et al. (2010) found BLTVA rates in C. tenellus ranging from 9.2% to 34.8% in specimens collected from potatoes, 5.6%e28.3% in specimens collected from weeds, and 39.3%e44.5% in specimens collected from infected colonies. Through screenhouse experiments, researchers have estimated that the severity of potato yield loss in the Columbia Basin changes in relation to C. tenellus density, indicating up to 12% when one beet leafhopper is present on plant, 6%e19% with two per plant, and 6%e20% with five per plant (Murphy et al., 2014).

9.2.3.3 Pest management Due to C. tenellus importance as the only known vector of BLTVA, this insect is monitored weekly in potatoes every growing season in the northwestern USA Columbia Basin region (Wohleb et al., 2010; Rondon, 2012; Wenninger et al., 2020). Annand (1932) reported movements of C. tenellus from different areas in Idaho (USA) and emphasized the importance of extensive and thorough surveys in the fall and spring as a closer check on the distribution, abundance, and development of the insect relative to economic conditions determined by timing and migration into cultivated areas.

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FIG. 9.4 Damages caused by BLTVA in potato. Common phytoplasma infection symptoms include: rolling upward of the top leaves with yellowish, reddish or purplish discoloration (left); formation of aerial tubers and early plant decline (right). Photos: Tiziana Oppedisano (Oregon State University).

Current recommendations encourage producers to monitor C. tenellus by using yellow sticky cards placed 1.5e3 m from the edge of a potato field starting from 2 weeks after emergence until 4 weeks before harvest (Rondon and Oppedisano, 2020). Rondon and Murphy (2016) evaluated effective monitoring techniques like sweep net and the use of an inverted leaf blower, demonstrating that significantly more C. tenellus are collected by using the inverted leaf blower compared to a sweep net. The same authors identified timing of insecticide applications by testing four active ingredients such as oxamyl, esfenvalerate, imidacloprid, and cyfluthrin. They showed that insecticide applications reduce the total mean numbers of C. tenellus but did not increase yield; also, early applications worked better reducing overall C. tenellus populations compared to late applications. Munyaneza et al. (2010) reinforced these findings with epidemiology studies, reporting that young potatoes are more susceptible to BLTVA transmission. Weed control can also be used as cultural methods to reduce C. tenellus infestations since it is well known that weeds such as kochia, Russian thistle, tumble mustard, and redstem filaree host large beet leafhopper populations and they are common weeds near potato fields in the western USA (Rondon and Oppedisano, 2020). Selection of tolerant cultivars is also a way to reduce phytoplasma infection in potatoes. Munyaneza et al. (2009) described ‘Russet Norkotah’, ‘Ranger Russet’ and ‘Umatilla Russet’ as susceptible cultivars, ‘Alturas’ and ‘Shepody’ as moderately susceptible, while ‘Russet Burbank’ as the cultivar showing a reasonable amount of resistance. Attempts to regulate C. tenellus by biological control were initiated in the early 1900’s (Vosler, 1919; Henderson, 1928). In California, Meyerdirk and Moratorio (1987) collected C. tenellus eggs parasitized with wasps belonging to the Mymaridae family including Anagrus nigriventris Girault, Polynema sp., Gonatocerus sp.; also Trichogrammatidae such as Aphelinoidea sp. and Paracentrobia sp. Rondon and Oppedisano (2020) listed several species of generalist predators such as green lacewings, spiders, stilt bugs, assassin bugs and big-eyed bugs present in potato fields.

9.2.4 Macrosteles quadrilineatus (aster leafhopper) The aster leafhopper or six-spotted leafhopper Macrosteles quadrilineatus (previously Macrosteles fasciifrons Stål) is a polyphagous pest with over 300 host plant species, including vegetable and cereal hosts (Wallis, 1962; Peterson, 1974). Numerous weed species are also used by this pest for feeding, oviposition, and overwintering (Hagel and Landis, 1967). The aster leafhopper is native to North America, and it is found in almost all the states of the USA and Canada. M. quadrilineatus was found to be one of the most abundant leafhoppers in the main potato-producing areas of Alaska (Pantoja et al., 2009). Besides potato, several other vegetable crops are damaged by the aster leafhopper, including carrot,

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celeriac, celery, corn, lettuce, parsley, and radish. Carrot, potato, and radish are considered good food plants, but not as breeding hosts (Capinera, 2008). Macrosteles quadrilineatus can disperse effectively over large distances (Frost et al., 2013).

9.2.4.1 Biology and ecology The adults of M. quadrilineatus are small, with females about 3.5e3.8 mm long and males about 3.2e3.4 mm. This leafhopper appears yellowish/light green in color, with the forewings tending toward grayish green and the abdomen yellowish green. There are six pairs of black spots, some of which are elongated almost into horizontal bands, starting at the top of the head and extending along the front of the head almost to the base of the mouthparts (Fig. 9.5). This insect can overwinter in the egg stage in northern locations, and as adult in warmer climates. Macrosteles quadrilineatus undergoes many generations in a single season (Hagel and Landis, 1967). In northern areas, there are three generations per year, whereas up to five generations may occur in more favorable Midwestern locations. Eggs are laid singly but also in short rows of up to five eggs in leaf, petiole, or stem tissue. The eggs are translucent to white or yellow (Fig. 9.5). Five instars are required before develop into adults in about 19e26 days. Newly hatched nymphs are nearly white, but soon become yellow and gain brownish markings, including dark markings on the head (Munyaneza et al., 2012) (Fig. 9.5). As the nymphs mature, they gain spines on the hind tibiae and the tip of the abdomen. The wing pads become apparent in the fourth instar and overlap the abdominal segments in the fifth instar (Capinera, 2008).

FIG. 9.5 Macrosteles quadrilineatus (aster leafhopper) life stages: eggs are laid singly or in short rows of up to five in leaves and stem tissues (A); five instars are required before develop into adults (B); Drynidae larva parasitizing an aster leafhopper adult (C). Photos: Tiziana Oppedisano (Oregon State University).

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9.2.4.2 Damage and pest status In potato, this insect transmits the aster yellows phytoplasma (“Ca. Phytoplasma asteris”, AYP, 16SrI group) that causes purple top disease (Lee et al., 1998). Aster leafhoppers acquire the AYP horizontally by feeding on infected perennial and biennial weeds and/or crop plants other than potato. The acquisition process requires a prolonged period of feeding, usually at least 2 hours. After acquisition, the phytoplasma multiplies in the body of the leafhopper with an incubation period of about 14 days in nymphs and 6e10 days in adults before the insects are capable of transmit this pathogen. The aster leafhoppers remain infective for all their life, and there is no evidence of vertical transmission through the egg stage (Capinera, 2001). Symptoms of purple top caused by AYP transmitted by M. quadrilineatus, and purple top caused by BLTVA transmitted by C. tenellus are almost identical and only a molecular diagnosis can discriminate the two casual agents. Similar to BLTVA, for AYP infections the most common symptoms are purpling, reddish, or yellowing of the bases of young leaflets. Interestingly, discoloration does not appear until the flowering stage is reached. In addition, proliferation of axillary buds is common on infected plants as well as the exhibition of stunting due to shorten internodes; chlorosis can affect the entire plant and the leaves usually turn upward. Due to phloem tissue damage caused by the presence of AYP, which prevents the movements of carbohydrates to the developing tubers, the formation of aerial tubers in the axillary buds is also a common symptom. Phytoplasmas usually are not passed to daughter tubers, but some AYP strains were demonstrated to prevent infected tubers from sprouting that produce weak plants with low marketable tuber production (Leyva-López et al., 2002; Jones et al., 2005; Munyaneza et al., 2012). Consequently, potato fields with severe AYP infections may have reduced yields. Even if tubers from infected potato plants usually appear normal at harvesting, sugar balance can be altered in stored tubers (Banttari et al., 1993; Munyaneza et al., 2012). Tubers from infected plants may also develop stem-end necrosis (Rich, 1983). This physiological change results in high concentrations of sucrose and reducing sugars (glucose and fructose), which can cause undesirable color development upon tuber processing (Banttari et al., 1993; Munyaneza et al., 2006).

9.2.4.3 Pest management Macrosteles quadrilineatus is typically controlled using repetitive applications of insecticidal compounds belonging to the synthetic pyrethroid group (Frost et al., 2013) and carbamates (Godfrey et al., 2015a). The most important natural enemies are the parasitoids Pachygonatopus minimus Fenton, Neogonatopus ombrodes Perkins, and Epigonatopus plesius Fenton (all Hymenoptera: Dryinidae) (Fig. 9.5). For instance, P. minimus parasitism can reach up to 37% (Capinera, 2008). Predators like spiders also feed on aster leafhoppers. In small plot studies in rice paddies, the spider, Pardosa ramulosa McCook, significantly reduced populations of aster leafhopper (Godfrey et al., 2015a). Broadleaf weeds and sedges serve as overwintering and sheltering sites for aster leafhoppers. Thus, controlling natural weed hosts and monitoring leafhoppers during the summer can be good approaches to predict movement of leafhoppers into potato fields. Godfrey et al. (2015a) indicated that an early and effective weed control program is an important way to discourage the development of economically damaging populations of leafhoppers on weeds and future movement of leafhoppers.

9.3 Planthoppers Planthoppers constitute a large group of sap-feeding insects in the order Hemiptera. Their name refers to their jumping ability. Currently, 20 families and more than 9000 species of planthoppers have been described (O’Brien and Wilson, 1985), which are collectively organized in the super family Fulgoroidea (Denno and Roderick, 1990; Denno and Perfect, 2012). Planthoppers include several well-known agricultural pests (Denno and Roderick, 1990). Many of them are pests of economic significance affecting major agricultural crops such as corn, solanaceous crops, wheat, rice, barley, grapes and sugarcane (O’Brien and Wilson, 1985; Brezíková and Linhartová, 2007). As for leafhoppers, planthoppers can damage plants directly causing “hopperburn” or indirectly as vectors of a variety of plant pathogens. Some planthoppers (family Cixiidae), are known to be pests in some potato growing regions of Europe and Asia. The family Cixiidae is easily differentiated from other Fulgoroidea by the large and transparent forewings, surpassing the tip of the abdomen, and by displaying distinct venations and tubercles (Bertin et al., 2010). Cixiid pests in potato are known vectors of “Ca. Phytoplasma solani”, phytoplasma group 16SrXII (Quaglino et al., 2013). In the European Union, this phytoplasma has a quarantine status and is one of the most significant pathogens affecting potato (EPPO/CABI, 1996). “Ca. Phytoplasma solani” is transmitted by grafting and vegetative propagation of infected host plants, and vectored by Hyalesthes obsoletus Signoret and Reptalus panzeri Löw, and possibly others as Reptalus quinquecostatus Dufour

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(Pinzauti et al., 2008; Cvrkovic et al., 2014). Hyalesthes obsoletus also transmit other plant pathogens (Safarova et al., 2011). Furthermore, R. panzeri is known vector of this phytoplasma in maize fields and vineyards (Jovic et al., 2007; Cvrkovic et al., 2014) and H. obsoletus in vineyards and sugar beet fields (Maixner et al., 1995; Sforza et al., 1998; Bressan et al., 2006). “Ca. Phytoplasma solani” vectored by cixiid species causes a serious grapevine yellows disease known as bois noir. In potatoes, potato stolbur is the disease caused by the “Ca. Phytoplasma solani” and it has an economically significant impact on potato production. Symptoms are similar to the other potato purple top disease, and include reddening and upward rolling of leaflets, reduced size of leaves, shortened internodes, and aerial tuber formation (Holeva et al., 2014). Plants grown from infected tubers give rise to normal or spindly sprouts (hair-sprouting). Where normal sprouts arise, symptoms are first apparent about 60e80 days after sowing, and the first symptom is a yellowing and rolling of the leaves, followed by the production of aerial stolons and tubers in different parts of the stems close to the axils (EPPO/CABI, 1996). Severe outbreaks of potato stolbur have been reported in the Czech Republic, Hungary, Romania, and Russia, causing 30%e80% yield loss and reduction in tuber and seed quality (Ember et al., 2011). Composition of the Auchenorrhyncha fauna in the potato fields in Serbia and the presence of “Ca. Phytoplasma solani” in the wild plants indicate a rather complex epidemiology of potato stolbur disease, with several plausible spread pathways (Mitrovic et al., 2016). Below, we provide a brief description of these three cixiid potato pests.

9.3.1 Hyalesthes obsoletus Hyalesthes obsoletus is a Palearctic planthopper considered primarily a Mediterranean species. It is distributed across most of mainland Europe and through the Middle East to North Africa including Iran, Kazakhstan, Afghanistan, Tajikistan and Uzbekistan, and Asia Minor (Kosovac et al., 2018). Hyalesthes obsoletus adults are polyphagous and feed on a wide range of herbaceous plant species. In Europe, field bindweed, ribwort plantain, pigweed, common nettle, and lavender are the preferred hosts, along with about 20 others plant species. The phenology of this planthopper is closely related to its host plants. For instance, it is univoltine in Europe, while they have two generations in Israel where they are mainly found on chaste tree, field bindweed, and wine grapes (Klein et al., 2001; Sharon et al., 2005). Adults of H. obsoletus are 4e5 mm long, the body is mostly black, and the wings are hyaline with dark patches. Females produce several hundred wax-covered eggs, and the progeny, which mostly feed on roots, require several months to mature. Eggs are laid in batches in the upper level of the soil close to the root collar of herbaceous plants. All of the five larval instars feed on the roots of their host plants. Second and third instar larvae hibernate 20e25 cm blow the soil surface (Langer et al., 2003) where they are usually protected from frost damage. During April and May, they gradually move up the soil profile close to soil level. The speed of development and thereby the start of the flight activity of adults depend on spring temperatures (Maixner and Langer, 2006). The beginning of the flight activity can be predicted by a degree-day model (Maixner and Langer, 2006). Populations living on bindweed start approximately three to 4 weeks in advance of those that develop on common nettle (Maixner, 2007; Mori et al., 2020).

9.3.2 Reptalus panzeri and R. quinquecostatus The genus Reptalus includes 29 recognized species distributed in temperate areas of central and southern Europe, the Mediterranean Basin, Asia, and Canada (Bourgoin et al., 2015; Taszakowski et al., 2015). Species of this genus are polyphagous (Taszakowski et al., 2015). Identification of Reptalus spp. is based on morphological characteristics and mainly relies on the shape of the male genitalia, thus hampering the identification of juveniles and adult females. Thus, DNA-based approaches offer valuable support to traditional taxonomic methods and nowadays are widely used for insect species identification (Bertin et al., 2010). The biology and behavior of the Reptalus species is poorly known because of the peculiar characteristics of this planthopper family. Emeljanov (2002) published a detailed description of the morphology of this genus. Reptalus quinquecostatus is a mesophilic species found in moderate temperature regions. Adults live mostly on grassy, rarely woody plants on prairie and dry or isolated habitats. Females lay eggs in the soil near the base of a host plant, and the five nymphal instars live underground and feed on roots. Newly emerged adults fly to leaves and shoots for feeding and mating (Wilson and Tsai, 1982; O’Brien and Wilson, 1985). The involvement of Reptalus spp. in phytoplasma transmission has prompted an active monitoring program. The epidemiological studies and application of control strategies rely on careful surveys of the spread of cixiid species. The reliable identification of each species becomes essential, but may sometimes produce uncertain results.

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9.4 True bugs The true bugs (Heteroptera) group comprises 90 families and more than 45,000 described species present in almost all the biogeographic regions of the world (Cassis, 2019). Even if many heteropteran families are known as beneficial insects due to their predatory behavior (e.g., Reduviidae, Nabidae, Anthocoridae), many others are mainly known as agricultural pests (e.g., Lygaeidae, Pentatomidae, Miridae). Only some of potato-related species will be discussed below.

9.4.1 Lygaeidae (seed bugs) The Lygaeidae is a worldwide distributed family of true bugs (Burdfield-Steel and Shuker, 2014). Several species of this family are well known as economic pests of a variety of crops, including cabbage, rape, carrots, potato, beets, turnip, clover, lucerne, cucumber, cotton, sorghum, tomatoes, strawberries, and all types of squash, barley, wheat and many more crops (Schaefer and Panizzi, 2000). They are commonly found within grassy or weedy fields (Demirel and Cranshaw, 2006). In potatoes, the lygaeid genus Nysius can cause feeding damage. The most representative pest species is the false chinch bug Nysius raphanus Howard, a polyphagous species present throughout North America, Mexico, and the West Indies (Ashlock and Slater, 1988; Sweet, 2000). Adults of false chinch bug are small insects 3e4 mm long, mostly gray, with some brown markings (Panthi et al., 2018). The eggs are laid in the soil around the base of host plants (Demirel and Cranshaw, 2006). After hatching, eggs develop through five nymphal instars which are often found in the leaf litter at the base of plants (Whitworth et al., 2012; Panthi et al., 2018). False chinch bugs move into potato fields during summer following periods of drought or unavailability of weed hosts or preferred hosts like alfalfa (Wene, 1958; Whitworth et al., 2012). The damage is correlated with large aggregations of these bugs and damage looks similar to wind burn. Pavlista (2014) reported a detail description of damage on potato. Briefly, the young top potato leaves are mainly attacked, appearing wilting and slightly curled at the beginning, then rapidly turning brown along the edges and curl until they dry out and die. This process can occur in a matter of a few days. Fully formed leaves are not affected, explaining why the rest of the plant appears normal. In general, the window for potato damage is about 3 weeks after emergence. Yield losses may occur if large parts of the field are damaged during early to mid-bulking. Since damage occurs by sucking water from stems, tuber deformation might result from a severe attack right before tuber formation (Whitworth et al., 2012; Cranshaw, 2007). The false chinch bug rarely requires control on cultivated plants. However, when economically important aggregations occurred, several systemic insecticides can successfully contain populations. Removal of weeds adjacent to cultivated fields is also recommended (Panthi et al., 2018).

9.4.2 Pentatomidae (stinkbugs) The Pentatomidae family is the fourth most numerous within Heteroptera families (after Miridae, Reduviidae, and Lygaegidae). Pentatomidae includes more than 4700 species with more than 800 genera (Grazia et al., 2015). The economic importance of stinkbugs varies greatly from species to species. Many stinkbugs pests belong to the subfamilies Edessinae and Pentatominae, which contains the majority of species that are pests of crops (Schuh and Slater, 1995; Panizzi et al., 2000). Some Edessinae members like the brown-winged stinkbug Edessa meditabunda Fabricius feed on Solanaceae and are pests of potato and tomato in South America and in the Caribbean (Panizzi, 2015). While some Pentatominae are considered minor pests of potatoes in the USA Pacific Northwest, like Chlorochroa, a common genus affecting potatoes in the Columbia Basin (USA) (Rinehold et al., 2018). These stinkbugs colonize potatoes from other nearby crops and from native plants. In potatoes, stinkbug adults often congregate in large groups close to where egg masses were laid. The female lays egg masses of approximately 12 eggs at time, and nymphs develop through five stages. When development is completed, they can form large populations under the right conditions. Like for other sucking-sap feeders, the feeding damage causes flagging of leaflet, and leaf or stem distortion. Moreover, damage caused by feeding at the base of a leaf can cause the entire leaf to wilt. Even if stinkbug adults and nymphs are both easily detected during normal scouting operations using a beating sheet/tray, detecting infestations can be challenging due to its random distribution in the field. Indeed, finding a congregation of these stinkbugs in one small area may lead to incorrect assumptions about the level of infestation throughout the field (Rinehold et al., 2018). Bagrada hilaris Burmeister (painted bug) has as main hosts plants belonging to the mustard family, and a secondary or occasional host other plants including potatoes (Dharpure, 2002). It is native to Africa, India, and Asia (Panizzi, 2015), and

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has been recently reported in California (USA) (Reed et al., 2013). Adults and nymphs of the painted bug feed on leaves, stems, flowers, and seeds. They insert their stylets into leaves and stems, injecting digestive enzymes, and sucking the sap. Feeding damage by B. hilaris is characterized by circular or star-shaped chlorotic lesions that may become necrotic; leaves eventually have large stippled areas and may wilt and die. Painted bugs are particularly damaging to small plants and may kill seedlings (Palumbo et al., 2016). Two other stinkbug species reported on potatoes are Euschistus variolarius Palisot (one-spotted stinkbug) and Arvelius albopunctatus DeGeer (greenewhite spotted bug) (Panizzi et al., 2000). The one-spotted stinkbug can be found on a diversity of wild and cultivated plant species, including field crops and tree fruits (McPherson, 1982). Adults overwinter in protected locations, such as under dry leaves, logs, and dead grass in fencerows (Parish, 1934). This species has been reported as univoltine or bivoltine (McPherson, 1982). The greenewhite spotted bug is reported on plants of the family Solanaceae including tomato, potato, and eggplant, as well as sweet potato and several wild species (Panizzi, 2015) in North, Central, and South America (Froeschner, 1988; Martinez and Folcia, 1999; Rebagliati et al., 2005). Similar to the other sinkbugs it causes wilting of potato leaves by its feeding (Panizzi et al., 2000). It is important to note that some species of large stinkbugs are predators of Colorado potato beetle and caterpillars in potatoes (Rinehold et al., 2018).

9.4.3 Miridae (plant bugs) Miridae represents along with leafhoppers the second most diverse family of Hemiptera (Cassis et al., 2007). Some plant bugs exhibit significant economic impacts in food and fiber crops (Wheeler,s 2001). For example, the genus Lygus, usually referred to as lygus bugs, is an important pest of grain, seed, vegetable, and fruit crops. Lygus bugs have been reported to feed on over 300 host plant species (Scott, 1977; Young, 1986). Schwartz and Foottit (1997) reported 51 Lygus species described so far, 29 of those are distributed in the Nearctic region, 20 in the Palearctic region, while two species are considered Holarctic. Lygus bugs typically feed on leaf buds and reproductive plant parts such as flower buds, mature flowers, developing/mature seeds and fruits (Tingey and Pillemer, 1977). Lygus pratensis L. is widespread all over Europe, Northern Africa, the Middle East, Northern India, China and Siberia. It has many host plants and can cause 10%e30% yield losses in cotton and several species of fruit trees in China (Liu et al., 2015). Lygus rugulipennis Poppius is widespread in cultivated crops in Europe where it is considered a pest on oats, wheat, strawberries, and sugar beets (Holopainen and Varis, 1991). Lygus pratensis and L. rugulipennis have been found infected by potato stolbur phytoplasma in Czech Republic (Brezíková and Linhartová, 2007) but their vector abilities as well as their pest status in potato are still unknown. In the USA, three species, including the western tarnish plant bug (L. hesperus Knight), the pale legume bug (L. elisus L.), and the tarnished plant bug (L. lineolaris Palisot de Beauvois) are considered economically important pests affecting several agricultural crops. Lygus hesperus and L. elisus are prevalent in western regions of the USA and Canada (Scott, 1977), while L. lineolaris is a major pest in eastern and southern regions of the USA (Tingey and Pillemer, 1977). Below we present a description of the most representative lygus bug pests in potatoes.

9.4.4 Lygus hesperus and L. elisus In the USA Northwest, particularly in the Columbia Basin of Oregon and Washington, L. hesperus and L. elisus often colonized potato fields (Antwi and Rondon, 2019). Lygus bugs can be one of the major limiting factors for local potato producers, potentially affecting yield and quality. Morphological identification of these two species and others belonging to the Lygus genus is not always easy, and molecular tools are often required (Antwi and Rondon, 2019).

9.4.4.1 Biology and ecology Lygus bug adults are 4.4e6.5 mm long, with bodies flattened on the back and a conspicuous triangle corresponding to the scutellum (Mueller et al., 2003). Several characteristics can be used to distinguish between L. hesperus and L elisus adults. Adults of L. hesperus color vary from yellowish to reddish brown, while L. elisus adults are often pale or yellowish green (Hasey et al., 2015). Lygus hesperus are relatively longer in size (5.3e6.5 mm) compared to L. elisus (4.4e5.8 mm) (Mueller et al., 2003), and show several pairs of spots on the pronotum compared to L. elisus, which has a single black spot above each callus. Moreover, L. hesperus wing membrane is tinted black, while the L. elisus has a clear wing membrane (Mueller et al., 2003) (Fig. 9.6). Eggs of both species are creamy white in color, flask shaped, and the wider end presents a flat cap. The eggshell is hardened and smooth (Fig. 9.7). Earlier stages of nymphs (i.e., first and second instar) range in size from 1 to 1.2 mm long, they are pale green in color and appear very similar to aphid nymphs (Zalom et al., 2011) (Fig. 9.7). However, compared to aphids, lygus bug nymphs move faster and have red tips on their antennae. Also, they do not have cornicles which in

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FIG. 9.6 Morphological characteristics to discriminate two common Lygus species presents in potatoes. Lygus hesperus (left) has several pairs of dark spots on pronotum (A); median lines form a deep heart shape on scutellum (B); wing membrane is tinted black (C). Lygus elisus (right) has a single pair of dark spots (a); no median line is formed on scutellum (b); wing membrane is clear (c). Photos: Govinda Shrestha (Oregon State University).

FIG. 9.7 Lygus spp. immature life stages: egg (A), second instar nymph (B), and fourth instar nymph (C). Photos: Govinda Shrestha (Oregon State University).

aphids, are located at the tip of the abdomen. Later nymphal stages (i.e., third to fifth instars) are bright green, and have five black dots on the back; two of those dots are located on the prothorax, two on the mesothorax and one on the abdomen (Zalom et al., 2011) (Fig. 9.7). In the USA Pacific Northwest, lygus bugs overwinter as adults in plant debris, leaf litter, and weedy areas adjacent to crop fields (Fye, 1980). Preferred overwintering hosts of adults include alfalfa, Russian thistle, lambsquarters, pigweed, and wild radish (Fye, 1980). Overwintered adults emerge when air temperature increases above 12.2
C in early spring (Pickel et al., 1990). Shortly after emergence, adults become active, mate close to overwintering sites, and eventually disperse to nearby green weeds and host plants where they immediately lay eggs (Fye, 1980). Eggs are laid into plant tissues flush with the tissue surface, and they hatch within one to 4 weeks, depending on abiotic conditions (Mueller and Stern, 1973; Bommireddy et al., 2004). For instance, the eggs of L. hesperus and L. elisus can hatch in 7 days at 27
C, and in 14 days at 20
C (Mueller and Stern, 1973). There are five nymphal stages, each instar requires 2e6 days to complete, except the fifth instar that requires 4e9 days to complete, depending on abiotic and biotic

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conditions (Mueller and Stern, 1973; Chen and Parajulee, 2010). No significant differences have been reported on total nymphal developmental time between both species (Mueller and Stern, 1973). Newly emerged females begin laying eggs in about 10 days. Lygus hesperus adult female has an average oviposition period of 23 days at optimum temperature (27
C), and lay an average total of 162 eggs throughout their life (Mueller and Stern, 1973). For L. elisus, the adult female has an oviposition period of 15 days; and can lay an average total of 48 eggs throughout their life (Mueller and Stern, 1973). Adults of both species can have an average life span of 30 days. There are two to three overlapping generations during a potato field season. During the fall, when crops are harvested or dried out, lygus bugs move back to any surrounding green area where they may overwinter. Adults will emerge the following spring to continue their life cycle.

9.4.4.2 Damage and pest status Lygus bugs can inflict significant damage to potato plants throughout the growing season. Both nymphs and adults feed on plants by inserting their piercing-sucking mouth parts called stylets into various parts of plants including leaf buds, leaves, stems, and flowers (Antwi et al., 2017). Lygus bugs tend to prefer to feed on the upper foliage of potatoes, leaving much of their damage on terminal leaves. Symptoms of lygus bug damage on potatoes include leaf flagging (leaves shrivel and turn brown or die and finally topple down), abnormal tissue growth resulting in leaf deformation, brown lesions or dead tissue on stems, leaf petioles, and midribs; and occasionally plant sap oozes from the point of feeding (Antwi et al., 2017) (Fig. 9.8). Lygus bug damage is more apparent in JuneeJuly, coinciding with flowering of potato plants in the region.

9.4.4.3 Pest management Yellow sticky traps, sweep nets, and inverted leaf blowers are recommended to scout lygus bugs in potato fields (Antwi and Rondon, 2019). Although preliminary studies show that yellow sticky traps may not be the best approach, they can help determine whether lygus bugs adults are present or not in potatoes, and determine when insects begin to disperse from overwintering sites. An economic threshold for lygus bugs in potatoes has not been firmly established yet. However, Antwi et al. (2017) recommend to monitor lygus bugs in the field to circumvent any potential yield losses due to excessive feeding damage. Scouting in the early stages of potato development is important. This will allow for early pest detection and more effective management. Pesticides are commonly used to control lygus bug populations in other crops such as alfalfa, cotton, and strawberry (Zalom et al., 2011). In the USA Pacific Northwest, potato growers spray pesticides 1e3 times per field season for lygus control. Interestingly, most of the registered pesticides are effective controlling earlier nymphal stages compared to later ones or adults (Zalom et al., 2011; Rondon and Thompson, 2017). Pesticide resistance has been reported in certain

FIG. 9.8 Lygus hesperus feeding damage symptoms on potato. Leaves are shriveled, dead or start to fall from plants; upper foliage is the most damaged part. Photo: Govinda Shrestha (Oregon State University).

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populations of lygus bugs in crops such as cotton, alfalfa hay, and alfalfa seed field (Snodgrass, 1996; Snodgrass and Scott, 2000; Godfrey et al., 2015b). There are no resistance reports in potatoes thus far. Little is known about biological control of lygus bugs in potatoes. Several native and introduced parasitoid species, including an egg endoparasitoid, Anaphes iole Girault (Hymenoptera: Mymaridae), and nymphal endoparasitoids Peristenus howardi Shaw, P. diagoneutis Loan, and P. relictus Ruthe (Hymenoptera: Braconidae) are known to parasitize lygus bugs found in a variety of crops (Conti et al., 1997; Seymour et al., 2005; Pickett et al., 2009). Naturally occurring predators such as big-eyed bugs, damsel bugs, lady bugs, minute pirate bugs, and several species of spiders are known to prey on lygus bug nymphs (Hagler et al., 2018; Zalom et al., 2011). Further studies on biological control in potatoes may help to understand the role of natural enemies in minimizing lygus bug populations in this crop. Cultural practices can help minimize lygus bug populations and damage in a variety of agricultural crops (Stern et al., 1964; Goodell, 2009). Although cultural practices may not be enough in managing economic lygus bug infestations, they can aid in preventing the pest from becoming a serious issue. In potatoes, the effectiveness of cultural practices to reduce or control lygus bugs has not been studied. However, weed management around potato fields (Goodell, 2009; Godfrey et al., 2015b), or strip cutting nearby alfalfa fields are known to minimize the migration of lygus bug populations to neighboring crops and could be incorporated in potato production systems (Stern et al., 1964).

9.5 Conclusion Several groups of hemipterans can potentially affect the potato crop worldwide. The insect pests listed in this chapter are vectors of phytoplasmas or cause feeding damage. The majority of phytoplasma vectors in potatoes are leafhoppers (Deltocephalinae) and planthoppers (Cixidae). However, as different phytoplasmas produce almost identical symptoms, visual symptomatology of infections is not reliable enough for a correct diagnosis; thus, the use of molecular techniques such as polymerase chain reaction (PCR) is essential to detect the causal agent of the phytoplasma disease. Other Hemiptera groups like psyllids and aphids are known to vector other pathogens (bacteria and viruses); separate sections of this book are dedicated to those groups. Among plant feeders affecting potatoes we found leafhoppers (Typhlocybinae) which cause hopperburn, and Heteroptera (true bugs) which cause mechanic damage and early plant decline. Understanding the biology, ecology, insect plant interaction, and how to improve the role of natural enemies can help design better management programs.

Acknowledgments The authors thank Dr. James Crosslin for editing and reviewing this manuscript.

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Vosler, E., 1919. Some work of the insectary division in connection with the attempted introduction of natural enemies of the beet leafhopper. California State Commission of Horticulture. Mon. Bull. 8, 231e239. Wallis, E., 1962. Host plant preference of the six-spotted leafhopper. J. Econ. Entomol. 55, 871e874. Weintraub, P.G., Beanland, L., 2006. Insect vectors of phytoplasmas. Annu. Rev. Entomol. 51, 91e111. Weintraub, P.G., Trivellone, V., Krüger, K., 2019. The biology and ecology of leafhopper transmission of phytoplasmas. In: Phytoplasmas: Plant Pathogenic Bacteria-II. Springer, pp. 27e51. Wene, G., 1958. Control of Nysius raphanus Howard attacking vegetables. J. Econ. Entomol. 51, 250e251. Wenninger, E.J., Rashed, A., Rondon, S.I., Alyokhin, A., Alvarez, J.M., 2020. Insect pests and their management. In: Stark, J.C., Thornton, M., Nolte, P. (Eds.), Potato Production Systems. Springer International Publishing, Cham, pp. 283e345. Wheeler, A.G., 2001. Biology of the Plant Bugs (Hemiptera: Miridae): Pests, Predators, Opportunists. Cornell University Press. Whitworth, R.J., McCornack, B., Davis, H., 2012. False Chinch Bug, Agricultural Experiment Station and Cooperative Extension Service, Kansas. Wilson, M.R., Weintraub, P.G., 2007. An introduction to Auchenorrhyncha phytoplasma vectors. Bull. Insectol. 60, 177. Wilson, S.W., Tsai, J.H., 1982. Descriptions of the immature stages of Myndus crudus (Homoptera: Fulgoroidea: Cixiidae). J. N. Y. Entomol. Soc. 166e175. Wohleb, C.H., Jensen, A., Waters, T., 2010. Sampling Network for Potato Insect Pests in the Columbia Basin of Washington. Poster presented at the Washington State University Academic Showcase, Pullman, WA. Young, O., 1986. Host plants of the tarnished plant bug, Lygus lineolaris (Heteroptera: Miridae). Ann. Entomol. Soc. Am. 79, 747e762. Zalom, F., Jianlong, B., Pat, T., 2011. Managing Lygus Bugs in Strawberries. California Strawberry Comission, Watsonville, CA, pp. 1e6. Zhang, Y., Chen, W., Yang, L., Chen, X., Dong, M., Li, X., 2019. DNA barcoding of genus Empoasca Walsh, 1862 (Hemiptera: Cicadellidae) based on COI gene sequences. Int. J. Agric. Biol. 22, 697e702.

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Chapter 10

Potato ladybirds Andrei Alyokhina and Yulin Gaob, c a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bState Key Laboratory for Biology of Plant Disease and Insect

Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, China; cNational Center of Excellence for Tuber and Root Crops Research, Chinese Academy of Agricultural Science, Beijing, China

10.1 Underappreciated defoliator Lady beetles, also known as lady bugs and ladybird beetles (Coleoptera: Coccinellidae) comprise a relatively large (ca. 6000 described species in 360 genera worldwide) and ubiquitous family of beetles (Escalona et al., 2017; Majerus, 1994). Lady beetles are rather charismatic and well-known to the general public. In part, this is due to the bright aposematic coloration of many species in this family, which makes them easily noticeable. Another contributing factor is the high abundance of some common species. More importantly, members of this group have been recognized as highly beneficial biological control agents that play important roles in suppressing agricultural pests, particularly aphids and other Hemiptera (see Chapters 5, 6, and 13 for more information). Human veneration of lady beetles is quite obvious from the fact that their common names in many languages are dedicated to deities (Exell, 1991). For example, in English the name ladybird refers to Our Lady, The Virgin Mary. In Hebrew, Coccinellidae is called Cow of Moses our Teacher, in HindidIndra’s Cowherd, and in RussiandGod’s Cow. Along the same lines, in Italian (specifically in Genoa region) lady beetles are referred to as Luck Bringers. In Cherokee, lady beetle is referenced as Jaguar Beetle. However, it is considered to be disrespectful to use this name in the presence of an actual lady beetle. Instead, it is referred to as Great Beloved Woman, which is also the title of the highest female-held office in the Traditionalist Native Cherokee Government. Holders of this office wear lady beetle-inspired face paint during official ceremonies (Exell, 1991; Majerus, 1994). As is often the case, however, there are a few “black sheep” in the otherwise highly respectable coccinellid family. Some lady beetles (mostly in subfamily Epilachninae) are phytophagous, and a few of them are important pests of cultivated plants. These include closely related species Henosepilachna (¼Epilachna) vigintioctomaculata (Motschulsky) and H. vigintioctopunctata (Fabricius). These two species are morphologically similar and cannot be easily distinguished from each other without special training. As a result, they share the same common name of a potato ladybird, hadda beetle, or 28-spotted lady beetle. Potato ladybirds can be economically devastating pests of potatoes and other crops. However, most damage is done in Asia. Until recently, most potato pest research published in international journals has been conducted in North America and, to a smaller degree, in Europe. Consequently, historically potato ladybirds received considerably less attention compared to some other potato pests, with an implicit understanding that they are of local importance. This is misleading because both their distribution range and pest status warrant considering them to be major pests of potatoes. Therefore, this book dedicates a separate chapter to these pests.

10.2 Morphology Detailed description of both species is provided by Xu et al. (2013). Potato ladybirds are relatively small (7e8 mm for H. vigintioctomaculata and 5e7.5 mm for H. vigintioctopunctata) beetles that have a characteristic “ladybug” appearance. Adults are hemispherical in shape, yellowish-brown to reddish-brown in color with black spots on pronotae and elytra and covered with dense light-brown hair. Each elytron has 14 spots. Larvae are campodeiform, yellowish-brown in color with black spots, and with prominent dorsal spines. Pupae are exarate and similar to adults in coloration (Fig. 10.1). Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00002-0 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 10.1 Dorsal views of various life stages of Henosepilachna vigintioctopunctata (Fabricius) and H. vigintioctomaculata (Motschulsky).

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Henosepilachna vigintioctomaculata and H. vigintioctopunctata closely resemble each other in appearance. Henosepilachna vigintioctopunctata is slightly smaller, but there is an overlap in the ranges of possible sizes between the two species. Another morphological distinction is arrangement of spots on elytra. In both species, each elytron has 14 spots, three of which are located at its base. The four spots behind them, however, are arranged in a straight line in H. vigintioctopunctata but not in H. vigintioctomaculata. Also, spots at the conjunction of elytra are in contact in H. vigintioctomaculata but do not touch each other in H. vigintioctomaculata. In addition, pronotum in H. vigintioctomaculata has a longitudinal sword-shaped spot in the center and two small spots on each side, which can be combined into one in some individuals. Pronotum in H. vigintioctopunctata, on the other hand, has a horizontal double diamond spot in the center (Xu et al., 2013). Since potato ladybird species are difficult to distinguish based on external morphological characteristics, it is necessary to develop an alternative method that allows rapid and accurate differentiation between them. A recent study established a molecular identification technique using species-specific PCR primers for the mitochondrial cytochrome oxidase I (mtCOI) of the two species. Two pairs of SS-mtCOI primers, Hvp and Hvm, were designed based on sequence variations in the mtCOI gene between H. vigintioctopunctata and H. vigintioctomaculata. This approach was shown to identify H. vigintioctopunctata and H. vigintioctomaculata rapidly, accurately, and sensitively (Guo et al., 2021a).

10.3 Geographic distribution, host range, and taxonomy Ranges of both ladybird species overlap, particularly in China. However, H. vigintioctomaculata inhabits mostly temperate areas of Asia, including China, Japan, Korea, and Russian Federation. Its northern limit correlates with the presence of the broadleaf and mixed forests (Ivanova, 1962), while its southern limit approximately follows the boundary between warm and cool temperate forests (Katakura, 1981). This range continues to expand in northern and western directions (Kovalenko, 2006), possibly due to the climate change. H. vigintioctopunctata, on the other hand, is common in warmer climates of Southeast and South Asia, including Pakistan. It has also been introduced to Australia, New Zealand, several Pacific islands, and South America, where it is of an increasing concern as an agricultural pest (Katakura, 1981; Naz et al., 2012; Xu et al., 2013). Potato ladybirds are considered to be highly polyphagous, with reported feeding on 29 plant species belonging to 13 families (Hoshikawa, 1983; Xu et al., 2013). Among cultivated crops, the most affected plants are in families Solanaceae and Cucurbitaceae (Kovalenko, 2006; Xu et al., 2013). However, high polyphagy may be at least partially explained by potato ladybirds being a group of several currently poorly defined species that are closely related to each other but prefer different host plants. Still, many of these species display at least some degree of polyphagy (Hoshikawa, 1983). Katakura (1973, 1981) suggested the existence of an H. vigintioctomaculata complex that consists of more than 10 forms of closely allied phytophagous ladybirds. These forms differ from each other in morphology and host plant reference and can be possibly arranged in 2e5 separate species (Hoshikawa, 1983; Katakura, 1973, 1981). There is incomplete reproductive isolation between some of these species, with heterospecific hybrids suffering considerably lower egg hatch (Katakura, 1986; Katakura and Nakano, 1979; Katakura and Sobu, 1986). In other species of the complex, there is no intrinsic penalty for interspecific breeding. Some interspecific crosses, however, result in lower survivorship of hybrid larvae on ancestral host plants, indicating ecological reproductive isolation between sympatric species (Kuwajima et al., 2010). Genetic studies confirmed reproductive barriers among the species (Kobayashi et al., 2011). Kobayashi et al. (2000) analyzed partial sequences of mitochondrial cytochrome c oxidase I genes in H. vigintioctopunctata from eight localities in east and southeast Asia and found two genetically distinct groups, which also had distinct karyotypes. Furthermore, there was strong postmating reproductive isolation between the two groups. Virtually none of the eggs hatched when females mated with males from a different group, while 90% or more of eggs hatched when females mated to males from the same group. The authors concluded that what is currently known as H. vigintioctopunctata consists of at least two separate biological species, one of which is found in Japan and Thailand and another one is found in Indonesia. Similarly (Karthika et al., 2017), investigated genetic diversity and intrapopulation polymorphisms of H. vigintioctopunctata from South India, China, Indonesia, and Japan using DNA barcoding and found two genetically distinctive lineages. In addition, high genetic divergences among several haplotype comparisons indicated the influence of microevolutionary pressures. Existence of several additional species within what is currently known as potato ladybirds may have important implications for selecting the right natural enemies for their biological control (see Chapter 13 for a detailed discussion of this approach). Another consideration is designing insecticide resistance management plans, where different plant species may serve as untreated refuges for maintaining overall susceptibility of sympatric beetle populations (see Chapter 24 for

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details). Yet another consideration is that possible differences in phenology or susceptibility to insecticides may require developing region-specific management plans, resulting in additional expenses. Hopefully, as more research efforts are dedicated to studying potato ladybirds, their taxonomy will become more defined.

10.4 Damage Both adults and larvae of potato ladybirds skeletonize potato leaves by removing their parenchyma (Fig. 10.2). Extensively damaged leaves eventually turn yellow, dry up and die (Kovalenko, 2006). In addition, leaf injury may facilitate infections by gray mold, Botrytis cinerea Pers. ex Fr. (Yao et al., 1992). Third and fourth instars are most damaging, although adult feeding can cause considerable damage to small plants early in the season (Kovalenko, 2006). Defoliation by potato ladybirds can have a significant negative impact on potato production, although its extent depends on abiotic conditions, presence of natural enemies, and potato variety (Kovalenko, 2006). In China, yield losses have been estimated to reach 10%e15% in normal years, and 20%e30% in the years of heavy infestation (Song et al., 2008). In Russia, 25% defoliation of potatoes at an early flowering stage resulted in harvesting 5.3e7.4 t fewer tubers per hectare (Kovalenko, 2006). In especially severe cases, complete crop destruction is possible (Jackson, 2016). Sobko et al. (2021) recently reported that 50% of H. vigintioctomaculata collected in or near potato fields in Russian Far East tested positive for Potato virus Y (PVY) using PCR. They suggested that potato ladybirds may serve as vectors of this virus. Mechanic transmission among damaged plants may be indeed important for PVY spread in potatoes (Fageria et al., 2015; MacKenzie et al., 2018). However, (Sobko et al., 2021) did not specifically test PVY transmission from infected to uninfected plants by H. vigintioctomaculata. Therefore, epidemiological importance of potato ladybirds in regard to this virus remains to be determined. More information on this virus and its insect vectors can be found in Chapter 5.

10.5 Biology In addition to morphological resemblance, the two currently described potato ladybird species are also similar ecologically. Their main known differences pertain to Henosepilachna vigintioctopunctata being a more warm-climate species.

10.5.1 Life cycle Potato ladybirds overwinter as adults. Prior to entering diapause, they usually aggregate outside of potato fields and enter shelters, such as rock crevices or hollow tree trunks. Diapause is facultative. Henosepilachna vigintioctomaculata usually

FIG. 10.2 Feeding damage caused by Henosepilachna vigintioctomaculata (Motschulsky).

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has one-two generations in the northern parts of its range and three-four generations in the southern parts (Katakura, 1997; Kovalenko, 2006; Xu et al., 2013). Henosepilachna vigintioctopunctata has three-five generations per year in areas with seasonal climates but can be active year-around in areas with warm winters (Xu et al., 2013). After diapause termination, the beetles colonize their host plants and begin feeding and reproduction. If potatoes are not available at the time of their emergence from the overwintering sites, beetle populations may first build up on wild vegetation and then move into potato fields (Kovalenko, 2006; Xu et al., 2013). Adults mate multiple times, usually on their host plants (Nakano, 1985; Xu et al., 2013). More than half of newly emerging females of H. vigintioctomaculata mate before entering hibernation. After copulation, spermatozoa remain viable and fertile for up to several months (Katakura, 1982). Potato ladybirds usually lay their eggs in clusters of 15e50 on lower leaf surfaces, with lifelong fecundity ranging between 150 and 750. Hatching larvae disperse over short distances and start feeding. There are four instars. Pupation takes place on leaf surfaces. Development rates are dependent on temperature; under typical field conditions, life cycle from a newly laid egg to a reproductive adult is concluded in 30e40 days (Huang et al., 2018; Kovalenko, 2006; Wang et al., 2017). Adult females can live up to 3 months, while adult males can live up to 4 months. Females reproduce for 45e80 days (Huang et al., 2018; Wang et al., 2017). As a result, there is a significant overlap between beetle generations in the field (Kovalenko, 2006; Xu et al., 2013). Adults are capable of flying (Kovalenko, 2006; Xu et al., 2013), but not much scientific information exists on their flight behavior.

10.5.2 Interactions with host plants Potato ladybugs are considered to be highly polyphagous. As discussed above, at least part of such a vast host range can be explained by lumping together several biologically distinct species with somewhat narrower host ranges. However, these species are probably not monophagous, and there are overlaps in the ranges of plants that they utilize. The main host plant of one species may be a secondary host plant of the other species, and different species may even coexist on the same plants (Katakura, 1997). Plants in the family Solanaceae, including potatoes, tomatoes, and eggplants, comprise a major part of potato ladybird diet (Kovalenko, 2006; Xu et al., 2013). Not all host plants are equally suitable for potato ladybirds, as is the case for other polyphagous insect herbivores. Wang et al. (2017) studied demographic parameters of H. vigintioctopunctata on three eggplant, Solanum melongena L., cultivars and on a wild host, Solanum nigrum L, under laboratory conditions. They detected no significant differences among the rates of development of immature stages, durations of oviposition periods, adult longevities, and fecundities of the beetles reared on the eggplants. Survival rates were lower on one of the cultivars compared to another cultivar, but neither of the two was different from the third cultivar. On S. nigrum, the beetles developed quicker and laid more eggs when on eggplants. However, their survivorship was lower than on two of the eggplant cultivars. Kovalenko (2018) screened 13 potato varieties under field conditions. While none of them showed strong resistance to H. vigintioctomaculata, there were significant differences in their colonization by potato ladybirds, defoliation, and yield losses. Early maturing varieties generally suffered heavier damage. Feeding on host plants by potato ladybirds is stimulated by interactions of several chemicals contained in the foliage of their host plants, with synergisms between methyl esters of unsaturated fatty acid and sugars being particularly important (Hori et al., 2011). Fructose, maltose, glucose, and sucrose have been identified as potato ladybird phagostimulants in the foliage of several host plant species. Methyl linoleate and methyl linolenate, on the other hand, did not elicit any responses by themselves, but synergized responses triggered by these sugars (Endo et al., 2004; Hori et al., 2005a,b). Their effects can be also modulated by other compounds. For example, hozuki plant, Physalis alkekengi L., is a host for H. vigintioctopunctata but not for H. vigintioctomaculata. Luteolin 7-O-glucoside contained in the leaves of this plant acted as a feeding stimulant for both species under laboratory conditions. However, P. alkekengi also contained feeding deterrents that overruled phagostimulatory effects of luteolin 7-O-glucoside and caused its rejection by H. vigintioctomaculata (Hori et al., 2005b). Alkaloids a-solanine, a-chaconine, and tomatine are common and abundant in the foliage of H. vigintioctomaculata in the family Solanaceae. They act as feeding deterrents for many insect species, but no such effect was detected for H. vigintioctomaculata. Alkaloids nicotine and capsaicin from nonhost plants, on the other hand, inhibited beetle feeding (Hori et al., 2011). Phytophagous insects often use visual cues for finding their hosts. Little is currently known in this regard for potato ladybirds. Although H. vigintioctomaculata adults exhibited positive phototactic responses in laboratory experiments by Zhou et al. (2015), they did not exhibit any significant sensitivity to green wavelengths. However, those experiments were not specifically designed to test visual attraction of potato ladybirds to host plants. Additional studies are needed before drawing any definite conclusions on this subject.

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Performance to H. vigintioctopunctata is dependent on the nutritional quality of its diet. Maximum development and survival of its larvae was detected when the protein : carbohydrate ratio was 33:20 (Wang et al., 2018). Currently, little is known about secondary plant compounds that may confer plant resistance to potato ladybirds. Host plants have been also shown to affect gut microbiota of H. vigintioctopunctata. Bacterial communities in the beetles fed on Solanum melongena were significantly different from the bacterial communities in the beetles fed on S. nigrum (Lü et al., 2019a). Specific ecological implications of that difference remain unknown at this point.

10.5.3 Abiotic effects Lower developmental thresholds for eggs, larvae, and pupae of H. vigintioctomaculata were determined to be 10, 9.5, and 9 C, respectively, with the accumulation of 69, 239, and 75 -days required to complete these life stages. The supercooling and freezing points of the overwintered adults were 7.52  2.80 C and 5.05  2.85 C, respectively. Temperatures above 27 C inhibited adult reproduction and larval development (Zhang, 1997). However, (Xiong, 1991) reported that a lower threshold of 15 C and 141 -days were necessary for completion of larval stages of H. vigintioctomaculata. The discrepancies in lower thresholds could be possibly explained by methodological differences or geographic variation between the studied populations and should be addressed by further investigations. Kovalenko (2006) reported that larvae completed their development in 24 days at temperatures of 19e20 C, and in 20 days at temperatures of 20e22 C. This is similar to the rates of development reported by both Xiong (1991) and Zhang (1997), but no developmental threshold was determined in that study. For H. vigintioctopunctata, the lower thresholds were 11 C for eggs, 12 C for larvae, and 14.3 C for pupae, while degree-day accumulations for those life stages were 63, 217, and 53, respectively. Developmental rates decreased at temperatures above 30 C (Chen et al., 1989). Temperature, humidity, and precipitation appear to have a significant effect on potato ladybird populations, which is similar to many other insect species. Most currently available information is on of H. vigintioctomaculata. Cold and dry conditions in winter and early spring were reported to cause high mortality of overwintered adults (Cui et al., 2007), while cold late spring delayed their emergence from diapause and colonization of potato fields (Kovalenko, 2006). Frequent light rainfalls, relative humidity greater than 70%, and temperatures of 20e25 C appear to be the most suitable conditions for potato ladybirds during the summer. To the contrary, dry hot weather is detrimental to developing eggs and larvae (Cui et al., 2007; Kovalenko, 2006). In particular, up to 55% of eggs were observe dying in hot dry years (Kovalenko, 2006), which was consistent with laboratory observations that eggs do not hatch when relative humidity is below 50% (Zhang, 1997). On the opposite side of the spectrum, strong rains dislodge eggs and larvae from plants, thus increasing their mortality (Cui et al., 2007).

10.5.4 Natural enemies Potato ladybirds have a generally robust complex of natural enemies, although its size and composition vary among geographic areas and between H. vigintioctomaculata and H. vigintioctopunctata. An array of species attacking potato ladybirds is described in considerable detail in Chapter 13. They include generalist predators that mostly consume eggs and larvae, such as predatory lady beetles (Coleoptera: Coccinellidae), green lacewings (Neuroptera: Chrysopidae), predatory mites (Mesostigmata: Uropodidae) (Kovalenko, 2006) and predatory stinkbugs (Hemiptera: Pentatomidae) (Cheglik, 2018). Potato ladybirds are also susceptible to generalist entomopathogenic fungi, with 3.5%e27% of H. vigintioctomaculata larvae dying from mycosis in potato fields in Russian Far East according to Kovalenko (2006). There are also several species of parasitoids attacking potato ladybirds and, under certain circumstances, responsible for considerable mortality in their populations. For H. vigintioctomaculata, the most important parasitoid appears to be Nothoserphus afissae (Watanabe) (Hymenoptera: Proctotrupidae) that can parasitize up to 98.6% of its larvae (Kovalenko, 2002; Kovalenko et al., 2006; Lee et al., 1988). H. vigintioctopunctata is attacked predominantly by a larval-pupal parasitoid Pediobius foveolatus (Crawford) (Hymenoptera: Eulophidae) that can parasitize as much as 50%e60% of its field populations (Puttarudriah and Krishnamurti, 1952; Venkatesha, 2006). Continuous expansion of Colorado potato beetle’s range in Asia (see Chapter 4) is likely to result in its considerable overlap with the range of H. vigintioctomaculata. Both species are ecologically similar; therefore, they are likely to compete within potato fields. At this point, the outcomes of this competition and their consequences for potato production remain to be seen.

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10.6 Management 10.6.1 Chemical control Potato ladybirds are usually successfully controlled by an array of common broad-spectrum insecticides (Kovalenko, 2006; Xu et al., 2013). Several botanical products, in particular azadirachtin, can be also used for managing these pests (Ghosh and Chakraborty, 2012; Jeyasankar et al., 2014), but are considerably less popular with potato growers than their synthetic counterparts. Unfortunately, undesirable environmental effects of chemical control are well-known, as discussed in Chapter 11. Insecticide resistance does not appear to be a problem for potato ladybirds. It is possible that their ability to colonize a variety of host species creates an unstructured refuge for susceptible individuals, while tendency to aggregate at overwintering sites creates a gene flow between populations exposed to insecticides and unexposed populations. However, polyphagy does not necessarily prevent insecticide resistance (see Chapter 24). It is likely that increasing consolidation and industrialization of potato farming in the areas of potato ladybirds’ distribution will increase selection pressure on their populations, thus increasing the probability of development of resistant populations. Recently, there is considerable interest in developing new insecticides that are effective against potato ladybirds based on dsRNA technology (Lü et al., 2019b, 2020a,b, 2021a,b; Guo et al., 2021b; Wu et al., 2021). This will potentially allow creating custom-made compounds that interfere with the expression of specific genes. At least in theory, such insecticides will be highly effective against target pests while being safe to nontarget organisms, including natural enemies. Detailed discussion of this approach and its applications in managing insect pests of potato is provided in Chapter 12.

10.6.2 Biological control As discussed above and in Chapter 13, potato ladybirds are affected by multiple natural enemies. Under favorable conditions, they can keep ladybird populations under economic threshold and eliminate the necessity to apply additional control measures (Kovalenko, 2006; Puttarudriah and Krishnamurti, 1952; Venkatesha, 2006). Unfortunately, this is not always the case and careful monitoring of ladybird populations is highly advisable to prevent losses. When natural enemy impact is not sufficient for preventing crop losses, it may sometimes be enhanced through several conservation practices. Avoiding excessive chemical use, especially that involving broad-spectrum active ingredients, is a simple way to boost natural enemy populations in potato fields that has been recommended to improve biological control of potato ladybirds (Puttarudriah and Krishnamurti, 1952; Wang et al., 1998). However, selective insecticides that kill potato ladybirds but not their predators or parasitoids are currently lacking (Chapter 13). Hopefully, this will be addressed through developing active ingredients based on dsRNA (Chapter 12), but no such product is currently available to potato growers. Supplying additional resources, in particular nectar-producing plants, is another approach to improving natural enemy well-being. Providing carbohydrates almost quadrupled life expectancy of an important parasitoid N. afissae and resulted in ca. three-fold increase in its fecundity (Kovalenko, 2006). The best results were achieved using the nectar extracted from buckwheat plants. Potato ladybirds can be also controlled by releasing natural enemies reared in insectaries. Technology for mass production of P. foveolatus has been developed in the United States, where this parasitoid is used against the Mexican bean beetle, Epilachna varivestis Mulsant, and is commercially available from several insectaries (Chapter 13). Technology for captive breeding of N. afissae has been developed in Russian Federation, and subsequent inoculative field releases of this parasitoid early in the growing season showed good potential for controlling H. vigintioctomaculata (Kovalenko, 2002, 2006; Kovalenko et al., 2006). However, that technology has not been yet commercialized and applied on a large scale. Entomopathogenic fungi Beauveria bassiana and Metarrhizium anisopliae have been suggested as another option for biological control of potato ladybirds (Vishwakarma et al., 2011). Kovalenko (2006) reported that applications of B. bassiana reduced populations of H. vigintioctomaculata by no more than 54%. However, low efficacy could have been explained by hot and dry weather during the trials (Kovalenko, 2006). Strategies for optimizing the use of entomopathogenic fungi are discussed in Chapter 13.

10.6.3 Host plant resistance As discussed above, there were differences in potato ladybird performance on different varieties of eggplant (Wang et al., 2017) and potato (Kovalenko, 2018), although all of them remained ultimately susceptible to ladybird defoliation. This suggests existence of genetic variation in host plants that can be possibly used for breeding ladybird-resistant germplasm.

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Approaches to developing insect-resistant potato varieties are discussed in Chapter 14. Currently, no commercial potato varieties are specifically resistant to potato ladybirds. This may change as potato breeding programs in the areas affected by potato ladybirds become better equipped and more sophisticated. Also, some potato varieties developed to be resistant against the Colorado potato beetle may be resistant against potato ladybirds because of their ecological similarities (Fasulati et al., 2011).

10.6.4 Other methods Practicing good sanitation by destroying potato vines after harvest significantly increases mortality of resident potato ladybirds by depriving them of food (Jackson, 2016; Xu et al., 2013). Also, overwintering aggregations can be discovered and manually destroyed (Xu et al., 2013).

10.7 Conclusions and future directions Although common and often causing considerable damage, potato ladybirds are the least studied of all major pests of potatoes. This can be explained in part by their being distributed in regions that were historically outside of the main research foci in potato entomology, and in part by somewhat lower crop losses compared to other major pests. With the increasing consolidation and technical sophistication of potato production in Asia, the situation is likely to change. It is reasonable to expect a significant increase in the number of publications in international peer-reviewed journals dedicated to these species. Also, novel insecticides based on dsRNA technology will probably appear on the market, biological control will become more prominent, and breeding programs will develop traits against potato ladybirds.

References Cheglik, L.G., 2018. Use of Picromerus bidens L. as an agent of biological control of potato beetle Epilachna vigintioctomaculata Motsch. In: Biological Protection of Plantsdthe Basis for Stabilizing Agroecosystem. September 11e13. Krasnodar, Russian Federation, pp. 304e306. Chen, L.F., Lu, Z.Q., Zhu, S.D., 1989. Biology and effective accumulated temperature of Henosepilachna vigintioctopunctata. Plant Prot. 15, 7e8. Cui, N.Z., Bai, X.E., Gao, Y.C., Han, Y.G., 2007. Infection law and the control of 28-star ladybird in potato. J. Shangxi Agric. Sci. 35, 77e79 (in Chinese). Endo, N., Abe, M., Sekine, T., Matsuda, K., 2004. Feeding stimulants of Solanaceae-feeding lady beetle, Epilachna vigintioctomaculata (Coleoptera: Coccinellidae) from potato leaves. Appl. Entomol. Zool. 39, 411e416.  nski, A., Escalona, H.E., Zwick, A., Li, H.S., Li, J., Wang, X., Pang, H., Hartley, D., Jermiin, L.S., Nedved, O., Misof, B., Niehuis, O., Slipi Tomaszewska, W., 2017. Molecular phylogeny reveals food plasticity in the evolution of true ladybird beetles (Coleoptera: Coccinellidae: Coccinellini). BMC Evol. Biol. 17, 151. https://doi.org/10.1186/s12862-017-1002-3. Exell, A.W., 1991. The History of the Ladybird, Second. ed. Erskine Press, Norfolk, U.K. Fageria, M., Nie, X., Gallagher, A., Singh, M., 2015. Mechanical transmission of potato virus Y (PVY) through seed cutting and plant wounding. Am. J. Potato Res. 92, 143e147. Fasulati, S.R., Limantseva, L.A., Ivanova, O.V., Rogozina, E.V., 2011. Integrated resistance of potato to Colorado potato beetle, potato ladybird, and golden nematode. Plant Protect. Q. 10, 14e17 (in Russian). Ghosh, S.K., Chakraborty, G., 2012. Integrated field management of Henosepilachna vigintioctopunctata (Fabr.) on potato using botanical and microbial pesticides. J. Biopestic. 5S, 151e154. Guo, M.J., Lin, M.J., Pan, G., Yu, J.Q., Guo, W., Zhang, Y., Yang, C., Qiu, B., Zhou, X.G., Pan, H.P., 2021a. Rapid identification of Henosepilachna vigintioctopunctata and Henosepilachna vigintioctomaculata based on species-specific mitochondrial cytochrome oxidase I primers. J. South China Agr. Uni. 43, 59e66 (in Chinese). Guo, W., Guo, M.J., Yang, C., Liu, Z.Q., Chen, S.M., Lü, J., Qiu, B., Zhang, Y., Zhou, X.G., Pan, H.P., 2021b. RNAi-mediated silencing of vATPase subunits A and E affect survival and development of the 28-spotted ladybeetle, Henosepilachna vigintioctopunctata. Insect Sci. 00, 1e12. https:// doi.org/10.1111/1744-7917.12899. Hori, M., Ohkawara, Y., Nagamine, J., Tanaka, T., Matsuda, K., 2005a. Feeding stimulation of nutrient chemicals to Epilachna vigintioctopunctata and E. vigintioctomaculata. Tohoku Kontyû 43, 1e4 (in Japanese). Hori, M., Araki, Y., Sugeno, W., Usai, Y., Matsuda, K., 2005b. Luteolin 7-O-glucoside in hozuki leaves, Physalis alkekengi, is involved in feeding stimulation in Epilachna vigintioctopunctata. Jpn. J. Appl. Entomol. Zool. 49, 251e254 (in Japanese). Hori, M., Nakamura, H., Fujii, Y., Suzuki, Y., Matsuda, K., 2011. Chemicals affecting the feeding preference of the Solanaceae-feeding lady beetle Henosepilachna vigintioctomaculata (Coleoptera: Coccinellidae). J. Appl. Entomol. 135, 121e131. Hoshikawa, K., 1983. Host-race formation and speciation in the Henosepilachna vigintioctopunctata complex (Coleoptera, Coccinellidae) I. Host-plant ranges and food-preference types. Kontyu 51, 254e264.

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Huang, H.-W., Chi, H., Smith, C.L., 2018. Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. J. Econ. Entomol. 111, 1e9. Ivanova, A.N., 1962. Potato Lady Beetle in Far East. Nauka, Vladivostok, Russian Federation. Jackson, G., 2016. Potato Ladybird Beetle (255). Pacific Pests and Pathogens Fact Sheet. PestNet, Queensland, Australia. Jeyasankar, A., Premalatha, S., Emulai, K., 2014. Antifeedant and insecticidal activities of selected plant extracts against Epilachna beetle, Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae). Adv. Entomol. 2, 14e19. Karthika, P., Vadivalagan, C., Krishnaveni, N., Murugan, K., Nicoletti, M., Canale, A., Benelli, G., 2017. Contrasting genetic diversity and intrapopulation polymorphism of the invasive pest Henosepilachna vigintioctopunctata (Coleoptera, Coccinellidae): a DNA barcoding approach. J. Asia Pac. Entomol. 20, 23e29. Katakura, H., 1973. Variation analysis of elytral maculation in Henosepilachna vigintioctomaculata complex (Coleoptera, Coccinellidae). J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 19, 445e455. Katakura, H., 1981. Classification and evolution of the phytophagous ladybirds belonging to Henosepilachna vigintioctomaculata complex (Coleoptera, Coccinellidae). J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 22, 301e378. Katakura, H., 1982. Long Mating Season and its Bearing on the Reproductive Isolation in a Pair of Sympatric Phytophagous Ladybirds (Coleoptera, Coccinellidae), vol. 50. Kontyû, Tokyo, pp. 599e603. Katakura, H., 1986. Evidence for the incapacitation of heterospecific sperm in the female genital tract in a pair of closely related ladybirds (Insecta, Coleoptera, Coccinellidae). Zool. Sci. 3, 115e121. Katakura, H., 1997. Species of Epilachna ladybird beetles. Zool. Sci. 14, 869e881. Katakura, H., Nakano, S., 1979. Preliminary experiments on the crossing between two puzzling phytophagous ladybirds, Henosepilachna vigintioctomaculata and H. pustulosa (Coleoptera). Kontyû, Tokyo 47, 176e184. Katakura, H., Sobu, Y., 1986. Cause of low hatchability by the interspecific mating in a pair of sympatric ladybirds (Insecta, Coleoptera, Coccinellidae): incapacitation of alien sperm and death of hybrid embryos. Zool. Sci. 3, 315e322. Kobayashi, N., Kumagai, M., Minegishi, D., Tamura, K., Aotsuka, T., Katakura, H., 2011. Molecular population genetics of a host-associated sibling species complex of phytophagous ladybird beetles (Coleoptera: Coccinellidae: Epilachninae). J. Zool. Syst. Evol. Res. 49, 16e24. Kobayashi, N., Shirai, Y., Tsurusaki, N., Tamura, K., Aotsuka, T., Katakura, H., 2000. Two cryptic species of the phytophagous ladybird beetle Epilachna vigintioctopunctata (Coleoptera: Coccinellidae) detected by analyses of mitochondrial DNA and karyotypes, and crossing experiments. Zool. Sci. 17, 1159e1166. Kovalenko, T.K., 2002. Ecology of Nothoserphus afissae (Watanabe) (Hymenoptera, Proctotrupidae), a parasite of potato ladybird Henosepilachna vigintioctomaculata Motschulsky (Coleoptera, Coccinellidae) in Primorskii Krai. Readings Mem. A.I. Kurentsov 12, 38e42 (in Russian). Kovalenko, T.K., 2006. Biology of Potato Ladybird, Henosepilachna Vigintioctomaculata (Coleoptera) and its Parasitoid Nothoserphus Afissae (Hymenoptera) in Maritime Krai. Ph.D. Dissertation. Biological and Soil Institute, Far Eastern Division of the Russian Academy of Sciences, Vladivostok, Russian Federation (in Russian). Kovalenko, T.K., 2018. Resistance of potato varieties to the potato ladybird Henosepilachna vigintioctomaculata (Motsch.). Far East. Agrar. News 48, 83e88 (in Russian). Kovalenko, T.K., Potemkina, V.I., Kuznetsov, V.N., 2006. Promising natural enemy of potato ladybird in Primorskii Krai. Zaschita Rastenii 10, 22e24 (in Russian). Kuwajima, M., Kobayashi, N., Katoh, T., Katakura, H., 2010. Detection of ecological hybrid inviability in a pair of sympatric phytophagous ladybird beetles (Henosepilachna spp.). Entomol. Exp. Appl. 134, 280e286. Lee, J., Reed, D.K., Lee, H., Carlson, R.W., 1988. Parasitoids of Henosepilachna vigintioctomaculata (Moschulsky) (Coleoptera: Coccinellidae) in Kyonggido area, Korea. Kor. J. Appl. Entomol. 27, 28e34. Lü, J., Guo, W., Chen, S., Guo, M., Qiu, B., Yang, C., Lian, T., Pan, H., 2019a. Host plants influence the composition of the gut bacteria in Henosepilachna vigintioctopunctata. PLoS One 14, e0224213. https://doi.org/10.1371/journal.pone.0224213. Lü, J., Liu, Z., Guo, W., Guo, M., Chen, S., Li, H., Yang, C., Zhang, Y., Pan, H., 2019b. Feeding delivery of dsHvSnf7 is a promising method for management of the pest Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae). Insects 11, 34. https://doi.org/10.3390/insects11010034. Lü, J., Guo, M., Chen, S., Noland, J.E., Guo, W., Sang, W., Qi, Y.X., Qiu, B.L., Zhang, Y.J., Yang, C.X., Pan, H.P., 2020a. Double-stranded RNA targeting vATPase B reveals a potential target for pest management of Henosepilachna vigintioctopunctata. Pestic. Biochem. Physiol. 165, 104555. https://doi.org/10.1016/j.pestbp.2020.104555. Lü, J., Guo, W., Chen, S., Guo, M., Qiu, B., Yang, C., Zhang, Y., Pan, H., 2020b. Double-stranded RNAs targeting HvRPS18 and HvRPL13 reveal potential targets for pest management of the 28-spotted ladybeetle, Henosepilachna vigintioctopunctata. Pest Manag. Sci. 76, 2663e2673. Lü, J., Guo, W., Guo, M., Chen, S., Yang, C., Zhang, Y., Pan, H.P., 2021a. Oral delivery of dsHvlwr is a feasible method for management of the pest Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae). Insect Sci. 28, 509e520. Lü, J., Yang, C., Liu, Z.Q., Vélez, A.M., Guo, M., Chen, S., Qiu, B.L., Zhang, Y.J., Zhou, X.G., Pan, H.P., 2021b. Dietary RNAi toxicity assay suggests a and g subunits of HvCOPI as novel molecular targets for Henosepilachna vigintioctopunctata, an emerging coccinellid pest. J. Pest. Sci. 94, 1473e1486. MacKenzie, T.D.B., Arju, I., Gallagher, A., Nie, X., Singh, M., 2018. Evidence of Potato virus Y spread through post-emergence management practices in commercial potato fields. Am. J. Potato Res. 95, 720e728.

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Majerus, M.E.N., 1994. Ladybirds. HarperCollins, London. Nakano, S., 1985. Effect of interspecific mating on female fitness in two closely related ladybirds (Henosepilachna). Kontyu 53, 112e119. Naz, F., Inayatullah, M., Rafi, M.A., Ashfaque, M., Ali, A., 2012. Henosepilachna vigintioctopunctata (Fab.) (Epilachninae; Coccinellidae); its taxonomy, distribution and host plants in Pakistan. Sarhad J. Agric. 28, 421e427. Puttarudriah, M., Krishnamurti, B., 1952. Problem of Epilachna control in Mysore. Insecticidal control found inadvisable when natural incidence of parasites is high. Indian J. Entomol. 16, 137e141. Sobko, O.А., Matsishina, N.V., Fisenko, P.V., Kim, I.V., Didora, A.S., Boginskay, N.G., Volkov, D.I., 2021. Viruses in the agrobiocenosis of the potato fields. IOP Conf. Ser. Earth Environ. Sci. 677, 052093. Song, G.H., Wu, W.W., Zhao, Q.L., 2008. Quarantine law and the control of 28-spot ladybird. Jilin Veg 1, 50 (in Chinese). Venkatesha, M.G., 2006. Seasonal occurrence of Henosepilachna vigintioctopunctata (F.) (Coleoptera: Coccinellidae) and its parasitoid on Ashwagandha in India. J. Asia Pac. Entomol. 9, 265e268. Vishwakarma, R., Prasad, P., Ghatak, S., Mondal, S., 2011. Bio-efficacy of plant extracts and entomopathogenic fungi against epilachna beetle, Henosepilachna vigintioctopunctata (Fabricius) infesting bottle gourd. J. Insect Sci. 24, 65e70. Wang, G., Li, H., Sheng, J., 1998. Effects of insecticides on Henosepilachna vigintioctopunctata and its larval parasite, Pediobius foveolatus. Nat. Enemies Insects 20, 164e168. Wang, Z.-L., Li, C.-R., Yuan, J.-J., Li, S.-X., Wang, X.-P., Chi, H., 2017. Demographic comparison of Henosepilachna vigintioctopunctata (F.) (Coleoptera: Coccinellidae) reared on three cultivars of Solanum melongena L. and a wild hostplant Solanum nigrum L. J. Econ. Entomol. 110, 2084e2091. Wang, Z.-L., Wang, X.-P., Li, C.-R., Xia, Z.-Z., Li, S.-X., 2018. Effect of dietary protein and carbohydrates on survival and growth in larvae of the Henosepilachna vigintioctopunctata (F.) (Coleoptera: Coccinellidae). J. Insect Sci. 18, 3. https://doi.org/10.1093/jisesa/iey067. Wu, J., Mu, L., Kang, W., Ze, L., Shen, C., Jin, L., Anjum, A.A., Li, G., 2021. RNA interference targeting ecdysone receptor blocks the larvalepupal transition in Henosepilachna vigintioctopunctata. Insect Sci. 28, 419e429. Xiong, J., 1991. Study on the development threshold temperature and the effective accumulated temperature of 28-spot ladybird. Chinese Potato J 5, 175e178. Xu, J., Liu, N., Zhang, R., 2013. Other pestsdChina. In: Giordanengo, P., Vincent, C., Alyokhin, A.V. (Eds.), Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Oxford, UK, pp. 193e226. Yao, X.L., Li, C.Q., Gao, Z.L., Lu, H.M., Lan, L., Liu, H., 1992. Preliminary observations on biology of potato ladybird. J. Shaanxi Agric. Sci. 5, 28e29 (in Chinese). Zhang, Z.Y., 1997. Effects of temperature and humidity on the development of 28-spot ladybird Henosepilachna vigintioctomaculata (Coleoptera, Coccinellidae). Acta Agric. Sin. 6, 30e34 (in Chinese). Zhou, J., Xu, R., Chen, Z., Jia, Y., Xu, K., 2015. Phototactic behavior of Henosepilachna vigintioctomaculata Motschulsky (Coleoptera: Coccinellidae). Coleopt. Bull. 69, 806e812.

