Proceedings of the Meetings Comptes Redus De Les Réunions Edited By

IOBC / WPRS

Working Group “Integrated Protection in Field Vegetable Crops”

OILB / SROP

Groupe de Travail « Lutte Intégrée en Culture de Légumes »

Proceedings of the Meetings Comptes Redus de les Réunions

at / à

Gödöllö (Hungary) 31.10. – 3.11.1999

and

Krakow (Poland) 15. – 17.10.2001

Edited by Stefan Vidal

IOBC wprs Bulletin Bulletin OILB srop Vol. 26 (3), 2003

The content of the contributions is in the responsibility of the authors

The IOBC/WPRS Bulletin is published by the International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC/WPRS)

Le Bulletin OILB/SROP est publié par l‘Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux et les Plantes Nuisibles, section Regionale Ouest Paléarctique (OILB/SROP)

The Publication Commission of the IOBC/WPRS:

Horst Bathon Luc Tirry Federal Biological Research Center University of Gent for Agriculture and Forestry (BBA) Laboratory of Agrozoology Institute for Biological Control Department of Crop Protection Heinrichstr. 243 Coupure Links 653 D-64287 Darmstadt (Germany) B-9000 Gent (Belgium) Tel +49 6151 407-225, Fax +49 6151 407-290 Tel +32-9-2646152, Fax +32-9-2646239 e-mail: [email protected] e-mail: luc.tirry@ rug.ac.be

Address General Secretariat:

INRA – Centre de Recherches de Dijon Laboratoire de recherches sur la Flore Pathogène dans le Sol 17, Rue Sully, BV 1540 21034 DIJON CEDEX France

ISBN 92-9067-151-1 Web: http://www.iobc-wprs.org

Introduction

This Bulletin is exceptional in containing the papers of the last two meetings of the IOBC/wprs Working Group on “Integrated Protection in Field Vegetables”. The reason for this unusual form is that that the editor did not manage to finish his editing duties in time before the last meeting took place. I am aware of the shortcomings, which are related to a delay of publishing the manuscripts; this is especially unsatisfactorily for students. I apologize for any inconvenience related to this delay.

The first part of the Bulletin contains 38 papers presented at the penultimate meeting of the Working Group at the Gödöllö University of Agricultural Sciences, Hungary, from 31st October to 3rd November 1999, organised by Prof. Dr. G. Bujaki, T. Bukovinsky and H. Tréfás. The second part of the Bulletin contains 20 papers of the last meeting of this Working Group at the Agricultural University of Krakow, from 13th October to 18th October 2001, organised by Prof. Dr. K. Wiech and M. Pniak. We all enjoyed the outstanding hospitality and the perfect organisation of both the scientific and social part of the meetings. More than 50 colleagues attended both meetings, coming from Eastern and Western parts of Europe; we also acknowledged the participation of colleagues from the USA and Canada. At both meetings we had presentations at a very high standard and the intensive discussions underlined that both basic research and extension of protection measures are integral parts of the group. Attempts to integrate colleagues working on issues related to the protection of field vegetables from plant diseases were only in part successfully.

Since several years the production of “Guidelines” for field vegetable crop production has been discussed within the group quite controversially; however, Dr. Joerg presented some preliminary ideas on this topic during the Krakow meeting and we are now looking forward to discuss a first version of these “Guidelines” during the next meeting, which will be held at Ghent, Belgium in 2003.

Stefan Vidal, Goettingen, 26 February, 2003

List of participants of the Gödöllö Meeting

Binks, Richard Ceglarska, Elzbieta ADAS DAU, Agriculture College Woodthorne Wergs Road Planta u. 18. fsz. 3. Wolverhampton WC6 8TQ (UK) 1025 Budapest (Hungary) [email protected] Chaput, Jim Blood Smyth, Jennie Ontario Ministry of Agriculture and Food ADAS Agriculture and Rural Division Mepal, Ely, Camps (UK) 1 Sotne Road West, ARD [email protected] Guelph, Ontario (Canada) [email protected] Bobnar, Alexander University of Ljubljana, Collier, Rosemary Biotechnical Faculty Horticulture Research International Jamnikarjeva 101 Wellesbourne, Warwick 1111 Ljubljana (Slowenia) CH 35 9EF (UK) [email protected] [email protected]

Bohár, Gyla DenBelder, Eefje Plant Protection Institute IPO Hungarian Academy of Sciences Binnenhaven Pob. 102 POB 9060 1525 Budapest (Hungary) 6700 GW Wageningen (The Netherlands) [email protected] [email protected]

Bozsik, András Ellis, Peter Robin DAU, Dept. Crop Protection Horticulture Research International PF. 36 Wellesbourne, Warwick 4015 Debrecen (Hungary) CH 35 9EF (UK) [email protected] [email protected]

Bujáki, Gabor Érsek, László Gödöllö University of Agricultural NTA Sciences Arató u. 5. Pater K. u. 1 9018 Györ (Hungary) 2100 Gödöllö (Hungary) [email protected] Esbjerg, Peter

The Royal Vet and Agricultural University Bukovinsky, Tibor Department of Ecology, Zoology Section Gödöllö University of Agricultural Tharväldsensvej 40 Sciences 1871 Frederiksberg (Denmark) Pater K. u. 1 [email protected] 2100 Gödöllö (Hungary) [email protected] iii

Ester, Albert Ilovai, Zoltán Applied Research for Arable Farming and Plant Helath and Soil Conservation Station Field Production of Vegetables of Budapest POB 430 Budaörsi út 141-145. 8200 AK Lelystad (The Netherlands) 1118 Budapest (Hungary) [email protected] [email protected]

Everaarts, Tjarda Johansen, Tor Jacob De Groene Vlieg The Norwegian Crop Research Institute Duivenwaardsedijk 1 Holt Research Centre 3244 LG Nieuwe Tonge (The Netherlands) 9292 Tromsoe (Norway) [email protected] [email protected]

Felkl, Gisela Jönnson, Bodil Danish Institute of Agricultural Sciences Swedish board of Agriculture Dept. Plant Pretection Plant Protection Centre Research Centre Flakkebjerg Box 12 4200 Slagelse (Denmark) 23053 Alnarp (Sweden) [email protected] [email protected]

Finch, Stan Kacem, Nabila Horticulture Research International Lab. d’Ecobiologie des Insectes Wellesbourne, Warwick Parasitoides CH 35 9EF (UK) Université de Rennes 1 [email protected] Avenue du Général Leclerc Compus de Beauben Flood, Brian 35042 Rennes (France) Del Monte Co., Research Division [email protected] POB 89 Rochelle, Illinois, 61608 (USA) Kazinczi, Gabriella [email protected] University of Veszprém Georgikon Agricultural Sciences Keszthely Hartfiled, Chris Institute of Plant Protection Horticulture Research International 8360 Keszthely (Hungary) Wellesbourne, Warwick CH 35 9EF (UK) Kienegger, Manuela [email protected] L. Boltzmann-Institute for Biological Agriculture and Applied Ecology Hommes, Martin Rinnboeckstr. 15 BBA 1110 Wien (Austria) Institute for Plant Protection in [email protected] Horticultural Crops Messeweg 11/12 Kiss, Edit 38104 Braunschweig (Germany) Csongrád County Plant Health and Soil [email protected] Conservation Station Rárósi ut. 110 Pob. 99 6800 Hódmezövásárhely (Hungary) [email protected] iv

Kristóf, Lászlóné Nádasy, Miklós National Institute for Agricultural Quality University of Veszprém control Geeorikon Agricultural Sciences Keszthely Keleti Károly u. 24 Institute of Plant Protection 1024 Budapest (Hungary) Deák F. u. 57 8360 Keszthely (Hungary) Kromp, Bernhard [email protected] L. Boltzmann-Institute for Biological Agriculture and Applied Ecology Narkiewicz.Jodko, Jan Rinnboeckstr. 15 Research Institute of Vegetable Crops 1110 Wien (Austria) ul. Konstytucji 3 Maja 1/3 [email protected] 96-100 Skierniewice (Poland)

Lehmhus, Jörn Nawrocka, Bozena Institute for Plant Disease and Plant Research Institute of Vegetable Crops Protection ul. Konstytucji 3 Maja 1/3 Herrenhäuser Str. 2 96-100 Skierniewice (Poland) 30419 Hannover (Germany) [email protected] Nissinen, Anne Agricultural Research Centre of Finland Maisonneuve, Jean Charles Plant Protection S.R.P.V. Bretagnes 31600 Jokioinen (Finland) 14, rue du Colonel Berthaud [email protected] 29283 Brest (France) [email protected] Otto, Mathias BBA Malmber, Karoliina Institute for Plant Protection in University of Horticulture and Food Horticultural Crops Szüret u. 2-17- Messeweg 11/12 1118 Budapest (Hungary) 38104 Braunschweig (Germany) [email protected] McKinlay, Rod SAC. West Mains Road Pákzodi, Anita Edinburgh, EH9 3JG (UK) Plant Helath and Soil Conservation Station [email protected] of Budapest Budaörsi út 141-145. Meadow, Richard 1118 Budapest (Hungary) Norwegian Crop Research Institute [email protected] Plant Protection Centre Department of Entomology and Pálfi, Katalin Nematology Fellesbygget Plant Helath and Soil Conservation Station 1432 As (Norway) of Budapest [email protected] Budaörsi út 141-145. 1118 Budapest (Hungary) Morely, Kate [email protected] Horticulture Research International Wellesbourne, Warwick CH 35 9EF (UK) [email protected] v

Pniak. Michal Swejda, Jerzy Agricultural University of Krakow Institute of Vegetable Crops Department of Plant Protection ul. Konstytucji 3 Maja 1/3 At. 29-Listopada 54 96-100 Skierniewice (Poland) 31-425 Krakow (Poland) [email protected] Theunissen, Jan Research Institute for Plant Protection Regös, Mária (IPO) Csongrád County Plant Health and Soil Wageningen (The Netherlands) Conservation Station [email protected] Rárósi ut. 110 Pob. 99 6800 Hódmezövásárhely (Hungary) Trdan, Stanislav [email protected] University of Ljubljana, Biotechnical Faculty, Agronomy Department, Richter, Ellen Institute for Phytomedicine Institute of Vegetable and Fruit Crops Jamnikarjeva 101 University of Hannover 1111 Ljubljana (Slowenia) Herrenhaeuser Str. 2 [email protected] 304199 Hannover (Germany) [email protected] Tréfás, Hajnalka Gödöllö University of Agricultural Riedel, Werner Sciences The Royal Vet and Agricultural University Pater Karoly u. 1 Department of Ecology, Zoology Section 2100 Gödöllö (Hungary) Tharväldsensvej 40 [email protected] 1871 Frederiksberg (Denmark) [email protected] Valic, Nevenka University of Ljubljana, Biotechnical Saucke, Helmut Faculty FB 11, Dept. of Ecol. Plant Agronomy Dept., Protection/Entomology Institute for Phytomedicine University of Kassel Jamnikarjeva 101 Nordbahnhofstr. 1a 1111 Ljubljana (Slowenia) 37213 Witzenhausen (Germany) [email protected] [email protected] van de Steene, Frans Seress, Zoltán Department of Crop Protection University of Horticulture and Food Lab. of Agrozoology, F.L. & T. B. W. Ménesi út 44. Coupure Links 563 1118 Budapest (Hungary) 9000 Gent (Belgium) [email protected] [email protected]

Seredi, Attila vanNassau, Eric Szeredi Ltd. Nuhems Zaden Bv Ladány major, Pob. 4 Pob. 4005 6775 Kiszombo (Hungary) 6080 AA Haelen (The Netherlands) [email protected] [email protected]

Vidal, Stefan Institute for Plant Pathology and Plant Protection Georg-August-University Grisebachstr. 6 37077 Göttingen (Germany) [email protected]

Villeneuve, Francois Départment Légumes et Technologie Domaine de Lanxade BP 21 24130 La Force (France) [email protected]

Weber, Axel Institute for Plant Disease and Plant Protection University of Hannover Herrenhäuser Str. 2 30419 Hannover (Germany) [email protected]

Wiech, Kazimierz Agricultural University of Krakow Department of Plant Protection At. 29-Listopada 54 31-425 Krakow (Poland) [email protected]

William, Parker ADAS Woodthorne, Wolverhampton WV6 8TQ (UK) [email protected]

Wyman, Jeffrey University of Wisconsin, Dept. of Entomology 637 Russell Habs. Madison, WIS. 53706 (USA) [email protected] vii

List of participants of the Krakow Meeting

Baur, Robert Cichoi, Sylvia Dept. of Cop Protection Academy of Agriculture Swiss Federal Research Station Dept. of Plant Protection 8820 Wädenswil (Switzerland) Al 29 Listopada 54 [email protected] 31-425 Krakow (Poland)

Bednarek, Andrej Collier, Rosemary Dept. of Biology Animals Environment Horticulture Research International Warsaw Agriclutural Univ. Wellesbourne, Warwick Nowoursynovski 166 CH 35 9EF (UK) 02-7790 Warsaw (Poland) [email protected] [email protected] DenBelder, Eefje Blood Smyth, Jennie IPO ADAS Binnenhaven Mepal, Ely, Camps (UK) POB 9060 [email protected] 6700 GW Wageningen (The Netherlands) [email protected] Bobnar, Alexander University of Ljubljana, Dirksmeyer, Walter Biotechnical Faculty Institute of Horticultural Economics Jamnikarjeva 101 University of Hannover 1111 Ljubljana (Slowenia) Herrenhäuser Str. 2 [email protected] 30419 Hannover (Germany) [email protected] Bujáki, Gabor Gödöllö University of Agricultural Esbjerg, Peter Sciences The Royal Vet and Agricultural University Pater K. u. 1 Department of Ecology, Zoology Section 2100 Gödöllö (Hungary) Tharväldsensvej 40 [email protected] 1871 Frederiksberg (Denmark) [email protected] Bukovinsky, Tibor Wageningen University Ester, Albert Dept. of Plant Sciences Applied Research for Arable Farming and Lab. Of Entomology Field Production of Vegetables Binnenhaven 7 POB 430 6709 PD Wageningen (The Netherlands) 8200 AK Lelystad (The Netherlands) [email protected] [email protected] viii

Everaarts, Tjarda Jörg, Erich De Groene Vlieg Landesanstalt für Pflanzenbau und -schutz Duivenwaardsedijk 1 Essensheimer Str. 144 3244 LG Nieuwe Tonge (The Netherlands) 55128 Mainz (Germany) [email protected] [email protected]

Finch, Stan Jowonska, Teresa Horticulture Research International Academy of Agriculture Wellesbourne, Warwick Dept. of Plant Protection CH 35 9EF (UK) Al 29 Listopada 54 [email protected] 31-425 Krakow (Poland)

Fischer, Serge Komorowska-Kulik, Ioanna Swiss Federal Research Station for Plant Institute of Industrial Organic Chemistry Production Ul. Amopol 6 Changings 03-236 Warsaw (Poland) 1260 Nyon (Switzerland) [email protected] [email protected] Kucharczyk, Halina Flood, Brian Dept. of Zoology UMCS Del Monte Co., Research Division 19 Akadeicka Str. POB 89 20-033 Lublin (Poland) Rochelle, Illinois, 61608 (USA) [email protected] [email protected] Legutowska, Hanna Freuler, Jost, Dept. of Applied Entomology Swiss Federal Research Station for Plant Warsaw Agricultural University Production Nowoursynowska 166 Changings 02-787 Warsaw (Poland) 1260 Nyon (Switzerland) [email protected] [email protected] Modic, Spela Hommes, Martin University of Ljubljana, BBA Biotechnical Faculty Institute for Plant Protection Agronomy Department, in Horticultural Crops Jamnikarjeva 101 Messeweg 11/12 1111 Ljubljana (Slowenia) 38104 Braunschweig (Germany) [email protected] Nawrocka, Bozena Research Institute of Vegetable Crops Jönnson, Bodil ul. Konstytucji 3 Maja 1/3 Swedish board of Agriculture 96-100 Skierniewice (Poland) Plant Protection Centre Box 12 Pobozniak, Maria 23053 Alnarp (Sweden) Academy of Agriculture [email protected] Dept. of Plant Protection Al 29 Listopada 54 31-425 Krakow (Poland) [email protected] ix

Riedel, Werner van de Steene, Frans The Royal Vet and Agricultural University Department of Crop Protection Department of Ecology, Zoology Section Lab. Of Agrozoology, F.L. & T. B. W. Tharväldsensvej 40 Coupure Links 563 1871 Frederiksberg (Denmark) 9000 Gent (Belgium) [email protected] [email protected]

Rogowska, Maria Vidal, Stefan Research Institute of Vegetable Crops Institute for Plant Pathology and Plant Ul. Konstytucji 3 Maja 1/3 Protection 96-100 Skierniewice (Poland) Georg-August-University Grisebachstr. 6 Saucke, Helmut 37077 Göttingen (Germany) FB 11, Dept. of Ecol. Plant [email protected] Protection/Entomology University of Kassel Wiech, Kazimierz Nordbahnhofstr. 1a Agricultural University of Krakow 37213 Witzenhausen (Germany) Department of Plant Protection [email protected] At. 29-Listopada 54 31-425 Krakow (Poland) Trdan, Stanislav [email protected] University of Ljubljana, Biotechnical Faculty Wojciechowicz-Żytko, E. Agronomy Department, Institute for Academy of Agriculture Phytomedicine Dept. of Plant Protection Jamnikarjeva 101 Al 29 Listopada 54 1111 Ljubljana (Slowenia) 31-425 Krakow (Poland) [email protected] [email protected]

Tréfás, Hajnalka Wyman, Jeffrey Szent István University University of Wisconsin, Dept. of Crop Protection Dept. of Entomology Pater Karoly u. 1 637 Russell Habs. 2100 Gödöllö (Hungary) Madison, WIS. 53706 (USA) [email protected] [email protected] x

Table of Contents

Gödöllö-Meeting

Coping with complexity Theunissen, J...... 1

Monitoring Pest Populations

Characteristics of population-dynamics of onion fly (Delia antiqua Meigen) by an area- wide monitoring system Ilovai, Z...... 7

Monitoring root flies in Brassicae - Recent developments Meadow, R...... 13

Population dynamics and supervised control of the leek moth, Acrolepiopsis assectella, in Germany Richter, E. & Hommes, M...... 17

Monitoring of western flower thrips (Frankliniella occidentalis Pergande) in the vicinity of greenhouses in different climatic conditions in Slovenia Trdan S. & Jenser, G...... 25

Monitoring the flight activity and damage of Thrips tabaci (Lind) in different varieties of white and red cabbage Van de Steene, F. & Tirry, L...... 33

Further development and use of simulations of within-field distributions of Brevicoryne brassicae to assist in sampling plan development Parker, W.E., Perry, J.N., Niesten, D., Blood Smyth, J.A., McKinlay, R.G. & Ellis, S.A...... 39

Integrated Pest Management

The exploitation of plant resistance in controlling insect pests of vegetable crops Ellis, P.R. & Kift, N.B...... 47

New ways of manipulating field populations of the carrot fly Collier, R., Finch, S. & Davies, J...... 57

The effect of strips of flowers on pests and beneficial arthropods in adjacent broccoli plots Kienegger, M., Kromp, B. & Kahrer, A...... 61

Elements of Integrated Control in Field Vegetables in Slovenia Milevoj, L., Osvald, J. & Valič, N...... 71

Simulating the population dynamics of the onion fly Delia antiqua in chives using an extended Leslie Model Otto, M. & Hommes, M...... 75

Population dynamics of Platyparea poeciloptera and its implications for an integrated pest management in asparagus Otto, M. & Hommes, M...... 77

Use of Plant Protection Information System in field vegetable growing Pákozdi, A., Pálfi, K., Mohai, K., Érsek, L. & Biber, K...... 81

Variety as the biological basis of the integrated plant protection Kristof, E. & Debreceni, A.O...... 87

Vegetable crops, integrated crop management programs and research in Central Canada Chaput, J...... 93

Possibilities to reduce damage by games in vegetable crops M. Nádasy & A. Takács ...... 95

Ecology of Pest Insects

Host-plant Selection by Insects - the “Missing Link” Finch, S. & Collier, R.H...... 103

Oviposition preference of carrot psyllid (Trioza apicalis) on different carrot varieties Nissinen, A., Kainulainen, P., Piirainen, A., Tiilikkala, K., & Holopainen, J.K...... 109

Diptera occurring on vegetables in Poland Szwejda, J...... 113

Predators and Parasitoids

Role of beneficial mirid bugs in control of tomato pests in open fields Ceglarska, E.B...... 121

Releasing the rove beetle Aleochara bilineata in the field as a biological agent for controlling the immature stages of the cabbage root fly, Delia radicum Hartfield, C. & Finch, S...... 127

Effect of the host-plant on the biological characteristics of Trybliographa rapae W. (Hymenoptera: Figitidae), endoparasitoid of the cabbage root fly Delia radicum L. (Diptera: Anthomyiidae) Kacem-Haddj El-Mrabet, N. & Nenon, J.P...... 135

Observations on the composition and effectiveness of diamondback moth (Plutella xylostella L.) parasitoids Wiech, K. & Kalmuk, J...... 141

Biological control with Chrysoperla lucasina against Aphis fabae on artichoke in Brittany (France) Maisonneuve, J.C., Hugon, N. & Lolivier, F...... 149

xii

Undersowing or Intercropping Crops

Detailed studies of how undersowing with clover affects host-plant selection by the cabbage root fly Morley, K. & Finch, S...... 155

Performance of the aphid Myzus persicae on intercropped and monocropped cabbages in glasshouse experiments Seress, Z., McKinlay, R.G. & Pénzes, B...... 163

The effects of undersowing (Brussels sprouts – black mustard) on population density of Brevicoryne brassicae and natural enemies of aphids Bukovinszky, T., Rasztik, V., van Lenteren, J.C., Vet, L.E.M. & Bujáki, G...... 167

Thrips species in leeks and their undersown intercrops Legutowska, H.& Theunissen, J...... 177

Insecticidal Control

Light oil based pesticides as an effective mean for IPM Ilovai, Z., Kajati, I. & Kiss, E...... 183

Field trials with lambda-cyhalothrin against carrot flies in Norway Johansen, T.J...... 189

Efficacy of insecticide seed treatments of dwarf French bean to control bean seed fly, Delia platura (Meig.) Ester, A, Brommer, E., Neuvel, J.J. & van Ijzendoorn, M.T...... 193

Disease Control

Pepper pathogen viruses and their control by resistance breeding and light summer oils Kiss, E.F., Huszka, T. & Ocskó, I...... 201

The role of the fungicide resistance examination system in the Integrated Plant Protection of vegetables in Hungary Aponyi, I & Vendrei, Z...... 211

Parsnip Yellow Fleck Virus in carrots: Development of a disease management strategy Binks, R. H., Morgan, D., Spence, N. & Blood-Smyth, J...... 217

Virus disease problems on field cucumber in Hungary Kiss, E.F., Kazinczi, G., Horváth, J., Kobza, S., Baranyi, T., Varga, M., Havasréti, B. & Fehér, A...... 219

Experiences of the use of Coniothyrium minitans based biofungicide against Sclerotinia diseases Bohár, G., Vajna, L., Aponyiné Garamvölgyi, I., Csete, S., Kerényiné Nemestóthy, K., Balogh, P., Illés G. & Becsey, Z...... 229

Characterisation of Hungarian Phytophthora infestans isolates in the 1990’s Dula, T., Aponyi, I., Varga, K., Bohár, G., Bakonyi, J. & Érsek, T...... 233 xiii

Krakow-Meeting

Monitoring Pest Populations

Cutworm (Agrotis segetum) forecasting. Two decades of scientific and practical development in Denmark Esbjerg, P...... 239

Survey of aphids on outdoor lettuce and strategies for their control Van de Steene, F., Tirry, L. & Driessen, R...... 245

Evaluation of 9 years supervised carrot fly control in the Netherlands Loosjes, M...... 253

Integrated Pest Management

Economies in transition and integrated pest management on vegetables: The case studies in Poland Dąbrowski, Z.T., Wiech, K...... 259

The influence of cabbage whitefly (Aleyrodes proletella L., Aleyrodidae) abundance on the yield of Brussels sprouts Trdan, S., Modic, Š. & Bobnar, A...... 265

Connection between herbicide treatments and nitrate accumulation of green onion Nádasy, E...... 271

The role of banker plants in the enhancement of the action of Diaeretiella rapae (M’Intosh) (Hymenoptera, Aphidiinae) the primary parasitoid of the cabbage aphid Brevicoryne brassicae (L.) Freuler, J., Fischer, S., Mittaz, C. & Terrettaz, C...... 277

The use of onion sets as „trap plants” to protect onion seed against insect pest Wiewióra, I. & Łuczak, I...... 301

Effects of flowering field margins on flight activity of the diamondback moth (Plutella xylostella L.) and its parasitoids Diadegma spp., and observations on distance from field edge, and vertical position of traps Bukovinszky, T., Brewer, M.J., Winkler, K., Trefas, H., Vet, L.E.M. & van Lenteren, J.C...... 307

The effect of winter cover crops on occurrence some of pest in cauliflower and cabbage Kotliński, S...... 315

Economic importance and the control method of Thrips tabaci Lind. on onion Nawrocka, B...... 321

The effect of broad bean cultivars sowing time on the occurrence of Aphis fabae Scop. and its predators Wojciechowicz-Żytko, E...... 325

xiv

Ecology of Pest Insects

A strategy for the control of carrot psylla (Trioza apicalis Förster) in Switzerland Fischer, S. & Terrettaz, C...... 331

Phytophagous entomofauna of horseradish Szwejda, J. & Rogowska, M...... 339

Occurrence of bean aphid (Aphis fabae Scop.) on red beet in relation to different coverage of soil by weeds Pobożniak,M...... 345

Undersowing or Intercropping Crops

The effect of intercropping leek with clover and carrot on thrips infestation Legutowska, H., Kucharczyk, H. & Surowiec, J...... 355

Insecticidal Control

Effects of film-coating flax seeds with various insecticides on germination and on the control of flea beetles Ester, A., Huiting H.F. & Nijënstein, J. H...... 361

Effects of chemical control programs against cabbage pests on ground dwellingfauna Freuler, J., Blandenier, G., Meyer, H. & Pignon, P...... 371

Efficiency of Proagro 100 SL ( imidacloprid ) in controlling of cabbage aphid Brevicoryne brassicae L on cauliflower cv. Berliński Narkiewicz-Jodko J., Nawrocka B. & Świętosławski, J...... 373

Preliminary trials on the efficiency of the Pirimix 100 PC (pirimicarb) in controlling of black bean aphid (Aphis fabae Scop.) on broad bean cv. Hangdown biały Narkiewicz-Jodko, J., Rogowska, M. & Świętosławski, J...... 377

Gödöllö Meeting

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 1-5

Coping with complexity

J. Theunissen Research Institute for Plant Protection (IPO), Wageningen, The Netherlands.

Abstract: The influence on our ordinary life of increasing knowledge and changing attitudes in our society are paralleled in the increasing complexity of scientific knowledge and attitudes in our working life as researchers. This increasing complexity has a number of facets: economical, biological, technical, organizational and psychological. These facets are discussed and illustrated by examples. Conclusions have to be drawn from these developments and challenges for the near future recognized.