Part III

Management approaches

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Chapter 11

Chemical control Thomas P. Kuhar, Christopher Philips, Anna Wallingford, John D. Aigner and Adam Wimer Department of Entomology, Virginia Tech, Blacksburg, VA, United States

11.1 Introduction For more than a century, chemical control has been one of the most widely-used pest management tactics in potato production. Although environmental and human safety concerns have influenced the registration status of many insecticides around the world, and effective non-chemical strategies have been identified for most pests (see other chapters in this book), chemical control still remains one of the most widely-used strategies for eliminating crop damage by arthropod pests, and will likely remain the base of pest management for the foreseeable future (Alyokhin, 2009). In this chapter we will review where we’ve been and where we are present day with the use of insecticides in potato production.

11.2 Early history of chemical control in potatoes In North America and Europe, chemical control in potatoes has largely been driven by the pest management challenges brought on by the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). This insect species greatly impacted the history of insecticide use in potatoes and agriculture in general. Gauthier et al. (1981) provides a very good review of the early history of chemical control in potatoes. In the 19th Century, the aceto-arsenite of copper called Paris Green was first used to control Colorado potato beetle (Riley, 1871), and other types of arsenical compounds such as lead arsenate and calcium arsenate would continue to be used for its control into the 1940s (Gauthier et al., 1981). However, arsenical insecticides were difficult to mix, difficult to apply effectively, did not have a long residual on plants, and sometimes caused phytotoxicity. Thus, alternatives to arsenicals were sought for use in potatoes throughout the early 1900s. Botanical insecticides such as veratrine alkaloids from Sabadilla, ryania extract, and rotenone were evaluated for the control of Colorado potato beetle (Brown, 1951). Although rotenone demonstrated sufficient efficacy against Colorado potato beetle, the focus on botanical insecticides as a replacement for arsenicals would soon be overshadowed as the “Age of Pesticides” began in the 1940s following the invention of synthetic pesticidal compounds that relied on organic molecules as active ingredients (Metcalf, 1980).

11.3 The pesticide treadmill The pesticide treadmill is a commonly used term that refers to the necessity for constant replacement of active ingredients that have failed due to the development of resistance in populations of target pests with new chemicals. Just as with real treadmills, the end result is that a vast amount of effort leads to no actual movement forward (Alyokhin et al., 2015). Evolutionary mechanisms of this phenomenon are discussed in Chapter 24. The mistakes and risks of indiscriminate and excessive use of insecticides could not have been more clearly demonstrated than it was with the Colorado potato beetle in the U.S. by 1990 (Casagrande, 1987). Over a 40-year span in the U.S., Colorado potato beetle would develop resistance to all classes of insecticides. Many potato growers had to change insecticides every few years as well as tank mix multiple compounds for a single spray application (Casagrande, 1987). By 1990, it was reported that Colorado potato beetle had developed resistance to over 25 insecticides from all major classes of insecticides (Forgash, 1985; Harris and Turnbull, 1986; Roush et al., 1990; Tisler and Zehnder, 1990; French et al., 1992; Grafius and Bishop, 1996). By 2008, that number doubled (Alyokhin et al., 2008a). In certain potato-producing areas of Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00007-X Copyright © 2022 Elsevier Inc. All rights reserved.

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the eastern U.S., there were time periods when growers were running out of effective insecticide options for Colorado potato beetle. Multiple mechanisms for resistance have been identified in Colorado potato beetle, including target site insensitivity, enhanced metabolic enzyme activity, reduced insecticide penetration, and increased excretion (Rose and Brindley, 1985; Ioannidis et al., 1991; Argentine et al., 1994; Wierenga and Hollingworth, 1994; Alyokhin et al., 2008a). In addition to resistance problems in Colorado potato beetle, the frequent applications of these broad-spectrum insecticides decimated natural enemy populations resulting in pest resurgences and outbreaks of secondary pests (Metcalf, 1980). Moreover, insecticide resistance to chlorinated hydrocarbons, carbamates, organophosphates, and pyrethroids also occurred in other potato pests including green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), and beet armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), among others (Penman and Chapman, 1988; Brewer and Trumble, 1994; Kerns et al., 1998; Foster et al., 2007; Castañeda et al., 2011). Regardless past failures, the conventional control strategy today for Colorado potato beetle has not changed. Chemical control is the primary tool used, and very little regard is given to integrated pest management (Alyokhin, 2009). Over the past 2 decades, there has been a major shift in insecticide development to more targeted or narrow spectrum insecticides with novel mode of actions. These new insecticides are often less toxic to non-target species, and the environment and compared to carbamates, organophosphates, and pyrethroids. While some of the older chemicals are no longer available, in the U.S. there are over 30 insecticides from at least 15 different IRAC groups currently registered for Colorado potato beetle control on potatoes (Alyokhin et al., 2008a), and even more are in development or are currently in the registration process (Table 11.1).

11.3.1 Chlorinated hydrocarbons In the 1940s, Colorado potato beetle was one of the first agricultural targets for the chlorinated hydrocarbon insecticide, DDT, and it also became one of the first pests to develop resistance to the chemical in the U.S. during the 1950s (Hofmaster, 1956). Other chlorinated hydrocarbons (mostly cyclodienes) including aldrin, dieldrin, endrin, heptachlor, methoxychlor, endosulfan, and others would be widely used on potatoes, but Colorado potato beetle quickly developed resistance to those insecticides as well (Gauthier et al., 1981; Alyokhin et al., 2008a). Nonetheless, the long residual activity of these insecticides in the soil made them ideal for control of subterranean pests of potatoes such as wireworms (Coleoptera: Elateridae) (Merrill, 1952; Gunning and Forrester, 1984; Parker and Howard, 2001). Cyclodienes would be used on potatoes until most agricultural uses would eventually be canceled (in the U.S. by 1980) because of the persistence of these compounds in the environment, resistance that developed in several insect pests, and biomagnification in some wildlife food chains (Ware and Whitacre, 2004).

11.3.2 Organophosphates and carbamates Gradually, carbamates and organophosphates replaced the chlorinated hydrocarbons in potato production. These cholinesterase-inhibiting neurotoxins have broad-spectrum activity against most insect pests attacking potatoes. In addition, the systemic activity of many of these compounds including aldicarb, disulfoton, fensulfothion, carbofuran, phorate, and oxamyl introduced insecticides that could be absorbed into growing plant parts via soil application. This enabled longer residual activity of the chemical and, in theory, the need for fewer foliar insecticide sprays (Gauthier et al., 1981). However, Colorado potato beetle would eventually develop resistance and cross resistance to carbamates and organophosphates, rendering virtually all insecticides in these two classes practically useless against this pest (Casagrande, 1987). Nonetheless, a few carbamates and organophosphates are still widely used today in commercial potato production; oxamyl and dimethoate are listed among the top five insecticides in total amount of active ingredient applied to potatoes in the U.S (USDA NASS, 2014). These insecticides are generally not applied for Colorado potato beetle control, but rather for control of plant parasitic nematodes and wireworms in the soil, and for control of aphids, potato psyllids, and potato tuberworms.

11.3.3 Pyrethroids In the 1970s, the first synthetic pyrethroid insecticides fenvalerate and permethrin were registered on potatoes in the U.S. Modeled after the plant-derived pyrethrins, these insecticides offered a similar mode of action as DDT, modulating the sodium channel on neuronal membranes (Ware and Whitacre, 2004). Throughout the 1970s until the 1990s, a number of pyrethroid insecticides would be registered throughout the world (Table 11.1). These insecticides were shown to be active on a broad range of insect pests, were efficacious at extremely low use rates, and typically did not breakdown quickly in

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203

TABLE 11.1 Insecticides and miticides currently registered for use on potatoes in the U.S. as of 2020. All products are not registered for use in all states. IRAC classification numbera

Group

Mode of action

Insecticide(s)

1A

Carbamate

Acetylcholine esterase inhibitor (reversible)

Carbaryl Methomyl Oxamyl

1B

Organophosphate

Acetylcholine esterase inhibitor (irreversible)

Dimethoate Ethoprop Malathion Phorate Phosmet

2B

Phenylpyrazoles

GABA-gated chloride channel blocker

Fipronil

3A

Pyrethroids

Sodium channel modulator

Beta-cyfluthrin Bifenthrin Cyfluthrin Esfenvalerate Lambda-cyhalothrin Permethrin Zeta-cypermethrin

4A

Neonicotinoid

Nicotinic acetylcholine receptor competitive modulator

Acetamiprid Clothianidin Dinotefuran Imidacloprid Thiamethoxam

4C

Sulfoximines

Sulfoxaflor

4D

Butenolides

Flupyradifurone

5

Spinosyns

Nicotinic acetylcholine receptor allosteric modulator - site I

Spinetoram Spinosad

6

Avermectins

Glutamate-geated chloride channel allosteric activator

Abamectin

7C

e

Juvenile hormone mimic

Pyriproxyfen

8C

Fluorides

Miscellaneous non-specific (multi-site) inhibitor

Cryolite

9B

Pyridine azomethine derivatives

Chordotonal organ TRPV channel modulator

Pymetrozine Pyrifluquinazon

9D

Pyropenes

Afidopyropen

10A

e

Mite growth inhibitor affecting CHS1

Hexythiazox

11A

None

Microbial disruptors of insect midgut membranes

Bacillus thuringiensis var. tenebrionensis Bacillus thuringiensis var. kurstaki Continued

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TABLE 11.1 Insecticides and miticides currently registered for use on potatoes in the U.S. as of 2020. All products are not registered for use in all states.dcont’d IRAC classification numbera

Group

Mode of action

Insecticide(s)

12C

e

Inhibitors of mitochondrial ATP synthase

Propargite

15

Benzoylureas

Inhibitors of chitin biosynthesis affecting CHS1

Novaluron

17

e

Molting disruptor, dipteran

Cyromazine

20D

e

Mitochondral complex III electron transport inhibitor

Bifenazate

21A

METI acaricides and insecticides

Mitochondral complex I electron transport inhibitor

Tolfenpyrad

22A

None

Voltage-dependent sodium channel blocker

Indoxacarb

23

Tetronic and tetramic acid derivaties

Inhibitors of acetyl CoA carboxylase

Spiromesifen

Diamide

Ryanodine receptor modulator

28

Spirotetramat Chlorantraniliprole Cyantraniliprole Cyclaniliprole

29

e

Chordotonal organ modulator - undefined target site

Flonicamid

UNE

e

Botanical essence - unknown MoA

Chenopodium extract

UN

e

Unknown or uncertain MoA

Azadirachtin

a

Insecticide Resistance Action Committee (IRAC) mode of action classification is the definitive global authority on the target site of insecticides.

sunlight like natural pyrethrins. However, because the mode of action of pyrethroids is similar to that of DDT (Ware and Whitacre, 2004), Colorado potato beetle quickly developed resistance to this insecticide class (Casagrande, 1987; Tisler and Zehnder, 1990; Alyokhin et al., 2008a).

11.3.4 Neonicotinoids Neonicotinoids are also referred to as nitro-quanidines, neonicotinyls, nicotinoids, chloronicotines, and chloronicotinyls. The first neonicotinoid insecticide, imidacloprid, was introduced in Europe and Japan in 1990, and was registered on potatoes in the U.S. in 1996. Other neonicotinoids, including thiamethoxam, acetamiprid, dinotefuran, and clothianidin were registered a few years later. Since that period, these chemicals have been the most commonly-used insecticides on potatoes for control of Colorado potato beetle as well as other insect pests including leafhoppers, potato psyllids, aphids, and flea beetles. Neonicotinoids are neurotoxins that target the nicotinic acetylcholine receptor (nAChR) acting as agonists (Maienfisch et al., 2001; Matsuda et al., 2020). Although they are effective as contact insecticides, it is the ability of these chemicals to translocate from the soil into the plant as systemic insecticides that has been one of the primary reasons for their popularity. Most commercial potato growers apply these chemicals in the seed furrow at planting or as a pre-planting treatment to seed pieces. Both application methods provide long-term systemic protection to the potato plant against Colorado potato beetle (Boiteau et al., 1997; Kuhar et al., 2003b, 2007; Kuhar and Doughty, 2018), and sucking pests such as leafhoppers, aphids and psyllids (Boiteau et al., 1997; Pavlista, 2002; Kuhar and Speese, 2005b, 2005c). Neonicotinoids also provide efficacy against wireworms in the soil (Kuhar et al., 2003a; Kuhar and Alvarez, 2008). Currently, neonicotinoid insecticides represent the foundation for insect control in most potato-growing regions (USDA NASS, 2014). Field dissipation rates for neonicotinoids are variable. For example, the half-life for imidacloprid has been reported to be as short as 60 days (Liu et al., 2011) or as long as 280 days in field soils (Saran and Kamble, 2008). The half-life for thiamethoxam is much shorter and ranges from 9 days in field soils (Karmakar and Kulshrstha, 2009) and up to 75 days in lab soils (Maienfisch et al., 2001). Field efficacy trials conducted on sandy loam soils in Virginia (USA) in the early 2000s

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TABLE 11.2 Counts of Colorado potato beetle (CPB) larvae at 64 days after planting (DAP) and potato leafhopper (PLH) nymphs at 79 DAP on potatoes with seed (ST) or in-furrow (IF) treatments of various neoneonicotinoid insecticides in a small-plot field experiment conducted in Painter, Virginia (USA), AprileJuly 2003. Treatment

Rate kg AI/ha

Untreated control

No. CPB larvae/10 stems

No. PLH nymphs/10 leaves

66.0 a

51.0 a

Thiamethoxam (IF)

0.11

0.0 b

0.0 b

Imidacloprid (IF)

0.28

0.0 b

0.0 b

Imidacloprid (ST)

0.14

0.0 b

1.0 b

Imidacloprid (ST)

0.28

0.0 b

0.0 b

Clothianidin (ST)

0.17

0.0 b

0.0 b

Clothianidin (ST)

0.22

0.0 b

0.0 b

Numbers within a column with a letter in common are not significantly different according to analysis of variance followed by Fisher’s protected LSD to separate means.

showed that imidacloprid, thiamethoxam, or clothianidin applied to potato seed pieces at planting provided effective control of both Colorado potato beetle and potato leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae), for more than 60 days after planting (Table 11.2). Soil type, pH, groundcover, cultivation (i.e., exposure to sunlight), moisture, temperature, and microbial communities present all play a role in the residual life of an insecticide in the soil. Both imidacloprid and thiamethoxam are stable in neutral and acidic water, although these compounds will slowly degrade in basic solutions (Liu et al., 2006). Soil-dwelling microorganisms have been described that degrade imidacloprid and thiamethoxam (Anhalt et al., 2007; Pandey et al., 2009). Baer-ground soils will see longer half-lives for imidacloprid than soils with groundcover (Scholz and Spiteller, 1992), likely due to higher populations of those microorganisms in soils with growing vegetation. Higher levels of organic matter in the soil make for longer half-life as sorption of imidacloprid increases as organic carbon content increases (Cox et al., 1997, 1998); thereby, decreasing the bioavailability to microorganisms that degrade the compound. Concerns regarding the environmental persistence of neonicotinoids and adverse effects on non-target organisms, have grown over the use of these chemistries (Cressey, 2017). Pollinating insects can be exposed to potentially harmful concentrations of neonicotinoids via nectar and pollen of treated plants. Soil- and water-dwelling organisms can be exposed via pesticide residues in treated soil, contaminated agricultural run-off and groundwater (Blacquiere et al., 2012; van der Sluijs, 2013; Hallmann et al., 2014; Lundin et al., 2015; Eng et al., 2017; Cressey, 2017; Basley and Goulson, 2018; Ertl et al., 2018; Sumon et al., 2018). These concerns have led to some regulatory restrictions in the sale and use of many neonicotinoid-containing products. As result of a 2012 E.U. European Food Safety Authority Review, use of clothianidin, imidacloprid and thiamethoxam was banned for use on bee-attractive crops (e.g., maize, oilseed rape, and sunflower), with exceptions for uses in the greenhouse and winter-grown crops (EFSA, 2013). In 2018, the European ban was expanded to all outdoor uses of these products (EFSA, 2018a,b,c). Several manufacturers have voluntarily canceled the U.S. registrations of products containing thiamethoxam and clothianidin (EPA, 2019). Sale of these products after May 2020 is prohibited. Potential non-target exposure from pesticide residues in crop plant nectar and pollen are of minor concern in potato. Potato flowers do not produce nectar and therefore only attract pollen-collecting insects, such as the buzz-pollinating Bombus impatiens (Batra, 1993; Buchanan et al., 2017). While a broad range of pollinating insects are documented to forage in or near potato fields, few species have been reported to forage from solaneaceous flowers themselves (Buchmann and Cane, 1989; Buchanan et al., 2017). Ecotoxicology of potato systems is therefore relatively understudied in potato systems compared to bee-attracting crops. However, there have been some investigations regarding concerns over pesticide residues taken up by crop- and non-crop plants via runoff, ground water infiltrations, and residues that remain in the soil following potato crops. Rogers and Kemp (2003) investigated the fate of imidacloprid and two of its metabolites (olefin and hydroxyl), finding barely detectable levels in 27.3% of clover leaves sampled from fields in the year following an imidacloprid-treated potato. They found no detectable pesticide levels in any clover flowers, nearby wildflowers, or the pollen, nectar and unripe honey of nearby honey bee hives. Huseth and Groves (2014) reported detection of clothianidin, imidacloprid, and thiamethoxam residues in groundwater associated with Wisconsin potato production, in concentrations

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ranging 0.21e3.34, 0.26e3.34, and 0.20e8.93 mg/L, respectively. Their investigation of the movement of thiamethoxam from potato production did find lower levels of pesticide in soil leachate when applied as two foliar treatments compared to seed treatment or in-furrow. However, all three application approaches resulted in detection of thiamethoxam in irrigation water more than 200 days from planting. Unfortunately, as has been the case for virtually all other insecticides that preceded it, Colorado potato beetle developed resistance to imidacloprid with greater than 100-fold resistance levels detected in populations from Long Island, NY in 1997 (Olson et al., 2000; Zhao et al., 2000). Since that time, many other populations of the beetle in North America have developed resistance to imidacloprid as well as cross-resistance to thiamethoxam (Mota-Sanchez et al., 2000, 2006; Tolman et al., 2005; Alyokhin et al., 2006, 2008a). However, on many farms across the U.S., neonicotinoids are still providing excellent control of Colorado potato beetle after 20 years of regular use on potatoes (Kuhar and Doughty, 2018). Entomologists have attempted to be proactive with slowing the rate of resistance development to this important class of insecticides. In the interest of insecticide resistance management (IRM), it is strongly recommended that growers explore non-chemical control options such as crop rotation, avoid using neonicotinoids where beetle populations have demonstrated resistance, avoid foliar applications of neonicotinoids if at-planting systemic applications were made, use economic thresholds, only spray if necessary, leave untreated refuge areas in fields, and apply full rates of products (Sexson et al., 2005; Alyokhin, 2011). Moreover, neonicotinoid resistance monitoring of Colorado potato beetle populations from across North America is conducted annually, and alternative insecticide mode of actions are recommended to potato growers when resistance is suspected. Insecticide rotation is strongly encouraged in general as a sound IRM practice in agriculture (Huseth et al., 2014).

11.4 A plethora of chemical control options still available in the 21st century Despite all the challenges posed by resistance and environmental regulations, today there are a wide range of effective insecticides for control of Colorado potato beetle and other insect pests (Table 11.1). These include some biologicallyderived products as well as synthetic compounds with novel modes of action. For most of these foliar spray products, monitoring potato fields for beetle eggs and larvae allows growers to accurately target needed sprays. This strategy reduces the number of sprays and avoids excessive selection of resistant beetles and other pests (Sexson et al., 2005). Several alternative and novel classes of insecticides for control of Colorado potato beetle are discussed below.

11.4.1 Diamides The anthranilic diamide insecticides were introduced in the 2000s and have provided an effective alternative to neonicotinoids for control of Colorado potato beetle. Diamides, which include chlorantraniliprole, cyantraniliprole, and cyclaniliprole activate the insect ryanodine receptors affecting calcium release during muscle contraction (Cordova et al., 2006). Insects treated with diamides exhibit rapid feeding cessation, lethargy, regurgitation, muscle paralysis, and ultimately death (Hannig et al., 2009). All three aforementioned diamides have demonstrated strong efficacy against a variety of lepidopteran and coleopteran pests, including Colorado potato beetle, in potatoes (Kuhar and Doughty, 2009, 2010, 2016; Sewell and Alyokhin, 2009; Groves et al., 2017). Chlorantraniliprole and cyantraniliprole are also xylemmobile for root uptake providing long-lasting systemic control of Colorado potato beetle from seed- ¼ piece or in-furrow applications (Sewell and Alyokhin, 2009, 2011; Kuhar and Doughty, 2010; Groves et al., 2011a,b).

11.4.2 Cryolite Cryolite is an inorganic fluoride insecticide that was used for control of insecticide-resistant Colorado potato beetles in the 1990s. The fluoride ion inhibits many enzymes that contain iron, calcium, and magnesium. Several of these enzymes are involved in energy production in cells, as in the case of phosphatases and phosphorylases (Ware and Whitacre, 2004). Cryolite has been used as a relatively safe fruit and vegetable insecticide in integrated pest management programs, and provides effective control of Colorado potato beetle (Noetzel and Holder, 1996; Sorensen and Holloway, 1997).

11.4.3 Avermectins Avermectins are macrocyclic lactone derivatives from the fermentation of Streptomyces avermitilis, a soil actinomycete (Campbell, 1989). The insecticide abamectin is a mixture of avermectins containing more than 80% avermectin B1a and less than 20% avermectin B1b. Abamectin blocks the transmittance of electrical activity in nerves and muscle cells by

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stimulating the release and binding of gamma-aminobutyric acid (GABA) at nerve endings, which causes an influx of chloride ions into the cells leading to hyperpolarisation and subsequent paralysis of the neuromuscular systems (Bloomquist, 1996, 2003). Abamectin is toxic to a wide range of insects and mites, and has been shown to be highly effective at controlling Colorado potato beetle larvae and adults (Nault and Speese, 1999a; Kuhar et al., 2006a; Marcic et al., 2009; Sewell and Alyokhin, 2010b; Kuhar and Doughty, 2016; Groves et al., 2017). Prior to the introduction of neonicotinoid insecticides, abamectin was one of the top insecticides used for control of insecticide-resistant Colorado potato beetles. In the U.S., as of 2020, there has been renewed interest in the use of abamectin for potato beetle control.

11.4.4 Novaluron Novaluron is an insect growth regulator that belongs to the benzoylphenyl urea (or benzoylurea) class of chemicals (IRAC Group 15). These insecticides target and disrupt chitin biosynthesis on the larval stages of many insects (Ishaaya et al., 2003; Ware and Whitacre, 2004). Novaluron is very effective at controlling the larval stage of Colorado potato beetle (Cutler et al., 2007), but can also cause egg mortality (Alyokhin et al., 2008b) and a decrease in reproductive viability of adult females when ingested (Alyokhin et al., 2010). Two foliar applications of novaluron will provide effective control of Colorado potato beetle (Kuhar et al., 2006b; Kuhar and Doughty, 2009; Sewell and Alyokhin, 2009, 2010b; Groves et al., 2017). Novaluron will also control European corn borer (Kuhar et al., 2006b).

11.4.5 Cyromazine Cyromazine, a triazine, is also a potent chitin synthesis inhibitor (Ware and Whitacre, 2004). It is selective toward dipterous insects and is used for the control of leafminers and root maggots (Thetford, 1993). However, the insecticide has also been shown to provide effective control of Colorado potato beetle larvae (Sirota and Grafius, 1994; Linduska et al., 1996).

11.4.6 Indoxacarb Indoxacarb is a broad-spectrum insecticide belonging to the oxadiazine class of insecticides. Indoxacarb is a voltagedependent sodium channel blocker (Wing et al., 2000) that is efficacious against most lepidopteran pests. Indoxacarb alone provides moderate control of Colorado potato beetle as well as potato leafhopper (Davis et al., 2003; Linduska et al., 2002; Kuhar and Speese, 2005a), but when tank mixed with the synergist piperonyl butoxide, it is highly efficacious against those pests (Linduska et al., 2002; Sewell and Alyokhin, 2003).

11.4.7 Metaflumizone Metaflumizone is a semicarbazone oxadiazine insecticide that is currently not registered for use in the U.S. Potato leaf-dip bioassays as well as field efficacy evaluations confirmed a high level of toxicity of metaflumizone to L. decemlineata and demonstrated a potential benefit of tank mixing a low rate of the pyrethroid esfenvalerate with metaflumizone at one-10th the recommended field rate (Hitchner et al., 2012). These research findings, as well as those of others (Sewell and Alyokhin, 2009, 2010b), confirm that metaflumizone is highly active against L. decemlineata larvae and adults and could provide an effective alternative insecticide for potato pest management.

11.4.8 Tolfenpyrad The pyrazole (or phenoxybenzylamide) insecticide tolfenpyrad was first registered as a broad-spectrum insecticide in Japan in 2002 and is now widely registered for use on potatoes in many countries, including the United States. Pyrazole pesticides (IRAC group 21) are respiratory poisons that inhibit mitochondrial electron transport at the NADH-CoQ reductase site, leading to the disruption of adenosine triphosphate (ATP) formation (Ware and Whitacre, 2004). Tolfenpyrad has demonstrated to be an effective insecticide for control of Colorado potato beetle larvae and adults (Sewell and Alyokhin, 2011; Wimer et al., 2015; Buzza and Alyokhin, 2017; Bradford et al., 2020)

11.4.9 Spinosyns Spinosyns are a group of insecticidal macrocyclic lactones derived from the fermentation of Saccharapolyspora spinosa, which is a soil actinomycete (Thompson et al., 1995, 2000). The insecticide spinosad is a mixture of spinosyns A and D.

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Spinosad disrupts binding of acetylcholine in nicotinic acetylcholine receptors at the postsynaptic cell, exciting neurons in the central nervous system. This causes tremors and spontaneous muscle contractions, paralysis, and loss of body fluids (Salgado, 1998). The insecticide is active against most lepidopterans, thysanopterans, dipterans and some coleopterans (Thompson et al., 2000). Foliar applications of spinosad provide excellent control of Colorado potato beetle larvae (Byrne et al., 2006; Kuhar and Doughty, 2009, 2016; Sewell and Alyokhin, 2009, 2010b; Groves et al., 2017). However, some populations of Colorado potato beetle that are resistant to neonicotinoids have demonstrated cross resistance (or inherent reduced susceptibility) to spinosad (Mota-Sanchez et al., 2006). Spinetoram is a more recent spinosyn insecticide that was derived from spinosyns J and L, which have been chemically modified to produce a semi-synthetic insecticide (Sparks et al., 2008). Spinetoram is active against the same pest groups as spinosad, and has shown excellent control against most lepidopteran pests as well as Colorado potato beetle (Sewell and Alyokhin, 2007; Kuhar and Doughty, 2009; Groves et al., 2011a, 2017). However, unlike spinosad, spinetoram is not allowed for use in organic agriculture because the compound is synthetically modified.

11.5 Insecticide options for organic potatoes Spinosad is currently a chemical of choice in organic potato production. However, its extensive use has been already shown to result in the resistance of the targeted Colorado potato beetle populations (Mota-Sanchez et al. 2006). Therefore, overreliance on this active ingredient must be avoided. Several other insecticides that are derived from plants such as pyrethrins and azadirachtins, or derived from bacteria, fungi, or other microbes such as spinosad and Bacillus thuringiensis are permitted for use in organically certified operations, and these are discussed below.

11.5.1 Pyrethrins Pyrethrins are derived from the flowers of Chrysanthemum cinerariifolium and are nerve poisons that modulate the sodium channel on axon neuronal membranes (Casida, 1980). They are fast-acting broad spectrum contact poisons, but do not have long residual efficacy, and because of the resistance to DDT and pyrethroids in many Colorado potato beetle populations, these insecticides are generally ineffective against that pest.

11.5.2 Azadirachtin Azadirachtin is a tetranortriterpenoid (limonoid) found in the seeds of the neem tree (Azadirachta indica). This compound has been shown to be an antifeedant and disrupt insect growth by blocking the release of the morphogenic peptide hormone (Mordue and Blackwell, 1993; Seymour et al., 1995; Abudulai et al., 2003). It has been shown to be effective on a wide range of insects including lepidopteran pests and Colorado potato beetle. In general, azadirachtin is most effective as a growth regulator on eggs and small larvae (Trisyono and Whalon, 1999; Kowalska, 2007), and therefore, application timing is paramount for successful control, particularly when targeting Colorado potato beetle. Azadirachtin has demonstrated moderate efficacy in the field for Colorado potato beetle control (Zehnder and Warthen, 1988; Marcic et al., 2009). Because the active ingredients are biologically derived, azadirachtin formulations are approved for use in organic agriculture.

11.5.3 Bacillus thuringiensis subspecies tenebrionis (Bt) Bt is a bacterium that produces delta-endotoxins that are toxic to the midgut of insect pests. If the endotoxins are ingested, they form an ion channel that causes shrinking or swelling in the epithelium cells, leading to cell lysis and eventual death of the insect (Slaney et al., 1992). Bt subsp. tenebrionis applications are most effective against small larvae of Colorado potato beetle, and thus, as with azadirachtin, application timing is critical for effective control in the field (Ghidiu and Zehnder, 1993). Even with proper application timing the efficacy of this insecticide against Colorado potato beetle has been moderate at best (Sewell and Alyokhin, 2009). Moreover, resistance to Bt subsp. tenebrionis was reported in isolated populations of Colorado potato beetle in the early 1990s (Whalon et al., 1993). This insecticide has not been widely used in the U.S. since the 1990s, but new improved formulations of this insecticide have shown promise (Wantuch et al., 2016; Nault and Seaman, 2019). Several beta proteobacteria have recently been shown to produce insecticidal compounds that can be formulated into insecticides. For example, Chromobacterium subtsugae, produces insecticidal compounds that are active against a variety of insect pests including Colorado potato beetle (Martin et al., 2007). An extract of C. subtsugae was approved by the U.S.

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EPA for use as an organic insecticide commercially available as GrandevoÒ (Marrone BioInnovations Incorporated, Davis, CA, USA). Another relatively new biological insecticide from this same company is VenerateÒ, which contains heat-killed cells and fermentation solids of the bacteria Burkholderia spp. The insecticide works by contact and ingestion to disrupt insect exoskeletons and interfere with molting (Asolkar et al., 2013). Nault and Seaman (2019), evaluated the organic insecticides, pyrethrin, spinosad, azadirachtin, sabadilla alkaloids, Bacillus thuringiensis, and Chromobacterium subtsugae, on potatoes over 2 years. In that study, spinosad consistently had the highest level of efficacy against Colorado potato beetle followed by B.t. tenebrionis and azadirachtins. Very little control was provided by any of the other organic insecticides. Groves et al. (2017) also achieved excellent control of Colorado potato beetle with spinosad and virtually no control with either Ch. subtsugae or Burkholderia spp.

11.6 Chemical control of hemipteran pests Potatoes are attacked by several phloem-feeding hemipteran pests. In North America, the major hemipteran pests include potato psyllid, Bactericerca cockerelli (Sulc) (Hemiptera: Triozidae), potato leafhopper, and various aphids (Hemiptera: Aphidae), including green peach aphid, potato aphid, Macrosiphum euphorbiae (Thomas), and buckthorn aphid, Aphis nasturtii Kaltenbach. In other parts of the world potatoes are also attacked by cotton aphid, Aphis gossypii Glover and the leafhopper, Amrasca biguttula biguttula Ishida (Kumar et al., 2011). Feeding by potato psyllid causes yellowing of the leaves referred to as “psyllid yellows,” stunting, leaf curling, and yield loss (Wallis, 1995; Gharalari et al., 2009; see Chapter 6 for more details). In addition, this species transmits the alphaproteobacteria Candidatus Liberibacter solanacearum that causes Zebra chip syndrome (Munyaneza et al., 2007; Gao et al., 2009). Potato leafhopper nymphs and adults feed on leaves and stems and secrete a salivary toxin into the plant, which causes cellular abnormalities that result in “hopperburn” and subsequent yield loss (Backus and Hunter, 1989; see Chapter 9 for more details). Aphids are considered important pests of potato primarily because of their role as vectors of viruses to seed potatoes; the two most important viruses transmitted to potato by aphids are Potato leaf roll virus (PLRV) and Potato virus Y (PVY or Mosaic) (see Chapter 5 for more details). Often the insecticides that are applied to potato for other pests such as Colorado potato beetle will also provide control of most hemipteran pests. Most insecticides targeted specifically at hemipteran pests are applied in an effort to control or reduce viral infections. Because these viruses spread rapidly, prevention by use of insecticides is difficult. Nevertheless, some insecticides will help to slow the spread of viruses (Collar et al., 1997). While thresholds exist for most hemipteran pests (Sexson et al., 2005; Goolsby et al., 2007), the concept is not widely used for these pests, particularly in potato seed production, where most growers apply a systemic insecticide at planting (Sexson et al., 2005). For decades, carbamates or organophosphates such as aldicarb, phorate and disulfoton have provided effective early-season control of hemipteran pests (Gerhardt and Turley, 1961; Harding, 1962; Gerhardt, 1966; Cranshaw, 1997). Neonicotinoids such as imidacloprid, thiamethoxam, and clothianidin also provide excellent control of hemipteran pests (Boiteau et al., 1997; Pavlista, 2002; Kuhar et al., 2003b; Liu and Trumble, 2005; Kund et al., 2006; Kuhar and Doughty, 2010; Groves et al., 2011b). Kumar et al. (2011) developed controlled-release formulations of carbofuran and imidacloprid that were found to control the aphid, A. gossypii, and leafhopper, A. biguttula biguttula, better than commercial formulations. If foliar insecticide applications are needed, many pyrethroid, organophosphate, and carbamate insecticides will provide rapid knockdown of hemipteran pests (Sexson et al., 2005; Berry et al., 2009) and can reduce probing by aphids, which will slow the spread of viruses (Van Emden and Harrington, 2017). However, because insecticide resistance to carbamates, organophosphates, and pyrethroids has developed in several key hemipteran pests, most notably, green peach aphid (Foster et al., 2007; Castañeda et al., 2011), combining or rotating insecticide modes of action is strongly recommended. Berry et al. (2009) showed that abamectin, azadirachtin, and thiacloprid were highly toxic to potato psyllid resulting in almost 100% mortality after 48 h. Gharalari et al. (2009) also showed that abamectin was highly effective against potato psyllid and suggested the translaminar activity of the insecticide enables it to perform better against sucking insects often found on the undersides of leaves, that may be difficult to reach with contact insecticides. However, Groves et al. (2017) did not achieve effective control of potato leafhopper with applications of abamectin. They also failed to control potato leafhopper with several other insecticides that are typically applied for Colorado potato beetle including novaluron, spinosad, spinetoram, cyantraniliprole, and chlorantraniliprole. Numerous insecticides have been proven to work in controlling aphid pests as well. Nevertheless, the push for safer insecticides has stimulated the development of several novel insecticides specifically designed to control hemipteran pests. New classes of nAChR modulators have been developed, with similar pesticidal activity as neonicotinoids (Table 11.1); these include sulfoxaflor (IRAC 4C; Sparks et al., 2013; Watson et al., 2017), and flupyradifurone (IRAC 4D; Nauen et al., 2015; Jeschke et al., 2015). These compounds provide excellent

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control of aphids (Bradford et al., 2019) and potato leafhoppers (Groves et al., 2017; Kuhar and Doughty, 2010). Other selective insecticides that target hemipteran pests include pymetrozine, pyrifluquinazon, afidopyropen, flonicamid, and spirotetramat (Table 11.1).

11.6.1 Pymetrozine Pymetrozine belongs to the pyridine-azomethine class of chemicals (IRAC, Group 9). This insecticide is active on a number of different hemipteran pests such as aphids, whiteflies and leafhoppers. The mode of action of pymetrozine is a chordotonal organ modulator that interferes with the regulatory mechanism of food intake (Kristinsson, 1995). It is highly effective against aphids (Sewell and Alyokhin, 2010a; Bradford et al., 2019), but has provided only marginal control of potato psyllid in field trials (Russell et al., 2001; Liu and Trumble, 2005). Pyrifluquinazon and afidopyropen, relatively new insecticides with similar modes of action, are excellent aphicides; however, additional research is needed to determine their complete pest spectrum in potatoes.

11.6.2 Flonicamid Flonicamid is an insecticide belonging to the pyridinecarboxamide class of chemicals (IRAC Group 29). Flonicamid is a novel systemic compound with activity on hempiterous pests such as aphids (Bradford et al., 2019), whiteflies and thysanopterous pests. The mode of action of this compound cause the normally rigid stylet of piercing sucking pests to become flaccid inhibiting afflicted insects from piercing the leaf tissue and feeding; this inability to feed is observed until death (Morita et al., 2007).

11.6.3 Spirotetramat Spirotetramat is a unique insecticide derived from spirocyclic tetramic acid, and has a unique mode of action (IRAC, Group 23) as a lipid biosynthesis inhibitor that reduces lipid content, inhibits ecdysis, and reduces fecundity and fertility (Nauen et al., 2008). When applied to plant foliage, spirotetramat penetrates the leaf surface and is hydrolyzed to an active enol form that enables it to enter both phloem and xylem transport systems of the plant, resulting in unique two-way systemicity (Brücka et al., 2009). This is advantageous for many sucking insects that frequently hidden in plant parts, or may develop on newly emerging shoots and leaves after insecticide application. Spirotetramat has activity on a number of pests such as aphids, psyllids, scale insects, mealy bugs, and whiteflies (Bretschneider et al., 2007; Nauen et al., 2008; Sewell and Alyokhin, 2010a; Bradford et al., 2019). It has demonstrated excellent long-lasting efficacy against potato psyllid (Brücka et al., 2009). It is also toxic to twospotted spider mites (Popov and Alyokhin, 2019) but not currently registered as an acaricide on potatoes.

11.7 Chemical control of wireworms Many species of wireworms (Coleoptera: Elateridae) can be serious pests of potato throughout the world, and chemical control of these subterranean pests is difficult (Hancock et al., 1986; Kwon et al., 1999; Parker and Howard, 2001; Kuhar et al., 2003a). For more information on wireworms, please refer to Chapter 7. To be most effective, it is recommended that insecticides be incorporated into the soil prior to planting to reach their target (Thomas et al., 1983), but also be very persistent in the soil to ensure adequate protection of daughter tubers late in the season (Parker and Howard, 2001). In the 1950s, soil-applied organochlorine insecticides such as DDT and aldrin became the standard treatment for wireworms in many parts of the world (Merrill, 1952; Gunning and Forrester, 1984; Parker and Howard, 2001). However, widespread concerns over the environmental impact of organochlorine insecticides led to the removal of these chemicals from agricultural use (Ware and Whitacre 2004). Organophosphate and carbamate insecticides have served as replacements for the organochlorines in potatoes for more than 30 years in the U.S. and Europe (Edwards and Thompson, 1971; Parker et al., 1990; Kuhar et al., 2003a). These chemicals, which include aldicarb, bendiocarb, carbofuran, carbosulfan, chlorpyrifos, diazinon, disulfoton, ethoprophos, fonofos, phorate, and phosmet, have provided effective, but not always consistent wireworm control in potatoes (Hancock et al., 1986; Toba, 1987; Noetzel and Ricard, 1988; Jansson et al., 1988; Parker et al., 1990; Sorensen and Kidd, 1991; Pavlista, 1997; Shamiyeh et al., 1999; Nault and Speese, 2000; Kuhar et al., 2003a). All of the aforementioned insecticides are relatively toxic to humans and nontarget organisms, and subsequently, several are no longer registered or used on potatoes in the U.S. or other countries.

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As of 2019, chlorpyrifos and phosmet are two organophosphates that have maintained registrations on potatoes in Canada and the U.S. Both of these insecticides have been shown to reduce wireworm injury to tubers by >90% compared with the neonicotinoids imidacloprid, clothianidin, and thiamethoxam, which reduced tuber damage by, respectively, 19.1%, 71.6%, and 90.6% (Vernon et al., 2013). These researchers also showed that the tuber protection provided by the neonicotinoids is from long-term intoxication of the wireworm rather than mortality. Significant recovery over time of wireworms from neonicotinoid poisoning has been demonstrated (Vernon et al., 2013). Fipronil is a phenylpyrazole insecticide that was registered for use on potatoes in the U.S. in the mid-2000s. Fipronil blocks the gamma-aminobutyric acid (GABA)-regulated chloride channel in neurons antagonizing the “calming” effects of GABA, similar to the action of the cyclodienes. Fipronil is a systemic material with contact and ingestion activity. Although it has been shown to be effective as a foliar insecticide on Colorado potato beetle (Moffat, 1993; Noetzel and Holder, 1996; Nault and Speese, 1999b) and as a systemic material for control of European corn borer (Nault and Speese, 1999a; Kuhar et al., 2010), the primary targets for this insecticide in agriculture are soil pests such as wireworms. In Canada, Vernon et al. (2013) showed that in-furrow applications of fipronil reduced wireworm damage to potato tubers by 94%. Fipronil has been shown to be one of the most toxic of all current insecticides to wireworms (van Herk et al., 2015). In the U.S., Kuhar and Alvarez (2008) showed that fipronil, as well as the pyrethroid bifenthrin, and the neoneonicotinoids imidacloprid and thiamethoxam, each applied to seed pieces in the soil at-planting provided similar reduction of wireworm damage (50%e80%) to that of the organophosphates phorate or ethoprop. In that study, combinations of imidacloprid or thiamethoxam with fipronil or bifenthrin did not enhance the efficacy of any one compound used alone. Other researchers have also shown effective wireworm control in potatoes with these insecticides (DeVries and Wright, 2005). van Herk et al. (2015) demonstrated that a high level of repellency was observed when wireworms were exposed to pyrethroids applied as seed treatments. In potatoes, repellency could lead to wireworms not acquiring a lethal dose of insecticide applied to the seed piece in furrow, and potentially attacking daughter tubers later in the season. Relatively few insecticide options are available for wireworm control after planting. Bifenthrin and phorate may be applied during post-planting cultivation (hilling), which can work the insecticide into the soil to reach its target. In addition, spirotetramat offers an opportunity to suppress wireworms without applying insecticides to the soil. Because of its unique two-way systemicity, applications of spirotetramat to plant foliage allows the active ingredient to travel from the point of application in the foliage down into the roots where can help suppress root feeding organisms such as phytoparasitic nematodes and wireworms (Bayer Crop Science 2019; Shirley et al., 2019).

11.8 Chemical control of potato tuberworm Potato tuberworm, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae), is the primary pest of potato throughout tropical and subtropical regions of the world. It is also a pest in the Pacific Northwest of the U.S. An excellent review of the biology, ecology, and management of this pest can be found in Rondon (2010; 2020; Rondon and Gao, 2018) and is discussed in Chapter 8 of this book. While many cultural control tactics help in managing P. operculella, chemical controls remain the primary approach to management programs globally (Rondon and Gao, 2018; Rondon, 2020). Chemical control of the P. operculella has posed a challenge for potato growers because larvae mine the leaves feeding between the upper and lower epidermal tissue (Rondon 2010; Rondon and Gao 2018), eggs can be deposited on tubers after they are harvested (Rondon, 2010), and insecticide efficacy on this pest has been unpredictable (von Arx et al., 1987; Berlinger, 1992). Resistance to the pyrethroid, esfenvalerate and the phenylpyrazole, fipronil was documented in 2005 from field-collected P. operculella from the Pacific Northwest of the United States (Dogramaci and Tingey 2008). Contact insecticides targeting adults should be applied in the evening when most activity occurs (Gubbaiah and Thontadarya, 1977). Systemic or translaminar insecticides will be most effective, because P. operculella larvae feed within the leaf, avoiding many other foliar insecticides that must be consumed to be effective. Since the 2000s, more narrow-spectrum systemic insecticides have become available, offering a more targeted and IPM-compatible option for lepidopteran control in potatoes (e.g., chlorantraniliprole, spinetoram). These insecticides have shown very good efficacy on P. operculella (Lawrence, 2009; Dobie, 2010), and are also effective at controlling other lepidopteran pests such as beet armyworm, Spodoptera exigua (Hübner) (Kund et al., 2011; Natwick and Lopes, 2011; Palumbo, 2011) and European corn borer, Ostrinia nubilalis (Sewell and Alyokhin, 2007; Kuhar et al., 2011). These insecticides often have improved ecotoxicology profiles and are less disruptive to natural enemies than pyrethroids or organophosphates.

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When foliage naturally senesces or is artificially desiccated, larvae will readily move from the leaves into the tubers making any exposed tubers susceptible to high risk of infestation (Rondon et al., 2007; Rondon and Hervé, 2017; Rondon, 2020). Clough et al. (2010) found that rotations of esfenvalerate and indoxacarb applications before and at vine kill were effective at reducing P. operculella damage, thus indicating that application timing is critical for effective control (Clough et al., 2008, 2010; Rondon, 2010). Moreover, in addition to chemical control, rapid harvest of potatoes after vine-kill is strongly recommended because the risk of P. operculella damage increases if the tubers are left in the field (Rondon, 2010; Rondon and Gao, 2018).

11.9 Final thoughts Chemical control remains the most widely-used strategy for eliminating potato damage by pests, and will likely remain the base of pest management for the foreseeable future (Alyokhin, 2009). However, a more sustainable and responsible approach to chemical control is possible, one that avoids past mistakes and uses insecticides efficiently, with a better understanding of the pest’s biology, and as part of an integrated pest management program. A number of novel insecticides have been registered in recent years and many more are in development for example spiropidon, tetraniliprole, broflanilide. In addition, rapid development of RNAi technology, which is described in Chapter 12, opens exciting opportunities for development of highly customized target-specific insecticides. Modern insecticides will undoubtedly be safer for the user, have less of an impact on beneficial insects, and fit better into potato IPM programs, as discussed in Chapter 27. If chemical control is truly needed for a given pest situation on potatoes, it should be the job of entomologists and crop consultants to recommend the use of these new chemical tools over the more disruptive, broad-spectrum insecticides. Also, frequent rotation of insecticide classes should minimize insecticide resistance development in Colorado potato beetle and other pests.

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Development of controlled release formulations of carbofuran and imidacloprid and their bioefficacy evaluation against aphid, Aphis gossypii and leafhopper, Amrasca biguttula biguttula Ishida on potato crop. J. Environ. Sci. Health, Part B 46, 678e682. Kund, G.S., Carson, W.G., Trumble, J.T., 2006. Effect of insecticides on pepper insects, 2005. Arthropod Manag. Tests 31, E44. Kund, G.S., Carson, W.G., Trumble, J.T., 2011. Effect of insecticides on celery insects, 2009. Arthropod Manag. Tests 36, E27. Kwon, M.Y., Hahm, I., Shin, K.Y., Ahn, Y.J., 1999. Evaluation of various potato cultivars for resistance to wireworms (Coleoptera: Elateridae). Am. J. Potato Res. 76, 317e319. Lawrence, J.L., 2009. Damage Relationships and Control of the Tobacco Splitworm (GELECHIIDAE: Phthorimaea Operculella) in Flue-Cured Tobacco. M.S. thesis. North Carolina State University, Raleigh, NC. http://repository.lib.ncsu.edu/ir/bitstream/1840.16/784/1/etd.pdf. Linduska, J.J., Ross, M., Mulford, K., Baumann, D., 1996. Colorado potato beetle control on potatoes with foliar insecticide sprays, 1995. Arthropod Manag. Tests 21, E83. Linduska, J.J., Ross, M., Abbott, B., Steele, S., Ross, E., Eastman, R., 2002. Colorado potato beetle control on potatoes, 2001. Arthropod Manag. Tests 27, E69. Liu, D., Trumble, J.T., 2005. Interactions of plant resistance and insecticides on the development and survival of Bactericerca cockerelli [Sulc](Homoptera: Psyllidae). Crop Protect. 24, 111e117. Liu, W.P., Zheng, W., Ma, Y., Liu, K.K., 2006. Sorption and degradation of imidacloprid in soil and water. J. Environ. Sci. Health, Part B 41, 623e634. Liu, Z., Dai, Y., Huang, G., Gu, Y., Ni, J., Wei, H., Yuan, S., 2011. Soil microbial degradation of neonicotinoid insecticides imidacloprid, acetamiprid, thiacloprid and imidaclothiz and its effect on the persistence of bioefficacy against horsebean aphid Aphis craccivora Koch after soil application. Pest Manag. 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Maienfisch, P., Angst, M., Brandl, F., Fischer, W., Hofer, D., Kayser, H., Kobel, W., Rindlisbacher, A., Senn, R., Steinemann, A., Widmer, H., 2001. Chemistry and biology of thiamethoxam: a second generation neoneonicotinoid. Pest Manag. Sci. 57, 906e913. Marcic, D., Peric, P., Krasteva, L., Panayotov, N., 2009. Field evaluation of natural and synthetic insecticides against Leptinotarsa decemlineata Say. Acta Hortic. 830, 391e396. Martin, P.A., Gundersen-Rindal, D.E., Blackburn, M.B., Buyer, J., 2007. Chromobacterium subtsugae sp. nov., a betaproteobacterium toxic to Colorado potato beetle and other insect pests. Int. J. Syst. Evol. Microbiol. 57, 993e999. Matsuda, K., Ihara, M., Sattelle, D.B., 2020. Neonicotinoid Insecticides: molecular targets, resistance, and toxicity. Annu. Rev. Pharmacol. Toxicol. 60, 241e255. Merrill, L.G., 1952. Reduction of wireworm damage to potatoes. J. Econ. Entomol. 45, 548e549. Metcalf, R.L., 1980. Changing role of insecticides in crop protection. Annu. 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Association of Bactericera cockerelli (Homoptera: Psyllidae) with “zebra chip”, a new potato disease in southwestern United States and Mexico. J. Econ. Entomol. 100, 656e663. Natwick, E.T., Lopes, M.I., 2011. Anthranilic diamide worm control in romaine lettuce, 2010. Arthropod Manag. Tests 36, E34. Nauen, R., Reckmann, U., Thomzik, J., Thielert, W., 2008. Biological profile of spirotetramat (Movento)- a new two-way systemic (ambimobile) insecticide against sucking pest species. Bayer CropSci. J. 61, 245e278. Nauen, R., Jeschke, P., Velten, R., Beck, M.E., Ebbinghaus-Kintscher, U., Thielert, W., Wolfel, K., Haas, M., Kunz, K., Raupach, G., 2015. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Manag. Sci. 71, 850e862. Nault, B.A., Seaman, A., 2019. Colorado potato beetle control with insecticides allowed for organic production, 2017 and 2018. Arthropod Manag. Tests 44, tsz081. https://doi.org/10.1093/amt/tsz081. Nault, B.A., Speese, J., 1999a. Evaluation of Agri-mek for CPB control in potatoes, 1998. Arthropod Manag. Tests 24, E74. Nault, B.A., Speese, J., 1999b. Evaluation of Agenda for control of ECB in potatoes, 1998. Arthropod Manag. Tests 24, E75. Nault, B.A., Speese III, J., 2000. Evaluation of insecticides to control soil insect pests on potatoes, 1999. Arthropod Manag. Tests 25, 148. Noetzel, D., Ricard, M., 1988. Wireworm and white grub control in potato, 1987. Arthropod Manag. Tests 13, 160e161. Noetzel, D.M., Holder, B., 1996. Control of resistant Colorado potato beetles Andover, MN 1994. Arthropod Manag. Tests 21, E87. Olson, E.R., Dively, G.P., Nelson, J.O., 2000. Baseline susceptibility to imidacloprid and cross resistance patterns in Colorado potato beetle (Coleoptera: Chrysomelidae) populations. J. Econ. Entomol. 93, 447e458. Palumbo, J.C., 2011. Evaluation of new insecticides for control of lepidopterous larvae on head lettuce, 2010. Arthropod Manag. Tests 36, E43. 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Gender-specific acaricidal properties and sexual transmission of spirotetramat in two-spotted spider mite (Tetranychidae: Acariformes). J. Econ. Entomol. 112, 2186e2192. Penman, D.R., Chapman, R.B., 1988. Pesticide-induced mite outbreaks: pyrethroids and spider mites. Exp. Appl. Acarol. 4, 265e276. Riley, C.V., 1871. Third Annual Report on the Noxious, Beneficial, and Other Insects of the State of Missouri. Horace Wilcox, Jefferson City, MO. Rogers, R.E.L., Kemp, J.R., 2003. Imidacloprid, potatoes, and honey bees in Atlantic Canada: is there a connection? Bull. Insectol. 56, 83e88. Rondon, S.I., 2010. The potato tuberworm: a literature review of its biology, ecology, and control. Am. J. Potato Res. 87, 149e166. Rondon, S.I., Gao, Y., 2018. The potato tuberworm journey around the world. In: Perveen, K. (Ed.), Moths: Pests of Potato, Maize, and Sugar Beet. IntechOpen, UK, pp. 17e52. Rondon, S.I., Hervé, M., 2017. Effect of planting depth and irrigation regimes on potato tuberworm (Lepidoptera: Gelechiidae) damage under central pivot irrigation in the Lower Columbia Basin. J. Econ. Entomol. 110, 2483e2489. Rondon, S.I., DeBano, S.J., Clough, G.H., Hamm, P.B., Jensen, A., Schreiber, A., Alvarez, J.M., Thornton, M., Barbour, J., Dŏgramaci, M., 2007. Biology and Management of the Potato Tuberworm in the Pacific Northwest. Oregon State University Extension. PNW 594. Rondon, S.I., 2020. Decoding Phthorimaea operculella (Lepidoptera: Gelechiidae) in the new age of change. J. Integr. Agric. 19, 316e324.

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Rose, R.L., Brindley, W.A., 1985. An evaluation of the role of oxidative enzymes in Colorado potato beetle resistance to carbamate insecticides. Pestic. Biochem. Physiol. 23, 74e84. Roush, R.T., Hoy, C.W., Ferro, D.N., Tingey, W.M., 1990. Insecticide resistance in the Colorado potato beetle (Coleoptera: Chyrsomelidae): influence of crop rotation and insecticide use. J. Econ. Entomol. 83, 315e319. Russell, J.S., Grichar, J., Besler, B., Brewer, K., 2001. Evaluation of selected insecticides against potato psyllids on potatoes, 2000. Arthropod Manag. Tests 26, E62. Salgado, V.L., 1998. Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic. Biochem. Physiol. 2, 91e102. Saran, R.J., Kamble, S.T., 2008. Concentration-dependent degradation of three termiticides in soil under laboratory conditions and their bioavailability to eastern subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 101, 1373e1383. Scholz, K., Spiteller, M., 1992. Influence of ground cover on the degradation of 14C- imidacloprid in soil. Brighton Crop Prot. Conf. Pests Dis. 2, 883e888. Sewell, G.H., Alyokhin, A., 2003. Control of Colorado potato beetle on potato, 2002. Arthropod Manag. Tests 28, E63. Sewell, G.H., Alyokhin, A., 2007. Control of European corn borer on potato, 2006. Arthropod Manag. Tests 32, E42. Sewell, G.H., Alyokhin, A., 2009. Control of Colorado potato beetle on potato, 2008. Arthropod Manag. Tests 34, E52. Sewell, G.H., Alyokhin, A., 2010a. Control of aphids on Irish potato, 2009. Arthropod Manag. Tests 35, E18. Sewell, G.H., Alyokhin, A., 2010b. Control of Colorado potato beetle on potato, 2009. Arthropod Manag. Tests 35, E19. Sewell, G.H., Alyokhin, A., 2011. Control of Colorado potato beetle on potato, 2010. Arthropod Manag. Tests 36, E63. Sexson, D.L., Wyman, J.A., Radcliffe, E.B., Hoy, C.W., Ragsdale, D.W., Dively, G., 2005. Chapter 5: potato. In: Foster, R., Flood, B.R. (Eds.), Vegetable Insect Management. Meister Media Worldwide, Willoughby, OH, pp. 93e106. Seymour, J., Bowman, G., Crouch, M., 1995. Effects of neem seed extract on feeding frequency of Nezara viridula L. (Hemiptera, Pentatomidae) on pecan nuts. J. Aust. Entomol. Soc. 34, 221e223. Shamiyeh, N.B., Pereira, R., Straw, R.A., Follum, R.A., 1999. Control of wireworms in potatoes, 1998. Arthropod Manag. Tests 24, 164e165. Shirley, A.M., Noe, J.P., Nyczepir, A.P., Brannen, P.M., Shirley, B.J., Jagdale, G.B., 2019. Effect of spirotetramat and fluensulfone on population densities of Mesocriconema xenoplax and Meloidogyne incognita on peach. J. Nematol. 51, 34. https://doi.org/10.21307/jofnem-2019-012. Sirota, J.M., Grafius, E., 1994. Effects of cyromazine on larval survival, pupation, and adult emergence of Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 87, 577e582. Slaney, A.C., Robbins, H.L., English, L., 1992. Mode of action of Bacillus thuringiensis toxin CryIIIA: an analysis of toxicity in Leptinotarsa decemlineata (Say) and Diabrotica undecimpunctata Howardi barber. Insect Biochem. Mol. Biol. 22, 9e18. Sorensen, K.A., Kidd, K.A., 1991. Wireworm control, Currituck county, 1989. Arthropod Manag. Tests 16, E106. Sorensen, K.A., Holloway, C.W., 1997. Colorado potato beetle and European corn borer control with insecticides, 1996. Arthropod Manag. Tests 22, E88. Sparks, T.C., Crouse, G.D., Dripps, J.E., Anzeveno, P., Martynow, J., DeAmicis, C.V., Gifford, J., 2008. Neural network-based QSAR and insecticide discovery: spinetoram. J. Comput. Aided Mol. Des. 6, 393e401. Sparks, T.C., Watson, G.B., Loso, M.R., Geng, C., Babcock, J.M., Thomas, J.D., 2013. Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pestic. Biochem. Physiol. 107, 1e7. 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Chapter 12

Insecticidal RNA interference (RNAi) for control of potato pests Swati Mishra and Juan Luis Jurat-Fuentes Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, United States

12.1 Introduction Initially observed as a defensive mechanism against tobacco ringspot virus (Wingard, 1928), RNA interference (RNAi) was first formally described in the nematode Caenorhabditis elegans (Fire et al., 1991) and subsequently across Eukaryota. The RNAi process in the cell is initiated by the presence of a double stranded RNA (dsRNA), a class of non-coding RNA comprised of two complementary strands that can be endogenous or delivered exogenously. The result of the RNAi process is the degradation of the messenger RNA (mRNA) complementary to the dsRNA sequence, effectively suppressing gene expression (i.e., the protein encoded by the gene is not made). Applications of dsRNA-based technology in agriculture range from protecting plants and beneficials (Vogel et al., 2019) to managing herbicide resistance in weeds (Perotti et al., 2020). Two different types of RNAi response have been described based on whether reduction in gene expression is limited to the cells in which the dsRNA is introduced or expressed (cell-autonomous RNAi), or if the response is also observed in cells or tissues beyond the site of dsRNA application (non-cell autonomous RNAi). Within non-cell autonomous RNAi, silencing may involve dsRNA taken up from the environment (environmental RNAi) or transferred from other cells and tissues (systemic RNAi). As an example of non-cell autonomous RNAi, injection of dsRNA into the head or tail of C. elegans produced silencing of the target gene throughout the individual, and transgenerational silencing was also observed in its progeny (Fire et al., 1998). Insects belonging to different taxonomic orders display systemic RNAi (Aronstein and Saldivar, 2005; Bolognesi et al., 2012; Zhang et al., 2010; Zhou et al., 2006) and there are also examples of knockdown in eggs from dsRNA-treated females, a process called parental RNAi. However, unlike in plants and nematodes where systemic RNAi requires a mechanism termed transitive RNAi involving an RNA-dependent RNA polymerase (RdRP) that produces secondary small interfering RNAs (siRNAs), insect genomes seem to lack RdRP genes (Gordon and Waterhouse, 2007) and production of secondary siRNAs (Li et al., 2018). Thus, systemic RNAi in insects is not transitive and may involve different mechanisms for spread of silencing. One possibility is that siRNAs resulting from dsRNA processing incorporate in extracellular vesicles (EVs), which are capable of inducing an RNAi response in recipient cells (Mingels et al., 2020). The Colorado potato beetle (Leptinotarsa decemlineata) is an important pest of potato (see Chapter 4 for details) that has been used as a model species to characterize the steps involved in insecticidal RNAi and their relevance (Fig. 12.1). Uptake of dsRNA in gut cells of L. decemlineata involves channel proteins with homology to the systemic RNA interference-deficiency (SID) proteins of C. elegans, as well as clathrin-mediated dsRNA endocytosis (Cappelle et al., 2016). Upon uptake into the cytoplasm, the dsRNA is cleaved into 21e25 bp long small interfering RNAs (siRNAs) by action of a multidomain ribonuclease (RNase) type III enzyme called Dicer. Processing of dsRNA to siRNAs in L. decemlineata seems to require the dsRNA-binding protein StaufenC, and reduced StaufenC expression is associated with resistance to dsRNA in cultured cells (Yoon et al., 2018). The generated siRNAs are loaded into the RNA induced silencing complex (RISC) and unwound, yielding a guide strand complementary to the target mRNA and a passenger strand that is degraded. The guide strand directs binding of the RISC complex to the complimentary mRNA, which is followed by its degradation by the RNAase protein Argonaute. Degradation of a target mRNA encoding an essential insect protein can result in growth inhibition (Mao et al., 2007; Zhu et al., 2012), developmental abnormalities (Xiong et al., 2013) and/or mortality (Baum et al., 2007). Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00021-4 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 12.1 Schematic diagram of the mode of action of insecticidal RNAi in the Colorado potato beetle.

12.2 Parameters affecting insecticidal activity of dsRNA Efficiency of dsRNA varies depending on a number of factors including insect species, target gene, dsRNA design, method of delivery and dsRNA dosage. In general, species in Coleoptera are the most sensitive to dsRNA while lepidopterans and hemipterans are largely recalcitrant (Cooper et al., 2019). Critical but not sufficient to insecticidal RNAi is the existence of a complete core RNAi machinery, including Argonaute (Ago), Dicer (Dcr) and RNA binding protein (R2D2) genes in the targeted pest (Dowling et al., 2016). For example, distinct susceptibility to dsRNA among L. decemlineata instars correlates with expression levels of core RNAi machinery genes (Guo et al., 2015), and relatively high susceptibility to dsRNA in this insect may be associated with duplicated core components of the siRNA pathway (Schoville et al., 2018). Lack of susceptibility to dsRNA may also be dictated by physiological adaptations. For instance, gut nucleases degrading dsRNA and entrapment of dsRNA in early and late endosomes after uptake explain insensitivity of lepidopteran insects to dsRNA (Arimatsu et al., 2007; Yoon et al., 2017). Gut nucleases also affect dsRNA activity in other insects, including L. decemlineata (Spit et al., 2017). Consequently, efforts have focused on improving insecticidal RNAi by increasing dsRNA stability and/or uptake using nuclease inhibitors (Castellanos et al., 2019), formulating dsRNA with synthetic polymers (Christiaens et al., 2019; Parsons et al., 2018), and encapsulating with transfection reagents (Whyard et al., 2009) or clay nanosheets (Mitter et al., 2017). Recent evidence suggests that uptake of dsRNA with a “paperclip” structure by an undescribed mechanism may overcome insect recalcitrance to RNAi when is related to reduced dsRNA uptake (Abbasi et al., 2020). The choice of target gene also contributes to the probability of successful insecticidal RNAi. The optimal target gene has stable, high level expression and encodes a vital protein that performs essential functions that cannot be rescued by other gene products. Large scale RNAi screens in model insects, such as Tribolium castaneum (Ulrich et al., 2015) or Drosophila melanogaster (Bingsohn et al., 2017; Danielsen et al., 2016) have helped identify genes involved in immunity and the proteasome as prime targets. Orthologues in crop pests to targets identified in these model organisms are reported as effective targets (Knorr et al., 2018). Mechanisms explaining distinct target efficacy include feedback mechanisms increasing rates of target gene transcription, target transcripts being short-lived and not allowing completion of the RNAi process, and sequence-specific stability of certain dsRNA molecules (Bellés, 2010). For any specific target gene, the dsRNA sequence, length and dosage affect its ability to elicit an insecticidal RNAi response. Some evidence suggests that in insects dsRNA cleavage may have sequence preference (Guan et al., 2018).

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Longer dsRNA molecules allow production of a higher number of distinct siRNAs during cleavage by Dicer, potentially increasing RNAi efficiency. On the other hand, longer dsRNAs also have higher probability of producing siRNAs matching non-target mRNAs in the same or related insect species, potentially reducing specificity. In addition, there is evidence that dsRNA length may influence uptake by the cell (Bolognesi et al., 2012). Typically, dsRNAs in the 200e400 bp range are used for effective and specific activity, with a single 21 bp fragment matching the target mRNA being sufficient to elicit a lethal RNAi response. While increasing dsRNA dose is expected to augment RNAi efficacy, high dsRNA dosage or treatment with multiple dsRNAs can lead to oversaturation of the RNAi machinery, resulting in an inefficient RNAi response (Miller et al., 2012). Determining the optimal length, sequence and dosage for a particular dsRNA is important when considering the cost of dsRNA production, especially for application in large crop field extensions.

12.3 Delivery of dsRNA to potato pests Commercial development of dsRNA-based insecticidal products depends on the feasibility of a dsRNA delivery method for the target pest considered. The dsRNA should be available in parts of the plant involved in the feeding habits of the target pest (leaf chewing, sap sucking or root feeding). Typically, dsRNA delivery approaches are broadly classified into transgenic (or transformative) when they involve production of the dsRNA in the host (also called host-induced gene silencing, HIGS), and non-transgenic (or non-transformative) mostly involving formulations incorporating dsRNA. An example of HIGS against a potato pest is the use of transgenic potato plants producing dsRNA to control L. decemlineata. Nuclear dsRNA expression in this case can result in processing by plant cell nucleases to small RNAs which may be ineffective against the targeted insect. Alternatively, production of the dsRNA in the nuclease-free chloroplast environment overcomes this limitation and allows for stable accumulation of high levels of dsRNA. Therefore, transplastomic potato expressing dsRNA is more effective in L. decemlineata control compared to potato plants expressing the dsRNA in the nucleus (Zhang et al., 2015). An additional advantage of the transplastomic approach for regulatory purposes is that dsRNA expression is limited to photosynthetic (mainly leaves) tissues where the insect feeds, while potato tubers and pollen are essentially dsRNA-free and safe for animal and human consumption. In both nuclear and plastid expression, dsRNA may be combined with other plant-incorporated protectants (PIPs) with distinct mode of action, such as insecticidal proteins from bacteria, to broaden range of activity and extend durability. Non-transgenic dsRNA delivery against potato pests includes topical dsRNA sprays and root drenches. Both methods involve dsRNA products with lower developmental costs and a more streamlined regulatory pathway compared to transgenic technologies and are also not affected by still low acceptability of genetically modified plants by consumers. While sprays and drenches allow better control over the dsRNA dosage, they are also susceptible to dsRNA degradation by nucleases in the environment and wash-off, which may add extra labor and costs because of the need for repeated application. Effective use of foliar dsRNA sprays, also known as spray induced gene silencing (SIGS), has been demonstrated for L. decemlineata in greenhouse (San Miguel and Scott, 2016) and field tests (Bramlett et al., 2020; Petek et al., 2020). Although foliar dsRNA sprays provide an efficient control strategy for leaf-chewing insects, they are probably ineffective against insects feeding on phloem sap or plant stems. While not yet tested against potato pests, immersion, irrigation and root drenching with a dsRNA solution followed by absorption of the dsRNA by plant roots and tissues can induce insecticidal RNAi in insects feeding on the plant (Ghosh et al., 2018), providing effective control of pierce-sucking and stem-borer insects. To have practical application, non-transgenic dsRNA delivery methods require production of large quantities of dsRNA in a cost-effective manner, competitive with production costs for synthetic chemical insecticides. A proprietary cell-free bioprocessing platform has been used to produce Ledprona, the first sprayable dsRNA pesticide targeting an essentil gene to control L. decemlineata (Rodrigues et al., 2021a), currently undergoing regulatory review. While displaying slower toxicity, reduced production costs and comparatively high activity could make this product cost-competitive with chemical pesticides (Rodrigues et al., 2021b). An alternative approach is engineering microbes (bacteria, fungi, and viruses) to produce the dsRNA. For instance, in virus-induced gene silencing (VIGS) the dsRNA target is introduced in the genome of a virus specific to the target insect species so that viral replication produces dsRNA inside the host insect cell (Taning et al., 2018). This technique adds the specificity of virus-host interactions to the dsRNA sequence specificity of insecticidal RNAi technology. Similarly, a RNAase III-deficient strain of the bacterium Escherichia coli was engineered to produce dsRNAs targeting essential genes in L. decemlineata, and feeding on the bacteria caused significant reduction in target transcript levels and larval growth and survival (Zhu et al., 2011).

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12.4 Safety of insecticidal dsRNA As for any new insecticidal technology, it is important to consider the potential effects of dsRNA insecticides on non-target organisms, the environment, as well as safety of treated food products. Risks related to both transgenic (Bachman et al., 2016) and non-transgenic (Romeis and Widmer, 2020) dsRNA delivery approaches are examined as part of the registration process before approval for commercialization. The high specificity dictated by dsRNA sequence complementarity provides one of the most specific insecticidal modes of action available. Experimental evidence supports that dsRNA toxicity depends on the number of contiguous random 21 bp matches between the dsRNA and a transcript (Bachman et al., 2013). For instance, dsRNA targeting the V-ATPase subunit A gene of D. v. virgifera displayed >10-fold lower activity in L. decemlineata compared to D. v. virgifera, even though the gene displays 83% sequence identity between the two species (Baum et al., 2007). Thus, careful consideration of the dsRNA sequence is important to ensure little to no identity to any gene in a non-target organism. Availability of insect genomic and transcriptomic resources allows in silico prediction of potential risks to non-target species due to sequence identity (Mogren and Lundgren, 2017). However, any potential effects predicted in silico need to be experimentally tested because eliciting a toxic RNAi response depends on additional parameters beyond sequence identity. For instance, dsRNA targeting the V-ATPase subunit A gene in honeybee (Apis mellifera) had no impact on adult survival (Vélez et al., 2016), demonstrating that sequence identity alone is insufficient to observe a toxic RNAi effect and highlighting the importance of bioassays in assessing potential off-target effects. Environmental risk assessment for transgenic maize plants producing dsRNA targeting the vacuolar sorting protein Snf7 transcript in D. v. virgifera did not detect deleterious effects even at the maximum expected environmental exposure in any of the non-target arthropods, beneficial soil microbes, and aquatic and terrestrial vertebrates tested (Bachman et al., 2016). Another important consideration in assessing risks of dsRNA is its availability and persistence in the environment after application. Persistence tests in soil and sediment-water support that topical dsRNA degrades within 2 days of application (Dubelman et al., 2014; Fischer et al., 2017), reducing environmental risks of run off to water sources, bioaccumulation and biomagnification. However, dsRNA formulation that increases efficacy in field applications may involve enhanced stability and/or persistence. Therefore, it is advisable to conduct stability and off-target impact tests for finalized dsRNA products in a case-by-case manner. The vertebrate system presents physiological barriers to consumed dsRNAs, including nucleases in saliva or blood and gastrointestinal tract, along with the highly acidic environment in the stomach (Petrick et al., 2013). Consequently, significant systemic absorption of intact dsRNAs after ingestion of materials treated with dsRNA-based biopesticides is highly improbable in humans and other vertebrates (Rodrigues and Petrick, 2020). Additionally, studies have also shown that the bioavailability of diet-derived dsRNAs is considerably lower in magnitude compared to that required for biological activity (Cottrill and Chan, 2014; Dickinson et al., 2013; Snow et al., 2013). The long history of safe consumption of naturally occurring dsRNAs in plants and other foods (Zeng et al., 2019), even when significant identity between dsRNAs and human genes exists (Ivashuta et al., 2009; Jensen et al., 2013), further supports safety of dsRNA pesticides for food production.

12.5 Use of dsRNA against potato pests Insecticidal dsRNA technology has demonstrated promising results in a considerable number of studies testing diverse dsRNA gene targets against potato insect pests (Table 12.1), as discussed in the following sections. This technology represents a safer alternative to current control strategies for pests of cultivated potato, which mostly focus on the use of small molecule insecticides with broader specificity. Not included in Table 12.1 is the first sprayable dsRNA pesticide against a potato pest (L. decemlineata), which is currently undergoing regulatory review for commercialization and targets proteasome subunit beta 5 (Rodrigues et al., 2021a).

12.5.1 Potato psyllid (Bactericera cockerelli) The potato psyllid is a serious pest feeding on phloem of solanaceous plants and can also vector the zebra chip disease of potatoes caused by the endosymbiont Candidatus Liberibacter psyllaurous (solanacearum) (Munyaneza et al., 2007). Typically, hemipteran insects such as B. cockerelli are not as susceptible to dsRNA when compared to the vigorous response observed in coleopterans. Though not fully understood, factors such as lack of core RNAi machinery components, degradation of dsRNA in insect guts, and inefficient uptake of dsRNA by insect gut cells are some plausible explanations for this lack of robust RNAi response in hemipteran insects, as reviewed elsewhere (Christiaens and Smagghe, 2014). Accordingly, different dsRNA delivery methods tested to induce an RNAi response in B. cockerelli, resulted in

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TABLE 12.1 List of published examples of dsRNA targets effective against potato pests. Insect

Gene target

References

Potato psyllid (Bactericera cockerelli)

Actin, ATPase, Hsp70 and CLIC

Wuriyanghan et al. (2011)

Osmoregulatory genes

Tzin et al. (2015)

28-Spotted potato ladybird (Henosepilachna vigintioctopunctata)

vATPase B

Lu¨ et al. (2020a,b)

Ecdysone receptor

Wu et al. (2020)

Colorado potato beetle (Leptinotarsa decemlineata)

vATPase A and E

Baum et al. (2007)

Actin, Sec23, vATPase E and B, and COPb

Zhu et al. (2011)

Ecdysone receptor

Hussain et al. (2019)

Chitin synthase

Shi et al. (2016)

Taiman

Xu et al. (2019)

Juvenile hormone acid methyltransferase

Guo et al. (2018)

Inhibitor of apoptosis

Ma´ximo et al. (2020)

b-Actin

He et al. (2020), Zhang et al. (2015)

Hormone receptor 38 (HR38)

Shen et al. (2020)

Broad complex (BrC)

Xu et al. (2019)

Mesh

Petek et al. (2020)

Actin

Mehlhorn et al. (2020), San Miguel and Scott (2016)

Hunchback

Mao and Zeng (2014)

Voltage-gated sodium channels

Tariq et al. (2019)

Chitin synthase A

Mohammed et al. (2017)

Green peach aphid (Myzus persicae)

Potato tuber moth (Phthorimaea operculella)

modest reductions in target transcript levels and insect mortality. An initial study showed mortality doubled when comparted to controls in treatments with injection or oral delivery of dsRNAs or siRNAs targeting Actin, ATPase, Hsp70 or CLIC genes in adult B. cockerelli (Wuriyanghan et al., 2011). An alternative study used VIGS to deliver siRNAs targeting B. cockerelli Actin and ATPase genes through a recombinant tobacco mosaic virus, resulting in reduced psyllid fecundity (Wuriyanghan and Falk, 2013). Transgenic tomato plants expressing dsRNA against the aquaporin gene caused w40% mortality in female B. cockerelli (Tzin et al., 2015). These results suggest preliminary evidence that further optimization of delivery may lead to levels of activity needed for commercial use of insecticidal dsRNA against B. cockerelli.

12.5.2 The 28-spotted potato ladybird (Henosepilachna vigintioctopunctata) The 28-spotted potato ladybird or Hadda beetle is a pest of solanaceous and cucurbit plants native to southeastern Asia, but it has also spread to Brazil, Argentina, Australia, and New Zealand. Feeding damage on leaves by H. vigintioctopunctata results in plant growth retardation and subsequent yield losses. The amenability of coleopteran insects to a potent RNAi response suggested H. vigintioctopunctata as a potential candidate for control with dsRNA technology. Feeding third instar H. vigintioctopunctata larvae with dsRNA targeting the death-associated inhibitor of apoptosis protein 1 (diap1) gene resulted in rapid feeding cessation, but this was not observed with dsRNA targeting the v-ATPase A and E genes (Chikami et al., 2019). Similar results were reported when the dsRNA targeting diap 1 was encapsulated in the bacterium Corynebacterium glutamicum (Hashiro et al., 2019). Similarly, feeding on eggplant leaf discs coated with E. coli cultures expressing dsRNA targeting the v-ATPase B (Lü et al., 2020a) and vacuolar sorting protein SNF7 (Lü et al., 2020b) genes increased H. vigintioctopunctata mortality by 15- and 21-fold,

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respectively. Greenhouse assays using spraying of potato plants with bacteria expressing dsRNA targeting the ecdysone receptor gene inhibited the H. vigintioctopunctata larva-pupa transition and reduced leaf consumption (Wu et al., 2020). These observations confirm the potential for developing dsRNA-based products against H. vigintioctopunctata.

12.5.3 Colorado potato beetle (Leptinotarsa decemlineata) Larvae of L. decemlineata can completely skeletonize potato plants and result in complete crop losses, and this pest is known to have an impressive ability to develop resistance against almost all known classes of pesticides (Alyokhin et al., 2008). These features, together with the high susceptibility of L. decemlineata to dsRNA (Baum et al., 2007) identifies this pest as an optimal model for development of insecticidal RNAi products. In consequence, a number of target genes and various dsRNA delivery methods including foliar sprays, bacterially expressed dsRNA, and transgenic potato plants, have been shown effective against L. decemlineata. Diet feeding tests identified dsRNAs targeting the V-ATPase subunit A and subunit E genes as highly effective against L. decemlineata larvae (Baum et al., 2007). In greenhouse tests, dsRNA targeting the L. decemlineata Actin gene protected the plants for up to 28 days and was not readily washed off from the leaves once dried (San Miguel and Scott, 2016). Heatkilled E. coli cells expressing dsRNAs targeting the Actin, transport protein SEC23 (Sec23), vATPase B, and coatomer subunit beta (COPb) genes produced w100% mortality when fed to L. decemlineata larvae (Zhu et al., 2011). In the same study, dsRNA targeting the vATPase E gene resulted in w50% mortality, highlighting the importance of target gene selection for efficient insect control. The first product based on a sprayable dsRNA targeting L. decemlineata (Ledprona) has demonstrated promising results and is undergoing regulatory review for commercialization (Rodrigues et al., 2021b). This dsRNA induces downregulation of the proteasome subunit beta 5 (PSMB5) gene in L. decemlineata larvae, which in greenhouse trials translates to 100% mortality and reduced defoliation compared to controls 14 days after treament (Rodrigues et al., 2021a). In addition to sprayable dsRNA delivery, transgenic potato lines expressing dsRNA targeting the juvenile hormone acid methyltransferase (JHAMT) gene were shown to affect fecundity and reduce L. decemlineata populations in field trials (Guo et al., 2018). High levels of toxicity to L. decemlineata where achieved by expressing dsRNA targeting the actin gene in the chloroplast versus the nucleus (Zhang et al., 2015), supporting the future use of these transplastomic potato plants for L. decemlineata control.

12.5.4 Myzus persicae (green peach aphid) The major damage caused by M. persicae is not due to direct feeding on its host plants but due to the transmission of a variety of pathogens such as Potato Y and Potato leafroll viruses, making it one of the most destructive agricultural pests in the world (Hogenhout et al., 2008). Furthermore, development of resistance against pesticides has fueled interest in developing RNAi-based strategies to control this pest. As evidence for the potential use of RNAi in addressing vectoring capacity of M. persicae, silencing the cuticular protein MCPCP2 gene reduced Potato virus Y transmission 47% compared to controls (Bahrami Kamangar et al., 2019). However, the efficacy of dietary dsRNA in this insect appears greatly challenged by production of midgut nucleases (Ghodke et al., 2019). Experiments with artificial diet containing dsRNA targeting the voltage-gated sodium channels (VGSC) gene resulted in up to 65% mortality in third instar M. persicae nymphs, along with significantly lower fecundity and longevity in adults (Tariq et al., 2019). Delivery of dsRNA targeting the cuticle protein 19 (CP19) to M. persicae adults through a Brassica leaf resulted in 11,100fold) were recorded in a strain of L. decemlineata selected with a topically delivered dsRNA targeting the V-ATPase subunit A gene (Mishra et al., 2021). Although the mechanism of resistance in this strain is yet to be reported, crossresistance to an alternative dsRNA target supports that mutations in the target gene are not involved. Resistance in both D. v. virgifera and L. decemlineata was transmitted as an autosomal recessive trait located to a single locus in D. v. virgifera, while in L. decemlineata resistance was polygenic. In agreement with their distinct mode of action, dsRNAresistant D. v. virgifera and L. decemlineata remained susceptible to Cry3 insecticidal proteins from Bacillus thuringiensis. Whether resistance to dsRNA affects susceptibility to synthetic and semi-synthetic pesticides is yet unknown. Future identification of resistance genes will allow estimations of field allele frequency to assess the risk of resistance evolution. The available information from resistance studies guides the design of insecticide resistance management (IRM) strategies within an integrated pest management (IPM) framework for dsRNA pesticides and transgenic plants (see also Chapters 24, 26, and 27). Under the umbrella of IPM, one major focus of IRM is combining insecticides with distinct modes of action (MOA) at the required dose to avoid major selection pressure to a single insecticide. An alternative to this strategy is the use of rotations so that multiple generations of an insect are exposed to distinct MOA. Currently available information supports combining or rotating dsRNA with pesticides containing insecticidal proteins from B. thuringiensis or pyramiding with these protein genes in transgenic plants to reduce the risk of resistance evolution. Importantly, so far resistance to dsRNA seems independent of the target gene, arguing against combining different dsRNA targets in a single product. Based on the recessive transmission reported for the available cases of resistance to dsRNA so far, a beneficial IRM tool for transgenic dsRNA would be the use of the refuge paradigm of untreated plants from crops producing B. thuringiensis insecticidal proteins. This strategy provides a susceptible population for mating with resistant individuals, increasing the frequency of heterozygotes, which would be susceptible to the dsRNA, and effectively diluting resistance allele frequency. Economic issues related to maintaining an effective refuge risks refuge compliance by farmers, a major hurdle in the effective implementation of this strategy. c.

12.7 Conclusions and future prospects Suppression of vital insect gene expression using complementary dsRNA provides a highly specific and environmentally sustainable insecticidal mode of action. It is expected that dsRNA-based biopesticides will be approved and

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commercialized soon for the control of L. decemlineata. Transplastomic potato plants are highly effective and provide expression of dsRNA localized to tissues consumed by L. decemlineata and may possibly undergo regulatory review in the near future. The potential use of dsRNA technology to control other insect pests of potato requires further research to increase efficacy by identifying effective target genes and increasing dsRNA stability and delivery. This RNAi technology fits well with IPM programs aimed at maintaining potato pests under economic thresholds. As for any insecticidal technology, insects are expected to develop resistance against dsRNA technology. While information on resistance to dsRNA is currently limited, it supports implementation of IRM strategies such as combining multiple modes of action and implementing refuges to help ensure sustainable use of the insecticidal dsRNA technology against potato pests.

Acknowledgments The authors would like to thank support from the Biotechnology Risk Assessment Grant (BRAG) program grant no. 2020-33522-32315 from the USDA National Institute of Food and Agriculture.

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Mingels, L., Wynant, N., Santos, D., Peeters, P., Gansemans, Y., Billen, J., Van Nieuwerburgh, F., Vanden Broeck, J., 2020. Extracellular vesicles spread the RNA interference signal of Tribolium castaneum TcA cells. Insect Biochem. Mol. Biol. 122, 103377.

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Mishra, S., Dee, J., Moar, W., Dufner-Beattie, J., Buam, J., Dias, N.P., Alyokhin, A., Buzza, A., Rondon, S.I., Clough, M., Menasha, S., Groves, R., Clements, J., Ostlie, K., Felton, G., Waters, T., Snyder, W.E., Jurat-Fuentes, J.L., 2021. Selection for high levels of resistance to double-stranded RNA (dsRNA) in Colorado potato beetle (Leptinotarsa decemlineata Say) using non-transformative foliar delivery. Sci. Rep. 11, e6523. Mitter, N., Worrall, E.A., Robinson, K.E., Li, P., Jain, R.G., Taochy, C., Fletcher, S.J., Carroll, B.J., Lu, G.M., Xu, Z.P., 2017. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Native Plants 3, 1e10. Mogren, C.L., Lundgren, J.G., 2017. In silico identification of off-target pesticidal dsRNA binding in honey bees (Apis mellifera). PeerJ 5, e4131. Mohammed, A.M.A., Diab, M.R., Abdelsattar, M., Khalil, S.M.S., 2017. 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Plant Sci. 11, 1250. Petrick, J.S., Brower-Toland, B., Jackson, A.L., Kier, L.D., 2013. Safety assessment of food and feed from biotechnology-derived crops employing RNAmediated gene regulation to achieve desired traits: a scientific review. Regul. Toxicol. Pharmacol. 66, 167e176. Rodrigues, T.B., Petrick, J.S., 2020. Safety considerations for humans and other vertebrates regarding agricultural uses of externally applied RNA molecules. Front. Plant Sci. 11, 407. Rodrigues, T.B., Sambit, S.K., Sridharan, K., Barnes, E.R., Alyokhin, A., Tuttle, R., Kokulapalan, W., Garby, D., Skizim, N.J., Tang, Y.-W., Manley, B., Aulisa, L., Flannagan, R.D., Cobb, C., Narva, K.E., 2021. First sprayable double-stranded RNA-based biopesticide product targets Proteasome Subunit Beta Type-5 in Colorado potato beetle (Leptinotarsa decemlineata). Front. Plant Sci. 12. https://doi.org/10.3389/fpls.2021.728652. Rodrigues, T., Sridharan, K., Manley, B., Cunningham, D., Narva, K., 2021. 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Schoville, S.D., Chen, Y.H., Andersson, M.N., Benoit, J.B., Bhandari, A., Bowsher, J.H., Brevik, K., Cappelle, K., Chen, M.J.M., Childers, A.K., Childers, C., Christiaens, O., Clements, J., Didion, E.M., Elpidina, E.N., Engsontia, P., Friedrich, M., García-Robles, I., Gibbs, R.A., Goswami, C., Grapputo, A., Gruden, K., Grynberg, M., Henrissat, B., Jennings, E.C., Jones, J.W., Kalsi, M., Khan, S.A., Kumar, A., Li, F., Lombard, V., Ma, X., Martynov, A., Miller, N.J., Mitchell, R.F., Munoz-Torres, M., Muszewska, A., Oppert, B., Palli, S.R., Panfilio, K.A., Pauchet, Y., Perkin, L.C., Petek, M., Poelchau, M.F., Record, É., Rinehart, J.P., Robertson, H.M., Rosendale, A.J., Ruiz-Arroyo, V.M., Smagghe, G., Szendrei, Z., Thomas, G.W.C., Torson, A.S., Vargas Jentzsch, I.M., Weirauch, M.T., Yates, A.D., Yocum, G.D., Yoon, J.S., Richards, S., 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Sci. Rep. 8, 1931. Shang, F., Ding, B., Ye, C., Yang, L., Chang, T., Xie, J., Tang, L., Niu, J., Wang, J., 2020. Evaluation of a cuticle protein gene as a potential RNAi target in aphids. Pest Manag. Sci. 76, 134e140. Shen, C., Xu, Q., Mu, L., Fu, K., Guo, W., Li, G., 2020. Involvement of Leptinotarsa hormone receptor 38 in the larval-pupal transition. Gene 751, e144779. Shi, J., Mu, L., Chen, X., Guo, W., Li, G., 2016. RNA interference of chitin synthase genes inhibits chitin biosynthesis and affects larval performance in Leptinotarsa decemlineata (Say). Int. J. Biol. Sci. 12, 1319e1331. Snow, J.W., Hale, A.E., Isaacs, S.K., Baggish, A.L., Chan, S.Y., 2013. Ineffective delivery of diet-derived microRNAs to recipient animal organisms. RNA Biol. 10, 1107e1116. Spit, J., Philips, A., Wynant, N., Santos, D., Plaetinck, G., Vanden Broeck, J., 2017. Knockdown of nuclease activity in the gut enhances RNAi efficiency in the Colorado potato beetle, Leptinotarsa decemlineata, but not in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 81, 103e116. Taning, C.N., Christiaens, O., Li, X., Swevers, L., Casteels, H., Maes, M., Smagghe, G., 2018. Engineered flock house virus for targeted gene suppression through RNAi in fruit flies (Drosophila melanogaster) in vitro and in vivo. Front. Physiol. 9, 805. Tariq, K., Ali, A., Davies, T.G.E., Naz, E., Naz, L., Sohail, S., Hou, M., Ullah, F., 2019. RNA interference-mediated knockdown of voltage-gated sodium channel (MpNav) gene causes mortality in green peach aphid, Myzus persicae. Sci. Rep. 9, 5291. Tzin, V., Yang, X., Jing, X., Zhang, K., Jander, G., Douglas, A.E., 2015. RNA interference against gut osmoregulatory genes in phloem-feeding insects. J. Insect Physiol. 79, 105e112. Ulrich, J., Dao, V.A., Majumdar, U., Schmitt-Engel, C., Schwirz, J., Schultheis, D., Ströhlein, N., Troelenberg, N., Grossmann, D., Richter, T., Dönitz, J., Gerischer, L., Leboulle, G., Vilcinskas, A., Stanke, M., Bucher, G., 2015. Large scale RNAi screen in Tribolium reveals novel target genes for pest control and the proteasome as prime target. BMC Genom. 16, 674. Vélez, A.M., Jurzenski, J., Matz, N., Zhou, X., Wang, H., Ellis, M., Siegfried, B.D., 2016. Developing an in vivo toxicity assay for RNAi risk assessment in honey bees, Apis mellifera L. Chemosphere 144, 1083e1090.

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Vogel, E., Santos, D., Mingels, L., Verdonckt, T.W., Broeck, J.V., 2019. RNA interference in insects: protecting beneficials and controlling pests. Front. Physiol. 9, 1912. Whyard, S., Singh, A.D., Wong, S., 2009. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol. 39, 824e832. Wingard, S.A., 1928. Hosts and symptoms of ring spot, a virus disease of plants. J. Agric. Res. 37, 127e153. Wu, J.J., Mu, L.L., Kang, W.N., Ze, L.J., Shen, C.H., Jin, L., Anjum, A.A., Li, G.Q., 2020. RNA interference targeting ecdysone receptor blocks the larvalepupal transition in Henosepilachna vigintioctopunctata. Insect Sci. 1277. Wuriyanghan, H., Rosa, C., Falk, B.W., 2011. Oral delivery of double-stranded RNAs and siRNAs induces RNAi effects in the potato/pomato psyllid, Bactericerca cockerelli. PLoS One 6, e27736. Wuriyanghan, H., Falk, B.W., 2013. RNA interference towards the potato psyllid, Bactericera cockerelli, is induced in plants infected with recombinant Tobacco mosaic virus (TMV). PLoS One 8, e66050. Xiong, Y., Zeng, H., Zhang, Y., Xu, D., Qiu, D., 2013. Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. Int. J. Biol. Sci. 9, 370e381. Xu, Q., Deng, P., Mu, L., Fu, K., Guo, W., Li, G., 2019. Silencing Taiman impairs larval development in Leptinotarsa decemlineata. Pestic. Biochem. Physiol. 160, 30e39. Xu, Q., Meng, Q., Deng, P., Fu, K., Guo, W., Li, G., 2019. Impairment of pupation by RNA interference-aided knockdown of Broad-Complex gene in Leptinotarsa decemlineata (Say). Bull. Entomol. Res. 109, 659e668. Yoon, J.S., Gurusamy, D., Palli, S.R., 2017. Accumulation of dsRNA in endosomes contributes to inefficient RNA interference in the fall armyworm, Spodoptera frugiperda. Insect Biochem. Mol. Biol. 90, 53e60. Yoon, J.-S., Mogilicherla, K., Gurusamy, D., Chen, X., Chereddy, S.C.R.R., Palli, S.R., 2018. Double-stranded RNA binding protein, Staufen, is required for the initiation of RNAi in coleopteran insects. Proc. Natl. Acad. Sci. U. S. A. 115, 8334e8339. Zeng, J., Gupta, V.K., Jiang, Y., Yang, B., Gong, L., Zhu, H., 2019. Cross-kingdom small RNAs among animals, plants and microbes. Cells 8, 371. Zhang, J., Khan, S.A., Hasse, C., Ruf, S., Heckel, D.G., Bock, R., 2015. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347, 991e994. Zhang, X., Zhang, J., Zhu, K.Y., 2010. Chitosan/double-stranded RNA nanoparticle-mediated RNA interference to silence chitin synthase genes through larval feeding in the African malaria mosquito (Anopheles gambiae). Insect Mol. Biol. 19, 683e693. Zhou, X., Oi, F.M., Scharf, M.E., 2006. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. U. S. A. 103, 4499e4504. Zhu, F., Xu, J., Palli, R., Ferguson, J., Palli, S.R., 2011. Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Manag. Sci. 67, 175e182. Zhu, J.Q., Liu, S., Ma, Y., Zhang, J.Q., Qi, H.S., Wei, Z.J., Yao, Q., Zhang, W.Q., Li, S., 2012. Improvement of pest resistance in transgenic tobacco plants expressing dsRNA of an insect-associated gene EcR. PLoS One 7, e38572.

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Chapter 13

Biological and behavioral control of potato insect pests Donald C. Webera, Michael B. Blackburna and Stefan T. Jaronskib a

Invasive Insect Biocontrol and Behavior Laboratory, USDA Agricultural Research Service, Beltsville, MD, United States; bJaronski Mycological

Consulting LLC, Virginia Polytechnic Institute and State University, Department of Entomology, Blacksburg, VA, United States

13.1 Introduction Biological controls and semiochemicals which are usually more or less specific to the target pest have enormous potential to suppress potato insect pests in the context of integrated pest management, compatible with cultural controls, pest thresholds, and a variety of other intervention tactics such as trap cropping and selective insecticides. Here we discuss viral, bacterial, fungal, nematode and arthropod natural enemies of major potato pests with an emphasis on those pests more or less specific to the potato crop: Colorado potato beetle, gelechiid tuber moths, herbivorous lady beetles, Andean potato weevil complex, and potato psyllid. This excludes in-depth discussion of such important groups as aphids, leafhoppers, scarab grubs, and wireworms, which are, nevertheless, key pests in many potato systems. These are covered in more detail in other chapters.

13.2 Natural enemies of major potato pests 13.2.1 Colorado potato beetle (Coleoptera: Chrysomelidae) Colorado potato beetle (Leptinotarsa decemlineata (Say)) now ranges throughout most of the north temperate zone, with the exceptions of the British Isles, south and southeast Asia. Since it is native to southwestern North America, almost all of its current range reflects recent invasions, and its cultivated hosts e principally potato, eggplant, and tomato e are both novel and recent (Weber, 2003; see Chapter 4 on details of its biology). Native natural enemies of Colorado potato beetle were described by Walsh and Riley (1868), and only one major species (the carabid beetle Lebia grandis) has been added to that early list. Soon after Ferro’s (1994) review of the arthropod and microbial natural enemies, the introduction of the neonicotinoid imidacloprid decreased interest in Colorado potato beetle biological control in North America and elsewhere. This occurred despite pesticide resistance remaining an ever-present risk with this insect, and the repeated lesson that resistance risk is mitigated by a suite of alternative tactics such as crop rotation and other cultural practices, as well as microbial and biological controls (Alyokhin et al., 2013, 2015). The recent growth of organic potato culture has increased interest in non-chemical controls as part of sustainable Colorado potato beetle management. This trend, as well as the expansion of Colorado potato beetle to the east in Asia, where it threatens to impact the crops of the two leading potato-growing nations, China and India, has also heightened interest in possibilities for classical biological control with the three species of Colorado potato beetle parasitoids commonly attacking the pest in North America. Colorado potato beetle populations in North America are commonly preyed upon by several species of native and exotic lady beetles, a specialized carabid which is also a pupal parasitoid, a few species of asopine stink bugs, two species of tachinid parasitoids, and a variety of generalist arthropod predators including predatory bugs of the genera Orius, Geocoris, and Nabis, Carabidae, Cantharidae, and Opiliones (Ferro, 1994; Heimpel and Hough-Goldstein, 1992; Hilbeck and Kennedy, 1996; Weber et al., 2008). Entomopathogens can also be important as natural enemies and as inundative or augmented management tools (Sporleder and Lacey, 2013, and below). Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00013-5 Copyright © 2022, Published by Elsevier Inc.

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13.2.1.1 Bacteria and Colorado potato beetle Bacillus thuringiensis (Bt) is a spore-forming bacterium belonging to the Bacillus cereus complex. The feature that has classically been used to differentiate it from other members of this group is the production of a protein crystal when the bacterium sporulates. These crystalline proteins, or Cry proteins, may be toxic to certain insects upon ingestion, lysing cells of the midgut epithelium. Most often, Bt is toxic to lepidopteran, dipteran, or coleopteran species. Historically, Bt is the most widely used bacterial entomopathogen for insect control, and several varieties are effective against Colorado potato beetle. Bt formulations used for insect control are mixtures of dormant bacterial spores and crystalline toxin proteins. Insect suppression is achieved largely by the immediate action of the toxins on the midgut, and much less by the eventual bacterial growth from the spores. In this regard, Bt is more a bioinsecticide than a true biological control agent. Genes encoding Cry proteins have been also used to create Colorado potato beetle resistant transgenic potatoes, e.g., the oncecommercialized NewLeaf potato (Thornton, 2003). An early study demonstrated that Colorado potato beetle larvae were susceptible to the Cry proteins of Bt var. kurstaki (Btk), which is widely used for control of lepidopteran pests; first instar larvae fed potato foliage dipped in Btk experienced 57.8% mortality at a concentration of Bt similar to that used for control of lepidopteran pests, and 98.6% mortality at three times that concentration (Ignoffo et al., 1982). Shortly after this, Krieg et al. (1983) described a novel variety of Bt that was highly active against Colorado potato beetle, Bt var. tenebrionis (Btt). Although serologically identical to Bt var. morrisoni, which is not effective against the beetle, Btt was shown to control Colorado potato beetle in a field trial at 5
1014 spores per hectare. Subsequently, another strain with similar activity, Bt var. san diego, was described (Herrnstadt et al., 1986). However, Bt var. san diego was shown to be identical to Btt (Krieg et al., 1987), and considered the same variety (ReyesRamirez and Ibarra, 2005). The enhanced activity of these beetle active strains was ultimately attributed to a new class of crystal proteins designated as Cry3Aa (Herrnstadt et al., 1987; Sekar et al., 1987). Ferro and Gelernter (1989) found that Btt controlled Colorado potato beetle in field tests, but that it had to be combined with conventional insecticides to suppress potato leafhopper and aphid populations ordinarily reduced by the conventional insecticides. Zehnder and Gelernter (1989) also showed that Btt reduced numbers of Colorado potato beetle larvae in the field, and demonstrated that younger larvae were far more susceptible than older larvae or adult beetles. Third-instar larvae were found to be capable of recovering from a 24 h exposure to treated plants, an important point considering the short half-life of Bt in the field. Another phenomenon limiting the effectiveness of Btt revealed in this study was the need for conventional insecticides to control adult beetles migrating into Bt treated fields. Although the Cry3Aa toxin from Btt (including Bt var. san diego) has been the dominant toxin employed against Colorado potato beetle, a variety of other Bt toxins from different varieties have been shown to be active against the beetle. These include Cry1Ba (Bradley et al., 1995), Cry1Ia (de Escudero et al., 2006), Cry3Ba (Donovan et al., 1988), Cry3Bb (Park et al., 2009), Cry3Ca (Lambert et al., 1992a), Cry7Aa (Lambert et al., 1992b), Cry8Aa (Foncerrada et al., 1994), Cry8Bb (Abad et al., 2012), Mpp51Aa (formerly Cry51Aa; Baum et al., 2012), and Cyt2Ca (Rupar et al., 2000). Cry3Bb, identified in Bt var. kumamotoensis, was found to be substantially more toxic to Colorado potato beetle larvae than the Cry3Aa proteins found in Btt, and was quite toxic to adult beetles (Johnson et al., 1993). To generate a product that controlled both lepidopteran and coleopteran pests, Ecogen introduced a Cry3A encoding plasmid from a Bt var. morrisoni strain to a Btk strain via natural conjugation, resulting in FoilÒ (Baum et al., 1999). In the field, Whalen and Spellman (1991) found Foil provided simultaneous control of Colorado potato beetle and European corn borer in potato. A number of bacteria that are not actual entomopathogens, nor true biological control agents, produce insecticidal metabolites. These include well-established insecticides such as spinosad originating from Saccharopolyspora spinosa or abamectin originating from Streptomyces avermitilis, as well as a number of newer products. One of these, Chromobacterium subtsugae, was discovered in toxicity bioassays against Colorado potato beetle larvae (Martin et al., 2007). In addition to Colorado potato beetle, C. subtsugae was shown to be toxic to a variety of pest insects, and was registered as the microbial pesticide GrandevoÔ by Marrone Bio Innovations. Asolkar et al. (2015) identified the insecticidal compounds produced by C. subtsugae as a cyclic peptide dubbed chromamide A, and the violet pigment violacein. Although active against Colorado potato beetle in laboratory bioassays, several trials have shown GrandevoÔ to have no effect on field populations of Colorado potato beetle (Wimer, 2013; DuPont, 2015; Groves et al., 2017; Nault and Seaman, 2019). Other bacteria which are toxic to Colorado potato beetle, and may have some potential for control, have been reported. Castrillo et al. (2000, 2001) described several species of ice-nucleating Pseudomonas that lowered the cold-hardiness of adult Colorado potato beetle when ingested. In Turkey, among several bacteria isolated from Colorado potato beetle larvae, Leclercia adecarboxylata and Pseudomonas putida were toxic per os to third instar larvae, resulting in 100% mortality in 5 d (Muratoglu et al., 2009, 2011). The insecticidal protein Tca, produced by the entomopathogenic nematode symbiont

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Photorhabdus luminescens, was found to be highly toxic to first instar Colorado potato beetle larvae, with a 48 h LD50 of 2.7 ppm when incorporated into an artificial diet. Growth of second instar larvae assessed at 72 h was almost entirely inhibited by concentrations higher than 0.5 ppm (Blackburn et al., 2005).

13.2.1.2 Entomopathogenic fungi and Colorado potato beetle Until the advent of coleopteran-active B. thuringiensis strains, B. bassiana was the principle microbial tool to manage L. decemlineata. Beauveria was used against Colorado potato beetle in the Soviet Union as early as the 1970s (Ferron, 1981). There was resurgence in interest by the Soviet agriculture ministry in developing large scale Beauveria production in the mid-1980s in conjunction with Abbott Laboratories, with a goal of treating 1.3 million hectares of potatoes with Beauveria to control the beetle. However, that program was aborted with the massive economic, political, and social restructuring of the USSR, 1986e1987 (perestroika) (Jaronski, personal information). Abbott Laboratories briefly pursued commercialization of a Beauveria against Colorado potato beetle, but efforts were abandoned in 1985 largely because of apparent inconsistent efficacy (Jaronski, personal communication). Eggs are not susceptible (Long et al., 1998) whereas early instars are more susceptible than the late instars, from 6-fold to 163-fold depending on the Beauveria strain used (Akbarian et al., 2012). The soil dwelling pupae are susceptible, with the fungus treatments reducing the following adult generation by as much as 74% in one study (Watt and Lebrun, 1984). A spray program comprising one Beauveria application targeting late-instar larvae reduced subsequent adult populations by an average of 60% (Wraight and Ramos, 2015). The Colorado potato beetle larvae persisted until entry into the soil to pupate; most deaths from fungus occurred among the prepupae in the soil. In these studies, the GHA strain of Beauveria was applied at 2.5
1013 ha1 in 468e480 L spray ha1, a typical, efficacious rate for this strain. The Beauveria multiple spray programs produced potato yield 18% greater than controls. Early experimental field work in the U.S., e.g., Hajek et al. (1987), demonstrated very variable, generally poor efficacy with an experimental strain ARSEF 252. Most of the subsequent research in the U.S. has been conducted with the commercial GHA strain. Poprawski et al. (1997) discerned that four early season applications (green-row and touch-in-row stages), made at 3e4 day intervals as beetle eggs were hatching, resulted in >90% mortality and mycosis after the last application. Targeting the early instars reduced the number of more damaging later instars. Galaini (1984) and Wraight and Ramos (2002) verified the need for 3e4 day applications versus 6e8 day intervals for satisfactory efficacy. The necessity for repeated application arises from the fact that, except under unusual conditions (unbroken high humidity for several days), these fungi do not reproduce to any great extent to create epizootics in a pest population, but die with their hosts. In addition, persistence of spores on treated foliage is relatively short due to UV-B exposure. Thus, inundative application of the fungi is necessary to significantly impact the target pest population. Additionally, Wraight and Ramos (2017b), in greenhouse-based tests under dry conditions, observed 58% mortality of second-instar larvae exposed directly to B. bassiana GHA sprays versus . (Accessed 23 July 2021). Navarro, P., Acuña, I., 2019. Insectos asociados al cultivo de Papa con especial énfasis en áfidos [online]. Temuco: Boletín INIA - Instituto de Investigaciones Agropecuarias. no. 414. https://biblioteca.inia.cl/handle/123456789/6868>. (Accessed 23 July 2021). Navarro, P., Monje, A., 2021. Agenda de Campo “Áfidos asociados al cultivo de papa en la región de La Araucanía” [online]. Temuco: Instituto de Investigaciones Agropecuarias. Boletín INIA - Instituto de Investigaciones Agropecuarias. N 439. Available from: https://biblioteca.inia.cl/handle/ 123456789/67604>. (Accessed 23 July 2021). Navarro, P., Faundez, E., Monje, A., Tellez, F., 2020. Eurylomata picturata: potential plaga en cultivo de papa para el sur de Chile [on line]. Tierra Adentro. no. 113. https://biblioteca.inia.cl/handle/123456789/5484>. (Accessed 23 July 2021). Norambuena, H., Aguilera, A., 1988. Plagas de las praderas. In: Ruiz, I. (Ed.), Praderas para Chile. Alfabeta, Santiago de Chile, pp. 229e250.

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Nowicki, M., Foolad, M.R., Nowakowska, M., Marzena, E.U., Elzbieta, U., 2011. Potato and tomato late blight caused by Phytophthora infestans: an overview of pathology and resistance breeding. Plant Dis. 96, 4e17. ODEPA, April 2021. Boletín de la papa. Publicación de la Oficina de Estudios y Políticas Agrarias (Odepa) del Ministerio de Agricultura, Gobierno de Chile. www.odepa.gob.cl. Olalquiaga, G., 1955. Situación de las plagas de insectos en Chile. Boletín Fitosanitario FAO 3, 65e70. Pachano, A., 1918. Dos enfermedades de las papas. Quinta Normal Estación Exper. Circular 7, 1e11 (Ecuador). Prado, E., 1991. Artropodos y sus enemigos naturales asociados a plantas cultivadas en Chile, vol. 160. Instituto de Investigación Agropecuarias, INIA. Boletín técnico No, p. 270. Pumisacho, M., Sherwood, S., 2002. El cultivo de la papa en Ecuador. Editorial Abya Yala, p. 224. Reyes-Corral, C.A., Cooper, W.R., Horton, D.R., Karasev, A.V., 2020. Susceptibility of Physalis longifolia (Solanales: Solanaceae) to Bactericera cockerelli (Hemiptera: triozidae) and ‘Candidatus Liberibacter solanacearum’. J. Econ. Entomol. 113, 2595e2603. Rondon, S.I., 2010. The potato tuberworm: a literature review of its biology, ecology, and control. Am. J. Potato Res. 87, 149e166. Rondon, S.I., Gao, Y., 2018. A journey of the potato tuberworm around the world. In: Perveen, F.K. (Ed.), Moths - Pests of Potato, Maize and Sugar Beet. IntechOpen, London, UK. https://doi.org/10.5772/intechopen.81934. Scott, G., 2011. Growth rates for potatoes in Latin America in comparative perspective. Am. J. Potato Res. 88, 143e152. Spooner, D.M., McLean, K., Ramsay, G., Waugh, R., Bryan, G.J., 2004. A single domestication for potato based on multilocus amplified fragment length olymorphism genotyping. Proc. Natl. Acad. Sci. U. S. A. 102, 14694e14699. Suquillo, J., Rodríguez, P., Gallegos, P., Orbe, K., Zeddam, J.L., 2012. Manual para la elaboración del bioinsecticida Bacu-Turin a través de premezclas concentradas para el control de las polillas de la papa: Tecia solanivora, Phthorimaea operculella y Symmetrischema tangolias. Manual no. 94. INIAP, Carchi, Ecuador. Torres-Leguizamón, M., Dupas, S., Dardon, D., Gómez, Y., Nino, L., Carnero, A., Lery, X., 2011. Inferring native range and invasion scenarios with mitochondrial DNA: the case of T. solanivora successive north-south step-wise introductions across Central and South America. Biol. Invasions 13, 1505e1519. Wan, J., Wang, R., Ren, Y., McKirdy, S., 2020. Potential distribution and the risks of Bactericera cockerelli and its associated plant pathogen Candidatus Liberibacter Solanacearum for global potato production. Insects 11, 298. Zeddam, J., Carrera, M., Barragán, A., Pollet, A., López Ferber, M., Léry, X., 2003. Los virus entomopatógenos para el control de las polillas de la papa: Nuevas perspectivas en el manejo de Tecia solanivora (Lepidoptera: Gelechiidae). Memorias del III Taller Internacional de la Polilla Guatemalteca de la Papa, Tecia solanivora. Cartagena, Colombia.

Chapter 17

The United States of America and Canada Andrei Alyokhin School of Biology and Ecology, University of Maine, Orono, ME, United States

17.1 Introduction The United States of America (US) and Canada are important players on world’s potato markets and their economies are closely integrated with each other. Both countries share several large ecoregions that have many similarities in terms of climate, soils, and production practices depending on eco-regions. At the same time, the US is more geographically diverse, ranging from tropical areas to the Arctic tundra. This diversity is also well reflected in potato industry. For several reasons, scientists from the US and Canada have historically played a very prominent role in a relatively small field of potato entomology. Firstly, the US is the world’s largest economy in terms of nominal gross domestic product (GDP), and the second largest economy in terms of purchasing power parity gross domestic product (IMF, 2021). Therefore, there are both the need and resources to support research and development activities. As a result, public and private sectors in these countries make considerable investment into applied sciences, which include agricultural entomology (NSF, 2020). Secondly, throughout its history, agricultural sector, including growing and processing potatoes, has always played a prominent role in the US and Canadian economy (see below). Thirdly, there is a strong “publish or perish” culture in the scientific communities in these countries, with professional success measured mostly by quantity and (sometimes, to a smaller degree) quality of journal articles and book chapters authored by a scientist. Together with English being the current language of international communication, this ensures broad dissemination of research results, including those dealing with insect pests of potatoes. As a result, much of the general information on biology and control of insect pests presented in this book originated from America north of Mexico and is directly relevant to this region.

17.2 Potato farming in overall economy Both US and Canada are major agricultural powerhouses. In 2019, US industries related to agriculture and food produced $1.1 trillion in goods and services, of which $136.1 billion were farm output. However, while those certainly were large sums of money, they amounted to only 5.2% and 0.6% of an overall US GDP, respectively (USDA-ERS, 2021). Employment in these sectors added up to 22.2 million full- and part-time jobs, or 10.9% of total US employment. About 2.6 million people were employed on farms and ranches, comprising 1.3% of the total labor force in the country (USDAERS, 2021). Agriculture and food industries are also key components of the Canadian economy, accounting for 11% of Canada’s goods GDP and almost 10% of Canada’s total merchandise trade (CAFTA, 2021). In 2016, the year for which the most recent comprehensive data are available, agriculture contributed $111.9 billion to Canada’s GDP, amounting to 6.7% of its total GDP. Agricultural sector employed 2.3 million people, or 12.5% of the total workforce. Being responsible for 16.4% of the country’s total manufacturing sector’s GDP, the food and beverage processing industry was the largest among the manufacturing industries in Canada. It was also the largest employer, providing 17.3% of the total manufacturing jobs (AAFC, 2016). First recorded planting of potatoes in North America dates to 1719, when the first plot was reported to be planted in New Hampshire (AgMRC, 2018). Since then, this crop has become prominent both in the US and in Canada. In 2020, combined potato production for the two countries was approximately 23.5 million tons, of which 18.8 million tons were

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harvested in the US, and the remaining 4.7 million tons e in Canada. Potato yields in that year averaged 50.1 t/ha in the US and 33.2 t/ha in Canada. Production levels remained relatively stable over the last 10 years, with annual fluctuations of 2%e3% (USDA-NASS, 2021). Worldwide, the US is the fifth largest producer of potatoes after China, India, Russian Federation, and Ukraine (AgMRC, 2018).

17.3 Local agroclimatic conditions Both the US and Canada are among the world’s largest countries that together occupy most of the North American continent. The US (including Alaska and Hawaii) has all major climate zones according to Köppen-Geiger climate classification system, ranging from tropical to polar (NOAA, 2021). Due to its more northern location, Canada does not have areas with tropical climates, while its largest climate zone is subarctic (Canadian Geographic, 2021). In the US, potatoes are grown commercially in about 30 states (NPC, 2021), although detailed data are currently available only for 23 of them (USDA-NASS, 2020). Most potatoes are grown in cool temperate areas. However, there is some large-scale production in California and Florida, where potatoes can be grown in winter. Idaho is the biggest producer in terms of planted area in the country, which is responsible for 30.8% of the total harvest. The second biggest producer is Washington (24.7%). These are relatively dry areas in the northwestern part of the country, where conditions are generally favorable for growing potatoes, but mostly in the presence of artificial precision irrigation. Wisconsin is a distant third, accounting for 6.8% of the national production followed by Oregon with 6.3%. In Canada, commercial potato planting is currently reported for 10 provinces (Potatoes in Canada, 2021). Manitoba is the largest producer (23% of the national potato harvest), closely followed by Alberta (22.5%). Similar to Idaho and Washington in the US, growers in these inland provinces usually rely on artificial irrigation. Prince Edward Island is a close third (20%). It usually has sufficient precipitation for growing potatoes, although supplemental irrigation may still be important in dry years (Baerg, 2020). Global climate change is likely to have a significant effect on agroecosystem productivity, thus affecting potato yields. However, what exactly is going to happen with potato farming in the US and Canada is currently unclear. Haverkort and Verhagen (2008) speculated that potato yields in temperate climates, which include most potato-growing areas in the US and Canada may increase thanks to a longer growing season and higher carbon dioxide concentrations in the air, but only if enough water is available for irrigation that currently is becoming a big problem in most regions. At the same time, higher temperatures will also favor pests and diseases. Simulation modeling by Hijmas (2003) showed a small decline in the US potato yields but a small increase in the Canadian potato yields. In that study, negative impacts of the new climate conditions in some of the current production areas were at least partially compensated by the expansion of potato growing into the areas that are currently too cold for this crop. To the contrary, simulation modeling by Raymundo et al. (2018) suggested large yield declines in temperate North America, although uncertainty and variability were also high. Kukal and Irmak (2018) explored spatial and temporal trends in the yields of maize, soybean, sorghum, spring wheat, winter wheat, and cotton during 1900e2014 across the continental US using datasets collected at more than 1200 locations. They found that, on average, the first fall frost has been occurring later while the last spring frost has been occurring earlier. As a result, climatological growing season has become longer, and the annual accumulation of growing degree days has increased. The change was generally beneficial for the yields of the investigated crops. Jennings et al. (2020) used a smaller dataset compiled on a country level between 1980 and 2009 to model potato yields and predict their trajectory between 2040 and 2060. They found that globally, average potato yields will increase from 9% to 20% if farmers adapt to climate change through changing planting windows and crop varieties. This is consistent with forecasts by Haverkort and Verhagen (2008) and, to a smaller degree, by Hijmas (2003). However, model evaluation using existing data showed good correlation between predicted and actual yields in Europe, but not elsewhere in the world, including the US and Canada (Jennings et al., 2020). Furthermore, direct extrapolation between potatoes and other crops studied by Kukal and Irmak (2018) is potentially inaccurate. Therefore, it is too early to become excessively optimistic about potential future gains in potato yields. For example, problems with drought experienced by potato growers on nonirrigated fields on Prince Edward Island have been already attributed to climate change (Baerg, 2020).

17.4 Main producers and market conditions Potatoes in the US and Canada are still grown mostly on multigenerational family farms. This is different from most commodity crops, production of which is increasingly dominated by large corporate entities (NPC, 2021). However, the trend toward farm consolidation and increase in the size of remaining farms is also present. Largest potato growers, such as Simplot, R.D. Offutt, and Black Gold Farms, currently operate on tens of thousands of hectares in different locations.

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Potato farmers in the US and Canada usually belong to nonprofit trade organizations on the state or provincial level, such as Maine Potato Board, Wisconsin Potato & Vegetable Growers Association, Potato Growers of Alberta, North Western Consortium and many others. These organizations coordinate marketing and educational efforts to promote potato industries in their respective regions, lobby for policies favorable to their members, provide networking opportunities, and sponsor relevant research and outreach activities. The weight given to these focus areas varies among the organizations and may change from year to year. They are funded by member contributions, usually in the form of small fees imposed on sold potatoes (the so-called check-off funds). On the federal level, US potato growers are represented by the National Potato Council, which advocates their interests in legislature and government agencies. In Canada, the Canadian Potato Council serves a similar role. In addition, about 70% of fresh market potato growers belong to either the United Potato Growers of America or the United Potato Growers of Canada. These are grower cooperatives that coordinate voluntary efforts to manage potato supplies to ensure price stability and profitability (Hardesty, 2008; Guenthner, 2012). Most harvested potatoes are processed into a variety of products, such as frozen French fries, chips, dehydrated potatoes, and starch. Other uses include fresh market (also known as table stock) potatoes that are purchased by consumers as raw tubers for subsequent cooking; seed potatoes that are used for growing subsequent crops; potatoes fed to livestock; and miscellaneous minor uses. Based on the available US data (USDA-NASS, 2020), about 69.7% of tubers harvested in 2019 were processed, 24.7% were sold as table stock, 5% were designated as seed potatoes, and the remaining 0.6% were fed to livestock. Of the total Canadian potato harvest in 2018, approximately 69% went to the processing sector, 19% went to the fresh sector, and 12% went to the seed sector (AAFC, 2019). Considerable amounts of US and Canadian potatoes and potato products are exported to other countries. In 2019, US exported potatoes and potato products in the total amount of $1.91 billion. Of those, $1.66 billion were received for processed potatoes, $245 million e for table stock potatoes, and $9 million e for seed potatoes. Japan was the main destination for the US potatoes ($365 million), followed by Canada ($335 million) and Mexico ($254 million) (Trade Stats Northwest, 2020). Exports of Canadian potatoes and potato products were assessed at $1.88 billion in the 2018e19 crop year, of which processed potatoes were worth $1.58 billion, while fresh potatoes (table stock and seed combined) were worth $295 million. The US was the largest importer of Canadian potatoes (86.5% of total exports), with the Philippines (3.1%) and Japan (1.7%) occupying the distant second and third places (AAFC, 2019). Most potatoes are grown conventionally and rely on considerable inputs of synthetic fertilizers and pesticides. There is also a demand for organic potatoes. Sales of organic table stock potatoes in the US reached record levels between July 1, 2019, and June 30, 2020, increasing by 8.6% compared to the preceding 12-month period. Organic potatoes also commanded a retail price of $3.30 per kg, compared to $1.63 per kg for conventional potatoes. However, in terms of volume, organic potatoes accounted for only 2% of the market, with the remaining 98% grown conventionally (Jennings, 2020).

17.5 Main insect pests Wenninger et al. (2020) provide a comprehensive overview of insect pests affecting potato production in the US and Canada. In addition, chapters dedicated to individual pest species in this book (Part II, Chapters 4e9) provide an in-depth review of their biology and management. Here, we provide an annotated list of the common insect pests in the region and references to more detailed information about them within and outside of this book. Colorado potato beetle is present in all potato-growing areas of the US and Canada, where both adults and larvae feed on foliage (Chapter 4). Depending on the area, there are usually one to three generations per year. While there is variation in the Colorado potato beetle pressure among the fields and between the years, it is usually a persistent background problem that constantly requires grower attention. In the absence of adequate control, yield losses can be severe, sometimes to the point of complete crop failures especially if damage occurs early in the season. While these are uncommon due to a wide-spread insecticide use by commercial growers, the Colorado potato beetle also has a high propensity for developing insecticide resistance, especially in the eastern part of the continent due to genetic factors and crop management approaches (Alyokhin et al., 2008, 2015; see also Chapter 24). Aphids (Hemiptera: Aphididae) are another ubiquitous insect problem in potatoes throughout the US and Canada (Chapter 5). Green peach aphid, Myzus persicae (Sulzer), and potato aphid, Macrosiphum euphorbiae (Thomas), are the two species most commonly colonizing potato plants in this region. Several other species may also be present, but usually at much lower densities. In most cases, populations of colonizing aphids do not reach densities that are sufficient for causing significant reductions in tuber yields. Unfortunately, these aphids transmit two important viruses, Potato Leafroll Virus and Potato Virus Y, which affect plant growth and tuber quality. The latter is also transmitted by numerous other aphid species that do not colonize potato plants. However, they still probe them with their proboscises while searching for

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more suitable hosts and, thus, spread this nonpersistent virus. Green peach aphid is generally known for its ability to develop insecticide resistance (Chapter 24), but it does not seem to be a big problem in potato farming. Wireworms is yet another pest issue that is present in most potato-growing areas in the US and Canada (Chapter 7). Region-wide, this insect complex is comprised of soil-dwelling larvae of several dozen species of click beetles (Coleoptera: Elateridae). However, a particular area is likely to have only a few of these and is often dominated by one or two species. Unlike Colorado potato beetles and aphids, wireworm populations are usually patchier and more sporadic and usually a problem when potatoes follow small grains. Some fields may have consistent wireworm infestations while other fields are free of these pests despite being in the same general area and receiving no control measures against wireworms. When present, wireworms feed on plant roots and borrow inside tubers, often rendering them unmarketable. Cryptic underground habitat and a still poor understanding of the factors favoring wireworm populations make their detection difficult. Potato tuberworm, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae), is one of the most important pests of potato worldwide (Chapter 8, Rondon, 2010; Rondon and Gao, 2018). This moth is cosmopolitan in distribution, being present in most countries that have a significant potato production. However, it is a warm-climate species that does not survive long cold winters. Therefore, it is mostly prevalent in the areas with tropical, subtropical, Mediterranean, or at least warm temperate climates. In the US, potato tuberworm has been reported in at least 25 states across the warmer part of the country, with serious problems experienced in the major potato-growing area of Columbia Basin in Oregon and Washington (Gill et al., 2020). This pest currently is not a problem in Canada, where it was found in British Columbia in 1958 and, possibly, 1959 (Macnay, 1961), but apparently could not establish because of inability to survive its climate (Howard et al., 1994). Larvae feed on both foliage and tubers, with the latter resulting in most damage. They can be a problem both in the field and in storage. In the developing countries, economic damage is often most severe for stored tubers. In the US, however, commercial growers normally use hi-tech refrigerated storage facilities that are significantly less conducive for larval development. Therefore, most damage occurs in the field before harvest.  The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae), is another important pest that is common, but not universally present across the US and Canada (Chapter 6). This species is currently found throughout the central and western parts of the US. Potato psyllids also have been reported from the adjacent Canadian provinces, although they may have migrated there from the US without establishing overwintering populations (EPPO, 2020). Direct feeding by this species causes “psyllid yellows” syndrome that consists of foliar discoloration and curling, stunted growth, formation of aerial tubers, decrease in tuber size, premature senescence, and, ultimately, in the death of affected plants. Development of psyllid yellows has been attributed to the toxin(s) secreted by feeding insects with their saliva, but the exact etiology of this disease remains unknown. In addition, potato psyllids transmit bacterium Candidatus Liberibacter solanacearum that causes the Zebra chip disease of potato. Foliar symptoms of this disease are somehow similar to the symptoms of psyllid yellows; however, it also leads to vascular discoloration in tubers in the form of longitudinal striped necrotic patterns. Discoloration is particularly noticeable in fried products, such as French flies and chips, which also acquire an unpleasant taste. Given the importance of processing industry in North America, such damage is especially undesirable (Chapter 6, Munyaneza and Henne, 2013). Several species of leafhoppers (Hemiptera: Cicadellidae) feed on potatoes in the US and Canada (Chapter 9). Two of the most important species are potato leafhopper, Empoasca fabae Harris and beet leafhopper, Circulifer (¼Neoaliturus) tenellus (Baker). Potato leafhopper is a damaging pest in the eastern parts of the region (Wenninger et al., 2020). However, they are not capable of surviving winters in the northern United States and Canada. Instead, every year they are carried by wind northwards from the states surrounding the Gulf of Mexico, colonize potato plants, go through several generations, and then die out during winters (OMAFRA, 2021). Feeding by potato leafhoppers results in “hoper burn” syndrome, which is manifested as brown necrosis along leaf margins, leaf curling, and stunted growth, probably due to toxins contained in leafhopper saliva. Beet leafhopper is a problem in the western part of the region, in large part because of transmitting phytoplasmas Beet Leafhopper Transmitted Virescence responsible for the disease known as “purple top” that causes leaf curling with reddish or purplish discoloration, stunted growth, aerial tubers, and early plant decline (Munyaneza et al., 2005; Rondon and Oppedisano, 2020). There are also several pest species that cause minor or occasional damage to potato crops. Under some circumstances, these can create economically significant problems. However, in an average year on an average field, they do not require any control measures specifically directed toward suppressing their populations. These include flea beetles, cutworms, armyworms, white grubs, blister beetles, and a few other species such as Lygus bugs, blister beetles, thrips and mites that are described in detail by Wenninger et al. (2020). Interestingly, the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), was considered an important pest of potatoes in the past. However, its significance dramatically declined in recent years. It is possible that widespread planting of transgenic Bt corn, which serves as the main host for the

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European corn borer, resulted in an area-wide reduction of this insect in the US and Canada, thus decreasing the number of adult moths immigrating into potato fields (Dively et al., 2018). Another contributing factor could be its susceptibility to insecticides that are used in potatoes to manage other insects (Wenninger et al., 2020; see also Chapter 11).

17.6 Methods of pest control Commercial farmers mostly rely on insecticides for managing insect pests that affect their potato crops. This applies both to conventional, as well as to organic growers, although many fewer active ingredients are available to the latter (Chapter 11). Farmers usually have sufficient financial resources to afford insecticides. Therefore, all major pesticide companies are active in the region and have extensive networks of sale and technical support personnel. There are also considerable research efforts going into developing new active ingredients and optimizing the use of the existing ones. These are funded by chemical companies, public sector, and grower organizations. Pesticide use is fairly strictly regulated by the government, with some of the older and more toxic chemistries either removed from the market or being gradually phased out. As a whole, pesticide regulations are somewhat more stringent in Canada than in the US. Extensive insecticide use helps ensuring high yields typical for this region. However, it also creates strong selection pressure toward the evolution of insecticide resistance in targeted populations (Chapter 24). As mentioned above, the situation is especially serious with the Colorado potato beetles. Potato growers in some areas of the Northeastern US completely ran out of chemical control options in mid-1990s because the beetles had become resistant to every chemical that was available against them at that time. The situation improved dramatically after the introduction of imidacloprid and other neonicotinoids and remained relatively stable since then. However, the threat of a similar failure in the future remains and needs to be taken very seriously (Alyokhin et al., 2015). Perhaps counterintuitively, insecticide resistance is currently more of a problem on organic potato farms (Klein et al., 2021) because of a very limited number of active ingredients available to organic growers. Most potato growers in the US and Canada practice crop rotations. However, their duration is usually short, with potatoes being grown either every other year or every third year, because the economic value of rotation crops is often lower than that of potatoes. Also, current-year potato fields may be located close to the previous-year potato fields. Rotations are not specifically directed against insect pests, but still help reducing their populations (Chapter 15). They may also be instrumental in delaying insecticide resistance (Alyokhin et al., 2015). Biological control remains underutilized in potato farming (Chapter 13). Potato growers are generally aware of the effects of broad-spectrum insecticides on beneficial natural enemies, which may sometimes affect their choice of chemicals. Still, most decisions related to insecticide use are driven by economic considerations, such as their price and perceived efficacy. Introducing several nonnative lady beetle species in the second half of the last century likely helped suppressing populations of potato-colonizing aphids in some areas (Alyokhin and Sewell, 2004; Alyokhin et al., 2005). However, it also resulted in the decline of native lady beetle species (Alyokhin and Sewell, 2004). US and Canadian potato growers usually plant high-quality seed tubers. Agricultural authorities on the state or, in Canada, provincial level regulate the quality of seed tubers and the process of their certification (Frost et al., 2013; Karasev and Gray, 2013). While availability of insect-resistant varieties is rather limited (Chapter 14), this allows keeping low the proportion of tubers infected with aphid-transmitted viruses, thus mitigating their potential damage (Chapter 5). Also, as more insect-resistant varieties, hopefully, enter the market in the future, good seed management system will prevent accidental variety mixing in the seed lots and false advertisement by unscrupulous growers and dealers. Insect-protected transgenic plants are legal and widely grown in the US and Canada. However, no such potatoes are currently commercially available. In mid-1990s, Monsanto Company tried introducing Bt potatoes resistant to the Colorado potato beetle. However, that attempt failed, in part because of the low customer acceptance and in part because of the competition with neonicotinoid insecticides. Neonicotinoids could be applied on seed tubers at planting and provided season-long protection, making them functionally similar to Bt plants. Currently, in western US, for example, close to 90% of producers use neonicotinoid based product at planting (Rondon, personal communication). Nevertheless, research on transgenic potatoes continued (Chapter 14), and it is possible that new attempts to introduce insect-resistant transgenic potato cultivars will be made in the future. Integrated pest management (IPM; see Chapter 27 for definition and detailed discussion of this approach) is heavily promoted by agricultural researchers and regulators in the US and Canada. The importance of IPM is generally accepted by commercial growers, but actual implementation varies from farm to farm. Most commercial growers scout their fields for pest insects, sometimes with the help of professional crop consultants and trained university- or government-employed personnel. Results of this scouting is then used to make spraying decisions. However, calendar-based applications are still common, especially treatments of seed tubers with systemic neonicotinoids. Growers also practice crop rotations, plant

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certified seed tubers, and control volunteer potatoes that can serve as reservoirs of pests and diseases. Rotating different insecticides (Huseth et al., 2014) is the most common approach to managing insecticide resistance. Federal and local (state or provincial) governments in both countries dedicate considerable resources to IPM research and to dissemination of its results among farmers. Government-funded University Cooperative Extension facilitates communication between commercial growers on one side and agricultural researchers and regulators on the other side.

17.7 Problems and perspectives On one hand, the US and Canada have successful and technologically advanced potato industries that supply high-quality affordable tubers to customers in these countries and export them abroad. Yields are very impressive, especially in the US. Large part of this achievement is due to advanced agricultural practices, such as high degree of mechanization, proper soil fertilization, using superior plant germplasm, extensive precision irrigation, and effective pesticides. Another part can be attributed to favorable agroclimatic conditions. These are also largely responsible for a gap in yields between the US and Canada since farming methods are similar between the two countries. On the other hand, current success of potato farming in North America hinges on very high levels of external inputs, such as fossil fuels, mineral fertilizers, water, and chemical pesticides. These are derived, in large part, from nonrenewable resources (strictly speaking, water is renewable, but its supplies at a given location may be seriously limited and not easily replenishable). So, as discussed in Chapter 25, American farmers indeed harvest potatoes made mostly out of oil. While there is no need to paint an apocalyptic picture of an imminent collapse of potato farming, nonrenewable resources, by definition, will eventually run out. Furthermore, industrial approach to potato farming results in significant soil erosion, which may actually aggravate damage caused by insect pests (Chapter 25; see also Alyokhin et al., 2020). While soil is a renewable resource, its regeneration is a very slow process. In the near future, commercial farming in the US and Canada is likely to retain its intensively industrial features. This includes relying on chemical control for managing insect pests. It is reasonable to expect that recent technological advances, such as remote sensing, self-driving machinery, and decision support systems based on artificial intelligence will be widely adopted by potato farmers. This will further increase efficiency of potato production while reducing the amount of necessary inputs. For example, targeting insecticide applications in space and time using remote sensing and computerrun economic threshold algorithms may allow significant reduction in the amount of chemicals released in the environment. Remote sensing using small unmanned aircraft systems commonly known as drones has been already shown to have a good potential for detecting and quantifying Colorado potato beetle damage (Hunt and Rondon, 2017). Transitioning to a more ecologically based system of farming is likely to be more challenging. While harnessing the energy of ecological connections to replace the energy of external inputs is potentially an enormously powerful technology, it is not an easy process because these connections are complicated and often difficult to understand (Chapter 25). Furthermore, it requires a significant shift in a dominant socioeconomic paradigm from maximizing short-term profits to maximizing long-term sustainability of a production system. However, there is an increasing understanding among both general public and members of the farming community that such a shift is both necessary and inevitable. Sustainable production practices are becoming one of the mainstream consumer demands, which is increasingly reflected both in the requirements imposed by potato processors and distributors, as well as in the practices of an average commercial grower. Therefore, it should be anticipated that nonchemical approaches to controlling insect pests will become increasingly common, and that knowledge-based integration of various methods in IPM systems will eventually replace single-method (and usually chemical) approaches currently dominating potato farming in the US and Canada. In addition to changing farmer practices, this will also require changes in consumer attitudes and behaviors. For example, reduction in pesticide residues should start taking precedence over visual perfection of purchased tubers.

References Agriculture and Agri-Food Canada (AAFC), 2016. An Overview of the Canadian Agriculture and Agri-Food System 2016. Research and Analysis Directorate, Strategic Policy Branch, Agriculture and Agri-Food Canada, p. 107. Agriculture and Agri-Food Canada (AAFC), 2019. Potato Market Information Review, 2018-2019. Crops and Horticulture Division, Agriculture and Agri-Food Canada, p. 60. Agricultural Marketing Resource Center (AgMRC), 2018. Potatoes. https://www.agmrc.org/commodities-products/vegetables/potatoes (Accessed 2 August 2021). Alyokhin, A., Sewell, G., 2004. Changes in a lady beetle community following the establishment of three alien species. Biol. Invasions 6, 463e471. Alyokhin, A., Drummond, F.A., Sewell, G., 2005. Density-dependent regulation in populations of potato-colonizing aphids. Popul. Ecol. 47, 257e266.

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Alyokhin, A., Baker, M., Mota-Sanchez, D., Dively, G., Grafius, E., 2008. Colorado potato beetle resistance to insecticides. Am. J. Potato Res. 85, 395e413. Alyokhin, A., Mota-Sanchez, D., Baker, M., Snyder, W.E., Menasha, S., Whalon, M., Dively, G., Moarsi, W.F., 2015. Red Queen on a potato field: IPM vs. chemical dependency in Colorado potato beetle control. Pest Manag. Sci. 71, 343e356. Alyokhin, A., Nault, B., Brown, B., 2020. Soil conservation practices for insect pest management in highly disturbed agroecosystems e a review. Entomol. Exp. Appl. 168, 7e27. Baerg, M., 2020. The Island’s Irrigation Woes. Potatoes in Canada, October 26, 2020. https://www.potatoesincanada.com/the-islands-irrigation-woes/ (Accessed 2 August 2021). Canadian Agri-Food Trade Alliance (CAFTA), 2021. Agri-Food Exports. https://cafta.org/agri-food-exports/> (Accessed 30 June 2021). Canadian Geographic, 2021. The Canadian Atlas Online. Climate Zones. http://www.canadiangeographic.com/atlas/themes.aspx?id¼weather& sub¼weather_basics_zones&lang¼En> (Accessed 2 August 2021). Dively, G.P., Venugopal, P.D., Bean, D., Whalen, J., Holmstrom, K., Kuhar, T.P., Doughty, H.B., Patton, T., Cissel, W., Hutchison, W.D., 2018. Regional pest suppression associated with widespread Bt maize adoption benefits vegetable growers. Proc. Natl. Acad. Sci. Unit. States Am. 115, 3320e3325. European and Mediterranean Plant Protection Organization, (EPPO), 2020. EPPO Global Database. https://gd.eppo.int (Accessed 22 September 2021). Frost, K.E., Groves, R.L., Charkowski, A.O., 2013. Integrated control of potato pathogens through seed potato certification and provision of clean seed potatoes. Plant Dis. 97, 1268e1280. Gill, H.K., Chahil, G., Goyal, G., Gill, A.K., Gillett-Kaufman, J.L., 2020. Featured Creatures: Potato Tuberworm. University of Florida Publication Number EENY-587, Gainesville, FL. https://entnemdept.ufl.edu/creatures/VEG/POTATO/potato_tuberworm.htm> (Accessed 13 August 2021). Guenthner, J.F., 2012. The development of United potato growers cooperatives. J. Coop. 26, 1e16. Hardesty, S., 2008. Enhancing producer returns: United potato growers of America. Giannini Found. Agric. Econom. 11, 9e11. Haverkort, A.J., Verhagen, A., 2008. Climate change and its repercussions for the potato supply chain. Potato Res. 51, 223e237. Hijmans, R.J., 2003. The effect of climate change on global potato production. Am. J. Potato Res. 80, 271e279. Howard, R.J., Garland, J.A., Seaman, W.L., 1994. Diseases and Pests of Vegetable Crops in Canada: An Illustrated Compendium. The Canadian Phytopathological Society and the Entomological Society of Canada, Ottawa, Canada, p. 1024. Hunt, E.R., Rondon, S.I., 2017. Detection of potato beetle damage using remote sensing from small unmanned aircraft systems. J. Appl. Remote Sens. 11 (2), 026013. https://doi.org/10.1117/1.JRS.11.026013. Huseth, A.S., Groves, R.L., Chapman, S.A., Alyokhin, A., Kuhar, T.P., Macrae, I.V., Szendrei, Z., Nault, B.A., 2014. Managing Colorado potato beetle insecticide resistance: new tools and strategies for the next decade of pest control in potato. J. Integr. Pest Manag. 5 (4), A1eA8. https://doi.org/ 10.1603/IPM14009. International Monetary Fund (IMF), 2021, 2021. World Economic Outlook Report. https://www.imf.org/en/Publications/WEO/ (Accessed 30 June 2021). Jennings, J., 2020. Fresh organic potato sales hit all-time high. Organic Grower. https://organicgrower.info/news/fresh-organic-potato-sales-hit-all-timehigh/> (Accessed 3 August 2021). Jennings, S.A., Koehler, A.K., Nicklin, K.J., Deva, C., Sait, S.M., Challinor, A.J., 2020. Global potato yields increase under climate change with adaptation and CO2 fertilisation. Front. Sust. Food Syst. 4, 519324. https://doi.org/10.3389/fsufs.2020.519324. Karasev, A.V., Gray, S.M., 2013. Continuous and emerging challenges of Potato virus Y in potato. Annu. Rev. Phytopathol. 51, 571e586. Klein, C., Baker, M., Alyokhin, A., Mota-Sanchez, D., 2021. Geographic variation in dominance of spinosad resistance in Colorado potato beetles (Coleoptera: Chrysomelidae). J. Econ. Entomol. 114, 320e325. Kukal, M.S., Irmak, S., 2018. U.S. agro-climate in 20th century: growing degree days, first and last frost, growing season length, and impacts on crop yields. Sci. Rep. 8, 6977. Macnay, C.G., 1961. Some new records in Canada, from the Canadian Insect Pest Record, 1955-1959, of arthropods of real or potential economic importance: a review. Can. Insect Pest. Rev. 39 (Suppl. l) [1þ] 38. Munyaneza, J.E., Henne, D.C., 2013. Leafhopper and psyllid pests of potato. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato: Perspect. Biol. Manag. Academic Press, Oxford, UK, pp. 65e102. Munyaneza, J.E., Crosslin, J.M., Jensen, A.S., Hamm, P.B., Thomas, P.E., Pappu, H.R., Schreiber, A., 2005. Update on the potato purple top disease in the Columbia Basin. In: Proceedings, 44th Annual Washington State Potato Conference, 1-3 February 2005, Moses Lake, WA, pp. 57e70. National Potato Council, 2021. Annual Potato Yearbook. Washington, DC, p. 58. National Oceanic and Atmospheric Administration (NOAA), 2021. Climate Zones. https://www.weather.gov/jetstream/climates (Accessed 2 August 2021). National Science Foundation (NSF), 2020. The State of U.S. Science and Engineering. https://ncses.nsf.gov/pubs/nsb20201> (Accessed 30 June 2021). Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA), 2021. White Apple Leafhopper and Potato Leafhopper. Excerpt from Publication 310. Integrated Pest Management For Apples. http://www.omafra.gov.on.ca/english/crops/facts/whleaf.htm#potato> (Accessed 12 August 2021). Potatoes in Canada, 2021. StatsCan Shares Updated 2020 Potato Production Information. Editorial, February 26, 2021. https://www.potatoesincanada. com/statscan-shares-updated-2020-potato-production-information/ (Accessed 3 August 2021). Raymundo, R., Asseng, S., Robertson, R., Petsakos, A., Hoogenboom, G., Quiroz, R., Hareau, G., Wolf, J., 2018. Climate change impact on global potato production. Eur. J. Agron. 100, 87e98. Rondon, S.I., 2010. The potato tuberworm: a literature review of its biology, ecology, and control. Am. J. Potato Res. 87, 149e166.

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Rondon, S.I., Gao, Y., 2018. The journey of the potato tuberworm around the world. In: Perveen, K. (Ed.), Moths: Pests of Potato, Maize and Sugar Beet. InTech Open, London, UK, pp. 17e52. Rondon, S.I., Oppedisano, T., 2020. Biology and Management of Beet Leafhopper and Purple Top in Potatoes in the Pacific Northwest. Oregon State University Extension Publication EM 9282. https://catalog.extension.oregonstate.edu/em9282/html> (Accessed 3 August 2021). Trade Stats Northwest, 2020. United States Exports. Potato Commodities, Portland, Oregon, p. 27. US Department of Agriculture Economic Research Service (USDA-ERS), 2021. Ag and Food Sectors and the Economy. https://www.ers.usda.gov/dataproducts/ag-and-food-statistics-charting-the-essentials/ag-and-food-sectors-and-the-economy/ (Accessed 27 July 2021). US Department of Agriculture National Agricultural Statistics Service (USDA-NASS), 2020. Potatoes. 2019 Summary. Released on September 17, 2020, by the National Agricultural Statistics Service (NASS). Agricultural Statistics Board, United States Department of Agriculture (USDA), p. 25. Wenninger, E.J., Rashed, A., Rondon, S.I., Alyokhin, A., Alvarez, J.M., 2020. In: Stark, J., Thornton, M., Nolte, P. (Eds.), Insect pests and their management. Potato Production Systems, Springer, Cham, Switzerland, pp. 283e345. US Department of Agriculture National Agricultural Statistics Service (USDA-NASS), 2021. North American Potatoes (January 2021). Released on January 21, 2021, by the National Agricultural Statistics Service (NASS), Agricultural Statistics Board. United States Department of Agriculture (USDA), p. 4.

Chapter 18

Regional overview of potato pest problem in EU Aigi Margus and Leena Lindstro¨m Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

18.1 Potato has been cultivated in Europe for over 500 years Potato was brought to Europe most likely by the Spanish conquerors from South America in the 16th century. They realized that on the long voyages from South America, sailors who ate potatoes did not suffer from scurvy (vitamin C deficiency), and potatoes became important food for a long journey. It is likely that some excess tubers were planted in the home country after the long voyage. The first record of potato in Europe is from a ship cargo from Las Palmas to Antwerp in 1567, suggesting that potato might have already been cultivated on the Canary Islands at that time. It has been suggested that potato was first introduced to the European diets by scholars and noblemen. Indeed, in the end of the 18th century, there was a keen interest in potato farming among the statesmen because potato have good nutritional value (Kaldy, 1972; Kolasa, 1993) and people with good health conditions make a foundation of a good army (see e.g., Earle, 2018). It has been estimated that 17% of the population growth in Europe between 1700 and 1900 was due to the inclusion of potatoes in the diet (Nunn and Quinn, 2009). However, recent systematic studies suggest that potato usage was already relatively widespread in many countries among peasants by the turn of the 18th century (Earle, 2018; see also Glendinning, 1983). Despite the importance of potato as a crop, it is not clear how many times and from where potato was originally introduced to Europe. Based on the historical written records, it has been suggested that there were only few introductions in the 16th century, potentially from Colombia or Chile (see discussions in Glendinning, 1983; Jansky and Spooner, 2018). Recent genomic analysis of the 1650e1750 herbarium specimen, however, shows that multiple potato varieties/cultivars were introduced from various parts of South America (Gutaker et al., 2019). In the European potato pedigree database (van Berloo et al., 2007), there are 20 dated varieties registered in Europe before 1850 but 164 between 1851 and 1900. This shows that since the mid-19th century, there has been a keen interest by scholars to hybridize different potato species and/ or cultivars (Jansky and Spooner, 2018). This interest stemmed from the desire to increase yield and to improve disease resistance of the plants after the Irish potato famine.