Key words: intercropping, soil receptivity, endophytes, organic agriculture, IPM

Complexity What is complexity? According to English dictionaries complex means: ‘Made up of many parts’, ‘difficult to explain’, ‘intricate’ or terms of similar meaning.

Introduction

Once upon a time, life in plant protection research was simple. There was a crop, there were pests and diseases, there was always a budget, there were pesticides and one’s own special interest and off you went. Select an interesting pest, study its biology, find its weak spots, spray a pesticide in time and the problem was solved. At least for the time being. Basically, we dealt with single issue problems. Training in one’s own discipline provided the rationale, the theory and the methods. The results were expected to be an extension of this paradigm. Both problems and solutions were put and stored into a compartment where they belonged. This situation exists at present to a large extent. A clear example is the long list of pesticides which are available against nearly every problem encountered in growing crops, including chemical thinning and stem shorteners in grain. Another example is the increasing specialisation of scientists, which has the advantage of a steady scientific progress but carries the risk of obscuring a sufficient wide view on the scientific and public reality. I deliberately add ‘public’ because the bottom line of our functioning as scientists is to carry a shared responsibility for future development of a liveable society in which we and people after us have to exist. To be able to know what we are doing, apart from our own different specialties, we need a ‘helicopter view’ of our scientific and public environment. How to deal with the complexity in what we see from our elevated viewpoint is the subject of this paper.

Economic complexity

The traditional European way of farming and selling the products at more or less local markets is behind us. We can only look back in nostalgia. Because of overproduction, increasing international competition and liberalization of the world market, a sellers’ market has become a buyers’ market. Trading takes place by ever growing organizations and companies. The position of the grower as an independent business man has changed towards a

1 2

position as a link of a chain, from the seed producer up to the consumer. He is told by contract how to produce his crops and is held partially responsible for the total result. Government regulations limit his freedom to do whatever he would want to do in terms of fertilizer and pesticide use. Supermarkets and consumers’ representatives demand cheap, but healthy food products, free of high levels of nitrogen and pesticide residues. Due to major and minor scandals in the production of animals and plants these, once incidental, demands become structural. For many consumers organic agriculture has become the long term solution for achieving a sustainable and a safe way of food production. When we consider this bewildering turn of events having taken place in about one decade, crop production has become fairly complex. Crop protection is only one aspect of production, but a crucial aspect for quantity and quality. Our role to support the grower in these conditions should be to find acceptable alternatives for the pesticides he uses now. This should be our first priority, because harmonization of pesticide use within the EU is made more difficult by the lack of alternatives to pesticides in the various countries.

Biological complexity

By training we are used to respond to single issue questions like ‘how can we control ……’. Working on an acceptable answer, we usually find that the biological aspects are more complex than originally presumed. In natural conditions many more interactions between plants, their pests and diseases, the soil and environmental factors play an important role than we imagined and learned to handle in a reductionist way. For a holistic view we had nor the philosophy nor the methods. This is changing. Statistical methods like the ‘principle components analysis’ enable us to include more variables in our data analysis. At the same time we see that an increasing complexity requires additional and different scientific expertise. An example. When we started with our intercropping research we found interesting reductions of pest populations in various vegetables. The mechanisms behind these phenomena were and partly still are obscure. Of course we were eager to find out what was going on and we tried to isolate the system and to study it in the greenhouse, using clover intercropped leek and thrips as a model. Our efforts resulted in failures. We could not reproduce the field effect in the greenhouse. We understood only why, when we found that the effect was somehow mediated by the soil and close proximity of the roots of leek and clover was required. Root contact alone was not giving thrips suppression effects in the peat potting soil we used in the greenhouse trials. We concluded that probably root exudates alone were not inducing resistance to thrips in leek, but that some ‘soil factor’ is necessary to do the trick. This meant that our leek-thrips-clover system had to be enlarged to include the soil (Theunissen and Schelling, 1996). Indications for an influence of the presence of clover on the microflora in the soil were found by colleague bacteriologist Jim van Vuurde. He found a much larger abundance of bacterial endophytes in cauliflower and leek plants when undersown with clover than in the respective monocultures. From the extensive literature on endophytes we know that most endophytes seem to contribute positively to the physiology of their host plants, from the viewpoint of the plants anyway (a.o. Martensson et al., 1998). Cases are known that endophytes stimulate the defence mechanisms of their host plants to pests and diseases (a.o. Bargmann and Schönbeck, 1992; Bultman and Ganey, 1995; Vidal, 1996). The same has been observed for bacteria in the rhizosphere (Lazarovits and Nowak, 1997) and mycorrhiza (Gregorich et al., 1997).

Another effect of undersowing of clover on soil which has been found is the increased antagonism of the soil microflora against soil pathogens like Rhizoctonia solani in bio-tests on soil receptivity (Dijst, unpubl.data). This term was coined by Alabouvette et al. (1982). In the meantime there is a growing literature on soil receptivity (a.o. Oyarzun et al. 1997, 1998; van Loon et al. 1998; Postma et al. 1999). Both Oyarzun and Postma found that sterilization of soil or rockwool resp. increased the infectiousness of introduced soil pathogens enormously. Oyarzun et al. conclude that soil receptivity is ‘almost completely determined by the soil biota’. This is an important conclusion. In relation to intercropping, Dijst found that in soil from clover undersown fields soil borne plant pathogens were far less capable to infect test plants when compared to soil from the corresponding monocrops. This finding fits with our observations on suppression of cavity spot, Pythium spp., in carrots by undersowing with clover (Theunissen and Schelling, unpubl.). To conclude this example on intercropping, it seems to be made plausible that intercropped or undersown plant species affect the conditions of the soil and may influence the condition of the host-plant in relation to its defense capabilities. The undersown plants trigger in the host-plant a mechanism of self defense, mediated by soil biota. The same notion of the soil system as a part of the total ecosystem was reviewed by Ellert et al. (1997) and the contribution of soil biota to plant health by Gregorich et al. (1997). Thus, an ancient principle of organic agriculture on starting with a healthy soil is slowly getting a scientific base which cannot be ignored anymore. This means that in order to protect and enhance the presence and diversity of soil biota no biocides affecting soil organisms should be used. We must be very careful indeed with pesticides which affect life in the soil and in plant tissues. From this example we see how a single issue problem (pest on crop) may evolve into a multi issue potential solution with widely spread ramifications and increasing complexity. Scientifically, the single issue is only a part of the total picture of very interesting and potentially useful biological processes, waiting to be worked out.

Technical complexity

In the face of an increased biological complexity of problems and possible solutions, we need also an adequate methodology to tackle these matters. Apart from an open and unbiased mental attitude we need to develop and use techniques and methods which enable the researcher to get a grip on the multivariate abstractions of the biological reality. We need to learn to think in systems and to develop a holistic approach which is compatible with an unbiased, scientifically acceptable scrutiny of the observed research data. What we did and still do in a reductionist way must be equally possible in a holistic approach with the same severe scientific standards. This is another challenge for the next decade. An element of technical complexity is also the ‘translation’ of newly acquired insights into cropping methods for the grower. He cannot be denied his old tools before new ones have been developed without putting the burden of changing circumstances in crop production on his back alone.

Organizational complexity

How do we handle the increasing complexity of our scientific landscape? Where in the old days an entomologist was very cheap to keep, he needed only a sweepnet and an old marmelade bottle and made nearly all tools himself, to day science centers around 4

sophisticated equipment like those used for PCR’s, chromatographs, chemical analysis, growing chambers, specialised labs, etc. The expertise is costly and specialised. In the example which I worked out, it would mean that the old fashioned entomologist in boots with a clipboard, paper, pencil and a magnifying glass has to be replaced by a multi- disciplined team consisting of a phytopathologist, soil microbiologist, plant physiologist, organic chemist or biochemist and perhaps the odd entomologist. Government funds for research are shrinking and private funds do not exist for research on public interest which cannot be patented. Contrary to what is said, funding agencies are not conducive to multidiscipline basic research without a direct view on a marketable product. Researchers now are supposed to feed the ever increasing bureaucracies of the various management levels with data on all kind of activities. For research they have little time. This is carried out by students and post-docs. In spite of this kind of complexities, we have to organize our research in multidisciplinary teams to tackle the multiple issue questions and to arrive at meaningful results. This will be a challenge for the next decade. Another one will be to make the best of all fashions which come and go with the research funding in tow.

Psychological complexity

When we see a landscape from a plane, most of the time we see a mosaic of fields, local and connecting roads, canals and villages, industrial area’s, railroads. These elements form a complex pattern which changes as we travel. When we descend, this macro-complexity gradually changes into a micro-complexity of the spot where we stand on the ground. If we follow this picture of micro- and macro-complexity, we can consider our own field of research with its ins and outs as a spot of micro-complexity, where many factors interact. As we have seen, these factors have different natures: economical, biological, organizational and psychological. The most interesting and essential for us are, probably, the biological factors pertaining to the organisms and their ecology we choose to study. The macro-complexity which we have to cope with concerns our place in our social and scientific environment and our possibilities to be able to take our responsibility to society, to the benefit of the general public. Part of our job is to communicate our concerns and what we do to the public and our governments. And by doing this to influence public and governmental interest in issues we think are important. That is how concepts like sustainable food production, the health of our food, the protection of our drinking water resources, the conservation of landscapes and wildlife gain attention and weight. These items go beyond our daily work, but we have a shared civil responsibility to put and to keep them on the public agenda.

Conclusions

• As there are biological processes which can support the defense capabilities of plants against pests and diseases, one has to look for them actively and to be alert on principles which could be applied in crop protection. • As soil biota and endophytes play an important role in such processes, we must be extremely cautious with using pesticides, especially those which affect the soil or penetrate the plant tissue. • The increasing complexity in understanding of these processes requires a true and wide multi-disciplinary research effort. Therefore, plant protection researchers must seek strategic alliances with colleagues having relevant expertise. 5

• Since the groups with high financial stakes, within production and marketing chains of agricultural products, become larger it is both in their interest and in their power to finance organic crop protection research. • We need to learn to think in biological systems and to develop holistic methodologies designed to analyse complex situations. • An important practical necessity to support growers is to optimize the application of new principles into adapted or existing cropping methods. • In spite of increasing dependence of financing from the ‘market’ for our research, it is of vital importance to maintain our scientific integrity and independence of mind.

References

Bargmann, C. and Schönbeck, F. 1992: Acremonium kiliense as inducer of resistance to wilt diseases on tomatoes. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 99: 266- 272. Bultman, T.L. and Ganey, D.T. 1995: Induced resistance to Fall Armyworm (Lepidoptera: Noctuidae) mediated by a fungal endophyte. Environmental Entomology 24: 1196-1200. Ellert, B.H., Clapperton, M.J. and Anderson, D.W. 1997: An ecosystem perspective of soil quality. In: ‘Soil quality for crop production and ecosystem health’, Developments in soil science 25, Ed. E.G.Gregorich and M.R. Carter, Ch. 5: 115-141. Gregorich, E.G., Carter, M.R., Doran, J.W., Pankhurst, C.E. and Dwyer, L.M. 1997: Biological attributes of soil quality. In: ‘Soil quality for crop production and ecosystem health’, Developments in soil science 25, Ed. E.G.Gregorich and M.R.Carter, Ch. 4: 81- 113. Lazarovits, G. and Nowak, J. 1997: Rhizobacteria for improvement of plant growth and establishment. HortScience 32: 188-192. Loon, L.C. van, Bakker, P.A.H.M. and Pieterse, C.M.J. 1998: Systemic resistance induced by rhizosphere bacteria. Ann. Rev. Phytopathology 36: 453-483. Martensson, A.M., Rydberg, I. and Vestberg, M. 1998: Potential to improve transfer of N in intercropped systems by optimising host-endophyte combinations. Plant and Soil 205: 57- 66. Oyarzun, P.J., Dijst, G., Zoon, F.C. and Maas, P.W.T. 1997: Comparison of soil receptivity to Thielaviopsis basicola, Aphanomyces euteiches and Fusarium solani f.sp. pisi causing root rot in pea. Phytopathology 87: 534-541. Oyarzun, P.J., Gerlagh, M. and Zadoks, J.C. 1998: Factors associated with soil receptivity to some fungal root rot pathogens of peas. Applied Soil Ecology 10: 151-169. Postma,J., Willemsen-de Klein, M.J.E.I.M. and van Elsas, J.D. 2000: Effect of the indigenous microflora on the development of root and crown rot caused by Pythium aphanidermatum in cucumber grown on rockwool. Phytopathology (in press). Theunissen, J. and Schelling, G. 1996: Pest and disease management by intercropping: suppression of thrips and rust in leek. International Journal of Pest Management 42: 227- 234. Theunissen, J. and Schelling, G. Undersowing carrots with clover: suppression of carrot rust fly (Psila rosae) and cavity spot (Pythium spp.) infestation. (in review). Vidal, S. 1996: Changes in suitability of tomato for whiteflies mediated by a non-pathogenic endophytic fungus. Entomologia Experimentalis et Applicata 80: 272-274. 6

Monitoring Pest Populations

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3 ) 2003 pp. 7-12

Characteristics of population-dynamics of onion fly (Delia antiqua Meigen) by area-wide monitoring system

Z. Ilovai Plant Health and Soil Conservation Station of Budapest Capital, Budapest, Budaörsi út 141-145, H-1118, E-mail: [email protected]

Abstract: The onion fly Delia antiqua is one of the most important pest in Hungarian onion production. The damage caused to the crop varies by generation and depends on cultivation method. Present paper summarises the results of four-year study on the population-dynamics of the pest in time and in space in different cropping systems. The monitoring of population by trapping adults on the field level provides a good basis for determination of the optimal time for control.

Key words: onion pests, Delia antiqua, population dynamic, monitoring system

Introduction

In Hungary growing of onion (Allium cepa L.) possesses an over 200 years tradition. The crop is cultivated on about 6-8 thousand hectares, mainly in large-scale and well-developed, mechanized technology. The growing method contains both 1- and 2-years cultivation, carried out by seed sowing and seed-bulb planting respectively. Production of seeds and seed-bulbs is also significant. The concentrated onion growing regions were formed according to climatic and soil conditions. That is why characteristic varieties of the crop and growing systems have been developed. In the range of onion pests the onion fly Delia antiqua Meigen (Diptera: Anthomiidae) has been considered as the primary one by DARVAS et al. (1980), ILOVAI (1981) and ILOVAI et al.(1987). The proportion of fly-damaged bulbs in the yield depends on the presence of other primary and secondary pests (see Table 1).

Table 1. Diptera pests laying eggs on onion (by Darvas et al., 1980)

ONION PLANT Healthy Damaged by: Insecta / Fungi / Bacteria Delia antiqua Delia platura Liriomyza cepaea Eumerus strigatus Eumerus sogdianus Eumerus tuberculatus

The onion fly may generate 3 generations a year. However, the potential of damage depends on the stage of development of onion crops available. ILOVAI (1981) proved that, in areas where fields where crop are present at various developmental stages, the females prefere

7 8

to migrate for oviposition to plants having more than 3-4 leaves. Thus, the mobility of every generation is determined by the most optimal stage of the crop. From this point of view spatial and temporal monitoring of the pest is crucial. In order to follow the population dynamics different kinds of traps have been developed. In our experiments coloured sticky traps were used for observations on the field level, and water- plates for biocenological assays.

Table 2. Incidence of insects in different traps in onion fields (Mako region, HU)

Incidence, % Insects by Species, White White White baited1 Families and Orders water trap sticky tarp sticky trap Delia antiqua 1,0 0,3 1,1 Delia platura 81,3 41,0 37,0 Delia croarctata 0,5 0,7 0,1 Eumerus spp. 0,2 0,5 1,2 other Diptera species 13,4 2,4 2,4 DIPTERA 96,3 44,9 43,5 COLEOPTERA 0,8 20,1 16,3 Elateridae 0,6 19,4 15,9 LEPIDOPTERA 0,2 0,7 0,4 HYMENOPTERA 1,3 33,9 40,5 ONION’s PESTS 2,6 1,2 2,6 Other INSECTA 97,4 98,8 97,4 1The bait contained an extract of molasses (Nishyzawa et al., 1972)

In order to follow the process of colonization of onion fields cultivated in different ways, therefore being in different phenological stages and to clear the effect of weather conditions and mode of cultivation on quantitative/qualitative changes of the pest population it is necessary to monitor it in the same time, everywhere. The work presented here contains data of 4 years observations on flight activity of onion fly adults and the damage caused to the crop on the field/farm level. This data may be used in the region as a model for making decision about protection measures.

Materials and methods

The observations were carried out in the ancient and the most important region of Hungarian onion growing – in Mako area. All of three cultivation modes are present here: a. growing for seeds; b. 2 years cultivation of consumable onion, starting with seed-bulbs planting; c. 1 year cultivation of consumable onion, starting with seed sowing. The fields for the assays were chosen all over the region and all of the cultivation modes mentioned above were usually located at the same farm. In most cases cereals were preceding the onion growing. The seasonal flight activity of adults was monitored by placing white water-plates at the fields. The trapped material was collected every five days, determined (order-family- specimen) and counted. The damage caused by every generation was assessed using 100 plants-method. 9

In order to analyse the yearly changes in onion fly population dynamics 4-year data sets from three representative fields were processed. The yearly changes in number of trapped individuals were related to the degree of damage, which in fact, was a level of yield losses.

Results and discussion

The results of seasonal changes of onion fly population and damage caused to the crop are presented in Figures 1, 2, 3. The correlation between yearly levels of onion fly populations and the level of damage is shown in Figure 4. In Mako region all of three generations of onion fly cause damage to the crop. The separate generations occur spatially and chronologically in various densities. Independently from the place of emergence adults seek for onion crop suitable for laying eggs. Here the developmental stage of the crop is the decisive one. Therefore the role of separate generations in damaging onion differs by cultivation system: 1. generation (overwintering) − seed producing crop − overwintering crop (early onion) − volunteer 2. generation − 2-years cultivation − 1-year cultivation 3. generation − 1-year cultivation

40 damage, %; adult/trap 30

0 Adults/trap Year 3 Adults/trap Year 1 4 1 April 1 4 Damage Year 3 May 1 4

June Damage Year 1 1 4 July month, pentade 1 August Damage Year 1 Damage Year 2 Damage Year 3 Damage Year 4 Adults/trap Year 1 Adults/trap Year 2 Adults/trap Year 3 Adults/trap Year 4

Fig. 1. Flight activity of onion fly and damage caused to onion crop grown for seeds (Mako region, HU) 10

120

100

40 damage,%; adults/trap 20

0 Adults/trap Year 3 5 1 3 April Damage Year 4 1 5 June 3

5 Damage Year 1 1 3 August month,pentade

Damage Year 1 Damage Year 2 Damage Year 3 Damage Year 4 Adults/trap Year 1 Adults/trap Year 2 Adults/trap Year 3 Adults/trap Year 4

Fig. 2. Flight activity of onion fly and damage caused to onion crops cultivated in 2 years (Mako region, HU)

damage, %; adults/trap 15

10 5 0

4 Adults/trap Year 3 1 April 4 1 Adults/trap Year 1 May 4 1

June Damage Year 3 1 4 July

4 Damage Year 1 1

month/pentade 4 August 1 September

Damage Year 1 Damage Year 2 Damage Year 3 Damage Year 4 Adults/trap Year 1 Adults/trap Year 2 Adults/trap Year 3 Adults/trap Year 4

Fig. 3. Flight activity of onion fly and damage caused to onion crop cultivated in 1 year (Mako region, HU) 11

Starting the monitoring (trapping) at the endangered crop’s stage in accordance with the mode of cultivation would make supervised control of the pest on the field/farm level possible. Sometimes the density of the spring generation may be low; however, its danger for early crops can be serious, because at this time there are less fields at the optimal phenological stage Thus, the adults concentrate on suitable areas for egg-laying. In this case the critical time for the control will be much earlier.

damage %

30 R2 = 0,729

20 R2 = 0,9089 15

10 R2 = 0,995 5

0 0 50 100 150 200 250 300 350 400 450 500 Fly number/trap

seed prod. 2 years 1 year

Fig. 4. Correlation between population level and damage in different onion cultivation modes (data of 4 years)

The density of the summer generation is lower at the field level, but flies spread on larger territories, causing in finally higher yield losses. The third generation increases in summers which are cooler and do have heavy rain, but the damage remains low. With the help of the trapping method each generation of the pest can be followed well. The results presented above demonstrate that monitoring is necessary for making decision about the optimal control time.

References

Darvas, B., Deline-Draskovits, A. & Ilovai, Z. 1980: Eumerus species (Diptera: Syrphidae) developing in onion in Hungary. Növényvédelem 9-10: 433-440. Ilovai, Z. 1981: Population dynamics of onion fly in conditions of industrial onion production. PhD thesis, Horticultural University, Budapest 12

Ilovai, Z., Mile, L. & Szabó, P. 1987: Possibilities for the integrated control of onion fly. Proceedings of the 1st International Symposium on Vegetables for Processing, Kecskemét (HU), 3-7 August, 1987 Nishyzawa, S., Ashal, A., Nakamura, H., Tahara, S., Mizutani, J. & Obata, Y. 1972: Attraction of flies to some baits in an onion field. Memory of the Faculty of Agriculture, Hokkaido Univ. 8 (2):102-109.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 13-16

Monitoring root flies in Brassicae - recent developments

R. Meadow The Norwegian Crop Research Institute, Plant Protection Centre, Department of Entomology and Nematology, Høgskoleveien 7, N-1432 Ås, Norway E-mail: [email protected]

Abstract: An important part of systems for warning of attack by the cabbage root fly or the turnip root fly in cabbage, broccoli and cauliflower is monitoring of adult flies or eggs. In Denmark, felt traps have been used since the mid-1980s to monitor eggs. In Norway, egg-flotation was taken into use in the 1990s. Damage thresholds have now been established for the cabbage root fly in cabbage, broccoli and cauliflower based on felt traps or number of plants with eggs. These thresholds are being adapted for other crops and registration methods. Selective traps for adults of the brassica root flies were tested in the early 1990s, with disappointing results. These traps were modified at the Norwegian Crop Research Institute and have been very effective in catching adult root flies, while remaining selective. The first field trials with the new traps were conducted in 1999. The pilot experiments demonstrated that the traps are easy to use and that they catch the flies at the appropriate time of the season. Extensive trials will be performed in 2000 to determine whether the traps can replace egg- counting methods, either wholly or partially.

Key words: monitoring, oviposition, egg samples, felt trap, Delia radicum, Delia floralis, Brassica oleracea

Introduction

In recent decades, many different methods have been investigated for monitoring the root flies that attack Brassicae, the cabbage root fly Delia radicum and the turnip root fly D. floralis. Pan traps with soapy water to catch adult flies are easy to construct and have been used in many countries. Counting eggs at the base of plants or recording the presence of eggs has also been practiced in many places. Since the development of felt traps for eggs, these have been the basis of monitoring and warning of attack in cabbage, broccoli and cauliflower in Denmark (Bligaard et al. 1999). After investigations in a joint Nordic project of the various methods for monitoring eggs (Meadow et al. 1996), the egg-flotation method was taken into use in Norway. To improve the basis for these warnings, experiments were conducted to establish damage thresholds. Thresholds have now been established for the cabbage root fly in cauliflower based on felt traps (Bligaard 1999). These thresholds are being adapted for other crops, especially for the turnip fly in Swedish turnip, and for the egg-flotation method. The pan trap method of monitoring adult flies requires insect identification skills beyond those of most farmers. Selective traps for the brassica root flies have been tested, but the catches were disappointingly small (Meadow et al. 1996). These traps were modified at our laboratory to catch live flies for investigations on insect pathogens. The modified traps were very effective in catching adult root flies, while retaining the selectivity of the original traps, so that identification of the flies is unnecessary in practice (Klingen et al, in prep.). The traps are being reconstructed with the aim of making them more “user-friendly”. The first field trials with the new traps were carried out in 1999. The preliminary results are reported in this paper.

13 14

Materials and methods

Location The field trials reported here were conducted at two widely separated locations in western Norway. Both of the regions have intensive production of Brassica vegetable crops. The location on the southwest coast (Jæren) is approximately 25 km south of Stavanger. The location on the northwest coast (Smøla) is on an island approximately 100 km west of Trondheim. The crop in both trials was Swedish turnip.

Egg samples Eggs of both fly species were registered using the flotation method of Hughes & Salter (1959), but the soil around the base of the plants registered was removed and replaced with sand (see Meadow et al. 1996). Samples were taken twice weekly and the number of eggs per plant was recorded for 10 plants. Sample plants were in rows near edge-vegetation, but not the border row.

Traps for adult flies The traps used for monitoring adult flies were modified from the commercially produced Brassiceye® traps. These traps are cylindrical, with a bright yellow color and use an ethyl- isothiocyanate to attract the flies. The size of the entry holes and the isothiocyanate make the traps somewhat selective. The original traps have a small cup in the base filled with soapy water to catch the flies. In the modified version, the trap is inverted. This moves the attractant to the base of the trap. The top of the trap is an upside-down transparent cup with a funnel in the opening. This creates a bright top for the trap, which should cause the flies to move into the cup after they are in the cylinder. The funnel restricts movement back into the cylinder and the cup is coated with Tanglefoot®, to catch the flies. In practice, the flies can be counted through the clear cup, but in the experiments cups were removed and dated, and each fly was identified. The traps were placed on the field edge, well exposed to sunlight. The cups containing trapped flies were replaced twice weekly, at the same time as the egg samples were collected.

Results and discussion

The traps for adult flies functioned well and were reported to be easy to use. Figure 1 shows the number of D. radicum/floralis (unsorted) trapped at each location, compared to the number of eggs found by flotation. More extensive studies are planned for the season in 2000. These studies will focus on the relationship between first catch of flies and first eggs registered (time lag), size of trap catch and number of eggs, time and size of trap catch in relation to plant damage, and the effects of weather factors on trapping and oviposition.

140 35 Smøla, northwest Norway 120 30

100 25 Eggs Flies 80 20

60 15

40 10

20 5

0 0 25 26 27 28 29 30 31 32 33 34 35 36 37 38 Week

20 90 Jæren, southwest Norway 18 80

16 70 14 Eggs 60 12 Flies 50 10 40 8 30 6

4 20 2 10

0 0 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 Week

Fig. 1. The average number of eggs registered by flotation and flies trapped in the modified Brassiceye® trap throughout the season in 1999. See text for details about the two locations.