18.2 Two major pests of potato in Europe Soon after its introduction to Europe, potato did not appear to suffer from European herbivores, as none are mentioned as its pests. In initial cases, the potato crop losses were most likely due to viruses (Glendinning, 1983). Alternatively, it is also possible that those losses were due to the decades-long asexual propagation, which had resulted in a loss of genetic variability (Jansky and Spooner, 2018). Historically, the biggest problem for potato production in Europe has been fungal and oomycete pathogens. This partly explains the early interest to increase the disease resistance in potatoes with potato breeding. In the last half of the 19th century, amateur “selectionists” produced a range of potato varieties aiming to increase resistance against viruses, late blight (Phytophthora infestans), or wart disease (Synchytrium endobioticum). In the early 20th century, variety breeding by amateurs was replaced with more systematic efforts that followed scientific methods (Salaman, 1949). Also, new germplasm from Chile was introduced (Glendinning, 1983), as late blight epidemics eliminated almost all the previous varieties. This disease remains to be the biggest problem of potato production up until present.

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00017-2 Copyright © 2022 Elsevier Inc. All rights reserved.

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FIG. 18.1 Presence of the Colorado potato beetle in the European countries (grayebeetle is not present, blackebeetle present, whiteeno data available, EPPO, 2020).

The late blight oomycete was the first major potato pest in Europe, originally reported in the 1840s (Fry and Goodwin, 1997). It is not known when exactly it was introduced to Europe, but it likely originated from Mexico and was brought to Europe through trade (Glendinning, 1983). The oomycete caused an extremely damaging disease that resulted not only in infamous and widespread famine in Ireland, but also in significant problems in other European countries from Belgium to Russia throughout the mid-19th century. The situation was particularly dire in Ireland because dependence on the potato in that country was higher than elsewhere in Europe. Furthermore, Irish peasants mostly grew a single variety of potato, the Irish Lumper (Powderly, 2019), which was susceptible to the pathogen. As a result, 1 million people died, and 1.5 million emigrated out of a population of ca. eight million people that inhabited Ireland prior to the Potato Famine (Burton, 1948). The catastrophe was not purely based on the failure of the potato crops, however, poor choices were also made by the British government on overall agricultural policies (Kinealy, 1995). After the Second World War, the European potato production was threatened by the introduction of the Colorado potato beetle (Leptinotarsa decemlineata). The Colorado potato beetle became successfully established in France for the first time in the 1920s, after several introductions from 1876 onwards (CABI, 2020). Since then, the beetle has rapidly spread throughout Europe and is currently present in the majority of European countries despite the intensive control operations (Fig. 18.1). It may be responsible for up to 50% crop losses in some areas (Suffert and Ward, 2014; Wójtowicz et al., 2013). The beetle has been regulated as a quarantine pest for European and Mediterranean Plant Protection Organization (EPPO) since 1975 (EPPO, 2020). EPPO’s objective is to protect all crop plants by developing international strategies against the introduction and spread of the pests. EPPO monitors many different pests, creates early warning systems, and gives standards for dealing with outbreaks (e.g., see EPPO, 2004, 2017) and reports new pest introductions to European regions. The Colorado potato beetle has been listed as an A2 quarantine pest, which means that regulations protect those areas where the beetle is still a quarantine pest, although it is already present in the EPPO region as a whole. This means that despite the free trade, restrictions for potato trade (especially in seed potatoes) can be made within the EU. Fortunately, the Colorado potato beetle has been successfully controlled with insecticides in Europe since its introduction. Thus, it has not caused as big economical losses as late blight did in the pre-pesticide era (CABI, 2020).

18.3 Potato farming was worth EUR 11 billion in 2017 Potato is the most widely grown root vegetable in the EU (1.7 million hectares), followed by the sugar beet (1.5 million hectares) (Forti, 2017). Potatoes are grown primarily (up to 85%) as human food, while, for example, only 50% of harvested cereals are eaten by humans. In recent years, the amount of harvested potatoes has declined in Europe (Fig. 18.2),

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FIG. 18.2 The area harvested (km2) and potato production (in kilotons) has steadily decreased since 1961, whereas the yield (kg/ha) has increased in the European countries. Data from FAOSTAT, 2020. Crop Statistics for Potato. http://www.fao.org/faostat/en/#data/QC. (Accessed 31 January 2021).

partly due to the competition with the intensified production in other countries outside the EU (Hijmans, 2003) and partly due to increased pathogen and pest problems (Kapsa, 2008). In addition, in many areas potatoes are seen as a traditional and old-fashioned food; therefore, they are not readily eaten by young people (e.g., Europatat, 2020). In 2018, the European potato production had been estimated to decrease by half since 2000 (De Cicco and Jeanty, 2019). The 1.7 million hectares are cultivated by 1.5 million holdings. Therefore, 90% of the holdings (farms) grow potatoes on an area that is less than 1 ha (De Cicco and Jeanty, 2019). However, there is considerable variation among member states in EU. Whereas an average size of the cultivated area of potato per farm was 0.2 ha in Romania and 0.8 ha in Poland in 2016, it was 26.1 ha in Denmark and 16.5 ha in the Netherlands. Common agricultural policy in EU aims to safeguard farmers a reasonable living, as farming is inherently less stable compared to other economic pursuits. However, farm subsidies are paid by the individual member countries. As the subsidies are based on many factors, including location, area and production type, there is considerable variation in their size and structure. In Finland, for example, subsidies approach 500 V/ha for edible potatoes and 1100 V/ha for starch potato (Niemi and Väre, 2019). In the EU, potato production is concentrated in seven EU member states (Belgium, Germany, France, the Netherlands, Poland, Romania, and the United Kingdom) that produce 79.5% of this crop (EUROSTAT EU potato sector, 2019). Potato in the EU is grown mostly for table potatoes that are traded within Europe (65%), while 25% is grown for seed, 8% are early potatoes (young thin-skinned tubers harvested before reaching mature size), and the remaining 2% are used for making starch (De Cicco and Jeanty, 2019). Europe is the net exporter of potatoes, although the majority of potato trade is among the EU member states. Compared to the volume of domestic potato production (52 Million tons), EU members do not import a lot of potatoes (355,800 tons) from outside Europe. The majority of the imported tubers are early potatoes from Egypt and Israel.

18.4 Biggest current pest problems There are several different pests of potato in European countries (Fig. 18.3, Table 18.1), and the major producing countries also have the highest incidence of known pests. The most numerous and damaging pest groups of potato are insects, viruses, and bacteria (Fig. 18.4, EPPO, 2017, 2020). The main insect pests are the Colorado potato beetle (Leptinotarsa decemlineata), the green peach aphid (Myzus persicae), potato tuber moth (Phthotimaea operculella), wireworms, noctuid moths, common green capsid (Lygocoris pabulinus), and leafhoppers (Empoasca vitis, Empoasca solani and Eupteryx atropunctata). Out of non-quarantine pests, aphids are the most serious pests of potatoes. Their effects on plants are mainly indirect due to their ability to act as a vector for different diseases. For example, green peach aphids can transmit viruses to potato plants such as Potato virus Y (Bosquel et al., 2018). Chapter 5 includes more information on this subject. Since potato is not a native species in Europe, many of its pest species are also non-native and can be thus divided into quarantine and non-quarantine pests. This categorization is done to assist in monitoring and preventing their spread. The quarantine pests are further divided into subgroups based on their presence in the EPPO regions (A1-are not present in the EPPO region and A2-are present, but not everywhere) (Table 18.1). There are currently four A2-list insect species that attack potato in the EU: the Colorado potato beetle (Leptinotarsa decemlineata), potato flea beetles (Epitrix cucumeris and

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FIG. 18.3 Number of different insect pests of potato in the European countries on the scale ranging from no insect pests reported (white) to 20 different insect pest species reported (black). Data combined from EPPO, 2020. Eppo Standard PM 1/2(29). EPPO A1 and A2 Lists of Pests Recommended for Regulation as Quarantine Pests. https://www.eppo.int/media/uploaded_images/RESOURCE S/eppo_standards/pm1/pm1-002-29-en.pdf. (Accessed 23 July 2021) and CABI, 2020. Datasheet Leptinotarsa decemlineata (Colorado Potato Beetle). https://www.cabi.org/isc/datasheet/30380. (Accessed 12 October2020).

Epitrix papa), and Guatemalan tuber moth (Tecia solanivora). The most widespread and destructive pest out of these four is the Colorado potato beetle (Fig. 18.1, see also Chapter 20). The latest additions to the pest species list are two potato flea beetles Epitrix cucumeris and Epitrix papa, that have been added to the A2 list in the 2000s. Both of them are now present in Spain and Portugal (EPPO Global database) and are estimated to be capable of establishing further in the Mediterranean Basin (EPPO, 2011) and even in the northern parts of Europe (VKM, 2019). The control of Epitrix species can be challenging because both their biology and origin are poorly known, and their similarity to non-pest potato flea beetles is high (Boavida and Germain, 2009; Orlova-Bienkowskaja, 2015; Eyre and Giltrap, 2012). For example, Epitrix papa was initially misidentified as another rare North American potato flea beetle (Epitrix similaris), which has not been considered as a pest species in North America because it had not caused any significant damage in its native range (California) (Orlova-Bienkowskaja, 2015). The damage of Epitrix papa is done mainly by the larvae that eat the tubers, thus reducing their commercial value. Epitrix spp. seem to prefer Solanum tuberosum, even though they can also be found on other plants in Europe. However, all Epitrix spp. are very similar, so that their identification by non-specialists can only be done using molecular methods (Germain et al., 2013). Control in Europe can also be challenging because egg and larval stages are spent underground; therefore, insecticides can be applied only against adult beetles (Eyre and Giltrap, 2012). Furthermore, there is no published information on their effective natural enemies in Europe (EPPO, 2020). E. cucumeris is widely distributed in North America and mainly damages potato foliage (Eyre and Giltrap, 2012), while E. papa damages tubers. It is suggested that E. cucumeris was introduced to Portugal via imports of seed potatoes from Canada (Eyre and Giltrap, 2012). These species can have a large economic impact on potato production at high population densities (Boavida and Germain, 2009). Their presence also increases pesticide applications, as several additional sprays are needed to target early emerging adults (Eyre and Giltrap, 2012). In addition, Guatemalan tuber moth (Tecia solanivora) could become a problem in the future, if its spread throughout the EU is not prevented. It is one of the most important potato pests globally (EFSA Panel of Health, 2018), and it has arrived to Europe, first to the Canary Isles in 1999 and then to the mainland of Spain in 2015 (EPPO, 2020). Besides quarantine species, there are also many non-regulated potato pests. They include aphids (Myzus persicae, Macrosiphum euphorbiae, Aphis gossypii, Aphis nasturtii, and several other species), Phthorimaea operculella (potato tuber moth), wireworms (Agriotes spp., Melolontha spp.), noctuid moths (Agrotis ipsilon, Agrotis segetum), Lygocoris pabulinus, Empoasca vitis, Empoasca solani, Eupteryx atropunctata (EPPO standards potato PP2/002(2); PAN, 2007). While the presence of different quarantine species in different European countries is well documented (EPPO, CABI), there are no good databases for the distributions for the non-regulated potato pests.

TABLE 18.1 Example of the potato insect pests and their quarantine status on the European and Mediterranean regions (EPPO potato, 2020; EPPO, 2017; A1 absent and A2 present), or in EU decision with the year the regulations were given. With their origin (based on Encyclopedia of life and EPPO) as well as in how many countries (A2) species have been recorded in European region with the pest status. EPPO A1 or A2

EPPO decision (1)

EU

Origin

Countries recorded

A1-2019

Central and North America

e

South America

e

Latin name

Potato psyllid

Bactericera cockerelli

A1

A1-2012

Cucurbit beetle

Diabrotica speciosa

A1

A1-2002

Western potato flea beetle

Epitrix subcrinita

A1

A1-2010

Emergency measures 2012

Central and North America

e

Tuber flea beetle

Epitrix tuberis

A1

A1-1987

Emergency measures 2012

North America

e

Sugarbeet wireworm

Limonius californicus

A1

A1-2002

North America

e

Common wireworm

Melanotus communis

A1

A1-2002

North America

e

Andean potato weevil

Premnotrypes latithorax

A1

A1-1981

South America

e

Andean potato weevil

Premnotrypes suturicallus

A1

A1-1981

South America

e

Andean potato weevil

Premnotrypes vorax

A1

A1-1981

South America

e

Potato flea beetle

Epitrix cucumeris

A2

A2-2001

Emergency measures 2012

North America

2, restricted

Epitrix papa

A2

A2-2016

Emergency measures 2016

North America

2, restricted

The Colorado potato beetle

Leptinotarsa decemlineata

A2

A2-1975

PZ quarantine pest (annex III) 2019

Central and North America

36, restrictedwidespread

Central American potato tuber worm

Tecia solanivora

A2

A2-2002

A1 quarantine pest (annex II A) 2019

Central and South America

1, restricted

EPPO A1 pest-a pest recommended by EPPO to member countries, for regulations as a quarantine pest, and which is not present in the EPPO region. EPPO A2 pest-a pest recommended by EPPO to member countries, for regulations as a quarantine pest, and which is present in the EPPO region.

Regional overview of potato pest problem in EU Chapter | 18

Common name

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FIG. 18.4 The estimated relative abundances of various potato pests in Europe. Data from EPPO 2020. Eppo Standard PM 1/2(29). EPPO A1 and A2 Lists of Pests Recommended for Regulation as Quarantine Pests. https://www.eppo.int/media/uploaded_images/RESOURCE S/eppo_standards/pm1/pm1002-29-en.pdf. (Accessed 23 July 2021).

18.5 Means of mitigating pest problems The Irish potato famine made it obvious that food production can be affected greatly if foreign pests are introduced in Europe. Since the 1877 Destructive Insects Act in the United Kingdom, there have been rules and regulations designed to mitigate pest problems before they arrive to Europe (Dehnen-Schmutz et al., 2010). Another evidence of the historically keen interest in new pests is an article in Finnish newspaper Helsingfors Dagbladet dated from 1874 that warns its readers of a potential new threat to potato, the Colorado potato beetle, even though by that time the beetle had not even reached the Atlantic coast of the United States (Riley, 1876). A couple of years later, the press in Europe was advising readers to follow essentially the same quarantine measures that are in practice today: prevent introduction - prevent establishment - control the established pests (Dehnen-Schmutz et al., 2010). Since then, collective effort in proactive pest detection and quarantine regulations remain an important part of the effective pest management in the EU. Currently, this effort is coordinated by EPPO (EPPO, 2004) and EU directives. Similar to other regions, chemical control, which is covered in detail in Chapter 11, is the main approach to managing insect pests of potato in the EU. Many growers also try adopting effective IPM strategies; however, these still involve considerable use of pesticides (see Chapter 27 on the discussion of what constitutes an IPM approach). It is estimated that the yield gain from using plant protection products in potato is 42% (Oerke, 2006). Although agricultural authorities in the EU member states are obligated to collect various data on the usage of pesticides, there is no publicly available information on their use by crop and by area treated. This is unfortunate, because this type of data would be most useful when analyzing insecticide resistance development in pest populations (see Chapter 24 for discussion). Similar information would also be useful when analyzing the risks of pesticides for human health. According to the pesticide sales data, fungicides and bactericides are the two most used pesticide groups used in potato production in Europe, followed by herbicides and insecticides (Anonymous, 2019b). In a 5-year period (2010e14), farmers in 23 countries used, on average, 61.7 different active substances (ranging from 22 in Norway to 128 in Italy) on potato (Anonymous, 2019b). Organic potato farming has remained a relatively small segment in Europe, amounting to only 1.3% of all holdings. However, this is likely to change in the future (De Ciggo and Jeanty, 2019).

18.6 Future challenges Most important factors contributing to the potential increase in pest problems in the future are increasing trade, globalization, and climate change (Brasier, 2008; Pautasso et al., 2010; Bebber et al., 2013), as well as failures in pest control due to insecticide resistance (see Chapter 24 for the discussion of the latter). These threats are also likely to act in combination. It is difficult to predict the effects of changes in agricultural policies (e.g., the bans of glyphosate or neonicotinoids and new pesticide directive) and the development of consumer preferences on the potato farming in Europe. For instance, some effective control methods may involve GMO crops, whereas the current consumer bias is against them. It is also likely that various threats act differently in different parts of Europe (Oerke, 2006).

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18.6.1 International trade Globalization has increased the magnitude and diversity of biological invasions worldwide (Hulme, 2009). EPPO standards provide strict regulations for potato trade (Anonymous, 2000, 2002) in the EU. Additionally, there is not much import of potato from non-EU countries. Therefore, the risks of new pest introductions due to international trade are low relative to other commodities (Suffert and Ward, 2014). However, recent studies show that potato pests may also enter the EU with non-regulated host plants. For example, tomato imports from outside the EU are increasing (Eurostat, Anonymous, 2019). As tomato belongs to the Solanaceae plant family, it can share pests with potatoes. The effects of introducing new species through the international trade are difficult to predict because pest status may be different between the place of origin and the area where they became newly established. For instance, Epitrix spp. were not problematic in their native range, but caused damage to crop plants when introduced to Europe (Boavida and Germain, 2009). Thus, in the future, it is important to increase the awareness of different risks together with good prevention practices to halt the introduction and further spread of new pests (Suffert and Ward, 2014).

18.6.2 Warming climate Climate change will definitely affect potato production in Europe (Hijmans, 2003; Raymundo et al., 2018). As Europe spans over latitudes from 35 degrees to above 65 degrees, the predicted effects are not the same throughout the region. Warming could open new areas for potato production in the northern regions. At the same time, opportunities to grow potatoes will diminish in the south due to the increased temperatures and drought. Early estimates on the direct increases in temperature suggested potato yields decreasing by up to 32% (Hijmans, 2003). On the other hand, climate change and increase in CO2 concentrations is shown to affect the allocation of the plant biomass. This can lead to decrease in aboveground stem biomass but increase in tuber size (Högy and Fangmeier, 2009). Temperature changes may also further increase pest problems. In Finland, for example, climate effects have shown to advance the onset of late blight outbreaks in the summer (Hannukkala et al., 2006), which in turn has increased the use of fungicides against this disease (Kaukoranta, 1996). Similar situations should be expected for insect pests. Increases in pesticide usage can have negative effects if they promote pesticide resistance (see Chapter 24). At the same time, due to the climate change pests are predicted to invade new areas, thus enlarging their ranges (Bebber et al., 2013; Carter et al., 1996) and potentially resulting in increased overall yield losses. Warming climate may also aggravate insect pest problems in potatoes in northern areas, which historically have had relatively little problems with them. Increasing temperatures have accelerated pest invasions beyond what should be expected during natural range shifts by native species, possibly due to the interaction of changing climate with other human activities, such as changes in the land use (Bebber et al., 2013; Lindström and Lehmann, 2015). Alternatively, warming climate may prevent the damage by some pests when the temperatures rise over their thermal limits (Hannukkala et al., 2006) or when overwintering conditions become unfavorable (Lindström and Lehmann, 2015). A warming climate will also likely increase the range of some pest species, such as the Colorado potato beetle, toward northern latitudes (Boman, 2008; Jeffree and Jeffree, 1996).

18.6.3 Agricultural policies and consumer choices Global demand for food is expected to increase between 59% and 98% by 2050 (Conijn et al., 2018) due to the increase of human population. At the same time, there is an increasing demand for a sustainable vegetarian diet. Due to its nutritional value, potato could easily be an important part of the latter. However, potato production relies on various chemical aids from fertilizers to plant protection products. This may be in conflict with the European Green Deal policy, which aims to transform EU to a low-carbon economy that supports a thriving natural world. According to the seventh Environment Action Program by the European Commission, its goal is that “the use of plant protection products does not have any harmful effects on human health or unacceptable influence on the environment, and such products are used sustainably.” In the heart of the conflict are the alarming news on the decline of biodiversity (Hallmann et al., 2014, 2017), partially due to the effects of agricultural use of pesticides (Bartolomeis et al., 2019). As there is a strong citizen interest in Europe to improve agricultural policies, the key questions for the future will be how the EU restrictions against pesticide use (e.g., cancellation of herbicide glyphosate and the neonicotinoid insecticides) will affect potato production (see Pesticides Database, 2021). Historically, there has also been a strong resistance to GMO products among the European consumers. This makes the use of alternatives to pesticides challenging. Whether potato production survives the increase in crop loss due to restricted pesticide use and whether consumers are willing to pay more for organically grown potatoes remains to be seen. With changes in the EU policies and potentially also in consumer choices regarding potato, only the future will tell how the 500-year-old tradition of potato farming in Europe will develop.

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References Anonymous, 2000. Council Directive 2000/29/EEC of 8 May 2000 on protective measures against the introduction into the community of organisms harmful to plants or plant products and against their spread within the Community. Off. J. Eur. Communities L 169 1e146. Anonymous, 2002. Council Directive 2002/56/EC of 13 June 2002 on the marketing of seed potatoes. Off. J. Eur. Communities L 193 60e73. Anonymous, 2019a. For EU Agricultural Markets in 2019 and 2020. Short Term Outlook. Autumn 2019. Edition N
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Ecological and Genetic Factors Contributing to Invasion Success : The Northern Spread of the Colorado Potato Beetle (Leptinotarsa decemlineata). University of Jyväskylä. Bosquee, E., Boullis, A., Bertaux, M., Francis, F., Verheggen, F.J., 2018. Dispersion of Myzus persicae and transmission of potato virus Y under elevated CO2 atmosphere. Entomol. Exp. Appl. 166, 380e385. Brasier, C.M., 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 57, 792e808. Burton, W.G., 1948. The Potato: A Survey of its History and of Factors Influencing its Yield, Nutritive Value and Storage. Chapman & Hall, London. CABI, 2020. Datasheet Leptinotarsa decemlineata (Colorado Potato Beetle). https://www.cabi.org/isc/datasheet/30380. (Accessed 12 October 2020). Carter, T.R., Saarikko, R.A., Niemi, K.J., 1996. Assessing the risks and uncertainties of regional crop potential under a changing climate in Finland. Agric. Food Sci. Finl. 5, 329e350. 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Nature 511, 341e343. Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D., de Kroon, H., 2017. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One 12, e0185809. Hannukkala, A., Kaukoranta, T., Lehtinen, A., Rahkonen, A., 2006. Late-blight epidemics on potato in Finland, 1933e2002; increased and earlier occurrence of epidemics associated with climate change and lack of rotation. Plant Pathol. 56, 167e176. Helsingfors Dagpladet, 1874. https://digi.kansalliskirjasto.fi/sanomalehti/binding/490584?t erm¼decemlineata&page¼2. (Accessed 23 July 2021). Hijmans, R.J., 2003. The effect of climate change on global potato production. Am. J. Potato Res. 80, 271e279. Högy, P., Fangmeier, A., 2009. Atmospheric CO2 enrichment affects potatoes: 1. Aboveground biomass production and tuber yield. Eur. J. Agron. 30, 78e84.

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Hulme, M., 2009. Why We Disagree about Climate Change: Understanding Controversy, Inaction, and Opportunity. Cambridge University Press, Cambridge, UK, p. 432. Jansky, S.H., Spooner, D.M., 2018. The evolution of potato breeding. Plant Breed. Rev. 41, 169e214. Jeffree, C.E., Jeffree, E.P., 1996. Redistribution of the potential geographical ranges of mistletoe and Colorado beetle in Europe in response to the temperature component of climate change. Funct. Ecol. 10, 562e577. Kaldy, M.S., 1972. Protein yield of various crops as related to protein value. Econ. Bot. 26, 142e144. Kapsa, J.S., 2008. Important threats in potato production and integrated pathogen/pest management. Potato Res. 51, 385e401. Kaukoranta, T., 1996. Impact of global warming on potato late blight: risk, yield loss and control. Agric. Food Sci. Finl. 5, 3113e3127. Kinealy, C., 1995. This Great Calamity: The Irish Famine 1845-52. Roberts Rinehart Pub, p. 450. Kolasa, K.M., 1993. The potato and human nutrition. Am. Potato J. 70, 375e384. Lindström, L., Lehmann, P., 2015. Chapter 8. Climate change effects on agricultural insect pests in Europe. In: Björkman, C., Niemelä, P. (Eds.), Climate Change and Insect Pests. CABI Climate Change Series, Wallingford, UK, pp. 136e153. Niemi, J., Väre, M., 2019. Agriculture and food sector in Finland 2019. In: Natural resources and bioeconomy studies 37/2019. Nunn, N., Qian, N., 2009. The Potato’s Contribution to Population and Urbanization: Evidence from an Historical Experiment, NBER Working Papers 15157. National Bureau of Economic Research, Inc., Cambridge, MA, USA, p. 44. Oerke, E.-C., 2006. Crop losses to pests. J. Agric. Sci. 144, 3e431. Orlova-Bienkowskaja, M.J., 2015. Epitrix papa sp. n. (Coleoptera: Chrysomelidae: Galerucinae: Alticini), previously misidentified as Epitrix similaris, is a threat to potato production in Europe. Eur. J. Entomol. 112, 824e830. PAN, 2007. State of the Art of Integrated Crop Management & Organic Systems in Europe, with Particular Reference to Pest Management. https://www. pan-europe.info/sites/pan-europe.info/files/public/resources/reports/potato-production-review.pdf. (Accessed 23 July 2021). Pautasso, M., Dehnen-Schmutz, K., Holdenrieder, O., Pietravalle, S., Salama, N., Jeger, M.J., 2010. Plant health and global change e some implications for landscape management. Biol. Rev. 85, 729e755. Powderly, W.G., 2019. How infections shaped history: lessons from the Irish famine. Trans. Am. Clin. Climatol. Assoc. 130, 127e135. Raymundo, R., Assenga, S., Robertson, R., Petsakos, A., Hoogenboom, G., Quiroz, R., Hareau, G., Wolfd, J., 2018. Climate change impact on global potato production. Eur. J. Agron. 100, 87e98. Riley, C.V., 1876. Potato Pests. Orange Judd Company, New York, p. 108. Salaman, R., 1949. The History and Social Influence of the Potato. Cambridge University Press, Cambridge, UK, p. 599. Suffert, M., Ward, M., 2014. Emerging pests of potato in Europe: early warning, risk analyses and regulation. Potato Res. 57, 263e271. Stenberg, J.A., Flø, D., Kirkendall, L., Krokene, P., Alsanius, B., Magnusson, C., Nicolaisen, M., Thomsen, I.M., Wright, S.A.I., Rafoss, T., VKM, 2019. Pest Risk Assessment of Selected Epitrix Species. Scientific opinion of the panel on plant health. VKM report 2019, 17, ISBN 978-82-8259-333-5. ISSN: 2535-4019. Norwegian Scientific Committee for Food and Environment (VKM), Oslo, Norway. van Berloo, R., Hutten, R.C.B., van Eck, H.J., Visser, R.G.F., 2007. An online potato pedigree database resource. Potato Res. 50, 45e57. Wójtowicz, A., Wójtowicz, M., Sigvald, R., 2013. Forecasting the influence of temperature increase on the development of the Colorado potato beetle Leptinotarsa decemlineata (Say) in the Wielkopolska region of Poland. Acta Agric. Scand. B. 63, 136e146.

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Chapter 19

Russian Federation, Belarus, and Ukraine Andrei Alyokhina, Galina Benkovskayab, Galina Sukhoruchenkoc, Sergei Volgarevc and Ildar Mardanshind a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bInstitute of Biochemistry and Genetics, Russian Academy of

Science, Ufa, Russia; cAll-Russian Plant Protection Institute, Saint Petersburg, Russia; dBashkortostan Agricultural Scientific Research Institute, Russian Academy of Science, Ufa, Russia

19.1 History and local characteristics of potato production Potato was introduced to Russian Empire in the late 17th century from the Netherlands by Emperor Peter the Great. However, initially it was grown mostly as an exotic curiosity and did not enter the mainstream agriculture for another 100 years. During that period, adoption of potato was heavily promoted by the government, which imported seed tubers, organized public education campaigns, and mandated peasants to allocate a portion of their land for planting potatoes. The latter was often done against their will and met with considerable resistance. Nevertheless, growing potatoes eventually became a common practice. Similar to other countries, incorporating potatoes into people’s diets resulted in considerable improvements in their nutrition and, consequently, in public health. However, it was still done largely for personal consumption by peasants and their livestock until mid-19th century. After that, development of capitalist economy led to the creation of an increasing number of industrial enterprises processing potatoes into starch, molasses, and ethanol. That lead to a considerable expansion of potato farming. By 1913, 30 million tons of potatoes were harvested from four million ha (Anonymous, 2019). Potatoes are still an important crop in the Russian Federation, Belarus, and Ukraine, the three countries that comprised a considerable part of the Russian Empire and then the Soviet Union and have overlapping agroclimatic conditions (see below for details). Similar to other countries, potatoes are produced by large agricultural enterprises, some of which own both farmland as well as processing facilities, and by smaller family farms. However, one feature of agricultural production that is somewhat unique to Russia, Belarus, Ukraine, and, to a smaller degree, other former Soviet republics, is the importance of part-time amateur farming. Many urban families who lived in apartments and worked in cities also retained a plot of land and a house (dacha) in the country, where they spent weekends and summer vacations. Rural residents working at state-owned agricultural enterprises under communist regime also had small parcels of land that they farmed independently of their main jobs. One reason for such an arrangement was a relatively recent urbanization, so that a dacha served for the new city dwellers as a remaining link to a more familiar rural lifestyle. Another reason was that having access to a plot of arable land, albeit a small one, served as an insurance against food insecurity that repeatedly plagued these regions throughout the 20th century. Yet another reason was a better control over food quality and origins, including an ability to grow organically or at least without pesticides. Dachas remain very popular, although in recent years many of them have been either converted into year-around suburban residences or started being used more for recreational purposes rather than for supplementing food supply. Most fruits and vegetables, including potatoes, produced on dachas are for personal consumption. However, some are being sold on farmer’s markets and roadside stands. Private production by part-time farmers and gardeners is responsible for a large part of an overall potato harvest in the three countries that are reviewed in this chapter.

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19.2 Russian Federation 19.2.1 Potato farming in overall economy Russia is the third largest producer of potatoes after China and India, with the annual gross harvest of about 22.4e25.4 million tons in 2015e18. Potato fields occupy, depending on the year, between 1.3e1.6 million ha and rank seventh among all crops after wheat, barley, sunflower, soybeans, field corn, and canola (RosStat, 2019). Potato is grown for human consumption, animal feed, and processing into starch and ethanol (Popov and Yahyaev, 2003). Average yields in years 2015e18 ranged between 16.4e17.0 t/ha (RosStat, 2019). Almost all harvested potatoes are produced and consumed internally (Fursov, 2018). Imports amounted to 778,800e874,600 tons in 2017e18, a large part of which (293,600e536,900 tons) are early potatoes that are imported in the spring to provide high-quality tubers before local harvest (IAMS, 2020). Egypt is the largest importer of potatoes to Russian Federation (46.5%), followed by Belarus (54.3%) (AB Center, 2018). Potato exports are small and destined mostly to surrounding countries (Georgia, Azerbaijan, Belarus, Uzbekistan, and Serbia), although there is a trend toward their increase from 116,900 tons in 2017 to 268,600 tons in 2019 (IAMS, 2020).

19.2.2 Local agroclimatic conditions Potato is grown throughout the vast expanses of the Russian Federation in a variety of soils and under different climatic conditions. The only major exception are the areas immediately adjacent to the Arctic Ocean. However, the most suitable areas for its production are in the center of the European part of the country and along Volga river. More than one-third of all commercially grown potatoes are from five oblasts (districts): Bryansk (10.9%), Tula (7.8%), Nizhniy Novgorod (6.5%), Moscow (6.1%), and Astrakhan (4.5%). Except for arid areas in Astrakhan and Volgograd oblasts and North Caucasus, most potato fields are not irrigated. Therefore, southern regions are too hot and dry for commercial potato farming (AgroVesti, 2021). Because of a relatively short growing season, early and mid-season varieties are most common in the Russian Federation. Varieties that require more than 100 days to mature usually do not have enough time to complete their development (AgroPortal, 2014; Simakov, 2018). Storage losses of late varieties may reach 25%, especially when tubers are bruised during the harvest (Fursov, 2018).

19.2.3 Main producers and market conditions Most potatoes in Russian Federation are produced by part-time farmers and gardeners. In 2018, they harvested 68% of the 22.4 million tons of potatoes produced in the country, while agricultural corporations harvested 19.3%, and family farmers harvested the remaining 12.7% (RosStat, 2019). Similar distribution was present in 2019, when a total of 22.8 million tons were harvested (Yuzhaninova, 2019). Between 2015 and 2019, areas planted to potatoes by part-time farmers and gardeners decreased from 1,201,000 ha to 975,700 ha, and areas planted to potatoes by other types of growers decreased from 361,000 ha to 305,000 ha (RosStat, 2019). Part-time growers heavily rely on manual labor, do not practice crop rotation, and often grow their own seed. As a result, their yields are low (14.8e15.5 t/ha in 2015e18), which is responsible for an overall low yield in the country (16.4e17.0 t/ha during the same period). At the same time, commercial family farmers harvested 20.6 t/ha in 2017, while agricultural corporations harvested 24.8 t/ha (RosStat, 2019). In 2019, yield in the latter increased to 25.4 t/ha (AgroVesti, 2020a), and there is further potential for its growth (Goncharov and Salnikov, 2019). Overall demand for seed potatoes amounts to 3.7e4 million tons per year. Early-generation tubers are often imported and propagated by large agricultural corporations, which either plant resulting later-generation seed on their fields or sell it to other growers. In 2019, 9,400 tons of mini-tubers and first-generation field-grown tubers were imported from The Netherlands (40.8%), Germany (33.8%), Finland (12.9%), and Belarus (7.2%) (AgroVesti, 2020b). Foreign varieties heavily dominate the market because of their often superior agronomic characteristics and effective marketing by their producers. There are 428 potato varieties registered in Russian Federation, of which 221 are of local selection. However, the latter amounted to only 17.3% of planted tubers in 2017 (Anisimov et al., 2018). There are efforts to increase the share of locally developed and grown seed, but their success has been limited so far (Anisimov et al., 2018; Medvedeva, 2019). Currently, about 20% of potatoes, mostly those harvested by large corporations, are processed into French fries, chips, dehydrated mashed potatoes, starch, etc. (IAMS, 2020). These are mostly consumed locally, but export also amounted to 110,000 t in 2017 (Anonymous, 2018). Potato processing is highly profitable and there are several large plants operating in this area. Some of these belong to Russian entrepreneurs while other are either owned by multinational corporations or are joint ventures (Shakin, 2017).

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19.2.4 Main insect pests About 60 species of invertebrates, including nematodes, attack potatoes on the territory of the Russian Federation (Ahatov et al., 2013). These include both soil-dwelling species that attack roots and tubers, as well as foliar pests. Among the former, wireworms (Coleoptera: Elateridae) are most damaging and may be responsible for 30%e60% reduction in yield. Details on wireworms biology and management are discussed in Chapter 7. Species composition of this group depends on the area of the country. For example, the most common wireworms in north-western regions of the Russian Federation are Agriotes obscurus L., A. lineatus L., Selatosomus aeneus L., and Hemicrepidius (Athous) niger L. Corimbites sjelandicus Mull., Limonius (Сidnopus) aeruginosus Ol., Adrastus nitidulus Marh. ¼ pallens F., Athous (Grypocarus) haemorrhoidalis F. are also present, but in small numbers (Volgarev, 2003). South-east of the European part of the Russian Federation is dominated by A. gurgistanus Fald., A. sputator L., Melanotus fusciceps Gyll., and A. tauricus Heyd (Orlov and Zelenskaya, 2017). Another important group of soil-dwelling pests are white grubs (Coleoptera: Scarabaeidae), in particular Melolontha hipocastani F. and M. melolontha L. These species have 4-5-year life cycle. Most damage is done by late instars that consume roots and make holes in tubers. Feeding injury also opens a route of entry for several pathogens that cause tubers to rot. Damage is often particularly severe on fields that are adjacent to forested areas that serve as adult habitats (Berezina, 1960; Alekseeva, 2019). Cutworms (Lepidoptera: Noctuidae) attacking potatoes in Russia include Agrotis segetum L., A. exclamationis L., A. ipsilon Hufnagel and several other minor species. They often build up in large numbers on potatoes planted by part-time farmers and gardeners and then spread to commercial potato fields. Most damage is done by late instars that feed on stems and may also make holes in tubers. In some years, there are also serious outbreaks of another noctuid moth, potato stem borer Hydroecia micacea Hb., which is common throughout the country. Populations of this species usually build up on weedy vegetation and then late instars move to potatoes and borrow inside the stems, causing them to wilt (Ahatov et al., 2013). Mole cricket Gryllotalpa gryllotalpa L. (Orthoptera: Gryllotalpidae) is a serious pest of potatoes that is widely spread throughout Russia, except the far northern areas. Nymphs and adults of this species feed on tubers, making large holes that render them unusable. The problem is especially serious on small plots maintained by part-time farmers and gardeners (Ahatov et al., 2013). Colorado potato beetle, Leptinotarsa decemlineata Say, is the most important insect defoliator of potatoes in the Russian Federation (Chapter 4 provides details on this pest). Because of its high mobility, as well as its ecological and evolutionary plasticity (Chapter 24), this species spread into all major potato-growing areas of the country, where it formed populations specifically adapted to local conditions (Fasulati and Vilkova, 2000). Until 2003, the Colorado potato beetle was listed as a quarantine pest, but now it is considered to be well-established in the country. Control of this insect is greatly complicated by its ability to evolve resistance to insecticides, especially when chemicals are applied excessively and indiscriminately (Pavlyushin et al., 2009, see also Chapter 24). In maritime areas of Russian Far East and southern areas of Khabarovsk Krai and Amursk Oblast, potato ladybird Henosepilachna (¼Epilachna) vigintioctomaculata Motsch. (Coleopterа: Coccinellidae) replaces the Colorado potato beetle as the most damaging defoliating pest (Ivanova, 1962; Ahatov et al., 2013). This species may cause yield losses of up to 40% and may potentially facilitate transmission of potato viruses M, X, and Y (Sobko et al., 2021). For details on these species, refer to Chapter 10. Potato tuberworm Phthorimaea operculella Zell. (Lepidoptera: Gelechiidae) has recently become a serious pest of potatoes in southern Russia. This species is under quarantine but continues expanding its range despite all the efforts to contain it (Yusupov, 2006). Damage is done both in the field and in storage, with storage facilities being important breeding grounds for the tuberworm. More information on biology and management of this species can be found in Chapter 7. Several aphid species (Homoptera: Aphididae) infest potatoes in Russia, with species complexes being similar across the country. Species commonly colonizing potatoes are Aphis fabae Scop., Macrosiphum euphorbiae Thomas, Aulacortum solani Kalt., Myzus persicae Sulz., Aphis nasturtii Kalt., and Aphis frangulae Kalt. They cause direct damage through feeding during the outbreak years of high density. However, most damage is caused by transmission of plant viruses (Zamalieva, 2013; Zeiruk et al., 2017; Sukhoruchenko et al., 2019). For additional details on aphids and their control, see Chapter 5.

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19.2.5 Methods of pest control Commercial potato growers mostly rely on insecticides, while control methods vary greatly among amateur part-time growers depending on the size of their plots, personal preferences, and ability to spend money on crop protection. A total of 113 insecticides based on 23 different active ingredients from nine chemical classes are registered on potatoes, of which seven are biological in origin (MARF, 2020a). Overall, chemical control is currently effective in protecting potato fields in Russian Federation. However, insecticide resistance is common in Colorado potato beetle populations; it is also a concern for potato-colonizing aphids. Rotating insecticides with different modes of action is the most commonly recommended approach to resistance management (Sukhoruchenko et al., 2017). GMOs are not allowed in the Russian Federation. At the same time, considerable attention is being paid to traditional breeding of varieties that are resistant or tolerant to insect pests. More than 20 varieties offer at least some protection against the Colorado potato beetle, with 15 of them also having reduced susceptibility to nematodes: Bafana, Victoria, Gala, Danaya, Delfine, Ladozhskiy, Liga, Nayada, Radonezhskiy, Real, Ryabinushka, Santa, Sifra, Kholmogorskiy, Yanka (MARF, 2020b). However, as discussed above, commercial seed market is heavily dominated by imported varieties. Several integrated pest management (IPM; see Chapter 27 for a detailed discussion of what constitutes this approach) plans have been developed for protecting potatoes by different types of growers in the Russian Federation. These include using an array of methods including using high quality seed potatoes, planting adjacent potato fields within a short period to synchronize their phenology and the timings of subsequent treatments, proper fertilization, deep plowing to destroy soildwelling pests, selection of pest-resistant varieties, and separation of seed potato fields from table stock and processing potato fields. Extended rotations of 4e6 years are highly recommended, with legumes, crucifers, winter rye, or fallow ground immediately preceding potatoes. Under the IPM, wireworms populations are sampled prior to planting and highly infested fields are avoided. Monitoring for foliar pests continues throughout the season and serves as a basis for applying insecticides (Anisimov et al., 2018; Zeiruk et al., 2017; Sukhoruchenko et al., 2011, 2016).

19.2.6 Problems and perspectives Sufficient potato supplies are considered to be an important part of an overall food security in the country; thus, there is a Presidential Executive Order # 120 (http://kremlin.ru/acts/bank/30563) setting a goal of producing 95% of all consumed potatoes domestically. This amounts to a total harvest of 26 million tons per year, including 14 million tons of potatoes for table stock, five million tons for animal feed, four million tons of seed tubers, and one million for processing (Anisimov et al., 2018). Storage losses need to be reduced to 6% (1.5 million tons) due to building new and upgrading existing storage facilities, while there are plans to maintain exports of at least 112,000 tons per year. Average yields are projected to remain within the range of 25e26 t/ha at large agricultural corporations and between 20e22 t/ha on smaller farms (Anisimov et al., 2018). Producing sufficient amounts of high-quality seed tubers remains the main challenge facing potato industry in the Russian Federation. Local potato breeders are not competitive with the Western European companies due to insufficient experience with modern breeding technologies and often outdated equipment (Simakov, 2015). The importance of modernizing is acknowledged by the federal government that instituted in 2017 a program to develop a full-cycle system of potato breeding and seed production that integrates marker-assisted and genomic selection, quality control using PCRbased methods, and variety-specific adjustments in agronomic techniques (Resolution # 996, https://base.garant.ru/ 71755402). The end goal is developing at least 12 new potato varieties and producing 18,000 tons of early-generation seed domestically by 2026. Seed growers will be reimbursed 25%e35% of money spent on building or upgrading storage facilities, organizing breeding and seed distribution centers, testing seed quality, as well as on buying equipment and machinery, nuclear seed, and pesticides. In 2017e18, potato industry received 11 billion rubles ($220 million) from the federal budget and additional eight billion rubles ($160 million) in other government funding (Fedorenko et al., 2018).

19.3 Republic of Belarus 19.3.1 Potato farming in overall economy Agriculture comprises an important part of an overall economy in the Republic of Belarus. It amounts to 6.4% of the gross domestic product, 9.8% of total direct investment, and 15.6% of all exports. In 2018%, 7.6% of the population (more than 284,000 people) worked in that sector. Belarus also ranks first in the world in potato consumption, with an average person utilizing 170e177 kg per year (BelStat, 2019). It is also in the top 10 of potato-producing countries in the world. Residents

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of Belarus are even sometimes referred to as bulbashi (potatoheads). The nickname does not have negative connotations and is similar, for example, to the residents of Connecticut in the United States being called nutmeggers in recognition of their state’s historical importance in spice trade. Despite its importance in Belarus, there is a recent tendency toward a decrease both in the area planted to potatoes, as well as in the amounts of harvested tubers. Per capita production was 730 kg in 2012, but only 618 kg in 2018. Still, potato farming amounts to a significant part of an overall agricultural production: 17.9% in 2012% and 10.2% in 2018, when 4.7% of all agricultural land was planted to potatoes. Potato export increased from 47,300 tons to 299,500 tons during the same period (BelStat, 2019). There were 159 potato varieties grown in Belarus in 2019, of which 49 were developed locally (State Register of Varieties, 2019). Potato farming in Belarus is supported by the government. In addition to farm subsidies, the National Academy of Science has an active research center specifically dedicated to studying potatoes, as well as other vegetables and fruits. This center coordinates scientific efforts, development and implementation of new technologies, seed certification, and international collaborations (Uhatova, 2018).

19.3.2 Local agroclimatic conditions Belarus has a temperate continental climate that is influenced by the Atlantic and characterized by moderate rainy summers and mild winters (Brechko et al., 2016), which are generally favorable for potato production. However, the area is experiencing significant warming due to the global climate change. Since 1989, mean annual temperatures in Belarus increased by more than 1 C, mean durations of an established snow cover decreased by 10e15 days, and the depth of soil freezing decreased by 6e10 cm. This had a negative effect on potato production in the region. Having more than 10 days of a growing season with temperatures exceeding 30 С could explain over 33% of the instances of below-average yields (Davydenko and Lopukh, 2019). Probability of having such a season is currently about 70%, leading to average yield decrease of 1.27 t/ha (8%). Therefore, there is a considerable interest in breeding more heat-tolerant potato varieties, shifting to earlier planting dates, and installing irrigation systems (Davydenko and Lopukh, 2019).

19.3.3 Major potato producers As of January 1, 2019, 1,389 agricultural enterprises are incorporated in Belarus (BelStat, 2019). Family farms control only 2.3% of total agricultural land but produced 6.4% of potatoes in 2018. Among the six oblasts (districts) that comprise the Republic, most potatoes are grown in Minsk Oblast, where they occupy 60% of land belonging to 25.8% of agricultural enterprises. Sixteen farms in Belarus grow 1,000 or more ha of potatoes, but an average farm size is 73.5 ha (Grzelakowski, 2020). An average family farm allocates 54.8% of its overall production to potatoes and vegetables. Total area planted to potatoes on family farms increased from 12,900 ha in 2012 to 15,000 ha in 2018 (BelStat, 2019). Potatoes are very popular with part-time farmers and gardeners. Potato share increased to 83.4% of the total produce that they grew in 2018, compared to 78.2% in 2012 (BelStat, 2019). Average potato yields in Belarus are about 20 t/ha. They are higher for part-time farmers and gardeners (21 t/ha) and family farmers (26 t/ha). The most agriculturally advanced areas are Minsk Oblast and Brest Oblast (BelStat, 2019).

19.3.4 Main insect pests About 60 insect species are known to damage potatoes in Belarus. However, most of them are considered to be occasional or minor, with the exception of the Colorado potato beetle (Chapter 4) and virus-transmitting aphids (Chapter 5, Privalov et al., 2008, https://belbulba.by). Potato tuberworm (Chapter 8) is listed as a quarantine species (MAFRB, 2010, 2016). State Inspection for Seed Production, Quarantine, and Plant Protection publishes weekly updates on discoveries of quarantine pests and monthly updates on general phytosanitary conditions in the Republic (ggiskzr.by). For example, as of July 27, 2020, Colorado potato beetle was the only pest of concern reported for potatoes. Colorado potato beetle first invaded Belarus in 1959e60 (Brechko et al., 2016). Currently, it is a problem on 98%e100% of potato fields (Busko and Ficuro, 2016). Beetle damage varies depending on geographic location. It is usually the worst in southern regions of the Republic, where the beetles can produce two full and one partial generations in warm years. In severe cases, crop losses due to beetle damage may reach 40%. Economic threshold is set at 10% of plants inhabited by at least 20 first and/or second instars (Sokol et al., 2016).

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19.3.5 Methods of pest control Similar to other places, insect pests of potatoes in Belarus are mostly controlled with insecticides. Forty-seven different products from seven chemical groups are registered on potato in the Republic (Piskun et al., 2020). Fifteen of these are biological in origin. A study conducted in 2008 forecasted that an overall crop protection marked in Belarus would reach $96.3 million, of which more than $80 million would need to be imported. To promote national pesticide industry, a government-sponsored program aiming to increase the share of locally produced chemicals by 30%e40% was initiated (Privalov et al., 2008). Unfortunately, intensive chemical use was not accompanied by meaningful monitoring of resistance in insect populations, which is of particular concern for the Colorado potato beetle because of its high propensity for evolving insecticide resistance (Roslavtseva, 2009, see also Chapter 24). Failure of existing insecticides is a serious concern, and rotation of different active ingredients is recommended for its prevention (Busko and Ficuro, 2016). Neonicotionoids (Chapter 11) and biological insecticides (Chapter 13) are promoted as an alternative to pyrethroids, with a hope that rotations will also result in a gradual decline of the existing pyrethroid resistance in insect populations (Brechko et al., 2016). Published data indicated that thiamethoxam and Bacillus thurengiensis (Btt)-based materials were indeed highly effective. By 2014, a survey of 18,800 ha of potatoes in central and southern Belarus revealed that neonicotinoids accounted for 82.4% of the total volume of insecticides used (Sokol et al., 2016). GMOs are allowed in Belarus, and there are efforts to develop local transgenic varieties that are resistant to the Colorado potato beetle and diseases (Minchenko et al., 2013). However, no transgenic varieties have been commercialized as of beginning of 2020. Belarus is a signatory to the Cartagena Protocol on Biosafety, and there are 18 laboratories testing for the GMO presence on its territory (Lenivko and Boiko, 2019). There is a good potential for using alternative control methods for growing organic or ecofriendly potatoes (Sokol et al., 2016). Wide-scale field study showed that replacing chemical pesticides with mechanical cultivation and applications of materials based on Bacillus subtilis, Bt, and triterpenoids extracted from coniferous plants increased farming profitability by about 33% (Sokol et al., 2016).

19.3.6 Problems and perspectives In recent years, total area planted to potatoes in Belarus decreased from 335,000 ha in 2012 to 274,000 ha in 2018. Consequently, gross potato harvest decreased by almost 25% (Chepik and Demishkevich, 2019). Increase in fuel prices and transportation costs are often cited as being responsible for this decline. However, detailed analysis of the situation paints a more complicated picture. Higher temperatures during growing seasons promote outbreaks of potato diseases (Busko and Ficuro, 2016) and require development of new agrotechnical approaches that are still lacking (Davydenko and Lopukh, 2017). Furthermore, there is increasing international competition, higher labor and input demands compared to many other crops, and declining soil fertility due to insufficient fertilization. There are also labor shortages and lower consumer demand due to urbanization, aging, and negative population growth (Cheplyanskaya and Cheplyansky, 2018). As a result, there is a considerable unrealized potential in the production of both table stock and processing potatoes (Chepik and Demishkevich, 2019). Improvement in potato production is likely to involve better integration within frameworks of local agricultural systems, as well as increasing potato yields by using improved potato varieties (Chepik and Demishkevich, 2019). The latter includes more extensive use of molecular techniques, including transgenics, in potato breeding programs (Lenivko and Boiko, 2019). In addition, potato farming will benefit from changing the structure of state support from subsidizing specific crops to directly subsidizing farms based on their size (Chervinskaya, 2018).

19.4 Ukraine 19.4.1 Potato farming in overall economy Ukraine is one of the main producers of potatoes in the world, being essentially tied with the Russian Federation for the third place. However, area planted to this crop has decreased from a historic average of 1.5 million ha to 1.32 million ha in 2019 (Melnichuk et al., 2019), with a total harvest of 20.27 million tons. Average yield is 15.5 t/ha (FAOSTAT, 2021), which is considerably lower than possible under agroclimatic conditions of the area (Vorobyova and Ulyanich, 2014).

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19.4.2 Local agroclimatic conditions Potatoes are traditionally grown in six oblasts of Ukraine: Lviv, Rivne, Zhytomyr, Kyiev, Chernihiv, and Sumy. In the southern areas of the country, two potato crops can be harvested in 1 year. Unfortunately, due to the global climate change mean daily temperature increased by 0.8 С, while mean annual precipitation decreased by 19.4 mm. Consequently, the period of above-optimum temperatures during an average growing season increased from several days to approximately 2 months. As a result, growing potatoes in southern Ukraine currently has low profitability. The situation can be improved by planting heat- and drought-tolerant varieties and installing drip irrigation. However, this requires considerable additional investment (Lutsenko, 2013; Lavrinenko and Balashova, 2015; Lavrinenko et al., 2016). The situation is better in other areas of the country.

19.4.3 Major potato producers Almost all potatoes (98%) are grown in private sector (Gutsul and Parkhomenko, 2018). Most of them are produced by small private farmers, including part-timers (Stetsky and Shostak, 2010; Melnyk et al., 2017). Among the five to seven large agricultural enterprises that have significant interest in potatoes, 47% of the market are controlled by a single company, Mriya Agroholding (Melnyk et al., 2017; Michkovskaya, 2019). Most potatoes are sold as table stock for domestic consumption. Approximately 200,000 tons per year are processed, mostly into starch and ethanol. Internal production does not fully meet the internal demand. Therefore, 188,400 tons of potatoes were imported in 2019 (Michkovskaya, 2019), and the imports further increased to 259,140 tons in 2020 (Loshakova, 2020).

19.4.4 Main insect pests Over 70 species of invertebrates damage potatoes in Ukraine. Together, they are responsible for 35%e40% yield losses (Melnichuk et al., 2019). The most damaging insect pests are wireworms (ca. 15 different species), mole crickets, and Colorado potato beetles. The most important quarantine species are potato tuberworm and foxglove aphid, A. solani. Colorado potato beetle was removed from the quarantine list in 2014 after becoming established in all areas of the country (Klechkovskii and Titova, 2014; Berim and Saulich, 2018; Melnichuk et al., 2019). Foxglove aphid is a serious problem in southern Ukraine (Berim and Saulich, 2018; Melnichuk et al., 2019). Potato tuberworm causes significant damage in many areas of the country, possibly because initial quarantine regulations were not established nation-wide but covered selected areas as the pest became infested (Klechkovskii and Titova, 2014; Grichanov et al., 2017).

19.4.5 Methods of pest control Chemical control dominates potato protection in Ukraine (Vashchischin, 2016). Pesticide registry is maintained by the Ministry of Energy and Natural Resources. New pesticides must undergo testing that is conducted by the state-supported Institute for Plant Sciences (division of the National Academy of Agricultural Sciences) or other organizations approved by the government (Boiko and Patyka, 2017; Melnichuk et al., 2019). Particular attention is paid to testing efficacy of various biological products on different potato varieties (Vashchischin, 2016). This category is not limited to biological control agents and includes insecticides with active ingredients that are biological in origin like avermictins and spinosyns. In early 1990s, 216 production facilities produced biological pesticides in Ukraine that were applied at five million ha of agricultural fields (not only potatoes). Their number decreased dramatically in the subsequent years once government funding discontinued. However, it has been rebounding since 2008, with the acreage protected by such products increasing from 14,500 ha in 2008 to 185,000 ha in 2018. Currently, there are 40 production facilities manufacturing biological pesticides in Ukraine (Rethman et al., 2018). One of them, Metawhite, was developed domestically and is based on a mixture of Metarhizium anisopliae, Beauveria bassiana, and Bacillus thur{ng{ens{s. Potato Research Institute (another division of the National Academy of Agricultural Sciences) has a potato breeding program directed toward developing high-yielding varieties that are resistant to fungal and viral diseases (Podgayetsky, 2012; Tymko et al., 2018). It also tests domestic and foreign varieties for pest resistance. However, the only insect pest currently taken into consideration is the Colorado potato beetle (Borivskyi, 2016; Voitsekhovsky et al., 2017). In the study conducted in the Russian Federation, two Ukrainian varieties (k-25,281 and Polonez) showed good levels of resistance to this pest (Kostina et al., 2020).

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GMO is allowed in Ukraine, although each transgenic variety must be reviewed and approved by agricultural authorities (Torsky, 2020). No GMO potatoes are grown in the country. Monsanto grew several fields of NewLeaf and NewLeaf Plus Bt potatoes in 1997e99 without proper authorization, but the practice was discontinued afterward, and the remaining tubers were destroyed (Dudov and Terehin, 2014).

19.4.6 Problems and perspectives Potato consumption in Ukraine declined from 7.7 kg per person in 2010 to 6.3 kg per person in 2018 (Michkovskaya, 2019). Export potential is currently low because potatoes are traditionally not considered to be an export commodity, their quality does not meet international standards, and selection of available varieties is low (Melnyk et al., 2017). There is considerable competition for land and labor from other commodities, such as corn and sunflower. Also, recent increases in the costs of energy, water, and seasonal labor have a negative effect on profitability of potato farming (Michkovskaya, 2019). In plant protection, there are insufficient government resources dedicated to planning and implementing quarantine measures, as well as to regulating pesticide registration and use. The latter involves safety regulations in pesticide handling, and especially in disposal of expired chemicals (Vygovskaya, 2016). To address existing challenges, the Ukrainian government has developed a program for supporting potato industry in 2021e25. This includes increasing large-scale industrial production of this crop, increasing production of seed potatoes from the current 14,000 tons to 210,000 tons per year, installing irrigation systems on the additional 23,000 ha, and building six new processing plants (Anonymous, 2021). There is increasing interest in Ukrainian potatoes from foreign companies, but the extent of cross-border operations remains limited (Michkovskaya, 2019). In particular, there may be a good unrealized potential for an export business in seed potatoes. Another very promising area is production of certified organic potatoes (Melnyk et al., 2017).

19.5 Summary and conclusions Potatoes play an important, although slightly diminishing, role in economy and people’s diets in the Russian Federation, Belarus, and Ukraine. All three countries are among the largest producers of this crop in the world. However, a significant proportion of potatoes is grown by part-time farmers using relatively low-tech approaches; therefore, average potato yields are not particularly high. As more potato production shifts toward large agricultural enterprises, yields are likely to go up, but at the expense of increasing the amounts of purchased inputs (see Chapter 25 for the discussion of this trade-off). Pest complex is similar to other temperate areas of the world and is comprised mostly of Colorado potato beetle, aphids, wireworms, and, increasingly, potato tuberworm. One important pest that is specific to the region is mole cricket, which usually causes only occasional damage in other areas. Chemical control is the main approach to pest management, particularly on the large scale. Despite large areas planted to potatoes, growers in the region are heavily dependent on the early-generation seed tubers imported from Western Europe. Another challenge is warming climate that results in heat stress of potato plants during growing season. There are ongoing efforts, which are sponsored by the governments, to improve local potato breeding, including developing pest-resistant and heat-and drought-tolerant varieties.

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Invest. Russia 10, 31 (in Russian). Grichanov, I.Y., Yakutkin, V.I., Ovsyannikova, E.I., Saulich, M.I., 2017. Maps of Areas and Zones of Harmfulness of Potato and Sunflower Pests and Diseases, N21. Plant Protection News Supplements, p. 63. Grzelakowski, A., 2020. Top 16 thousand farmers in Belarus (in Russian). https://officelife.media. (Accessed 17 August 2020). Gutsul, T.A., Parkhomenko, K.M., 2018. Development of the potato market in Ukraine. Curr. Prob. Humanit. & Nat. Sci. 11, 59e61 (in Russian). Institute for Agricultural Market Studies (IAMS), 2020. Outcomes of 2019. Potato Market. http://ikar.ru/lenta/709.html. (Accessed 3 December 2020) (in Russian). Ivanova, A.N., 1962. Potato Lady Beetle in Far East. Nauka, Vladivostok, p. 53. Klechkovskii, Y.E., Titova, L.G., 2014. The object of internal quarantine of plants in Ukraine. Plant Protect. News 9, 33e35 (in Russian). Kostina, L.I., Kosareva, O.S., Truskinov, E.V., Kirpicheva, T.V., 2020. The collection of potato varieties as a reserve of source material for breeding for high yield, earliness, and resistance to diseases and pests. Proceed. Appl. Bot. Genet. & Breed. 181, 50e56 (in Russian). Lavrinenko, Y., Balashova, G., 2015. Growing of improved potato source material in primary seeding nurseries under irrigation in southern Ukraine. Agrobiology 2, 13e18. Lavrinenko, Y.A., Vlaschuk, A.N., Shapar, L.V., 2016. Water consumption by different varieties of winter canola planted at different times and densities in southern Ukraine. Improving Effic. Irrig. Agri. 63, 83e89 (in Russian).

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Loshakova, N., November 30, 2020. Potato imports to Ukraine increased four-fold: why we no longer grow “the second bread.” Delo. https://delo.ua/ business/proizvoditeli-kartofelja-na-grani-bankrotstva-ch-375540/. (Accessed 16 April 2021) (in Russian). Lenivko, S.M., Boiko, V.I., 2019. Biotechnological approaches to reduce biogenic risks in crop production: potato case. RUDN J. Agron. & Anim. Ind. 14, 403e422 (in Russian). Lutsenko, A.N., 2013. Optimization conditions for growing food potatoes in the conditions of irrigation of the northern steppe of Ukraine. In: Proceedings of the International Scientific-Practical Conference Dedicated to the 70th Anniversary of Victory in Stalingrad Battle, Integration of Science and Production - a Strategy for Sustainable Development of Agriculture of Russia in the WTO. Volgograd, January 30eFebruary 01, 2013, 21e25 (in Russian). Medvedeva, A., 2019. Market research on seed potatoes in Russia: import substitution is spinning its wheels. Agro-Ind. Portal Agro XXI. https://www. agroxxi.ru/analiz-rynka-selskohozjaistvennyh-tovarov/issledovanie-rynka-semennogo-kartofelja-importozameschenie-probuksovyvaet.html. (Accessed 11 April 2021) (in Russian). Melnichuk, F.S., Alekseeva, S.A., Hordiienko, O.V., 2019. Protection of potato crops against pests. Land Reclam. & Water Manag. 1, 99e107 (in Ukrainian). Melnyk, S.I., Kovchi, À.L., Stefkivska, Y.L., Kravchuk, Î.Î., Horytska, T.V., 2017. Potato market in Ukraine. Plant Variet. Study & Protect. 13, 206e210 (in Ukrainian). Minchenko, N., Kilchevskii, A., Dromashko, S., Makeeva, E., 2013. Cartagena protocol on biosafety in Belarus. Sci. Innov. 128, 70e72 (in Russian). Michkovskaya, N., August 13, 2019. Potato Crisis is Getting Close. KP in Ukraine. https://kp.ua/economics/644332-kartofelnyi-kryzys-uzhe-blyzko#comments. (Accessed 16 April 2021) (in Russian). Ministry of Agriculture and Food of the Republic of Belarus (MAFRB), 2010. List of pests, plant diseases, and weeds that are quarantine objects. In: Annex to Resolution No. 84 dated November 19, 2010. https://ggiskzr.by/doc/quarantine/List_Belarus.do. (Accessed 15 September 2020) (in Russian). Ministry of Agriculture and Food of the Republic of Belarus (MAFRB), 2016. List of Pests, Diseases of Plants and Weeds that are Quarantine Objects Used to Control Quarantine Phytosanitary Measures are Being Carried Out. The amendment to the resolution from 28.12.2016. https://ggiskzr.by/doc/ quarantine/List_Belarus.doc. (Accessed 15 September 2020) (in Russian). Ministry of Agriculture of the Russian Federation (MARF), 2020a. State catalog of pesticides and other agrochemicals. Part I. Pesticides. Insecticides and acaricides. Nematocides 136 (in Russian). Ministry of Agriculture of the Russian Federation (MARF), 2020b. State Register for Selection Achievements Admitted for Usage (National List), vol. 1. Plant varieties, p. 680 (in Russian). Orlov, V.N., Zelenskaya, O.M., 2017. Click beetles in agricultural ecosystems of south-eastern European Russia. Plant Protect. News 3, 60e62 (in Russian). Pavlyushin, V.A., Sukhoruchenko, G.I., Fasulati, S.R., Vilkova, N.A., 2009. Colorado potato beetle: spread, ecological plasticity, harmfulness, and control methods. Plant Protect. & Quarant. 2009 (3), 69e100 (in Russian). Piskun, A.V., Khvalei, O.A., Yablonskaya, S.A., 2020. Plant Protection Pesticides and Fertilizers Permitted for Use in the Republic of Belarus. Promkompleks, Minsk, p. 742 (in Russian). Podgayetsky, A.A., 2012. Interspecies crosses in potato breeding in Ukraine. Vavilov J. Genet. & Breed. 16, 471e479 (in Russian). Popov, A.A., Yahyaev, M.A., 2003. Agricultural Industrial Sector in Russia: Problems and Solutions. Economica, Moscow, p. 409 (in Russian). Privalov, F.I., Soroka, S.V., Sorochinsky, L.V., 2008. Plant protection in Belarus: today and tomorrow. Plant Protect. News 2, 6e9 (in Russian). Rethman, S.V., Tkalenko, A.N., Shita, O.V., 2018. Biological method of plant protection in Ukraine. Plant Protect. News 11, 9e11 (in Russian). Roslavtseva, S.A., 2009. Insecticide resistance in Colorado potato beetle populations. Agrochemistry 1, 87e92 (in Russian). RosStat, 2019. Agriculture in Russia. https://rosstat.gov.ru/folder/210/document/13226. (Accessed 4 September 2021) (in Russian). Simakov, E.A., 2015. Current progress in potato breeding based on private-public partnerships. In: Proceedings of the Conference “Potato Farming: History and Science.” Kraskovo, October 5e6, 2015, pp. 15e24 (in Russian). Simakov, E.A., 2018. Russian-selected Potato Varieties. VNIIKH Publisher, Moscow, p. 120 (in Russian). Shakin, A., 2017. Potato Processing: Products, Markets, and Prospects. Fruit News. https://fruitnews.ru/lenta-novostej/point-of-view/pererabotkakartofelya-produkty-rynki-sbyta-perspektivy.html. (Accessed 11 April 2021) (in Russian). Sobko, O.А., Matsishina, N.V., Fisenko, P.V., Kim, I.V., Didora, A.S., Boginskay, N.G., Volkov, D.I., 2021. Viruses in the agrobiocenoses of the potato fields. IOP Conf. Ser. Earth Environ. Sci. 677 (2021), 052093. Sokol, S.V., Fitsuro, D.D., Pischenko, l.I., Nazarov, V.N., 2016. Comparative productivity and quality of potato grown in accordance with ecologically based technologies in Minsk region. Proceed. Nat. Acad. Sci. Belarus Agric. Sci. Series 1, 53e59 (in Russian). State Register of Varieties, 2019. http://sorttest.by/gosudarstvennyy_reyestr_2019.pdf. (Accessed 15 September 2020) (in Russian). Stetsky, V.A., Shostak, A.V., 2010. Peculiarities of potato production technology in farms and peasant farms in Ukraine. In: Intellectual Potential of the XXI Century: Stages of Knowledge, vol. 4 (1). https://cyberleninka.ru/article/n/osobennosti-tehnologii-vyraschivaniya-kartofelya-v-fermerskih-ikrestyanskih-hozyaystvah-ukrainy. (Accessed 10 August 2020) (in Russian). Sukhoruchenko, G.I., Vasilyeva, T.I., Ivanova, G.P., 2017. Development of insecticide resistance in populations of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera, Chrysomelidae), in different areas of European Russia. Plant Protect. & Quarant. 8, 3e8 (in Russian). Sukhoruchenko, G.I., Ivanova, G.P., Volgarev, S.A., Berim, M.N., 2019. Species composition of aphids (Hemiptera: Aphididae) on seed potato plantings in Northwest Russia. Entomol. Rev. 99, 1e12.

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Sukhoruchenko, G.I., Ivanova, G.P., Volgarev, S.A., Zenkevich, S.V., Dolzhenko, O.V., et al., 2011. System of Integrated Protection of Tablestock and Processing Potatoes against Their Pest Complex in Northwestern Russian Federation. VIZR Publishing, St Petersburg-Pushkin, p. 43 (in Russian). Sukhoruchenko, G.I., Ivanova, G.P., Volgarev, S.A., Vilkova, N.A., Fasulati, S.R., et al., 2016. System of Integrated Protection of Seed Potatoes against Their Pest Complex in Northwestern Russian Federation. VIZR Publishing, St Petersburg-Pushkin, p. 64 (in Russian). Tymko, L.V., Furdyha, M.M., Vermenko, Y.Y., 2018. Adaptive capacity of different potato varieties under the conditions of the Right-Bank Polissia of Ukraine. Plant Variet. Study. & Protect. 14 (2), 224e229 (in Ukrainian). Torsky, E., 2020. Farmer, Take Notice: GMO in Crops May Lead to Criminal Liability. Business Slavyansk. https://slavdelo.dn.ua/2020/10/06/fermeruna-zametku-selhozkultury-s-gmo-zapreshheny-ispolzovanie-vlechet-otvetstvennost/. (Accessed 11 April 2021) (in Ukrainian). Uhatova, J.V., 2018. International scientific and practical conference state, problems and prospects of potato growing in the XXI century (90 years of scientific potato growing in Belarus). Works Appl. Bot. Genet. & Breed. 179 (3), 301 (in Russian). Vashchischin, O.A., 2016. Colorado beetle in the Western forest-steppe of Ukraine. Foothill & Mount. Farm. & Anim. Husband. 59, 1e8 (in Ukrainian). Voitsekhovsky, V.I., Slobodyanik, G.Y., Rebezov, M.B., Smetanskaya, I.N., 2017. Evaluation of promising potato varieties. Techn. Technol. Eng. 2, 90e92 (in Russian). (Accessed 16 January 2020). Volgarev, S.A., 2003. Wireworms damaging potatoes in Leningradskaya oblast and effective insecticides for their control. Plant Protect. News 2, 64e67 (in Russian). Vorobyova, N.V., Ulyanich, E.I., 2014. Assessment of Grades of Early Potatoes in the Forest-Steppe of Ukraine. http://doc.knigi-x.ru/22selskohozyaistvo/ 120111-1-udk-63521-6315547746-ocenka-sortov-kartofelya-rannespelogo-lesostepi-ukraini-vorobeva.php. (Accessed 4 August 2020) (in Russian). Vygovskaya, T.V., 2016. Environmental problems of handling pesticides and agrochemicals in Khmelnytskyi region. In: Proceedings of the Conference on Foundations of Spiritual and Molecular-Genetic Improvement of Human Health and Environmental Protection. London, October 03-07, 2016, pp. 72e75. Yusupov, T.M., 2006. Factors Responsible for Potato Tolerance to Potato Tuberworm (Phthorimaea Operculella Zell.). Ph.D. Dissertation. VIZR, Saint Petersburg (in Russian). Yuzhaninova, L., 2019. Potato in Russia: from import to self-sufficiency. In: Agro-Industrial Portal AgroXXI. https://www.agroxxi.ru/gazeta-zaschitarastenii/zrast/kartofel-v-rossii-ot-importa-do-samoobespechenija.html. (Accessed 11 April 2021) (in Russian). Zamalieva, F.F., 2013. Suppression of viral diseases of potato. Plant Protect. & Quarant. 3, 17e21 (in Russian). Zeiruk, V.N., Belyakova, N.A., Delov, G.L., Casilyeva, S.V., Derevyagina, M.K., Mitina, G.V., 2017. Biological control of virus vectors on seed potatoes grown from tissue culture in greenhouses. Potato Protect. 4, 3-1 (in Russian).

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Chapter 20

China and Central Asia Wenwu Zhoua, Asim Munawara, Runzhi Zhangb and Yulin Gaoc, d a

Institute of Insect Sciences, Zhejiang University, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Key Laboratory

of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Hangzhou, China; bInstitute of Zoology, Chinese Academy of Sciences, Beijing, China; cState Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Science, Beijing, China; dNational Center of Excellence for Tuber and Root Crops Research, Chinese Academy of Agricultural Science, Beijing, China

20.1 Potato production in China and Central Asia 20.1.1 China The earliest introduction of potato into China on record can date back to the mid-17th Century. In the early days of its production, potato was planted in Beijing, the capital city of Ming dynasty. It was mainly grown for the feudal nobles during that time and recognized as a great delicacy. Later, with the improvement of cultivation technologies, the production of potato continuously increased. As a result, potato became more and more popular among the general population and started its spread across the northern China. By the mid-18th century, this crop has been widely planted and consumed by the Chinese. Together with the introduction and cultivation of maize and sweet potato in China, adoption of potato promoted the doubling of the country’s population (Zhai, 2001). Potato harvests in China kept growing since its introduction and achieved w9-fold increase from 10 million tons in the early 1960s to 90.3 million tons in the late 2010s. Currently, the potato produced in China accounts for 24.5% of global production, while its yield in China (18.8 tons/ha) is less than the world’s average level (20.7 tons/ha) and far below that in the USA, Netherlands, France, and other developed countries (Gao et al., 2019). Potato is currently planted all over China, and its cultivation area can be divided into four parts: the northern region producing one crop in summer; the central plain region, where it produces two crops in spring and autumn; the southwestern region where it is cultivated year-round and the number of crops depends on management decisions by growers; and the southern region where it produces one crop in winter (Ma et al., 2020). As a result, potato can be harvested nationwide in China throughout the year. In general, potatoes are cultivated on large farms in the north, managed by family farmers, agricultural cooperatives, and private companies; and on small farms in the south, managed by smallholder farmers. As a result, the level of mechanization and management of potato cultivation is more highly developed in the north than in the south (Gao et al., 2019). Moreover, due to the well mechanized seed potato breeding, the seed potatoes used in China mainly come from Gansu province in north China. Currently, the total area under potato production in China is more than 4.8 million ha, and it is expected to double in the near future (Gao et al., 2019). China is the third largest potato exporter in the world, with about 0.48 million tons sold abroad in 2018 (Gao et al., 2019). The potato exported from China goes to Brunei, North Korea, Indonesia, Japan, Malaysia, Mongolia, Philippines, Russia, Singapore, Sri Lanka, Thailand, United Arab Emirates, Vietnam, and a number of other destinations. In 2016, China’s Ministry of Agriculture and Rural Affairs announced that potatoes would join wheat, rice, and corn as an officially designated major staple crop. It also set the target that about 50% of the annual production would be for domestic consumption.

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00018-4 Copyright © 2022 Elsevier Inc. All rights reserved.

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20.1.2 Central Asia Central Asia is comprised of the former Soviet republics: Uzbekistan, Kazakhstan, Kyrgyzstan, Tajikistan, and Turkmenistan. Apart from grain crops, potato is a major food and cash crop, especially in the highlands, but to some degree also in lowland agricultural systems in this region. It is among the most cost-effective diversified crops, with an important potential to contribute to poverty reduction. In this region, potatoes are usually grown by smallholder farmers, often belonging to disadvantaged socioeconomic groups (Carli, 2008; Gupta et al., 2009). Potato’s contribution to ensuring food security and economic development is discussed in more detail in Chapter 1. The total production of potato in central Asia countries was about 9.42 million tons in 2018. Among the five central Asia countries, Kazakhstan had the highest production of 3.8 million tons in 2018, whereas Uzbekistan had the highest yield of 30 tons/ha in 2018. Potato yield in the remaining four countries is similar to that in China, which is about 40%e50% of the developed countries such as the USA, Canada, and France. To meet the demand of consumption of fresh potatoes, these countries also import them from the neighboring countries such as China, Russia, and Belarus (see Chapter 19 for more information on potato production in that region). With a growing population in the five Central Asian countries, many policies have been established by their governments to promote potato production. Uzbekistan proposed to implement a set of strategies to boost up potato production by 35%, aiming to increase its total harvest to 3.6 million tons annually. Meanwhile, a potato research institute cofounded by Kazakhstan and China has been opened in northwest China with a mandate to develop high-quality potato cultivars that are well suitable for different local environmental conditions, and to cooperate in developing potato processing and cultivation technologies. In Tajikistan, many national and international organizations are carrying out research on increasing productivity, competitiveness, and stability of potato farming (https://cipotato.org/). In Turkmenistan, the government has declared its commitment to boosting the potatoes industry on a scientific basis, including expanding the area allocated for potatoes production, and supporting all categories of potato farms (https:// menafn.com). It is thus predictable that potato production will continuously grow in the central Asia countries in the near future.

20.2 Abundance, the relative importance of potato pests in China and Central Asia 20.2.1 China The insect pest problem is becoming more and more serious in potato fields in China, due to the factors like climate change, the expansion of planting area, intensive agricultural strategies, and insecticide resistance. Insect pests are causing a considerable damage on more than 2.6 million ha (47% potato planting area). Among the insect pests attacking potatoes in China, the green peach aphid Myzus persicae (Sulzer) and the ladybird Henosepilachna vigintioctomaculata (Motschulsky) are the most destructive above ground pests; and grubworms Amphimallon solstitialis (L.) and Holotrichia oblita (Falderman), cutworms Agrotis spp., wireworms Pleonomus canaliculatus (Falderman) and Agriotes subrittatus (Motschulsky), and mole crickets Gryllotalpa spp., are the most destructive below ground ones. In addition, many other pests, including the potato tuber moth Phthorimaea operculella (Zeller) (PTM), the Colorado potato beetle Leptinotarsa decemlineata (Say), the tomato leaf miner Tuta absoluta (Meyrick) are increasing in importance in the recent years (Ma et al., 2020, See Fig. 20.1). The green peach aphids are found in most potato fields in China. They produce regular outbreaks in the northern, central plain, and southwestern potato-growing regions in the provinces Gansu, Ninxia, Hebei, Guizhou, Shandong, Yunnan, and Sichuan. The total damage area for this pest is about 0.61 million ha, which is about 23.3% of the total potato area seriously damaged by insect pests in China. Green peach aphids affect potato plants by direct feeding or indirectly through transmitting Potato virus Y and Potato leaf roll virus (see Chapter 5 for more information). The yield loss caused by this insect pest in China exceeds 15,000 tons per year (Gao et al., 2019; Ma et al., 2020). Potato ladybird is usually a problem in the northern and central plain potato-growing regions in the provinces Shanxi, Shaanxi, Liaoning, Hebei, Gansu, and Ningxia. The total affected area is about 0.46 million ha, which is about 17.8% of the total potato area seriously affected by insect pests in China. In some areas, 30%e60% of the potato plants are routinely damaged by this insect, and sometimes 80%e100% plants are damaged, with the pest density of 0.5e7 insects per plant (Gao et al., 2019; Ma et al., 2020). The below ground potato pests, such as grubworms A. solstitialis and H. oblita, cutworms Agrotis spp., wireworms P. canaliculatus and A. subrittatus, and mole crickets Gryllotalpa spp. are also mostly present in the northern and central

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FIG. 20.1 Occurrence areas of major potato pests in four potato-producing regions in China during 2008e17. Data from Ma, Z.Z., Ren, B.Y., Zhao, Z.H., Li, C.G., Shen, J., Yan, S., 2020. Comparative analysis of the occurrence and control of pests and diseases in four major potato producing areas in China in recent years. J. Plant Prot. 47, 463e470.

plain regions in the provinces Gansu, Inner Mongolia, Shandong, Shaanxi, Shanxi, and Hebei. The total affected area is about 1.05 million ha, which is about 40.4% of the total potato area seriously affected by insect pests in China (Gao et al., 2019; Ma et al., 2020). Invasive pests have become increasingly prominent as a result of the globalization. The Colorado potato beetle is an important quarantine invasive pest that harms potatoes worldwide. This species invaded the northwest China in 1993, and since then it has been spreading across the north part of China at the speed of about 200 km per year. As of now, it has been reported in the provinces Xinjiang, Jilin, and Heilongjiang in north China. Recent findings suggested that multiple introductions may have happened during its invasion into China (Yang et al., 2020). Due to the serious attention paid to this pest by the government and farmers, its effective control has been possible in the past 27 years. As a result, its total distribution in China is limited to 20,200 ha (Wang et al., 2020). Potato tuber moth was first recorded in China in 1937 on tobacco plants. It is now widely distributed in all four potatogrowing regions, encompassing Sichuan, Yunnan, Guizhou, Guangdong, Guangxi, Hunan, Huber, Jiangxi, Anhui, Gansu, Shaanxi, Henan, Shanxi, Jilin, Shandong, Taiwan and some other provinces in China (Yan et al., 2019). Potato tuber moth damage is most serious in Yunnan province in the southwestern potato-growing region, where they have solanaceous host plants (potato, tomato, tobacco, etc.) year-round. In the field, it damages potato plants and causes yield losses up to 20%e30%; in storage, if left without control, it may cause a loss of 100%.

20.2.2 Central Asia Viral and bacterial diseases are considered to be the critical limiting factors in potato production in Central Asia. However, due in large part to global climate change, a significant increase in potato insect pests have been also observed in recent years. The potato tuber moth, potato aphid Macrosiphum euphorbiae (Thomas), green peach aphid, and the Colorado potato beetle are known to be the most important potato pests in Central Asian countries.

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20.2.2.1 Uzbekistan Around 50 insect pest species have been identified on potato crops in Uzbekistan. The pests of economic importance include the Colorado potato beetle, the tomato russet mite Aculops lycopersici (Tryon), the turnip moth Agrotis segetum (Denis and Schiffermuller), and several aphid species including Aphis fabae (Scopoli), Aulacorthum solani Kaltenbach, M. persicae, Aphis gossypi (Glover), and M. euphorbiae. In addition, the potato tuber moth and the tomato leafminer are also gaining significance in recent years (Carli and Baltaev, 2008). The Colorado potato beetle is the major pest of potato plants causing extensive defoliation of potato in Uzbekistan. This pest was first observed in Tashkent region of Uzbekistan in 1972. It may cause yield loss up to 40%e50% in severe cases, and sometimes may completely destroy potato plants. Aphid species which transmit diseases to potato plants are also becoming key pest species of potato crops in Uzbekistan (Zokirov et al., 2020; Khujamshukurov, 2016).

20.2.2.2 Kazakhstan The Colorado potato beetle and the cutworm A. segetum are the key potato pests in Kazakhstan. In some areas, A. segetum caused 50% loss in 2005% and 70% loss in 2007 (Toleubayev et al., 2011). There are also other economically important potato insect pests such as A. fabae, Aphis nasturtii (Kaltenbach), and M. persicae, but they are not considered key pests in this country (Karpova et al., 2019; Toleubayev et al., 2011).

20.2.2.3 Kyrgyzstan The most abundant potato pest is the Colorado potato beetle, and some cutworms have been reported occasionally. Several aphid species, in particular M. persicae and M. euphorbiae, and whitefly species have also been reported. However, they do not have economic importance (Konurova et al., 2016).

20.2.2.4 Tajikistan and Turkmenistan The Colorado potato beetle is the most important and destructive insect pest found in potato fields of both countries. The other pests such as aphids, whiteflies, the cutworm A. segetum, the potato tuber moth, nematodes, and spider mites are reported to cause infestation occasionally (Central Asia IPM CRSP, 2007; http://crsps.net/; https://cipotato.org; www.cabi. org). Potato yield losses in these two countries are increasing in recent years, reaching 23%e29% and up to 50% in severe cases. The Colorado potato beetle alone caused 19%e45% yield reductions in Tajikistan, depending upon potato variety and year (http://www.fao.org; http://mfc.org.pl; www.sard3tm.org).

20.3 Management practices of key potato pests in China and Central Asia 20.3.1 China Since potato has been planted in China for a long time, farmers have adopted many strategies for the control of its insect pests. The management practices vary among different regions in China due to the diversity of agricultural environments and the complexity of pest problems. Pest management practices are generally better developed in the northern than in the southern part of the country. In the north, potato fields are normally located in large plain areas and belong to large crop growers, including agricultural cooperatives and corporations. These growers are commonly well educated and equipped, especially in the modern pest control technologies. Potato production is also well mechanized in this region. As a result, the average yield in the north part of China could reach 30 tons/ha. In the southern part of China, many small potato fields are located in relatively remote mountain areas and are managed by smallholders. Potato cultivation in this region usually involves a considerable amount of manual labor, and pest management knowledge and technology remain to be improved. As a result, the average yield in the southern part of China could be lower than 15 tons per ha (Gao et al., 2019). Chemical control has been widely adopted by farmers in China, and it plays an important role in protecting the potato yield. In general, potato fields in the northern part of China receive a lot of insecticides. The overuse of insecticides (sometimes w30 applications per growing season) frequently occurs because their cost is greatly reduced by the economy of scale typical for industrial pest management practices. On the contrary, potato fields in the southern part of China receive less insecticides, owing to their higher relative cost in small-scale agriculture. The overuse of insecticides has brought about insecticide resistance and many other environmental problems in China. Exploring and developing “green ways” of pest management have gained more and more attention in the recent years. Resources have been invested into the development and application of sustainable and ecological strategies of pest management in potato fields, supported both by the central government and the local governments. As a result, insecticide

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applications have been more and more scientifically based and standardized, and many “green” pest control solutions, including biological control with natural enemies and biopesticides, have been widely applied for the management of potato insect pests in China.

20.3.1.1 Aphids Chemical control is the most widely used approach for suppressing aphids on potato plants. The commonly used insecticides are avermectin, beta cyhalothrin, clofluthrin, imidacloprid, thiamethoxam, and chlorfenapyr. To achieve optimal control, the aphids should be suppressed by insecticides before their migration from the alternative hosts into the potato fields. The yellow sticky traps are widely used for monitoring aphid populations in the fields and greenhouses. On a small scale, such as production of nuclear seed potatoes in greenhouses, aphids can be even suppressed by these traps. If left in the field, however, used sticky traps may become environmental contaminants. Adult aphids can be repelled when potato plants are protected by silver plastic mulch on the ground or floating row covers.

20.3.1.2 Ladybirds Chemical control is the most widely used approach for suppressing these pests. Fenvalerate, malathion, deltamethrin, cypermethrin, phoxim, cyhalothrin, applied alone or in mixtures with each other, are the commonly used pesticides in China. To achieve optimal control, overwintered adults and the newly hatched first generation larvae should be targeted. The efficiency of chemical control may exceed 90% (Li et al., 2001; Dong et al., 2007; Sun, 2008). On a smaller scale, ladybirds can be manually controlled by destroying overwintered adults or egg masses. Installing mesh web in the field could also prevent adults from colonizing potato plants. Moreover, light traps could attract and kill adults, although they may also kill many natural enemies and neutral insects in the field. Biological pesticides, including the entomopathogen Bacillus thuringiensis (Berliner) and plant defensive secondary metabolites also have been used in China for the management of ladybirds. The efficiency of B. thuringiensis is higher for the control of the first and second instar larvae than for the other developmental stages.

20.3.1.3 Below ground insect pests Chemical control is also the most widely used approach for suppressing these pests. Phoxim, quinalphos, rogor, and dipterex are used by farmers for their control. Phoxim or imidacloprid could be used to protect seed tubers. Foliar and soil sprays with insecticides (lambda-cyhalothrin and chlorfluazuron) are effective for the control of early instars, while trap plants (the paulownia Paulownia fortunei (Seem.) or lettuce Lactuca sativa L.) treated with insecticides (trichlorfon) could be used for the control of later instars (Xu et al., 2013). Moreover, baits made by mixing insecticides with sugar, vinegar and wine could also be used in the control of below ground pests, while some of them are not well cost-effective. Sanitation is helpful for reducing the populations of below ground insect pests. For instance, solanaceous weeds or volunteer plants in the field could be removed before the cropping season and after the harvesting to reduce the early instars and the adults, respectively. Moreover, light traps could attract and kill the adults (Chen et al., 2003). Deep plowing could reduce the pest populations. Biological pesticides, such as the entomopathogen B. thuringiensis, could also be used for the management of the below ground insect pests.

20.3.1.4 Potato tuber moth Sex pheromone-based traps have been successfully developed and widely applied in the monitoring potato tuber moths in China. Chemical control is commonly used in the control of this pest. The insecticides used include cymperator, cypermethrin, abamectin, chlorophos, malathion, dimethoate, and fenvalerate. Since potato tuber moth also causes serious problem in storage, warehouses are usually fumigated with methyl bromide, and the tubers are usually treated with chlorophos or phoxin before the storage (Yan et al., 2019) (Fig. 20.2). A, Products of sex pheromone lure for potato tuber moth. B, Application of sex pheromone lure for the management of potato tuber moth in fields in Yunnan province, China. C, Potato tuber moth pupae infected by the entomopathogenic fungus Beauveria bassiana (Fig.20.2). Intercropping between tobacco and potato, or between tomato and potato, should be avoided because potato tuber moth damage frequently happens in the southwestern region where these crops are grown together on mixed farms. Planting seed tubers as deeply as possible and hilling at least three times during the growing season could reduce the oviposition of adult moths. Tubers should not be kept in the field overnight after harvest, and cull tubers should be disposed to avoid the

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FIG. 20.2 Developing and application of sex-pheromone traps and entomopathogenic fungus in China.

oviposition by adult moths. Moreover, intercropping potato with maize can also reduce the population of aphids in the field, possibly because natural enemies are promoted by this cropping strategy (Zheng et al., 2020). Biological pesticides, including B. thuringiensis and the entomopathogenic nematodes Steinernema carpocapsae (Weiser) could be used to kill potato tuber moth larvae in the field.

20.3.1.5 Colorado potato beetle Since the first discovery of Colorado potato beetles in 1993, China has become the frontier for its spread. Policies have been established and strategies have been developed for the strict control of this pest since then. As a result, the CPB has been effectively controlled, and for a long time its occurrence has been limited to Xinjiang-Uighur Autonomous District. Unfortunately, new invasion points have recently emerged in other provinces in northeast China. However, based on genetic analysis those beetles most likely invaded from Russia rather than from Xinjiang. Several management practices have been used for this quarantine pest. For instance, potential geographical distribution analysis was conducted to select the monitoring areas. Subsequently, the best monitoring methods, including manual inspection, erial vehicles, light trap monitoring, lure trapping (a mixture of Methyl phenylacetate, b-Caryophyllene, and 2-Phenylethanol) were determined. After that, based on the occurrence, dispersal, and interception of the beetles, strict quarantine measures were imposed. For instance, the movement of potato tubers and plants from beetle-invaded areas to beetle-free areas is strictly prohibited (Wang et al., 2020). Chemical control of Colorado potato beetles is widely used, even though this species rapidly develops insecticide resistance. Fipronil and acetamiprid insecticides are effective for the control of this pest. Crop rotation with land plowing in autumn and irrigation in winter, and removing wild solanaceous plants, is helpful for reducing the numbers overwintering beetles. Light traps can also be used in the control of this species. The blue lamps are designed to emit light at the untraviolet wavelength, and they can mass-trap both sexes of the flying insects and substantially reduce the pests. In addition, the management of Colorado potato beetles also depends on the stage of potato growth. In the early and middle stages of potato growth, the beetles are killed, whereas host plants should not be destroyed. In the late stages of potato growth after tuber bulking is complete, the beetles can be destroyed together with the damaged potato plants and the adjacent vegetation (Zhang et al., 2012).

20.3.2 Central Asia Potato is also not a native crop in Central Asian countries. After the introduction of potato into this region, its importance kept growing, especially during the last several decades. As insect pressure also grew, it became more and more challenging for farmers to further increase potato production in the region and to secure the food supply necessary to feed rapidly growing population. As a result, there is a pressing need to enhance research activities to improve pest control in this region.

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Potato pests are currently being controlled by extensive use of chemicals in monoculture cropping systems. In order to reduce this unsustainable practice, different organizations such as International Potato Center (CIP), Food and Agriculture Organization of the United Nations (FAOs), The International Center for Agricultural Research in Dry Areas (ICARDAs), Michigan State University (MSU) and The University of California (UC Davis) have implemented regionally based Integrated Pest Management (IPM) Programs in the region since 2005. Those included training farmers and other agricultural professionals in ecologically based IPM tactics. Therefore, there is a reason to believe that chemical-centered approach to pest control will be gradually replaced by more integrated and environmentally friendly techniques.

20.3.2.1 Uzbekistan From the past decades, the chemical applications for potato pest control are declining; however, chemicals are still widespread. Insecticides such as fipronil, beta cyfluthrin, pyriproxyfen, and chlorpyrifos are being applied for potato pest control, especially for the Colorado potato beetle. There are also locally developed formulations of biopesticides, such as Antibac Uz (Bacillus thuringiensis), that allow reducing chemical applications (Kuo et al., 2005). Potato cropping area under biological control programs is expanding in the region. The egg parasitoid Trichogramma evanescens (Westwood) have been extensively used in biological control of potato pests and has been applied on more than three million ha in Uzbekistan. A large network of biological laboratories and insectaries has been established, with certified entomological facilities distributed throughout the country (Asia IPM, CRSP Program, 2007; www.cacilm.org). However, similar to other areas of the world, biocontrol of the Colorado potato beetle has remained a major challenge. Manipulation of landscape ecology and habitat management to enhance biocontrol of potato insect pests is growing steadily in Uzbekistan. Considerable research effort has been invested into identification, screening, and field testing of native plants that could be integrated into cropping systems to replace monocultures. The attractiveness of native plants to natural enemies of potato pests was also evaluated. Higher plant diversity resulted in higher biodiversity of predators and pollinators (Christmann et al., 2017). Currently, potato growers in the region are moving toward IPM based pest control technologies. They were found to be keenly interested in embracing and in learning new innovative technologies to reduce chemicals residues levels and to improve their potato production. Meanwhile, there is a considerable breeding effort to develop new potato varieties which are resistant to insect pests and adapted to local conditions (Central Asia IPM Project; www.canr.msu.edu/ipm).

20.3.2.2 Kazakhstan Many farmers in Kazakhstan consider pesticides as the only option to control pests, and they are commonly unaware of the harmful impacts of indiscriminate and judicious use of pesticides. During the past decades, farmers mostly used pesticides belonging to the pyrethroid group for the control of potato pests. The insect pests have developed resistance against these types of pesticide and forced farmers to use fipronil. To diversify their management approaches, farmers need the information regarding specifics of potato crop protection and the importance of approaching a field as an agroecosystem (Toleubayev et al., 2011; http://moa.gov.kz). The biocontrol of potato pests in Kazakhstan is still secondary to the chemical control; however, from the beginning of 1970s and onwards it has been showing considerable improvements. There are more than 1500 small insectaries involved in the rearing of Trichogramma spp. These wasp species parasitize w86% of the eggs of A. segetum and other pest species. Farmers also use biopesticides based on fungi (Beauveria bassiana), bacteria (Bacillus thuringiensis) and viruses (e.g., Virin-X) which estimated to kill 85% of targeted pest populations. For the control of aphid species, the parasitoid Cicloneda limbifer is widely used (Broka et al., 2016; Toleubayev et al., 2011). There is also a considerable effort toward developing local varieties of potatoes resistant to pests (Krasavin, 2009).

20.3.2.3 Kyrgyzstan The Kyrgyzstan farmers heavily rely on chemicals applications for the control of potatoes pests. They are normally not familiar with the safe use of permitted chemical pesticides. The farmers also lack information or awareness about alternative pest management strategies such as biological control or cultural control as well as the use of pest-resistant varieties. Similar to other countries in the region, the biocontrol strategies for the control of potato pests steadily growing in Kyrgyzstan. However, these practices are still not sufficient to solve the problems caused by insect pests. Several biocontrol facilities have been established with the support of national and international organizations. They are producing many beneficial organisms, including green lacewings and Trichogramma spp.(www.canr.msu.edu/ipm/central-asi).

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The ecologically based pest management strategies are emerging in Kyrgyzstan. The country has diverse and complicated landscape containing rich biodiversity of potential natural enemies and sources of biopesticides. More than 50 native flowering plants have been evaluated for this purpose, with some showing promise to suppress pest populations. Yellow sticky traps are used in the fields to monitor pest populations and to assist in pest control decisions. Mulching is applied to control cutworms and pest infected plants pulled out to avoid further infestations (http://www.cac-program.org; Abdulhamidov et al., 2015). Local researchers are also collaborating with international potato breeders to develop pest-resistant varieties. As a result, the pesticides use has been reduced while the local farmers started to rely more on IPM based tactics for the control of potato pests.

20.3.2.4 Tajikistan and Turkmenistan During the past decades, the pesticides were the most powerful tool used for the control of potato pests. However, for the past few years, a significant reduction of pesticide applications was observed due to their high costs. Farmers spend around 20% of their total input costs on buying pesticides. Upon pest infestations, local farmers look at nearby markets to buy chemicals and then spray them, often without reading application instructions. Knowledge of alternative control strategies is still inadequate (IPM CRSP, 2007; www.fao.org; https://moa.tj). The control of potato pests by releasing natural enemies is growing steadily in the two countries. Several insectaries produce beneficial insects such as Trichogramma sp., Bracon hebetor Say, and Chrysopa carnea Steph. During the year of 2006, beneficial insects were released on more than 130,000 ha of land in Tajikistan. In addition, Tajikistan is inhabited by more than 4500 plant species that either have insecticidal properties or attract natural enemies (IPM CRSP, 2007). These have potential to be integrated in the future IPM programs. There is little information about bio-based pest control strategies in Turkmenistan; however, many naturally occurring organisms, especially braconid wasps, have been reported very efficient for several lepidopterous pests. Also, government of Turkmenistan has purchased pest control agents from foreign companies to reduce pesticide use in the region (Saidov, 2000; Tobias and Saidov, 1992; http://tdh.govt.tm; http://www.fao.org; www.cbd.int).

20.4 Conclusions Potato is an increasingly important crop in China and Central Asia, with both public and private sector putting considerable effort in increasing its production. However, average yields in this region are considerably lower than in developed countries and can likely be improved by adopting new technologies. Insect pests are an important factor negatively affecting potato farming. Their control is largely dependent on chemical insecticides, but there is also a considerable progress in developing alternatives and adopting integrated approaches to pest management.

References Broka, S., Giertz, Å., Christensen, G., Rasmussen, D., Morgounov, A., Fileccia, T., Rubaiza, R., 2016. Agricultural Sector Risk Assessment Kazakhstan. World Bank Group Report, p. 201. Washington, DC 20433. Carli, C., 2008. Recent Advances in Potato Research and Development in Central Asia and Caucasus. Working Paper. International Potato Center, Lima, Peru. Carli, C., Baltaev, B., 2008. Aphids infesting potato crop in the highlands of Uzbekistan. Potato J. 35, 134e140. Central Asia IPM CRSP Program, 2007. Integrated pest management in Central Asia. In: Proceedings of the Central Asia Region Integrated Pest Management Stakeholders Forum, Dushanbe, Tajikistan, May 27e29. Chen, B., Li, Z.Y., Gui, F.R., Sun, Y.X., Yan, N.S., 2003. Integrated control of potato pest insects in Yunnan province. Yunnan Agric. Sci. Technol. 1, 136e141. Christmann, S., Hassan, A.A., Rajabov, T., Khamraev, A.S., Tsivelikas, A., 2017. Farming with alternative pollinators increases yields and incomes of cucumber and sour cherry. Agron. Sustain. Dev. 37, 24. Dong, F.L., Guo, Z.Q., Ma, G.Y., 2007. Occurrence characteristics and integrated control methods of potato pests and diseases in Guyuan City. Chin. Potato J. 21, 238e239. Gao, Y.L., Xu, J., Liu, N., Zhou, Q., Ding, X.H., Zhan, J.S., Cheng, X.Y., Huang, J., Lu, Y.W., Yang, Y.H., 2019. Current status and management strategies for potato insect pests and diseases in China. Plant Prot. 45, 106e111. Gupta, R., Kienzler, K., Martius, C., Mirzabaev, A., Oweis, T., Pauw, E., Qadir, M., Shideed, K., Sommer, R., Thomas, R., Sayre, K., Carli, C., Saparov, A., Bekenov, M., Sanginov, S., Nepesov, M., Ikramov, R., 2009. Research prospectus: a vision for sustainable land management research in Central Asia. In: ICARDA Central Asia and Caucasus Program. Sustainable Agriculture in Central Asia and the Caucasus Series No.1, CGIAR-PFU, Tashkent, Uzbekistan, p. 84.

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Karpova, O.V., Alexandrova, A.M., Nargilova, R.M., Kryldakov, R.V., Yekaterinskaya, E.M., Romadanova, N.V., Kushnarenko, S.V., Iskakov, B.K., 2019. Diagnosis of potato viruses in Kazakhstan: molecular characterization of isolates. Eurasian J. Appl. Biotechnol. 1, 58e67. Khujamshukurov, N.A., 2016. Efficiency of antibac Uz biopesticide against Colorado potato beetle. ESAIJ 12, 198e201. Konurova, D.S., Levchenko, M.V., Turgunbayev, K.T., Smagulova, S.B., Uspanov, A.M., Lednev, G.R., 2016. Virulence of Kyrgyzstan natural isolates of anamorphic ascomites for larvae of the Colorado potato beetle. Plant Prot. News 3, 85e86. Krasavin, V.F., 2009. Potato Breeding in the Southeast of Kazakhstan Almaty, p. 224 (in Russian). Kuo, C.G., Mavlyanova, R.F., Kalb, T.J., 2005. Increasing marketed oriented vegetables production in Central Asia and the Caucasus through collaborative research and development. In: Workshop proceedings; 25e27 April, Tashkent, Uzbekistan. Li, T.J., Li, Y., Wang, X.H., 2001. Occurrence and control of Henosepilachna vigintioctopunctata (Fabricius) on potato in youyang county. Southwest Chin. J. Agric. Sci. 14, 90e91 (in Chinese). Ma, Z.Z., Ren, B.Y., Zhao, Z.H., Li, C.G., Shen, J., Yan, S., 2020. Comparative analysis of the occurrence and control of pests and diseases in four major potato producing areas in China in recent years. J. Plant Prot. 47, 463e470. Saidov, N.S., 2000. The fauna of Braconid wasps (Hymenoptera, Braconidae) in alfalfa biocenosis in the south of Tajikistan. In: Proceedings of the Second Annual Conference of Young Scientists of Tajikistan. Dushanbe, pp. 169e171. Sun, Y.P., 2008. Current occurrence status and integrated control methods of potato pests and diseases in Yuzhong County. Gansu Sci. Technol. 24, 141e143 (in Chinese). Tobias, V.I., Saidov, N.S., 1992. Effect of wind on daily activity of parasitic Hymenopterous insects (with Braconid wasps as an example) (Hymenoptera: Parasitica: Braconidae). Entomol. Rev. 72, 339e347. Toleubayev, K., Jansen, K., Huis, A.V., 2011. From integrated pest management to indiscriminate pesticide use in Kazakhstan. J. Sustain. Agric. 35, 350e375. Wang, C., Xu, H., Pan, X.B., 2020. Management of Colorado potato beetle in invasive frontier areas. J. Integr. Agric. 19, 360e366. Xu, J., Liu, N., Zhang, R.Z., 2013. Chapter 7 - other pests e China. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Oxford, UK, pp. 193e216. Yan, J.J., Zhang, M.D., Gao, Y.L., 2019. Biology, ecology and integrated management of the potato tuber moth, Phthorimaea operculella (Lepidoptera: gelechiidae). Acta Entomol. Sin. 62, 1469e1482. Yang, F.Y., Guo, J.J., Liu, N., Zhang, R.Z., 2020. Genetic structure of the invasive Colorado potato beetle Leptinotarsa decemlineata populations in China. J. Integr. Agric. 19, 350e359. Zhai, Q.X., 2001. Preliminary exploration of the introduction time of potato in China. Agric. Hist. China 20, 91e92 (in Chinese). Zhang, R., Jiao, X.D., Zu, Y.Z., Jia, J.W., Zhang, Q.F., 2012. Current situation and suggestions of potato beetle epidemic surveillance in Heilongjiang Province. Plant Quarant. 30, 82e84 (in Chinese). Zheng, Y.Q., Zhang, L.M., Chen, B., Yan, N.S., Gui, F.R., Zan, Q.A., Du, G.Z., He, S.Q., Li, Z.Y., Gao, Y.L., Xiao, G.L., 2020. Potato/Maize intercropping reduces infestation of potato tuber moth, Phthorimaea operculella (Zeller) by the enhancement of natural enemies. J. Integr. Agric. 19, 394e405. Zokirov, I.I., Mansurkhodjaeva, M.U., Akhmedova, Z.Y., Khashimova, M.K., Turaeva, Z.R., 2020. Phytophagous insects of vegetable and melon agrocenosis of Central Fergana. IJAEB 5, 64e71.

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Chapter 21

Insect pests of potato in India: biology and management R.S. Chandela, V.K. Chandlab, K.S. Vermaa and Mandeep Pathaniaa a

Department of Entomology, Himachal Pradesh Agriculture University, Palampur, Himachal Pradesh, India; bDivision of Plant Protection, Central

Potato Research Institute, Shimla, Himachal Pradesh, India

21.1 Introduction The potato is the world’s fourth most important food crop after rice, wheat, and maize. During the triennium ending in 2006e07, India was the third largest potato producer (24.61 million tonnes) after China (71.09 mt) and Russia (37.55 mt), and followed by Ukraine. Scientific advances made by Indian scientists have led to higher average potato productivity in India than in those three countries. India produces 7.72% of the world’s potatoes from 7.57% of the total global potatogrowing area, with productivity levels higher than the world’s average (Rana, 2011). In India, potato is cultivated in almost all states under very diverse agroclimatic conditions. On the basis of geographical variability and climatic differences, the potato-growing areas of India have been divided into six zones (Table 21.1). More than 85% of India’s potatoes are grown in the vast Indo-Gangetic plains of north India during short winter days from October to March. The states of Uttar Pradesh, West Bengal, and Bihar account for more than 75% of the potato-growing area in India and for about 80% of total production. Hilly areas, where the crop is grown during the summer from April to September, account for less than 5% of production. In the plateau regions of south-eastern, central, and peninsular India, which constitute about 6% of the potato-growing area, potato is mainly a rain-fed crop or is irrigated as winter crop. In the Nilgiri and Palni hills of Tamil Nadu, the crop is grown year-round under both irrigated and rain-fed conditions. Most potatoes are produced by large-scale commercial farmers (Pandey and Kang, 2003). Insect pests cause variable and complex problems for potato farmers. India has a great diversity of insect pests that attack potato. Some of these insects were transported to new locations with seed tubers; others were already present in locations where potato was introduced and expanded their host ranges to take advantage of the new plant. Because potato crops are vegetatively propagated from tubers, which easily carry some pathogens and pests, many pest problems have followed potatoes to areas where they are grown (Chandel et al., 2007). These pests can damage potato plants by feeding on leaves, reducing the photosynthetic area and efficiency by attacking stems, weakening plants and inhibiting nutrient transport, and by attacking the potato tubers destined for consumption or for use as seed (Chandel and Chandla, 2003). In India, approximately 60 billion rupees (US$1.2 billion) worth of potato tubers are lost annually due to pest damage, which accounts for 10%e20% of total production. The annual demand for pesticides in India is approximately 80,000 tonnes and is likely to increase in coming years. However, productivity trends indicate that heavy application of insecticides will not proportionately increase crop productivity (Misra et al., 2003). Potato is one of the most input-intensive crop and is the heaviest user of chemical pesticides of all major food crops. Pesticide consumption in potato can often reach up to 20% of its cost of production (Anonymous, 1991). The potato pests are grouped into soil pests, foliage feeders, sap feeders, and storage pests. In seed production, the pests of greatest concern are typically aphid vectors of potato viruses, especially Myzus persicae (Sulzer). In ware production, the key pests may be insects which attack tubers, such as tuber moth, white grubs, and cutworms. In some situations, foliage feeders such as noctuid moths and coccinellid beetles are also important.

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.11001-7 Copyright © 2022 Elsevier Inc. All rights reserved.

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TABLE 21.1 Potato-growing zones in India. Zones

States

Crop seasons

North-Western plains

Punjab, Haryana, Rajasthan

SeptembereNovember OctobereJanuary/February JanuaryeApril/May

West-Central plains

Madhya Pradesh, West-Central Uttar Pradesh, North-Western Gujrat

OctobereJanuary/February

North-Eastern plains

Assam, Bihar, Jharkhand, West Bengal, Orissa, Eastern Uttar Pradesh, North-Eastern Madhya Pradesh, Eastern Chattisgarh

NovembereFebruary/March

Plateau region

Maharashtra, Karnataka, parts of Gujrat, Madhya Pradesh, and Orissa

June/JulyeSeptember/October NovembereJanuary/February

North-Western and Central hills

Jammu & Kashmir, Himachal Pradesh, and Uttrakhand

AprileSeptember JanuaryeMay

North-Eastern hills

Meghalaya, Manipur, Mizorum, Tripura, Nagaland, Arunachal Pradesh

JanuaryeMay AugusteDecember

Southern hills

Nilgiri and Palni hills of TamilNadu

AprileSeptember AugusteDecember JanuaryeMay

21.2 Root and tuber-eating pests Soil insect pests pose one of the most difficult problems for potato growers. To a large degree, the difficulty can be attributed to the very persistent nature of these pests, coupled with the fact that new insecticides are less effective in the soil. Moreover, these organisms often go unnoticed for several years, building up their numbers slowly with each successive potato crop. In India, there are many pests which damage potato roots and tubers inside the soil. Those of major concern are cutworms, white grubs, and potato tuber moth. These pests cause significant economic losses, although they rarely cause substantial damage in one field during a single season. Secondary infection from various diseases can follow, further rendering tubers unfit for marketing. Geographic location, soil characterization, and production practices usually favor specific pests. In this chapter the important soil pests are discussed individually, as well as specific management practices that are effective for each pest.

21.2.1 White grubs White grubs (Coleoptera: Scarabaeidae) are most destructive and troublesome soil insects, threatening potato production in hilly states. These soil-dwelling larvae of scarab beetles are present in the soil at a depth of 5e20 cm during the crop season (Chandla, 1985). Being polyphagous both in grub and adult stages, they feed on a wide variety of cultivated and uncultivated plants. After hatching, the young grubs orient themselves toward roots and start feeding (Musthak Ali, 2001). Almost all field crops grown during rainy season e i.e., potato, vegetables, groundnut, sugarcane, maize, pearl millet, sorghum, cowpea, pigeon pea, green grass, cluster bean, soybean, rajmash, upland rice, ginger, etc. are damaged (Mishra, 2001). In potato the damage is only caused by grubs, which feed on rootlets, roots, and tubers. The first-instar grubs can survive on the organic matter present in the soil, but roots are preferred and are fed upon when encountered (Mehta et al., 2010). They often remain unnoticed but may suddenly increase in population in places with enough food and with low disturbance of the soil. The damage to potato is mainly caused by the second and third instars, which make large, shallow, and circular holes in tubers. In cases of heavy infestation, an entire tuber can be transversed by deep tunnels (Fig. 21.1A and B). Tubers infested by the white grubs have poor market value and are sold at a highly reduced price. The white grubs damage the tubers without causing any symptoms on the foliage; thus, farmers remain unaware of the damage done to tubers until harvest. In India, 20 species of white grubs have been reported on potato (Table 21.2). Of these, Brahmina coriacea (Hope), Holotrichia seticollis Moser, Holotrichia longipennis (Blanchard), Anomala dimidiata Hope, and Melolontha indica Hope are most destructive in the north-western hills. Holotrichia serrata (Fab.) damages potato in Karnataka (Misra and Chandel, 2003).

Insect pests of potato in India: biology and management Chapter | 21

FIG. 21.1 Tuber damage by white grubs (A) Brahmina coriacea (B) Melolontha indica.

TABLE 21.2 Different species of white grubs damaging potato in India. Species

Place of occurrence

Reference(s)

1. Brahmina coriacea (Hope)

Himachal Pradesh

Butani and Jotwani (1984) Misra and Chandla (1989) Chandel et al. (1997)

2. B. flavoserica Brenske

Himachal Pradesh

Mehta et al. (2008)

3. Melolontha indica Blanch.

Himachal Pradesh

Bhalla and Pawar (1977)

4. Holotrichia longipennis Blanch.

Himachal Pradesh & Uttranchal

Butani and Jotwani (1984), Haq (1962), Misra and Chandla (1989), Rai and Joshi (1988)

5. Holotrichia repetita Sharp

Karnataka

Veersh et al. (1991)

6. H. rustica Burmeister

Karnataka

Veersh et al. (1991)

7. H. serrata (F.)

Karnataka

Veersh et al. (1991), Butani and Jotwani (1984)

8. H. conferta Sharp

South India

Butani and Jotwani (1984)

9. H. excisa Moser

Tamil Nadu

Regupathy et al. (1997)

10. H. nototiocollis

Tamil Nadu

Regupathy et al. (1997)

11. Holotrichia sp.

North-Eastern India

Anonymous (1989)

12. H. seticollis Moser

Himachal Pradesh & Uttranchal

Chandel et al. (1997) Sushil et al. (2006)

13. Anomala dimidiata Hope

Himachal Pradesh

Misra and Chandla (1989)

14. Anomala polita (Blanch.)

Himachal Pradesh

Misra and Chandla (1989)

15. A. rugosa Arrow

Himachal Pradesh

Misra and Chandla (1989)

16. A. rufiventis Redt.

Uttar Pradesh

Rai and Joshi (1988)

17. Anomala sp.

Karnataka

Lingappa and Giraddi (1995)

18. A. communis Brenske

Tamil Nadu

Regupathy et al. (1997)

19. A. nathani Frey

Tamil Nadu

Regupathy et al. (1997)

Himachal Pradesh

Misra and Chandla (1989)

A. Subfamily: Melolonthinae

B.Subfamily: Rutelinae

C. Subfamily: Dynastinae 20. Phyllognathus dionysius F.

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21.2.1.1 Biology of white grubs Most of the white grubs are similar in shape and color and have fleshy, curved bodies with brown heads and welldeveloped legs which are hardly used for locomotion (Mehta et al., 2010). Adult beetles usually remain unnoticed throughout the year, and their appearance in large numbers occurs just after break in a monsoon. The beetles’ attack on potato persists for a month or two. Most of the beetle’s life cycle is spent in the larval stage underground (Chandel and Kashyap, 1997). The beetles spend the winter in the soil as larvae in hard earthen cells. 21.2.1.1.1 Brahmina coriacea B. coriacea was first reported in India from the Kullu valley of Himachal Pradesh feeding on pear, apple, plum, fig, and grapevine (Beeson, 1941). Sharma et al. (1969) observed B. coriacea adults defoliating peach, plum, apricot, and pear in the mid-hills of Himachal Pradesh. It has become a serious problem in the north-western Himalaya, which comprise Himachal Pradesh, Uttrakhand, and Jammu & Kashmir (Mehta et al., 2010). In the spring, when apples and other fruits have produced leaves, the adults become active, disperse by flight at night, and feed on the foliage of apples and other plants (Chandel and Kashyap, 1997). They leave the soil at dusk and remain on the leaves during night, mating and feeding. Mating normally lasts for 7e11 min. The preoviposition period ranges from 2 to 4 days, with an average of 3.14 days. Mated females under laboratory conditions lay 10e31 eggs, with a mean of 20 eggs per female (Chandel et al., 1995). At the first streaks of dawn the adults return promptly to the soil, where the females lay their pearly white eggs. The eggs are generally laid in grassland or on patches of grassy weeds in cultivated fields. The eggs hatch in 9e12 days, and the young grubs feed on the roots of grasses until they are about 11 mm long. After hatching, the grubs burrow into the soil. There are three distinct larval instars. Larvae are about 5e6 mm long following hatching, and attain a length of about 11.6, 20.7, and 29.9 mm by the end of instars 1, 2, and 3, respectively. The head capsule width is about 1.5, 2.4, and 4.3 mm, respectively. In the mid-hills (650e1800 m), development of the first- and second-instar grubs requires about 14.4 and 20 days (Chandel et al., 1995). In higher hills (1800e2000 m), the first and second instars are completed in 20.1 and 29.6 days, respectively (Chandla et al., 1988). The third-instar grubs (Fig. 21.2) are most active, and have immense capacity for damage. These grubs continue feeding until October and are therefore responsible for heavy damage. Most of the third-instar grubs attain their full size in approximately 50 days before the onset of winter (Misra and Chandel, 2003). During the later part of the rainy season, the white grubs stop feeding, construct earthen cells, remain inside these cells until spring, and then metamorphose into pupae. Pupation takes place in March and April. Ecdysis from pupa to adult occurs in earthen cells in 20 days (Chandel and Kashyap, 1997). The pupa is about 17 mm long and 7 mm wide, and is light brown to creamy in color. The pupa generally resembles the adult, although the wings are short and twisted toward the ventral surface. Adults remain confined in these cells for some time. With the onset of rain, the earthen cells are softened, and the beetles emerge from these cells. Adults are black beetles (Fig. 21.3) with an average length and width of 13e15 mm and 7e8 mm, respectively. They are commonly found on apple. Maximum adult emergence takes place in mid-June (Chandel et al., 2003). The adult longevity ranges from 32 to 46 days for females, and from 17 to 44 days for males (Chandel et al., 1995).

FIG. 21.2 Fully-fed grubs of Brahmina coriacea.

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FIG. 21.3 Adult beetles of Brahmina coriacea.

21.2.1.1.2 Holotrichia longipennis Beetle emergence begins during the first fortnight of May. The beetles (Fig. 21.4) have been reported to feed upon the foliage of a wide variety of fruit/forest trees, but Rubus ellipticus Smith, apple, walnut, chestnut, and plum are its preferred hosts (Shah and Shah, 1990). Eggs are laid singly inside earthen cells, and the incubation period is 11e18 days. The young grubs soon begin to feed on rotten organic matter in soil, and grow rapidly. The first instar stage lasts for 38e44 days. Two molts occur during the rainy season, and the second instar can be seen damaging tubers by the end of July. The full-grown grubs measure 38.12 mm in length. They cease to feed, move 15e20 cm deep into the soil, and construct earthen cells for overwintering by mid-November. They can go as deep as 2.5 m into the soil to overwinter. The total larval period is 243e282 days (Shah and Shah, 1990). The diapausing grubs start their upward movement by the end of March, and pupate at a soil depth of 20e30 cm. The pupal period lasts from 22 to 28 days. During the first week of May, almost all the pupae are transformed into adults (Mishra and Singh, 1993). Adult beetles live for 28e56 days.

FIG. 21.4 Adult beetles of Holotrichia longipennis.

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21.2.1.1.3 Holotrichia seticollis H. seticollis is an important species in the hilly tracts of Uttrakhand (Yadava and Sharma, 1995). Chandel et al. (1994a) also reported this species from Himachal Pradesh. The grubs cause damage to all rainy season crops. Beetle emergence may start in the month of May, after the area has received a good amount of precipitation. Emergence may vary in different localities depending on the amount of rain, and may be observed till the end of August. Immediately after emergence, adults mate on host trees such as walnut. Copulation lasts for 6e11 min. Females may lay 10e20 elongate white eggs. The average length and width of eggs is 2.65 and 1.70 mm, respectively, and the incubation period ranges from 9 to 11 days. The newly hatched grubs measure about 8.32 mm in length; the second and third instars average about 17.8 and 35.5 mm in length, respectively. Fully-fed third instars transform into pupae in the beginning of October at a depth of 30e50 cm inside an earthen cell. The pupal period ranges from 15 to 20 days. The adults remain in the soil until emergence, which is triggered by premonsoon rains during May. The beetles are dark brown in color and medium in size (ca. 15e16 mm long). One generation of beetles occurs per year (Yadava and Sharma, 1995). 21.2.1.1.4 Holotrichia serrata This species is prevalent in Karnataka, Maharashtra, Andhra Pradesh, Tamil Nadu, Kerala, South Rajasthan, the Tarai belt of Uttrakhand, and South Bihar. The beetles of H. serrata may start emerging from soil prior to rain during AprileMay, and will continue until the onset of a monsoon (Mathur et al., 2010). The adults are attracted to neem, palas, babul, guava, grapevine, etc. The grubs cause extensive damage to vegetables, pulses, oilseed, cereals, millets, tobacco, sugarcane, and sorghum (Yadava and Sharma, 1995). A gravid female lays up to 40 eggs in her lifetime. Newly laid eggs are spherical and measure, on average, 2 mm in diameter. Eggs hatch in 12e15 days, and 1e2 days before hatching the egg swells to up to 4.0 mm in diameter. The first instar comes out of the earthen cell if there is sufficient moisture. Under drought, it remains inside the cell until favorable conditions occur. First-, second- and third-instar grubs are 10.8, 20.0, and 47.0 mm long, respectively, and the average durations of each instar are 22.5, 35 and 124.5 days, respectively. The grubs become full grown in October, stop feeding, burrow deeper in the soil, and construct earthen cells for pupation. The pupal stage continues for 15.5 days. Adults are 22.4 mm long and 14.0 mm wide. The color of the pupa is dull brown, with a light brown abdomen and dark brown legs (Yadava and Sharma, 1995). 21.2.1.1.5 Anomala dimidiata Anomala dimidiata is a prevalent species in the Himalayan ranges and causes severe crop damage in Himachal Pradesh, Uttrakhand, and Jammu & Kashmir. The adults are strongly phototactic (Mehta et al., 2008). Beetle emergence begins by the end of the May. Adults prefer to feed on leaves of apple, walnut, plum, toon, poplar, and shisham. The beetles typically lay eggs in slightly sandy soil with 30%e40% soil moisture and rich decaying vegetative matter. The mated female lays, on an average, 29 eggs. The newly laid eggs are oval in shape and white in color. Prior to hatching, the eggs turn spherical in shape and dark brown in color. Eggs hatch in 13e15 days. By completion of the first instar, the larva usually attains a length of 11e13 mm. The second and third instars are similar in appearance but larger in size, with body lengths of about 23 and 38 mm attained for the second and third instars, respectively. The duration of instars is about 15, 38 and 255 days for instars 1, 2, and 3, respectively. The grubs cause maximum damage during September. With the onset of winter, the grubs make earthen cells and enter overwintering diapause. At the beginning of March, the grubs again resume their activity and feed. After feeding for about 1e2 weeks, they pupate at the end of March; the duration of the pupal stage is about 2 weeks. Pupae transform into adults during the month of April. The adults are shiny, metallic green beetles (Fig. 21.5). The length and width of the beetles range from 20 to 22 mm and 12e15 mm, respectively. Adults normally live for 21e28 days after mating. There is only one generation in a year (Mishra, 2001).

21.2.1.2 Management As a rule, adults do not deposit eggs in clover and alfalfa unless there is a considerable admixture of grasses or other weeds. Thus, grub populations could be reduced by rotating these crops with potato. One of the best ways to clean grubs out of a field is to pasture the land with pigs, as when pigs are allowed to forage on heavily infested land they will usually root out and eat the grubs. Plowing infested fields when most the grubs are pupating kills many of the pupae and newly formed adults (Misra and Chandel, 2003). The beetles are also collected at night and killed in water mixed with kerosene. Fertilization with compost, as opposed to fresh farmyard manure, provides less nutrients to early instars. Preferred hosts (see above) which attract adult beetles could be planted to trap them so they can be killed.

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FIG. 21.5 Adult beetles of Anomala dimidiata.

Chemical control options used by Indian farmers include spraying methyl parathion, carbaryl, or monocrotophos (Chandel et al., 1994b; Chandla et al., 1988; Anonymous, 2000). Damage can also be minimized by the application of phorate at the time of hilling. Chlorpyriphos application at the time of hilling is also equally effective. To obtain the best results, insecticide application should occur soon after adult emergence, and should coincide with egg laying or egg hatching (Chandel et al., 2008a).

21.2.2 Cutworms Cut worms, Agrotis spp (Lepidoptera: Noctuidae), are polyphagous insects of cosmopolitan distribution. In India, Agrotis ipsilon (Hufn.), A. segetum (Schiff.), A. flammatra Schiff., A. interacta Wlk., and A. spinifera Hb. occur on potato. Of those, A. segetum and A. ipsilon are the most serious pests; the former is common in the hills and the latter is common in the plains. Peak activity occurs during MayeJune in the Shimla hills, in August in peninsular India, and in MarcheApril in Bihar and Punjab (Singh, 1987). Cutworms are found in the upper layer of soil. They come out during the night and cut plant shoots at the base. In some cases entire rows of the plants are cut, making replanting necessary. The attack is more pronounced during dry periods when potato vines have reduced turgor. Tuber damage does not occur on rainy season crops, but larvae inflict considerable tuber damage on the spring crop. Smooth, grayish-brown, greasy, and plump-looking caterpillars are found during the daytime hiding in soil close to the stems of plants. Newly hatched larvae feed on potato haulms for the first week after hatching, then drop from the plants and feed underground on stems and tubers. While still on the plant, young caterpillars are susceptible to death by drowning in rain or irrigation water. The cutworms chew off the plants just above, or at a short distance below, the surface of soil. Most of the plant remains intact, but enough tissue is usually removed from the stem to cause it to fall over. Consequently, these caterpillars have a great capacity for causing damage. Tuber injury is manifested in the form of deep irregular holes in the flesh (Fig. 21.6), which reduce tuber quality and may allow secondary pathogens and pests to invade and cause further damage. The holes can look like those caused by slugs, but slugs are typically only a problem in wet, heavy soils. Cutworm damage is usually only significant in nonirrigated crops in lighter soils during hot and dry summers. Das and Ram (1988) reported 12.7% tuber damage due to cutworms in Bihar. In Himachal Pradesh, 9.0%e16.4% tubers were found to be damaged by cutworms (Kishore and Misra, 1988).

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FIG. 21.6 Tuber damage by larva of A. segetum.

21.2.3 Surface cutworm, Agrotis spinifera This species occurs in Punjab, Bihar, Andhra Pradesh, and Karnataka. Adult moths appear in August, and their peak population is found in September, followed by a gradual decline during OctobereNovember. Damage is usually first noticed in December. Larvae and pupae are found during February and April, respectively (Trivedi and Rajagopal, 1999). The moths become active at 7 p.m., and a female lays 431e901 eggs over a period of 4e10 days. The mated males and females survive for 4e18 and 6e12 days, respectively. Larvae feed only on leaves and growing shoots (Chandel et al., 2008a).

21.2.4 Greasy cutworm, Agrotis ipsilon This is generally a cool-climate pest. In India, it is a more serious pest in the northern region than in the south. On the plains it is active from October onwards, and it migrates to hilly regions at the onset of summer (Butani and Jotwani, 1984). The female starts laying eggs 4e6 days after emergence, and lays 649e1711 eggs over a period of 4e11 days. Eggs are laid during the night, starting at 9 p.m., either singly or in batches of 7e42 eggs. Eggs are laid on the ventral surfaces of leaves or on the surface of moist soil. Freshly plowed fields are preferred for oviposition (Srivastava and Butani, 1998). Eggs hatch in 3e5 days. The caterpillars are light brown with a reddish tinge, which turns greenish thereafter. Fully grown larvae are 40e50 mm long and feel greasy to the touch, hence the common name “greasy cutworms”. The larval period lasts from 22 to 30 days. Occasionally, the caterpillars may also nibble on tubers. Pupation takes place in the soil and lasts for 12e15 days during March. The moth’s life cycle is completed in 39e53 days (Singh, 1987). Moths are medium-sized, stout, and dark greenish brown with a reddish tinge, and have grayish-brown wavy lines and spots on their forewings; the hindwings are hyaline with a dark terminal fringe (Fig. 21.7).

21.2.5 Common cutworm, Agrotis segetum The moths are a pale whitish brown with forewings ocherous-brown, having double-waved subbasal ante and postmedial lines and a marginal series of specks; the hindwings are iridescent white with dark marginal lines (Fig. 21.8). The wingspan is 40e48 mm. Adult moths emerge from late May to the end of June and lay eggs in clusters of 18e40 on the leaves and stems of plants. Some of the cutworms feed until late July or August, and then pupate and emerge to produce a second

FIG. 21.7 Adult moth of A. ipsilon.

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FIG. 21.8 Adult moth of A. segetum.

generation of moths. Most, however, overwinter as caterpillars in the soil and pupate during the following April or May; the moths emerge in May and June. The eggs hatch in 4e7 days. The eggs are dome-shaped and creamy white in color. Full-grown caterpillars are 35 mm in length. The larvae complete their development in 22e30 days. The prepupal and pupal periods range between 2e3 and 12e20 days. Normally, pupation takes place in soil or between the folds of dried potato leaves. Male moths live for 2e4 days and female moths live for 5e8 days. Mean fecundity is 161 eggs per female. Two generations are completed during a potato crop season (Misra et al., 1995).

21.2.6 Gram cutworm, Agrotis flammatra This pest is distributed in Punjab and the subHimalayan region. Moths of A. flammatra are much bigger in size than other cutworm species, with an average wing span of 56 mm. The forewings have characteristic markings and smoky patches, with two-thirds of the proximal areas being pale. On each wing, there is a semicircular spot below the pale area and a grayish-brown, kidneyshaped spot toward the apical area. The caterpillars are dark gray or dull green, measuring 40e50 mm (Chandel et al., 2008a). The pest is active from OctobereApril in the plains and migrates to the mountains in the summer. In October, the moths lay eggs on the undersides of leaves, on shoots, stems, or in the soil. A female lays up to 980 eggs during her lifespan of 7e13 days. The eggs hatch in 4e7 days during summer and in 10e14 days during winter. Larvae complete their development in 4e7 weeks. The pupal stage lasts 12e15 days. The life cycle is completed in 7e11 weeks, and there are generally two generations in a year (Chandel et al., 2007).

21.2.6.1 Agrotis interacta A. interacta moths are more or less similar in appearance and size to A. segetum. The moth is exclusively subterranean and feeds generally on roots and tubers by chewing inside cavities. Information on its biology is lacking. 21.2.6.1.1 Management Forking the soil exposes the larvae and makes them readily available for feeding by generalist avian predators. Efficient chemical control of cutworms can only be achieved by properly applying sprays when the young caterpillars are still on the haulms and are therefore vulnerable. Once below ground, cutworms are unlikely to be significantly affected by insecticides applied to the soil or to foliage. Older caterpillars are generally less susceptible to insecticides than young caterpillars. Routine treatments are likely to be applied at the wrong time, or when the risk of damage is small. Young caterpillars can be killed by rain or irrigation, and an insecticidal spray would probably be unnecessary in these conditions (Chandel et al., 2008a). Treatments should be applied when the soil is dry and the weather is warm. Good control of cutworms depends on a thorough coverage of the foliage with a high-volume application, preferably using at least 1000 L/ha of water. Chlorpyriphos, cypermethrin, and triazophos are used by Indian farmers for the control of cutworms on potatoes. However, applying pesticides to crops suffering from drought may result in phytotoxicity. Severe losses caused in a spring crop can be reduced significantly by using oxydemeton methyl. The economic threshold level is one larva per 10 plants (Trivedi and Rajagopal, 1999).

21.2.7 Wireworms Wireworms are the larvae of various click beetles (Coleoptera: Elateridae), most commonly Drasterius spp., Agronichis spp., or Lacon spp. Occasionally, they can cause a lot of damage to potatoes. Wireworms are often a problem when

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FIG. 21.9

Tubers showing wireworm damage.

potatoes follow cereal crops or are planted in fields taken out of sod, pasture, or grass (Chandel and Chandla, 2003). Seed tubers may be attacked by wireworms in the spring to early summer, but such damage rarely affects the establishment of the crop. Major damage occurs from the time of tuber initiation until harvest, and can reduce the marketable quality of the tubers (Chandel et al., 2008a). Wireworms bore into the tubers, making cylindrical holes (Fig. 21.9). Secondary infection from various diseases can follow, further reducing the quality of the crop. Because tuber quality is so important, very low levels of wireworm damage can have a large effect on the price of the crop. Sometimes tubers still contain wireworms when they are lifted, but stored potatoes rarely contain them Chandel and Chandla (2003). The economic threshold level is low, and treatment may be initiated if any wireworms are detected in a preplanting soil sample.

21.2.7.1 Biology The wireworms take 4e5 years to complete their development, and spend the entire time feeding in the soil. Eggs are laid in grassland or grassy stubble in May and June. After about 1 month, the eggs hatch and the young wireworms initially feed on organic matter in the soil. When newly hatched, the wireworms are about 1.5 mm long and whitish in color. Fully developed wireworms are about 25 mm long and yellow (Fig. 21.10). Older wireworms feed on the roots of many crops and weeds and bore into stems and other plant organs, including potato tubers. The mature larvae pupate in small cells that they form in the soil and emerge as adults during the following spring. Most damage to potato is caused by the larvae in their second and third years of development. The presence of wireworms can be monitored by using buried baits. Pieces of carrot can be buried about 7.5 cm deep at 10e20 marked sites throughout the field. In 2e3 days, the carrot pieces are retrieved and checked for wireworms. Another type of bait can be prepared by wrapping two to three tablespoons of coarse whole-wheat flour in a small piece of netting or nylon stocking and tying it shut. If more than 1.32 wireworms/m2 are found, the field should either be treated before planting potatoes, or not be used for potato production (Chandel and Chandla, 2003). However, this action threshold may vary from one region to another.

FIG. 21.10 Fully-fed wireworms.

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21.2.7.2 Management When the risk of damage is very high and wireworm populations in the soil are large, it may be preferable to avoid growing potatoes and plant a more resistant crop, or one in which quality is less important. Legume crops are good rotational choices in fields prone to wireworm infestation, as long as they are kept weedfree. Insecticides incorporated into ridges immediately before planting can reduce tuber damage, but are unlikely to give complete control where wireworm levels are high. Phorate applied in furrow is approved for the control of wireworms in potatoes in India (Chandel and Chandla, 2003). It can also be side-dressed after potato shoots begin to emerge.

21.2.8 Termites and ants Several species of termites, such as Microtermes obesi (Holmgren), Odontotermes obesus (Rambur), and Eromotermes spp (Isoptera: Termitidae), have been reported as damaging potato crops (Butani and Jotwani, 1984). Rain-fed crops are more prone to termite damage than frequently irrigated crops. Deep black soils and continuously irrigated areas are free from termite damage. More damage occurs under drought conditions. Termites are soft-skinned, slender insects varying in color from creamy white to dark brown. They are about 2.5 cm long and dirty white in color with brown heads. They are social in habit, and live in colonies in nests that they build below the ground. Workers are wingless, and can be easily recognized by their vertically-carried head with small, broad jaws. Termite nests contain fungal combs which are lodged either in the central chamber of the nest or far apart in the soil with interconnected galleries. Fungi are maintained and harvested for food. Odontotermes obesus builds tall, subcylindrical mounds up to 2e4 m in height with series of buttresses on the surface. The inner walls are pitted, without any openings to the outside. A large central cavity contains a number of fungal combs arranged unilocularly. The work of the colony is efficiently organized, and there is division of labor. The winged forms, or reproductives, leave the nest in swarms, generally at the start of the rainy season. Most of the individuals perish, but the few that survive mate, shed their wings, and burrow in the soil to form a new colony of which they become kings and queens. The queen lays the first batch of 10e130 eggs about a week after swarming, but continues to lay in very large numbers (about 70,000e80,000 eggs per day) throughout her life, which may be as long as 5e10 years. The worker caste of termites is responsible for crop damage by damaging roots and making deep holes in potato tubers. The tubers become hollow and are often filled with soil. The leaves of affected plants start to yellow and wilt, and will ultimately dry up (Srivastava and Butani, 1998). When infested plants are pulled out, numerous feeding holes are present on the roots and tubers. The red ant species Dorylus orientalis Westwood and D. labiatus Shuck (Hymenoptera: Formicide) have a termitelike habit of attacking plants underground. Unlike termites, they do not shun light. They live in colonies that each has several specialized castes for performing different duties (Fig. 21.11). In a nest, there may be one or several queens e the reproductive females e and two or three forms of sterile females and the workers. The ants that are commonly seen in the field are workers. Red ants are reported as a pest of potato, cauliflower, cabbage, groundnut, sugarcane, and coconut seedlings in the North-Eastern states, Bihar, and Uttar Pradesh (Roonwal, 1976). The pest appears during December and remains active until April, causing more than 10% of the damage in irrigated potato crops. High temperatures and dry weather favor population build-up (Kishore et al., 1993). The pest damages potato stems and tubers by chewing holes (Fig. 21.12). Severely damaged plants wilt in direct sunlight and will eventually dry up (Trivedi and Rajagopal, 1999).

21.2.8.1 Management Once a colony is established, it is not easy to eradicate. To avoid damage caused by termites and ants, raising potatoes in sandy soils or areas infested with these pests (especially termites) should be avoided whenever possible. The use of fresh or incompletely decomposed farmyard manure should be avoided. The damage can also be reduced by irrigation (Pandey, 2002). Applying a soil spray with chlorpyriphos to the soil as a preplanting dust formulation or as a postplanting spray has been found effective, particularly in managing termites (Raj and Parihar, 1993). The best cultural method in termite management involves locating and destroying termite nests. This is achieved by breaking open the mounds and removing the queen termite. Clearing and burning of crop residues deprives termites of food and helps to keep their populations at low levels. Mound-building termites are also suppressed by treating the mounds with fumigants, either aluminum phosphide or phorate, as well as by direct applications of liquid formulations of chlorpyriphos or fenvalerate.

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FIG. 21.11 Damage-causing workers of red ants.

FIG. 21.12 Tubers showing red ants damage.

21.2.9 Potato tuber moth The potato tuber moth, Phthorimaea operculella (Zeller), is a serious pest of stored potato tubers (Fig. 21.13) that also causes considerable damage to potato plants and developing tubers in the field (Fig. 21.14). The potato tuber moth was introduced into India in 1906 through seed potato from Italy (Lefroy, 1907). Thereafter, damage to potato tubers under country storage conditions was reported in different parts of the country (Woodhouse, 1912; Rahman, 1944; Lal, 1945; Kumar and Nirula, 1967). Fletcher (1919) reported tuber moth occurring in Pune (Maharashtra), Sitamarihi, Pusa, Purnea (Bihar), Pratapgarh (Uttar Pradesh), and Chhindwara (Madhya Pradesh). Infestation rates ranged between 30% and 70% of the stored tubers (Nirula, 1960). Recently, Chandel et al. (2001) observed 31.3%e60.0% infestation in different villages of the Kangra valley, Himachal Pradesh after 3 months of storage. Heavy damage occurs in country stores in Maharashtra, Tamil Nadu, Himachal Pradesh, and the North-Eastern hill states and the plateau region. Trivedi et al. (1994) found up to 100% tuber infestation in Karnataka. In Himachal Pradesh, Singh et al. (1990) reported 30%e60% infestation of tubers from the Kangra valley.

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FIG. 21.13 Heavily infested tubers by potato tuberworms.

FIG. 21.14 Leaf mining by potato tuber worms.

Moths emerge from overwintering larvae in the early spring and lay eggs, chiefly on the undersides of leaves. The eggs hatch in 4e7 days. The larvae are fully fed within 15e20 days. The pupal period ranges from 6 to 8 days. An entire generation may be completed in 22e25 days in warm weather conditions, and five to six generations are produced per year in the Kangra Valley of Himachal Pradesh (Chandel et al., 2001). The damage is most severe in years of low rainfall and high temperatures. In a year, as many as 11 generations have been reported to occur in Assam, eight to nine generations in the northern plains, and 10e13 generations in the plateau region.

21.2.9.1 Management Chandel et al. (2008b) reported that cultural practices significantly contribute to the reduction of tuber infestation at harvest. It is crucial to reduce initial infestation of stored potatoes and the subsequent population build-up in storage. To control this pest, healthy seed tubers should be planted at 10 cm depth, and potato fields should be kept well cultivated and deeply hilled during their growth. Irrigating the field well before the soil dries, so that there is no formation of cracks in the soil, has been observed to reduce tuber infestation. Tuber infestation is also lower on fields with sprinkler irrigation than on fields with in-furrow irrigation (Chandel et al., 2005). Infestations in growing potatoes are controlled by spraying the foliage with monocrotophos or synthetic pyrethroids after mid-March, when worms begin to infest the leaves (Chandel et al., 2000). The infested wilting vines are cut and removed from the field a few days before digging, and should be never piled over dug potatoes. Harvesting should be done before 75% of the foliage dries up. The tubers should not be left exposed to egg-laying moths during late afternoon or overnight (Chandel et al., 2008a). Storage of healthy, uninfested tubers in cold stores is the best way to control tuber moth. In traditional rustic stores, tuber infestation can be prevented by covering stores with a 2-cm layer of dry leaves of Lantana or Eucalyptus

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(Anonymous, 2000). The application of insecticides to tubers intended for human consumption is highly undesirable, and illegal. Granulosis virus (GVs) is extremely effective in reducing PTM damage under storage conditions (Chandel and Chandla, 2005). Traditional country stores could be improved by blocking air holes. Openings should have good air circulation to keep the inside temperature cool, but wire-mesh screens should be used to limit access by potato tuber moths. Seed potatoes that are not to be used for food may be treated at the time of storage with malathion dust. A thorough cleanup of potato storage sheds after tuber removal helps to prevent reinfestation (Chandel et al., 2000).

21.2.10 Mole cricket, Gryllotalpa africana Palisot This is a sporadically severe pest that has been reported from Bengal. It is especially damaging to young seedlings in moist soils. The species is widely distributed in warm regions of Eurasia. Konar et al. (2005) reported 5%e6% plant damage, along with 10%e15% tuber damage, in West Bengal. Eggs are laid during the rainy season, 100e150 mm deep in the soil in earthen chambers prepared by females. A female makes three to four chambers in her lifetime and deposits 20e30 eggs in each chamber. Eggs are oval in shape, about 1.5 mm long, and are brown in color. Nymphs live underground in branching burrows and feed on the roots of cultivated and wild plants. They also tunnel into newly planted seed tubers. Both nymphs and adults come out of the soil during the night and feed on the leaves of plants. Adults are 22e28 mm long, brown in color, with short wings folded over the abdomen without covering the abdomen completely (Butani and Jotwani, 1984).

21.2.10.1 Management Mole crickets are usually controlled by applying phorate and chlorpyriphos (Konar et al., 2005).

21.2.11 Minor pests Darkling beetles Gonocephalum hofmannseggi (Steven) and Hopatroides seriatoporus Fairmaire (Coleoptera: Tenebrionidae) have been reported from Karnataka (Srivastava and Butani, 1998). These beetles feed on roots and occasionally on tubers. Feeding damage may result in the death of young sprouting plants, but has little effect on a mature crop.

21.3 Sap-feeding pests Sap-feeding insects can affect the health of a potato crop, both directly by causing feeding damage as well as indirectly by transmitting viruses and viruslike pathogens that cause important diseases. As vectors, aphids and whiteflies are especially critical in the production of seed potatoes because tuber-borne viruses can severely limit yields in subsequent crops. They have elongated mouthparts which form a tube composed of paired mandibular and maxillary stylets, with a central food canal and a separate salivary canal. This tube is inserted into the plant, typically to reach and withdraw sap from the phloem. Sap removal is, by itself, damaging to plants, but toxic saliva and infectious virus particles may also be injected during feeding (Chandel et al., 2008c).

21.3.1 Aphids Aphids (Hemiptera: Aphididae) can injure a potato plant directly by sap feeding, and are capable of transmitting several important potato viruses. High aphid populations can have substantial direct effects on yield, but such populations are uncommon in commercial potato production. The primary concern with aphids is usually their role as virus vectors. The honeydew excreted by aphids is deposited on the plant, where it provides a good growth medium for sooty molds (Chandel et al., 2008c). Five aphid species are commonly found on potato crops in the India; the green peach aphid (Myzus persicae (Sulzer)), cotton aphid (Aphis gossypii Glover), potato root aphid (Rhopalosiphum rufiabdominalis (Sasaki)), tuber aphid (Rhopalosiphoninus latysiphon (Davidson)), and bean aphid (Aphis fabae Scopoli). The cosmopolitan aphid, M. persicae, is the most important pest on potatoes (Chandel et al., 2008c).

21.3.1.1 Biology of M. persicae In M. persicae, only eggs are produced by sexual reproduction, whereas all subsequent reproduction is viviparous and parthenogenetic (Verma and Chandla, 1999). The aphids have both winged and wingless forms. Wingless forms

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FIG. 21.15 Sucking wingless green peach aphid, M. persicae.

(Fig. 21.15) are predominant on potato during most of the year. Myzus persicae overwinter as eggs on a very restricted number of primary host species, usually woody plants, with peach being the most important host. In spring, wingless aphids called stem mothers hatch from eggs, feed on the primary host, mature, and produce young asexually. The offspring of stem mothers are generally wingless. Aphids molt four times, with the mean number of offspring per wingless aphid ranging from 60 to 75 (Chandla and Verma, 2000). Optimum temperature for reproduction is around 21 C. There may be several generations on a primary host, but eventually winged adults (spring migrants) develop and fly away to colonize “secondary”, often herbaceous, host plants (Chandel et al., 2007). Winged spring migrants are not produced until at least the second generation on the primary host, and peak production occurs in the third generation. Spring migrants leave the primary host in search of suitable secondary hosts, usually herbaceous plants, one of which is the potato. These spring migrants are capable of traveling long distances e up to 1600 km e and have been found at altitudes of up to 3048 m (Chandel et al., 2008c). Winged aphids land at random, since they cannot visually distinguish a host from a nonhost plant. To find a suitable host, winged aphids feed for short periods on sap from epidermal tissues of plants on which they land. This is called “sap sampling”. They move from plant to plant until they locate a suitable secondary host. Sap sampling can result in the transmission of certain viruses, even by aphid species incapable of colonizing potato. Once an acceptable host is found, the spring migrants settle and reproduce. Their offspring are mostly wingless, but a small proportion of each succeeding generation is winged. Each unfertilized fundatrix produces around 50e60 young ones viviparously. As many as eight apterous generations have been found on primary host plants (Verma and Chandla, 1999). As the quality of host plants declines, more winged summer migrants are produced, which then fly to other secondary host plants. As the day length shortens, fall migrants are produced with both males and females. They return to the primary host plant, on which the females give birth asexually to wingless females, which then mate with the male fall migrants and lay fertilized overwintering eggs. The eggs measure about 0.6 mm long and 0.3 mm wide and are elliptical in shape. They are initially yellow or green, but soon turn black. Nymphs are initially greenish, but soon turn yellowish, greatly resembling viviparous adults. Verma and Chandla (1999) reported four instars in this aphid, with duration of each instar ranging from 1 to 2, 2e3, two to three, and 4e5 days, respectively. Alate aphids have a black head and thorax and a yellowishegreen abdomen, with a large dark patch dorsally. They measure 1.8e2.1 mm long. The apterous aphids are yellowish or greenish. They measure about

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1.7e2.0 mm long. Medial and lateral green stripes may be present. The cornicles are moderately long, unevenly swollen along their length, and match the body in color. The appendages are pale. Each gynopara produces about 5e15 ovipare. A male is capable of fertilizing several ovipare. Each oviparous female lays 4e13 eggs. Each viviparous female produces 30e80 nymphs (Verma and Chandla, 1999). The eggs are deposited near buds of the primary host. In mild climates, winged migrants also develop from aphid populations that survive the winter as adults. Occasionally the life cycle is incomplete, in which case asexual breeding takes place throughout the year and overwintering takes place on stored, sprouting potatoes, on hardy herbaceous plants, or on glasshouse crops (Chandel et al., 2008c).