Acknowledgements

Thanks to Stein Winæs and Annette Folkedal of the Norwegian Crop Research Institute for technical assistance. Thanks also to Olav Inge Edvardsen and Kari Aarekol of the Norwegian 16

Agricultural and Extension Groups for providing the localities for the studies and for technical assistance.

References

Bligaard, J. 1999: Damage thresholds for cabbage root fly [Delia radicum (L.)] in cauliflower assessed from pot experiments. Acta Agriculturae Scandinavica, 49: 57-64. Bligaard, J., Meadow, R., Nielsen, O. & Percy-Smith, A. 1999: Evaluation of felt traps to estimate egg numbers of cabbage root fly, Delia radicum, and turnip root fly, Delia floralis in commercial crops. Entomologia Experimentalis et Applicata, 90: 141-148. Hughes, R.D. & Salter, D.D. 1959: Natural mortality of Erioschia brassicae (Bouche) (Diptera, Anthomyiidae) during the immature stages of the first generation. Journal of Animal Ecology, 28: 231-241. Klingen, I., Meadow, R. & Eilenberg, J. (in prep.): Levels of fungal infections in adult Delia radicum and Delia floralis trapped on the edge of a cabbage field. Meadow, R., Bligaard, J. & Shelton, A. M. 1996: Is there an easy method for monitoring root flies in Brassicae? IOBC wprs Bulletin 19 (11): 12-17. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 17-23

Population dynamics and supervised control of the leek moth, Acrolepiopsis assectella, in Germany

E. Richter, M. Hommes University of Hanover, Institute of Vegetable and Fruit Crops, Herrenhaeuser Strasse 2, 30419 Hannover, Germany Federal Biological Research Centre for Agriculture and Forestry, Institute for Plant Protection in Horticulture, Messeweg 11/12, 38104 Braunschweig, Germany

Abstract: The leek moth Acrolepiopsis assectella Zell. (Lepidoptera, Yponomeutoidae) occurs all over Germany and in several regions infestation is a serious problem, which can result in total destruction of the crop. Because there is little information on the population dynamics of A assectella , investigations on flight activity were made in different parts of Germany from 1994 to 1996. Investigations on its life cycle and supervised control are still being continued. Pheromone traps were used to detect the flight activity. The first flight period lasted from the end of April to the beginning of May. The second lasted from the beginning of July to the end of August and showed two peaks. This was reflected by results of rearing trials under outdoor conditions, where three generations per year were observed. The first egg deposition period occurred at the beginning of May, the second at the beginning of July and the third at the end of August. For a specific control of the leek moth, different control strategies were tested. The first tool was a net covering, which showed best results with no losses in yield or quality. However, it was expensive and labour-intensive. The second tool was the use of an action threshold of 10 % infested plants, which showed good results. The beginning of the flight activity and the egg deposition period showed a good correspondence for the first and second generation. This result led to a third strategy, a directed control approximately three weeks after the beginning of the egg deposition periods. This was sufficient to control the most important second and third generations of the leek moth.

Key words: Leek moth, Acrolepiopsis assectella, flight activity, life cycle, leek, Allium porrum, control, action threshold, net covering

Introduction

In a research project, investigations on the supervised control of pests and diseases on leek (Allium porrum L.) and onion (Allium cepa L.) were carried out from 1994 until 1997. Although the results showed that today the onion thrips (Thrips tabaci Lindeman) is the most important pest in leek, the leek moth was much more important until the 80th (Jansen, 1981). This change can probably be explained by the massive insecticide use to control the onion thrips in recent years (Hommes et al., 1994, Hoffmann et al., 1995, Villeneuve et al., 1996) which controls the summer generation of the leek moth as well. Nevertheless, the leek moth is still a serious pest in several regions of Germany and other European countries like the Netherlands (Nyrop et al., 1989; Minks, 1994), Switzerland (Imhof et al., 1996) and especially France (Geoffrion, 1979; Rahn, 1982). To develop strategies for a supervised control it is necessary to obtain precise information on the biology of the insect. The leek moth is a small insect with a wingspan of 13 to 16 mm, which deposits eggs on the leaves of leek. Damage is caused by the small larvae which first mine in the leafs and then move into the heart of the plants. Young plants can be totally destroyed by infestation, older

17 18

plants show losses in yield or at least quality. Results of the investigations on population dynamics and supervised control of the leek moth are presented.

Material and methods

Rearing of A. assectella Rearing took place in perspex cages (40 x 40 x 50 cm) in an outdoor insectary with potted leek and onion plants. Rearing lasted from July 1995 to July 1997.

Pheromone traps During the years 1994 to 1996 observations were made on the flight activity of A. assectella during the whole growing period by using pheromone traps (Research Institute for Plant Protection IPO-DLO, the Netherlands). Investigations were made in cooperation with the plant protection services of several federal states. Each plant protection service had two traps at a minimum of one location, which were controlled weekly.

Plant samples Pheromone traps only catch males. To get information on whether these catches correlate with the beginning of and the actual infestation in the field, plant samples were taken weekly during the whole growing season. Samples consisted of 15 plants from untreated fields and were examined in the laboratory. The number of larvae and pupae of A. assectella were counted and the percentage of damaged leaf area was estimated.

Control Several strategies to control the leek moth were tested. In 1999 experiments were carried out using a randomised block design with five replications including an untreated control. Plots consisted of 5 rows (20 cm between rows) of 5 m length (30 cm between plants). Leek, cv. ‘Longina‘ was planted in mid-May or mid-June.

Action threshold Samples of 10 plants per replication (50 plant in all) were taken and examined for infestation with leek moth larvae. The sampling procedure was a binomial, presence-absence sampling which showed the percentage of infested plants. Furthermore, the damaged leaf area was estimated. Like the sampling procedure, the frequency of sampling was a compromise between the costs and the essential precision. The sampling plan was used for all pests and diseases, hence the pest with the shortest life cycle, Thrips tabaci, gave the sampling frequency, which was every fortnight. This period is suitable for the leek moth with a developmental time of 80 days at a mean temperature of 18° C (Siegrist, 1945). Tested was a provisional threshold of 10 % infested plants (Hommes, 1992; Hommes et al., 1994).

Directed control The insecticide deltamethrin (liquid Decis) was used three weeks after the beginning of the egg deposition period in order to control the second and third generation of the leek moth.

Net covering The net was tested in 1994 to 1996 and in 1999 in early and late leek in different regions. The net ‘Insecta 500’ (Rovero Rolso Pak, The Netherlands) with a mesh width of 500 µm was used to protect the crop from leek moth infestation.

Results and discussion

Life cycle of Acrolepiopsis assectella The period of the individual life stages differed each year a little, depending on the different weather conditions. Hence not the absolute time of development is mentioned, but the time when certain life stages occured. In all years three generations were observed (Fig. 1). Egg deposition of the overwintering generation started at the beginning of May. In May larvae were found, in June pupae. Adults of that pupae hatched in the second half of June and, shortly after emergence, started egg deposition. The adults of this first summer generation lived for only six weeks. The time of completion of the second generation was shorter because of the higher temperature in summer, but the adults lived longer and could partly overwinter. Overwintering of the second generation may have its reason in the uncertainty of being able to complete the development under uncertain climatic conditions for the third generation. The last egg deposition took place at the end of August. These larvae could be found from September to the beginning of December in the leek plants. On account of the low temperature in autumn, the developmental time was considerably extended. In the middle of November a part of the adults hatched. These adults and the remaining pupae were able to overwinter. Adults from the overwintering pupae hatched in January. Even in the cold winter 1995/1996 with an average temperature of -4 °C, adults hatched in the few warmer days at 0°C to 4°C in the middle of January.

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Egg Larva Pupa Adult

Fig. 1. Life cycle of Acrolepiopsis assectella under outdoor conditions, Braunschweig (July 1995 to July 1997).

Catches of pheromone traps The first flight of the overwintering generation started with a few insects in the middle of April. Most insects were caught from the last week in April until to the middle of May (Fig.

2). For the next six weeks until the beginning of July only a few insects were found in the traps. Flight activity of the summer generations started at the beginning of July and lasted with variations in height until to the end of August. In September flight ended and only a few insects were found in the traps. Considering the maximum and minimum values of the catches it is obvious that the number of insects but not the time of flight activity changed in the various years and locations. Flight activity is described for varying periods during the season. Crueger & Hommes (1990) mention May/June for the first flight and August for the second. Other authors describe the middle of June and the middle of August for the flights (Gerst et al., 1977; Heil & Zotzmann, 1981). In those investigations the flight of the overwintering insects was probably not detected. Normally traps are not set in the field so early in the season, because there is no crop threatened. But there are hints of a flight of overwintering insects early in May (Heil & Zotzmann, 1981; Minks et al., 1994) and this corresponds with results from Siegrist (1945). He mentioned that egg laying begins at an average temperature of 10° C, which is at the end of April in central Europe and this was found in the presented investigations. An earlier flight period is described by Minks et al. (1994). It is possible that there is an additional generation in warmer areas and flight activity takes place already at the beginning of March. Geoffrion (1979) described five generations in areas with a warm climate like the south of France. If the detected egg deposition periods are added to Fig. 2, the good correspondence between the beginning of flight activity and the time of egg deposition for the first and second generation is obvious.

Distribution of A. assectella catches in % 20

0 Mar Apr May Jun Jul Aug Sept Oct

Fig. 2: Relative weekly catches of A. assectella in pheromone traps during the year (Mean of 7 locations with minimum and maximum values in 1994 to 1996); black horizontal bars = periods of egg deposition.

Plant samples The catches from the pheromone traps showed flight activity in April/May and from July to August in all regions. Nevertheless, crops planted late in June showed no or only minor damages for the whole growing season, which did not lower quality at harvest. Only plants

from overwintering crops and crops planted early in May had been infested. There, first larvae were found in May. In 1994 leek was only infested by the insects, which had overwintered, but showed no infestation by the summer generations (Fig. 3). In 1995 and especially 1996 plants were severely infested during the whole growing season. Usually there was only one larva per plant, so that the number of larvae found was similar to the number of infested plants. More larvae per plant were rarely found. Only few larvae pupated on the leek, hence no connection between the number of larvae and pupae could be found. The larvae of the leek moth are very active, looking for a good place for pupating. This observation was confirmed by the rearings, where most larvae pupated at the sides of the cages.

% infested plants

100 1994

1995 80

1996 60

0 May June July August Sept. Oct. Nov. Dec.

Fig. 3. Infestation with leek moth larvae in the field. Samples from untreated leek plots planted in May at Braunschweig in the years 1994 to 1996 (n=15).

Control of the leek moth using the action threshold In 1999 infestation with larvae of the second generation was low with a small peak in August. The third generation was much more significant, because of the excellent weather conditions in August and September (Fig. 4). Hence 12 % of the plants in the untreated plot were infested. This seems to be a low value, but the percentage of damaged plants was 64 % two weeks later (unpublished data). This reveals the major problem, the sampling method. It is simply impossible for the grower to sample plants with eggs. Sampling damaged plants is difficult, because damages can be found over a long period, even when larvae have long gone, and may induce unnecessary treatments. It may be possible to sample plants with early feeding symptoms (Nyrop et al., 1989), but under bad weather conditions, larvae die early and control would no longer be necessary. Because of these difficulties, the parameter infested plants seems to be the best tool for measurement. And this is the reason for such a low threshold of 10 % infested plants. In the experiment there was only one treatment according to the action threshold at the end of August which decreased infestation. Although the effect of a decreasing infestation was similar for all plots, the difference becomes obvious by considering the percentage of plants in the various quality classes (Table 1)

Directed control The length of the egg deposition period was much shorter than described in the literature (Jansen, 1981). Crops are threatened for only two weeks for each generation. With subsequent

insecticide treatments it is possible to control the pest. Hence treatments according to the directed control had a very strong effect. The first treatment after the egg deposition period in July already reduced the infestation to a great extent (Fig. 4). Decreasing that generation led to a decrease in the next generation. The final treatment at the end of August mad sure that plants were free from infestation. The result in quality of plants at harvest gives evidence of the impressive efficacy of this strategy, which leads to an excellent treatment guidance on timing for the grower. However, not all crops in all areas are threatened, so the grower should combine this strategy with monitoring at the right time to see if his crop is threatened, to be sure he only sprays when necessary. Costs are low because only two monitorings are needed.

% infested plants 20

0 25.06. 08.07. 22.07. 05.08. 20.08. 30.08. 16.09. 30.09. 14.10. untreated action-threshold directed-control

Fig. 4. Percentage of infested plants in an untreated plot, with chemical control according to the action threshold and the directed control (n = 50 plants; 1999)

Table 1. Quality and weight of leek plants form untreated, net covered and treated plots according to the action threshold or directed control in 1999 (bc = before cleaning, ac = after cleaning; ia = insecticide application).

Percentage of plants in quality classes Weight in g Treatment 1 2 3 4 5 ia bc ac

untreated 50 30 18 2 0 - 546 366 action threshold 60 36 4 0 0 1 508 333 directed control 96 2 2 0 0 2 552 379 net covering 100 0 0 0 0 - 564 376

Net covering The net simply prevented the crop from being infested in all experiments since 1994 in which infestation with the leek moth was found. Leek was without any damage or losses in yield and

of the best quality (Table 1). A problem is the high price and the amount of work involved, but nevertheless it is a good choice for the organic grower. Another adantage of the net is the effect in reduction of thrips infestation (Richter, 1998)

Acknowledgement

The research project was supported by the Federal Ministry of Food, Agriculture and Forestry.

References

Crueger, G. & Hommes, M. 1990: Krankheiten und Schädlinge an Porree. Gemüse 26(2): 130-135. Gerst, J.-J., Gachon, C., Stengel B. & Stengel, M. 1977: La teigne du poireau en Alsace. Réflexions sur cinq années de piégage sexuel. P.-H.-M.-Revue Horticole 182: 31-39. Geoffrion, R. 1979: La teigne du Poireau. Phytoma – Defense des cultures: 5-7. Heil, M. & Zotzmann, K.F. 1981: Über die Kontrolle des Flugverlaufes der Lauchmotte Acrolepia assectella Zell. mit Hilfe von Licht und Pheromonfallen. Gesunde Pflanzen 33(7): 153-156. Hoffmann, M.P., Petzold, C.H., MacNeil, C.R., Mishanec, J.J., Orfandes, M.S. & Young, D.H. 1995: Evaluation of an onion thrips pest management program for onions in New York. Agriculture, Ecosystems and Environment 55: 51-60. Hommes, M., 1992: Simple control threshold for foliage pests of leek. IOBC wprs Bulletin 14(4): 115-121. Hommes, M., Hurni, B., Van de Steene, F. & Vanparys, L. 1994: Action thresholds for pests of leek – Results from the co-operative experiment. IOBC wprs Bulletin 17(8): 67-74. Imhof, T., Baumann, D.T., Städler, E. & Wyser-Hammel, I. 1996: Untersaat in Herbstlauch reduziert die Thripspopulation. Agrarforschung 3(7): 337-340. Jansen, W. 1981: Lauch und Lauchmotte. Gemüse 17(3): 82. Minks, A.K., Voermann S. & Theunissen, J. 1994: Improved sex attractant for the leek moth, Acrolepiopsis assectella Zell. (Lep., Acrolepiidae). Journal of Applied Entomology 117: 243-247. Nyrop, J.P., Shelton, A.M. & Theunissen, J. 1989: Value of a control decision rule for leek moth infestation in leek. Entomologia Experimentalis et Applicata 53: 167-176. Rahn, R. 1982: Incidence du changement de méthode culturale sur le dévelopment des phyttophages: cas de la culture de l`oignon (Allium cepa) et de la dynamique de population de la teigne de poireau, Acrolepiopsis assectella Z. (Lep., Plutellidae). Agronomie, 2(8): 695-699. Richter, E., 1998: Populationsdynamik und Integrierte Bekämpfung von Thrips tabaci Lind. (Thysanoptera: Thripidae) an Porree und Zwiebeln. Dissertation, University of Hanover, Publisher: Cuvillier, Göttingen. Siegrist, H. 1945: Untersuchungen über die Lauchmotte Acrolepiopsis assectella und ihre Bekämpfung. Dissertation ETH Zürich. Villeneuve, F., Bosc, J.-P., Letouzé, P. & Levalet, M. 1996: Flight activity of Thrips tabaci in leek fields and the possibility of forecasting the period of attack. OILB wprs Bulletin 19(11): 25-32.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 25-31

Monitoring of western flower thrips (Frankliniella occidentalis Pergande) in the vicinity of greenhouses in different climatic conditions in Slovenia

S. Trdan1, G. Jenser2 1 University of Ljubljana, Biotechnical Faculty, Agronomy Department, Institute for Phytomedicine, Jamnikarjeva 101, 1111 Ljubljana, Slovenia 2 Plant Protection Institute, Hungarian Academy of Sciences, Herman Ottó út 15, 1525 Budapest II., Hungary

Abstract: To study the bionomics of western flower thrips (Frankliniella occidentalis Perg.) in Slovenia in the open, monitoring of this pest was performed on six locations in the vicinity of the greenhouses using light blue sticky boards. From the data obtained during this investigation - from September 1997 till April 1999 - it was established that in the inner part of the country western flower thrips can exhibit mass occurences in the period from June till August, average populations occur in May and September and those low in number in April and October. The climate in region of the Slovenian Primorje (the warm climate because of the influence of the Adriaric sea) enables mass occurences of the pest in the open from May till September and average populations in April and October, at the seaside single specimens can be found even in December, while a little bit further from the sea these are limited to the periods of March and November. Therefore it can be concluded that in Slovenia western flower thrips (Frankliniella occidentalis Perg.) does not overwinter in the open in the stage of an active imago. For the time being it be considered an economically important pest only in greenhouses.

Key words: monitoring, Frankliniella occidentalis, environment, Slovenia.

Introduction

The mass occurrence of western flower thrips (Frankliniella occidentalis Perg.) in Slovenia in some greenhouses and their vicinities after 1992 (Janežič, 1993; Trdan et al., 1999), when its presence in our country was first confirmed, together with the fact that in Europe it is considered one of the most important pests on vegetable and ornamental plants especially in greenhouses and other indoor places (Brødsgaard, 1989; Schmidt and Frey, 1995; Tommasini and Maini, 1995), was the reason that we undertook an investigation of its life and development (bionomics) in various districts of our climatically very diverse country. The European literature describing relationships between the western flower thrips and its environment is relatively scarce. So, up to now, it has been reported that in the littoral part of Spain the pest remains active in the open air all the year round (Lacasa et al., 1995), or that in the central part of Italy imago can overwinter in a torpid (dormant) form on some hosts also outside the greenhouses (Del Bene and Gargani, 1989) and that in Hungary it has been found outside the greenhouses only in warmer periods (Jenser, 1990). Until recently, the western flower thrips has been considered an exclusively greenhouse pest in Slovenia, so only few payed attention to the direct influence of the environment on its occurrence in various geographic districts. The 18-months investigation of the bionomics of the western flower thrips was undertaken to get data on these influences. The bionomics of

25 26

Frankliniella occidentalis Perg. in the open air was conducted on six locations in five districts in Slovenia (Trdan, 1999a).

Material and methods

We were studying the fluctuations in the number of the pest specimens in the open air all the year round. Because of the interesting geographic position of Slovenia, agricultural land is located in three major districts with different climate (subpannonical/continental in the eastern part, subalpine in the central lower part and mediterranean in the western part of the country). These districts also exhibit several local climatic differences (Rakovec and Vrhovec, 1998). We wanted to study the survival of western flower thrips (Frankliniella occidentalis Perg.) in the open air during the winter period under these different conditions. The monitoring of the species was performed using light blue sticky boards, which are worldwide most frequently used for such purposes during the last decade – and are recently (in the last years) becoming popular also in Slovenia (Cabello et al., 1991; Brødsgaard, 1993; Trdan, 1999bc). Rectangular sticky traps (11 x 13 cm) were used in the period from September 1997 till April 1999 on the following UTM locations: Ljubljana (VM50), Kočevje (VL95), Juršinci (WM74), Vrtojba near Nova Gorica (UL98), Šempeter near Nova Gorica (UL98) and Koper (VL04). These are the locations where more or less numerous populations of this pest has been reported in the greenhouses during the years preceeding the monitoring. During the chosen periods the sticky traps were placed round the greenhouses: 16 boards on the top of pillars app. 1 m high, 4 of them immediately at the greenhouse, 4 at the distance of 10, 4 at the distance of 20 and 4 at the distance of 50 m from the greenhouse. The time of exposure was different for different periods of the year, in summer usually shorter than in winter. After the exposure, the boards were collected and kept in PE bags. Till the examination they were kept in refrigerator (temperature 2-4 °C). They were examined under a classical stereomicroscope (15-times magnification). On both sides only the females were considered, since the determination of males under a stereomicroscope is difficult and unreliable.

Results and discussion

On all the locations the first females were observed already in September or October 1997. With the exception of Ljubljana, where the population of the pest went through a mass gradation in the greenhouse some months before the monitoring started and remained in it also during the first two observations, the distribution of the specimens on the boards which were placed at different distances from the greenhouses was rather uniform. In the beginning of November no female imagos we found any more in the central part of Slovenia, only single specimens were found on the three locations in Primorje. The unusually warm December 1997 - February 1998 period made us proceed with the monitoring in Ljubljana and Juršinci but no thrips were found on the boards. The species Frankliniella occidentalis Perg. did not reach its activity threshold in spite of the very warm period, so the thrips did not leave the nearby greenhouses, where they overwintered very probably as imagos or as non adult stages in soil. No female imagos were found in Vrtojba near Nova Gorica, Šempeter near Nova Gorica and in Koper during the winter months, the rare specimens caught very probably originated from the greenhouses nearby. In the spring 1998 the first females were observed in the period from the end of February till the beginning of March in Koper. This has been expected, as the average temperatures on this location were the highest and so these females were the first to enter the active period.

The greenhouse on this location was empty during the winter months and we assume that the specimens would have been found even earlier if not so. In Šempeter near Nova Gorica the female imagos were detected app. one month later, they were found also 50 m from the greenhouse, which could mean that they could overwinter on the host plants (trees, bushes or wild growing grasses) or in soil. In Vrtojba near Nova Gorica the first females were observed in the period between the end of April and the beginning of May. This may be due to non heated greenhouse on this location which is also considerably more exposed to wind compared to the location in Šemperter near Nova Gorica. In Juršinci first females were observed app. at the same time as in Šempeter near Nova Gorica, they came very probably from the greenhouse where ornamental flowers were grown at that time. In Kočevje and in Ljubljana the first females were found app. at the same time as in Vrtojba near Nova Gorica. In the period from May 1998 till September 1998 different numbers of females were caught on the sticky boards. The differences obviously have various reasons, the amount of the rainfall being the decisive parameter. The agrotechnical measures undertaken also play an important part. So, intensive insecticide treatments of chrysanthemums in the greenhouse in Kočevje resulted in a greater number of pests further from the geenhouse, where plenty of suitable host plants were available. Using of herbicides to control weeds in the greenhouses or turf in their vicinity can drastically reduce the number of the specimens at small distances from the greenhouses. This was true for Kočevje, Juršinci and Vrtojba near Nova Gorica. The pronounced decline of the pest population in the greenhouse in Ljubljana is a result of the spring weed control in it. Namely, during autumn 1997 and winter 1997/98 the species could comfortably survive as imagos on the weeds present (e. g. Stellaria media (L.) Vill. and Convolvulus spp., only single specimens were found on the latter). The constantly present uniform population in Juršinci had plenty of vegetables to feed on, the abundant foliage was a shelter from bad weather conditions. The pronounced maximum in the number of the western flower thrips caught on the light blue sticky boards in Vrtojba near Nova Gorica can be attributed to the less abundant rainfall in the period before the boards were placed. On such exposed sites, these have a pronounced influence on the bionomics of the species in the open air. The low number of the specimens caught in Koper was very probably due to relatively empty greenhouse during the entire vegetation period. The thrips fed on wild growing plants, so they were found also at greater distances from the greenhouse. The occurrence of western flower thrips (Frankliniella occidentalis Perg.) in Šempeter near nova Gorica was rather uniform, due to the great variety of plants grown there, so the pests have many host plants to choose from when they look for shelter in bad weather conditions. In September 1998 the pest became less frequent on all the locations, in October only single specimens were found on some locations. During the last period of this investigation (March 1998) first females were already found on the sticky boards, on these location (e. g. Šempeter near Nova Gorica) they appeared at the same time as during the previous year. The data on the number of the western flower thrips (Frankliniella occidentalis Perg.) females caught on the sticky boards during chosen intervals were combined with the data on the temperatures of the environments and cumulative rainfall during the same intervals in order to constuct practical climatograms for the six locations in question. These have a ecological value only if combined with the lowest and the highest higrothermal requirements of the species investigated. Using the data obtained, practical climatograms for the locations under investigation were constructed, average monthly temperatures for a 30-year period (1961-1990) were considered. During the monitoring the cumulative rainfall differed too much from the 30-year average, so these were not used in the constructing of climatograms.

Kočevje Ljubljana

35 400 30 350 300 25 50 m 250 50 m 20 20 m 20 m 200 15 10 m 10 m 150 1m 1 m 10 100 No. of females caught No. of females caught 5 50 0 0 9.03.- 5.05.- 8.10.- 26.03.- 21.04.- 19.09.- 21.10.- 11.11.- 15.09.- 17.10.- 21.01.- 13.07.- 21.09.- 10.06.- 13.07.- 17.08.- 17.09.- 9.04.1998 6.05.1998 26.09.1997 24.10.1997 30.01.1998 18.03.1998 20.05.1998 24.07.1998 30.09.1998 29.09.1997 15.10.1997 30.10.1997 22.11.1997 22.06.1998 23.07.1998 25.08.1998 29.09.1998 The period of positioning of sticky boards The period of positioning of sticky boards

Juršinci Vrtojba near Nova Gorica

45 90 40 80 35 70 30 50 m 60 50 m 25 20 m 50 20 m 20 10 m 40 10 m 15 30 1 m 1 m 10 20 5 10 No. of females caught 0 caught females of No. 0 13.1.1998 22.12.1997- 4.10.-11.10.1997 18.10.-1.11.1997 8.11.-17.11.1997 3.05.-16.05.1998 8.06.-21.06.1998 11.03.–2.04.1998 15.01.–9.02.1999 11.03.–1.04.1999 26.11.-26.12.1998 21.09.-28.09.1997 14.02.-22.02.1998 27.03.-12.04.1998 11.07.-24.07.1998 15.08.-22.08.1998 17.09.–25.09.1997 28.10.–10.11.1997 30.01.–20.02.1998 22.04.–15.05.1998 14.07.–21.07.1998 18.09.–29.09.1998 12.09.–26.09.1998 17.10.–24.10.1998 The period of positioning of sticky boards The period of positioning of sticky boards

Šempeter near Nova Gorica Koper

25 7 6 20 50 m 5 50 m 15 20 m 4 20 m 10 10 m 3 10 m 1 m 2 1 m 5 1 No. of females caught caught females of No. 0 No. of females caught 0 13.1.1998 15.1.1999 22.12.1997- 26.12.1998- 13.1.–30.1.1998 11.03.–2.04.1998 15.01.–9.02.1999 11.03.–1.04.1999 26.11.-26.12.1998 2.04.–22.04.1998 9.02.–11.03.1999 6.10.–16.10.1997 2.12.–22.12.1997 17.09.–25.09.1997 28.10.–10.11.1997 30.01.–20.02.1998 22.04.–15.05.1998 14.07.–21.07.1998 18.09.–29.09.1998 20.02.–11.03.1998 10.06.–24.06.1998 18.08.–25.08.1998 19.10.–26.10.1998 The period of positioning of sticky boards The period of positioning of sticky boards

Fig. 1-6: Average number of western flower thrips (Frankliniella occidentalis Perg.) females caught at various distances from the greenhouses on six locations in Slovenia in the period from September 1997 till April 1999.

The data on the number of the western flower thrips (Frankliniella occidentalis Perg.) females caught on the sticky boards during chosen intervals were combined with the data on the temperatures of the environments and cumulative rainfall during the same intervals in order to constuct practical climatograms for the six locations in question. These have a ecological value only if combined with the lowest and the highest higrothermal requirements of the species investigated. Using the data obtained, practical climatograms for the locations under investigation were constructed, average monthly temperatures for a 30-year period (1961-1990) were considered. During the monitoring the cumulative rainfall differed too much from the 30-year average, so these were not used in the constructing of climatograms.

Kočevje Ljubljana

168 168 November June 148 June Oktober September August 148 November September August 128 March 128 December April October May July 108 108 May July December April 88 March January February Januar88 February 68 y 68

48 48 Cumulative rainfall (mm) 28 rainfall (mm) Cumulative 28

8 8

-5-12 0 5 10 15 20 25 -5-12 0 5 10 15 20 25 o Average temperature ( C) Average temperature (oC)

Juršinci Vrtojba near Nova Gorica

168 168 November 148 148 June October 128 128 September August August December April July 108 108 September May November June January March July 88 October 88 February May 68 April 68 December March 48 48 January February Cumulative rainfall (mm) rainfall Cumulative Cumulative rainfall (mm) Cumulative 28 28

8 8

-5-12 0 5 10 15 20 25 -12 0 5 10 15 20 25 o Average temperature (oC) Average temperature ( C)

Šempeter near Nova Gorica Koper

169 169 November June 149 October 149 August 129 September 129 Januar May December September 109 y April July 109 November March October August December 89 89 February June Januar April May 69 69 March July February 49 49 Cumulative rainfall (mm) 29 Cumulative rainfall (mm) 29

9 9

-11 0 5 10 15 20 25 -11 0 5 10 15 20 25 Average temperature (oC) Average temperature (oC)

Fig. 7-12: Practical climatograms for the locations where the monitoring of the western flower thrips (Frankliniella occidentalis Perg.) took place, temperature intervals with different probabilities of the pest occurences in the open are given (...... small probability; average probability; extremely probable)

In the practical climatograms three temperature intervals with different probability of the pest occurrence in the open were presented. The lower and the higher limits of each interval were determined considering the average number of the western flower thrips females caught on all six locations in comparable time intervals. It was shown that the months with an average temperatue between 15,5 and 23 °C are the most favourable for the occurrence of the species Frankliniella occidentalis Perg., those with an average temperature between 10 and 20 °C are less favourable and those with an average temperature between 6 and 18 °C are the least favourable. The intervals overlap quite a bit, which can be explained by the influence of

30 other climatic conditions, especially rainfall. Rainfall can drastically reduce the number of the specimens in the open also under otherwise favourable weather conditions (temperature). As far as temperature is considered, the most favourable period for the development of the pest in the open air in the inner Slovenia (data from the locations Ljubljana, Kočevje and Juršinci) is that from June till August and under some conditions also September, the months May, September and October (and under some conditions also April) are less favourable, while April and October are the least favourable. In the region of the Slovenian Primorje (data from the locations Vrtojba near Nova Gorica, Šempeter near Nova Gorica and Koper) the most favourable period for the development of the pest in the open air is that from May till September, the months April and October (and under some conditions also November) are less favourable, while practical climatograms revealed March and November (and on the locations at the seaside as e.g. in Koper also December) as the months during which the survival in the open is just possible. The results of similar investigations in the northeastern part of the USA which have a similar climate as Slovenia can be used to confirm the conclusions presented in this work. They state, that the first imagos are found in May and they overwinter in soil in the open air in spite of the fact that the temperatures during the winter can be below zero as long as 35 days in succession. (Felland et al., 1993, 1995). The climate in Slovenia is milder even in the continental part of the county. The data for January, the coldest month in Slovenia, are as follows: in Kočevje and in Maribor the lowest temperatures are not below zero for more than 26 days and in Ljubljana not for more than 24 days in succession (Hydrometeorological Institute of Slovenia, 1996). Though western flower thrips can be active in the open all the year round in the littoral region in Spain, the climate in the Slovenian Primorje is obviously colder and gives no such opportunities. The overwintering in an non active form, though in the open air, does not give the pest any possibility to develop a resistance to lower temperatures on the short term. Trials of systematic adaptation of active larvae and imagos to lower temperatures which were conducted in England, failed. The insects were not able to overwinter in an active form (McDonald et al., 1997). Though the results of the monitoring show that the pest can survive unfavourable weather conditions either in protected places (e. g. greenhouses etc.) or in soil, no serous damages by this pest are probable on its hosts which are grown in the open. Meaning that in Slovenia, the western flower thrips (Frankliniella occidentalis Perg.) can be considered an economically important pest only in greenhouses, at least until it develops strains which would be resistant to lower temperatures or untill the climate in Slovenia has changed considerably. Though the results of the monitoring show that the pest can survive unfavourable weather conditions either in protected places (e. g. greenhouses etc.) or in soil, no serous damages by this pest are probable on its hosts which are grown in the open. Meaning that in Slovenia, the western flower thrips (Frankliniella occidentalis Perg.) can be considered an economically important pest only in greenhouses, at least until it develops strains which would be resistant to lower temperatures or untill the climate in Slovenia has changed considerably.

References

Brødsgaard, H.F. 1989: Frankliniella occidentalis (Thysanoptera; Thripidae) – a new pest in Danish glasshouses. A review. Dan. J. of Plant and Soil Sci. 93: 83-91. Brødsgaard, H.F. 1993: Monitoring thrips in glasshouse pot plant crops by means of blue sticky traps. IOBC/WPRS Bull. 16(8): 29-32.

Cabello, T., Abad, M.M., Pascual, F. 1991: Capturas de Frankliniella occidentalis (Pergande) (Thys.: Thripidae) en trampas de distintos colores en cultivos en invernaderos. Bol. Sanid. Veg. Plagas 17: 265-270. Del Bene, G., Gargani, E. 1989: Contributo alla conoscenza di Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Redia 72(2): 403-420. Felland, C.M., Hull, L.A., Teulon, D.A. J., Cameron, E.A. 1993: Overwintering of western flower thrips (Thysanoptera: Thripidae) in Pennsylvania. Can. Entomol. 125: 971-973. Felland, C.M., Teulon, D.A.J., Hull, L.A. 1995: Overwintering and Distribution of Western Flower Thrips in the Mid-Atlantic United States. Thrips Biology and Management, Plenum Press, New York and London: 461-464. Hydrometeorological Institute of Slovenia, 1996: Climate of Slovenia (ed. Cegnar, T.). Ljubl., Minist. of Environ. and Phys. Plan.: 70 pp. Janežič, F. 1993: Third contribution to the knowledge of thrips species (Thysanoptera) on plants in Slovenia. Res. Rep. Biotech. Fac. Univ. of Ljubl. 71 (Agric. issue): 161-180. Jenser, G. 1990: Über das Freiland-Auftreten von Frankliniella occidentalis (Perg.) (Thysanoptera) in Ungarn. Anz. Schädlingskde., Pflanzenschutz, Umweltschutz, 63: 114- 116. Lacasa, A., Esteban, J.R., Beitia, F.J., Contreras, J. 1995: Distribution of Western Flower Thrips in Spain. Thrips Biology and Management, Plenum Press, New York and London: 465-468. McDonald, J.R., Bale, J.S., Walters, K.F.A. 1997: Low temperature mortality and overwintering of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). Bull. of Entomol. Res. 87: 497-505. Rakovec, J., Vrhovec, T. 1998: Osnove meteorologije za naravoslovce in tehnike. Ljubl., Drus. mat., fiz. in astron. Slov.: 253-258. Schmidt, M.E., Frey, J.E. 1995: Monitoring of western flower thrips Frankliniella occidentalis in greenhouses. Med. Fac. Landbouww. Univ. Gent 60 (3a): 847-850. Tarman, K. 1992: Osnove ekologije in ekologija živali. 1. izdaja.- Ljubl., Drž. založ. Slov.: 87-89. Tommasini, M.G., Maini, S. 1995: Frankliniella occidentalis and other thrips harmful to vegetable and ornamental crops in Europe. In: Biological control of thrips pests, Wageningen Agric. Univ. Pap. 95 (1): 1-42. Trdan, S. 1999a: Bionomics of western flower thrips (Frankliniella occidentalis Pergande, Thysanoptera) in Slovenia. Master of Sci. Thesis, Ljubl., Biotech. Fac., Agron. Dep.: 101 pp. Trdan, S. 1999b: Colour preference of some economically important Thysanoptera species. Lect. and Pap. present. at the 4th Slov. Conf. on Plant Prot., Portorož, March 3-4, 1999, Plant Prot. Soc. of Slov., Ljubljana: 493-498. Trdan, S. 1999c: Monitoring cvetličnega resarja (Frankliniella occidentalis Perg.) z barvnimi lepljivimi ploščami. Sodob. kmet. 32 (10): 475-480. Trdan, S., Seljak, G., Jenser, G. 1999: Western flower thrips (Frankliniella occidentalis Perg.) in Slovenia. Lect. and Pap. present. at the 4th Slov. Conf. on Plant Prot., Portorož, March 3-4, 1999, Plant Prot. Soc. of Slov., Ljubljana: 239-246.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 33-37

Monitoring the flight activity and damage of Thrips tabaci (Lind) in different varieties of white and red cabbage

F. Van de Steene and L. Tirry Faculty of Agriculture and Applied Biological Sciences, University Ghent, Department of Crop Protection, Laboratory of Agrozoology, Coupure Links 653, 9000 Gent, Belgium.

Abstract: The flight activity of Thrips tabaci was monitored in 1998 and 1999 in white and red cabbage to obtain a better understanding of its population dynamics. Maximum flight activity occurred from 14 to 28 July in 1998 and from 20 July to 10 August in 1999. Peak flight activity was recorded on 21 July 1998 and 3 August 1999. In order to evaluate their possible resistance to onion thrips, a range of commercially important white and red cabbage varieties for fresh market was tested in the field. Thrips damage was assessed by counting the number of larval and adult thrips on the leaves and the number of damaged leaf layers at two points of time. No white cabbage varieties were found to be resistant, but there were substantial differences in the number of layers injured and in the severity of the injuries. The red cabbage varieties "Lectro" and "Reliant" proved to be resistant.

Key-words: Thrips tabaci, white and red cabbage, plant resistance.

Introduction

Cabbage is generally a late season crop in Belgium, planting starts in May and harvesting ends in November. The onion thrips, Thrips tabaci (Lind) is a severe pest of cabbage crops. Large populations of thrips may develop on cabbage crops and render the crop unmarketable. Thrips feed on the leaves and cause a bronze colour and rough texture on white cabbage and white bumps known as oedema on red cabbage. Cabbage affected by oedema are generally rejected by the market. Even small number of thrips can cause severe losses in fresh and stored produce and therefore growers need to achieve high levels of control. Thrips live in the cabbage heads in the small spaces between the layers of the leaves. Hence, the are well protected against both adverse environmental conditions and sprays of insecticide. Chemicals often fail to kill thrips deep in the developping heads and so repeated applications are necessary. Problems in achieving satisfactory control with insecticides have led in Belgium to research for more understanding about the flight activity of T. tabaci in cabbage fields and for the susceptibility of commercially important white and red cabbage varieties to thrips attack. In addition, host plant resistance is one alternative which is receiving attention in several countries to reduce insecticide inputs against thrips in white cabbage (Shelton et al., 1983, 1988, 1998; Stoner et al., 1989; Ellis et al., 1994) and if measures are to be taken to improve crop protection, it is important to know more about the populations dynamics of the pest. To obtain more information on the flight activity of thrips and on the susceptibility for attack, two field experiments with different varieties of white and red cabbage were carried out in 1998 and 1999.

Materials and methods

The experiments were done at the Provincial Vegetable Research Centre at Kruishoutem. Two early: "Perfecta" and "Touchma" and seven late varieties of white cabbage: "Rivera",

33 34

"Roboston", "Marathion", "Galaxy", "Lennox", "Bartolo" and "Bingo" and four varieties of red cabbage: "Rodima", "Reliant", "Lectro" and "Autoro" were chosen for the experiments. The cabbage were transplanted in the field on 15 May 1998 and on 6 May 1999. Two rows of each variety grew according to local commercial practice. The movement of T. tabaci from a wide range of early-season hosts into the cabbage field was studied from planting by aerial counts of adults on 15x18 cm light blue sticky traps. This colour is more attractive to T. tabaci than the other blue colours (Villeneuve, 1995). Three traps were used and the individual traps were spaced at least 5 m apart. The traps were placed 5-10 cm above the crop and their height was adjusted as the cabbages grew. The numbers of thrips caught were counted weekly, from the beginning of May until the end of September. Thrips damage was assessed on 6 and 24 August in 1998 and on 10 and 31 August in 1999 by lifting six white cabbages at random from each row and peeling off the leaves until symptoms of oedema were no longer visible. The number of thrips on each damaged leaf were counted. Thrips damage on the red cabbage was assessed on 24 August 1998 and on 31 August 1999.

Results and discussion

Figure 1 shows the flight activity of T. tabaci in 1998 and 1999. In both years, there was a clearly defined peak. Peak flight activity was recorded on 21 July in 1998 and on 3 August in 1999. The maximum number of T. tabaci caught/trap/week was 198 in 1998 and 412 in 1999. The period of mass-flight to the cabbage fields occurred in both years from begin July. Questions arose about the origin of these individuals. Thrips were reported to invade cabbage fields when cereals are harvested (Kahrer, 1994; Shelton, 1997). Shelton found that the numbers of T. tabaci which were caught in the traps above wheat or oat crops roughly correspond to the number of larvae which were produced on cabbage. On the other hand, the time of peak flight activity appears to depend on weather factors. However, data collected during only two seasons of monitoring are not sufficient to test any specific theory.

Table 1: Mean number (n=6) of Thrips tabaci on white cabbage.

1998 1999 Variety 6th August 24th August 10th August 31th August Adults Larvae Adults Larvae Adults Larvae Adults Larvae Perfecta 8.8 7.2 4.5 22.3 Touchma 46.3 9.3 21.5 30.1 Rivera 4.3 5.6 5.3 13.7 3.3 14.6 8.8 2.3 Robuston - 3.7 0.0 0.3 8.8 3.3 4.8 6.5 Marathon 2.3 0.7 4.7 0.7 6.1 7.4 19.3 15.6 Galaxy 1.3 2.0 0.3 1.7 2.3 - 3.5 1.3 Lennox 0.3 5.0 1.7 7.0 2.5 2.0 5.8 3.1 Bartolo 8.3 11.5 11.3 19.0 15.7 24.4 19.3 6.5 Bingo 3.7 5.3 3.7 5.3 7.8 13.3 25.5 14.8

Table 1 shows the number of trips collected by carefully removing each leaf at its base, noting the leaf number. High numbers (45/cabbage in 1998 and 51 in 1999) of live thrips were counted between the leaves of the early variety "Touchma". The thrips infestation level is shown figure 2 and 3. Thrips damage was found on practically all white cabbage heads. Furthermore, there were differences between the varieties in the number of infested leaves and the number of live thrips per plant. "Robuston", "Galaxy", "Lennox" and "Perfecta" were the least damaged varieties with 2-4 leaves damaged and "Touchma", "Rivera", "Bartolo" and "Bingo" the most damaged with 8-12 leaves damaged. Early-maturing varieties were damaged more than late-maturing types. By evaluating these commercial with cabbage varieties, it is possible to recommend to growers to minimise oedema and to identify highly susceptible varieties so that these can be avoided. No thrips or damaged leaves were found on the red cabbage varieties "Lectro" and "Reliant". Few thrips and 1 or 2 damaged leaves were found on the varieties "Rodima" and "Autoro".

200

175

150

125

100

50 Mean number thrips/trap/week

0 05/05 12/05 19/05 26/05 02/06 09/06 16/06 23/06 30/06 07/07 14/07 21/07 28/07 04/08 11/08 18/08 25/08 01/09 08/09 15/09 22/09 29/09 06/10 13/10 20/10 27/10

425 400 375 350 325 300 275 250 225 200 175 150 125 100

Mean number thrips/trap/week 75 50 25 0 04/05 11/05 18/05 25/05 01/06 08/06 15/06 22/06 29/06 06/07 13/07 20/07 27/07 03/08 10/08 17/08 24/08 31/08 07/09 14/09 21/09 28/09 05/10 12/10 19/10 26/10

Fig. 1: Numbers of T. tabaci collected from traps situated in a cabbage field in Kruishoutem in 1998 (above) and in 1999 (below).

13 6th August 12 24th August

(n=12) 11

1 Mean number infested leaves/plant 0

a n a a go ho m fect River Galaxy Bin uch obuston Lennox Bartolo Per o R Marat T

Fig. 2: Thrips damage to nine white cabbage varieties grown at Kruishoutem in 1998.

13 10th August 12 31th August

(n=12) 11

1 Mean number infested leaves/plant Mean number infested 0

x o a on on axy tol ct ivera l nno r e R Ga Bingo Le Ba Perf Robust Marath Touchma

Fig. 3: Thrips damage to nine white cabbage varieties grown at Kruishoutem in 1999.

Acknowledgements This rechearch is supported by the Ministry of Small Entreprises, Traders and Agriculture, Research and Development DG6. L. DE REYCKE, Provincial Vegetable Research Centre at Kruishoutem is thanked for his assistance with the experiments.

References

Ellis, P.R.; E. Kazantzidou; A. Kahrer; R. Hildenhargen & M. Hommes, 1994. Preliminary field studies of the resistance of cabbage to Thrips tabaci in three countries of Europe. IOBC/WPRS Bulletin 17 (8): 102-108. Kahrer, A., 1994. The flight activity of Thrips tabaci (Lind) in relation to cabbage and cereal crops. IOBC/WPRS Bulletin 17(8): 12-16. Shelton, A.M., 1997. Temporal and spatial dynamics of thrips populations in a diverse ecosystem: theory and management. J. Econ. Entomol.: 425-431. Shelton, A.M.; R.F. Becker & J.T. Andaloro, 1983. Varietal resistance to onion thrips (Thysanoptera: Thripidae) in processing cabbage. J. Econ. Ent. 76: 85-86. Shelton, A.M.; C.W. Hoy; R.C. North; M.H. Dickson & J. Bernard, 1988. Analysis of resistance in cabbage varieties to damage by Lepidoptera and Thysanoptera. J. Econ. Entomol. 81: 634-640. Shelton, A.M.; W.T. Wilsey & M.A. Schmaedich, 1998. Management of onion thrips (Thysanoptera: Thripidae) on cabbage by using plant resistance and insecticides. J. Econ. Entomol. 91: 329-333. Stoner, K.A.; M.H. Dickson & A.M. Shelton, 1989. Inheritance of resistance to damage by Thrips tabaci Lindeman (Thysanoptera: Thripidae) in cabbage. Euphytica 40: 233-239. Villeneuve, F., 1995. Piégeage chromatique de Thrips tabaci sur culture de poireau. Infos Ctifl 113: 29-33.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 39-45

Further development and use of simulations of within-field distributions of Brevicoryne brassicae to assist in sampling plan development

W.E. Parker1, J.N. Perry2, D. Niesten2, J.A. Blood Smyth3, R.G. McKinlay4 & S.A. Ellis5

1 ADAS, Woodthorne, Wolverhampton WV6 8TQ , U.K. 2 IACR Rothamsted, Harpenden, Herts., AL5 2JQ, U.K. 3 ADAS Arthur Rickwood, Mepal, Ely, Cambs., CB6 2BA, U.K. 4 SAC, West Mains Road, Edinburgh, EH9 3JG, U.K. 5 ADAS High Mowthorpe, Duggleby, Malton, N Yorks, YO17 8BP, U.K.

Abstract: Work done on quantifying the magnitude of an ‘edge effect’ in the within-field distribution of Brevicoryne brassicae, and its spatial and temporal variation around field boundaries, is summarised. Firm evidence for a consistent but variable edge effect, usually associated with plants on the extreme edge of the field was found. However, the incidence of infested edge plants around fields varied both spatially and temporally, and was not necessarily related to field margin type. Examples of how these data can be incorporated into simulations of B. brassicae infestations to help develop efficient sampling plans are also presented.

Key words: Brevicoryne brassicae, sampling, simulation, within-field distribution.

Introduction

Brevicoryne brassicae (mealy cabbage aphid) is the principal aphid pest of horticultural brassicas in the UK, and accounts for the majority of foliar insecticide usage on long-season crops such as Brussels sprouts. Despite the fact that aphid population levels vary considerably on individual crops and from year to year, many insecticide applications for B. brassicae control are frequently made on a calendar basis without reference to actual infestation levels. Thus there is a clear need for the development of more rational supervised control systems of insecticide use against B. brassicae based on field sampling. The key to the successful commercial adoption of supervised control systems (Theunissen, 1984; Theunissen & Den Ouden, 1985) is the development of a sampling system that accurately reflects the pest situation in the field with the minimum time input. A considerable amount of work has been done on supervised control of brassica pests, both on a pan-European level (Ellis et al., 1988) and specifically with reference to U.K. cropping conditions (Blood Smyth et al., 1992; Emmett, 1994; Paterson et al., 1994; Lynn & Mead, 1994). However, the sampling approaches developed in these projects have tended to be labour-intensive, making them unattractive to the industry. In addition, the validation of such sampling schemes requires extensive field work.

39 40

This paper summarises work done during 1998 as part of a project designed to develop (Parker et al. 1997, 1999; Perry et al., 1998) and test sampling schemes for B. brassicae that allow both for the variance-heterogeneity of counts and their spatial arrangement, and which can be validated without recourse to extensive field sampling. The 1998 work investigated the magnitude of ‘edge effects’ in B. brassicae distributions in the field, and quantified the variation in B. brassicae incidence along the edge of the crop over time relative to the level of infestation in the middle of the field. Examples of how simulations based on these and other data can be used to help evaluate sampling plans are also presented.

Materials and methods

Work was done in three commercial crops of Brussels sprouts (on each in Lancashire, Yorkshire and Lothian) and in a smaller (2 ha) untreated experimental area at ADAS Arthur Rickwood. Sampling was done in three distinct patterns at each site:

1. Within-field sample areas: four blocks of 50 plants in a 10 x 5 arrangement (200 plants in total per site). These were located in separate corners of the field approximately 15 m from the edge of the field. 2. Edge plants: edge plants were defined as those on the extreme edge of the field (i.e. the outermost plants in the field). A total of 200 plants were assessed, divided into 40 groups of five plants spaced regularly around the entire field boundary. 3. ‘Field boundary’ and ‘false headland’ transects: Field boundary transects consisted of 10 consecutive plants running into the field at 90o to the field edge. The first plant in the transect was an extreme edge (outermost) plant. 12 transects in total were used, again spaced evenly around the entire field boundary. Where a false headland (access track) was present in the field, a further 12 transects of 10 plants each were also used. The 10 plants in each of these ‘false headland’ transects were split into 5 consecutive plants running at 90o on either side of the access track.

Assessments of aphid infestation were made weekly at all sites for the first six weeks after the onset of aphid infestation, and thereafter continued fortnightly until harvest. Assessments primarily recorded the presence or absence of aphids, though some data on actual aphid numbers on plants were also obtained. Data analyses concentrated on evaluating and statistically defining the existence and magnitude of an edge effect in cabbage aphid distributions. Previous years’ work (and data from other sources, R. Collier, pers. comm) had suggested the existence of an edge effect on plants on the extreme edge of the field only.

Results

Comparison of infestation incidence between edge plants, transect plants and inner plants Data from the Lancashire site are presented (Table 1) to illustrate the results. At this site, the proportion of edge plants (i.e. those on outermost row of plants in the field) infested with aphids significantly exceeded the infestation incidence on other plants on seven out of 10 sampling occasions, and on one occasion it was significantly smaller. The results overall are consistent with the existence of a variable but definite edge effect. 41

Table 1. Comparisons between edge plants, transect plants and inner (within-field) plants at the Lancashire site (r.m.d. = residual mean deviance after fitting Generalized Linear Model with binomial errors and logit link function).

Date Average Average Average Average Regression analysis proportion proportion proportion proportion (edge versus inner versus transects) infested infested infested infested (edge) (transect) (inner) (overall) F d.f. P r.m.d. 20/07/98 0.0140 0.0000 0.0100 0.0109 3.91 2,56 0.0260 0.3454 30/07/98 0.0094 0.0083 0.0100 0.0092 0.03 2,56 0.9690 0.3665 11/08/98 0.0140 0.0083 0.0100 0.0125 0.31 2,56 0.7380 0.4359 19/08/98 0.0094 0.0083 0.0250 0.0102 3.20 2,56 0.0480 0.3265 08/09/98 0.0094 0.0000 0.0000 0.0068 8.11 2,56 <.001 0.2262 22/09/98 0.0800 0.0170 0.0100 0.0617 7.74 2,56 0.0010 1.0080 06/10/98 0.1440 0.0080 0.0150 0.1078 15.91 2,56 <.001 1.2100 20/10/98 0.1440 0.0420 0.0200 0.1149 10.13 2,56 <.001 1.2990 03/11/98 0.1408 0.0500 0.0250 0.1136 8.77 2,56 <.001 1.2150 17/11/98 0.1440 0.0330 0.0250 0.1215 9.64 2,56 <.001 1.3540

Relative incidence of infestation on ‘edge’ plants compared with plants further into the field On the basis of previous results, we expected that the average proportion of aphid- infested plants within the transects to decline with the distance from the edge, i.e. for logit regressions of proportion infested versus plant number in from the field edge to yield negative slopes. Results of these analyses from the site at ADAS Arthur Rickwood are given in Table 2.