21.3.1.2 Management of aphids Young plants are particularly susceptible to viral infection, and seed plots must therefore be kept free of aphids whenever possible, in particular early in the season. High-altitude areas of the north-western Himalaya (>2000 m above sea level) are the best seed-growing areas in India because they remain practically aphid-free during the summer season when the potato seed crop is grown. The selection and rouging of plants infected with a virus must also be done, even under aphid-free conditions. An action threshold of 20 aphids per 100 compound leaves is strictly followed in Indian seed production (Chandla et al., 2004). The most vulnerable period in the aphid life cycle is passed on the overwintering hosts. The application of chemical defoliant to peach trees in fall, the denial of foliage to fall migrants, and the pruning of trees to remove most overwintering eggs are useful. When peach trees are pruned the twigs that are removed must be destroyed, or else the eggs can still hatch (Chandel et al., 2008c). Several soil-applied systemic insecticides give good early-season control of aphids. However, late-season aphid pressure is often more severe in potatoes treated with a soil systemic insecticide at planting. Late-season outbreaks in aphid populations may be a consequence of early-season control measures that prevent the establishment of the aphids’ natural enemies (Chandel et al., 2007). Foliar sprays of dimethoate or metasystox and phorate applied in-furrow at planting are widely recommended in seed potato for aphid control (Chandla et al., 2004). Imidacloprid and thiamethoxam also provide effective protection for about 2 weeks (Chandel et al., 2008c).

21.3.2 Leafhoppers Leafhoppers (Hemiptera: Cicadellidae) are strong fliers and are much more mobile than aphids. Unlike aphids, leafhoppers are important mainly because of the direct feeding damage that they cause. The potato leaf hopper (Empoasca devastans Distant) is the most important species, and has long been recognized as a major pest of potato. Several other species are important on potato in certain regions. These include Amrasca biguttula biguttula (Ishida), Alebroides nigroscutulatus Distant, Seriana equata Singh, Empoasca solanifolia Pruthi, Empoasca kerri motti Pruthi, E. fabae Harris, and E. punjabensis Pruthi (Butani and Jotwani, 1984; Misra, 1995).

21.3.2.1 Nature of damage Prolonged feeding by the potato leafhopper causes a condition known as “hopper burn”, manifested in the form of brown triangular lesions at the tips of the leaves. Both adults and nymphs are injurious, but late-instar nymphs can reduce yields more than twice as much as an equal number of adults. Damage results from disruption of phloem (Trivedi and Rajagopal, 1999). Toxins in the saliva of potato leaf hopper induce swelling of cells, which eventually crushes the phloem. There is also depletion of plant reserves due to an increase in plant respiration subjected to leafhopper attack. Infestations are most damaging during early tuber bulking (growth stage IV).

21.3.2.2 Transmission of diseases Potato yellow dwarf virus and beet curly top virus are transmitted by leafhoppers (Empoasca spp.). Purple top in potato, which is caused by aster yellows mycoplasma-like organisms, is also transmitted by leafhoppers (Misra, 1995).

21.3.2.3 Biology of leafhoppers The leafhoppers have a broad host range. On potato, they usually complete two to four generations in a year. The population density is dependent upon the date of aphid arrival on the crop and the temperature.

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21.3.2.3.1 Amrasca biguttula biguttula Amrasca biguttula biguttula, commonly known as cotton leafhopper, is a polyphagous pest. Although its main hosts are cotton and okra, it also causes serious damage to brinjal and potato (Shankar et al., 2008). Both nymphs and adults suck cell sap, usually from the ventral surfaces of leaves. Adults are wedge-shaped, about 2 mm long, and pale green in color with a black dot on the posterior portion of each forewing. Eggs, which are pear-shaped, elongated, and yellowish-white in color, are deposited individually on leaves. A single female lays 15e30 eggs that hatch within 4e10 days. The nymphal period lasts for 7e21 days, and the nymphs are whitish to pale green in color. Peculiarly, they move diagonally across leaves. The longevity of the adults is about 2 weeks (Srivastava and Butani, 1998). 21.3.2.3.2 Empoasca kerri motti This species breeds throughout the year, but it is most active from October to March. Beside potato, this hopper attacks brinjal, chili pepper, cowpea, and tomato. In the absence of these hosts, it migrates to castor, alfalfa, and barseem (Butani and Jotwani, 1984). The adults are 3 mm long and yellowish-green in color; the vertex is flat, greenish-yellow, and smaller than the protonum, which is also smooth and flat; the front wings are long, narrow, semitransparent, and pale green in color, with green at the costal and gray at the distal regions (Srivastava and Butani, 1998). A female lays 25e60 eggs in 25e30 days. The incubation period is 4e11 days, and the nymphal period averages 25 days. Adult longevity is about 2 weeks in males and as many as 13 weeks in females (Butani and Jotwani, 1984). 21.3.2.3.3 Empoasca punjabensis E. punjabensis produces symptoms of hopper burn on leaves. These symptoms are manifested in the forms of etiolated spots and patches on leaves, browning, rotting of margins and tips, and drying of leaves. Females lay eggs in leaf veins. Eggs hatch in 4e9 days, nymphal development takes 19e21 days, and adult longevity is 7e15 days (Butani and Jotwani, 1984). Adults are, on average, 3.5 mm long and yellowish-green in color. The vertex is flat, smooth, and pointed, and the protonum is transparent and longer than the vertex. The abdomen is yellowish, and the ovipositor is stout and green in color. The front wings are longer than the body and are transparent greenish-yellow in color, with deep-green coastal margins (Srivastava and Butani, 1998). 21.3.2.3.4 E. solanifolia This species causes similar damage to E. punjabensis. The adults are bigger in size, being about 4.0 mm long, robust, and pale brown in color; the vertex is flat and slightly raised; the protonum is 1½ times longer than the vertex; the abdomen is tinged with yellow; the ovipositor is stout and the pygopher is covered with a few minute hairs. The hemelytra are transparent and are twice as long as the abdomen, having thin, distinct veins (Butani and Jotwani, 1984). 21.3.2.3.5 E. fabae Commonly called potato leafhopper, this species is more common outside India. Similar to other leafhoppers, it produces hopper burn symptoms such as stunted growth and crinkling of the leaves (Srivastava and Butani, 1998). The adults are pale green and marked with a row of white spots on the anterior margins of the protonum. They are about 3.5 mm long. Females lay transparent to pale yellow eggs, which are inserted into the veins and petioles of leaves. Total egg production is about 200e300 eggs per female, and the average incubation period is 10 days. The average development time for nymphs is 15 days. Adult longevity is typically 30e60 days.

21.3.2.4 Control of leafhoppers Foliage of early-maturing cultivars is generally more susceptible to leafhopper damage. However, they bulk more rapidly, and their yield may actually be less affected compared to later-maturing cultivars. It is more important to control leafhoppers under drought conditions, when potato is more susceptible to leafhopper injury. In seed crop, soil systemic insecticides applied in furrow at planting or side-dressed at plant emergence give 6e8 weeks of control. On fresh market potatoes, the standard practice is to apply foliar sprays. Dimethoate and methyl demeton applied at the appearance of the pest, and phorate applied at planting, are approved for the control of leafhoppers in India (Pandey, 2002).

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21.3.3 Thrips Thrips are the vectors of tospo viruses, which cause stem necrosis in potato. Seven species of thrip are associated with potato. Of these, Thrips palmi Karny, Scirtothrips dorsalis Hood, Caliothrips collaris (Bagnall) (Thysanoptera: Thripidae), and Haplothrips sp. (Thysanoptera: Phlaeothripidae) are important. These are tiny, slender, fragile insects, with adults having heavily fringed wings. The females have extremely slender wings with a fringe of long hairs around their margins.

21.3.3.1 Nature of damage Both adults and larvae scrape the epidermal tissues of leaves, usually near the tips, and rasp the oozing sap (Butani and Jatwani, 1984). The surface of leaves becomes whitened and somewhat flecked in appearance. The tips of leaves wither, curl up, and die. The undersides of leaves become spotted with small, brownishblackish specks (Fig. 21.16). When damage is severe, the whole field has a “dry blight” appearance, where most of the infected plants have dry leaves hanging on blighted stems. Eventually, such plants wilt and die (Khurana et al., 2001).

21.3.3.2 Biology Parthenogenesis is common. The males are wingless and very scarce; the females regularly reproduce without mating. In case of T. palmi, eggs are deposited in leaf tissue, in a slit cut by the female. Females produce up to 200 eggs, but average about 50 per female. The bean-shaped egg is colorless to pale white. Duration of the egg stage is about 16 days at 15 C, 7.5 days at 26 C, and 4.3 days at 32 C (Khurana et al., 2001). The larvae (Fig. 21.17) resemble the adults in general body form, though they lack wings and have a smaller body size. There are two instars during the larval period. Larvae require about 14, 5, and 4 days to complete their development at 15 C, 26, and 32 C, respectively. At the completion of the larval stage the insect usually descends to the soil or leaf litter, where it constructs a small Earthen chamber for a pupation site. There are two instars during the pupal period. The prepupal instar is nearly inactive, and the pupal instar is inactive. Both instars are nonfeeding stages (Khurana et al., 2001).

FIG. 21.16 Spots due to thrips feeding.

FIG. 21.17 Nymphs of thrips.

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The combined prepupal and pupal development time is about 12, 4, and 3 days at 15, 26, and 32 C, respectively. After the fourth molt, the adult females return to the plants and soon lay eggs for another generation. The total time required for each generation is about 20 days. The high temperatures (30e35 C) and dry weather during SeptembereOctober are highly favorable for aphid/thrip activity and, consequently, higher disease incidence (Khurana et al., 2001). Adults are pale yellow or whitish, measuring 0.8e1.0 mm in body length, with females being slightly larger than males. Unlike the larval stage, the adults tend to feed on young growth, and thus are found on new leaves. Adult longevity is 10e30 days for females and 7e20 days for males.

21.3.3.3 Transmission of tospo viruses These viruses are acquired by the first instars shortly after they hatch from the eggs and start feeding on infected plants. The latent period is 3e10 days. Transmission is mainly via the adult thrips. During the latent period, the virus circulates in the vector and replicates throughout the life of viruliferous thrips (Chandel et al., 2008c).

21.3.3.4 Control In potato, there is a strong positive correlation between early planting and thrip activity. Therefore, early planting (September/October) must be avoided whenever possible. Certain varieties are resistant to injury by this pest. In the plains, the Kufri Sutlej, Kufri Badshah, and Kufri Jawahar strains are comparatively resistant (Singh et al., 1997), and the Kufri Chandramukhi and Kufri Bahar strains are susceptible. After the plants start growing they should be watched carefully, and if the thrips or the characteristic injury appears upon them then the plants should be sprayed with imidacloprid. Imidacloprid, applied as a foliar spray or as a side-dressing at the first signs of thrip damage, usually provides good control (Singh et al., 2000). Generally, chemical applications are limited to the first and second weeks of crop emergence, when thrip activity is at its maximum and viruliferous thrips land on the germinating crop.

21.3.4 White flies Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is widely distributed throughout the world. This pest is distributed throughout the northern and western regions of the Indian subcontinent, and has recently emerged as a very serious pest in potato seed production, particularly in the autumn crop in the Indo- Gangetic plains (Kumar et al., 2003). B. tabaci is a highly polyphagous insect and is a serious pest of cotton, tobacco, okra, and various other vegetables and weed plants (Puri et al., 1995). The population of B. tabaci is highly diverse, and many biotypes have been identified. Infestation is heavier on early potato crops planted in September. The maximum population on potato occurs in November, followed by a sharp decline by December (Chandel et al., 2010).

21.3.4.1 Nature of damage Adults and nymphs use their piercing-sucking mouthparts to feed on the phloem of host plants. This results in direct damage, which is manifested in localized spotting, yellowing, or leaf drop (Broad and Puri, 1993). Under heavy feeding pressure, wilting and severe growth reduction may occur (Malik et al., 2005). Systemic effects may occur, with noninfested leaves and other tissues becoming severely damaged as long as feeding whiteflies are present on the plant (Butter and Kular, 1999). The affected plants remain stunted, and their leaves show distinct upward or downward curling. Leaves of affected plants show dark green veins as compared to the normal translucent veins of healthy plants. Whiteflies excrete honeydew that promotes the growth of sooty molds. Those, in turn, adversely affect plant photosynthesis, leading to a reduction in yield (Reddy and Rao, 1989). Once the whiteflies are removed, new plant growth is normal. In addition to direct damage, B. tabaci also causes damage indirectly by transmitting gemini viruses. Some viruses, such as potato apical leaf curl virus (PALCVs), cause more damage than insect feeding alone (Lakra, 2002). The first report of potato apical leaf curl virus in India was made around the year 2000 (Garg et al., 2001). Tuber formation is adversely affected in virus-infected plants. Dhawan and Mandal (2008) reported that potato plants infected with apical leaf curl virus showed stunting, crinkling, vein thickening, curling, waviness of leaf margins, and leaf distortion. 21.3.4.1.1 Biology of B. tabaci B. tabaci can complete a generation in about 20e30 days under favorable weather conditions (Saini, 1998). Whiteflies produce many generations in a year and quickly reach high population densities. At least three generations are completed on potato. Temperatures in the range of 26e32 C, with an RH of 60%e70%, are optimal for whitefly development (Chandel et al., 2010).

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Whiteflies insert their eggs in leaf tissues. The egg is about 0.2 mm long, elongate, and tapers distally; it is attached to the plant by a short stalk (Rao and Reddy, 1989). The whitish eggs turn brown before hatching, which occurs in 4e7 days. The female deposits 90%e95% of her eggs on the lower surface of young leaves (Arneja, 2000). The older stages prevail on older leaves. There are four nymphal instars (Dhawan et al., 2007), all of which are greenish and somewhat shiny. The flattened first instar is mobile, and is commonly called the “crawler” stage. The crawler stage measures about 0.27 mm long and 0.15 mm wide. Movement is usually limited to the first few hours after hatching, and only to a distance of 1e2 mm. The remaining instars are scalelike and stationary. The wax that the ovipositing whiteflies deposit, the spines adorning the nymphs, and the exuviae of early instars retained by the later instars help in protecting the whiteflies against natural enemies (Reddy and Rao, 1989). Whiteflies normally feed on the lower surface of leaves. Duration of the first instar is usually 2e4 days. The second and third instars are each completed in about 2e3 days (Chandel et al., 2010). Body length and width are 0.36 and 0.22 mm and 0.49 and 0.29 mm for the second and third instars, respectively. The sessile fourth instar is usually called the “pupa”, although it may still participate in some feeding. The fourth instar measures about 0.7 mm in length and 0.4 mm in width. Duration of the fourth instar is about 4e7 days (Arneja, 2000). The total nymphal period ranges from 10 to 14 days. Nymphs transform into pupae on the leaves, and in 2e3 days adult whiteflies emerge from the pupae (Sharma and Rishi, 2004). Total preadult development time averages 15e18 days (Dhawan et al., 2007). The lower and upper developmental thresholds are about 10 and 30 C (Chandel et al., 2010). The adult is white in color and measures 1.0e1.3 mm in length (Fig. 21.18). The antennae are pronounced, and the eyes are red. Oviposition begins 2e5 days after emergence of the adult, often at a rate of about five eggs per day. Adults typically live 10e20 days and may produce 50e150, or even up to 300, eggs (Reddy and Rao, 1989).

21.3.4.2 Transmission of potato apical leaf curl virus Geminiviruses are transmitted in a persistent circulative mode. For efficient transmission, an acquisition-access feeding period of 2e24 h, followed by an inoculation-access feeding period of 2e3 days, is required. Transmission occurs only after a latent period of 4e10 h. After acquisition, whiteflies can transmit virus for 5e20 days (Chandel et al., 2010).

21.3.4.3 Control Whiteflies are very difficult to control with conventional insecticides. Seed treatment with imidacloprid and foliar applications at emergence, with the second application occurring after 15 days, has been found to be effective (Malik et al., 2005). However, under conditions of severe whitefly attack none of the control measures are effective to prevent virus spread. The whitefly population can be successfully managed only by adopting a package of practices specifically targeted for its control. The cultivation of varieties susceptible to leaf curl virus should be avoided. Varieties like Kufri Bahar have shown high tolerance (Lakra, 2003), while cultivars like Kufri Sutlej and Kufri Anand are highly susceptible. Elimination of alternative hosts of the virus and the virus vector, as well as of the infected potato plants, helps to reduce virus transmission to potato plants. Excessive use of nitrogenous fertilizers may promote whitefly growth (Puri et al., 1995).

FIG. 21.18 Adults of Bemisia tabaci.

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21.3.5 Sap-sucking bugs 21.3.5.1 Green potato bug, Nezara viridula (Linn.) The green potato bug (Hemiptera: Pentatomidae) is cosmopolitan in distribution, and has been recorded from South Europe and Japan at its northernmost range to Australia and South Africa at its southernmost range. These bugs occasionally cause economic damage to potato. The green potato bug is a polyphagous pest; its main hosts are castor and coriander, but it also breeds on coffee, citrus, cotton, millets, pulses, potato, rice, tomato, wheat, etc. Nymphs and adults suck the cell sap from tender leaves and shoots, devitalizing the same. Adults are medium-sized, 15 mm long, and light green in color, and nymphs are brownish-red with multicolored spots. A female lays up to 300 eggs in clusters of 50e60 eggs on the dorsal surfaces of leaves. The eggs are deposited in regularly shaped, hexagonal clusters, with the individual eggs ordered in uniform rows and glued together. Eggs are barrel-shaped and measure about 1.3 mm long and 0.9 mm wide. They are yellowish-white to pinkish-yellow, and the top, or cap, is clearly indicated by a ring and 28e32 spines. The eggs darken in color during the incubation process, and hatching occurs after about 5 days. Nymphs remain aggregated in the first instar before they disperse and start feeding during the second instar (Butani and Jotwani, 1984). There are five instars. Nymphs are brownishred with multicolored spots, and the body length of the fifth instar is about 10 mm. Total nymphal development time is about 32 days, and egg-toadult development requires 35e37 days. The optimal temperature for development is 30 C. The adult is uniformly light green, both dorsally and ventrally, though the ventral surface is paler. Adults measure about 13e17 mm long and 8 mm wide (Srivastava and Butani, 1998). No separate control measures are generally required for these bugs, as damage is very limited. The chemical control of aphids is generally sufficient in preventing damage. 21.3.5.1.1 Creontiades pallidifer (Walker) C. pallidifer (Hemiptera: Miridae) is another polyphagous pest with a wide range of host plants, including brinjal, crucifers, melons, okra, and potato. Nymphs and adults suck the cell sap from leaves and cause small, irregular brown spots on young leaves and growing tips; gradually, the affected leaves die. This bug has been found to breed throughout the year in the Delhi area; from January to April it feeds on brinjal, peas, and potato; from April to June on melons, and from July to September on other cucurbits; during October it is found on maize and pulses; finally, during NovembereDecember, the bugs migrate and attack cole crops (Butani and Jotwani, 1984). Adult bugs are delicate, 7 mm long, and ocherous-green in color, with transparent light-green wings. A female lays 100e200 eggs, and the incubation period is 4e5 days. The eggs are deposited within tender tissues of growing points such as petioles and axils of branches. Nymphal development takes, on average, 18 days, and the total life cycle is completed in about 22 days. Adult longevity of females is 15 days; in males, the longevity is less than a week (Srivastava and Butani, 1998). 21.3.5.1.2 Piezodorus hybneri (Gmelin) (Hemiptera: Pentatomidae) This bug is a minor pest and has been reported feeding on potato leaves. Eggs are laid in clusters of 25e30 eggs each, on the dorsal surfaces of leaves. The incubation period is 3e4 days, and nymphal development takes 22e26 days. 21.3.5.1.2.1 Recaredus sp. The lace-wing bug (Hemiptera: Tingidae) attacks stored tubers in some parts of India. Nymphs and adults suck sap from cortical tissues of tubers. Eggs are laid on tubers. The total life cycle is completed in about 30 days, and as many as seven generations have been reported in a year. Adult longevity is 7e8 months, and hibernation takes place in the adult stage (Butani and Jotwani, 1984).

21.4 Leaf-eating and defoliating insects Leaf defoliators are either coleopteran or lepidopteran insects causing variable damage, depending on the geographic region and environmental conditions (Trivedi and Rajagopal, 1999). In addition to defoliation, some lepidopteran larvae also burrow into potato stems.

21.4.1 Defoliating caterpillars 21.4.1.1 Cabbage semilooper, Plusia orichalcea (Fab.) Cabbage semilooper (Lepidoptera: Noctuidae) is a polyphagous pest that has a wide host range including pea, cole crops, radish, turnip, celery, indigo, linseed, etc. It is widely distributed in India and often inflicts damage to potato throughout its range (Misra et al., 1995). The leaves are riddled with large holes of irregular shape and size and covered with masses of greenish to brown frass. In case of severe infestation, the entire plant may be defoliated.

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The adult is light brown, with a large golden patch on each forewing (Fig. 21.19). Wing span is 42 mm. The caterpillars are pale green (Fig. 21.20) and form characteristic half loops when they walk. The moths are very active at dusk on flowers during spring season. Each female lays 350e450 eggs singly on leaves. Eggs hatch in 3e5 days following oviposition. The caterpillars feed individually. Larvae are fully grown in 20e28 days, and they pupate in debris on the ground. The pupal stage lasts 8e15 days (Misra et al., 1995).

21.4.2 Oriental armyworm, Mythimna separata (Walker) The oriental armyworm (Lepidoptera: Noctuidae) is a polyphagous pest that is found all over the Indian subcontinent, South-east China, Japan, South-east Asia, Korea, the Philippines, Indonesia, Australia, and New Zealand. Young larvae scrape the leaf tissues and skeletonize the leaves, while the advanced instars feed gregariously and voraciously on whole leaves and migrate from one leaf to another. Even medium-level infestation may result in complete defoliation of vines. The moths are pale brown with dark specks, and the hindwings are white. The eggs are laid in rows or in clusters and hatch in 4e5 days. Freshly emerged larvae are very active and are dull white in color, later turning green. Larvae are fully grown in about 2 weeks. Mature larvae are cylindrical in shape, 45 mm in length, and dark green to greenish-brown, with four distinct longitudinal black green stripes on either side of the mid-dorsal line. Pupation takes place in soil, under dry leaves, or among stubbles. The pupal period is completed in 9e13 days. The entire life cycle is completed in 4e5 weeks (Chandel et al., 2011).

21.4.3 Bihar hairy caterpillar, Spilosoma obliqua (Walker) The bihar hairy caterpillar (Lepidoptera: Arctiidae) is most common during late winter and spring. It is a polyphagous pest and has been reported damaging a number of fruit trees, tobacco, pulses, vegetables, potato, and sweet potato. The newly

FIG. 21.19 Adult moth of Plusia orichalcea.

FIG. 21.20 Larva of Plusia orichalcea.

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FIG. 21.21 Adult moth of Bihar hairy caterpillar, Spilosoma obliqua.

hatched caterpillars feed gregariously, skeletonizing leaves. More mature caterpillars segregate and feed voraciously on leaves, often completely defoliating vines. The caterpillars move from plant to plant and from field to field; older leaves of older plants are preferred (Chandel et al., 2011). Wings of adult moths are pinkish-buff with numerous black spots (Fig. 21.21), spanning 40e45 mm. The head, thorax, and ventral side of the body are dull yellow. The female lays more than 400 eggs in clusters on the undersides of leaves. The eggs are spherical in shape and light green in color. They hatch in 8e13 days. Larvae pass through seven instars and are ready to pupate in 4e8 weeks. Fully grown caterpillars are stout, about 40 mm long, and have seven orange-colored, broad, transverse bands with tufts of yellow hairs (Fig. 21.22). Pupation takes place in plant debris or in the soil, and adults emerge in 1e2 weeks. The life cycle is completed in 4e5 weeks, and there may be three to eight generations per year. The caterpillars of a winter brood burrow into soil to diapause (Srivastava and Butani, 1998).

21.4.4 Hairy caterpillar, Dasychira mendosa (Hubner) The hairy caterpillar (Lepidoptera: Lymantriidae) is a polyphagous pest that feeds on potato, coffee, red gram, castor, cauliflower, and many other plant species. The larva is grayish-brown with dark prothoracic and preanal tufts. The prolegs are crimson-red. Fully grown larvae are 38e44 mm long with red stripes on their heads. The adult is smoky brown with hindwings that are pale gray in color. Forewings are uniformly brown, with black specks and a pale patch outside the subbasal line. The wing span of a female moth is 46e54 mm (Chandel et al., 2011).

21.4.5 Tobacco cutworm, Spodoptera litura (Fab.) The tobacco cutworm (Lepidoptera: Noctuidae) is a sporadically serious pest. It is highly polyphagous and is widely distributed in many parts of the world. The caterpillars hide during day in crevices and feed at night. Eggs are laid in clusters on the lower sides of leaves and are covered with brown hairs. A single female (Fig. 21.23) lays, on average, 400 eggs in three to four clusters of 80e150 eggs. Freshly hatched larvae feed gregariously, scraping the leaves. Later, these

FIG. 21.22 Larva of Bihar hairy caterpillar, Spilosoma obliqua.

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FIG. 21.23 Female moth of Spodoptera litura.

larvae disperse. During severe infestation, an entire crop may be defoliated overnight. Fully grown larvae are 40e50 mm long and are pale brown in color with a green to violet tinge (Fig. 21.24). Incubation, larval, and pupal stages last for 3e5, 20e28, and 7e11 days, respectively. The entire life cycle is completed in 30e40 days (Butani and Jotwani, 1984). A related species, Spodoptera exigua (Hubner), also occurs on potato as a serious defoliator (Butani and Jotwani, 1984). A female lays up to 1300 eggs in batches of 50e200 eggs on the ventral surfaces of leaves. The immature stages are more or less similar in appearance as those of S. litura. The larvae grow to a length of about 3.8 cm. Adults have a wingspan of 25e35 mm. Egg, larval, and pupal stages last for 2, 15, and 16e17 days, respectively. Pupation takes place on the soil surface or, rarely, at depths of 5e10 cm.

21.4.6 Gram pod borer, Heliothis armigera (Hubner) H. armigera (Lepidoptera: Noctuidae) is a highly polyphagous pest distributed throughout India. The adult is a mediumsized light-brown moth (Fig. 21.25). Eggs are deposited individually on tender leaves and hatch in 3e7 days. The young larvae are leaf scrapers, while older larvae are leaf chewers (Fig. 21.26). The mature larvae are about 35 mm long and greenish-brown in color, with dark yellow stripes. The larvae become fully grown in 17e22 days (Misra et al., 1995). They pupate in the soil for 6e12 days and hibernate as pupae. The total life cycle is completed in 4e6 weeks Chandel et al., 2011). There are five to eight generations in a year.

FIG. 21.24 Fully-fed larva of Spodoptera litura.

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FIG. 21.25 Adult moth of H. armigera.

FIG. 21.26 Leaf defoliation by larva of H. armigera.

21.4.7 Eggplant borer, Leucinodes orbonalis Guenee Eggplant borer (Lepidoptera: Crambidae) is a minor pest of potato across India (Regupathy et al., 1997). Caterpillars bore into the shoots, causing them to wilt and droop. Females deposit eggs individually on leaves and shoots. The eggs hatch in 3e5 days. The pink-colored larva becomes fully grown in 10e15 days Measuring about 1.6 cm in length. Pupation takes place in a cocoon on the plant for a period of 6e8 days (Chandel et al., 2011). To control this pest, the affected shoots may be clipped off and destroyed by burning or deep burying.

21.4.7.1 Management of lepidopterous defoliators Every effort should be made to destroy early instars. Alternate weed hosts of these insects, on which the first generation of caterpillars may develop, should be destroyed. The visible egg masses, as well as leaves with gregarious young larvae, should be collected and destroyed mechanically. Plowing could be used to expose and kill pupae in the soil. Flood irrigation may drown the hibernating caterpillars and pupae. In case of severe attack, spraying fields with carbaryl, endosulfan, monocrotophos, quinalphos, chlorpyriphos, or malathion is recommended. Two to three applications are usually required, beginning soon after initial infestation and repeated at 2-week intervals, if needed (Pandey 2002).

21.4.8 Leaf-eating beetles 21.4.8.1 Hadda beetles Epilachna beetles (Coleoptera: Coccinellidae) and their larvae are important pests of potato in India. The two species commonly found all over India are the 12-spotted (Epilachna ocellata Redt.) and 28-spotted beetles (Epilachna vigintioctopunctata (Fab.)). The former is generally found in higher hills, while the latter is restricted to lower elevations

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(Misra et al., 2003). Plant damage is caused by adults and larvae skeletonizing the leaves. The adults (Fig. 21.27) are active fliers and readily move from plant to plant. The larvae (Fig. 21.28) stay on the leaves and occur in large numbers. In case of heavy infestations, plants can be completely defoliated before tuber maturation. The yellowish, cigar-shaped eggs are laid in clusters on the lower surfaces of leaves. A female lays 500e750 eggs that hatch in 3e4 days. The larval period Lasts 8e10 days on potato, and pupation takes place on leaves and lasts from 3 to 6 days (Trivedi and Rajagopal, 1999). The life cycle is completed in 21e36 days. Adults overwinter under grass and weeds. Control: Where the beetles are abundant, it is suggested that eggs and larvae are collected and destroyed mechanically. Good control may be obtained by thoroughly spraying the foliage with malathion, dichlorvos, endosulfan, chlorpyriphos, or carbaryl (Pandey, 2002). Application should occur as soon as the beetles or their eggs are found on the plants.

21.4.9 Flea beetles, Psyllodes plana Maulik Flea beetles (Coleoptera: Chrysomelidae) have enlarged hind legs and jump vigorously when disturbed. The adult flea beetles chew small rounded holes in the leaves (Fig. 21.29), often starting on the lower side of a leaf (Chandla, 1985). They attack plants as soon as they emerge from the soil, and the damage continues until the crop is harvested. When flea beetles are abundant, the foliage is so badly damaged (Fig. 21.30) the plant dies. Flea beetles overwinter as adults under leaves, grass, and in other protected places. Beetles terminate their diapause in April. They feed on weeds before Migrating onto potatoes. The inconspicuous eggs are scattered in the soil around the plants and hatch after about a week (Chandel et al., 2011). The whitish larvae burrow into the soil and feed for 2e3 weeks on the rootlets within 3e8 cm of the surface. After spending about a week as a whitish pupa in the soil, the new adult emerges. There are generally one or two generations in a year.

FIG. 21.27 Adult beetle of Epilachna vigintioctopunctata.

FIG. 21.28 Grubs of Epilachna vigintioctopunctata.

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FIG. 21.29 Initial symptoms of flea beetle attack.

FIG. 21.30 Potato leaves severely damaged by flea beetles.

Control: Keeping down weeds around the fields is often the most important method of holding these pests in check, since the adults often feed on weeds in early spring and late fall, and the larvae may develop in great numbers on the roots of certain weeds. If the beetles get into the field and attack the plants in large numbers, they can be controlled by spraying malathion, endosulfan, or chlorpyriphos. Application of Bordeaux mixture with endosulfan gives excellent control of flea beetles in potato.

21.4.10 Blister beetle, Epicauta hirticornis Hagg Epicauta hirticornis (Coleoptera: Meloidae) are slender black beetles, about four times as long as wide, and are soft, with the head distinctly separated from the prothorax and the tip of the abdomen exposed beyond the tip of the elytra. Adults feed on the foliage (Fig. 21.31) and may be very damaging. They are very active and are usually found in large groups. The females lay their elongated yellow eggs in clusters of 100e200 in holes they make in the soil (Chandel et al., 2011). Newly hatched larvae burrow through the soil until they find a grasshopper egg mass. They then gnaw into the egg pod and feed on the eggs. During the next 3e4 weeks the larvae molt four times, with instars being very morphologically different from one another (a phenomenon known as hypermetamorphosis). Control: Where the beetles are very abundant, they may be controlled by spraying with chlorpyriphos or carbaryl. Bordeaux mixture acts as a repellent to the beetles and will give fair protection to potato vines. Blister beetles may be handcollected in polythene bags and emptied into a pan of kerosene.

21.4.11 Gray weevil, Myllocerus subfasciatus Guerin Myllocerus subfasciatus (Coleoptera: Curculionidae) has been reported from Tamil Nadu (Nair, 1975). Both larvae and adults cause damage. Adult feeding leaves notches on leaf margins, while larvae make small feeding holes in young tubers (Chandla, 1985).

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FIG. 21.31 Potato leaves damaged by blister beetles, Epicauta hirticornis.

The brown weevils lay about 500 eggs in soil. The egg hatches in about a week, and the grubs are fully fed in 2e2½ months. The grubs are small, white, and legless. They feed on roots. Pupation takes place in soil in earthen cocoons. The pupal period lasts from 10 to 12 days. Adults can be manually collected and mechanically destroyed. Spraying with dichlorvos or endosulfan is also effective.

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Puri, S.N., Baranwal, V.K., Surender, K., 1995. Cotton Leaf Curl Disease and its Management. NCIPM Extension Folder 1, National Centre for Integrated Pest Management, New Delhi, India.

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Rahman, K.A., 1944. Prevention of damage to stored potatoes by the potato tuber moth. Curr. Sci. 13, 133e134. Rai, K.M., Joshi, R., 1988. Control of white grubs (Kurmula) damaging potato crop in U.P. Hills Progress. Horticulture 20, 333e334. Raj, B.T., Parihar, S.B.S., 1993. Red ant damage on potato in western Uttar Pradesh. J. Indian Potato Assoc. 20, 61e62. Rana, R.K., 2011. The Indian potato processing industry: global comparison and business prospects. Outlook Agric. 40, 237e243. Rao, N.V., Reddy, A.S., 1989. Seasonal influence on the developmental duration of whitefly (Bemisia tabaci) in upland cotton (Gossypium hirsutum). Indian J. Agric. Sci. 59, 283e285. Reddy, A.S., Rao, N.V., 1989. Cotton whitefly (Bemisia tabaci Genn.). Indian J. Plant Protect. 17, 171e179. Regupathy, A., Palanisamy, S., Chandramohan, N., Gunathilagaraj, K., 1997. A Guide on Crop Pests. Sooriya Desktop Publishers, Coimbatore, India. Roonwal, M.L., 1976. Plant pest status of root eating ants, Dorylus orientalis with notes on taxonomy, distribution and habits (Insects: Hymenoptera). J. Bombay Nat. Hist. Soc. 72, 305e313. Saini, H.K., 1998. Effect of Synthetic Pyrethroids on Biology of Whitefly Bemisia tabaci (Gennadius) on Gossypium hirsutum (Linn.). MS thesis. Punjab Agricultural University, Ludhiana, India. Shah, N.K., Shah, L., 1990. Bionomics of Holotrichia longipennis (coleptera: Melolonthinae) in western Himalayas. Indian J. For. 13, 234e237. Shankar, U., Priya, S., Kumar, D., 2008. Vegetable Pest Management: Guide for Farmers. International Book Distributing Company, Lucknow, India. Sharma, P., Rishi, N., 2004. Population build-up of the cotton whitefly, Bemisia tabaci in relation to weather factors at Hissar, Haryana. Pest Manag. Econ. Zool. 12, 33e38. Sharma, P.L., Attri, B.S., Aggarwal, S.C., 1969. Beetles causing damage to pome and stone fruits in Himachal Pradesh and their control. Indian J. Entomol. 31, 377e379. Singh, S.P., 1987. Studies on some aspects of biology e ecology of potato cutworms in India. J. Soil Biol. Ecol. 7, 135e143. Singh, M.B., Bhagat, R.M., Sharma, D.C., 1990. Life history and host range of potato tuber moth (Phthorimaea operculella Zeller). Himachal J. Agric. Res. 16, 59e62. Singh, R.B., Khurana, S.M.P., Pandey, S.K., Srivastava, K.K., 1997. Screening germplasm for potato stem necrosis resistance. Indian Phytopathol. 51, 222e224. Singh, R.B., Khurana, S.M.P., Pandey, S.K., Srivastava, K.K., 2000. Tuber treatment with imidacloprid is effective for control of potato stem necrosis disease. Indian Phytopathol. 53, 142e145. Srivastava, K.P., Butani, D.K., 1998. Pest Management in Vegetables. Part I Periodicals and Book Publishing House, El Paso, Texas. Sushil, S.N., Mohan, M., Selvakumar, G., Bhatt, J.C., 2006. Relative abundance and host preference of white grubs (Coleoptera: Scarabaeidae) in Kumaon hills of Indian Himalayas. Indian J. Agric. Sci. 76, 338e339. Trivedi, T.P., Rajagopal, D., 1999. Integrated pest management in potato. In: Upadhayay, R.K., Mukeriji, K.G., Dubey, O.P. (Eds.), IPM System in Agriculture, Cash Crops, vol. 6. Aditya Books Pvt. Ltd., New Delhi, India, pp. 299e313. Trivedi, T.P., Rajagopal, D., Tandon, P.L., 1994. Environmental correlates of the potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Int. J. Pest Manag. 40, 305e308. Veersh, G.K., Kumar, A.R.V., Musthak Ali, T.M., 1991. Biogeography of pest species of white grubs of Karnataka. In: Veersh, G.K., Rajagopal, D., Viraktamath, C.A. (Eds.), Advances in Management and Conservation of Soil Fauna Oxford and IBP. Publishing Company Pvt Ltd., Bangalore, India, pp. 191e198. Verma, K.D., Chandla, V.K., 1999. Potato Aphids and Their Management. Tech. Bull. (No. 26). CPRI, Shimla, India. Woodhouse, E.J., 1912. Potato moth in bengal. Indian Agric. J. 7, 264e271. Yadava, C.P.S., Sharma, G., 1995. Indian White Grubs and Their Management. Tech. Bull. (No. 2) All India Coordinated Research Project on White Grubs, Jaipu, India.

Chapter 22

Australia and New Zealand Paul Horne and Jessica Page IPM Technologies Pty Ltd, Hurstbridge, VIC, Australia

22.1 Overview of the industry Potatoes are produced in all States of Australia, with the largest production in the south-eastern states of Victoria, South Australia, and Tasmania. There are differences in the type of potatoes grown in these areas targeting fresh (ware), processing (crisping and French fries), or seed markets. There are many family farms and some that began as family farms but have developed into large corporate operations, often with smaller farms supplying potatoes to them for packaging. Details are presented in Table 22.1. South Australia (SA) is the largest producer of fresh potatoes, with 80% of the national crop. Overall, processing potatoes account for 56% of national production (www.potatoessa.com.au). Certified seed potatoes are grown primarily in Victoria and Tasmania, but there are also significant seed production operations on Kangaroo Island (SA), near the SA e Victoria border, as well as in New South Wales and Western Australia. Potatoes are the most valuable horticultural crop grown in Australia as measured by total value of production (around Aus$717 million in 2016e17). However, with their price per tonne being significantly lower than those of many other vegetable crops, this is mostly due to the large number of tonnes produced (AusVeg data). Total potato production is estimated to be around 1.4 million tonnes, of which processing potatoes make up the biggest portion, of around 900,000 tonnes per year (Table 22.1). In New Zealand, over 200 growers produce around half a million tonnes of potatoes per annum, but there are big differences in regions producing for different sectors. Seed production and growers producing for a large transnational food processor McCain Co. are all in the South Island, while growers producing for a New Zealand potato processor Mr. Chips Ltd. are based in the North Island. Significant production areas of both processing and ware potatoes are around Pukekohe (Auckland area), Hawkes Bay and Manawatu in the North Island and on the Canterbury Plain in the South Island. The growing area is around 10,500 ha (Potatoes NZ website; https://potatoesnz.co.nz/).

22.2 Main pests The main pests of potatoes in Australia and New Zealand are introduced species that are found in most production areas of the world such as potato tuber moth (Phthorimaea operculella (Zeller)) and green peach aphid (Myzus persicae (Sulzer)) (Anderson and Ogden, 2017; Horne and Page, 2008). There are also minor pests that can be locally of concern, including species that are native to Australia. Colorado potato beetle (Leptinotarsa decemlineata (Say)) does not occur in Australia and New Zealand as of 2020. Tomato-potato psyllid (Bactericera cockerelli (Sulc)) is found in New Zealand and Western Australia but not in the eastern states of Australia. The major pests that are encountered in Australian potato crops are Phthorimaea operculella (Zeller), Helicoverpa armigera (Hubner), green peach aphid (Myzus persicae), potato aphid (Macrosiphum euphorbiae (Thomas)), onion thrips (Thrips tabaci Lindeman), tomato thrips Frankliniella schultzei (Trybom), western flower thrips (F. occidentalis Pergande), whitefringed weevil (Naupactus leucoloma Boheman) (all exotic species to Australia), looper caterpillars (Chrysodeixis argentifera (Guenee) and C. eriosoma (Doubleday)) and potato wireworm (Hapatesus hirtus Candeze), but there are many other minor, local or infrequent pests which include species native to Australia (Horne and Page, 2008; Horne et al., 2002). For example, potato wireworm in Australia is different to species of potato wireworm elsewhere in the world and has a very different life-history. Horne and Horne (1991) estimated that juvenile stages might live for 7 years Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00015-9 Copyright © 2022 Elsevier Inc. All rights reserved.

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TABLE 22.1 Production of potatoes in Australia. Region

Number of potato producers

Potato production (area/tonnes)

1. Gippsland, VIC

50 businesses - certified seed, processing, fresh market and crisping growers

2. Ballarat, VIC

50 businesses - certified seed, processing, fresh market and crisping growers

3. Kinglake, VIC

1 certified seed business

4. Murray, VIC

10 businesses

5. Mt Gambier, SA Portland, VIC

14 businesses mainly processing; also certified seed producers

5,000 ha

6. Virginia, SA

6 large farms þ 25 smaller producers who generally supply them; fresh and small quantity crisping

1,000 ha

7. Mallee/Riverland, SA

2 large farms þ 20 producers who generally supply them

5,000 ha

8. Kangaroo Island, SA

8 certified seed producers

400 ha

12,000 tonnes

9. North West Coast and Northern, TAS

200 processing growers approx. 30 certified seed producers

6,900 ha 520 ha

400,000 tonnes 26,000 tonnes

10. Riverina, NSW 11. Tablelands, NSW

10 businesses e certified seed, fresh and processing

12. Atherton Tableland, QLD

7,600 ha 236,700 tonnes

11,000 ha 360,000 tonnes (SA)

4,100 ha 110,800 tonnes 3,468 ha 97,578 tonnes

13. Bundaberg, QLD 14. Lockyer Valley, QLD 15. Perth/Myalup/Busselton/ Manjimup, WA

78 growers Half is fresh, half split between seed, processing and export.

1,900 ha 84,800 tonnes

Based on information provided by Australian Horticulture Statistics Handbook, 2018/19; Industry leaders and representatives.

before pupating and developing into adults. Other pests that can be of local concern include Rutherglen bug (Nysius vinitor Bergroth) which can fly in to crops in large numbers and cause leaf-scorching or damage to growing tips and brown leafhoppers (Orosius argentatus (Evans)) which can vector several phytoplasma diseases including purple-top wilt. Wingless grasshoppers (Phaulacridium vittatum (Sjöstedt)) can be locally severe when they move from drying pastures and grasslands into irrigated potato crops. Tomato-potato psyllid (Bactericera cockerelli (Sulc)) was first detected in New Zealand in 2006 and then in Western Australia in 2017. For more information on this insect, please see Chapter 6. Control of this pest in New Zealand has caused significant increases in insecticide use. Prior to the arrival of this pest, aphids and potato tuber moth were the main pests, but now the tomato-potato psyllid is of equal concern. This species is a vector of the bacteria Candidatus Liberibacter solanacearum (LSO) which causes “zebra-chip” in processing potatoes as well as serious yield reductions. In Western Australia, the tomato-potato psyllid has not been found to cause direct economic losses, and so far the major economic impact to potato growers has been caused by quarantine requirements which initially restricted trade. The eastern states of Australia are so far free of this pest. Although the tomato-potato psyllid is present in Western Australia, so far there has been no detection of Liberibacter (LSO) which is unique in the world. Pests of potatoes can be categorized into either soil dwelling or foliar pests and the foliar pests can be divided into those causing either direct damage or acting as virus vectors. There are several species of beetles that are of concern as pests of potatoes in Australia, including potato wireworm (H. hirtus), African black beetle (Heteronychus arator F.), whitefringed weevil (N. leucoloma), red-headed pasture cockchafer (Adoryphorus couloni (Bermeister)) and garden weevil (Phlyctinus callosus (Schönherr)). It is the larval stages of these beetles that damage potatoes as they feed on tubers. However, H. arator adults can also damage plants by feeding on the stems at or just below ground level. All of these species have life cycles of 1 year or more, and H. hirtus is estimated to spend up to 7 years at the larval stages (Horne and Horne, 1991).

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Potato tuber moth is a pest in over 90 countries (Kroschel and Lacey, 2008; Rondon, 2010), including Australia and New Zealand (Horne and Page, 2008; Hermann, 2008b), where it was first recorded as a pest of potatoes (Berthon, 1855). It is important in the final stages of production where caterpillars can burrow into tubers before they are harvested. The highest risk of damage occurs when tubers are harvested during hot dry summers. It is not usually a problem after harvest because potatoes are kept in refrigerated storage facilities. This is very different from many developing countries where cool stores are not readily available and post-harvest damage by the potato tuber moth is a serious problem. For more information on this pest, see Chapter 8. Looper caterpillars (Ch. argentifera and Ch. eriosoma) can cause damage to potato plant leaves, but it is usually minor. Chrysodeixis eriosoma is cosmopolitan, while Ch. argentifera is found mainly in Australia and New Zealand. Chrysodeixis eriosoma has been recorded as feeding on a wide range of plant species and has been considered a serious horticultural pest in the past (Roberts, 1979). Similar damage can be caused by two species of Helicoverpa (still often commonly referred to as Heliothis): Helicoverpa punctigera and H. armigera. Unless numbers are particularly high, insecticide applications are normally not required. Wingless grasshoppers (Ph. vittatum) can migrate into potato crops in Australia from adjacent pastures or grasslands and can cause significant damage to foliage when in high numbers. However, crop destruction is usually localized to field perimeters (Capinera, 2008; NSW DPI, 2017). Rutherglen bug (N. vinitor) is a native Australian lygaeid bug that can invade crops in the hotter months of the year. Numbers can be extremely high in some years, depending on the weather and abundance of preferred non-crop plants (Horne et al., 2002). Damage occurs to growing tips and plants can look scorched as a result. Plants can tolerate the pest in most years in most locations but may require treatment with insecticides in some years. Green vegetable bug (Nezara viridula (L.)) and small potato bug (Cuspicona simplex (Walker)) are minor pests of potatoes in Australia (Clarke, 2007). Nezara viridula is an introduced pest but C. simplex is native to Australia (Martin, 2018b). Both species also occur in New Zealand (Anderson and Ogden, 2017; Martin, 2018a). Several native species of Miridae can also feed on potatoes, causing minor distortion in growing tips and subsequent small holes in leaves. Several species of cosmopolitan aphids are also pests of potatoes in Australia and New Zealand (Persley, 2012; Anderson and Ogden, 2017). The most common are green peach aphid (M. persicae) and potato aphid (M. euphorbiae), but foxglove aphid (Aulacorthum solani (Kaltenbach)) can also breed in potato crops. As is the case in other parts of the world, these are of concern as vectors of viruses such as leaf-roll virus and potato virus Y (PVY). Other species of aphids found in cereal crops can also occur as winged adults in potato crops when they are migrating. More information on aphids that affect potatoes can be found in Chapter 5. Three species of introduced thrips: western flower thrips (F. occidentalis), onion thrips (Th. tabaci), and tomato thrips (F. schulzei) are of concern in Australian potato crops as vectors of tomato spotted wilt virus (Horne and Wilson, 2000). A native Australian species, plague thrips (Thrips imaginis Bagnall) can also occur in very high numbers as the name suggests. This species does not vector this disease. However, potato growers usually do not identify thrips to a species and assume that all thrips vector tomato spotted wilt virus, which can result in unnecessary and disruptive applications of insecticides.

22.3 Control methods Control methods for insect pests can either rely on insecticides or follow the Integrated Pest Management (IPM) approach. The arrival of TPP in New Zealand has resulted in a significant increase in insecticide use on potato crops specifically targeting TPP (Anderson et al., 2013). Anderson et al. (2013) reported that “The current commercial insecticide program for TPP control in northern New Zealand typically involves the application of ‘blocks’ of two to four applications of different mode of action (MoA) insecticides every 7e10 days from about mid-December onwards”. Many of these insecticides, which include organophosphates, synthetic pyrethroids and neonicotinoids, kill biological control agents of both TPP and other pests such as potato tuber moth, thus preventing successful IPM. In Australia, this has not been the case. Therefore, a considerable percentage of potato production in Australia is grown using IPM. As with an IPM strategy in any crop, IPM in potatoes relies on biological control agents and cultural methods as the primary controls, supported by selective pesticides, but only when necessary (see also Chapter 27). Broad-spectrum insecticides, such as synthetic pyrethroids, organophosphates, and others are avoided as foliar sprays. A range of native and introduced natural enemies of pests are used in IPM strategies. These include both predators and parasitoids (Horne et al., 2002). The most important of the predators are species that are native to Australia and New Zealand, and include the following: damsel bugs (Nabis kinbergii Reuter), pentatomid bugs (Oechalia schellembergii Guerin-Meneville), brown lacewings (Micromus tasmaniae Walker), ladybird beetles Coccinella transversalis (Fabricius), Hippodamia variegata

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PART | IV Problems and solutions in major potato-producing areas of the world

(Goeze) and Harmonia conformis (Boisduval) and red and blue beetles (Dicranolaius bellulus (Guerin-Meneville)). Hoverflies (Syrphidae) are also important in control of aphids. There are many parasitoids of potato pests, and these include native species that attack the native pests, and also (in Australia) introduced species such as Orgilus lepidus Muesebeck, Apanteles subandinus Blanchard and Copidosoma koehleri Annecke and Mynhardt that parasitize potato tuber moths (Horne, 1990, 1993). The impact of these parasitoids was previously reported (Callan, 1974; Briese, 1981) to be less than estimated by Horne (1990, 1993), but those earlier reports did not take into account the impact of insecticide applications. Ten species of parasitoids have been introduced into Australia as biological control agents of potato tuber moth, but these three species are the most important (Waterhouse and Sands, 2001). They were also introduced into New Zealand but only Apanteles subandinus became established (Hermann, 2008a). Parasitoids that attack aphids are also very common and include species such as Aphidius colemani Viereck. Waterhouse and Sands (2001) state that “several exotic parasitoids have been recorded from M. persicae in Australia.” In our experience A. colemani is extremely important in control of aphids in potatoes in Australia (Horne and Page, unpublished data). Parasitism can be easily overlooked or underestimated by growers and advisors because the adult parasitoids are often small, highly mobile, and difficult to see, while the larval stages are hidden in the bodies of their hosts. Control of soil dwelling pests is accomplished largely by cultural and chemical methods. Cultural controls include rotation (avoiding legumes prior to potatoes if whitefringed weevil is a concern), weed control, including pasture management where redheaded pasture cockchafers are an issue. Soil-applied insecticides before planting is a common method of dealing with these pests, but insecticide-treated seed potato pieces can be used as a bait for potato wireworm control. A key cultural control method for pests that vector disease begins with clean seed at planting, which means using certified seed where possible. To ensure good quality seed, there are several organizations that provide certified seed in the different states of Australia. These organizations established the Australian Seed Potato Council (ASPC) in 2013, which is a collaboration of all seed certification authorities in Australia with representation of seed growers and buyers. The ASPC sets minimum standards for seed potatoes in Australia, but there is allowance for variation between the states. All of the seed potato certification programs aim to provide tubers that growers can be confident have minimal levels of viral and other diseases. Standards are updated as technology changes and the last review was in 2016 (https://www.horticulture. com.au/globalassets/laserfiche/assets/project-reports/pt.15004/pt.15004-final-report-6353.pdf). Other important cultural controls, for seed growers in particular, to minimize the impact of disease vectors (particularly aphids and thrips) include isolation from other potato crops, removal of volunteer potatoes, and proper handling and cutting of seed tubers. Biological control agents, as listed above, provide significant control of aphids and potato tuber moth when broadspectrum insecticides are avoided. This is described by a grower in a recent (2019) article in Potatoes Australia (a potato industry magazine), where he described his experience of using IPM which uses such biological control agents, starting in 1995 (https://ausveg.com.au/app/uploads/publications/PA%20Feb%20Mar%202019%20Web.pdf). His conclusion to the article is the most telling, where he states, “In the last 20 years I have used fewer insecticide applications on all paddocks than I might have used in a single season per crop before IPM”. Previously he would have applied insecticide sprays approximately every 14 days on each crop. In addition to the contribution of biological control agents, cultural controls such as overhead irrigation and soil preparation are important in helping prevent potato tuber moth caterpillars from reaching tubers under the ground. The use of rollers may also be possible (depending on soil type) to restore soil cover by breaking up cracked potato hills. There is a range of insecticides registered for use on potato crops in Australia and New Zealand. However, there are differences between the countries, and also between Australian states, as to what products are available. The products that can be used include broad-spectrum insecticides and those that will kill some beneficial species but not others, as well as highly selective products that will kill the target pests with minimal to no impact on beneficial species. Therefore, growers can choose to use an insecticide-based approach or an IPM approach that incorporates biological control agents and insecticides as well as suitable cultural controls. The key element is for growers to have access to information about the impact of insecticides on the key biological control agents of importance in their crops at any time. This information is not always easy to find but some sites such as www.biologicalresearchcompany.com.au do now offer such information for a range of crops, including potatoes. An example of an IPM approach used in Australia incorporating such information can be seen in Chapter 27 of this volume and in Horne and Page (2008). The same generalist predators listed above that feed on aphids and potato tuber moth are also predators of tomatopotato psyllid in New Zealand (MacDonald et al., 2016). Their impact on this species, as well as on aphids, and potato tuber moth depends on the type of insecticides applied and so their importance varies depending on whether or not an IPM strategy is being used.

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Acknowledgments We thank the following people for their assistance with information about the potato industry in Australia and New Zealand: Iain Kirkwood (Potatoes NZ), Les Murdoch (Simplot Australia), Robbie Davis (Potatoes SA), Nigel Crump (AuSPICA) and Wayne Tymensen. We also thank Janet Horne, Rebecca Addison, and Prof Andrei Alyokhin for comments on the manuscript.

References Anderson, J.A.D., Walker, G.P., Alspach, P.A., Jeram, M., Wright, P.J., 2013. Assessment of susceptibility to zebra chip and Bactericera cockerelli of selected potato cultivars under different insecticide regimes in New Zealand. Am. J. Potato Res. 90, 58e65. Anderson, S., Ogden, S., 2017. Handbook of Pests and Diseases for New Zealand Potato Growers, second ed. Potatoes New Zealand, p. 128. Berthon, C.H., 1855. On the potato moth. Proceed. R. Soc. Van Diemen’s Land 3, 76e80. Briese, D.T., 1981. The incidence of parasitism and disease in field populations of the potato moth Phthorimaea operculella (Zeller) in Australia. J. Aust. Entomol. Soc. 20, 319e326. Callan, E.C., 1974. Changing status of the parasites of potato tuber moth Phthorimaea operculella (Lepidoptera: Gelechiidae) in Australia. Entomophaga 19, 97e101. Capinera, J.L., 2008. Grasshopper and locust pests in Australia. In: Capinera, J.L. (Ed.), Encyclopedia of Entomology. Springer, Dordrecht. https:// doi.org/10.1007/978-1-4020-6359-6_1164. Clarke, A.R., 2007. Current distribution and pest status of Nezara viridula (L.) (Hemiptera: Pentatomidae) in Australia. Aust. J. Entomol. 31, 289e297. Hermann, T.J.B., 2008a. Biological control of potato tuber moth by Apanteles subandinus Blanchard in New Zealand. In: Kroschel, J., Lacey, L. (Eds.), Integrated Pest Management for the Potato Tuber Moth, Phthorimaea operculella (Zeller) e a Potato Pest of Global Importance. Margraf Publishers, Weikersheim, Germany, pp. 73e80. Hermann, T.J.B., 2008b. Integrated Pest Management of potato tuber moth in New Zealand. In: Kroschel, J., Lacey, L. (Eds.), Integrated Pest Management for the Potato Tuber Moth, Phthorimaea operculella (Zeller) e a Potato Pest of Global Importance. Margraf Publishers, Weikersheim, Germany, pp. 119e126. Horne, P.A., 1990. The influence of introduced parasitoids on potato moth Phthorimaea operculella (Zeller) in Victoria, Australia. Bull. Entomol. Res. 80, 159e163. Horne, P.A., 1993. Sampling for the potato moth (Phthorimaea operculella) and its parasitoids. Aust. J. Exp. Agric. 33, 91e96. Horne, P.A., Horne, J.A., 1991. The biology and control of Hapatesus hirtus Candeze (Coleoptera: Elateridae) in Victoria. Aust. J. Agric. Res. 42, 827e834. Horne, P., DeBoer, R., Crawford, D., 2002. Insects and Diseases of Australian Potato Crops. Melbourne University Press, p. 80. Horne, P., Page, J., 2008. Integrated pest management dealing with potato tuber moth and all other pests in Australian potato crops. In: Kroschel, J., Lacey, L. (Eds.), Integrated Pest Management for the Potato Tuber Moth, Phthorimaea operculella (Zeller) e a Potato Pest of Global Importance. Margraf Publishers, Weikersheim, Germany, pp. 111e117. Horne, P., Wilson, C., 2000. Thrips and tomato spotted wilt virus e on the increase: situation report. In: Proceedings of the Potatoes 2000 Conference, pp. 103e106. Kroschel, J., Lacey, L.A., 2008. Preface. In: Kroschel, J., Lacey, L. (Eds.), Integrated Pest Management for the Potato Tuber Moth, Phthorimaea operculella (Zeller) e a Potato Pest of Global Importance. Margraf Publishers, Weikersheim, Germany. MacDonald, F.H., Connolly, P.G., Larsen, N.J., Walker, G.P., 2016. The voracity of five insect predators on Bactericera cockerelli (Sülc) (Hemiptera: Triozidae) (tomato potato psyllid; TPP). N. Z. Entomol. 39, 15e22. Martin, N.A., 2018a. Green Vegetable Bug - Nezara Viridula Fact Sheet. Landcare Research. https://nzacfactsheets.landcareresearch.co.nz/factsheet/ InterestingInsects/Green-vegetable-bug—Nezara-viridula.html> (Accessed on 23 July 2021). Martin, N.A., 2018b. Green Potato Bug - Cuspicona Simplex Fact Sheet. Landcare Research. https://nzacfactsheets.landcareresearch.co.nz/factsheet/ InterestingInsects/Green-potato-bug—Cuspicona-simplex.html> (Accessed on 23 July 2021). New South Wales Dept. of Primary Industries, 2017. Wingless Grasshoppers. Fact Sheet. www.dpi.nsw.gov.au/__data/assets/pdf_file/0007/204577/ Wingless-grasshoppers.pdf (Accessed on 23 July 2021). Persley, D., 2012. Integrated Viral Disease Management in Vegetable Crops. Report to Horticulture Australia. Available at: https://ausveg.com.au/app/ data/technical-insights/docs/120029_VG07128_pdf_file_3719.pdf> (Accessed on 23 July 2021). Roberts, L., 1979. Biology of Chrysodeixis eriosoma (Lepidoptera: Noctuidae) in New Zealand. N. Z. Entomol. 7, 52e58. Rondon, S.I., 2010. The potato tuberworm: a literature review of its biology, ecology and control. Am. J. Potato Res. 87, 149e166. Waterhouse, D.F., Sands, D.P.A., 2001. Classical biological control of arthropods in Australia. ACIAR Monogr. 77, 560.

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Chapter 23

Management of potato pests and diseases in Africa Joseph E. Munyanezaa and Benoit Bizimungub a

United States Department of Agriculture, Agricultural Research Service, Office of National Programs, Crop Production and Protection, Beltsville,

MD, United States; bAgriculture and Agri-Food Canada, Fredericton Research and Development Centre, Fredericton, NB, Canada

23.1 Overview Potato arrived relatively late in Africa, compared to other parts of the world. However, its production and popularity has increased in the past few decades, rising from two million tons in 1960 to a record 24 million tons in 2018. According to FAO statistics, Africa has had one of the most rapid potato production expansion in recent years (http://www.fao.org/ faostat/en/#data). Potato is seen as a potential crop for enabling smallholder farmers to attain food security and as an important source of income (Belay et al., 2021). It is cultivated under a wide range of regions and productions systems, from irrigated commercial farms in northern Africa and South Africa to small subsistence farms in tropical highland zones of subSaharan Africa. Because potato does not perform well under conditions of high temperature, in the tropics it is grown in the cool highlands, whereas in the subtropics, it is grown during the cool season (winter, autumn, or spring) or at midelevations (Hijmans, 2001). A recent study focusing on East and Central Africa indicated that the long-term upward trends in production and area harvested contrast with the sharp decline in the growth rates for output, area planted, and yields over the last decade. The study also pointed out the emerging changes in fresh markets and processed products (French fries and chips) to meet the growing need of urban consumers (Scott et al., 2013). With increasing urbanization and population growth in many parts of Africa, potato processing, especially French fries manufacture, is expected to become particularly popular. Analysis of trends in consumption shows that the frozen French fry industry has potential for further growth and that industry expansion is limited by the shortage of suitable raw potato stock linked to lack of suitable cultivars (Ngobese and Workneh, 2017). Recent figures of potato production areas and harvested crop are presented in Table 23.1. Production and yield vary greatly according to countries, growing conditions, size of the farm and level of inputs. The level of sophistication of the production system also varies considerably depending on whether production is on a commercial farm or on a small subsistence farm. However, in many parts of subSaharan Africa, potato is generally produced under rain-fed conditions on small farms with low agricultural inputs as staple food and source of income (Scott, 2021). There are many small-scale potato growers who produce for home consumption and local markets using variable levels of inputs such as improved seed, nutrients, or irrigation water. A combination of interacting yield limiting factors contributes to low yields obtained on farmers’ field (Franke and Sekoboane, 2021). The average potato yield is estimated at 16 T/Ha, although a much higher yield is potentially achievable. A recent survey study by Harahagazwe et al. (2018) indicated that potato farmers across subSaharan Africa could increase their production by 140% if they had access to high quality seed along with improved pest and disease management practices. The survey revealed that poor quality seed and bacterial wilt were the main yield gap drivers between research plots and farmers’ fields. The availability of agricultural inputs, lack of well-established value-chain, short rotations or continuous potato cropping have often been cited among constraints faced by potato growers in Africa. Other factors contributing to low crop productivity include poor soil fertility and nutrient imbalance and depletion resulting from continuous potato cropping (Ngobese and Workneh, 2017, Nduwamungu and Gaidashova, 2019; Nyawade et al., 2019; Nyongesa, 2019).

Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00016-0 Crown Copyright © 2022, Published by Elsevier Inc. All rights reserved. Joseph Eulade’s contribution is in public domain.

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TABLE 23.1 Potato acreage (hectares) and production (tons) in Africa in 2018. Country

Ha

T

Algeria

149,665

4,653,322

Angola

131,403

806,552

Burkina Faso

752

e

Burundi

27,097

302,665

Cameroon

20,449

302,706

Central African Republic

1578

e

Chad

4237

41,583

Democratic Republic of the Congo

22,002

101,398

Egypt

176,670

4,896,476

Ethiopia

66,933

743,153

Guinea

11,753

151,326

Lesotho

7640

130,602

Libya

17,918

348,361

Madagascar

43,435

257,379

Malawi

68,133

1,125,874

Mali

13,689

310,902

Mauritius

719

17,033

Morocco

62,033

1,869,149

Mozambique

18,022

273,335

Namibia

1201

14,520

Niger

5672

168,569

Nigeria

371,341

1,363,358

Rwanda

92,800

847,302

Senegal

3356

79,499

South Africa

68,277

2,467,724

Sudan

35,584

442,988

Swaziland

4035

e

Tanzania

190,053

1,768,154

Tunisia

25,082

423,800

Uganda

37,754

162,151

Zambia

1809

13,546

Zimbabwe

3538

60,521

Adapted from FAOSTAT, http://www.fao.org/faostat/en/#data.

Besides constraints related to cropping systems, several endemic pests and diseases are additional important limiting factors to potato productivity in Africa, especially aphid-vectored viruses, soil-borne nematodes, tuber moth and leafminers, as well as late blight and bacterial wilt diseases (Fuglie, 2007; Chilipa et al., 2021). In contrast to developed countries where pest and disease management rely heavily on the use of certified disease-free seed potatoes along with chemical and cultural controls, many subSaharan Africa countries use informal seed systems as they face limited availability of and access to agricultural inputs. Therefore, breeding disease and pest resistant varieties adapted to different environmental conditions is an important component of management measures that could greatly benefit both smallholder

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and commercial farmers in Africa (Krüger and van der Waals, 2020). Improved storage facility and better marketing opportunity are also considered crucial needs for farmers to potentially reduce postharvest waste and improve potato production systems in Africa (Ayalew, 2014; Ait-Oubahou, 2013). This chapter discusses important potato pests and diseases and their management in Africa, with emphasis on subSaharan Africa.

23.2 Potato pests and diseases The sustainability of potato production globally, and particularly in developing countries, is threatened by adverse abiotic and biotic factors. In Africa, pests and diseases are major biotic constraints severely affecting potato yield and tuber quality. In this part of the world, potato yield losses due to pest and disease attacks can be as high as 100% depending on crop tolerance level, climatic conditions, soil, type of pests and diseases. In subSaharan Africa in particular, where most potato crops are produced by small-scale or subsistence farmers, not only information on accurate identification of pests and diseases is not readily available, but also management tools are lacking. This makes it difficult, if not impossible, for growers to compartmentalize problems into pest and disease types while trying to practice integrated pest management (IPM). Therefore, unlike most of the chapters in this book, we will address both pests and diseases, including insects and nematodes. This will allow potato producers in Africa to find the information in one place, thereby allowing them to make timely and more effective management strategies based on informed decisions when confronted with pest and disease challenges.

23.2.1 Insect pests Insect pests are major biotic factors affecting potato yields and tuber quality worldwide (Munyaneza et al., 2007; Munyaneza, 2012, 2015; Munyaneza and Henne, 2013; Kroschel et al., 2020). The global tendency for excessive pesticide use to control insect and other arthropod pests is costly, of high human and environmental health concern, and is expected to get further exacerbated through impacts of climate change and increase in international trade. In Africa, the major insect pests of potato are the potato tuber moth, aphids, and the pea leafminer. Minor and sporadic insect pests include loopers, cutworms, armyworms, thrips, and spider mites (Nderitu, 1991; Otieno, 2019; Were et al., 2013; Mwesige et al., 2019).

23.2.1.1 Potato tuber moth The potato tuber moth or potato tuberworm, Phthorimaea operculella, originated in the tropical mountainous regions of South America. Currently, this insect has a worldwide distribution and is considered the most damaging potato pest in the developing world. It is present in almost all tropical and subtropical regions of the world, in North, Central, and South America, Africa, Asia, Australia, and Europe. For detailed discussion of this pest, please refer to Chapter 8. Potato tuber moth is the most important pest affecting production of potatoes in warm and dry conditions experienced in many parts of Africa (Nderitu, 1991; Otieno, 2019). The attack begins from the field and proceeds into the storage. This insect pest attacks potato by mining the leaves and stems and by feeding on the tubers. Mines are the typical symptoms of leaf damage caused by the larvae eating the mesophyll without damaging the upper and lower epidermis. When the foliage dies, the larvae enter the soil through cracks where they may eventually find and feed upon tubers. Larvae enter potato tubers via the eyes and continue to bore or tunnel through the tuber just below the skin. Larval excrements are pushed out through the holes, which can be observed immediately after larvae start their mining activity. The excrements in the tunnels also attract fungal and bacterial growth, leading to further infections and damage, while the holes created provide secondary infection-entry points for pathogens. Under heavy field infestation, potato foliage can be destroyed, which can result in substantial yield loss of up to 100%. High foliar infestations early in the season can affect tuber yield. However, the most devastating yield losses are largely a result of earlier tuber infestation in the field, generally where moths have laid eggs through soil cracks on the developing tubers, or when harvest is delayed. Potato tuber moth also damages harvested potato tubers in storage. The destruction of potatoes in rustic stores can be complete within a few months if the tubers are left untreated. Infested tubers are unsuitable not only for human consumption but also for use as seed. Infested tubers produce smaller yields and initiate a fast development of a new field potato tuber moth population (Clough et al., 2010; Ahmed et al., 2013; Otieno, 2019; Kroschel and Schaub, 2013; Kroschel et al., 2020).

23.2.1.2 Aphids Aphids are major pests of potato and other crops worldwide (Saguez et al., 2013; see also Chapter 5), including Africa. Important aphid species commonly found on potato in Africa include green peach aphid (Myzus persicae), potato aphid

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(Microsiphum euphorbiae), cotton or melon aphid (Aphis gossypii), black bean aphid (Aphis fabae), and foxglove or glasshouse-potato aphid (Aulacorthum solani) (Nderitu, 1991; Were et al., 2013; Otieno, 2019). Green peach aphid and potato aphid are the two most important species and are extremely polyphagous, being capable of feeding on several hundred plant species (Radcliffe and Ragsdale, 2002; Alvarez et al., 2003; Saguez et al., 2013). Aphids can damage potato plants directly by feeding on sap, and indirectly by transmitting various viral diseases. Continuous sucking of sap by large numbers of aphids considerably weakens and slows plant development, even leads to plant death (aphid holes). Removing sap and injecting toxic saliva causes leaf deformation. The weakened plant produces low quality tubers. During feeding, aphids excrete honey dew which promotes growth of a sooty black mold on plant leaves or stems, hence reducing the photosynthetic area for the plant. However, the by far most important damage caused by aphids in potato is transmission of viral diseases which cause serious losses to potato crops (Radcliffe and Ragsdale, 2002; Alvarez et al., 2003; Srinivasan et al., 2013; Kroschel et al., 2020). Potato leafroll virus (PLRV) and potato virus Y (PVY) are considered the most economically important aphid-transmitted potato viruses and will be discussed in Section 23.2.3 of this chapter.

23.2.1.3 Leafminers Leafminers (Liriomyza spp.) are polyphagous fly pests causing severe damage to potato and several other crops (Mujica, 2016; Weintraub et al., 2017; Kroschel et al., 2020). The pea leafminer, Liriomyza huidobrensis, is one of the most damaging leafminers worldwide. Endemic to South America, this pest has recently spread to many countries around the world, presumably in association with the global trade of ornamental and other horticultural plants (Mujica et al., 2016; Weintraub et al., 2017; Kroschel et al., 2020). In Africa, pea leafminer has been reported in several countries, including Kenya, Rwanda, Uganda, Tanzania, South Africa, Union of the Comoros, Mauritius, Morocco, Reunion, Seychelles, and Morocco (Kroschel et al., 2020; Mujica et al., 2016; Mwesige et al., 2019). Both adults and larvae of pea leafminer damage the plant foliage. Adults cause damage by puncturing the leaf surface to feed on the leaf tissue and to lay eggs. Newly hatched larvae mine into the leaf and feed on the chloroplast-rich mesophyll, making a serpentine mine whose diameter increases as the larva grows. A large proportion of grown larvae remain close to the midrib. Once feeding is completed, mature larvae cut a slit in the leaf surface, exit the leaf, and drop to the ground where they pupate. Leaf tissue affected by larval mining becomes necrotic and brownish. Plant injuries caused by adult and larval activities reduce photosynthesis activity and cause leaf wilting. Highly infested crop fields appear burned (Cisneros and Mujica, 1999). Potato yield losses of up to 100% have been reported in several countries, including Argentina, Chile, Indonesia, and Uganda (Cisneros and Mujica, 1999; Mwesige et al., 2019). This insect is notoriously known to rapidly develop resistance to insecticides. Leafminer populations vary with season and temperatures. Environmental conditions in Africa are favorable to pea leafminer, posing an emerging high risk for potato production areas of most countries of East, Central, and Southern Africa (Mujica et al., 2016). Ecological and economical sound control of this leafminer fly is best realized when based on integrated pest management that promotes natural enemies, in combination with cultural and physical control.

23.2.1.4 Loopers Loopers (Trichoplusia spp.) feed on several crops, including crucifers and potato. Larvae are greenish, white-stripped, and variable in size. The adult moths are gray-brown miller moths. Loopers are named so because of their larval looping, wobbly movement. The middle of the larvae is characteristically humped when the insect rests or moves. Loopers usually stay on the underside of the leaves. Feeding injury is within the margin of the leaf and consists of round to oval holes with even borders. Damage to potato is not usually of economic importance (Alvarez et al., 2003).