Table 2. Decline of proportion of plants infested with aphids with distance from field edge at ADAS Arthur Rickwood.

Date Average Regression analysis proportion infested Estimate s.e. F df P r.m.d 04/06/98 0.6333 Intercept -0.9150 0.4240 15.83 1,8 <.001 0.7009 Slope 0.2811 0.0756 12/06/98 0.5417 Intercept 0.5630 0.4020 1.25 1,8 0.2640 0.9897 Slope -0.0716 0.0644 18/06/98 0.0250 Intercept -2.0900 1.0200 2.55 1,8 0.1100 0.6064 Slope -0.3770 0.2720 09/07/98 0.0167 Intercept -4.8400 1.8000 0.25 1,8 0.6170 0.7908 Slope 0.1260 0.2570 22/07/98 0.2833 Intercept 0.8860 0.4450 21.96 1,8 <0.01 0.8028 Slope -0.3722 0.0891

Excluding dates with low numbers of aphids and the period from 7 August 1998 to 23 October 1998 when the proportion of plants infested was high, there was one 42 significant positive regression and one significant negative regression. Variation amongst the five slopes (0.281, -0.072, -0.377, 0.126, -0.372) was considerable; the average was negative, being -0.083, with average s.e. of 0.152. This would predict that, for a threshold proportion of 10%, P = 0.1, that the proportion of edge plants infested would be exp(9*0.083)/(1+(0.1exp(9*0.083))) or 2.11 times the proportion of plants infested 10 plants in from the edge, effectively in the inner part of the field. This value, of approximately a two-fold increase at the edge, is completely consistent with values obtained during the previous two years of this project. Again, the overall conclusion, given the previous years’ results, is one of a variable, but definite, edge effect.

The variability between different groups of edge plants There were 40 groups of edge plants around each field, each yielding a single observed proportion of 5 sampled plants infested. These 40 were classified into four roughly equal groups, each group representing a single edge of the rectangular field. These groups were analysed to seek differences between the groups. The analysis was repeated with a different classification, into the four ‘corners’ of the field. Differences between the means of these three groups were estimated by fitting a generalized linear model with binomial errors and logit link, and differences between the three groups tested with F-tests. Results for the Yorkshire site are given in Table 3. When infestations were around 5%, on all four occasions there were differences between the four edge groups, and on two occasions there were differences between the corners. Also, the ranking of the four edges in the proportion of plants infested changed between occasions. Denoting the highest infestation incidence as 1 and the smallest as 4, the east, south, west and north edges were ranked: 4,2,3,1 on 27 August; 2,1,4,2 on 10 September; 2,1,4,3 on 24 September and 4,4,2,1 on 8 October.

Table 3. Comparison of infestation incidence between different groups of edge plants and between different corners at the Yorkshire site.

Date Average proportion Grouping Regression analysis infested (entire edge) F df P r.m.d 27/08/98 0.0600 edge 7.85 3,36 <0.001 0.681 corner 5.41 3,36 0.004 0.777 10/09/98 0.0550 edge 5.56 3,36 0.003 0.730 corner 0.70 3,36 0.558 1.009 24/09/98 0.0500 edge 5.88 3,36 0.002 0.609 corner 0.88 3,36 0.460 0.845 08/10/98 0.0600 edge 10.92 3,36 <0.001 0.811 corner 5.44 3,36 0.003 1.066

Incorporation of ‘edge effects’ into simulations Based on the extensive field data collection and analysis done during 1996, 1997 and 1998 (e.g. Parker et al., 1999, Perry et al., 1999), computer programs for generating definitive simulations (e.g. Figure 1), incorporating edge effects, were written. Three different simulations at each of 18 infestation levels (incidence of aphid infestation set at 1%, 2%, 2.5%, 3%, 4%, 5%, 6%, 7.5%, 8%, 9%, 10%, 12.5%, 15%, 17.5%, 20%, 43

25%, 30%, 35%, 40%) were generated. These were used to assess the errors associated with identifying a pre-defined aphid infestation level using different ‘plant’ sample sizes taken either from the whole ‘field’ or from the extreme edges of the ‘field’ only. By doing this, a definitive judgement on the accuracy of using different sample sizes to identify different infestation levels can be derived. No attempt was made to alter the pattern of sampling, beyond constraining sampling to the ‘whole field’ or the edge ‘plants’ only, as the data analysis had shown conclusively that B. brassicae distribution in the field at low densities was essentially random.

Fig. 1. Simulated distribution of cabbage aphid in an artificial field of 8000 plants incorporating a predicted edge effect. Darker squares represent plants infested plants. Black squares = highly infested plants.

As an example of the type of information that can be extracted from this large data set, plots of sampling ‘variance’ using different sample sizes at different infestation levels using an ‘edge only’ approach to sampling is given in Figure 2. This shows that overall variability sharply decreases for all sample sizes at higher infestation levels. This is because in a field with, for example, a 40% overall aphid incidence, the incidence on the ‘edge’ plants is actually nearer 80%, and therefore the chances of repeatedly finding aphid-infested plants with a small sample are also high, thus reducing the sample variance.

Discussion

There were significant differences between parts of the field in the proportion of edge plants infested on about half the occasions sampled. Furthermore, the edge of the field with the greatest incidence of aphids did not remain the same, but changed unpredictably from occasion to occasion. This is an important finding as it indicates that the reasons for differences in infestation between edges cannot relate to 44 unvarying physical factors only, like the presence of hedges or drains. Changes in edge infestation must also be related to abiotic factors that vary over time such as wind speed and direction, or biotic factors such as the presence of natural enemies. The precise determination of such relationships would require a great deal of data, and is beyond the scope of this study. These results confirm the finding by in other work (R Collier & A Mead, pers. comm) that the edge effect is spatially heterogeneous, and further imply that it is temporally unpredictable. Overall, the results confirm that the incidence of aphids, measured by the proportion of plants infested, is on average about two times greater on extreme edge plants compared with those further into the field.

800

5 plants 700 10 plants 20 plants 600 30 plants 50 plants

500 100 plants

400

300 'Sampling Variance' 'Sampling 200

100

0 1 2 2.5 3 4 5 6 7.5 8 9 10 12.5 15 17.5 20 25 30 35 40 Infestation Level (% plants infested)

Fig. 2. Change in the variance of the estimated percentage plants infested with sample size and infestation level, based on random ‘field edge only’ samples from simulated B. brassicae distributions.

The simulation work suggests that a sampling strategy based on assessing a relatively low number (<50) of edge plants only might give acceptable results, although more than one edge would have to be included in the sampling process. Work is in hand to test such systems in the field. These clearly need to be integrated with similar work on within-field brassica caterpillar distribution and sampling plan development (Collier & Mead, 1999).

References

Blood-Smyth, J.A., Davies, J.S., Emmett, B.J., Lole, M., Paterson, C. & Powell, V. (1992) Supervised control of aphid and caterpillar crops in brassica crops. IOBC wprs Bulletin 15 (4): 9-15. Collier, R.H. & Mead, A. (1999). Simulating sampling strategies for aphid and caterpillar pests of brassica crops. IOBC wprs Bulletin 22 (5): 1-7. 45

Ellis, P.R., Hardman, J.A., Hommes, M., Dunne, R., Fischer, S., Freuler, J., Kahrer, A. & Terretaz, C. (1988) An evaluation of supervised systems for applying insecticide treatments to control aphid and foliage caterpillar pests of cabbage. Proceedings Brighton Crop Protection Conference - Pests & Diseases 1: 269-274. Emmett, B.J. (1994) Integrated pest management of insect pests in brassica crops (“supervised” control). Report to Horticultural Development Council on project FV119. HDC, East Malling, Kent, U.K. Lynn, J. & Mead, A. (1994) Use of the Wald sequential probability ratio test in supervised pest control. Aspects of Applied Biology (Sampling to Make Decisions) 37: 15-24. Parker W.E., Turner, S.T.D., Perry, J.N., Blood Smyth, J.A., Ellis, S.A. & McKinlay, R.G. (1997). Developing a GIS-based tool for testing field sampling plans by modelling the within-field distribution of Brevicoryne brassicae in Brussels sprouts. Proceedings of the 1st European Conference on Precision Agriculture 2: 811-819. Parker, W.E., Perry, J.N., Blood Smyth, J., Ellis, S.A., McKinlay, R.G. & Turner, S.T.D. (1999). A new approach to characterising within-field pest distributions using mealy cabbage aphid (Brevicoryne brassicae) on Brussels sprouts as an example. IOBC wprs Bulletin 22 (5): 9-13. Paterson, C.D., Mead, A., Blood Smyth, J.A., Davies, J.S. & Runham, S.R. (1994) Using a sequential sampling method for supervised control of pests in Brussels sprouts and calabrese. Aspects of Applied Biology (Sampling to Make Decisions) 37: 73-82. Perry, J.N., Parker, W.E., Alderson, L., Korie, S., Blood Smyth, J.A., McKinlay, R. & Ellis, S.A. (1998). Simulation of 16,000 counts of aphids over two hectares of Brussels sprout plants. Computers and Electronics in Agriculture 21: 33-51. Theunissen, J. & Den Ouden, H. (1985) Tolerance levels for supervised control of insect pests in Brussels sprouts and white cabbage. Zeitschrift für angewandte Entomologie 100: 84-87. Theunissen, J. (1984) Supervised pest control in cabbage crops: theory and practice. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft 218: 76-84. 46

Integrated Pest Management

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 47-55

The exploitation of plant resistance in controlling insect pests of vegetable crops

P.R. Ellis, N.B. Kift Horticulture Research International, Wellesbourne, Warwick, CV35 9EF, UK

Abstract: Insect-resistant varieties are a valuable component of integrated control programmes for pests of many crops. Their advantages over insecticides outweigh their disadvantages particularly in terms of environmental issues. At Horticulture Research International, Wellesbourne, numerous sources of partial resistance to important pests have been identified in gene bank collections of vegetable varieties and breeding lines. Higher levels of resistance have been identified in wild species of plants. However, great difficulty has been experienced in exploiting resistance of wild species. For example, using conventional breeding methods it has taken up to 15 years to transfer resistance to Psila rosae from wild Daucus species to commercial varieties of carrot. In the future, this process will be shortened by using biotechnological techniques such as genetic transformation of plant material. Complications exist in breeding varieties of vegetable crops, which can meet all consumer needs for quality characteristics, as well as possessing resistance to pests. Difficulties also exist in the integration of resistant varieties with other components of integrated pest management (IPM) partly because the resistance usually acts only against a single pest in a situation where many pests occur. Sources of resistance in brassicas, carrot and lettuce crops are referred to in this paper. Examples are given where resistant varieties can provide the principal control measure for a particular pest and examples of ways in which partial resistance can contribute to integrated control programmes in vegetable crops. It is concluded that, in the future, resistant varieties of crops will play an increasing role in reducing growers’ dependence on insecticides and thus contribute significantly to sustainable crop production systems.

Key words: Host plant resistance, resistant varieties, integrated pest management, brassicas, carrots, lettuce

Introduction

Members of the International Organisation for Biological Control (IOBC)Working Group on ‘Integrated Control in Field Vegetable Crops’ are serving an industry which is growing high value crops and which, in many cases, demands blemish-free produce. Supermarkets will reject iceberg lettuce crops which have aphids on their leaves and reject carrots which are damaged by carrot fly or infested with the maggots of this pest. These demands for completely clean crops are hard to achieve in crop protection programmes. In addition, production of crops is often highly intensive with repeated cropping of fields, in some cases with varieties of crops that are known to be susceptible to pests. This intensive cultivation of host crops favours insect survival and reproduction and so large populations develop rapidly. It is not surprising that growers treat their crops with insecticides repeatedly which leads to pests becoming resistant to these chemicals. The IOBC considers host plant resistance to be an important and desirable component of integrated control management of pests of vegetable crops. Hence the organisation’s continued support for the Working Group on ‘Breeding for Resistance to Insects and Mites’ founded in December 1976.

47 48

There are several reasons why resistant varieties are so valuable in integrated control programmes, particularly when growers are attempting to reduce pesticide inputs and move towards sustainable pest control methods in vegetable crops. Resistant varieties are cheap and straightforward to use, they have minimal effects on the environment, greatly reducing the pesticide residues left in the soil, crop, water courses or in the atmosphere. Resistant varieties offer season-long protection and provide all farmers, but especially growers of low-value crops and organic farmers, a satisfactory method of pest control. Resistant varieties are compatible with most other components of integrated pest management. There are excellent examples of where resistant varieties have been shown to complement the use of insecticides, in many cases leading to a reduction in the dose or in the number of applications of the chemical (Ellis, 1999). In this report, details of sources of resistance which exist in brassicas, carrots and lettuce will be reviewed and examples given of how this resistance can be exploited in integrated programmes of vegetable pest control.

Sources of resistance

The basis of all host plant resistance projects is a study of variation within plant species in relation to pest infestation. Two important resources in which to search for variation are firstly, collections of crop varieties and land races, and secondly, wild species of plants. Gene banks, such as that at HRI Wellesbourne, store several thousand accessions of vegetable crops. It is necessary to limit the number of accessions evaluated to a manageable level so that a representative collection is screened, e.g. the collection of material used in a EC-funded project to evaluate brassica genetic resources for pest and disease resistance (Leckie et al., 1996). Staff at the HRI Gene Bank collaborated with colleagues in The Netherlands and Portugal to create a core collection of brassicas (Table 1). The 400 accessions made available for screening against Brevicoryne brassicae (L.) included representatives of the genetic and geographic variation known to exist within the Brassica oleracea genome. All the widely- grown brassica crops were represented in this collection and they were evaluated in the glasshouse and field (Ellis et al., 1998). The identification of resistance requires simple, quick and reliable techniques for evaluating pest performance and plant responses to attack. Field, glasshouse and laboratory techniques are used in this work (Ellis et al., 1999b). As a general rule, commercial varieties of the crop of interest are screened first, followed by breeding lines, land races and then wild relatives. The main reason for proceeding in this order is that there is an increasing difficulty in selecting and crossing accessions the further they are removed from the commercially-acceptable crop variety (Flanders et al., 1992). Thus, breeding with wild species of plants can be slow, particularly if there are genetic barriers to securing crosses between species possessing different numbers of chromosomes. The situation has improved in recent years with advances in biotechnology, including transformation techniques, which permit the rapid transfer of genes from one species to another. Experience suggests that the likelihood of finding high levels of resistance increases as the plant accession is further removed from the crop variety. For example, results at HRI Wellesbourne in which vegetable crop accessions and wild species have been evaluated against three important pests illustrate this phenomenon (Table 2).

Table 1. The content of the Brassica oleracea project core collection used in the evaluation of European genebank resources for pest and disease resistance

Brassica European Common name No. accessions Database grouping

acephala kale 71 alboglabra chinese kale 10 botrytis cauliflower 67 italica broccoli 46 capitata cabbage 100 gemmifera Brussels sprouts 45 gongylodes kohl rabi 19 tronchuda Portuguese cabbage 41 undefined 4 wild relatives 7

Total 410

Table 2. Evaluation of vegetable crops for resistance to pests at HRI Wellesbourne

No. of Sources of resistance (%) Crop or species Pest accessions Partial High tested

Brassica oleracea var. capitata Delia 50 4 0 Brassica oleracea var. botrytis radicum 200 1 0 Raphanus sativus 200 0 0 Wild Brassica 9 85 78 Brassica oleracea var. capitata Brevicoryne 100 2 0 Brassica oleracea var. botrytis brassicae 100 2 0 Brassica oleracea var. acephala 50 8 0 Wild Brassica 23 43 17 Daucus carota Psila rosae 400 4 0 Wild Daucus 16 80 50

The variable pest

Variation exists within the pest as well as the plant. The occurrence of insecticide-resistant biotypes of pests is a good example of this. The recent identification of biotypes of Nasonovia ribisnigri (Mosley), resistant to the carbamate insecticide, pirimicarb, and the pyrethroid, cypermethrin (Barber et al., 1999) is a good example. Similarly, biotypes may develop which can multiply on resistant crop varieties. It is therefore important to evaluate any promising sources of resistance against a range of populations of the target pest and determine the virulence for different genotypes within a population (Caillaud et al., 1995). As part of the 50

project on Psila rosae (F.), the carrot fly, at HRI Wellesbourne, carrot varieties possessing different levels of resistance have been identified. Eight varieties, representing the range of resistance to P. rosae, were evaluated in 10 countries over two years to investigate the existence of biotypes (Ellis & Hardman, 1981). Resistance was confirmed in the different locations and there was no evidence of the existence of biotypes. Therefore, the decision was made at HRI to commence a breeding programme to exploit the resistance. In more recent studies at HRI Wellesbourne, resistance in the lettuce variety ‘Iceberg’ to Myzus persicae (Sulzer) has been screened against five different clones of the aphid collected from different parts of the UK. This pest is known to have developed different biotypes in relation to insecticides and therefore may be expected to adapt to sources of plant resistance.

Table 3. Sources and availability of resistance to aphid pests in lettuce

Commercial Insect Source of resistance varieties * Common Latin name Plant Basis Genetics Level name 'Charan''M 'Charan,' Antibiosis Polygenic Partial Macrosiphum Potato arbello' 'Marbello' euphorbiae Aphid ? ? ? Total None Peach- Myzus Not potato 'Iceberg' Polygenic Partial 'Iceberg' persicae Known aphid Single Nasonovia Lettuce Lactuca 'Fortunas' Antibiosis dominant Total ribisnigri aphid virosa 'Vetonas' gene Nr Lactuca 'Avoncrisp' Single serriola 'Avondefiance' Antibiosis dominant Total prickly 'Beatrice' gene Lra Pemphigus Lettuce lettuce 'Robinson' bursarius root aphid Single 'Adriatica' Antibiosis dominant Total 'Adriatica' gene

* 'Dynamite' is a butterhead variety which posseses a high level of resistance to Nasonovia ribisnigri and Pemphigus bursarius and also moderate resistance to Macrosiphum euphorbiae. ? A source of resistance identified by Dutch seed companies.

Exploiting host plant resistance to vegetable pests

Resistant varieties as a principal component of sustainable crop protection A range of lettuce varieties resistant to Pemphigus bursarius (L.), the lettuce root aphid, are now available following work done at HRI Wellesbourne and by seed companies (Table 3). The resistance provides total protection against the pest and therefore no further control

measures are required (Ellis, Pink & Ramsey, 1994). However, the resistance is based on a single dominant gene and therefore aphid biotypes may develop which can overcome the resistance. Since releasing the original material to the seed companies, another quite different gene has been found in the Bulgarian lettuce variety ‘Adriatica 2’ which will soon be released to seed companies (Ellis et al., 2000). The relevance of different strategies that maximise the effective life of any sources of resistance depends on the characteristics of the pest as well as the selection pressure exerted by different forms of resistance. In all cases, successful deployment of host-plant resistance is only possible with a detailed knowledge of the insect/plant relationships pertaining to a particular cropping situation. A wise strategy would be for growers to alternate the different sources of resistance and avoid growing one variety each year. Alternative methods, such as the use of insecticide seed treatments or the limited use of accurately-timed sprays of insecticides, may also have to be employed.

Resistant varieties as a supplementary component of sustainable crop protection At present, the carrot industry in the UK only has available varieties which possess partial resistance to P. rosae. However, the major difficulty in the economic control of this pest is the need to supply blemish-free produce. Unfortunately, P. rosae attacks the portion of the plant that is marketed, the root, and the complete protection of the roots is difficult to achieve with any method. At HRI Wellesbourne, it has been demonstrated that partial resistance to P. rosae can be integrated with other control measures to produce marketable crops. Two examples of this research work are summarised below:-

Partial resistance and careful choice of cropping schedules Psila rosae has two main generations each year which can be forecast (Finch, Freuler & Collier, 1999). It is well known that, by careful choice of sowing and harvest dates, growers can avoid much of the damage done by this pest. In two seasons at two sites in the UK (Wellesbourne, Warwickshire and Mepal, Cambridegshire), it has been shown that partial resistance can complement cropping schedules (Ellis et al., 1987). Partial resistance in the carrot variety ‘Sytan’ reduces levels of attack by 50% and, because larval development is slowed down on this variety, the crop will remain free of damage for about two weeks longer than on a susceptible carrot variety such as ‘Danvers’ (Ellis, Freeman & Hardman, 1984). In field experiments, seed of the two contrasting carrot varieties was drilled on five occasions in the spring and roots harvested on seven occasions in the autumn and winter (Ellis et al., 1987). The partially-resistant ‘Sytan’ was less damaged and supported fewer insects than the susceptible ‘Danvers’ on all lifting dates. Nine combinations of sowing and harvest dates provided more than 75% marketable roots of ‘Sytan’ while only three combinations of dates provided as many marketable roots of the susceptible variety. Sowing carrots in early June avoided the first generation of P. rosae, resulting in more than 90% of ‘Sytan’ roots being marketable in December. The benefits of the choice of specific sowing and harvest dates to avoid attack were confirmed when the numbers of pupae remaining in the soil after cropping were counted (Ellis et al., 1987). A combination of partial resistance and specific sowing and harvest schedules greatly reduced the number of pupae left behind on both varieties but the effect was particularly great with ‘Sytan’. The results of the experiments indicated that cropping between the two generations of P. rosae attack, and using partially-resistant carrot varieties, enables carrots to be grown without insecticides which is one of the important objectives in sustainable crop production.

Host plant resistance and reduced doses of insecticides It has been shown that the partially-resistant carrot variety ‘Sytan’ can reduce insecticide inputs by two thirds of the normal dose (Thompson, Phelps & Ellis, 1994). The two contrasting varieties ‘Sytan’ and the susceptible ‘Danvers’ were grown at two sites (Wellesbourne, Warwickshire and Mepal, Cambridgeshire), UK, in two seasons and were treated with a series of different doses of insecticide. Approximately 90mg of the insecticide were required to achieve marketable crops of the susceptible carrot ‘Danvers’ whilst on the partially-resistant ‘Sytan’ only 30mg were required. The recommended dose of chlorfenvinphos was 60mg. Thus, more insecticide would be required to protect a ‘Danvers’ crop. In a recent study in The Netherlands, lettuce varieties, both resistant and susceptible to Nasonovia ribisnigri, were grown in the field and treated with insecticides to control aphid infestations. The results of two seasons experiments at two sites showed that only one or two applications of insecticides were required to protect resistant crisphead varieties leading to a 60-90% reduction in the amount of insecticide used (Aarts et al., 1999).

Difficulties in the use of resistant varieties

Three main difficulties are often quoted:-

1. It takes a very long time to breed resistant varieties using conventional techniques. For example, in breeding carrots resistant to P. rosae, we have identified numerous sources of partial resistance in cultivated carrot and much higher levels of resistance in wild Daucus species (Table 4). Selection for higher levels of resistance in hybrids, resulting from the cross between Daucus capillifolius and Daucus carota, was done for 15 years before carrots with a reasonable appearance and moderate resistance were produced (Ellis et al., 1993). Selection within the cultivated carrot has concentrated on the partially-resistant variety ‘Sytan’. It has taken seed companies 10 years, using HRI breeding lines, to increase levels of resistance by 25% (Ellis et al., 1997). To speed up breeding programmes, we can use a number of different techniques. The identification and use of molecular markers for resistance to pests can make selection and breeding of new varieties a much more accurate and reliable process. The use of transgenic plants will help exploit genes for resistance which exist in wild relatives of crop plants. Thus, it should, in the future, be possible to use the genes from wild carrot species, such as Daucus broteri, which is completely resistant to carrot fly (Hardman, Ellis & Saw, 1990). 2. There is commonly a yield or quality penalty in producing a new resistant variety. Thus the lettuce variety ‘Avoncrisp’, bred at HRI Wellesbourne, which was made available to the growers over 25 years ago, has not been grown widely because its texture and shape does not conform to the crisp lettuce type demanded by the markets. It has taken seed companies over 20 years to achieve the breeding of crisp varieties which possess the resistance of ‘Avoncrisp’ plus the quality characteristics required for market-leading lettuce varieties. 3. Resistant varieties are usually effective against a single pest. Yet, for many of our crops, there are several important pests to be controlled. For example, four different species of aphid are major pests of lettuce in western Europe (Reinink & Dieleman, 1993) and yet we only have high levels of resistance to three of them in commercially-acceptable varieties (Table 3). In these cases, an integrated approach to sustainable crop production is required where several different control measures are integrated. In a recent project at HRI Wellesbourne, several different components of an integrated programme for controlling 53

aphids on lettuce were investigated (Tatchell, et al., 1998). As well as evaluating new resistant breeding lines, the project investigated the use of semio-chemicals to interrupt aphid behaviour, the use of entomopathogenic fungi to control P. bursarius, the performance of novel insecticides and the forecasting of aphid activity in the crop. Different control measures were targeted at key stages in aphid cycles using the forecasts. In this way it is possible to reduce insecticide inputs to a minimum. High levels of resistance have now been found in lettuce to Macrosiphum euphorbiae (Thomas), and, at HRI Wellesbourne, the resistance in lettuce to M. persicae is being studied (Table 3). The main objective of this research is to combine sources of resistance to all four major aphid pests of lettuce in a range of adapted commercially-acceptable varieties.

Table 4. Relative levels of resistance in carrot varieties and wild species to carrot fly, Psila rosae at HRI Wellesbourne

100% Daucus broteri 99% Daucus littoralis 98% Daucus capillifolius 75% 1998 Hybrids 60% 1995 Hybrids 55% ‘Sytan selection’, Daucus carota X Daucus capillifolius F6 50% ‘Sytan’, ‘Carentan’, ‘Fly Away’, ‘Maestro’, ‘Nandor’, ‘Touchon’, ‘Parano’, ‘Primo’ 35% ‘Danvers’ Half Long 126 2% Daucus carota, wild carrot

A similar situation occurs in brassicas, where the crop is attacked by several important pests. At HRI Wellesbourne, we have identified partial resistance in different cultivated brassicas to aphids (B. brassicae), caterpillars (Evergestis forficalis (L.), Mamestra brassicae (L.), Pieris brassicae (L.), root flies (Delia radicum (L.) and whiteflies (Aleyrodes proletella (L.), but no single plant or variety is resistant to all pests. Much higher levels of resistance exist in certain wild brassica species (Singh et al., 1994; Ellis et al., 1999a; 1999b). Brassica fruticulosa is highly resistant to B. brassicae, D. radicum and A. proletella. However, this wild Brassica species is in a different genome to horticultural brassicas (Brassica oleracea), and it is not possible to cross this wild species with B. oleracea using conventional plant breeding methods. More recently four other Brassica species, which are in the same group as Brassica oleracea and genetically compatible, were identified as being highly resistant to B. brassicae, D. radicum and A. proletella (Ellis et al., 1999a). Partial plant resistance is not an answer in itself. However, depending on the effects of partial plant resistance on the pest, it may be complimentary to the use of natural enemies, particularly where the effect of the resistance is to extend the life cycle of the pest (Kindlmann & Dixon, 1999). 54

Conclusions

At HRI Wellesbourne, the experience of 30 years of research into host plant resistance suggests that sources of resistance are not difficult to identify, although the highest levels of resistance would appear to be located in wild relatives of crop plants. Exploiting this resistance takes a long time but, with the advent of new biotechnology aimed at transferring genes from one species to another, the time taken to exploit resistance will be considerably reduced. As more and more sources of resistance are found, it should be possible to breed new varieties possessing resistance to a range of pests. Seed companies have identified host plant resistance to pests as a major objective in breeding new vegetable varieties, and the increased effort in this work will ensure that any new resistant variety conforms with all the market requirements demanded by the consumer. In conclusion, the future is bright for this method of crop protection. We believe that resistant varieties will play an ever-increasing role in integrated control in field vegetables and thus contribute significantly towards sustainable horticultural crop production.

References

Aarts, R., Schut, J.W., Driessen, R. & Reinink, K. 1999. Integrated control of aphids on lettuce varieties resistant to Nasonovia ribisnigri. Barber, M.D., Moores, G.D., Denholm, I., Tatchell, G.M. & Vice, W.E. 1999. Confirmation of insecticide resistance in UK populations of the currant-lettuce aphid, Nasonovia ribisnigri. Bull. Ent. Res. 89: 17-23. Caillaud, C.M., Dedryver, C.A., DiPietro, J.P., Simon, J.C., Fima, F. & Chaubet, B. 1995. Clonal variability in the response of Sitobian avenae (Homoptera: Aphididae) to resistant and susceptible wheat. Bull. Ent. Res. 85: 189-195. Ellis, P.R. 1999. The identification and exploitation of resistance in carrots and wild Umbelliferae to the carrot fly, Psila rosae (F.). Integrated Pest Management Reviews 4: 256-268. Ellis, P.R., Crowther, T.C., Welch, M.C., Vice, W.E. & Hardman, J.A. 1997. Evaluation of carrot varieties and seed company lines for resistance to carrot fly (Psila rosae (Fab.)) at Wellesbourne 1991-96. Tests of Agrochemicals and Cultivars No. 18, (Ann. Appl. Biol. 130 Supplement): 30-31. Ellis, P.R., Freeman, G.H. & Hardman, J.A. 1984. Differences in the relative resistance of two carrot cultivars to carrot fly attack over five seasons. Ann. Appl. Biol. 105: 557-564. Ellis, P.R. & Hardman, J.A. 1981. The consistency of the resistance of eight carrot cultivars to carrot fly attack at several centres in Europe. Ann. Appl. Biol. 98: 491-497. Ellis, P.R., Hardman, J.A., Cole, R.A. & Phelps, K. 1987. The complementary effects of plant resistance and the choice of sowing and harvest times in reducing carrot fly (Psila rosae) damage to carrots. Ann. Appl. Biol. 111: 415-424. Ellis, P.R., Hardman, J.A., Crowther, T.C. & Saw, P.L. 1993. Exploitation of the resistance to carrot fly in the wild carrot species Daucus capillifolius. Ann. Appl. Biol., 122: 72-91. Ellis, P.R., Kift, N.B., Pink, D.A.C., Jukes, P.L., Lynn, J. & Tatchell, G.M. 1999a. Variation in resistance to the cabbage aphid (Brevicoryne brassicae) between and within wild Brassica species. Genetic Resources and Crop Evolution (in press). Ellis, P.R., Pink, D.A.C., Barber, N.E., & Mead, A. 1999b. Identification of high levels of resistance to cabbage root fly, Delia radicum, in wild Brassica species. Euphytica 110: 207-214. 55

Ellis, P.R., Pink, D.A.C., McClement, S.J., Saw, P.L., Phelps, K., Vice, W.E. & Kift, N.B. 2000. Identification of sources of resistance in lettuce to the lettuce root aphid, Pemphigus bursarius. Euphytica (in prep.) Ellis, P.R., Pink, D.A.C., Phelps, K., Jukes, P.L., Breeds, S.E. & Pinnegar, A.E. 1998. Evaluation of a core collection of Brassica oleracea for resistance to Brevicoryne brassicae, the cabbage aphid. Euphytica 103: 149-160. Ellis, P.R., Pink, D.A.C. & Ramsey, A.D. 1994. Inheritance of resistance to lettuce root aphid in the lettuce cultivars ‘Avoncrisp’ and ‘Lakeland’. Ann. Appl. Biol. 124: 141-151. Finch, S., Freuler, J. & Collier, R.H. 1999. Monitoring Populations of the Carrot Fly, Psila rosae. VIII + 108 pp., Dijon, IOBC WPRS. Flanders, K.L., Hawkes, J.G., Radcliffe, E.B. & Lauer, F.I. 1992. Insect resistance in potatoes: sources, evolutionary relationships, morphological and chemical defences and ecogeographical associations. Euphytica 61: 83-111. Hardman, J.A., Ellis. P.R. & Saw, P.L. 1990. Further investigations of the host range of the carrot fly, Psila rosae (F.). Ann. Appl. Biol. 117: 495-506. Kindlmann, P & Dixon, A.F.G. 1999. Generation time ratios – Determinants of prey abundance in insect predator-prey interactions. Biological Control 16: 133-138. Leckie, D., Astley, D., Crute, I.R., Ellis, P.R., & Pink, D.A.C., Boukema, I., Monteiro, A.A., & Dias, J.S. 1996. The location and exploitation of genes for pest and disease resistance in European gene bank collections of horticultural brassicas. Acta Horticulturae 407: 95- 101. Reinink, K. & Dieleman, F.L. 1993. Survey of aphid species on lettuce. IOBC WPRS Bulletin 16 (5): 56-68. Singh, R., Ellis, P.R., Pink, D.A.C. & Phelps, K. 1994. An investigation of the resistance to cabbage aphid in brassica species. Annals of Applied Biology 125: 457-465. Tatchell, G.M., Ellis, P.R., Collier, R.H., Chandler, D., Mead, A., Wadhams, L.J., Parker, W. E., Blood-Smyth, J. & Vice, W.E. 1998. Integrated pest management of aphids on outdoor lettuce crops. Final Report on HDC Project FV162: 77 pp. Thompson, A.R., Phelps, K. & Ellis, P.R. 1994. Additive effects of soil-applied insecticides and partial host-plant resistance against carrot fly (Psila rosae) on carrots. Brighton Crop Protection Conference – Pests and Diseases: 749-754. 56

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 57-60

New ways of manipulating field populations of the carrot fly

R. Collier1, S. Finch1 and J. Davies2 1 Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK 2 Horticulture Research International, Stockbridge House, Cawood, Selby, North Yorkshire YO8 3TZ, UK

Abstract: Crop covers and isolated plots were used to obtain further detailed information on the biology and behaviour of the carrot fly (Psila rosae). Crop covers were applied to beds of carrots immediately after drilling to keep off the natural infestation of flies. Various covers were then removed at two-week intervals from mid July onwards, to identify the most damaging period of attack by the second generation of carrot fly. Severe crop damage occurred when the covers were removed during late July and early August, at the start of the second fly generation. In contrast, carrots, exposed to attack after mid September, suffered little damage, even though high numbers of flies were captured on sticky traps. The results showed clearly that only the offspring of flies that were in the field before the end of September damaged the crop during the winter. Small plots of carrots were drilled about 100m apart at distances of from 130-1300 m away from a highly infested field of carrots, to estimate how far flies disperse in the spring to find a new crop. The numbers of flies caught in the small plots declined markedly with increasing distance from the site of emergence. There were also consistent relationships between the fall-off in the numbers of flies, eggs, pupae and crop damage with increasing distance from the overwintering site. Estimates from this dispersal study, and from studies of fly distribution in commercial carrot crops, indicated that carrot flies appear to disperse about 50-100m/day both within crops and when trying to find new crops. If such estimates can be confirmed, they should help in future to decide where to site new crops to ensure that fly infestations remain low.

Key words: Psila rosae, crop covers, crop isolation, insect dispersal, overwintering crop damage

Introduction

The carrot fly (Psila rosae) is a serious pest of umbelliferous crops, particularly carrots. In the UK, crops may be attacked by up to three generations of the fly each year (Coppock, 1974). Although the biology and behaviour of the carrot fly have been studied for many years (Dufault & Coaker, 1987), there are still some biological questions that, if answered, would enable growers to reduce insecticide use and still maintain good carrot fly control. Experiments were done at HRI Stockbridge House and HRI Wellesbourne, using crop covers and isolated plots, to address some of these questions.

Experimental

Crop covers These were used to determine when the last spray should be applied to control carrot flies of the second and third generations. Carrots were sown on 16 May 1995 at HRI Stockbridge House. Each plot was 5 m x 1.8 m wide and adjacent plots were separated by a 1.8m width of bare soil to prevent the carrot fly larvae moving between plots. There were eight replicates of each treatment arranged in a double contiguous-replicate, 3 x 4 rectangular lattice. A granular insecticide (chlorfenvinphos) was applied to the whole experiment at sowing to control larvae of the first generation of carrot fly. Plots were then covered with fleece (Agryl

57 58

P17), which was secured along the edges with soil. The treatments consisted of a series of sequential uncovering dates. Selected plots were uncovered, at two-week intervals, from 19 July, just before the start of the second generation of carrot fly, until 8 November. There were three control treatments: 1) plots covered from sowing to harvest, 2) plots left uncovered, and 3) plots left uncovered but with foliar sprays of insecticide (chlorfenvinphos) applied on 27 July and 6 September. The timing of adult carrot fly activity was monitored using three orange sticky traps (RebellR) placed in an area of carrots approximately 100 m away from the plots. A sample of 200-250 roots/plot was taken from each plot on 30 November 1995 and 22 March 1996. The roots were washed and assessed for carrot fly damage. The results are summarised in Figure 1. A total of 1901 flies was captured between 4 July and 28 November 1995. Relatively high numbers of flies were captured until early November. The plots uncovered during July and August were the most heavily damaged. Less carrot fly damage occurred in plots uncovered after the end of August, and the percentage of damaged carrots in plots uncovered from 13 September onwards did not differ from that in the control plots, which had been covered permanently from drilling to harvest.

Isolated plots This experiment was done to estimate the distance that carrot flies disperse from their overwintering site. To do this, eleven small plots of carrots were drilled at HRI Wellesbourne in 1998 at distances of 130 to 1300m away from a field that contained a large population of overwintering flies. Each plot was drilled with three 10m long beds of carrots in March and the first generation of flies was monitored in May/early-June. Insect numbers were monitored using three sticky traps/plot/week, sampling eggs from three 20cm lengths of carrot row/week and by taking nine 10cm-diameter soil cores on 7 July, after the end of the fly generation. During the first generation in 1998, the numbers of flies caught in the small plots declined markedly with increasing distance from the site at which the flies emerged. There were also consistent relationships between the fall-off in the numbers of flies, eggs and pupae with increasing distance from the overwintering site. The numbers of flies captured in each plot varied from 30-1350, the numbers of eggs from 0-670 per 20cm length of carrot row, and the numbers of pupae from 0-120 in the nine soil cores. In addition, the percentage of roots damaged in each of the 11 plots reflected the level of the pest infestation recorded in the various plots. Analysis of the data indicated that there was an extremely strong linear relationship between (log) numbers of flies captured and (log) distance of the plot from the overwintering site. A ten-fold increase in distance from the overwintering site (e.g. 100-1000 m) caused the numbers of flies captured to decrease by 1/66. This relationship did not appear to have any “directional” effect. However, nine of the plots were located along the same axis (south-east), whilst the remaining two plots were north of the overwintering site. There was also evidence that the time of 50% capture was delayed by approximately 1 day for every 100m distance there was between a given plot and the overwintering site. This provides the first estimate of how long it takes flies to locate new crops and an indication of how long the start of first generation forecasts need to be delayed if the subsequent forecasts are to predict accurately the timing of the second fly generation in any given locality. There were also consistent relationships between the fall- off in the numbers of flies, eggs, pupae and crop damage with increasing distance from the overwintering site.

Discussion

Carrot flies can be caught on insect traps as late as December. However, the results of this experiment using crop covers and several similar experiments in other locations in the UK (S. Finch, J. Blood Smyth, personal communication; Finch & Collier, 1999), show that only the 59

offspring of flies that are in the field before the end of September damage the crop during the winter. In addition, at HRI Wellesbourne, where the immature stages of the carrot fly were extracted from the soil (Finch & Vincent, 1996), few eggs and no newly emerged larvae were found in any soil sample taken after the beginning of October (J. Vincent, personal communication; unpublished data). Hence, insecticide sprays need to be applied well before this date if they are to reduce the numbers of insects that damage carrot crops during the winter.

40 160

35 140

30 120

25 100

20 80

15 60

10 40 Number of flies/trap Percent damaged carrots 5 20

0 0 12-Jul 19-Jul 02-Aug 16-Aug 30-Aug 13-Sep 27-Sep 11-Oct 25-Oct 08-Nov Date plots uncovered

Harvested November Harvested March Flies

Fig. 1. The percentage of carrots damaged when carrots were covered at drilling and then uncovered at two-week intervals from the start of the second carrot fly generation.

It is well known that crop rotation and crop isolation reduce the size of carrot fly infestations in new crops (Stadler, 1972; Wainhouse, 1975; Dabrowski & Legutowska, 1976; Coaker & Hartley, 1988; Ellis, 1993). In this study, a ten-fold increase in distance from the overwintering site (e.g. 100-1000 m) caused the numbers of flies captured to decrease by 1/66. This relationship did not appear to have a “directional” effect. However, further studies are needed to confirm this, as nine of the eleven plots were located along the same axis. Estimates from this dispersal study and from studies of fly distribution (K. Phelps, personal communication), in which thousands of yellow sticky traps were placed into several commercial carrot crops (Finch & Collier, 1999), indicated that carrot flies appear to disperse about 50-100m/day both within crops and when trying to find new crops. If such estimates can be confirmed, they will help considerably in the siting of future crops to ensure that fly infestations remain low. In addition, the consistent relationships between the fall-off in the numbers of flies, eggs and pupae with increasing distance from the overwintering site indicated that mortality between the egg and pupal stages did not appear to be density dependent. It is likely that high temperatures and dry soil conditions cause most mortality and that the eggs and first-instar larvae are the stages most susceptible to adverse conditions (Vincent & Finch, 1999). 60

Acknowledgements

The authors thank Kelly Reynolds, Martin Torrance and Marian Elliott for sampling the carrot flies at HRI Wellesbourne. The work was funded by MAFF in Projects PI0321 and HH1924TFV.

References

Coaker, T.H. & Hartley, D. 1988: Pest management of Psila rosae on carrot crops in the eastern region of England. Integrated Control in Field Vegetable Crops IOBC WPRS Bulletin 11 (l): 40-52. Coppock, L. 1974: Notes on the biology of the carrot fly in Eastern England. Plant Pathology 23: 93-100. Dabrowski, Z.T. & Legutowska, H. 1976: The effect of field location and cultural practices on carrot infestation by the carrot fly, Psila rosae (F.). Wiadomosci Ekologiczne 22: 265- 277. Dufault, C.P. & Coaker, T.H. 1987: Biology and control of the carrot fly, Psila rosae (F.). Agricultural Zoology Reviews 2: 97-134. Ellis, P.R. 1993: Controlling carrot fly. The Garden 118: 130-132. Finch, S. & Collier, R.H. 1999: Carrot fly: strategic control options. Grower 132: 40-41. Finch, S. & Vincent, J. 1996: Extracting carrot fly larvae from soil samples. Integrated Control in Field Vegetable Crops IOBC WPRS Bulletin 19 (11): 7-11. Städler, E. 1972: Über die Orientierung und das Wirtswahlverhalten der Mohrenfliege, Psila rosae F. (Diptera: Psilidae). II. Imagines. Zeitschrift für Angewandte Entomologie 70: 29-61. Vincent, J. & Finch, S. 1999: Monitoring carrot fly populations, and the effect of low soil moisture on the mortality of eggs and first-instar larvae. Integrated Control in Field Vegetable Crops IOBC WPRS Bulletin 22 (5): 89-96. Wainhouse, D. 1975: The ecology and behaviour of the carrot fly Psila rosae (F.). PhD Thesis, University of Cambridge, UK, 284 pp. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 61-69

The effect of strips of flowers on pests and beneficial arthropods in adjacent broccoli plots

M. Kienegger1, B. Kromp1 & A. Kahrer2 1 L. Boltzmann-Institute for Biological Agriculture and Applied Ecology, Rinnböckstr. 15, 1110 Vienna, Austria; 2 Federal Office and Research Centre for Agriculture, Spargelfeldstr. 191, 1226 Vienna, Austria

Abstract: In Vienna, Eastern Austria, field experiments were done to find out whether strips of flowers in broccoli plots influence brassica pests and their antagonists in such a way that they can be used as a preventive means of pest control. Both in 1997 and in 1998, four plots of broccoli (20 m x 20 m) were compared to four broccoli plots intercropped with three annual strips of flowers each for differences in the abundance of the cabbage aphid (Brevicoryne brassicae), the cabbage moth (Mamestra brassicae), the diamondback moth (Plutella xylostella) and the small white butterfly (Pieris rapae), as well as for the occurrence of parasitism. The abundance of carabids was evaluated by means of live pitfall traps. Syrphids were surveyed in the broccoli plots as well as in the strips of flowers. The numbers of individuals of the cabbage aphid were significantly lower in plots with flowers as opposed to monocropped broccoli plots. The reduction of the cabbage moth was less pronounced. The abundance of the diamondback moth and the small white butterfly tended to be higher in plots with strips of flowers. There was no significant difference in parasitism between the two treatments. Carabids and syrphids were attracted by strips of flowers. This effect, however, did not lead to an increase of individuals in the adjacent broccoli plots.

Keywords: strips of flowers, broccoli, Brevicoryne brassicae, Pieris rapae, Mamestra brassicae, Plutella xylostella, syrphids, carabids

Introduction

Many insects which are predators or parasitoids of pests feed, as adults, on pollen and nectar. While these floral food resources are a prerequisite for egg maturation in some insect groups, e.g. hoverflies (Diptera: Syrphidae) (Schneider 1948) and parasitic wasps (Hymenoptera) (Jervis & Kidd 1986), they can also influence longevity, fecundity, and therefore the efficiency of any natural enemy (Lövei et al. 1993). As nectar- and pollen-producing food plants are usually scarce in large monocultures, some advisory services for organic farming, and in particular for organic vegetable growing, have been suggesting the establishment of flower strips. An increase in food resources could offer good possibility of attracting beneficial insects and stabilizing their populations at high densities and, as a consequence, contribute to biological control of crop pests. However, this cultural method is rather costly in terms of both money and farmland. The recommended area of flowers can amount to as much as 10% of the total farmland of a farmer. Therefore, before strips of flowers can be established in commercial vegetable growing, it is crucial to evaluate the effects of such strips on both beneficial and on pest insects. So far, agro-ecological effects of weed strips have been studied mainly in cereal crops (e.g. Hickmann & Wratten 1996, Nentwig et al. 1998), rape (Frank & Nentwig 1995) and

61 62

apple orchards (Wyss 1995, Wyss et al. 1995). Predatory arthropods, in particular aphidophagous insects, were commonly reported to be more abundant on crop plants adjacent to weed strips as opposed to those in monocropped stands. However, it is still not clear whether this effect is strong enough to reduce pest infestation to the low level demanded in agricultural practice. This is particularly true for field vegetable crops, which are often exposed to a more severe pest pressure compared to arable crops. The effect of strips of flowers as a control agent against vegetable pests has been investigated in only a few studies, e.g. Nunnenmacher (1998) and Chaney (1998) for lettuce, and Patt et al. (2000) for egg-plant. Brassicas have been studied by van Emden (1967), Zhao et al. (1992), White et al. (1995) and Schellhorn & Sork (1997). The objective of this study was to determine whether annual strips of flowers in broccoli plots influence brassica pests and their antagonists in such a way that they can be used as a means of preventive pest regulation in organic vegetable production.

Materials and methods

Experimental design In 1997 and 1998, broccoli were grown in field plots at a certified organic farm in Franzensdorf, near Vienna, Austria. The experimental design consisted of eight plots (20 × 20 m), four of which were monocropped with broccoli; the remaining four plots were cultivated with both broccoli and three parallel annual strips of flowers each (two at opposite margins and one in the middle of the plot). The width of each strip of flowers measured 1.8 m, which resulted in 28% flower area per plot. The plots were arranged in two rows, separated by 30 m spaces, both within and between the rows, plots with flowers always alternating with monocropped plots. To isolate the plots more effectively from each other, they were surrounded by sugar sorghum (Sorghum bicolor L.) and a mixture of Persian clover (Trifolium resupinatum L.) and Egyptian clover (Trifolium alexandrinum L.) in 1997 and 1998, respectively. Both surrounding crops, however, were removed in the course of the investigation period to prevent flowering plants. All plots were irrigated regularly and weeded when necessary.

Strips of flowers In 1997, a commercially available mixture of seed of mainly wild flowers was used for the strips of flowers (Tab. 1). As mallow and sunflower soon became dominant and suppressed virtually all other species, the composition of the strips was changed to mainly cultivated plants in 1998 (Tab. 1). Furthermore, to reduce competition, seeds were sown in rows, with seeds of two species of plant per row at the maximum. The strips were sown at the end of May 1997 and in mid April 1998 and were flowering at the time the broccoli were transplanted from the glasshouse into the field (end of June 1997 and mid June 1998).

Monitoring of insects Visual observation of broccoli A sample of ten randomly chosen broccoli plants per plot was censused for all occurring pest insects (eggs, larvae and pupae) and their parasitoids (i.e. parsitized developmental stages of the pests) weekly between 24 July and 19 September 1997, and between 17 June and 25 September 1998. As the most dominant species were cabbage aphid (Brevicoryne brassicae L.), cabbage moth (Mamestra brassicae L), diamondback moth (Plutella xylostella L) and small white butterfly (Pieris rapae L.), only these pests will be dealt with here. In addition, plants were checked for eggs and larvae of syrphids, chrysopids and coccinellids. 63

Table 1. Species composition of strips of flowers in 1997 and 1998.

1997 1998 mallow (Malva sylvestris L.) spinach (Spinacia oleracea L.) sunflower (Helianthus annuus L.) buckwheat (Fagopyrum esculentum Moench) catchfly (Silene alba L.) borage (Borago officinalis L.) evening primerose (Oenothera biennis L.) pea (Pisum sativum L.) parsnip (Pastinaca sativa L.) fennel (Foeniculum vulgare Miller) dill (Anethum graveolens L.) dill (Anethum graveolens L.) cornflower (Centaurea cyanus L.) cornflower (Centaurea cyanus L.) white clover (Trifolium repens L.) black medick (Medicago lupulina L.)

Pitfall traps Carabid beetles were sampled in four adjacent plots (two plots per treatment) using dry pitfall traps comprising plastic pots (diameter 85 mm, depth 80 mm) and small humid sponges, which prevented arthropods from drying up and provided hiding places for the smaller beetles. Rain covers (20 x 20 cm tiles of Perspex supported by lengths of wire) were positioned approximately 5 cm above each trap. A total of nine traps were arranged in three parallel rows in each plot, the traps being separated by 5 m spaces within the rows. The positions of the rows were: centrally between the rows of broccoli (5.5 m from the edge); either within a marginal strip of flowers (0.5 m from the edge) in plots with flowers or at the same distance from the edge but between rows of broccoli in plots without flowers; 5.5 m from the edge of the plot in the surrounding field. Sampling was performed biweekly over 2- day periods between 24 July and 19 September 1997 and between 24 June and 25 September 1998. Carabids were, if possible, identified to species in the field, or transferred to the laboratory for further identification.

Visual observation of adult syrphids Between 26 June and 25 August 1998, adult hoverflies were recorded weekly when they landed on flowers or on broccoli plants in randomly chosen 1 m2 plots within a 15-minute period. The flies were observed in strips of flowers, in broccoli adjacent to flower strips and in broccoli monoculture. There were 40 observations for each position. Hoverflies were identified to genera or, when possible, to species in situ. All observations took place between 9 a.m. and 1 p.m.

Analysis of data For each group of arthropods, the mean numbers per plants and plot were compared between monocropped and intercropped plots. T-tests and Mann-Whitney non parametric tests were carried out to test for significant differences in the numbers for each group of insect.

Results

Lepidopteran pests Table 2 summarizes the abundance of the various lepidopteran pest insects. While the diamondback moth and the small white butterfly seemed to be attracted by the strips of flowers, the cabbage moth tended to be more abundant in plots without flowers. However, except for Pieris rapae on 4 August 1998 (p < 0.01) and on 27 August 1998 (p < 0.05), there were no significant differences between the treatments. 64

Similarly, parasitism rates of the observed lepidopteran pests did not differ significantly between treatments. Nevertheless, rates of parasitized pupae of diamondback tended to be higher in plots intercropped with flowers, whereas in 1997 parasitism rates for the larvae of the small white butterfly seemed to be higher in plots without flowers.

Table 2. Cumulative totals of developmental stages of lepidopteran pests per plant and observation period in broccoli plots with (+ flowers) and without (control) strips of flowers. Rates of parasitism in % are given in brackets.

Year 1997 1998 Observation period 25 July – 20 September 17 June – 22 September Treatment control + flowers control + flowers Plutella xylostella eggs 144.1 200.9 3.9 3.7 larvae 145.7 161.9 39.3 49.7 pupae 39.3 (33) 29.1 (44) 20.0 (74) 15.4 (78) Pieris rapae eggs 8.8 10.5 4.1 6.5 larvae 10.1 (38) 10.5 (27) 7.9 (19) 10.9 (19) Mamestra brassicae eggs 64.7 (15) 48.6 (14) 13.6 (28) 1.8 (22) larvae 23.0 (2) 20.8 (4) 2.9 (0) 2.4 (0)

Aphids (Brevicoryne brassicae) As the cabbage aphid was not abundant in 1997, only the results of 1998 are given here. Whilst the numbers of individuals observed in the two treatments did not differ during the early summer generation, later in the year significantly fewer (p < 0.05) aphids were recorded in plots with flowers than in monocropped plots (Fig. 1a). Parasitoids started to respond to the increase in the aphid population at the beginning of July (Fig. 1b). However, no difference in the numbers of mummified aphids could be shown between the two treatments.