23.2.1.5 Cutworms Several species of cutworms (Agrotis spp.) feed on potatoes. All these species are long and smooth appearing as larvae. They range in various shade of color from gray to brownish to black, sometimes striped. Feeding occurs at night, while during the day cutworms hide under dirt clods. Adults are miller moths ranging from brown to silver in color. Unlike loopers, cutworms may cut off stems or strip the leaves, most often on the margins of the field. Damage is occasionally of economic importance. The impact of cutworms is high during droughts and in new and succulent sprouts. Due to their sporadic nature, the impact is not easily quantified. However, under heavy infestation, yield loss of about 20%e37% has been reported (Alvarez et al., 2003; Otieno, 2019; Kroschel et al., 2020).

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23.2.1.6 Armyworms Armyworms (Spodoptera spp.) feed on a wide range of crops and are important pests, especially for cereals. However, they have also been reported to feed on potato in absence of the primary hosts. The fall armyworm (Spodoptera frugiperda) is an emerging threat to agriculture in many parts of Africa (Goergen et al., 2016; Baudron et al., 2019). Armyworms are mainly forage feeders and feed during the day, do not make burrows, and may migrate in mass into potato fields from adjacent crops. They also feed on tubers that are exposed on the surface or accessible through cracks in the soil. Armyworms can cause up to 100% crop defoliation of potato plants. Some defoliation from armyworms can be tolerated. Keeping defoliation between 10%e15% will generally prevent yield losses (Alvarez et al., 2003; Kroschel et al., 2020).

23.2.1.7 Thrips Thrips are tiny, light brown or black insects that feed at night. Three species of thrips are of economic importance as pests of potato. The western flower thrips (Frankliniella occidentalis) originated in western North America and has since become a major pest on many crops across the United States and around the world. Also, the onion thrip (Thrips tabaci) is thought to have originated in the Mediterranean region but is now worldwide spread, including in Africa. In addition, the cotton thrips (Frankliniella schultzei) is commonly found on potato in Africa (Nyasani et al., 2012; Otieno, 2019). Thrips are minor pests of potato but can cause major damage mainly during dry climatic conditions. Potato leaves develop a silver or chlorotic dotting of the tissues and become curly under heavy feeding. The silver color is due to the sucking of plant sap from soft tissues and emptying of the cells. Some species are vectors of viruses, including tomato spotted wilt virus, with western flower thrips as the most important virus vector. The virus reduces potato yield and tuber quality (Marchoux et al., 1991; Alvarez et al., 2003; Jones, 2005; Reitz and Funderburk, 2012; Learmonth, 2017; Kroschel et al., 2020).

23.2.1.8 Mites Mite pests of potato are polyphagous. Major hosts include potato, tomato, tobacco, pepper, eggplant, pumpkin, squash, cucumber, watermelon, celery, maize, beans, strawberry, cotton, citrus, and papaya (Alvarez et al., 2003; Goftishu et al., 2016). Mites that damage potato in Africa include the tomato or tobacco red-spider mite (Tetranychus evansi), the two-spotted spider mite (Tetranychus urticae), and the broad mite (Polyphagotarsonemus latus), which are widely distributed in both tropical and subtropical areas of the world. Chlorotic spots caused by mites give leaves a tan coloring, whereas high infestation will cause leaf and plant wilting and death. Plants with severe damage of broad mites do not form tubers and remain very small. Heavy infestations can cause the destruction of entire potato crop. Two-spotted spider mites are sporadic and are usually brought into potato fields by wind from other infested crops such beans and maize or when planted along dusty roads (Alvarez et al., 2003). The female spins a fine web over the leaf, which apparently protects the eggs and mites from rain and predators. In severe infestations, leaves are tied together with dirty webbing. When populations become severely crowded, spider mites climb to the top of a plant, secrete a web strand and parachute to a new location. This is the reason why sudden infestations commonly develop downwind from previously infested fields (Alvarez et al., 2003).

23.2.2 Plant parasitic nematodes Several nematode species affect potato yields worldwide (Medina et al., 2017; Lima et al., 2018). They include root-knot nematodes and potato cyst nematodes. Nematodes damage roots through feeding thereby reducing water and nutrient uptake and accumulation. The affected tubers develop lesions, rot, and shrivel, leading to significant economic losses (Hafez and Palanisamy, 2003; Hay et al., 2016; Coyne et al., 2018). Symptoms include pale foliage, stunting, wilting during heat, and early vine death.

23.2.2.1 Root-knot nematodes Root-knot nematodes are the most widespread and economically important of all plant-parasitic nematodes. The highest global biodiversity of the genus Meloidogyne occurs in Asia, where 45 species have been reported; North America has 36, Central and South America 31, followed by Europe with 25, Africa with 21, and Oceania with 11 (Subbotin et al., 2021). Root-knot nematodes can cause significant yield and crop losses in potatoes (Hafez and Palanisamy, 2003; Powers et al., 2005; Lima et al., 2018). This loss cuts across the tropics, through subtropics, and to temperate regions. Susceptibility of

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the cultivar and the population load of root-knot nematode species present in the soil during planting play a pivotal role in determining the level of loss (Viaene et al., 2007). Moreover, root-knot nematode species can cause deformations in potato tubers in the form of galls, as well as brown spots that are characteristic of mature females residing just below the skin layer. Infected table and processing potato tubers are rejected in local or international markets, while infected seed tubers facilitate dissemination of these pathogens to new areas (Hafez and Palanisamy, 2003; Powers et al., 2005). Several species of root-knot nematodes have been identified and characterized from infected potatoes and other plant hosts but only six are currently considered to be globally destructive. These species are Meloidogyne chitwoodi, M. fallax, M. hapla, M. arenaria, M. incognita and M. javanica. Root-knot nematode species that have been reported in Africa include Meloidogyne incognita, M. arenaria, M. javanica, M. hapla, M. chitwoodi and M. enterolobii (Onkendi, 2014; Karuri et al., 2017; Otieno, 2019; Subbotin et al., 2021). The threat of root-knot nematodes extends beyond the damage they cause on their own. The root damage they cause may also increase susceptibility to diseases such as bacterial wilt, Phytophthora root rot, and Fusarium wilt.

23.2.2.2 Potato cyst nematodes Potato cyst nematodes (Globodera spp.) are the most recent pest threat to emerge in Africa (Mburu et al., 2020; Mwangi et al., 2021). High levels of infection lead to thousands of nematodes infecting each potato plant. They are, therefore, a difficult pest to control. These nematodes are subject to strict quarantine regulations in over a 100 countries and are globally considered as the most important pests threatening potato production. However, they are all too often overlooked in less developed countries (Coyne et al., 2018; Lima et al., 2018, Niere and Karuri, 2018, Dandurand et al., 2019a,b; Mwangi et al., 2021). These nematodes are parasitic worms that are microscopic, and therefore invisible to the farmer. They infect potato roots, suppressing crop growth and can cause huge yield losses of up to 80%, and sometimes total crop failure. Globodera rostochiensis and G. pallida, both found in several African countries, are among the most important pests of potatoes globally (Mwangi et al., 2021). They are particularly lethal because the hundreds of eggs produced by the female nematode can remain dormant in the soil for years, awaiting the next potato crop host. The eggs remain protected in a hardened, protective cyst long after the nematodes die. Chemical signals from newly planted potato roots trigger the eggs to hatch and start the life cycle again. Some management tactics for these nematodes focus on disrupting this life cycle using nonhost plants that stimulate suicide hatch of cysts. When the newly hatched juvenile nematode leaves its protective cyst, it is guided to the potato root by different chemical signals emitted from the roots. Nonhost trap crops such as litchi tomato (Solanum sisymbriifolium), which stimulate egg hatching but do not support nematode reproduction, can provide an effective strategy to control or eradicate potato cyst nematodes, since hatched juveniles have limited food reserves and die if they do not successfully parasitize plant roots (Dandurand et al., 2019a,b; Dandurand and Pillai, 2021).

23.2.3 Potato diseases Potatoes are affected by viruses, bacteria, and fungal pathogens. Diseases caused by these pathogens are the most important component of a biological constraint to potato production. Once in the tubers, some pathogens continue to develop and multiply even when the potatoes are stored, which means that 100% yield loss is possible depending on the period and conditions of storage, type of disease, and pathogen multiplication rate (Otieno, 2019). This section highlights several important viral, bacterial, and fungal diseases affecting potato production in Africa.

23.2.3.1 Potato viruses Most important potato viruses are transmitted by aphids. Potato leafroll virus (PLRV) and potato virus Y (PVY) are the two most important potato-infecting viruses. Both severely diminish potato yield and quality in most potato-growing regions, including Africa (Muthoni et al., 2009; Were et al., 2013; Otieno, 2019; Kruger and van der Waals, 2020; Onditi et al., 2021). PLRV is a persistent virus transmitted exclusively by potato colonizing aphid species, mainly Myzus persicae and Microsiphum euphorbiae. PVY is nonpersistently transmitted by at least 50 different aphid species, most of which probe potato plants with their proboscis, but neither settle nor reproduce on potato. M. persicae is the most effective vector of both persistent and nonpersistent viruses. It is also a highly polyphagous species that often moves into potato fields from surrounding crops and noncrop vegetation (Radcliffe and Ragsdale, 2002; Alvarez et al., 2003; Saguez et al., 2013). Additional important aphid-transmitted potato viruses include potato virus A (PVA), potato virus X (PVX), potato virus S (PVS), and potato virus M (PVM). A single or combination of these viruses, in addition to PVY, collectively cause the potato mosaic disease. All these viruses have been reported across potato producing regions in Africa (Were et al., 2013;

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Okeyo et al., 2019; Otieno, 2019; Kruger and van der Waals, 2020; Onditi et al., 2021). PLRV, PVY and mosaic viruses can be seedborne and have been reported to cause up to 90%, 80% and 40% reduction of potato yields, respectively, in some parts of Africa (Kaniewski et al., 1990; Otieno, 2019). Symptoms of virus infection vary depending on the virus and how it is transmitted. For example, while PLRV can be seedborne, it is generally spread by aphids. Current season (primary infection) results from spread of virus by aphids during current growing season. Symptoms are characterized by yellowing and upward rolling of leaves that starts on the top of the plant, but there is no dwarfing of the plant. Leaves of red-skinned varieties turn red or purple at their edges. When seedborne (secondary infection), plant often is dwarfed and pale in color. Lower leaves are rolled upward, and usually harsh and leathery in texture. Current season spread of PLRV may cause tuber net necrosis in some varieties (Alvarez et al., 2003; Srinivasan et al., 2013). The main characteristics of the mosaic diseases are mottling of the leaves and the ability to be transmitted by sap. Leaf mottling consists of small, light green spots scattered through the darker green areas of the leaf. Affected plants are somewhat stunted. They mature prematurely and their yields are reduced. Crinkling, curling, rugosity, and distortion of leaves often occur. Plants affected with mosaic lack vigor. Latent viruses such as PVX and PVS may cause no visible symptoms but still cause reduction in yield (Alvarez et al., 2003; Nolte et al., 2003; Srinivasan et al., 2013). Several recombinant and necrotic strains of PVY, including PVY NTN and PVY Wilga have been reported in Africa (Were et al., 2013; Kruger and van der Waals, 2020). Effective management of these aphid-transmitted diseases hinges on planting disease-free potato seed as insecticides are ineffective at preventing transmission of nonpersistent viruses.

23.2.3.2 Bacterial wilt Bacterial wilt, caused by Ralstonia solanacearum, is a serious threat to potato production in Africa (Were et al., 2013; Uwamahoro et al., 2020; Otieno, 2019; Muthoni et al., 2020; van der Waals and Kruger, 2020). This soil-borne disease can be spread by water, farm tools, infected seeds, previously infested crops residue, and volunteer potato crops. When infected, the whole plant wilts and dries up, tubers develop brown-black stains and rot, resulting in reduced marketable potato yield and quality. Yield losses ranging from 50% to 100% have been reported in some countries in Central and East Africa (Muthoni et al., 2012). The pathogen has several host plants such as pepper, tomato, tobacco, eggplant, ornamentals, as well as several species of weeds that are commonly found in or near potato farmers’ fields. Management of this disease using available agrochemicals is difficult. As a result, farmers should use disease-free potato material. Also, they should select resistant or tolerant potato varieties and avoid fields that are infested with bacterial wilt pathogen (Muthoni et al., 2012, 2020; Uwamahoro et al., 2020). Unfortunately, these options are not always available, especially for small-scale farmers. Rotating potatoes with crucifers such as cabbage and cauliflower could significantly reduce bacterial wilt disease inoculum (Larkin et al., 2011).

23.2.3.3 Common scab Common scab of potatoes is a soil-borne disease caused by the bacteria-like organism Streptomyces scabies. The disease occurs throughout the potato growing regions of the world, including Africa (Nolte et al., 2003; Otieno, 2019). The pathogen attacks potato stems, stolons, and roots. However, it is mostly a tuber disease and usually infects young, rapidly growing tubers, which stimulates the growth of unsightly corky tissue. Disease symptoms in tubers include dark brown, pithy patches that may be raised and warty. The distribution of these lesions can range from a small area to the entire tuber surface. Sometimes, the ridged portions are arranged in broken concentric rings. Severe infection can reduce the marketable yield, damage the eyes of seed potatoes, and reduce the market value of the crop. Common scab is most severe when tubers develop under warm, dry soil conditions with a soil pH above 5.2. The disease is greatly suppressed in soils with a pH of 5.2 or lower. No single measure provides effective control of common scab, but the disease can be managed using an integrated approach that combines the use of host plant resistance and cultural control methods. Chemical control methods have met with limited success. Crop rotation is important in the control of common scab because it reduces the levels of inoculum in potato fields. However, S. scabies can survive for many years in the absence of potatoes because of its ability to live saprophytically and infect other plants. It has been reported on many fleshy root vegetables, such as beets, carrot, radish, and turnip. Rotation with small grains or alfalfa appears to reduce disease in subsequent potato crops.

23.2.3.4 Powdery scab Powdery scab, a root and tuber disease caused by the pathogen Spongospora subterranea f.sp. subterranea, poses a major problem to potato producers worldwide, including Africa (Nolte et al., 2003; van deer Waals et al., 2013; Muzhinji and van deer Waals, 2019; van der Waals and Kruger, 2020). The pathogen causes powdery scab on potato tubers and galls on

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roots. Powdery scab lowers the quality of potato tubers destined for fresh, processing, and seed markets. Root galls impair plant growth and productivity and contribute to inoculum build-up and pathogen perpetuation in the soil. Spongospora subterranea f. sp. subterranea is also the vector of potato mop-top virus, another pathogen of economic and quarantine importance in other potato producing areas of the world (Andersen et al., 2002; Nolte et al., 2003). Inoculum can be seedborne or originate from contaminated growing soil or contaminated equipment. Control of powdery scab is difficult, but a reduction in disease incidence and severity can be achieved through integration of several management measures, including informed selection of pathogen-free fields, cultivar choice, seed and soil treatment, optimal plant nutrition, crop rotation with nonhosts or trapping crops, planting of disease- and pathogen-free tubers, and postharvest hygiene (van der Waals and Kruger, 2020). Also, continuous monitoring of the pathogen population dynamics will be helpful in implementing effective region-specific management strategies for the pathogen, especially in the development of resistant potato cultivars.

23.2.3.5 Late blight Late blight, caused by the fungus like oomycete pathogen Phytophthora infestans, is a devastating disease that can infect potato foliage and tubers at any stage of crop development (Nolte et al., 2003). This disease attacks potato crops, mostly during cool, cloudy, and wet conditions and may result in 100% yield loss under heavy infection on susceptible varieties. The primary host is potato, but P. infestans also can infect other solanaceous plants, including tomatoes, petunias, and hairy nightshade, which can act as source of inoculum to potato. Late blight is a serious threat to potato production in countries in Africa where conditions are favorable to the disease (Ojiambo et al., 2001; Olanya et al., 2001, 2002; Tumwine et al., 2002; Nyankanga et al., 2004; Otieno, 2019; van der Waals and Kruger, 2020). Due to both field and postharvest losses and control requirement, late blight is classified as the most expensive disease of potato crop (Cooke et al., 2011). The first symptoms of late blight in the field are small, light to dark green, circular to irregular-shaped water-soaked spots. These lesions usually appear first on the lower leaves. Lesions often begin to develop near the leaf tips or edges, where dew is retained the longest. During cool, moist weather, these lesions expand rapidly into large, dark brown or black lesions, often appearing greasy. Leaf lesions are also frequently surrounded by yellow chlorotic halos. The lesions are not limited by leaf veins, and as new infections occur and existing infections coalesce, entire leaves can become blighted and killed within just a few days. The lesions also may be present on petioles and stems of the plant. During active growth, especially in cool and wet weather, a white mildew-appearing area is visible at the edge of the lesions or along petioles. This is the area where the late blight pathogen is actively producing spores. As the weather changes to warm and dry, these lesions become dry, stop sporulating and become tan. A pale green to yellow border often surrounds the lesions. Severely infected fields often produce a distinct odor. Late blight infection of tubers is characterized by irregularly shaped, slightly depressed areas that can vary considerably from brown to purplish of variable size on the skin. These symptoms may be less obvious on russet and red-skinned cultivars. A tan to reddish-brown, dry, granular rot is found under the skin in the discolored areas and extending into the tuber. The extent of the rotting in a tuber depends on the susceptibility of the cultivar, temperature, and length of time after the initial infection. Under good management but without fungicide sprays, yield losses could be 40%e50% for the moderately resistant varieties and 50%e70% for the more susceptible varieties (Ojiambo et al., 2001; Rahman et al., 2008; van der Waals and Kruger, 2020). Proper irrigation management through minimized wetting on potato leaves and ensuring air circulation to dry leaves is important for late blight management. Chemical control should be used cautiously and only under heavy infestation (Nyankanga et al., 2004; Rahman et al., 2008).

23.2.3.6 Early blight Early blight is a disease of potato caused by the fungus Alternaria solani. It is found wherever potatoes are grown, including in Africa. The disease primarily affects leaves and stems, but under favorable weather conditions, and if left uncontrolled, can result in considerable defoliation, and enhance the chance of tuber infection. Premature defoliation may lead to considerable reduction in yield. The disease can also be severe on tomatoes and can occur on other solanaceous crops and weeds. The fungus overwinters either on potato tubers or in dead, infected plant debris either in the soil or on the soil surface. The concentration of initial or primary inoculum from these reservoirs is usually low. The fungus can penetrate the leaf surface directly through the epidermis and spots begin appearing in 2e3 days. Lesions are most numerous and pronounced on lower, older, and less vigorous leaves and on early maturing varieties. The lesions are dark brown and appear leathery with faint, concentric rings.

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At harvest time, spores from blighted vines may be deposited onto tubers. These spores germinate during wet and warm weather and invade the tissue, primarily through cuts, bruises, or wounded surfaces. Tuber infections appear as generally small, irregular, brownishdblack spots which are usually slightly sunken. Externally the spots resemble those caused by late blight, but internally they are shallower and darker in color. The rotted tuber tissue is firm, hard, and somewhat corky. Early blight tuber rot develops slowly and may not be severe until quite late into the storage period. This decay may allow the entry of secondary organisms such as Fusarium fungi and soft rot bacteria. Yield losses of up to 80% have been reported (Olanya et al., 2009; Horsfield et al., 2010; Tsedaley, 2014; Otieno, 2019). Control of early blight is difficult due to its capacity to produce huge amounts of secondary inoculum and survival in the soil (Campo et al., 2007; Pasche et al., 2004). Being a soilborne disease, the pathogen could easily be dispersed by wind and irrigation water. Therefore, farmers should regulate water and avoid splashing soils onto plant leaves during irrigation (Olanya et al., 2009). At harvesting, farmers should avoid causing injuries to the tubers that could lead to further contamination and spread in the storage. The storage structures should provide cool and aerated conditions that promote rapid suberization of bruises and cut edges to keep away the pathogens as they are unable to infect through intact periderm (Tsedaley, 2014). Most importantly, farmers should plant certified disease-free potato seed.

23.2.3.7 Verticillium wilt Verticillium wilt of potatoes is a fungal disease caused by either of two species of Verticillium: Verticillium dahliae or Verticillium albo-atrum. Both Verticillium species survive in the soil and in infected plant debris. The organisms may be in the soil, on the seed piece, or in the vascular system of a diseased plant. These pathogens grow through the vascular system of the plant causing it to wilt, usually late in the season. The fungus infects the potato plant through the roots and invades the water-conducting tissues, which can result in a premature yellowing and death of the vine. Premature dying of the plant reduces yield and tuber size. This disease is expressed more in plants under stress, especially water stress. It can also cause stem-end discoloration and reduce tuber quality for the tablestock and the chip market. When a cross section of an infected tuber is cut from the stem end, the vascular ring may have brown or black discoloration. The discoloration may extend throughout the tuber but usually is present only part way through the tuber. Seed tubers can transmit Verticillium spp., which can result in the long-distance spread of the pathogen. An infested seed tuber usually carries the fungus on the surface. A seed tuber can have infected vascular tissue. The fungus grows from diseased seed pieces into the new plant or grows through the soil to the roots of healthy plants. It penetrates the young roots and will grow through the stolons into the young tubers. Since the fungus may overwinter in infected plant parts, such as the stems, infected plant debris can be an important source for carry-over of the fungus. The disease is found in all potatoproducing areas of the world, including Africa (Otieno, 2019) and could cause up to 50% yield loss in the affected fields (Johnson and Dung, 2010). Controlling Verticillium wilt disease is very challenging due to the wide range of host plants that exist at any given time in the farmer fields. However, farmers should avoid introducing the pathogen into areas not infested by using high quality seed from fields without a history of Verticillium wilt problems. Also, rotating potatoes with cereals and nonhost plants have shown a significant reduction of the disease depending on the period of rotation (Larkin et al., 2011; Otieno, 2019). Some potato varieties are more susceptible to losses from Verticillium wilt than others, so selecting and planting resistant varieties are recommended.

23.3 Pest and disease management practices Integrated pest management (IPM) is the most effective approach to manage potato insects, nematodes, and pathogens (Radcliffe and Lagnaoui, 2007; Kroschel et al., 2020) that is defined in Chapter 27. To make informed decisions, IPM requires a good knowledge and understanding of individual potato production systems, accurate identification and monitoring of pest species, and knowledge of their biology and associated damage and infection symptoms. Also, management approaches depend on access to management tools and products, cost, and other resources. The major factor contributing to the low and declining potato yields for small scale and subsistence farmers in Africa include losses due to attack by a range of pests and diseases. A second main reason is the repeated cropping of potato on the same field without rotation since farmers have very limited land. The third constraint is the use of poor quality or substandard seed, partly due to limited availability of certified high-quality seed. Furthermore, farmers in Africa have little to no access to crop protection products or application equipment. Therefore, this potato pest and disease management section will emphasize more on plant host resistance, with a brief discussion on chemical, biological, and cultural control practices.

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23.3.1 Chemical control Pesticides, including insecticides, fungicides, and nematicides have been largely successful in controlling potato pests and diseases globally, and are commonly used in developed countries. However, there are serious concerns about long-term sustainability of chemical control approach. Negative impact of pesticides on environment, humans, pollinators, and beneficial organisms, is well documented. In addition, several pesticides are becoming phased out due to environmental concerns or have become ineffective due to resistance development in targeted pest and pathogen populations (Kuhar et al., 2013; Alyokhin et al., 2013, 2015). While pesticides can be effective in controlling several of potato pests and pathogens discussed in this chapter, small-scale and subsistence farmers in Africa often have no access to pesticides and equipment and, if they do, production costs are prohibitive. Also, environmental impacts of pesticide use may be particularly pronounced because of limited access to personal protective equipment and close vicinity of agricultural and residential areas. Therefore, nonchemical control alternatives to manage pests and diseases are essential for potato production in Africa and should be prioritized when making management decisions.

23.3.2 Biological control Natural enemies are a major component of biological control and include predators, parasitoids, and entomopathogenic nematodes that actively seek out the pest. They have an enormous potential to suppress potato insect pests in the context of a truly integrated pest management approach, locally adapted to include essential cultural controls, pest thresholds, and variety of compatible intervention tactics such as pheromone-based technologies, trap cropping, and selective insecticides (Weber, 2013). Biological control also involves biopesticides that contain microorganisms, including bacteria, fungi, or viruses, which attack specific pest species, or entomopathogenic nematodes as active ingredients (Sporleder and Lacey, 2013). Biological control is a major component of IPM for potato production in Africa, especially because conventional pesticides are often unavailable and not commonly used, which favors conservation of beneficial natural enemies that regulate important potato pests. Several arthropod predators, parasitoids, and entomopathogens are essential in keeping under control populations of important potato pests in Africa, including potato tuber moth, aphids, leafminers, loopers, cutworms, armyworms, thrips, and mites (Nderitu, 1991; Muchemi et al., 2014; Mujica et al., 2016; Otieno, 2019; Mwesige et al., 2019; Kroschel et al., 2020). Important predators include Cheilomenes spp., Alesia aurora, Scymnus trepedulus, Adonia variegate, Hyperaspis jocose, Thea variegate, and Dysis quadrilineata (Coleoptera: Coccinellidae); Harpactor albopilosus and Rhinocoris tibialis (Hemiptera: Reduviidae); Deraeocoris spp. (Hemiptera: Miridae); and Nabis capsiformis (Hemiptera: Nabidae) (Nderitu, 1991). An extensive list of important predators and parasitoids of important potato pests is also provided by Weintraub et al. (2017) and Kroschel et al. (2020). Several biopesticides effective against potato pests and pathogens in East Africa are discussed by Otieno (2019). Efforts should be made to continue protection and conservation of beneficial organisms in potato crops and adjacent nonpotato agroecosystems.

23.3.3 Cultural control Application of best cultural practices is a pilar of IPM for potato production. The practices include the use of healthy seed, suitable crop rotations, physical barriers, and intercropping systems among others, which also support natural biological control. A major obstacle in many subSaharan Africa countries is the high cost and limited availability of agricultural inputs, along with disease-free quality seed potatoes. Establishment and implementation of quality control through specialised seed production systems and certification schemes is critical to improve seed potato quality and reduce disease sources, including viruses, bacteria, fungal pathogens, and nematodes. Seed could be further improved by breeding pathogen-resistant varieties adapted to different environmental conditions combined with management measures adapted to small-scale farms in Africa (Kruger and van der Waals, 2020). As already mentioned, due to the limited availability of land for small-scale and subsistence farmers in subSaharan Africa, repeated cropping of potato on the same fields without rotation is common, making it difficult to incorporate this pest and disease cultural control tactic in overall IPM schemes. However, cultural practices to manage pests and diseases in potato crops in Africa should be considered whenever possible.

23.3.4 Plant host resistance While developed countries can partly rely on the use of pesticides, cultural control and seed certification schemes for the management of potato pests and diseases, the limited availability of agricultural inputs, and the lack of disease-free seed

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potatoes certification schemes render the use of host resistance a cornerstone of disease management. Seed quality improvement by breeding pest and disease resistant varieties adapted to different environmental conditions combined with management measures tailored to specific agricultural requirements is often presented as the best option to improve potato production and sustainability for smallholder or commercial farmers in Africa (Schulte-Geldermann, 2017; Krüger and van der Waals, 2020). Wild relatives of cultivated potato are credited with contributing most disease resistance genes to breeding programs (Jansky 2000; Simko et al., 2007). Conventional breeding methods has been used to genetically improve cultivated potato for many decades. Recent publication of the potato genome sequence has provided a better understanding of potato biology and opened avenues to accelerate the breeding of new potato cultivars and introducing desirable characteristics into existing cultivars more efficiently, such as enhanced pest and disease resistance (Dale et al., 2016; Bethke, 2019). This is especially important for potato crop, characterized by slow genetic gains inherent to its genetic complexity and vegetative propagation. Often, new improved varieties lack a single important trait that may limit their adoption by farmers. New precision-breeding tools such as gene editing are now available and can be used to remove negative traits and expedite the improvement of simply inherited resistance traits (Thiele et al., 2021). Access to highly diverse germplasm of potato is essential to varietal development, as demonstrated by the role played by the genetic material from The International Potato Center (CIP) genebank in the development of release of varieties grown by smallholder farmers in lower-income countries (Thiele et al., 2021). Germplasm with high levels of resistance to various pathogens and pests are maintained in various genebank collections, including wild species accessions, breeding germplasms or improved cultivars (FAO, 2010). Table 23.2 lists some of the most important holdings of potato germplasm available to breeders, researchers, and farmers worldwide under the International Treaty on Plant Genetic Resources for Food and Agriculture (ITPGRFA) of United Nations’ Food and Agriculture Organization of the United Nations. An important goal of the treaty is to facilitate global germplasm exchange and to provide a legal framework to distribute the genetic material for research, training, and breeding with the acceptance of a Standard Material Transfer Agreement (SMTA) by the recipient (http://www.fao.org/plant-treaty/). Information about genebanks holdings and reactions to major pests and diseases is available in several searchable on-line public databases or global platforms like the GRIN-Global database or Genesys, initiated by Bioversity International, the Global Crop Diversity Trust, and ITPGRFA. Genesys (https://www.genesys-pgr.org/welcome) provides information on more than 19,066 potato accessions comprising over 175 species maintained in various genebanks. The adoption of modern conventional breeding tools, such as marker-assisted selection is increasing globally and is expected to speed up breeding progress in developing countries. Several collaborative projects and platforms have been established and are aimed to provide capacity building support to national agricultural research systems in developing countries (https://doi.org/10.2144/btn-2020-0066). These include: the Genomic Open Breeding Informatics Initiative (GOBii) (http://gobiiproject.org/Google Scholar), the Integrated Breeding Platform (http://www.integratedbreeding. netGoogle Scholar) and the CGIAR Excellence in Breeding (EiB) platform (https://excellenceinbreeding.org/Google Scholar). As outlined by Bethke (2019), recent progress in the genomics era opens new avenues for genetic enhancement, shifting the focus from evaluating phenotypes to tracking and manipulating specific DNA sequences. Genetic engineering approaches provide alternative or complementary strategies for developing potatoes resistant to insects and diseases (Douches et al., 1998; Bakhsh et al., 2020). A list of transgenic plants, including potatoes approved for commercial use can be found in the GM Approval database (http://www.isaaa.org/gmapprovaldatabase/default.asp) of the ISAAA. Dozens of genetic transformation events related to potato insect resistance and disease resistance are indicated. Information related to field assessment and importation approval cases of transgenic potato is also available at the Biosafety Clearing House Mechanism homepage of the CPB (https://bch.cbd.int). The Biosafety Clearing House (BCH) is a mechanism set up by the Cartagena Protocol on Biosafety to facilitate the exchange of information on Living Modified Organisms (LMOs) and assist the Parties to better comply with their obligations under the Protocol. The website also provides a variety of scientific, technical, environmental, legal, and capacity building information. Below, we present a brief review of challenges and opportunities related to the deployment of host resistance as integral part of managing major potato insect pests and diseases in Africa, with highlights on the potato tuber moth, aphids, aphid-transmitted viruses, plant parasitic nematodes, bacterial wilt, late blight, and common scab.

23.3.4.1 The potato tuber moth Sources of resistance to this important potato pest has been identified in wild relatives of cultivated potato (Arnone et al., 1998; Horgan, 2013). To the extent that resistance mechanisms have been studied, resistance is attributed to

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TABLE 23.2 Major genebanks repositories holding potato germplasm resources for breeding. Country

Genebank

Name/Institution

Type

Website/contact info

Brazil

CENARGEN

National Center for Research on Genetic Resources and Biotechnology

National

www.cenargen.embrapa.br

Canada

PGRC

Canadian Potato Genetic Resources, Agriculture and Agri-Food Canada, Fredericton, New Brunswick

National

http://pgrc3.agr.gc.ca/index_e.html

China

ICGR-CAAS

Chinese Academy of Agricultural Sciences, Institute of Crop Sciences (CAAS/ ICS)

National

https://www.cgris.net

Czech Republic

RICP

Crop Research Institute

National

www.vurv.cz

Ecuador

INAP/ DENAREF

Intituto Nacional de Investigacoiones Agropecuaria

National

www.iniap.gob.ec

Ethiopia

IBC

Ethiopian Biodiversity Institute

National

https://www.ebi.gov.et/gm-access/gm/

France

INRARENNES

The Potato Collection of France, INRA/Universite´ Rennes 1, Rennes, France

National

http://www7.rennes.inra.fr/apbv

Germanya

IPK Gatersleben

Institute of Plant Genetics and Crop Plant Research, IPK, Gross Lu¨sewitz, Germany

National

http://glks.ipk-gatersleben.de/

India

NBPGR

National Bureau Of Plant Genetic Resources

National

nbpgr.ernet.in

The Potato Collection of Ireland, The Tops Potato Center, Raphoe, Co. Donegal, Ireland

National

www.agriculture.gov.ie/ farmingsectors/crops/seedcertification/ topspotatocentre/

a

Ireland

Japana

NIAS

NIAS Genebank

National

https://www.naro.affrc.go.jp/archive/ nias/eng/genresources/index.html

Kenya

KARI-NGBK

National Genebank of Kenya, Crop Plant Genetic Resources Center

National

https://ssl.fao.org/glis/wiews/detail? wiewsCode¼KEN015

Netherlands

CGN

Center for Genetic Resources, the Netherlands

National

https://www.wur.nl/.../Centre-forGenetic-Resources-the-Netherlands-1. htm

Nordic Countries

NGB

NordGen

National

https://www.nordgen.org/en/our-work/ nordgen-plants/the-genebank/

International Potato Center, Lima, Peru

CGIAR

http://cipotato.org/genebank

N.I. Vavilov Institute (VIR), 44 B Morskaya str., 190,000 St. Petersburg, Russia

National

www.vir.nw.ru

Spain

The Potato Collection of Spain, The Basque Institute for Agricultural Research and Development (Neiker-Tecnalia), Alava, Spain

National

www.neiker.net/neiker/germoplasma/

Sweden

The Nordic Genetic Resource Center (NordGen) Potato Collection, Alnarp, Sweden

National

www.ngb.se/sesto/index.php?scp¼ngb

UK

The SASA (Science and Advice for Scottish Agriculture) Potato Collection, Edinburgh, UK

National

www.sasa.gov.uk

The United States Potato Genebank (NRSP-6) Sturgeon Bay, Wisconsin

National

http://www.ars-grin.gov/ars/MidWest/ NR6/

Perua Russian Federationa

USAa

VIR

NPGS

a One of the major six countries that are holding 41% of world potato ex-situ accessions. Adapted from FAO, 2010. The Second Report on the State of the World’s Plant Genetic Resources for Food and Agriculture, Rome.

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unattractiveness of plants, adverse effects of feeding, and deleterious effects on reproduction of the insect (Pelletier et al., 2013). Variable reactions were also observed among breeding clones of cultivated potato (Salem et al., 2018; Alipour, 2018; Lopes, 2001; Mansouri, 2013; Rondon et al., 2013). However, progress deploying resistance genes in commercial cultivars to contribute to current management strategies against the potato tuber moth has been hampered by lack of effective screening methods and understanding of the mechanisms and possible trade-offs associated with tuber and foliage resistance to improve the efficiency of potato breeding programs (Horgan, 2010, 2013). There are several studies reporting development of resistant varieties by using genetic engineering approach (Douches et al., 1998; Rondon et al., 2009; Fatehi et al., 2017). A number of those transformed potatoes have been evaluated in several laboratories and in the target production areas in developing countries.

23.3.4.2 Aphids and aphid-vectored viruses Potential sources of resistance against major aphids affecting potato crop in Africa (M. persicae and M. euphorbiae) have been documented in wild Solanum accessions maintained in many genebanks, including United States Potato Genebank (NRSP-6) (Frechette et al., 2010; Pelletier and Smilowitz, 1990, Pompon et al., 2010; Le Roux et al., 2007). High heritability was reported suggesting the possibility of successful selection of resistant progenies in crosses although resistance to M. persicae did not appear to be correlated to resistance to M. euphorbiae (Tingey et al., 1982; Mndolwa et al., 1984; Tingey and Yencho, 1994). Resistance has been associated with the presence of glycoalkaloids or glandular trichomes on the leaves. Glandular trichomes are known to alter the ability of many herbivores to colonize, forage, and survive on the plant and were shown to play an important role in aphid resistance (Cho et al., 2017). However, it was demonstrated that resistance to M. persicae colonization was not directly related to resistance to M. persicae-transmitted PLRV infection, which justifies the shift of focus to breeding for aphid-vectored virus resistance rather than resistance to aphid colonization (Mndolwa et al., 1984). Similar approach could be envisioned for other insect-vectored diseases affecting potato crop such as the new and emerging potato disease called “Zebra Chip”, which is associated with potato psyllids and the fastidious bacterium ‘Candidatus Liberibacter solanacearum’ (Munyaneza et al., 2007; Munyaneza, 2012, 2015). Growing potato cultivars resistant to potato viruses offers the easiest and the most cost-effective solution to prevent the losses caused by aphids and their vectored diseases. As warmer climates generally favor aphids, thus increasing risks of viruses spread, deployment of potato cultivars carrying virus resistance is an important insect and disease management component. A review of major host resistance genes against potato viruses X, Y, A and V in potatoes, along with traditional and molecular breeding approaches were described by Solomon-Blackburn and Barker (2001). Several resistance genes originating from wild and cultivated potato species have been incorporated in commercial cultivars and breeding clones worldwide. A recent survey of 71 potato accessions from the National Potato Breeding Program at Kachwekano Zonal Agricultural Research and Development Institute in Uganda for the presence of resistance genes to viruses using diagnostic molecular markers revealed the presence of single of combinations of resistance genes for PVY, PVA, PVX and PVS (Byarugaba, 2021). Efforts to transfer major genes from resistant andigena landrace, LOP-868, and from wild species Solanum verrucosum to control PLRV are underway (Carrasco et al., 2000; Velásquez, 2007; Carneir,o 2017). Genetically engineered resistance provides alternative options to conventionally bred varieties in the protection against major viral diseases such as PVY, PVX, PLRV (Sharma et al., 2003; Valkonen et al., 2017; Orbegozo, 2016).

23.3.4.3 Plant parasitic nematodes Both Globodera rostochiensis and G. pallida are considered the most economically important pests affecting potato production in Africa (Mwaura et al., 2015; Mwangi et al., 2021). Genetic resistance is available in many commercial varieties and genebank accessions (Table 23.1). Breeding for resistance requires the knowledge of Globodera species pathotypes present in the soil. Two pathotypes, Ro1/4 and Ro2/3/5 for G. rostochiensis and Pa1 and Pa2/3 for G. pallida are known (Caromel et al., 2005; Castelli et al., 2005). The most deployed resistance gene is H1 originally found in Solanum tuberosum, group Andigena, which provides resistance against pathotypes Ro1 and Ro4 of G. rostochiensis (Gebhardt et al., 1993; Niewöhner et al., 1995). This gene is also present in several varieties cultivated in Africa, as demonstrated by Mwangi et al. (2021) with Kenyan potato varieties. However, H1 does not provide protection against G. pallida. For the latter, a different resistance gene, H2, has been identified wild species S. multidissectum, which is effective against pathotype Pa1 (Strachan et al., 2019). Sources of resistance to pathotype Pa2/3 of pale cyst nematode were identified in wild potato germplasm collection, including S. vernei, S. spegazzinii, S. acaule, S. circaeifolium, S. gourlayi, S. kurtzianum, S. oplocense, S. sparsipilum, S. brevicaule, S. demissum and S. microdontum (Bachmann-Pfabe et al., 2019). With regards to root-knot nematodes (Meloidogyne species), although sources of resistance have been identified in

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wild species such as S. sparsilum, S. hougasii and S. bulbocastanum for M. Chitwoodi (Berthou et al., 1993; Brown et al., 1989), resistance has not yet been deployed in commercial varieties (Chiuta et al., 2021; Subbotin et al., 2021). The availability of genetic resources and their characterization is expected to provide effective management strategies to control potato cyst nematodes in low input cropping systems in Africa (Chauvin et al., 2008).

23.3.4.4 Bacterial wilt Bacterial wilt or brown rot, caused by members of the Ralstonia solanacearum strains complex (RSSC), is one of the most important diseases of potato. Currently there are no known cultivars with durable resistance to the pathogen that also have desirable agronomic traits, although some show decreased susceptibility levels (Muthoni et al., 2020; Uwamahoro, 2020). The development of resistant cultivars is challenging due to the genetic complexity of resistance, pathogen variability, screening procedures, and the genetic complexity linked to the tetraploid background of the crop. Polygenic resistance has been identified in several wild species (Otieno, 2021). The search for new and more stable sources of resistance continues to be an important goal for several breeding programs worldwide, including the International Potato Center (Gutarra et al., 2015) in Peru, Kenya (Muthoni et al., 2015), University of Wisconsin in USA, the Brazilian Agricultural Research Corporation (Embrapa Hortalicas, Brazil), and Uruguay (Lopes et al., 2018). Classical breeding has achieved moderate unstable level of resistance/tolerance due to hostpathogen-environment interaction. In addition, hybridization of the cultivated potato with the wild relatives is accompanied with undesirable traits such high glycoalkaloid content. In recent years, genetic engineering has been explored and appear to show promising results, although there is still a long way to go before varieties with stable resistance coupled with good agronomic characteristic are released (Muthoni, 2020).

23.3.4.5 Late blight Because of its historic and economic importance, late blight caused by Phytophthora infestans has received and continues to receive a special attention in many potato breeding programs around the world. It is also a major potato disease in Africa, where it mostly affects smallholder farmers (Ghislain, 2019). Wild potato species represent a vast reservoir of useful traits for potato improvement and have been extensively used as sources of late blight resistance breeding. Phytophthora infestans has proven to be a highly adaptable and rapidly evolving pathogen, requiring a special strategy to ensure a more durable resistance (Goverse and Struik, 2009). The most sustainable strategy to ensure long-term protection of potatoes is to pyramid or stack broad-spectrum resistance genes into promising or adapted cultivars. Resistance genes stacking has been undertaken by using conventional breeding as well as by genetic transformation approaches (Rakosy-Tican, 2020; Ghislain, 2019; Orbegozo, 2016; Mambetova, 2018). The availability and access to diverse germplasm at the International Potato Center has allowed the development of resistant germplasm tailored to smallholders in lower-income countries (Forbes, 2012; Bernal-Galeano et al., 2020). Several late blight selections and varieties linked to the International Potato Center’s germplasm have been reported under evaluation or adoption in some parts of Africa (Muhinyuza, 2015; Ndacyayisenga, 2019). Integration of host resistance in late blight management was also reported by Belay et al. (2021). The International Potato Center, in collaboration with the Uganda’s National Agricultural Research Organization has recently developed and tested a promising blight-resistant potato named 3R potato. The new potato contains genes acquired from potato relatives that are naturally resistant to late blight and was developed using biotechnology to accelerate deployment of three genes from potato relatives into already popular varieties adopted by farmers (https://www.potatogrower.com/2021).

23.3.4.6 Common scab Because of the widespread of potato common scab, many research programs worldwide have committed efforts to evaluating management methods for this disease (Braun et al., 2017). Since variety resistance appears to be the best control of the disease, breeding for resistance is now a component of several breeding programs. Breeding for resistance to scab has been reviewed by many authors, including Braun et al. (2017), Jansky et al. (2018), and Bradshaw et al. (2000). Sources of resistance to scab exist in cultivated diploid and tetraploid potatoes. This resistance shows relatively simple inheritance, making breeding much easier (Bizimungu et al., 2011). However, the lack of stability of resistant genotypes has been reported (Clark et al., 2019; Haynes et al., 1997), suggesting that identification of new sources of resistance is needed. Progress in developing scab resistant cultivars is expected to be further enhanced by recent progress in genomics research and the identification of molecular markers aimed to facilitate the selection process (Kaiser et al., 2020; Koizumi et al., 2021; Yuan et al., 2020; Enciso-Rodriguez et al., 2018).

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23.4 Conclusion The major factor contributing to the low and declining potato yields and tuber quality for small scale and subsistence farmers in Africa include losses due to attack by a range of pests and diseases. This chapter provided information on the identification and management of important potato insect and nematode pests, in addition to major potato viruses, bacteria and fungal pathogens commonly found in Africa. Because most of potato growers in subSaharan Africa have very limited land, repeated cropping of potato on the same field without rotation is common, making cultural management practices difficult. Also, the use of poor quality or substandard seed, partly due to limited availability of certified high-quality seed, is a major production constraint. In addition, farmers in Africa have little to no access to crop protection products or application equipment. Therefore, the potato pest and disease management section of this chapter focused on plant host resistance since breeding disease and pest resistant varieties adapted to different environmental conditions is the most important management measure that could help both smallholder and commercial farmers in Africa effectively increase potato yields and tuber quality. Breeding for resistance to these pests and diseases reflects significant progress as evidenced by the fact that potato varieties resistant to cyst nematodes and viruses are currently in production in some regions of Africa.

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Nyankanga, R.O., Wien, H.C., Olanya, O.M., Ojiambo, P.S., 2004. Farmers’ cultural practices and management of potato late blight in Kenya highlands: implications for development of integrated disease management. Int. J. Pest Manag. 50, 135e144. Nyasani, J.O., Meyhöfer, R., Subramanian, S., Poehling, H.M., 2012. Effect of intercrops on thrips species composition and population abundance on French beans in Kenya. Entomol. Exp. Appl. 142, 236e246. Nyawade, S., Karanja, N., Gachene, C., Gitari, H., Elmar, S.-G., Parker, M., 2019. Short-term dynamics of soil organic matter fractions and microbial activity in smallholder potato-legume intercropping systems. In: Proceedings of 11th Triennial Conference of African Potato Association, APA, 25th29th August 2019, Kigali, Rwanda. Nyongesa, M., 2019. Applying balanced nutrient fertilizers increases yield of Irish potato in different soil types of Rwanda. 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Estimation of yield loss caused by late blight and the effects of environmental factors on late blight severity in Kenya and Uganda. Afr. Crop Sci. Proceed. 5, 455e460. Olanya, O.M., Honeycutt, C.W., Larkin, R.P., Griffin, T.S., He, Z., Halloran, J.M., 2009. The effect of cropping systems and irrigation management on development of potato early blight. J. Gen. Plant Pathol. 75, 267e275. Onditi, J., Nyongesa, M., van der Vlugt, R., 2021. Prevalence, distribution and control of six major potato viruses in Kenya. Trop. Plant Pathol. 46, 311e323. Onkendi, E.M., Kariuki, G.M., Marais, M., Moleleki, L.N., 2014. The threat of root-knot nematodes (Meloidogyne spp.) in Africa: a review. Plant Pathol. 63, 727e737. Orbegozo, J., Roman, M.L., Rivera, C., Gamboa, S., Tovar, J.C., Forbes, G.A., Lindqvist-Kreuze, H., Kreuze, J.F., Ghislain, M., 2016. Rpi-blb2 gene from Solanum bulbocastanum confers extreme resistance to late blight disease in potato. Plant Cell Tissue Organ Cult. 125, 269e281. Otieno, S.A., Collins, P., Coombs, J., Allen, C., Douches, D.S., 2021. Screening for Ralstonia solanacearum resistance in Solanum commersonii. Am. J. Potato Res. 98, 72e77. Otieno, H.M.O., 2019. Impacts and management strategies of common potato (Solanum tuberosum L.) pests and diseases in East Africa. Front. Sci. 9, 33e40. Pasche, J.S., Wharam, C.M., Gudmestad, N.C., 2004. Shift in sensitivity of Alternaria solani in response to Q (0) I fungicides. Plant Dis. 88, 181e187. Pelletier, Y., Horgan, F.G., Pompon, J., 2013. Potato Resistance Against Insect Herbivores: Resources and Opportunities. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato. Elsevier, pp. 439e462. Pelletier, Y., Smilowitz, Z., 1990a. Feeding behavior of the adult Colorado potato beetle, Leptinotarsa decemlineata (Say) on Solanum berthaultii. Can. Ent. 123, 219e230. Pelletier, Y., Smilowitz, Z., 1990b. Effect of trichome B exudate of Solanum berthaultii Hawkes on consumption by the Colorado potato beetle, Leptinotarsa decemlineata (Say). J. Chem. Ecol. 16, 1547e1555. Pillai, S.S., Dandurand, L.M., 2021. Effect of Steroidal Glycoalkaloids on Hatch and Reproduction of the Potato Cyst Nematode Globodera pallida. Plant Dis. First Look. https://doi.org/10.1094/PDIS-02-21-0247-RE. Pompon, J., Quiring, D., Giordanengo, P., Pelletier, Y., 2010. Role of host-plant selection in resistance of wild Solanum species to Macrosiphum euphorbiae and Myzus persicae. Entomol. Exp. Appl. 137, 73e85. Powers, T.O., Mullin, P.G., Harris, T.S., Sutton, L.A., Higgins, R.S., 2005. Incorporating molecular identification of Meloidogyne spp. into a large-scale regional nematode survey. J. Nematol. 37, 226e235. Radcliffe, E.B., Lagnaoui, A., 2007. Pests and diseases, Part D. Insects. In: Vreughenhil, D., Bradshaw, J., Gebhardt, C., Govers, F., Taylor, M., MacKerron, D., Ross, H. (Eds.), Potato Biology and Biotechnology: Advances and Perspectives. Elsevier, Amsterdam, Netherlands, pp. 541e567. Radcliffe, E.B., Ragsdale, R.W., 2002. Aphid-transmitted potato viruses: the importance of understanding vector biology. Am. J. Potato Res. 79, 353e386. Rahman, M.M., Dey, T.K., Ali, M.A., Khalequzzaman, K.M., Hussain, M.A., 2008. Control of late blight disease of potato by using new fungicides. Int. J. Sustain. Crop. Prod. 3, 10e15. Rakosy-Tican, E., Thieme, R., König, J., Nachtigall, M., Hammann, T., Denes, T.E., Kruppa, K., Molnár-Láng, M., 2020. Introgression of two broadspectrum late blight resistance genes, Rpi-Blb1 and Rpi-Blb3, from Solanum bulbocastanum dun plus race-specific R genes into potato pre-breeding lines. Front. Plant Sci. 11. https://doi.org/10.3389/fpls.2020.00699. Reitz, S.R., Funderburk, J., 2012. Management strategies for western flower thrips and the role of insecticides. In: Perveen, F. (Ed.), Insecticides - Pest Engineering. IntechOpen, London, UK, pp. 354e384. Rondon, S.I., Brown, C.R., Marchosky, R., 2013. Screening for resistance of potato lines to the potato tuberworm, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Am. J. Potato Res. 90, 71e82. Rondon, S.I., Hane, D.C., Brown, C.R., Vales, M.I., Dogramaci, M., 2009. Resistance of potato germplasm to the potato tuberworm (Lepidoptera: Gelechiidae). J. Econ. Entomol. 102 (4), 1649e1653.

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Saguez, J., Giordanengo, P., Vincent, C., 2013. Aphids as major potato pests. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Oxford, UK, pp. 31e64. Salem, S.A., El-Kholy, M.Y., Abd El-Salam, A.M.E., Ahmed, S.R., 2018. Field evaluation and susceptibility of different potato cultivars to Phthorimaea operculella (Zeller) infestation and role of physic-chemical contents in tuber crust on protection. Biosci. Res. 15, 2938e2943. Schulte-Geldermann, E., 2017. Potato research in Africa to improve farmers- livelihoods: priorities in crop improvement, seed system, crop management, nutritional value, policies and marketing. Potato Res. 60, 287e289. Scott, G.J., Labarta, R., Suarez, V., 2013. Booms, busts, and emerging markets for potatoes in East and Central Africa. Potato Res. 56, 205e236. Scott, G.J., 2021. A review of root, tuber and banana crops in developing countries: past, present and future. Int. J. Food Sci. Technol. 56, 1093e1114. Sharma, H.C., Sharma, K.K., Seetharama, N., Crouch, J.H., 2003. The utility and management of transgenic plants with Bacillus thuringiensis genes for protection from pests. J. New Seeds 5, 53e76. Simko, I., Jansky, S., Stephenson, S., Spooner, D., 2007. Genetics of resistance to pests and diseases. In: Vreughenhil, D., Bradshaw, J., Gebhardt, C., Govers, F., Taylor, M., MacKerron, D., Ross, H. (Eds.), Potato Biology and Biotechnology: Advances and Perspectives. Elsevier, Amsterdam, Netherlands, pp. 117e155. Solomon-Blackburn, R.M., Barker, H., 2001. Breeding virus resistant potatoes (Solanum tuberosum): A review of traditional and molecular approaches. Heredity 86, 17e35. Sporleder, M., Lacey, L.A., 2013. Biopesticides. In: Giordanengo, P., Vincent, C., Alyokhin, A. (Eds.), Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Oxford, UK, pp. 463e498. Srinivasan, R., Cervantes, F.A., Alvarez, J.M., 2013. 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Basic science in potato pest management

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Chapter 24

Evolutionary considerations in potato pest management Andrei Alyokhina, Yolanda H. Chenb, Maxim Udalovc, Galina Benkovskayad and Leena Lindstro¨me a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bUniversity of Vermont, Department of Plant and Soil Sciences,

Burlington, VT, United States; cIndependent Consultant, Ufa, Russia; dInstitute of Biochemistry and Genetics, Russian Academy of Science, Ufa, Russia; eDepartment of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

24.1 Introduction Almost 50 years ago, Theodosius Dobzhansky famously said that nothing in biology makes sense except in the light of evolution (Dobzhansky, 1973). While it could be argued ad nauseam if that statement was somewhat an exaggeration, there is little doubt among the scientific community that the modern theory of evolution provides a useful and convenient framework for understanding patterns and processes observed in the biosphere. In the first edition of this book, we seconded the opinion expressed by Smith and Bernatchez (2008) and Hendry et al. (2010) that applied biology in general, and agricultural pest management in particular, are still lagging behind the other fields of biology in placing their findings in a broader evolutionary context, even though it is likely to increase both the efficiency and sustainability of future integrated pest management programs. Since then, certain progress has been made in terms of both conceptualization (e.g., Alyokhin et al., 2015; Alyokhin and Chen, 2017), developing novel frameworks to explain the evolutionary success of insect herbivores in agroecosystems (Brevik et al., 2018a), as well as obtaining empirical data (Zhu et al., 2016; Crossley et al., 2017) in applying evolutionary principles to pest management. Increasingly, the success of insect pests in agroecosystems in viewed in a broader evolutionary and landscape context (Crossley et al., 2018a, 2019). Viewed through the lens of crop domestication and human-mediated migration, insect herbivores evolve an association with crops through variable ways (Chen, 2016). However, additional opportunities exist to reduce the gap between evolutionary biology and pest management (Chen and Schoville, 2018).

24.2 Fundamentals of evolution Classical definition of biological evolution that is based on the synthesis of the original insights on natural selection developed by Charles Darwin with later advances in understanding of the genetic basis of inheritance was formulated by Dobzhansky et al. (1977) as follows: Organic evolution is a series of partial or complete and irreversible transformations of the genetic composition of populations, based principally upon altered interactions with their environment. It consists chiefly of adaptive radiations into new environments, adjustments to environmental changes that take place in a particular habitat, and the origin of new ways for exploiting existing habitats. These adaptive changes occasionally give rise to greater complexity of developmental pattern, of physiological reactions, and of interactions between populations and their environment. Variability, selection, and adaptation are the three essential components of the evolutionary process. No two organisms living on Earth are exactly the same. Variation in observable traits (phenotypes) among organisms is due to both variations in their genetic make-ups (genotypes) and nongenetic inheritance (e.g., maternal effects), as well as to different environmental influences experienced during their lifetimes. Genetic variation arises from mutations, recombination of genes during sexual reproduction, and migration (gene flow) between populations. Natural selection, which is the major driving force behind evolutionary change, can operate whenever organisms differ in their rates of survival and/or reproduction

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(also known as fitness) under particular environmental conditions (Futuyma, 1986). As a result, genotypes resulting in the expression of most adaptive phenotypic traits increase in frequency over successive generations. There are three general modes of selection (Futuyma, 1986). When an extreme phenotype is characterized by superior fitness, selection is directional. It results in a shift in the mean value of a particular trait in the population. A typical example of directional selection is insect adaptation to insecticides. When intermediate phenotypes are the most fit, selection is stabilizing or balancing. For instance, an extreme deviation from a certain shape of mouthparts would interfere with an insect herbivore’s feeding behavior on its host plant. As a result, it would be unlikely to persist in a population. Consequently, evolutionary change does not diminish the probability of population’s persistence under current conditions (Mina, 2015). If two or more phenotypes have higher fitness than intermediate phenotypes, selection is disruptive or diversifying. Adaptation to different host plants by insect herbivores with a subsequent formation of host races and/or speciation is an example of disruptive selection. Not all shifts in phenotypic traits driven by environmental changes are genetically determined and subject to selection. A range of phenotypes may be expressed by a given genotype (or population or species) across a range of different environmental conditions (Stearns, 1989; Gluckman et al., 2009). For example, an adult Colorado potato beetle (Leptinotarsa decemlineata Say) that is starved as a larva will be much smaller than an adult of the same species that is well-fed at the same stage. However, due to current genetic constraints, it will never shrink to the size of a springtail, and neither will it grow as big as a Goliath beetle. If the variation among the individuals in different environments has a genetic component, then these reaction norms can also evolve in response to selection (Stearns and Koella, 1986; Olsen et al., 2004; Lande, 2009; Crispo et al., 2010). Depending on its scale, evolution is broadly divided into microevolution and macroevolution (Dobzhansky, 1937). Microevolution refers to the changes in gene frequencies within a population. Processes of agricultural significance, such as development of insecticide resistance or adaptation to new host plants, normally fall into this category. Macroevolution happens above the species level and includes grand events like the colonization of land by vascular plants or the radiation of the dinosaur lineage, as well as smaller events like the evolution of new genera of leaf beetles. Evolution of traits toward a better adaptation to changing environments might proceed through existing genetic variation or through new mutations. On a short time scale, the former is probably more important (Aitken et al., 2008; Barrett and Schluter, 2008; Orr and Unckless, 2008). As a result, species that are well adapted to unstable natural environments often make the most formidable pests in unstable artificial environments typical of human agriculture (see below). However, new mutations provide fuel for longer-term evolution, with the greatest contribution expected from large populations with short generation times (Hendry et al., 2011). Both mechanisms may result in similar phenotypic outcomes and may be indistinguishable from the economic standpoint. For example, Hartley et al. (2006) concluded that malathion resistance in blowflies (Lucilia cuprina) evolved based on a preexisting genetic variation, but resistance to diazinon in the same species evolved through a new mutation. When thinking about evolution, people often subconsciously invoke a geological time scale, with images of trilobites and dinosaurs coming to mind. While this is certainly appropriate for macroevolutionary developments, it is also important to remember that microevolutionary changes may occur in as little as one generation (although, at the other extreme, they may also take many thousands of years) (Hendry and Kinnison, 1999). Actually, meta-analysis of the existing data strongly suggested that contemporary microevolution (defined as taking place on the time scale of less than a few centuries) represents typical rates of microevolution in contemporary populations facing environmental change (Hendry and Kinnison, 1999). Such rapid changes should be expected to commonly have profound impacts on human economic activities.

24.3 Applied evolution Mismatches between the current phenotypes of organisms and phenotypes that would be best suited for a given environment are a major issue of interest throughout the diverse fields of applied biology (Hendry et al., 2011). Occasionally, scientific effort is directed toward finding ways to minimize such mismatches. For example, diversifying field edges may create a more favorable environment for natural enemies by supplying them with additional resources (see Chapter 25 for more information). At other times, the desirable outcome is to maximize the discussed mismatches. For example, destroying crop residues may decrease populations of overwintering pests (see Chapter 15). Theoretical evolutionary principles are essential for meeting applied goals because they help to achieve a better understanding of current mismatches and their potential responses to human manipulations (Hendry et al., 2011). “Density makes the pest” is one of the most important principles of scientifically based integrated pest management (IPM) (Rajotte, 1993). The idea that keeping populations of established pests below certain economically damaging levels is a more efficient and sustainable approach compared to a zero-tolerance policy that is widely accepted by the scientific

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community and is increasingly gaining traction among commercial growers. Clearly, adaptation to a particular environment is likely to affect population growth rate in that environment. Therefore, understanding population-level evolutionary processes is instrumental for designing scientifically sound IPM plans. Adaptive evolution influences population dynamics and sometimes allows evolutionary rescue of a severely depressed population in a mismatched environment (Saccheri and Hanski, 2006; Kinnison and Hairston, 2007; Bell and Gonzalez, 2009). In the absence of density-dependent regulation, better-adapted populations grow faster due to higher birth rates and/ or lower death rates. When density-dependent regulation is important, better-adapted populations sustain more individuals at a given resource level. Evolutionary principles have been applied in agriculture for thousands of years (Hendry et al., 2011). The best phenotypes - from the human perspective - were generated by simultaneously seeking the best genotypes and maintaining them in the most favorable environments. Superior genotypes were obtained through cultivar and variety development, domestication of new species, and introduction of species into new geographic areas. Superior environments were created through cultural practices (e.g., tillage), fertilization, pest control, etc. Optimal interactions between the two were also sought and found. Despite all errors, side effects, and imperfections, this approach allowed for the maintaining of an everincreasing level of agricultural output. Employing evolutionary principles to a similar extent in pest management is likely to further improve agricultural production. Perhaps more importantly, it is likely to improve its sustainability.

24.4 Evolution in agricultural ecosystems Agricultural fields represent a distinct and usually fairly unstable environment. Obviously, there are considerable differences among the various systems of production. However, as a whole they are characterized by low species diversity (especially in monocultures typical of highly industrialized commodity farming), high levels of disturbance, considerable outflow of harvested organic matter, and the presence of large amounts of xenobiotics in the form of pesticides and inorganic fertilizers. Inherent instability of agricultural ecosystems applies a strong selection pressure toward the traits that help organisms survive potentially catastrophic events such as tillage, crop rotation, and/or application of pesticides. At the same time, survivors are rewarded with an ample supply of food and a relative scarcity of natural enemies. This reduces the amount of energy demanded for competition and defense, which can then be channeled to other purposes. Although sometimes taken to an extreme, challenges facing organisms in agricultural systems are not unique. Many natural ecosystems are also highly disturbed and unstable. Furthermore, coevolution among organisms, defined as reciprocal changes in their genetic compositions (Janzen, 1980), applies considerable selection pressure toward overcoming the physical and chemical barriers to resource utilization. For example, insect herbivores evolve physiological and behavioral mechanisms to overcome defensive compounds produced by their host plants, while the host plants evolve new compounds that will be effective against resistant herbivores. Host-plant coevolution is often lacking from agricultural systems because higher concentrations of defensive compounds in plants often make them less suitable for human consumption. This allows reallocations of resources by pest organisms toward other purposes, such as reproduction or metabolizing toxic xenobiotics. As a result of prior adaptation to their natural environments, potential pests are likely to possess a suite of heritable traits that facilitate their adaptation to a crop environment (Alyokhin and Chen, 2017). These often include the ability to detoxify a variety of poisons, high mobility concomitant with the ability to escape unfavorable conditions and to distribute offspring in space, diapause associated with an ability to wait out unfavorable periods and to distribute offspring in time, flexible life histories, behavioral plasticity, and high fecundity. In fact, pest evolution in anthropogenic systems (including agriculture) can be viewed as a coevolution between humans and their pests. By taking advantage of their existing genetic variations and new mutations, pests can adapt to a potentially very rewarding and resource-rich environment. In turn, humans can use their cognitive abilities to modify the environment in order to make it unfavorable to existing populations. This applies a new selection pressure on pest populations, with only the genotypes that best match the modified environment surviving to the next generation. These genotypes build up in numbers, eventually leading to the failure of whatever control methods had been applied against them and forcing humans to come up with new techniques. Thus far, it seems that the pests are usually one step ahead of the humans. The potato production system is a vivid example of challenges and opportunities facing organisms that inhabit agricultural ecosystems. Agronomic practices of growing potatoes involve intensive soil disturbance and a low accumulation of organic matter (Alyokhin et al., 2020). It is an annual crop, with substantial biomass removed from the system every year. Chemical use is very high (Chapter 11). Furthermore, potato foliage has naturally high concentrations of glycoalcoloids, which are rather toxic to a variety of herbivores. As a result, the pest complex of potato is characterized by a high

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degree of plasticity and adaptability and has shown a remarkable ability to persevere in the face of adversity. Not surprisingly, one of the most important potato defoliators, the Colorado potato beetle (Chapter 4), has historically been a poster child among applied entomologists because of its ability to adapt to human attempts of its control (Weber and Ferro, 1994; Alyokhin, 2009; Brevik et al., 2018a,b).

24.5 Evolutionary process of becoming a pest A pest is one of those concepts that everybody understands, yet it is difficult to define in a uniform and comprehensive way. From the commonsense point of view, a pest is any organism that we do not like. Economically speaking, it is a group of organisms that is more profitable to control than to tolerate. Ecologically, it is a population that competes with humans for the same limited resource. While the first two aspects of being a pest are rather anthropocentric and are heavily influenced by processes taking place in human society, competition is a biological phenomenon. Furthermore, the competitive abilities of a species or a population are a direct result of the evolutionary process. Some species become pests of a particular crop as a result of extending their natural habitats. For example, it is doubtful that a highly polyphagous green peach aphid (Myzus persicae) had to undergo profound evolutionary changes to become an important pest of potatoes, even though potato may have been a totally new host. In other cases, however, considerable adaptations are required before a population can match its environment well enough to reach damaging levels. Those often involve developing abilities to feed on a new host or prey, to counteract human management effects (in particular, pesticide applications), and to survive in previously unsuitable environments.

24.6 An obscure leaf beetle turns into a major pest of potatoes The Colorado potato beetle, Leptinotarsa decemlineata, is the most important insect defoliator of potatoes, and is extremely difficult to control (Alyokhin, 2009). Range expansion is an important evolutionary process in this species, with initial evolutionary plasticity serving as a foundation for adaptations that allowed it to become a truly global pest (Cingel et al., 2016). Colorado potato beetle has been thought to originate from the central highlands of Mexico, in what is currently the state of Morelos (Tower, 1906; Hsiao, 1981; Casagrande, 1987). Its ancestral host is buffalobur, Solanum rostratum. It has been suggested that the adhesive burs of S. rostratum clung to horses and cattle and were brought northwards with Spanish settlers into what is now the southern and central plains of the United States (Gauthier et al., 1981; Casagrande, 1987; Hare, 1990; Lu and Logan, 1994a). The beetles then followed its host plant after the northern populations of S. rostratum became established (Casagrande, 1987). The Colorado potato beetle was first collected and described by Thomas Say on S. rostratum in 1824 near the border of Iowa and Nebraska (Casagrande, 1985). The beetle’s host expansion onto potatoes was first documented in eastern Nebraska in 1859 (Walsh, 1865). After acquiring the ability to feed on potatoes, the beetle spread rapidly, reaching Iowa in 1861 (Walsh, 1865) and the eastern seaboard in 1874 (Riley, 1871). Recently, this “outof-Mexico” hypothesis has been put into doubt. Izzo et al. (2018) found that pest Colorado potato beetle populations are clearly derived from populations that occur within the US Plains states using mtDNA, AFLP, and microsatellite markers. While the mtDNA haplotype difference between US and Mexico beetles was significant enough for them to be considered separate species, some of the beetles from two locations in the central highlands of Mexico (Texcoco and Tlaxcala) could be grouped with both the US and Mexico populations when the STRUCTURE analysis was set to two populations (K ¼ 2). Within the genus Leptinotarsa, the Colorado potato beetle has the widest host range, feeding on at least 10 species of wild and cultivated Solanum (Hsiao, 1978; Neck, 1983; Jacques, 1988). Its diet breadth is matched with an extensive geographic range that far exceeds all other species within the genus (Hsiao, 1978; Neck, 1983; Jacques, 1988). Throughout its expanded range in the U.S., beetle populations have been found feeding on both cultivated (S. tuberosum, S. melongena, and S. lycopersicum) and wild (S. saccharoides, S. carolinense, S. rostratum, S. elaeagnifolium, and Chamaesaracha sp.) solanaceous plants (Hsiao, 1978; Lu and Logan, 1994a; Crossley et al., 2018b). Tower (1906) recorded considerable variations in behavior and performance associated with different host plants among geographically-isolated Colorado potato beetle populations. Despite the presence of potato plants in Mexico since at least the 16th century (Ugent, 1968), and significant production of potatoes in the Mexican states of Guanajuato, Sonora, Chihuahua, Sinaloa, and Nuevo Leon since at least the 1940s (SAGARPA, 2007), the Colorado potato beetle has never been recorded as a pest of potatoes, or of any other solanaceous crops, in that region (Casagrande, 1987; Cappaert, 1988). Larvae collected from native plants S. rostratum, S. angustifolium, and S. eleagnifolium from Morelos in Mexico and from Arizona and Utah in the U.S. showed reduced fecundity and survival on potato compared to pest populations collected

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from potato plants in the northeastern potato-growing region of the United States (Hsiao, 1978; Lu and Logan, 1995). Horton and Capinera (1988) found variation among beetle populations associated with wild and cultivated Solanum spp. in larval development, survival, and their tendency to diapause. Lu and Logan (1995) also found that the Mexican beetles showed strong ovipositional and feeding preferences for wild Solanum species (S. rostratum and S. eleangnifolium), whereas pest populations (Rhode Island, USA) did not discriminate among host plants. Hsiao (1981) crossed beetles from the population adapted to feeding on S. eleangnifolium with beetles adapted to feeding on potato but that performed poorly on S. eleangnifolium. The survival rate of progeny from the cross on S. eleangnifolium was intermediate between the survival rates of the two parental populations. All the information discussed in the preceding paragraph suggests that there is indeed a genetic basis underlying the differences in host use among Colorado potato beetle populations. It is also consistent with the mitochondrial DNA evidence presented by Izzo et al. (2018) that Mexican Colorado potato beetles should probably be considered a separate species that is closely related to, but still sufficiently different from, potato-adapted Colorado potato beetles that could be traced to the Central Plains in the U.S. At the same time, beetles that feed on potato and beetles that feed on wild Solanum spp., including those from Mexico, are able to mate with each other and produce viable offspring (Hare and Kennedy, 1986; Lu and Logan, 1994b,c). Therefore, they have been historically considered to be the same biological species. Of course, boundaries between biological species are notoriously difficult to define, and their very existence is sometimes questioned by evolutionary biologists (see Kunz, 2012 for an excellent discussion of this issue). Although ancestors of the current potato-feeding Colorado potato beetles may have originated from the U.S. rather than form Mexico, they were still feeding on solanaceous plants other than S. tuberosum. The latter is native to the highlands of Peru (see Chapter 1 for details) and was introduced within the beetle’s natural range by humans. Furthermore, the newly acquired ability to utilize potato as a host plant appears to be a form of host expansion rather than a host shift because potato-feeding beetles have not lost their ability to feed on S. rostratum (Lu and Logan, 1994a). Geographic beetle populations vary in their preference in feeding on potato with pest beetles showing less stringent host preferences (Izzo et al., 2014a). It is unclear how much evolutionary change had to occur in order to allow the Colorado potato beetle to expand onto potato. Harrison (1987) observed considerable variability in the acceptances of marginal hosts within beetle populations. Beetles feeding on marginal hosts sampled them to a smaller extent before initiating feeding compared to beetles rejecting such hosts. In other words, they perceived such plants as more acceptable. In areas where plentiful alternative hosts are present, their somewhat low quality may be at least partially compensated by their abundance. Based on those findings, Harrison (1987) hypothesized that relaxation of stabilizing selection in the newly colonized areas resulted in populations of more generalist feeders taking advantage of local Solanum spp. Unfortunately, that included the cultivated potato, S. tuberosum. Hufnagel et al. (2017) also reported that adult oviposition preferences do not always correlate with larval performance on chosen plants, thus contributing to a possible shift onto marginally suitable host plants. Another possible hypothesis is that a certain number of genotypes in ancestral Colorado potato beetle populations were specifically preadapted to feeding on potato (Hsiao, 1982; Crossley et al., 2018b). The increased ability to feed on potato foliage in derived populations has been the result of directional selection, with an increase in the frequency of potatoadapted genotypes at the expense of less adapted genotypes. Acquiring an improved ability to utilize potato was apparently not associated with a decreased ability to utilize buffalobur. The two hypotheses are not mutually exclusive. On the contrary, relaxation of stabilizing selection is a logical step before directional selection can shift the mean value of host plant acceptability toward potato. Over time, fine-tuning of beetle behavior and physiology may lead to specificity in favor of newly adopted hosts (Harrison, 1987). Regardless of its exact mechanism, Colorado potato beetle expansion onto potato is clearly a result of an evolutionary process (Lu and Logan, 1993, 1994b,c,d, 1995; Izzo et al., 2018). Ancestral beetle populations collected from S. rostratum generally have poor performance on potatoes (Izzo et al., 2014a). However, adaptation to new hosts by the Colorado potato beetles can proceed at a very fast pace. For example, beetles collected from their native host S. eleangnifolium in Arizona (Hsiao, 1981) suffered more than 80% mortality on S. tuberosum in the first generation. Most mortality came from nonacceptance of foliage by young larvae. However, after only five generations of selection on potato, mortality had dropped to less than 20% (Cappaert, 1988). Among the 10 Leptinotarsa species that are found in North America, the lineage that contains the Colorado potato beetle has higher level of heterozygosity, indicating that the phylogenetic position of the beetle within a more diverse lineage may contribute to its ability to evolve rapidly as a pest (Cohen et al., 2021). Deciphering the evolutionary process of host range expansion in the Colorado potato beetle is a fascinating task that might improve our understanding of biological evolution as a whole. It might also have some applied value in forecasting future host range expansion by potential pests and biological control agents introduced for suppression of exotic weeds. However, its main practical significance is likely to be in delaying the beetle’s adaptation to resistant potato varieties.