Syrphids In 1997, eggs and larvae of hoverflies tended to be more abundant in plots intercropped with flowers than in control plots, whereas the opposite was true for 1998 (not significant, Tab. 3). Yet the syrphids-per-aphid ratio was more favourable in plots with flowers (Fig. 1c). During visual assessment of adult flies in strips of flowers and broccoli a total of 360 individuals was observed, comprising 10 species. Members of the genus Spaerosphoria were most abundant (1997: 72% and 1998: 43%). Of all flies recorded, 85% were observed on flowers, 9% on broccoli in plots with flowers and 6% on broccoli in plots without flowers. Eighty-five per cent of all individuals belonged to the aphidophagous subfamily of Syrphinae (six species).

Chrysopidae Lacewing eggs were found more often (p < 0.01 on 6 August 1997 and on 21 July 1998; p < 0.05 on 11 and 27 August 1998) on monocropped than on intercropped broccoli (Tab. 3). The numbers of larvae, however, did not differ between the treatments.

a) 300

200 * *

100 *

Individuals/plant 0

b) 80

20 Parasitism in % 0

c) 0,12 0,10

0,08 0,06 0,04 0,02

Syrphids/aphid 0,00

1.7. 7.7. 4.8. 1.9. 8.9.

17.6. 23.6. 15.7. 21.7. 29.7. 11.8. 18.8. 27.8. 22.9. Date of sampling

Plots without flowers Plots with flowers

Fig. 1. a) Mean number of individuals of Brevicoryne brassicae per plant in plots with and without strips of flowers in 1998. * indicates significant differences (p < 0.05) between treatments. b) Mean rate of parasitism of B. brassicae per plant. c) Numbers of egg, larvae and pupae of syrphids per B. brassicae and plant.

Coccinellidae Although many ladybirds were observed running on the soil, only a few were encountered on broccoli plants. There was no difference in the number of either adults nor larvae between monocropped and intercropped plots (Tab. 3). 66

Table 3. Cumulative totals of predators per plant and observation period in broccoli plots with (+ flowers) and without (control) strips of flowers.

Year 1997 1998 Observation period 25 July – 20 September 17 June – 22 September Treatment control + flowers control + flowers Syrphidae eggs 9.5 10.3 5.8 2.9 larvae 3.7 3.9 4.9 2.2 pupae 0.3 0.1 0.5 0.1 Chrysopidae eggs 2.8 0.9 20.7 9.9 larvae 0.4 0.4 0.4 0.2 Coccinellidae larvae 0.1 0.2 1.6 1.2 adults 0.0 0.0 0.9 0.6

Carabids In total 1432 and 1795 carabid beetles were caught in the dry pitfall traps in 1997 (ten trapping days) and 1998 (16 trapping days), respectively. Figures 2c and 2d indicate that most individuals were trapped within the strips of flowers (1997: 444 and 1998: 855), largely because of a concentration of species such as Harpalus rufipes (in both years), Pterostichus melanarius (1997) and Poecilus cupreus (1998). For a complete list see Kienegger & Kromp (2000). Irrespective of treatment, fewest individuals were caught in traps situated centrally within broccoli. The numbers of individuals caught in traps outside the experimental plots did not differ. This was true for both years of the study. Thirty-four species were identified from all traps in both observation periods. More species were caught in plots with strips of flowers (1997: 19 and 1998: 30) than in plots without flowers (16 for both years). The highest number of carabid species was found in the flower-strip position and the lowest at the crop centre (Fig. 2).

Discussion

The results from the plot experiments showed that the effect of intercropping broccoli with strips of flowers on brassica pests and their natural enemies depended on the species of insect studied. Although lepidopteran pest insects tended either to be reduced (cabbage moth) or favoured (diamondback moth and small white butterfly) in intercropped broccoli plots as opposed to monocropped plots, the presence of strips of flowers did not result in significant differences in the numbers of eggs or larvae between the treatments. This confirmed earlier studies by Latheef & Irwin (1979), Zhao et al. (1992) and White et al. (1995). As small white butterflies were repeatedly observed feeding on flowers, nectar-producing herbs neighbouring brassica plants may be attractive to the butterflies and result in higher damage to the crop than otherwise. In contrast, cabbage aphid was reduced significantly by the presence of strips of flowers. Similarly, White et al. (1995) found fewer aphids in cabbage plots with a boundary-strip of Phacelia tanacetifolia than in control plots. This effect, however, could be explained neither by higher numbers of hoverfly eggs nor by increased parasitism, which compares favourably with the current study. In contrast, Hickmann & Wratten (1996) ascribed a significant 67

reduction of aphids in winter-wheat fields bordered with P. tanacetifolia to increased densities of syrphid eggs, as differences in parasitism did not occur.

a) 30 b) 30 1997 1998 25 25

20 20

15 15 10 10

No. ofNo. species 5 No. ofNo. species 5 0 0

- F + F - F + F c) d) 1000 1997 1000 1998

750 750

500 500

250 250 No. ofNo. individuals ofNo. individuals

0 0 - F + F - F + F

Field Broccoli edge Broccoli centre Flower strip

Fig. 2. Total numbers of species and individuals of carabids from live pitfall traps at different positions in plots with (+ F) and without (- F) strips of flowers in 1997 and 1998.

Although strips of flowers did not result in increased numbers of eggs or larvae of hoverflies on broccoli compared to the control in the current study, they clearly attracted adults, as was shown by visual observation in the strips of flowers and on broccoli plants. White et al. (1995) captured more hoverflies in yellow traps in the experimental plots compared with the control plots, but again the highest numbers were found in the traps closest to the P. tanacetifolia border. Other studies on habitat manipulation for syrphids also revealed increases in adult fly numbers near the floral resources. (e.g. Cowgill et al. 1993, MacLeod 1999). Thus it appears that hoverflies do not disperse very far from the pollen and nectar sources. A similar behaviour could be observed with carabid beetles. Although they were attracted by strips of flowers, they did not seem to colonize the broccoli stands. According to Corbett (1998), strip vegetation can sometimes become a sink for natural enemies and decrease their abundance on a crop. This is likely to appear when strips act only as food resources rather than as an overwintering refuge which allows the enemies to be present in interplantings at crop germination. In such situations enemies tend to stay in the strips without hardly ever 68

leaving them for the crop. This could explain why species of carabid that were abundant in strips of flowers (1997: Pterostichus melanarius; 1998: Poecilus cupreus, Harpalus and Amara spp.) hardly ever occurred in traps situated in the centre of the plots. Possible explanations for the overall poor effect of strips of flowers on pest reduction and enhancement of natural enemies could be found in the experimental design. In an attempt to keep the vegetation management as flexible as possible for farmers, the strips of flowers were set up as annual strips. However, studies from Germany and Switzerland showed that an enhancement of predatory beneficials and significantly higher rates of parasitism can only be achieved in perennial strips, which can provide favourable overwintering sites (Denys et al. 1997, Thies et al. 1997). Furthermore, Corbett (1998) points out the importance of plot size in experiments on enhancement of beneficials with respect to mobility of the target organism. Syrphids, for example, could have been attracted by the flowers of the strips, but then moved on to control plots for oviposition, since, considering their wide range of action (Bastian 1994), the given inter-plot distance was rather small. Therefore, although field plot experiments like this can show tendencies of effects of flower strips on pest and beneficial insects, only experiments in real scale situations with individual fields as replicates and under commercial growing conditions will prove qualification of the method for implementation in practice.

Acknowledgements

We thank the Ministry of Agriculture and Forestry, the Regional Government of Lower Austria and the Association of Vegetable Growers of Lower Austria for supporting this project and T. Döring (University of Münster) for assistance with the hoverfly monitoring in 1998.

References

Bastian, O. 1994. Schwebfliegen. A. Ziemsen Verlag, Wittenberg Lutherstadt, Neue Brehm Bücherei Nr. 576. Chaney, E.C. 1998. Biological control of aphids in lettuce using in-field insectaries. In: Enhancing biological control. Habitat management to promote natural enemies of agricultural pests, eds. Pickett, C.H. and Bugg, R.L.: 73-83. Corbett, A. 1998. The importance of movement in the response of natural enemies to habitat manipulation. In: Enhancing biological control. Habitat management to promote natural enemies of agricultural pests, eds. Pickett, C.H. and Bugg, R.L.: 25-48. Cowgill, S.E., Wratten, S.D. & Sotherton, N.W. 1993. The selective use of floral resources by the hoverfly Episyrphus balteatus (Diptera: Syrphidae) on farmland. Ann. appl. Biol 122: 223-231. Denys, C., Tscharntke, T. & Fischer, R. 1997. Die Besiedelung von Wildkräutern durch Insekten in eingesäten und selbstbegrünten Ackerrandstreifen und im Getreideacker. Verhandlungen der Gesellschaft für Ökologie 27: 411-418. Frank, T. & Nentwig, W. 1995. Artenvielfalt von Laufkäfern (Carabidae), Schwebfliegen (Syrphidae) und Tagfaltern (Rhopalocera) in Ackerkrautstreifen und angrenzenden Feldern. Mitt. Dtsch. Ges. allg. angew. Ent. 9: 685-691. Hickmann, J.M. & Wratten, S.D. 1996. Use of Phacelia tanacetifolia strips to enhance biological control of aphids by hoverfly larvae in cereal fields. Journal of Economic Entomology 89: 832-840. 69

Jervis, M.A. & Kidd, N.A.C. 1986. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 61: 395-434. Kienegger, M. & Kromp, B. 2000. Blühstreifen im biologischen Brokkoli-Anbau: ein Beitrag zur natürlichen Schädlingsregulation. In: Streifenförmige ökologische Ausgleichsflächen in der Kulturlandschaft: Ackerkrautstreifen, Buntbrache, Feldränder. Nentwig, W. (ed), Verlag Agrarökologie Bern, Hannover: 229-250. Latheef, M.A. & Irwin, R.D. 1979. The effect of companionate planting on lepidopteran pests of cabbage. Can. Entomol. 111: 863-864. Lövei, G.L., Hodgson, D.J., MacLeod, A. & Wratten, D.S. 1993. Attractiveness of some novel crops for flower-visiting hoverflies (Diptera: Syrphidae): comparisons from two continents. In: Pest control & sustainable agriculture, Corey, S.A., Dall, D.J. & Milne, W.M. (eds.), CSIRO, Melbourne: 368-370. MacLeod, A. 1999. Attraction and retention of Episyrphus balteatus DeGeer (Diptera: Syrphidae) at an arable field margin with rich and poor floral resources. Agricult. Ecosyst. Environ. 73: 237-244. Nentwig, W., Frank, T. & Lethmayer, C. 1998. Sown weed strips: artificial ecological compensation areas as an important tool in conservation biological control. In: Conservation biological control, Barbosa, P. (ed.): 133-153. Nunnenmacher, L. 1998. Blattläuse auf Kopfsalat und deren Kontrolle durch gezielte Beeinflussung der Lebensgrundlage ihrer Prädatoren. Bayreuther Forum Ökologie 61. Patt, J.M., Hamilton, G.C. & Lashomb, J.H. 2000. Impact of strip-insectary intercropping with flowers in conservation biological control of the colorado potato beetle. http://www.rain.org/~sals/joe2.html Schneider, F. 1948. Beitrag zur Kenntnis der Generationsverhältnisse und Diapause räuberischer Schwebfliegen (Syrphidae, Dipt.). Mitt. Schweiz. Entomol. Ges. 21: 249- 285. Schellhorn, N.A. & Sork, V.L. 1997. The impact of weed diversity on insect population dynamics and crop yield in collards, Brassica oleraceae (Brassicaceae). Oecologia 111: 233-240. Thies, C., Denys, C., Ulber, B. & Tscharntke, T. 1997. Der Einfluss von Saumbiotopen und Ackerbrachen auf Schädlings-Nützlings-Interaktionen im Raps (Brassica napus spp. oleifera). Mitt. Ges. Ökol. 27: 393-398. van Emden, H.F. 1967. The effect of uncultivated land on the distribution of cabbage aphid (Brevicoryne brassicae) on adjacent crop. Appl. Ecol. 2: 171-196. White, A.J., Wratten, S.D., Berry, N.A. & Weigmann, U. 1995. Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera: Syrphidae). Journal of Economic Entomology 88: 1171-1176. Wyss, E. 1995. The effects of weed strips on aphids and aphidophagous predators in an apple orchard. Entomologia Experimentalis et Applicata 75: 43-49. Wyss, E., Niggli, U. & Nentwig, W. 1995. The impact of spiders on aphid populations in a strip-managed apple orchard. Journal of Applied Entomology, 119: 473-478. Zhao, J.Z., Ayers, G.S., Grafius, E.J. & Stehr, F.W. 1992. Effects of neighboring nectar- producing plants on populations of pest Lepidoptera and their parasitoids in broccoli plantings. Great Lakes Entomologist 25: 253-258. 70

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 71-74

Elements of integrated control in field vegetables in Slovenia

L. Milevoj, J. Osvald, N. Valič University of Ljubljana, Biotechnical Faculty, Agronomy Department, Jamnikarjeva 101, 1111 Ljubljana, Slovenia

Abstract: In Slovenia, growing of field vegetable crops in the open includes elements of integrated control such as: appropriate growing procedures and measures, biotechnical, biological (pest and disease) control as well as chemical control based on prognosis (forecasting) and choosing of optimal pesticides. The contribution deals with elements of integrated control, which are already commonly used as well as those under investigation which are to be included into growing of field vegetable crops in the open. A survey of the literature in Slovenia, covering these topics is also given.

Key words: pests, diseases, field vegetable crops, integrated control.

Introduction

In Slovenia, growing of vegetable crops in fields and gardens has a long tradition. It is well known, that supply of cities like Ljubljana, Trieste and Rijeka depended on these activities. Today, vegetable crops are grown of specialised farms where this is the main and basic activity, additionally it is practised as an alternative on the farms which choose cattle breeding, fruit growing or wine growing as their main activity and finally it is practised also on smaller farms as an additional activity or just to satisfy one's own needs (Černe, 1999). In Slovenia, vegetable crops are grown on 11,000 ha (2.6 % of the agricultural land); vegetables produced on 3,000 ha are market oriented. Diverse climatic and ecological conditions enable the cultivation of very different vegetable crops. In the past, traditional measures were used to cultivate field vegetables. Nowadays, integrated (biotechnical, biological and chemical) control is used to cultivate them. According to this, vegetable growing in Slovenia can be divided into conventional (70 %), integrated (25 %) and bio (5 %) production. Some of the characteristic elements of integrated control are already well established in Slovenia others are still under investigation and are to be introduced in future. This contribution deals with elements of integrated control, which have been implemented in Slovenia to different degrees: a) some of them have already been introduced and are commonly used, b) some of them are being investigated and are being implemented as experimental, c) some of them are being considered as being potentially of use for some selected vegetable crops in future. Different ecological conditions in Slovenia enable growing of different vegetable crops. More than 40 vegetable crops are grown in the open. The most important are: cabbage, cauliflower, lettuce, endive, tomatoes, peppers, cucumbers, onion and leek, while beans and other legumes are less common, the same being true also for carrots. To keep plants well and healthy it is not enough to take care of the immediate pest and disease threats, other factors have to be considered as well, among these: suitable crop rotation, optimal selection and applying of fertilisers, optimal nutrition supply as well as other decisive growing factors. These are the hot topics for agricultural research during the next ten years or so.

71 72

Methods of Integrated Control

Integrated production is based on integrated control, and introduces contemporary production methods. When possible, the problems should be prevented by implementing some of the following mechanisms of crop protection: • determining locations, suitable for the selected vegetable varieties, from geographical as well as climatic point of view; • selecting the indigenous and bred cultivars resistant to worse growing conditions; • using seedlings grown in greenhouses in new plantations; • planting fast growing seedlings of good quality, and caring for them optimally; • covering the soil using black mulch plastic sheets; • covering the crop, using PP materials (Covertan, Agryl, Basse, Vrtex) to speed-up the crop growth, to improve growing conditions, and to protect crop against pests; • selecting organic and mineral fertilisers; • irrigating by drop irrigation; • forecasting diseases by monitoring abiotic factors (microclimatic stations to monitor weather conditions – Adcon System) and biotic factors (Burkard apparatus to monitor infection with fungi, e.g. counting zoosporangia in the air) • monitoring aphids (suction traps); • monitoring pests using pheromone traps, sticky coloured boards; • protecting and stimulating indigenous beneficial species; • reducing pesticide consumption also by making the best use of knowledge on pests biology and their critical numbers.

IPM in practice

Integrated control in field vegetables was implemented in cucumber production. On a smaller scale, such a method has already been applied for growing tomatoes and green peppers. Direct covering and planting on beds is commonly used in growing of lettuce, endive and chicory, since it ensures better aeration and reduces the use of pesticides. Covering with PP sheets improves the germination of carrots, and also protects them against the carrot fly (monitored by Rebbel traps). PP coverings shortens the potato growing season for 15 to 30 days, it prevents the Colorado beetle attacks, and diminishes the danger of Phytophthora.

Orientation in the future

The program of integrated pest control in vegetable crops means: • continuous monitoring of diseases and pests as well as their natural enemies; • applying pesticides causing no or little harm to natural enemies of the pests; • use of undersowing crops; • introduction of bio-stimulators and organic-mineral fertilisers to improve the plant resistance against pests as well as to promote plant growth; • diminishing the quantities of applied fertilisers, and establishing the control of the intake of fertilisers/nutrients by the crop; • preparing test fields with the possibility to test nutrient quantity.

References

Celar, F. 1995: Antagonizmi med talnimi saprofitskimi in parazitskimi glivami-mehanizmi in možnost uporabe v biotičnem varstvu rastlin./Antagonisms between saprophytic and parasitic soil fungi–mechanisms and possible use in biological control of plant pathogens. Lect. and Pap. present. at the 2nd Slov. Conf. on Plant. Prot. in Radenci, February 21-22 1995: 437-445. Černe, M. 1999: Slovensko zelenjadarstvo./ Vegetable production in Slovenia./ Sodob. kmet., 32 (99) 9: 403-411. Dolinar, M. & Žolnir, M. 1995: Prognose des Auftretens des Falschen Gurkenmehltaues (Pseudoperonospora cubensis /Berk. et. Curt./Rost.) nach Bedlan, ergänzt durch Sporangienfang. Lect. and Pap. present. at the 2nd Slov. Conf. on Plant Prot. in Radenci 21.-22. February 1995: 283-286. Milevoj, L. & Osvald, J. 1991: Der Einfluss moderner Technologien auf das Auftreten des Falschen Gurkenmehltaues (Pseudoperonospora cubensis /Berk. et. Curt./ Rost.). Meded. Fac. Landbouwwet. Rijksuniv. Gent, 56 (2b): 539-543. Milevoj, L. 1991: Preučevanje zoofagne hržice Aphidoletes aphidimyza (Rond.) (Diptera, Cecidomyiidae) v Sloveniji./Investigation of Aphidoletes aphidimyza (Rond.) (Diptera, Cecidomyiidae) in Slovenia. Zb. Bioteh. fak. Univ. Ljubljana, Kmet. 57: 163-167. Milevoj, L. 1992: Erynia neoaphidis Rem. et Henn. na graškovoj uši (Acyrthosiphon pisum Harr.) u Sloveniji [Erynia neoaphidis Rem. et Henn. on Acyrthosiphon pisum Harr. in Slovenia.]. Glas. zašt. bilja 15: 317-318. Milevoj, L. 1992: Parazitoida Aphidius matricariae Hal. in Diaeretiella rapae (M’Intosh) (Hym., Aphidiidae) na Rhopalosiphum padi L. (Hom., Aphididae) v Sloveniji. [Parasitoids Aphidius matricariae Hal. and Diaeretiella rapae (M’Intosh) (Hym., Aphidiidae) on Rhopalosiphum padi L. (Hom., Aphididae) in Slovenia.]. Zb. Bioteh. fak. Univ. Ljubljana, Kmet. 59: 163-167. Milevoj, L. & Osvald, J. 1994: The effects of drip irrigation on the occurrence of downy mildew of cucumber (Pseudoperonospora cubensis /Berk. et. Curt./ Rost.). Meded. Fac. Landbouwwet. Rijksuniv. Gent 59 (3a): 853-858. Milevoj, L. & Osvald, J. 1996: Integrated cultivation of cucumbers (Cucumis sativus L.). 1st Slovenian Congress on Food and Nutrition. 21.-25. April, 1996, Bled. Proceedings: 294- 299. Milevoj, L. & Štukelj, A. 1996: The effects of some pesticides on the parasitoid Diaeretiella rapae (M’Intosh). Meded. Fac. Landbouwwet. Rijksuniv. Gent 61 (3b): 949-954. Milevoj, L. 1996: A study on Aphelinus asychis Walk. in Slovenia. Res. Rep. Biotechn. Fac. Univ. Ljublj., Agric. 67: 115-120. Milevoj, L. 1996: Control of soilborne pathogens by solar heating in Slovenia. Biometeoro- logy: proceedings of the 14th International Congress of Biometeorology, September 1-8, 1996. International Society of Biometeorology; Ljubljana: Slovenian Meteorological Society, Part.2, vol. 2: 84-91. Milevoj, L. 1998: Perspektive biotičnega varstva rastlin v Sloveniji. [Prospect for biological plant control in Sloevnia.] Kmetijstvo in okolje: proceedings of the conference, Bled, March 12-13 1998: 163-171. Milevoj, L. 1999: Biotično varstvo jajčevca, paprike in paradižnika. [Biological control of eggplant, pepper and tomato diseases and pests.] Sodob. kmet., 32 (99) 5: 252-255. Milevoj, L. 1999: Biotično varstvo kapusnic. [Biological control of brassicas.] Sodob. kmet., 32 (99) 11: 540-542. 74

Trdan, S. 1999a: Barvna dovzetnost nekaterih gospodarsko pomembnejših vrst resarjev (Thysanoptera). [Colour preference of some economically important Thysanoptera species.] Lect. and Pap. present. at the 4th Slov. Conf. on Plant Prot., Portorož, March 3-4, 1999, Ljubljana: 493-498. Trdan, S. 1999b: Monitoring cvetličnega resarja (Frankliniella occidentalis Perg.) z barvnimi lepljivimi ploščami. [Monitoring of western flower thrips (Frankliniella occidentalis Perg.) with coloured sticky boards.] Sodob. kmet. 32 (99) 10: 475-480.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 p. 75

Simulating the population dynamics of the onion fly Delia antiqua in chives using an extended Leslie Model

M. Otto 1) & M. Hommes 2) 1 State Institute for Agronomy and Plant Protection (LPP), Mainz, Germany 2 Fed. Res. Centre for Agriculture and Forestry (BBA), Institute for Plant Protection in Horticulture, Braunschweig, Germany

Abstract: The onion fly (Delia antiqua) (DA) is a serious pest in many species of the Allium family, including onions and chives. Within the last three years a simulation model for DA was developed as a decision tool for the integrated control of DA in chives and onions. The structure and desktop appearance of the model are derived from SWAT3.3, a previously developed package of programmes, including the cabbage root fly (Delia radicum) and the carrot fly (Psila rosae) as pest species. Like the previous models the simulation model for the onion fly is based on an extended Leslie model. The model simulates the developmental rates for different life stages of DA for each day based on air and soil temperature. Transition rates between the life stages as well as reproductive parameters and periods of quiescence are taken into account. Behaviour of DA such as oviposition and flight activity can be simulated using, amongst other factors, wind speed as a variable. Model parameters were obtained from both laboratory studies with a German strain of DA and data available from literature. To compare simulated and observed population dynamics the flight activity of DA was monitored in the main chives growing regions of Germany where the onion fly is a key pest. A comparison between the observed and simulated flight activity from 1997-99 shows a good correspondence for the first two generations of DA but fails to predict the third generation with the necessary accuracy to time insecticide applications. The model will be available for German extension services via the PASO software by the start of the year 2000.

Key words: Delia antiqua, onion, chives, model, population dynamics

75 76

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 77-79

Population dynamics of Platyparea poeciloptera and its implications for an integrated pest management in asparagus

M. Otto 1 & M. Hommes 2 1 State Institute for Agronomy and Plant Protection (LPP), Mainz, Germany 2 Fed. Res. Centre for Agriculture and Forestry (BBA), Institute for Plant Protection in Horticulture, Braunschweig, Germany

Abstract: The flight activity of P. poeciloptera was monitored with sticky pole traps over a period of three years in different asparagus growing regions in Germany. For the first time data over the complete vegetation period are available. The observations show that the flight activity of the asparagus fly in Germany lasts from April to August over a period of up to four months. Variations in the flight activity with regard to its start, peak, and end date showed large variations up to two months. These variations could be observed both on a regional and on a local level. Because the allowed number of insecticide treatments is limited, sprays cannot cover the whole flight period of P. poeciloptera especially in young stands. We therefore propose that traps should be used to optimise the timing of sprayings. Fields should be monitored individually because of the large within-region variation in the flight activity of P. poeciloptera.

Keywords: Platyparea poeciloptera, asparagus, population dynamics, traps, integrated control

Introduction

The asparagus fly is, along with the asparagus beetle, the most important insect pest in asparagus in Germany (Crüger 1991). Flies are univoltine and with a life span of one to two weeks relatively short lived (Dingler 1935). Damage by P. poeciloptera is caused by the larval stages which tunnel inside asparagus ferns. A high infestation level with asparagus flies is known to kill young plantations and suspected to decrease the yield of older asparagus fields. Despite this our knowledge about the biology and population dynamics of the pest is either very limited or virtually absent. In the following we present basic information about asparagus fly flight activity and suggest an integrated control strategy.

Material and methods

Using green sticky pole traps (Otto et al. 2000) the flight activity of P. poeciloptera was recorded during the years 1997 to 1999 in different asparagus growing regions all over Germany. Traps were checked twice a week during the start of April until the end of August. Trapping did not interfere with harvesting or influence the farmers´ disease or pest management decisions.

Results

Flight activity of P. poeciloptera could be observed over an extended period of four months from the start of April until mid August. However, start, peak, and end of the flight period

77 78

differed substantially both between and within regions (Figs 1,2). Differences in the peak of flight activity were recorded to be as large as 70 days between fields spaced less than two kilometres apart within the same growing region. In several fields the flight activity of P. poeciloptera appeared to have several peaks.