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Improving plant resistance to Colorado potato beetle damage is an underutilized yet potentially valuable tool in the beetle control arsenal (a detailed review of this method is provided in Chapter 14). Unfortunately, there is a serious concern that beetles can overcome host plant resistance just as easily as they can overcome exposure to insecticides (see below). For example, in the study by Groden and Casagrande (1986) oviposition and survival rates on resistant S. berthaultii became comparable to those on susceptible S. tuberosum after only two generations of selection. Pelletier and Smilowitz (1991) and França et al. (1994) confirmed the existence of genetic variability in several performance attributes for adaptation to S. berthaultii, although França et al. (1994) argued that adaptation is not always going to be as rapid as stated by Groden and Casagrande (1986). Similarly, Cantelo et al. (1987) observed gradual adaptation to feeding on resistant S. chacoense after 12 months of selection. Understanding mechanisms of Colorado potato adaptation to host plants is likely to improve the sustainability of using resistant potato varieties in the future. By resequencing 85 Colorado potato beetles across North America, Pélissié et al. (2021) found that beetle populations are geographically structured. Pest populations show only a modest decrease in nucleotide diversity compared to nonpest ancestral populations.

24.7 Insecticide resistance 24.7.1 Insecticide treadmill Insecticide resistance is a serious world-wide problem, with at least 489 different insect species having become resistant to about 400 different compounds (Mota-Sanchez and Wise, 2021). It is a typical example of directional selection: the chemical kills off susceptible genotypes, increasing both the frequency of resistant genes in the population and the mean dose of insecticide required to suppress insect densities below economically damaging levels. In some cases, selection by one chemical leads to resistance to other chemicals through shared physiological or biochemical mechanisms, a phenomenon known as cross-resistance. Since the midtwentieth century, commercial agriculture has been firmly stuck on the “insecticide treadmill,” the concept originally introduced by van der Bosch (1978). An insecticide is introduced by the agrochemical industry, pests develop resistances to it, a replacement chemical becomes available and is used until it also fails, and the cycle goes on and on. Furthermore, insecticide applications kill natural enemies, thus altering selection pressures experienced by pest species and further increasing the speed of the treadmill (van der Bosch, 1978). Just as development of insecticide resistance, insecticide treadmill is an evolutionary process, even though it is often not regarded as such. It is similar to a fundamental coevolutionary phenomenon known as The Red Queen Principle. This principle postulates that continuing change and adaptation is needed for a population to survive because its antagonists, including predators, prey, and competitors, also undergo constant evolutionary change that allows them to increase negative impact on this population. Both insect pests and human pest managers must constantly adapt to each other in order to stay in business (Alyokhin et al., 2015). Although ultimately unsustainable, the pesticide treadmill approach has been working reasonably well for some time. Unfortunately, the tradition of abundant and cheap broad-spectrum insecticides is coming to an end. Development and registration of new insecticides is an increasingly complicated and costly process. Furthermore, existing chemicals are being lost to resistance or removed from the market because of environmental concerns. As a result, preservation of existing products has become a progressively more important task for those involved in commercial agriculture (Alyokhin et al., 2008). Unfortunately, potato fields have the outstanding distinction of harboring two of the most resistant pests in the world: the Colorado potato beetle and the green peach aphid (Mota-Sanchez and Wise, 2021). Because of their serious damaging potentials, failure to control these two pests may have dire consequences for commercial growers.

24.7.2 Colorado potato beetle as a resistant superbug The Colorado potato beetle has been a major target for insecticide applications since 1864, and is credited with being an important driving force behind creating the modern insecticide industry (Gauthier et al., 1981). However, over the years this species has proven to be remarkably resilient, developing resistances to all major chemicals ever used against it (Alyokhin et al., 2008). Currently available international database (Mota-Sanchez and Wise, 2021), contains 300 cases of the Colorado potato beetle resistance to 56 different chemicals in North America, Europe, and Asia (Fig. 24.1). This number is likely an underestimation of the problem because some resistance cases might have been overlooked. For example, none of the cases reported from Russia (Leontieva et al., 2006; Benkovskaya et al., 2006, 2008a,b;

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Progression of insecticide resistance in the Colorado potato beetle (Mota-Sanchez and Wise, 2021).

Sukhoruchenko and Dolzhenko, 2008; Udalov and Benkovskaya, 2010) are included. Additional information is available from the database maintained at the Russian Plant Protection Institute, as well as from the atlas showing distribution and status of potato (Sukhoruchenko et al., 2017, 2018; Benkovskaya and Dubovskiy, 2020; see also Chapter 19). Insecticides that have so far failed to control the Colorado potato beetle are classified into 10 groups of chemicals and eight modes of action, including effects on the sodium channel for DDT and pyrethroids, inhibition of acetylcholinesterase for carbamates and organophosphates, blockage of chloride channels for cyclodienes, activation of GABA receptors for avermectins, agonist activity at nicotine acetylcholine receptors for neonicotinoids and spynosins, antagonism for the same receptors for nereistoxin compounds, and binding of receptors in the midgut cells by the endotoxin of Bacillus thuringiensis var. tenebrionis. Known mechanisms of resistance of the Colorado potato beetle to conventional insecticides include reduced insecticide penetration, target site insensitivity (including knock-down resistance and aceylcholinesterase insensitivity), and enhanced metabolism by esterases, carboxylesterases and monooxigenases (Rose and Brindley, 1985; Argentine et al., 1989; Ioannidis et al., 1991, 1992; Wierenga and Hollingworth, 1994, Anspaugh et al., 1995; Zhu et al., 1996, Lee and Clark, 1996; Clark et al., 2001). Frequently, multiple mechanisms of resistance have occurred in a single population, and different mechanisms of resistance have occurred in populations from different geographical locations. For instance, acetylcholinesterase from one strain (Michigan) was insensitive to carbamates, and the same enzyme from another strain (Long Island, NY) was insensitive to organophosphates (Wierenga and Hollingworth, 1993). The same Colorado potato beetles populations are often resistant to multiple chemicals (Ioannidis et al., 1991; Olson et al., 2000; Alyokhin et al., 2006, 2007). Sometimes this happens due to multiple selection pressures by different chemicals throughout the population’s history, For instance, the intense application of organophosphates in the 1980s and pyrethroids in the 1990s in the Rostov and Bashkortostan regions of Russian Federation resulted in the appearance of populations with resistances to both classes of insecticides (Vilkova et al., 2005; Benkovskaya et al., 2008a). In other cases, internal mechanisms that confer a resistance to one insecticide may also make the population less susceptible to another insecticide. For example, the rapid development of resistance to pyrethroids in Colorado potato beetle populations has been at least partially attributed to cross resistance with DDT (Harris and Svec, 1981). Similarly, selection with a carbamate insecticide has led to Colorado potato beetle resistance to organophosphate insecticides, and vice versa (Boiteau et al., 1987; Ioannidis et al., 1992). Alyokhin et al. (2007) found a significant correlation between the toxicities of two neonicotinoid insecticides, imidacloprid and thiamethoxam, even when populations previously exposed to thiamethoxam were excluded from the analysis. There was no statistically detectable difference in the toxicities of those insecticides between populations exposed to both chemicals and populations exposed to imidacloprid alone. The Colorado potato beetle populations have the dubious distinction as being one of fastest insects to evolve resistance to insecticides (Brevik et al., 2018b) The beetle has been named as No. Seven in the list of the Top 10 Most Significant

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Influences on the potato industry over the last 50 years (McCallum, 2012). Resistance reached critical levels in the early 1990s, when many potato growers completely ran out of chemical control options. The northeastern United States was the most severely affected area, but insecticide failures have been reported from a wide variety of geographic regions (Alyokhin et al., 2008). The situation improved dramatically after neonicotinoid insecticides became commercially available in 1995. Unfortunately, this group of chemicals followed the same fate as earlier compounds, with multiple cases of beetle resistance reported from a variety of places (Mota-Sanchez et al., 2006; Alyokhin et al., 2007; Udalov et al., 2010; Szendrei et al., 2012). Spinosad, which is another relatively new and highly effective chemical, also has lost its efficacy against some of the beetle populations (Alyokhin et al., 2015; Klein et al., 2021). Similarly, fipronil use resulted in a significant increase in the frequency of resistant beetles over a 10-year period (Kitaev et al., 2017). While other chemicals still successfully suppress the Colorado potato beetle (see Chapter 11), this clearly manifests another turn of the pesticide treadmill. Being native to North America, the Colorado potato beetle did not undergo genetic bottleneck typical of introduced pests (Hawthorne, 2001; Weber, 2003; Izzo et al., 2018). Therefore, it has been speculated that its populations retained genetic variability necessary to ensure evolutionary plasticity for their adaptations to adverse conditions. However, the relative importance of the last factor is unclear because resistance is also a problem in Europe, where the Colorado potato beetle is an introduced species (Weber, 2003), and where it shows marked reduction in neutral genetic variability compared to US populations (Grapputo et al., 2005). Furthermore, insecticide applications create genetic bottlenecks of their own by eliminating susceptible genotypes and thus reducing the genetic variability of the surviving population. Resistant founders may possess genetically determined neutral characteristics. For example, Udalov and Benkovskaya (2011) observed a much higher frequency of phenotypes with certain spot patterns on their heads, pronota, and elytra in the populations of insecticide-resistant beetles compared to the populations of susceptible beetles in the same area of Bashkortostan, Russian Federation. An overall diversity of spot patterns decreased over the 10-year period, presumably due to insecticide selection pressure. A similar process was observed in populations of the Colorado beetle in other areas of the Russian Federation: the Moscow region (Roslavtseva and Eremina, 2005), Bryansk region (Oleinikov et al., 2006), and Kaliningrad, Rostov, and Vologda regions (Vasil’eva et al., 2005). Subsequent laboratory experiments confirmed differential survival following exposure to insecticides for beetles with different spot patterns on their pronota (Udalov and Benkovskaya, 2011; Benkovskaya et al., 2008b). Colorado potato mating behavior is strongly directed toward maximizing genetic diversity of its offspring and may at least partially compensate for bottlenecks associated with colonizing new areas, switching to new hosts, and being sprayed with insecticides. Colorado potato beetles are highly promiscuous (Szentesi, 1985). Both males and females perform multiple copulations with different partners, with at least three matings required to completely fill the female’s spermatheca (Boiteau, 1988). For prediapause beetles, sperm from different copulations mixes and the female produces offspring that were fathered by different males (Boiteau, 1988; Alyokhin and Ferro, 1999a; Roderick et al., 2003). Males guard females following copulation and display aggressive behavior toward other males (Szentesi, 1985). However, the duration of such guarding is usually rather short; therefore, it is unlikely to prevent subsequent mating by other males (Alyokhin, unpubl. data). On the contrary, mated males increase their flight activity, probably to maximize their number of copulations with different mates (Alyokhin and Ferro, 1999b). Postdiapause females overwinter some viable sperm from the previous fall; however, mating in the spring significantly increases the number of their offspring (Ferro et al., 1991; Baker et al., 2005). Sperm from spring mating takes complete precedence over overwintered sperm from the previous year’s mating (Baker et al., 2005). The Colorado potato beetle’s impressive ability to evolve resistances to insecticides has also often been attributed to high concentrations of toxic glycoalkaloids in the foliage of solanaceous plants. Coevolution of the beetle and its host plants resulted in the development of the physiological capability to detoxify or tolerate poisons, including humanproduced xenobiotics (Ferro, 1993; Bishop and Grafius, 1996). As a consequence, insecticide-adapted genotypes may already exist in the population when exposed to a newly developed chemical, or they may arise due to a relatively small mutation (Alyokhin and Chen, 2017). Another contributing factor is generally high Colorado potato beetle fecundity in the environment of a potato field, usually allowing it to reach high population densities. This is a rather prolific species, with one female laying 300e800 eggs, or more (Harcourt, 1971). Furthermore, integrating dispersal with diapause, feeding, and reproduction allow the Colorado potato beetle to employ “bet-hedging” reproductive strategies, distributing its offspring in both space (within and between fields) and time (within and between years). This reduces the risk of catastrophic losses of offspring due to insecticides or crop rotation (Voss and Ferro, 1990). The resulting large populations increase the probability of random mutations, while their high growth rates ensure a rapid build-up in numbers of resistant mutants once such a mutation has occurred (Bishop and Grafius, 1996).

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Although the relative fitness of resistant mutants is often reduced compared to susceptible beetles due to the pleiotropic effects of resistant genes (Alyokhin et al., 2008), on rare occasions the selection of superiorly fit genotypes may be also solely responsible for the evolution of resistant strains. In this case, exposure to a toxic compound leads to the selection of the most robust genotypes (Richards et al., 2006). For example, Colorado potato beetles selected for feeding on a very unfavorable host S. berthaultii produced 1.7 times more eggs compared to the unselected strain when fed on a much more favorable S. tuberosum. Fecundity of the selected strain was reduced on S. berthaultii, but to levels not statistically significant from those recorded for the unselected strain on S. tuberosum (Groden and Casagrande, 1986). A completely overlooked factor potentially contributing to the rapid evolution of insecticide resistance in the Colorado potato beetle is hormesis. Hormesis (also known as hormoligosis) is a relatively wide-spread, yet often neglected, phenomenon that occurs when a chemical (or some other stressor) that is normally detrimental to an organism at higher doses is stimulatory for some biological parameters at very low doses. The stimulatory effects are believed to be the result of compensatory biochemical processes following a destabilization of normal homeostasis (Calabrese and Baldwin, 2001, 2003; Cohen, 2006; Dutcher, 2007; Calabrese, 2009). Hormesis has been demonstrated in Colorado potato beetles exposed to a number of stressors. Cutler et al. (2005) reported increase in the weight of second instars developing from eggs treated with sublethal concentration of the chitin synthesis inhibitor novaluron compared to the larvae hatching from the control eggs. Sublethal doses of several insecticides enhanced the cold and heat tolerances of adult beetles in experiments performed by Benkovskaya (2009). Also, Alyokhin et al. (2009) detected increased oviposition in adult beetles that had been exposed to novaluron soon after eclosing from pupae. However, none of the eggs collected in that experiment hatched; therefore, that particular case could not qualify as true hormesis (Guedes et al., 2009). It has been also shown that the Colorado potato beetles exposed to sublethal dosages of pyrethroids can grow bigger and have a better adult survival than those not exposed to the insecticides (Margus et al., 2019). Some of these effects may be passed also on the next generation. El Tahtaoui (1962) and Bajan and Kmitova (1972) observed increased fecundity in Colorado potato beetles surviving infection by the entomopathogenic fungus Beauveria bassiana (Bals.) Vuillemin, but that could have been also explained by selection toward the generally superior genotypes as discussed above. Field label rates of insecticides applied by farmers to their crops are, by definition, sublethal for resistant beetles. Also, the spray coverage can be spotty during application, leading to variable levels of exposure to the active compound. Therefore, it is possible that they have a hormetic effect on resistant organisms, at least partially compensating for their often reduced general fitness. As a result, the fitness differential between insecticide-exposed resistant insects and unexposed susceptible insects may be smaller compared to the differential between unexposed resistant and susceptible insects that is typically measured in laboratory resistance studies. Ultimately, this would lead to an increase in the net reproductive rates and intrinsic growth rates of resistant populations. In other words, hormetic effects may compensate, at least to a certain degree, for the fitness costs of resistant genes. It is also known that although the resistance against antibiotics in bacteria carries costs in the beginning, compensatory mutations will accumulate through repeated directional selection and reduce the costs of resistance, leading to situations where the resistant bacteria genotypes perform as well as the susceptible genotypes without the antibiotics (e.g., Normark and Normark, 2002). Of course, bacteria have much faster growth rates than the beetles, making evolution much faster. Still, it is also possible that this type of selection will take place in beetles, making the resistance problem even bigger. The selection pressure on Colorado potato beetle populations toward resistance development is usually enormous. Historically, commercial potato growers rely almost exclusively on insecticides for beetle control because, with the exception of crop rotation, other control techniques do not provide a feasible alternative (Harcourt, 1971; Casagrande, 1987; Bishop and Grafius, 1996). Moreover, the Colorado potato beetles have a narrow host range, and both larvae and adults feed on the same host plants. This limits the size of an unstructured refuge where susceptible genotypes may escape exposure to chemicals (Bishop and Grafius, 1996; Whalon and Ferro, 1998) by relocating to untreated volunteer potatoes or closely related solanaceous weeds. Not surprisingly, this is usually insufficient for reducing the frequency of resistant alleles below the economically significant level. Using genome resequencing of 85 beetles and comparative transcriptome data, Pélissié et al. (2021) tested how Colorado potato beetle resistance evolution conforms to different models of rapid evolution: rapid evolution on regulatory regions, consistent selection on novel mutations, and repeated selection on standing genetic variation. They found that repeated selection across distinct CPB populations, and resistance is derived from selection on different genes across different populations. Furthermore, each resistant population showed a particular transcriptional pattern of constitutive upregulation of candidate genes associated with insecticide resistance. Therefore, they concluded that insecticide resistance in the Colorado potato beetle is clearly polygenic and evolves from standing genetic variation.

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Although it is common to talk about insecticide resistance in the Colorado potato beetle as a species, a very important to keep in mind is that there is often a tremendous amount of variation among its populations in the levels and characteristics of resistance and in the speed of its evolution (e.g., Szendrei et al., 2012; Chen et al., 2014; Crossley et al., 2018a; Dively et al., 2020). Possible reasons for these differences and their implications for resistance management are discussed in Chapter 26.

24.7.3 Green peach aphid e resistance in a mostly parthenogenic organism The green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae), is a highly polyphagous cosmopolitan species that commonly colonizes potato plants. Its populations seldom reach densities sufficient to cause noticeable crop injury by sap feeding. However, the green peach aphid is a very competent vector of Potato Leaf Roll Virus and Potato Virus Y, both of which represent an ominous threat to commercial potato production (see Chapter 5 for more information on this group of insects). Green peach aphids have both winged (alatae) and wingless (aptera) body forms and alternate between several host species. They overwinter as eggs on their primary woody hosts (Rosaceae, especially Prunus spp.). After hatching in the spring and reproducing parthenogenetically on the primary host for at least two generations, the aphids start producing winged spring migrants that leave the primary host in search of suitable secondary hosts, which include several hundred species of herbaceous plants in addition to potatoes. Once an acceptable host is found, the spring migrants settle and reproduce (Shands et al., 1969, 1972; Shands and Simpson, 1971). The majority of the offspring produced by the spring migrants are wingless, but a few winged individuals are produced throughout the summer. The production of winged summer migrants is encouraged by overcrowding and poor quality of host plants (Muller et al., 2001). Many overlapping generations are produced during the summer. In the fall, a short day photoperiod induces production of sexual fall migrants that migrate back to the primary winter hosts. On primary hosts, female fall migrants give birth parthenogenically to wingless females, which then mate with male fall migrants and lay fertilized overwintering eggs. Populations that have both sexual and asexual generations are called holocyclic. In areas with warm climates, some green peach aphid populations do not produce sexual forms and persist year-round as parthenogenic forms on secondary hosts. Such populations are known as anholocyclic. Similar to Colorado potato beetles, green peach aphids have shown a rather remarkable ability to evolve resistances to a variety of insecticides (Bass et al., 2014). According to a currently available data compilation (Mota-Sanchez and Wise, 2021), there are at least 475 cases of resistances to 80 different chemicals in North America, South America, Europe, Asia, and Oceania (Fig. 24.2). As is the case with Colorado potato beetles, this is likely to be an underestimation of the number

FIG. 24.2 Progression of insecticide resistance in the green peach aphid (Mota-Sanchez and Wise, 2021).

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of resistant populations. Resistances to organophosphates, pyrethroids, and pirimicarb (a dimethyl carbamate) are now widespread (Fenton et al., 2010). Resistance to neonicotinoids, particularly to imidacloprid, is also a problem (Foster et al., 2003a; Srigiriraju et al., 2010; de Little et al., 2017). Insecticide resistance has arisen independently in different green peach aphid populations on a number of occasions. Its mechanisms include mutations of target proteins d which decreases their affinity for binding insecticide molecules d as well as the enhanced production of metabolic enzymes, which detoxify and/or sequester insecticides (Fenton et al., 2010; Bass and Field, 2011). For example, target site mutation known as MACE (modified acetylcholinesterase) confers virtual immunity to pirimicarb. Knock-down resistance, which is also known in the Colorado potato beetle (see above), is effective against pyrethroid insecticides. Overproduction of metabolic enzymes confers a strong resistance to organophosphates (Fenton et al., 2010). A major evolutionary driver of insecticide resistance in the green peach aphid is gene amplication: the reiteration of a segment of DNA to generate one or more additional copies in the genome (Bass and Field, 2011). This results in the production of metabolic enzymes in amounts sufficient for the detoxification of otherwise lethal concentrations of toxic chemicals. Furthermore, this mechanism may play a role in pesticide resistance conferred by target-site insensitivity. For example, duplication of a g -aminobutyric acid (GABA) receptor subunit gene has been reported in association with the green peach aphid resistance to the cyclodiene insecticide endosulfan (Anthony et al., 1998). Review of recently published studies (Bass and Field, 2011) indicates that gene amplification may be a fairly common mechanism of adaptive evolution in arthropods, and that certain genomic loci may be “hot spots” for gene duplication, as evidenced by parallel evolution in several arthropod species. However, the green peach aphid’s genome appears to have a special propensity for gene amplification (Bass and Field, 2011). As discussed in the beginning of this chapter, evolution is impossible without initial variation within a given population. In asexual organisms, genotypic variation arises from mutations. In sexual organisms, it is the result of a combination of mutations and recombination during meiosis and fertilization. Green peach aphids are capable of both sexual and asexual reproduction, although some populations have lost their ability for the former. Their sexual stages provide an opportunity to increase the overall genetic diversity of a population, while rapidly reproducing asexual stages provide a means for a quick increase in the frequency of well-adapted genotypes. Evolutionary successful aphid genotypes are capable of rapidly expanding their ranges and colonizing new geographic areas, both on their own and with human assistance. Winged forms can be carried by wind over considerable distances. Perhaps more importantly, small body sizes and somewhat cryptic habits promote the spread of green peach aphids by humans moving around their host plants (Fenton et al., 2010). As a result, there are several common and widespread clones, whose successes appear to stem from selection for insecticide resistance in agriculture (Fenton et al., 2005, 2010; Zamoum et al., 2005; Kasprowicz et al., 2008; van Toor et al., 2008). The number of such genotypes is still relatively limited, despite the possibility of resistance genes combining into more genotypes in sexual populations each year (Fenton et al., 2010). Although gene flow is important in spreading resistance to new areas, similar resistant phenotypes have been also shown to evolve independently in geographically separated green peach aphid populations (Gillespie et al., 2008). Unlike the Colorado potato beetle, the green peach aphid is a highly polyphagous species. Many of its host plants (including potato and tobacco) produce highly toxic phytochemicals in their foliage. Therefore, it is likely that the green peach aphid had naturally evolved physiological mechanisms to deal with a variety of poisons (Alyokhin and Chen, 2017). Polyphagy also may decrease selection pressure on aphid populations by creating refuges on alternative hosts growing outside of the treated crop area. For example, Rubio-Meléndezet al. (2018) found higher frequency of resistant alleles on the insecticide-treated peach trees than on the untreated nearby weeds. Similar to the situation discussed above for the Colorado potato beetle, hormetic effects of insecticide applications may increase the fitness of exposed resistant aphids (Lowery and Sears, 1986), thus expediting selection toward resistant populations. For example, Tang et al. (2015) observed increased reproductive output in green peach aphids exposed to a sublethal concentration of sulfoxaflor. In another example, Sial et al. (2018) reported that exposure to sublethal doses of acetamiprid and imidacloprid significantly increased fecundity of the affected green peach aphids. Furthermore, there was a significant upregulation of CYP6CY3 gene associated with resistance to neonicotinoids.

24.7.4 Resistance to nonchemical control methods Pesticide resistance is commonly cited as one of the main reasons for switching from a chemical-based pest management system to a system based on using nonchemical alternatives. Although such an argument is definitely valid, it is important to remember that pests can also adapt to nonchemical methods of control. Effective nonchemical techniques apply a considerable selection pressure on pest populations, which in some cases might be even stronger than the pressure applied

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by synthetic chemicals. Therefore, the evolution of resistances to nonchemical methods should not be a surprise to anyone. Since pest control in commercial agriculture has been dominated by pesticides for many decades, most reported cases of pest adaptation involve resistances to toxic chemicals. As more alternative methods enter (or, in some cases, reenter) mainstream agriculture, their increasing failures due to resistance development in pest populations should be expected. Several existing studies confirm that green peach aphids are fully capable of evolving resistances to biological control agents. The parasitoid wasp Aphidius colemani (Hymenoptera: Braconidae) is routinely released by greenhouse growers to control this pest, and this method has typically been found to be successful (Gillespie et al., 2008). However, in 2002 and 2003, growers in British Columbia experienced severe green peach aphid outbreaks. The clone involved in those outbreaks showed reduced vulnerability to parasitoids and a higher reproductive rate compared to the other two clones tested in the same study (Gillespie et al., 2008). Aphids from the resistant clone were less frequently stung by wasps, and a lower proportion of these stings resulted in mummy development. Herzog et al. (2007) conducted a laboratory study in which caged aphid populations were maintained for six to eight generations with or without A. colemani. Populations confined with A. colemani evolved to contain only a single, highly resistant clone. The control treatment consisted of a diverse suite of clones, although their relative frequencies shifted toward predominance of more prolific genotypes. Except for several cases of adaptation to resistant potato species that were already discussed above, there are no reports of Colorado potato beetle resistances to nonchemical methods of its control. However, there is certainly a good possibility of such a development. For example, the efficiency of annual crop rotation for reducing field colonization by overwintering adults could be compromised by multi-year diapause. Extended diapause is not unusual in the Colorado potato beetle (Isely, 1935; Ushatinskaya, 1962, 1966; Biever and Chauvin, 1990; Tauber and Tauber, 2002). In some populations, as many as 21% of overwintering adults emerge after spending 2 years in the soil (Biever and Chauvin, 1990). Selection for multiyear diapause has been responsible for the eventual failure of annual crop rotation to control another leaf beetle, the northern corn rootworm (Diabrotica barberi) (Levine et al., 1992). Obviously, potential problems with insect adaptation do not mean that nonchemical techniques should not be used for pest control. However, they should not be treated as an everlasting silver bullet solution that is sustainable by definition. Resistance management discussed in the following section is an important consideration for all methods of pest management.

24.7.5 Resistance management Successful pest control depends on increasing mismatches between pestiferous organisms and their environments. Application of toxic chemicals achieves this goal by creating a highly unfavorable environment for target pests. It also applies a very strong selection pressure toward resistance development. After resistant genotypes take over the population, this mismatch effectively disappears. Moreover, conditions may become more favorable for them because of the removal of susceptible competitors and natural enemies. Resistance management approaches are based on either restoring the mismatch between newly resistant pests and their habitat or by decreasing selection pressure on pest populations before they become resistant. In practice, the former is usually achieved by rotating insecticides with different modes of action. Although despized by the proponents of sustainable agriculture, the pesticide treadmill has been serving the farming community fairly well. A steady flow of new products to the pesticide market allowed for the quick and relatively painless replacement of failing compounds with new chemistries. However, developing new active ingredients is an increasingly difficult and expensive task (Alyokhin et al., 2008). As a result, it is safe to say that the era of abundant and cheap pesticides is largely over. Therefore, relying on the chemical industry to keep inventing new products is a risky approach. Selection pressure is usually reduced by leaving untreated crop areas within or near treated fields. Susceptible populations persist within these plots and mate with newly resistant genotypes that arise in adjacent treated areas. However, most commercial growers perceive leaving part of their crop untreated as risky and are reluctant to do it on their farms. Furthermore, a number of assumptions need to be met for this refuge-based strategy to succeed. First, resistant alleles should be at least partially recessive, which means that progeny (heterozygotes at the resistance locus) of one resistant parent and one susceptible parent are not as resistant as their resistant parent and can be killed by a sufficiently high dose of an insecticide. This is usually true for the Colorado potato beetle (Alyokhin et al., 2008), but less applicable for the green peach aphids, which reproduce parthenogenically for most of their life cycles. Secondly, in the absence of pesticides, resistant alleles should be associated with the decreased fitness of resistant individuals, such as fewer offspring, shorter life spans, longer times of development, lower tolerances of unfavorable conditions, etc. This way, resistant individuals are at a selective disadvantage in the refuge, and their frequency there remains relatively low. Reduced fitness is indeed very common among insecticide-resistant insects, including the Colorado potato beetle and the green peach aphid (Alyokhin

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et al., 2008; Fenton et al., 2010). It is also associated with the multi-year diapause in the Colorado potato beetle, with females diapausing for 2 years having lower fertility and lower larva-to-adult survivorship compared to females diapausing for 1 year (Margus and Lindström, 2020). Finally, there should be sufficient movement between main crop and the refuge with subsequent mating upon arrival, so that resistant individuals do not mate with each other and do not leave highly resistant offspring. Although both the Colorado potato beetle and the green peach aphid can be highly mobile and travel over long distances, there is also evidence that significant segments of their populations do not move far and probably interbreed (Alyokhin et al., 2008; Fenton et al., 2010). Practicing integrated pest management by combining multiple techniques and using economic thresholds is by far the best approach to delaying the evolution of resistance. This creates a complex environment with multiple factors that are unfavorable to the target pest. Simultaneous adaptations to multiple unrelated influences, which may be as different as toxic chemicals, mechanical barriers, and predators, are likely to require profound genetic changes. As a result, it is statistically less probable than the adaptation to a single factor stemming from a single-gene mutation. Furthermore, resistance to one factor may be offset by increased susceptibility to another factor. For example, esterase-based insecticide resistance was negatively correlated with resistance to parasitoids in several clones of the green peach aphid (Gillespie et al., 2008; Foster et al., 2003b, 2007). Also, using economic thresholds eliminates unnecessary insecticide applications, thus reducing selection pressure on target pests.

24.7.6 Epigenetic considerations While harnessing the principles of Darwinian evolution is useful for a better understanding and management of insecticide resistance, relying exclusively on such an approach may also have its limitations. Perhaps the biggest paradox of insecticide resistance evolution is its very existence, despite the fact that undergoing strong selection episodes caused by insecticide applications reduces insect population size and genetic variation (Brevik et al., 2021). As discussed above, this should decrease insect ability to adapt to subsequent exposure to new chemicals. Yet, insects retain this ability seemingly in perpetuity, resulting in a continuous rotation of the insecticide treadmill (Alyokhin et al., 2015). There is a mounting body of evidence that changes in gene expression without changing the underlying DNA sequence of an organism, collectively known as epigenetics, may be responsible for this apparent inconsistency (Brevik et al., 2018a, 2021). DNA methylation is the addition of a methyl group to cytosines that alters gene transcription and is widespread in insects (Thomas et al., 2020). Exposure to imidacloprid led to decreases in global DNA methylation for parents and their progeny in the Colorado potato beetle. Many of the altered sites were located within genes associated with insecticide resistance, such as cytochrome P450s, confirming their likely importance for the emergence of resistant phenotypes (Brevik et al., 2021). Along the same lines, when methylation was lost on the esterase genes that are involved in insecticide detoxification in the green peach aphid, affected organisms lost their insecticide-resistant properties (Field et al., 1989). That strongly suggested that methylation of esterase genes likely led to their increased expression, while demethylation led to their suppression. Methylation patterns also persisted over multiple generations, confirming their heritability (Field et al., 1989; Brevik et al., 2021). Epigenetic process triggered by exposure to insecticides and changing expression of the existing genes responsible for the detoxification of these insecticides is likely to result in a significantly quicker adaptation of affected populations compared to a classical multi-generational selection process. Furthermore, they will not cause severe bottlenecks characteristic of survival of very few resistant mutants typical for Darwinian selection. As a result, their understanding has large practical implications in safeguarding the existing active ingredients. Unfortunately, research in this area is still insufficient, although substantial advanced have been made in recent years (Brevik et al., 2021). Advances in this relatively new field of epigenetics are likely to shed additional light on Colorado potato beetle’s evolution into a major global pest. Directional selection due to higher survival of favorable genotypes is an important process. However, it is increasingly likely that effective regulation of large gene clusters responsible for important physiological processes, such as detoxification of natural and synthetic xenobiotics or induction of photoperiodic reactions, are also making important contributions to this species’ impressive adaptability to a range of adverse conditions (Cingel et al., 2016; Clements et al., 2017; Kaplanoglu et al., 2017; Schoville et al., 2018; Nikonorov et al., 2018).

24.8 Interactions with abiotic environment Insect adaptation to abiotic conditions (temperature, water availability, solar irradiation, etc.) is an increasingly important consideration in pest management. First, extensive human traffic and commerce results in the constant introduction of potentially pestiferous species to new areas. Predicting a pest’s ability to adapt to conditions typical of a newly colonized

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location is essential for forecasting future pest outbreaks and taking the actions necessary for their prevention. Secondly, changing climate is likely to apply new selection pressures on pest populations inhabiting a given geographic area as well as opening previously unsuitable areas for colonization and range expansion. Range expansion to new environments requires that the species in question adjusts its life cycle to the new environment. The Colorado potato beetle currently continues expanding its range, often with dire economic consequences for newly colonized areas (Alyokhin, 2009). Researchers have tried to understand the limits of range expansion of the Colorado potato beetle by testing its performance in various abiotic conditions. Similar to the majority of insects, two important abiotic factors have been suggested for limiting the Colorado potato beetle’s range expansions: temperature and light regime. Temperature is important for ectotherms, as all life stages are affected by its changes. Typically, growth is reduced by temperature decreases from the optimum (Logan et al., 1985), which can in turn have various effects on other life-history traits, such as size (Boman et al., 2008; Lyytinen et al., 2008). Thus, the beetle cannot invade areas where it cannot complete its development from egg to adult, as only the adult stages survive over winter. Temperature can also directly limit range expansion if the individuals have no means of surviving temperature extremes. For instance, the thermal extremes during winters (freezing) have been suggested to limit the range expansion of the Colorado potato beetle in many areas (see Lehmann et al., 2020). The supercooling point in Colorado potato beetles ranges between 19 and 5 C and is related to the water content of the body (Costanzo et al., 1997; Izzo et al., 2014b). However, beetles that dig into the ground to overwinter may not encounter these extreme temperatures because soil temperatures are much warmer than ambient temperatures. Beetles are also rather tolerant to cold exposures during their larval stage, as only 3.1% die when exposed to 4 C (Lyytinen et al., 2009). Furthermore, they can adapt, to some extent, to cold temperatures by upregulating heat shock proteins (Lyytinen et al., 2012) but lack physiological tools to manage especially thermal stress during winters (Lehmann et al., 2020). However, geographic populations of Colorado potato beetles vary in terms of both behavioral and physiological adaptations for winter survival (Izzo et al., 2014b; Lehmann et al., 2014, 2020). Climate change models suggest that beetles with low diapause termination thresholds will be able to successfully complete the second summer generation in Europe (Pulatov et al., 2016). Temperature has been also shown to affect Colorado potato beetle interactions with their host plants. De Wilde et al. (1969) reported that, when given a choice between potato and bittersweet nightshade, S. dulcamara, the beetles chose potato more frequently at low temperatures, but S. dulcamara at high temperatures. Similarly, beetle survival on horsenettle, S. carolinense, increased with increasing temperatures (Hilbeck and Kennedy, 1998). The mechanisms behind this phenomenon are unknown and may involve temperature-mediated changes in both insects and plants. Regardless, the observed temperature mediation may have important implications for range expansion and host adaptation in the Colorado potato beetle (Hilbeck and Kennedy, 1998). A photoperiod gives cues for the timing of the life cycle for many temperate insects. Therefore, it has been identified as an important limiting factor for range expansion. The Colorado potato beetle is a multivoltine species in the areas where conditions are suitable (de Kort, 1990), and it has a facultative diapause that has to be initiated at the correct time. The diapause initiation is very crucial because the decision cannot be reversed. Since winters in northern latitudes arrive early in relation to the photoperiod, there is selection to enter diapause under relatively long-day conditions. Species invading those areas from the south must, therefore, be able to adjust their diapause behavior to overwinter successfully (Yamanaka et al., 2008; Lehmann et al., 2015). The correct timing of diapause is assured by having a sensitive stage that responds to a shortening of the photoperiod (Lefevere and de Kort, 1989; Noronha and Cloutier, 1998, 2006). The Colorado potato beetle has a photosensitive phase primarily just after adult emergence from a pupa, but also to some degree at the last larval stage (de Wilde et al., 1959). The critical day length is dependent on the population, ranging between 12 h of light at 32 N latitude (Tauber et al., 1988) and 15e16 h of light at latitudes above 45 N (Danilevsky, 1965, de Wilde et al., 1959; Tauber et al., 1988; Lehmann et al., 2015). Furthermore, it has been estimated that some proportion of beetles will enter diapause in photoperiods longer than a 16 h day length (Danilevsky, 1965). In Europe, 10%e24% of beetles reared in long day conditions (20L:4D) will enter diapause immediately when allowed, irrespective of their origin, suggesting that not all beetles respond to light conditions similarly (Peferoen et al., 1981; Piiroinen, 2010). Although these beetles reared in long day conditions entered diapause, their survival was lower, probably because they had not accumulated enough resources for successful completion of diapause (Lehmann et al., 2012, 2014, 2015). The beetle also responds to photoperiod responses of the host plant, so the beetle may use multiple mechanisms to initiate diapause (Izzo et al., 2014c). Nevertheless, polymorphism existing for diapause initiation can be crucial when populations are exposed to new conditions. The question of range expansion is more complicated than performance at a certain temperature or at a certain light regime. It is also related to the potential to adapt to new environments. Such a potential is determined by genetic variation in traits that are under selection when a population is exposed to new conditions. Although there is extensive experimental evidence for beetle performances under different conditions, the additive genetic variation in many traits has not been

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adequately assessed (but see Boman et al., 2008). The retrospective analysis of the beetle’s geographic distribution (EPPO, 2011) suggests that the beetle has had the potential to adapt to various climatic conditions. Although the beetle did lose considerable genetic variation when invading Europe (see also Piiroinen et al., 2013), it managed to expand its range almost as quickly as it did in North America (Grapputo et al., 2005). The established populations still have additive genetic variance in development rates, and thus have the potential to respond to changes in summer temperatures (Boman et al., 2008; Lyytinen et al., 2008). However, successful overwintering also requires adaptive genetic changes in diapause-related behaviors (Lehmann et al., 2014), metabolism, or body mass. Insufficient genetic variation in these traits is likely to limit the Colorado potato beetle’s potential to respond to selection due to harsher winters, which in turn could restrict range expansion (Piiroinen et al., 2011; see also Lehmann et al., 2020). Unfortunately, some of these traits are difficult to measure. Furthermore, genetic potential is the property of a population; therefore, results obtained for one population may not be representative of other populations of interest.

24.9 Human turn to adapt? Humans are recognized to be the biggest evolutionary force operating at the moment (Palumbi, 2001). While this is certainly true, it is important to recognize that we are also at the receiving end of the selection pressures that we generate. New technologies, such as the full sequencing of the Colorado potato beetle genome and gene silencing, have the potential to provide important insight on the evolutionary success of insect pests (Schoville et al., 2018). Despite all technological advances, pest and disease outbreaks continue plaguing humankind, sometimes at an increasing frequency and/or severity. This is in large part due to the plasticity of pestiferous species and their abilities to adapt to whatever poison we are trying to unleash against them. Furthermore, human health and the environment often fall victim to the collateral damage resulting from our mostly xenobiotic-based endeavors. Clearly, a simplistic approach of measuring pest management success as the number of dead “bugs” is extremely near-sighted. Instead, this statistic should be treated as the number of dead susceptible genotypes, and the evolutionary consequences of their removal from a population should be addressed before creating an economically important problem. On the other hand, it is important to examine further how human crop management processes themselves may contribute to the rapid evolution of insect pests. For instance, insecticide exposure may have carry-over effects into subsequent generations that enables rapid resistance evolution (Brevik et al., 2018a). Incorporating our knowledge of fundamental evolutionary processes into pest control practices will take time and effort, but it is essential for maximizing their efficiency. Essentially, we need to learn to better adapt to the environment of our own creation.

24.10 Conclusions Studies in evolutionary theory have been historically considered to be fundamental in nature and lacking immediate practical applications. However, currently there is an increasing appreciation of their importance in improving efficiency and sustainability of agricultural production. Applying evolutionary principles to processes taking place in agricultural ecosystems, such as adaptation to host plants or development of insecticide resistance, provides additional opportunities for their manipulation to our benefit. In addition, theoretical understanding of insect adaptations to abiotic conditions helps predicting range expansions and future pest outbreaks. These are the prime examples of the synergy resulting from bridging a gap between fundamental and applied sciences.

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Schoville, S.D., Chen, Y.H., Andersson, M.N.N., Benoit, J.B., Bhandari, A., Bowsher, J.H., Brevik, K., Cappelle, K., Chen, M.-J.M., Childers, A.K., Childers, C., Christiaens, O., Clements, J., Elpidina, E.N., Engsontia, P., Friedrich, M., Garcia-Robles, I., Goswami, C., Grapputo, A., Gruden, K., Grynberg, M., Henrissat, B., Jennings, E.C., Jones, J.W., Kalsi, M., Khan, S.A.A., Kumar, A., Li, F., Lombard, V., Ma, X., Martynov, A., Miller, N.J., Mitchell, R.F., Munoz-Torres, M., Muszewska, A., Oppert, B., Palli, S.R., Panfilio, K.A., Pauchet, Y., Perkin, L.C., Petek, M., Poelchau, M.F., Record, E., Rinehart, J.P., Robertson, H.M., Rosendale, A.J., Arroyo, V.M.M.R., Smagghe, G., Szendrei, Z., Szuter, E.M., Thomas, G.W.C., Torson, A.S., Jentzsch, I.M.,V., Weirauch, M.T., Yates, A.D., Yocum, G.D., Yoon, J.-S., Richards, S., 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Sci. Rep. 2, 1931. Shands, W.A., Simpson, G.W., Wave, H.E., 1969. Canada plum, Prunus nigra Aiton, as a primary host of the green peach aphid, Myzus persicae (Sulzer), in northeastern Maine. Maine Agric. Exp. Stn. Bull. V. 39. Shands, W.A., Simpson, G.W., 1971. Seasonal history of the buckthorn aphid and suitability of alder-leaved buckthorn as a primary host in northeastern Maine. Maine Life Sci. Agric. Exp. Stn. Bull. V. 51. Shands, W.A., Simpson, G.W., Wave, H.E., 1972. Seasonal population trends and productiveness of the potato aphid on swamp rose in northeastern Maine. Maine Life Sci. Agric. Exp. Stn. Bull. V. 52. Sial, M.U., Zhao, Z., Zhang, L., Zhang, Y., Mao, L., Jiang, H., 2018. Evaluation of insecticide induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Sci. Rep. 8, 16601. Smith, T.B., Bernatchez, L., 2008. Evolutionary change in human altered environments. Mol. Ecol. 17, 1e8. Srigiriraju, L., Semtnera, P.J., Bloomquist, J.R., 2010. Monitoring for imidacloprid resistance in the tobacco-adapted form of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in the eastern United States. Pest Manag. Sci. 66, 676e685. Stearns, S.C., 1989. The evolutionary significance of phenotypic plasticity e phenotypic sources of variation among organisms can be described by developmental switches and reaction norms. Bioscience 39, 436e445. Stearns, S.C., Koella, J.C., 1986. The evolution of phenotypic plasticity in life-history traits e predictions of reaction norms for age and size at maturity. Evolution 40, 893e913. Sukhoruchenko, G.I., Dolzhenko, V.I., 2008. Problems of resistance development in arthropod pests of agricultural crops in Russia. EPPO Bull. 1, 119e126. Sukhoruchenko, G.I., Vasilyeva, T.I., Ivanova, G.P., 2017. Insecticide resistance development in Colorado potato beetle populations from different regions of European part of Russia. Plant Prot. News. 8, 3e8 (In Russian). Sukhoruchenko, G.I., Vasilyeva, T.I., Ivanova, G.P., Volgaryov, S.A., 2018. Situation with Colorado beetle Leptinotarsa decemlineata Say resistance to insecticides in the North-Western region of Russia. Plant Prot. News. 97, 49e55 (In Russian). Szendrei, Z., Grafius, E., Byrne, A., Ziegler, A., 2012. Resistance to neonicotinoid insecticides in fieldpopulations of the Colorado potato beetle (Coleoptera: Chrysomelidae). Pest Manag. Sci. 68, 941e946. Szentesi, A., 1985. Behavioral aspects of female guarding and inter-male conflict in the Colorado potato beetle. Res. Bull. 704. In: Ferro, D.N., Voss, R.H. (Eds.), Proceedings, Symposium on the Colorado Potato Beetle. XVIIth International Congress of Entomology, vol. 347. Mass. Agric. Exp. Stn. Circ., pp. 127e137 Tang, Q., Xiang, M., Hu, H., An, C., Gao, X., 2015. Evaluation of sublethal effects of sulfoxaflor on the green peach aphid (Hemiptera: Aphididae) using life table parameters. J. Econ. Entomol. 108, 2720e2728. Tauber, M.J., Tauber, C.A., 2002. Prolonged dormancy in Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): a ten-year field study with implications for crop rotation. Environ. Entomol. 31, 499e504. Tauber, M.J., Tauber, C.A., Obrycki, J.J., Gollands, B., Wright, R.J., 1988. Voltinism and the induction of aestival diapause in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrysomelidae). Ann. Entomol. Soc. Am. 81, 748e754. Thomas, G.W.C., Dohmen, E., Hughes, D.S.T., Murali, S.C., Poelchau, M., Glastad, K., Anstead, C.A., Ayoub, N.A., Batterham, P., Bellair, M., Binford, G.J., Chao, H., Chen, Y.H., Childers, C., Dinh, H., Doddapaneni, H.V., Duan, J.J., Dugan, S., Esposito, L.A., Richards, S., 2020. Gene content evolution in the arthropods. Genome Biol. 21, 15. Tower, W., 1906. Investigation of Evolution in Chrysomelid Beetles of the Genus Leptinotarsa. Carnegie Institution of Washington, Washington. Udalov, M.B., Benkovskaya, G.V., 2010. Polymorphism CoxI gene of Colorado potato beetle in South Ural populations. Resist. Pest Manage. News. 2, 29e32. Udalov, M.B., Benkovskaya, G.V., 2011. Change in the polymorphism level in populations of the Colorado potato beetle. Russ. J. Genet. Appl. Res. 5, 390e395. Udalov, M.B., Benkovskaya, G.V., Khusnutdinova, E.K., 2010. Population structure of the Colorado potato beetle in the Southern Urals. Russ. J. Ecol. 2, 159e166. Ugent, D., 1968. The potato in Mexico: geography and primitive culture. Econ. Bot. 22, 108e123. Ushatinskaya, R.S., 1962. Colorado potato beetle diapause and development of its multi-year infestations. Zashchita Rastenii (Mosc.) 6, 53e54 (In Russian). Ushatinskaya, R.S., 1966. Prolonged diapause in the Colorado beetle and conditions of its development. In: Arnoldi, K.V. (Ed.), Ecology and Physiology of Diapause in the Colorado Beetle. Nauka, Moscow, pp. 120e143. van der Bosch, R., 1978. The Pesticide Conspiracy. Doubleday, Garden City, NJ. van Toor, R.F., Foster, S.P., Anstead, J.A., Mitchinson, S., Fenton, B., Kasprowicz, L., 2008. Insecticide resistance and genetic composition of Myzus persicae (Hemiptera: Aphididae) on field potatoes in New Zealand. Crop Protect. 27, 236e247.

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Vasil’eva, T.I., Ivanova, G.P., Ivanov, S.G., 2005. Changes of the phenotypic structure of the Colorado potato beetle population depending on the intensity of using insecticides. In: Proceedings of the Second All-Russian Congress on Plant Protection. Phytosanitary Remediation of Ecosystems, St. Petersburg, Russia, pp. 14e15 (In Russian). Vilkova, N.A., Sukhoruchenko, G.I., Fasulati, S.R., 2005. Strategy of agricultural plants protection from adventive species of phytophagous insects by the example of Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera, Chrysomelidae). Plant Prot. News 1, 3e15. Voss, R.H., Ferro, D.N., 1990. Phenology of flight and walking by Colorado potato beetle (Coleoptera: Chrysomelidae) adults in western Massachusetts. Environ. Entomol. 19, 117e122. Walsh, B.D., 1865. The new potato bug and its natural history. Practical. Entomol. 1, 1e4. Weber, D., 2003. Colorado beetle: pest on the move. Pestic. Outlook 14, 256e259. Weber, D.C., Ferro, D.N., 1994. Colorado potato beetle: diverse life history poses challenge to management. In: Zender, G.W., Jansson, R.K., Powelson, M.L., Raman, K.V. (Eds.), Advances in Potato Pest Biology and Management. APS Press, St. Paul, MN, pp. 54e70. Whalon, M.E., Ferro, D.N., 1998. Bt-potato resistance management. In: Mellon, M., Rissler, J. (Eds.), Now or Never: Serious New Plans to Save a Natural Pest Control. UCS, Cambridge, MA, pp. 107e136. Wierenga, J.M., Hollingworth, R.M., 1992. Inhibition of insect acetylcholinesterase by the potato glycoalkaloid-chaconine. Nat. Toxins 1, 96e99. Wierenga, J.M., Hollingworth, R.M., 1993. Inhibition of altered acetylcholinesterases from insecticide-resistant Colorado potato beetles (Coleoptera: Chrysomelidae). J. Econ. Entomol. 86, 673e679. Wierenga, J.M., Hollingworth, R.M., 1994. The role of metabolic enzymes in insecticide- resistant Colorado potato beetles. Pest. Sci. 40, 259e264. Yamanaka, T., Tatsuki, S., Shimada, M., 2008. Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest. J. Anim. Ecol. 77, 585e596. Zamoum, T., Simon, J.C., Crochard, D., Ballanger, Y., Lapchin, L., Vanlerberghe-Masutti, F., 2005. Does insecticide resistance alone account for the low genetic variability of asexually reproducing populations of the peachepotato aphid Myzus persicae? Heredity 94, 630e639. Zhu, F., Moural, T.W., Nelson, D.R., Palli, S.R., 2016. A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple Cytochrome P450s. Sci. Rep. 6, 1e10. Zhu, K.Y., Lee, S.H., Clark, J.M., 1996. A point mutation of acetylcholinesterase associated with azinphosmethyl resistance and reduced fitness in Colorado potato beetle. Pestic. Biochem. Physiol. 55, 100e108.

Chapter 25

Ecology of a potato field Andrei Alyokhina and Vadim Kryukovb a

School of Biology and Ecology, University of Maine, Orono, ME, United States; bInstitute of Systematics and Ecology of Animals, Siberian Branch

of the Russian Academy of Sciences, Novosibirsk, Russia

25.1 “Potatoes partly made of oil” Potato had a profound, yet often underappreciated, impact on the development of human civilization. Domestication of potato and its subsequent spread throughout the world resulted in a considerable improvement in human nutrition and food security and was at least partially responsible for a considerable growth in human population (See Chapters 1 and 20 for further discussion and several examples). Potato farming also sent an early warning about shortcomings of monoculture, as well as about the perils of replacing sustainable and comprehensive social and economic development with reliance on a single “silver bullet” solution that allows meeting the short-term needs of an otherwise dispossessed and disadvantaged population. Terrible events surrounding the Irish Potato Famine caused by an outbreak of Phytophthora infestans in the middle of the 19th century had strong impacts well beyond the Emerald Island, the lessons of which are still important at our time. The necessity to protect potato crops was also a major driving force behind development of the modern chemical crop protection industry. Pesticides to combat late blight and Colorado potato beetle were among the first to be used on a large scale in commercial agriculture and continue to amount for a significant share of an overall crop protection market. Furthermore, evolution of insecticide resistance by Colorado potato beetles, green peach aphids, and a few other species of potato pests provides a continuous impetus for discovering and commercializing new active ingredients. For more details, please refer to Chapters 4, 12, 24, and 26 of this book. A less known fact is that potatoes also provided a major inspiration behind development of the rapidly growing scientific field of agroecology, which emerged from the interdisciplinary studies that combined ecology and an array of applied agricultural sciences. Ecology is the study of interactions among living organisms and between living organisms and their environment (Stiling, 2002). Agriculture is an industry that produces its outputs using activities of living organisms such as crops and livestock (Shiyomi and Koizumi, 2001). Agroecology is a relatively new scientific discipline that defines, classifies, and studies agricultural systems from an ecological and socio-economic perspective (Altieri, 1987). Its main goal is investigating ways to improve sustainability of agricultural practices (Altieri, 1989). Modern mainstream agriculture is highly successful in generating unprecedented by historical measures productivity of an average farm worker. At the same time, it is heavily dependent on inputs that are derived from fossil fuels and other nonrenewable resources. These inputs are entered into the system where they undergo a number of transformations, ultimately generating harvestable outputs that can be further processed and delivered to consumers. Such an approach is similar to approaches used in industrial manufacturing; hence, modern commercial agriculture is often called industrial agriculture. Benefits of ecological interactions within agricultural systems are usually given little consideration; to the contrary, such interactions are often viewed as constraints on achieving maximum possible outputs (Shiyomi and Koizumi, 2001). However, both depletion of nonrenewable resources, as well as environmental degradation surrounding their use require a wider adoption of alternative approaches. Manipulation of interactions among organisms and between organisms and their environment is one such approach that offers additional opportunities for optimizing agricultural production. Agroecology as a science emerged in the 1930s, expanded in the 1970 and 1980s, became institutionalized and consolidated in the 1990s, and then matured and branched out into social sciences and policymaking since 2000s (Wezel and Soldat, 2009). Among early proponents of this approach who made a significant contribution to its development were brothers Eugene P. Odum and Howard T. Odum. Both were prominent fundamental ecologists who were responsible for Insect Pests of Potato. https://doi.org/10.1016/B978-0-12-821237-0.00003-2 Copyright © 2022 Elsevier Inc. All rights reserved.

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jointly developing a paradigm of systems ecology (Odum, 1994). Eugene Odum also authored a highly influential textbook in ecology, which has undergone five editions since its original publication in 1953 (Odum and Barrett, 2004). He is even sometimes referred to as the father of modern ecology (Craige, 2019). However, it was Howard Odum (1971) who said that: This is a sad hoax, for industrial man no longer eats potatoes made from solar energy; now he eats potatoes partly made of oil.

While the same applies to any other major staple crop, the choice of potatoes to illustrate the biggest problem facing industrial agriculture clearly highlights their importance. Based on their work studying energy flows through ecosystems, both brothers developed a serious concern that American agriculture essentially represents a vast experiment in replacing natural ecosystems with artificial monocultures that are heavily dependent on inputs made of nonrenewable resources (Madison, 1997). Such monocultures are highly successful in feeding American population and exporting agricultural commodities to the rest of the world. However, external energy subsidies create a dangerously unstable system. To approach a relatively steady state of a natural ecosystem at late successional stages of its development, a human ecosystem needs to achieve an equilibrium between production and respiration. Under such a scenario, a common economic goal of maximizing output growth must be replaced with a goal of maximizing long-term sustainability (Odum, 1971).

25.2 An underappreciated challenge Over the last several decades, agroecology has attracted considerable attention from scientists, farmers, and consumers of agricultural products. The meaning of the term has expanded to include both a movement aiming toward improving agricultural sustainability, as well as practices employed for achieving this aim (Wezel and Soldat, 2009). Since every human being on the planet is a consumer of agricultural products, the pool of potential stakeholders in further development of this concept is rather extensive. However, agroecological approaches are still very far away from being commonplace in agricultural production. Considerable advances have been made in their application on small-scale subsistence and semisubsistence farms in developing countries, often together with the revival of time-tested indigenous farming practices (Nicholls and Altieri, 2018). They are also making inroads in industrialized nations, particularly in conjunction with organic farming, local food sovereignty, and small farm revitalization movements within a broader framework of environmentalism and social justice (Anderson et al., 2019; van der Ploeg, 2020). However, most agricultural commodities around the world are still produced by industrial farming enterprises, usually with very limited (if any) attention being paid to ecological interactions happening during the production process. Numerous economic and policy barriers to a wider adoption of agroecological principles by mainstream agriculture have been identified, with the bottom line being that high yields and profitability are favored under the existing status quo over sustainability and food security (Nicholls and Altieri, 2018; Anderson et al., 2019; van der Ploeg, 2020). Overcoming these barriers is very important; however, there is also another issue that often receives less attention than it deserves. A good understanding of ecological interactions within a given agroecosystem is essential for their successful manipulation for the purpose of improving agricultural production. However, these interactions are inherently very complex and changeable. Therefore, building up a scientifically sound knowledge base for the future development of agroecological approaches to crop management is not an easy task. Traditional agricultural practices that predate modern industrial agriculture contain a treasure trough of relevant information (Nicholls and Altieri, 2018). At the same time, they do not provide a set of ready-made recipes that are universally applicable on each and every field. Furthermore, to fully harness their potential, it is still important to understand how they work, not just to know that they work under certain conditions. The first edition of this book contained a section entitled The Potato Field as a Managed Ecosystem. Comprised of four chapters, it contained information on effects of biodiversity on biological control of potato pests (Lynch et al., 2013), plant mediated effects of soil management on the Colorado potato beetle (Alyokhin and Gross, 2013), Potato virus Y dynamics as affected by weeds and crop plants (Srinivasan et al., 2013), and dispersal and migration strategies of Colorado potato beetles (Boiteau and Heikkilä, 2013). The section spun exactly 100 printed pages of a reasonably concise text and contained a lot of interesting and useful information. Yet, it covered only a small portion of ecological interactions and was limited to potato fields located in temperate North America. Most of organisms present in the same fields were not even mentioned, and most interactions were not considered. This is very illustrative of the challenge facing agroecology as applied science. Obviously, difficult does not mean impossible. Even small improvements in our understanding of ecology of a potato field may lead to considerable improvements in managing potato crop. For example, as discussed in Chapter 27, rather

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straightforward changes in pesticide applications may result in dramatic increase in performance of natural enemies. Furthermore, small improvement is better than lack of improvement. Consequently, in this chapter we provide further information on ecology of organisms inhabiting potatoes and discuss a broader context of its possible applications. Still, it is important to remember that part of this context is a clear realization that adopting an ecological approach to pest management is not just a matter of deciding to do so. A lot of research effort may be necessary in order to succeed.

25.3 Healthy soils and healthy plants Good soil health, defined as the sustained capacity of soil to function as a living system that maintains long-term biological productivity, is foundational for an overall integrity of an agroecosystem (Doran and Safley, 1997; Nicholls and Altieri, 2007). Healthy soils support diverse biological communities that are characterized by multiple alternative pathways of energy and material flow through its levels and are relatively stable in the face of biotic and abiotic disturbances (Nicholls and Altieri, 2007). Unfortunately, current potato farming relies on agronomic practices that result in intensive tillage, exposed soil surface, and removal of most crop residue. As a result, soils on potato fields commonly suffer from low organic matter, low porosity, and are structurally unstable (Alyokhin et al., 2020). Improving soil health is commonly achieved by adding organic soil amendments, such as manure or compost, to either replace or supplement synthetic fertilizers. There is considerable evidence that doing so also results in a decrease in insect herbivory in a wide variety of agroecosystems (Eigenbrode and Pimentel, 1988; Phelan et al., 1995; Morales et al., 2001; Hsu et al., 2009; Staley et al., 2010; Cardoza, 2011). Schmitt-Jeffris et al. (2020) even obtained some evidence that preferential attraction of ovipositing European corn borer, Ostrinia nubilalis, females to Bt corn grown in synthetically fertilized soils on conventional farms may be responsible for significant overall declines in populations of this highly polyphagous pest following wide-scale adoption of the Bt corn. Three different hypotheses have been suggested for explaining lower abundance of insect herbivores that is commonly observed on organically amended soils (Alyokhin and Gross, 2013). The mineral balance hypothesis suggests that the organic matter and microbial activity associated with organically managed soils affords a buffering capability to maintain nutrient balance in plants (Phelan et al., 1996; Phelan, 1997). An optimal nutrient balance results in good plant growth. It also results in resistance to herbivory through production of primary or secondary compounds needed for protection from herbivores and/or for healing of wounds inflicted by herbivore feeding. The induced defense hypothesis suggests that organic amendments enhance populations of naturally-occurring soil microorganisms. Being related to plant parasites (or even facultatively parasitic themselves), these microorganisms provide general physical or chemical stimuli that induce innate plant defenses that are also effective against insects (Stotz et al., 2000; Vallad and Goodman, 2004). The natural enemy hypothesis suggests that organically amended soils provide a better physical habitat and alternative prey in the form of various detritivores to natural enemies of herbivorous pests (Morales et al., 2001). The three hypotheses are not mutually exclusive, and these mechanisms may be complementary or even synergistic with each other. Alyokhin et al. (2005) and Alyokhin and Gross (2013) reported results of a multi-year field study investigating the effects of soil amendment practices on Colorado potato beetle, Leptinotarsa decemlineata, populations. Colorado potato beetle densities were almost always lower in field plots that had received, over the course of a decade, manure soil amendments in combination with reduced amounts of synthetic fertilizers compared to plots that had received full rates of synthetic fertilizers, but no manure (Alyokhin et al., 2005), for the same period of time. Unlike beetle abundance, plant height and canopy cover were comparable between plots receiving manure and synthetic fertilizer. Furthermore, tuber yields were higher in manure-amended plots. Thus, the difference in beetle density was unlikely to be explained simply by poor plant vigor in the absence of synthetic fertilizers. Subsequent field-cage and laboratory experiments (Alyokhin and Atlihan, 2005) confirmed that potato plants grown on manure-amended plots were indeed inferior Colorado potato beetle hosts compared to plants grown in synthetically fertilized soil. The observed negative effects were broad in scope. Female fecundity was lower in field cages set up on manure-amended plots early in the season, although it later became comparable between the treatments. Fewer larvae survived past the first instar, and the development of immature stages was slowed on manure-amended plots. In the laboratory, first instars also consumed less foliage excised from plants grown in manure-amended soils (Alyokhin and Atlihan, 2005). Laboratory experiments conducted by Boiteau et al. (2008) provided more evidence that organic soil amendments make potato plants less suitable for the Colorado potato beetles. They measured beetle performance on foliage excised from synthetically fertilized potato plots and on potato plots fertilized with several rates of dehydrated and pelletized poultry manure. Larval mortality between the first and the end of the third instar was similar, regardless of the fertilizer treatment. However, larval development took 1.4 times longer on organically fertilized plants compared to plants fertilized by an

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equivalent (based on kg N/ha) amount of synthetic fertilizer. Furthermore, adult beetles consumed 6.6 times more synthetically fertilized foliage when given a choice between the two fertilization regimes and 2.7 times more synthetically fertilized foliage in no-choice tests. The data collected by Alyokhin and Atlihan (2005) and Boiteau et al. (2008) indicated that deleterious effects of organic soil-amendments on Colorado potato beetles were at least partially plant-mediated. Consistent with that hypothesis, the mineral content of potato leaves explained 40%e57% of the variation in Colorado potato beetle populations observed among the field plots in the study by Alyokhin et al. (2005). There was also a dramatic dissimilarity in the mineral composition of potato leaves collected from manure-amended and synthetic fertilizer-treated plots, including significant differences in concentrations of nitrogen, calcium, magnesium, phosphorus, aluminum, boron, copper, iron, manganese, and zinc. Among the studied elements, boron was the most dramatically affected by soil amendment, with concentration being about two-fold higher in the foliage of plants grown on manure-amended soil (Alyokhin et al., 2005). However, a subsequent laboratory experiment, which created a gradient of boron concentrations in hydroponically grown potatoes, failed to establish any relation between larval survivorship and the boron contents of potato foliage. Field sprays with a solution of boron on potato plots also did not show any effects (Alyokhin and Gross, 2013). It is likely that suitability of plants for insect herbivores are determined by interactions of different minerals in their tissues rather than by a titer of a single mineral (Beanland et al., 2003). Reduced performance of insect herbivores on plants growing in improved soils is a widespread phenomenon. However, it is not universal. These interactions may be potentially affected by many factors, including climate, soil type, potato cultivars, and many others. For example, a large-scale multi-disciplinary field study compared Colorado potato beetle populations on soils amended with compost containing lignocellulosic substrates and nonamended soils on a conventional and on an organic farm (Alyokhin and Gross, 2013; Bernard et al., 2014). Results of that study were more variable and less promising from an economic standpoint than the results reported by Alyokhin et al. (2005). Compost amendment increased the numbers of early-season colonizing Colorado potato beetle adults at the conventional farm, but not on the organic farm. The numbers of egg masses were also higher in composted plots early in the season at the conventional farm for two out of the 3 years, but no such difference was detected on the organic farm (Alyokhin and Gross, 2013). Postdiapause beetle aggregation on compost-amended plots was likely explained by earlier plant emergence, which is fairly common for plants grown on composted soils (McCallum et al., 1998; Willekens et al., 2008). Despite the adult build-up, larval populations were more often lower on the composted plots at both farms, suggesting that potato plants grown on compost-amended soils are less suitable for Colorado potato beetle larval development. As a result, a considerable 21% overall increase in adult numbers observed in the study was followed by a small (2%e7%) decrease in the numbers of immature stages (Alyokhin and Gross, 2013). More pronounced compost effects on the conventionally managed farm than on the organically managed farm were probably due to the latter receiving organic amendments for many years. Therefore, soil on the organic farm may have previously acquired the capacity to affect Colorado potato beetles. While effects of composts reported by Alyokhin and Gross (2013) were less pronounced than effects of manure reported by Alyokhin et al. (2005), both fit the same general pattern. To the contrary, Krey et al. (2019) reported that survivorship of first-instar Colorado potato beetles was almost three times higher on plants grown in organic than in conventional soils. They attributed it to marginally lower foliar carbon in the leaves of potato plants grown in organic soils because high carbon content in leaves can interfere with herbivore performance by diluting concentrations of key nutrients that facilitate animal growth and maturation (Awmack and Leather, 2002). It is important to note, however, that Krey et al. (2019) found no differences in soil chemistry or organic matter between organic and conventional potato fields where they collected soils used in their study. They speculated that the time since conversion to organic management may not have been sufficient for detectable divergence in soil properties. Therefore, it is possible that in the future, suitability of plants grown in these soils to Colorado potato beetles will start resembling that reported by Alyokhin et al. (2005) and Boiteau et al. (2008). Soil improvement is unlikely to solve the problems caused by herbivorous insect pests on its own. Furthermore, its primary goal is increasing soil fertility and preventing erosion, while a commonly observed reduction in herbivore performance on plants grown on organically amended soils is somewhat of a secondary bonus. Relationship between soil management and insect herbivory is complicated and decreases in insect populations cannot be taken for granted. Nevertheless, soil management could be an important component of integrated pest management programs, with Chapters 15 and 27 providing more information on these applications. Also, insect responses to soil amendments highlight the importance of going beyond the input/output paradigm typical for a modern industrial agriculture and paying attention to the network of connections that comprise functioning agroecosystems.

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25.4 Dawn of the killer fungi As discussed in Chapter 13, fungal entomopathogens are a valuable biological control agent against several potato pests, including the Colorado potato beetle. One big advantage is that they can be applied in the same manner and using the same equipment as insecticides. Therefore, their adoption does not require additional investment in equipment or training. However, coming out of a sprayer does not make them just another type of an insecticide. It is important to remember that we are dealing with living organisms, that form intricate relationships with other members of an agroecosystem. Here, we review current information on their ecology. Among entomopathogenic ascomycete fungi, species of genera Beauveria, Metarhizium and some species of Cordyceps (e.g., Cordyceps fumosorosea and C. farinosa, formely Isaria fumosorosea and I. farinosa) are widespread in agricultural systems. The main reservoirs of these fungi are the soil and plant rhizosphere. In addition, they can colonize internal tissues of plant roots and shoots. The fungi infect insects mostly by penetration through the cuticle and less commonly, through oral ingestion (Mannino et al., 2019). Stages of host infection, virulence factors, as well as insect defense reactions are described in detail in many reviews (e.g., Butt et al., 2016). Here, we focus on the ecology of entomopathogenic fungi in the context of a potato agroecosystem. Potato fields, like other crop systems, are characterized by the predominance of above mentioned three genera of the fungi (Bajan and Kmitova, 1977). The genera Beauveria and Metarhizium include cryptic species that can be distinguished from each other only using molecular techniques (Bishoff et al., 2009; Rehner et al., 2011; Mayerhofer et al., 2019). Metarhizium brunneum, M. robertsii, Beauveria bassiana, B. pseudobassiana, and B. brongniartii dominate temperate agroecosystems (Kepler et al., 2015; Steinwender et al., 2015; Inglis et al., 2018; Medo et al., 2016). These species are generalists that infect insects from different orders, except B. brongniartii that infect mostly beetles in the family Scarabeidae (Rehner et al., 2011). Cryptic species have ecological differences regarding temperature preferences, resistance to UV radiation, and associations with certain habitats (Bidochka et al., 2001; Wyrebek et al., 2011; Nishi et al., 2013). For example, isolates of M. robertsii are characterized by higher thermotolerance and virulence toward Colorado potato beetle larvae under dry environmental conditions compared to the isolates of M. brunneum (Kryukov et al., 2017). Similarly, B. pseudobassiana is a more mesophilic fungus than B. bassiana (Medo et al., 2016). Species composition of Cordyceps (Isaria) in agroecosystems is much less studied compared to the other two genera, even though the most widespread species C. farinosa may cause considerable Colorado potato beetle mortality (Bajan and Kmitova, 1977). Abundance of entomopathogenic fungi in soils, quantified as counts of colony-forming units on artificial media (CFUs), is significantly affected by soil properties, such as texture, temperature, and moisture contents, as well as by agricultural practices. Jaronski (2007) provides an excellent summary on this subject. Loam, clay, and silt soils are likely to be more favorable for the persistence of fungi and their infectivity compared to sandy soils. Fungi are actively developing at temperatures ranging between 20 and 28
C, whereas low temperatures (10e16
C) are more appropriate for persistence of conidia in soil. Optimal moisture for persistence of the fungi ranges between Aw ¼ 0.9890e0.9985 depending on temperature, while conidia germination requires water activity Aw > 0.935. To the best of our knowledge, no studies specifically compared abundance and species composition of entomopathogenic fungi between potato fields and other agroecosystems. However, we do not expect any dramatic differences, particularly when crop rotation is practiced. Laengle et al. (2005) noted that Beauveria abundance in sandy soil planted with potato in Austria was 0.1e3.7  103 CFU/g. Gaugler et al. (1989) showed that Beauveria CFU count in sandy loam soil of potato plantations in USA (New Jersey) ranged 0e104 per gram, with maximum CFU count observed in autumn. According to our data, in West Siberia private kitchen gardens with continuous potato cultivation (more than 10 years) on sandy clay and silty clay soils, CFU counts were 7.7  1.5  103 (max.: 1.8  0.3  104) per g of dry soil for Metarhizium, and 1.2  0.4  103 per g of dry soil for Beauveria during 2019e20 (Tyurin et al., 2021). Both pairs of cryptic species (M. robertsii and M. brunneum, as well as B. bassiana and B. pseudobassiana) were present in those samples (Tyurin et al., 2021; Kyukov and Yaroslavtseva, unpublished). Conventional rotated fields (potatoes following cabbage) with sod-podzolic sandy clay loam soils had lower titers e 102 CFU/g dry soil of Metarhizium, and 102 CFU/g dry soil of Beauveria (Tomilova et al., 2020). The indicated titers are similar to those reported for other agricultural ecosystems, where they usually range between 102e104 CFU/g soil (Scheepmaker and Butt, 2010). Herbicide and fungicide applications have weak or no effect on fungi in the soil, as have been shown in nonpotato agroecosystems (Jaros-Su et al., 1999; Bruck, 2009; Clifton et al., 2015). At the same time, tillage may decrease abundance of Beauveria and Metarhizium (Sosa-Gomez and Moscardi, 1994). Fungal conidia are sensitive to UV radiation and high temperatures; therefore, moving them to soil surface by tillage leads to their inactivation. Frequency of fungi in the soils of organic agroecosystems is significantly greater compared to conventional agroecosystems (Klingen et al., 2002; Clifton et al., 2015; Ramos et al., 2017), likely because of high contents of organic matter and high numbers of arthropods on the

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organically managed farms. It is possible that the abundance of entomopathogenic fungi in the soils of potato fields may also depend on the density of abundant insect pests such as Colorado potato beetles and wireworms. However, these correlations have not been studied. Interactions between entomopathogenic fungi and insects on potato fields were investigated mostly using different life stages of the Colorado potato beetle. Larvae of this species are susceptible to Metarhizium spp. and Beauveria spp. under laboratory and field conditions (reviewed by Wraight et al., 2007). However, natural epizootics are extremely rare among its feeding stages (Sikura and Sikura, 1981). For example, > 100,000 Colorado potato beetle larvae were collected in 2005e20 from private fields of Western Siberia and Kazakhstan. Of those, only a few individuals (