10 Magdeburg

0 20 Braunschweig 10

20 Mainz / trap N flies 10

30 Freiburg 20 10 0 1.Mai 1.Jun 1.Jul 1.Aug

Fig. 1. Flight activity of P. poeciloptera in different regions of Germany 1999

Fig. 2. Flight activity of P. poeciloptera within the region of Braunschweig 1998

Discussion and conclusion

The data in this presentation show for the first time the flight activity of P. poeciloptera recorded by traps over the whole growing season. The asparagus fly is an univoltine species despite the long duration and the often jagged appearance of its flight curve, which was wrongly interpreted as the existence of several generations of asparagus flies. The flight activity of P. poeciloptera can last until August. Because the flight activity of P. poeciloptera was commonly thought to be terminated at the end of June no control measures against the fly were applied after this date. However, the assessment of plant damage (Otto et al. 1999) in combination with the observed flight activity clearly showed that the occurrence of P. poeciloptera at the end of July is sufficient to cause high infestation levels. We therefore propose that asparagus fly control should be continued throughout July to avoid high infestation levels especially in old stands. The long flight period and the large variation of flight activity even on a local level both pose severe problems for the control of P. poeciloptera. Sprays with fixed time intervals cannot cover the complete flight period because of a restricted number of insecticide applications and a narrow range of insecticides which the farmers are allowed to use. Because of the large variation in the flight activity of the asparagus fly general warnings as issued presently by extension services are not ideal. To date, decisions on the timing of insecticide applications against P. poeciloptera are not based on trap catches. As a result control of P. poeciloptera is likely to lack efficiency. An unsatisfactory control practice is indeed indicated by the high infestation levels recorded in many of our field sites despite regular insecticide sprayings by the growers. To improve asparagus fly control we suggest omitting spraying schedules on a regular basis. Instead, traps should be used to monitor the flight activity of P. poeciloptera to time insecticide applications correctly (Otto et al. 2000).

Acknowledgements

We thank the Ministry of Agriculture (BML) for financial support.

Literature

Crüger, G. 1991: Pflanzenschutz im Gemüsebau. 3rd ed. Ulmer Verlag, Stuttgart: 344 pp. Dingler, M. 1934 a: Die Spargelfliege (Platyparea poecilioptera, Schrank). Arbeiten über Physiologie und angewandte Entomologie Berlin-Dahlem 1 (2): 131-162. Dingler, M. 1934 b: Die Spargelfliege (Playtyparea poeciloptera, Schrank). Arbeiten über Physiologie und angewandte Entomologie Berlin-Dahlem 1 (3): 185-217. Otto, M., Hommes, M., & Burghause, F. 1999: Spargelfliegenbefall im November kontrol- lieren. Gemüse 35 (11): 666. Otto, M., Burghause, F., & Hommes, M. 2000: Die Spargelfliege in der Falle – Entwicklung und Test eines Fallentyps. Gemüse 36(3): 35-37.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 81-86

Use of Plant Protection Information System in field vegetable growing

A. Pákozdi1, K. Pálfi1, K. Mohai1, L. Érsek2, K. Biber3 1 Plant Health and Soil Conservation Station of Budapest, Coordination Unit 2 Plant Health and Soil Conservation Station of Győr-Moson-Sopron County 3 Ministry of Agriculture and Regional Development

Abstract: Data on occurrence and spread of pests have been supplied by Hungarian plant protection organisation since 1954. The country-wide forecasting network was formed in 1968 from the forecasting groups of 20 county stations of the plant protection organisation and of the centre, coordinating their work. Data recorded on pest occurrence and developmental stage of pests and plants allowed to run a forecasting system at local and national levels. Development of a more reliable and flexible, computer-aided system (Plant Protection Information System, PPIS) became necessary, adjusting better to occurred political and economic changes. Major element of the new system introduced in 1997 is that excessively detailed recording was replaced by global approach based on a more practical, general aspect with less subjective errors. 73 pests of 20 crops are included in the system, out of this 18 pests of 7 field vegetable crops are being monitored: potato, pea, sweet pepper, tomato, onion, cucumber, melon. Data are input in the PPIS program processing them to well-arranged charts and maps showing plant health situation in the particular counties and the country, preparing decisions for plant protection measures. The PPIS allows to observe the economic threshold, as well as to prepare short and long term forecasts for the county and regions. Databases of the system addresses the organisations of crop production and extension service. Their task is to tailor the control measures to be taken by farmers based on warnings of the system.

Key words: plant protection, information system, warning

Introduction

Since 1954 a plant protection organisation has been operating in Hungary, which has been doing forecasting jobs as well from the beginning. In 1968 the Plant Protection Service established the Forecasting Department which resulted in fundamental changes. Its tasks were to create, coordinate the country-wide forecasting network and to control their activity. The network was formed in 1968 from the forecasting groups of 20 county of the plant protection organisation and of the centre, coordinating their work. It was operated as an integrated forecasting system of regions. The districts (regions) as units of forecasting were defined based on growing traditions taking plant geographic, economic, and ecological aspects into consideration. Regular data recording was done by the members of the group. These data recordings were devided into 3 groups. At the first one, at the phenological sites (60) developmental changes of 10-20 pests were monitored. By this, forecasting groups were informed about the occurrence of pests and diseases. At the second one, at the representative sites (350), changes in population density of 110 pests were recorded at critical growth stages of 33 crops. These data supplied information about the occurrence and spread of pests based on growing traditions. The 3rd group, the guided recordings were done to survey the spread and population relations of all pests. Data recording and primary summing up were carried out by

81 82

the plant protection stations. The national processing took place at the centre of the plant protection organisation. The encoded data were transferred by using cable every day. The centre published national warnings based on processing of field data. The system was detailed and time consuming causing errors in the recording and evaluation. Because of the political and economic change of regime, the demand arose for modifying the principle of the information system. Instead of the inflexible and the excessively accurate existing system, the new Plant Protection Information System (PPIS) became essential which is operated by other principles. The responsibility of the state to prevent epidemic has changed, under the new ownership conditions, it could not be related directly to the farmers. The PPIS allows to observe the economic threshold, as well as to prepare short and long term forecasts for the county and regions. The database of the system addresses the organisations of crop production and extension service. Their task is to tailor the control measures to be taken by farmers based on warnings of the system.

Materials and methods

Crops and pests 73 pests of 20 crops are included in the system, 21 pests of 5 crops are being monitored throughout the country, 52 pests of 15 crops are being observed in certain regions. Within this group 18 pests of 7 field vegetable crops are being monitored: potato, pea, sweet pepper, tomato, onion, cucumber, melon. The system can be enlarged by observation of new crops and their new pests as well. Monitoring is going on from the beginning of the season to the end of it, from March to the end of November.

Phenology recording The infection pressure of particular pests and the susceptible growth stage of host plants are changing in time. That is why the recording period and its frequency were defined by phenological stages. They were formed regarding the time of unacceptable risk for plant damage when accumulation of infection materials for the next cycle of infection or vegetation can be estimated. In case of the pests, where the risk of damage is not related to certain growth stages, the recording time was determined by the period when appropriate information can be obtained to evaluate risk of damage and the expected consequences.

Data recording Major element of the new PPI system introduced in 1997 is that the excessively detailed recording was replaced by the method of global approach based on general impression. This system is more practical and less time consuming, combined with wide ranging data collection. Simply manageable categories of epidemic dynamics were formed from professional data of many decades. These are compared to the actual plant health status of the crop. The system has been created using basic methods of data recording of valuable professional experiences; it helps determining quantity of pest in an uniform way. Observations take place on representative areas exposed to similar epidemic conditions. In order to estimate the plant health status of a district, the specialist makes record on pest occurrence, first on a fixed observation place, and states infection level with the global approach method. He classifies crop stand for epidemic dynamics on the basis of infection level. After that, the inspector evaluates pest infection in similar way in other, generally 5-10 fields, too compared to the fixed site. With all these, the plant health situation of the district is formed. 83

Method of evaluation Category formation of epidemic and gradation dynamics is needed in order to define the level of infection. These categories were made considering economic thresholds formed by developed forecasting methods. There are 5 categories, infection-free area (the pest has not appeared yet), low (pest occurrence is below the economic threshold) and medium infection level (pest occurrence is increasing), mass outbreak (significant damage of pest) and intensive mass outbreak (increasing damage). Recording is guided by sheets (Figure 1). They are the basis of system operation. On the axis X there are the dates of recordings. On axis Y there are the values for infection categories, giving us a quick help to determine infection categories for recording by the global approach. The infection level observed at the representative site is indicated by the horizontal line.

Fig. 1. Infestation dynamics of Leptinotarsa decemlineata (LEPDE) in 1998

Data transfer, summing up, output Data recordings are done by plant-protection inspectors of county stations who are well aware of the plant health problems in their own district. Number of inspectors varies from 4 to 10 depending on the size of the county, altogether the total number is 125 persons. Inspectors can record data on the spot by using the computerised system on their note- books. After that, they forward the diskette every two weeks to the county stations where data are summed up. County stations send the data to the national central computer using the 84

network. Data processing and summing up are carried out by the Plant Protection Information System 2.0 software having been operated since 1998.

Results

Examples of infection development Different processings can be made by using the PPIS. Status map can provide information on infection/infestation by a pest in a crop at a certain growth stage (Figure 2).Trend map shows infection conditions of more (at maximum four) years or times on a single map sheet and infection development in time can be followed.

Fig. 2. Infestation of Meligethes sp. in rape in 1999

Representation with diagrams is based on the values of average infection in the districts. The statistical analysis refers to the proportion of area in the different infestation categories expressed in % of the cropping area (Figure 3). Opportunity is provided in the system to analyse the monthly meteorological data. Temperature and rainfall maps are suitable for showing the difference among many years’ values. The difference among the values is indicated with difference patterns. Graphs of the monthly data on the actual and many years' temperature and rainfall in a county for the whole year can be drawn. Light and sex traps are operated in county stations to study development of a certain pest. Data on flight activity can be obtained from the recorded data. Catching results can be 85

summed up in maps, charts and graphs (Figure 4.). Daily, five and ten days’ changing of flight activity can be demonstrated also in diagram of flight activity. Several years’ data can be compared in the diagrams. On axis X we can see the time scale, on axis Y, there are the numbers of caught beetles.

Fig. 3. Infestation of Cricetus cricetus in 1998

Fig. 4. Flight activity of Melolontha melolontha in 1997 and in 1998 86

The following data can be reached among the crop protection statistics: treated areas, chemical weed control, weed infestation, qualification of crop stand, qualification of pruning, qualification of emergence, qualification of overwintering, lodging of winter wheat, Lymantria egg masses, frost damage in orchards, foliar fertiliser application, desiccation- defoliation.

Discussion

Uses of information system The PPIS is used for observing the economic threshold. Forecasting officers send information about the plant health situation of their. This information is summed up in the centre, and after that, report of the plant health situation of the country is prepared, which is sent back to the county stations and to the Department for Plant Protection and Agro-environment of Ministry of Agriculture and Regional Development. Forecasts for different time periods for the county and the regions are prepared out of the data at the county stations and are sent to the centre of PPIS for further use. The centre makes country-wide forecasts for short and long terms. In 1998 an opportunity arose to publish communications as „Current problems” about the pest imposing high risk at the moment (mass outbreak) on the the home page of the ministry in the internet. Articles are published regularly in professional journals to provide information about the current plant health situation.

Monitoring epidemics, gradations The system is appropriate for recording the current plant health situation and used for monitoring the pest infection/infestation. It does not contain forecasting, later on development will be needed for forecasting mass outbreaks.

Uses of information The PPIS provide different comparisons and processing which can give information for users, extension services and integrators. In the future it will be the task of these organisations to recommend ready-to-use control measures for farmers based on the data or prognosis of PPIS.

References

Biber, K. & Mohai K. 1997: Növényvédelmi Információs Rendszer, kézirat (in Hungarian) [The Plant Protection Information System, manuscript]. Benedek, P. Surján, J. & Fésűs, J. 1974: Növényvédelmi előrejelzés (in Hungarian) [Forecasting in plant protection]. Balázs, G. & Sáringer, Gy. 1982: [Pests in horticulture]. Kertészeti kártevők (in Hungarian) Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 87-91

Variety as the biological basis of the integrated plant protection

E. Kristof, O. Debreceni National Institute for Agricultural Quality Control, Keleti Karoly u.24., 1024 Budapest, Hungary

Abstract: Resistance of the variety can be used very well by the integrated plant protection. This resistance can be genetically determined but in many cases the growing vigor, revival and adaptability to the environment is a great help to overcome problems of plant protection.

Key words: vegetable, variety, disease resistance, pickling cucumber, Pseudoperonospora cubensis

Introduction

One of the main goals of vegetables breeding is to improve disease resistance of the varieties. The genetically determined disease resistance is a vertical one in general. It means that resistance ensures protection only against certain races or strains of the pathogen. The most disease resistance can be found in tomato varieties. Breeding for resistance has the most success against fungus diseases but good results are achieved against virus and bacterium diseases as well.

Material and methods

During the picking time of the pickling cucumber the chemical treatment is limited by food- hygienics waiting time. Therefore the integrated plant protection and especially selection of the good variety is very important. We examined the infection of the varieties, the yield and the vigor in the comparative trials in Fertőd.

Results and discussion

From practical point of view it is important to know the so called field resistance of the varieties. In case of pickling cucumber downy mildew is a very dangerous disease in Hungary and there are only a few varieties which have genetically determined resistance against Pseudoperonospora cubensis. In field trials it has been proved that there are differences between varieties in susceptibility which is more or less correlated to growing vigor of the plant. Minerva F1: The state of health of this variety is the best, its vigor and yield is the biggest. Accordia F1: The yield was below the average, the vigor was weak in the case of 16,3 % infection. Claudia F1: In the case when the infected leaf area was 20,0 %, the vigor was weaker and the yield was above the average. Nati F1: In the case when the infected leaf area was 22,5 % and the vigor was stronger the yield was under the average.

87 88

Table 1: Existing disease resistance in certain varieties of vegetable species

pepper disease caused by virus bacterium fungus tobamoviruses Phytophtora capsici tobacco mosaic virus tomato mosaic virus bell pepper mosaic virus tobacco mild green mosaic virus dulcamara yellow fleck virus pepper mild mottle virus potato Y virus cucumber mosaic virus

tomato disease caused by virus bacterium fungus tomato mosaic virus strain Pseudomonas tomato Fusarium oxysporum f.sp. 0,1,2 lycopersici tobacco mosaic virus strain Pseudomonas solanacearum Fusarium oxysporum f.sp. 0,1,2,1-2 race 1,2 radicis lycopersici tomato yellow leaf curl virus Clavibacter michiganensis Verticillium alboatrum, subsp. michiganensis Verticillium dahliae tomato spotted wilt virus Cladosporium fulvum race 0, A, B, C, D, E Alternaria solani Phytophtora infestans Stemphylium spp. Pyrenochaeta lycopersici Leveillula taurica Didymella lycopersici Oidium lycopersicum Meloidogyne incognita

cucumber disease caused by virus bacterium fungus cucumber mosaic virus Pseudomonas lachrimans Colletotrichum lagenarium watermelon mosaic virus Cladosporium cucumerinum zucchini yellow mosaic virus Sphaerotheca fuliginea, Erysiphe cichoracearum cucumber vein yellowing Corynespora cubensis virus papaya ring spot virus Pseudoperonospora cubensis

melon disease caused by virus bacterium fungus melon necrotic spot virus watermelon mosaic virus Fusarium oxysporum f.sp. melonis race 0, 1, 2 zucchini yellow mosaic virus Sphaerotheca fuliginea, Erysiphe cichoracearum

watermelon disease caused by virus bacterium fungus Fusarium oxysporum f.sp. niveum race 1,2 Sphaeroheca fuliginea race 1,2 Erysiphe cichoracearum Colletotrichum lagenarium race 1

cabbage disease caused by virus bacterium fungus turnip mosaic virus Xanthomonas campestris pv. Fusarium oxysporum f.sp. campestris conglutinans race 1 cauliflower mosaic virus Alternaria brassicicola Erysiphe communis Peronospora brassicicola

red cabbage disease caused by virus bacterium fungus Fusarium oxysporum f.sp. conglutinans race 1 Erysiphe communis

savoy cabbage disease caused by virus bacterium fungus Xanthomonas campestris pv. Fusarium oxysporum f.sp. campestris conglutinans race 1 Albugo candida

cauliflower disease caused by virus bacterium fungus Erysiphe communis Fusarium oxysporum f.sp. conglutinans race 1 Mycosphaerella brassicicola

kohlrabi disease caused by virus bacterium fungus Fusarium oxysporum f.sp. conglutinans race 1 90

Chinese cabbage disease caused by virus bacterium fungus Fusarium oxysporum f.sp. conglutinans race 1 Erysiphe communis

broccoli disease caused by virus bacterium fungus Fusarium oxysporum f.sp. conglutinans race 1 Peronospora brassicae

brussels sprout disease caused by virus bacterium fungus Fusarium oxysporum f.sp. conglutinans race 1

pea disease caused by virus bacterium fungus seedborne mosaic virus Pseudomonas syringae pv. Fusarium oxysporum f.sp. pisi pisi pea enation mosaic virus Erysiphe pisi Ascochyta pisi race C

bean disease caused by virus bacterium fungus bean mosaic virus Pseudomonas syringae pv. Colletotrichum phaseolicola lindemuthianum Xanthomonas campestris pv. phaseolicola

sweetcorn disease caused by virus bacterium fungus maize dwarf mosaic virus Erwinia stewartii Ustilago majdis Puccinia sorghi Helminthosporium turcicum

carrot disease caused by virus bacterium fungus Cercospora carotae Erysiphe heraclei Alternaria dauci

radish disease caused by virus bacterium fungus Fusarium oxysporum

lettuce disease caused by virus bacterium fungus lettuce mosaic virus Bremia lactucae

spinach disease caused by virus bacterium fungus beet mosaic virus Peronospora spinaciae

Table 2: Differences in susceptibility of some cucumber varieties to Pseudoperonospora cubensis (Vigor: was registered UPOV recommendation; Yield: is given in % of trials average

Variety Infected leaf area % Yield % Vigor (1-9) 1998 1999 Mean 1998 1999 Mean 1998 1999 Mean Minerva F1 12,5 3,0 7,8 107,0 112,0 109,5 8,2 7,9 8,0 Accordia F1 20,0 12,5 16,3 87,0 99,0 93,0 5,6 6,0 5,8 Claudia F1 25,0 15,0 20,0 95,0 111,0 103,0 6,8 6,2 6,0 Nati F1 22,5 22,5 22,5 90,0 109,0 99,5 7,3 6,9 7,1

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 93-94

Vegetable crops, integrated crop management programs and research in central Canada

J. Chaput Ontario Ministry of Agriculture & Food, Guelph, Ontario, Canada

Vegetable crops are an important industry in Canada. The provinces of Ontario and Quebec are the two most important vegetable producing regions. The major vegetables discussed include Alliums, Crucifers, Lettuce and Carrots, however Canadian growers produce significant amounts of tomatoes, potatoes, cucurbits, sweet corn, beans and peas. All vegetables in Canada total about 300,000 acres. Our proximity to the USA is a major factor in both crop management and marketing. The USA has 10 times the acreage that Canada does in major vegetable crops. The Canadian climate is particularly suited to the production of Crucifers, Carrots and Lettuces. Trade with the USA is very important whereas Canadian trade with Europe in vegetables is minimal. Crop management problems however are very similar between Canada and Europe. A review of the ´pest´ complex (insects, diseases, weeds, disorders) for each crop, will reveal many similarities. Development of Integrated Pest Management (IPM) and Integrated Crop Management (ICM) programs has been ongoing for the past 20 years in many vegetables. Despite Canada's large size and varied climatic regions, IPM programs have developed similarly in most provinces. In addition, Canadian researchers, growers and suppliers work closely with colleagues in the USA. Research centers are located in representative regions across Canada, each addressing regional climatic or crop production trends. Research focuses on the same issues as elsewhere, pest monitoring and control, cultivar evaluations, fertility, weed management, biological control, forecasting models and storage management to name a few. Resources for research have been greatly reduced in the past decade. More research is now conducted by private companies or by processing companies. For very small vegetable crops very little research is available unless the growers are well organized. The most recent trend is the move toward developing a more comprehensive 'integrated crop management' approach which takes into account all variables in the production system. This approach requires a team of expertise, a large knowledge base and years to develop. The key aspects of a crop management program include starting with clean, healthy seed and transplants, regular and consistent monitoring using practical tools, understanding all of the possible variables which effect crop growth and development and keeping good records. In Ontario, the provincial government provides some regional IPM information, however field- specific crop scouting is provided by private consultants, grower-hired students or by growers and their families. In other regions of Canada there is more crop monitoring provided by private consultants. Growers pay from $30 to $80 (CAN$) per acre ($75 to $200 per ha) for these services. For IPM practitioners one of the key elements is access to practical and cost-effective monitoring tools. Tools such as sweep nets, sticky traps, trap crops, interception traps, field weather stations and sampling methods each have recognized limitations. Each monitoring tool must be reliable, simple to use and provide timely, useful information to the grower. Access to diagnostic facilities and personnel is also vital. Researchers, pest control product suppliers, extension personnel, growers, scouts, buyers and consumers need to work together

93 94

to help produce healthy vegetable crops. The development of crop production guidelines which incorporate 'ICM' techniques is being adopted in some parts of North America. Currently the major challenges facing vegetable crop managers are soil-borne diseases, nematodes, weed management, eroding research base, unpredictable marketplace and the costs of IPM delivery. Continued collaborative, international research and sharing of ideas is vital to the success of all vegetable producers.

Canadian vegetable websites:

http://www.gov.on.ca/omafra http://res.agr.ca/riche/crdh.html http://aceis.agr.ca/misb/hort/veg.html http://www.gov.mb.ca/agricuIture/crops/wid.html http://www.cisti.nrc.ca/cisti/Rournals/40700/40700e.html http://res.agr.ca/Iond/pmrc/pmrchome.html http://res.agr.ca/harrow/

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 95-102

Possibilities to reduce damage by games in vegetable crops

M. Nádasy & A. Takács Veszprém University of Agricultural Sciences Georgikon FacuIty of Agriculture, 8360 Keszthely, Deák Str. 16 (Hungary)

Abstract: In the Plant Protection Institute of the Veszprém University of Agricultural Sciences, investigations of game repellency began is 1987, motivated by the number of game that substantially exceeded the national average, the severe agricultural and sylvicultural losses caused by game, and the out-of-date and ecologically harmful chemical methods used so far. In the course of the experiments a new ecologically safe technology and game repellents were developed, whereby the action of the products has been prolonged, the environment spared and the expenses of the control reduced. The products have been put into circulation in Hungary, Slovenia and Austria under the nemas VADOC and VADICELL. The most important results of the 10 year experiments are. 1. The products have decreased the extent of damages by 50-80% in agricultural areas and by 40-60% in forest areas. 2. The best effect was achieved in the ease of damages done by rabbits and deers. 3. No good result could be attained with losses caused by wild-hog in autumn. 4. Among the protected crops potato, grape-vine, vegetables, melon, and in spring maize yielded the best results. 5. The size of the area influences the success of control; on an area of 1-2 ha the damage by game was below 20%, while on areas larger than that a mere 50% result was obtained. 6. After 14 days the game gets used to the smell, the products must therefore be changed. 7. The experiments will be continued with the following objectives. 8. Developing a new carrier; namely, the effect of perlite has left much to be desired. 9. Placing new game repellents on the market in order to increase the efficiency of protection (to achieve a minimum 10% reduction of damages), and growing the number of products so as to make their change easier VADUK, our new product will be licensed this year in Hungary.

Key words: Game deterring, plant protection, environment

Introduction

In consequence of the rising number of game (deer, roe-deer, wild-hog) in Hungary damages caused by game have recently increased in a considerable measure in forest- and agricultural areas alike. Protection from damages done by game is therefore an absolute requirement. The new hunting law which prescribes for the owner to protect his land from damages done by game as well as the number of small farms grown after the change of regime encourage the game control.

Literary review

The methods of protection from damages done by game can be divided in direct und indirect techniques. The indirect control methods include the regulation of the number of wild animals, feeding, establishment of game lands, etc. These are common tasks of all foresters and agriculturists (Kölüs, 1986; Nagy, 1990).

95 96

The direct methods can be either individual for area protection. Individual protection is recommended for crops of high value, since it involves expensive procedures. The area protection is cheaper, it is used first of all to protect field crops, The methods can be mechanical, biological and chemical ones (Köhalmy, 1994; Walterné, 1991).

Materials and methods

In our Institute we have studied chemical techniques for ten years (1988-1998). The earlier methods did not fulfil the requirements in Hungary. Preparations sprayed or placed out with pieces of textile soaked in them remained active only for a couple of days und contaminated the environment. The workers of our Institute (Nádasy et al., 1992) have elaborated a new technology whereby the preparations' efficiency increases, the expenses decrease and the environment will not be contaminated (Nádasy et al., 1990, 1994). In the course of the experiments two new products VADICELL and VADÓC were put in circulation. Besides Hungary experiments were carried on in Slovenia and Austria where the products are at present in process of licensing (Table 1). The experiments were set up in almost all important crops in forest- and agricultural areas (Table 2).

Table 1. Sites of the game repellency experiments (1987-1997)

Hungary Forestries BEFAG (Keszthely, Pápa, Sümeg, Ugod, Bakonybél, Farkasgyepü, Monostorapáti), VERGA (Veszprém, Zirc, Ajka), ZEFAG (Nagykanizsa, Lenti, Csömödér, Letenye, Bak), SEFAG (Szántód, Kaposvár, Iharosberény, Lábod, Marcali, Nagyatád), Gemenc, Baja, Sopromi Tanulmányi Erdögazdaság (Iván), Pilisi Erdögazdaság (Visegrád) State Farms 70 (Balatonboglár, Balatonfenyves, Siófok, Bak, Mezöhegyes, Szarvas, Orosháza, Gyomaendröd, Bölcske, Paks, Pusztaszabolcs, Nemesgulács, Kisgörbö, Bajánsenye, Somogybabod, Veszprémvarsány, Barcs) Hunting companies 30 (Hubertus, Nimród) Research Institute PATE, Kertészeti Egyetem, Iregszemcse, Szeged Gabonamag, Jászboldogháza, Sopronhorpács, Pölöske) Private Farms 100 Austria Burgenland, St. Pölten, Amsteten Slovenia Ljubljana, Kocevje, Bled, Zalec, Lendva, Muraszombat USA Virginia – Blackburg Ohio – Sanduky 97

Table 2. Crops (1986-1997)

wheat, barley, maize, potato, sugar-beet, lucerne, bean, pea, sunflower, lettuce, carrot, tomato, paprika, melon, vegetable marrow, Agriculture apple, apricot, grape-vine, strawberry, raspberry, meadow-pasture, forestry acorn sowing, nursery Forestry oak, beech, pine, poplar

Results of experiments

The results of the past 10 years are shown in Fig. 1. From the data of Fig. 1 the following can be established: − The VADICELL and VADÓC considerably reduced in all crops the extent of damage done by game, the latter being a mere 10-20% after 14 days on the protected areas. − The VADÓC proved more effective than the VADICELL. − The worst result was obtained for maize in autumn, when the damage done by game (deers and wild-hogs) was nearly 50% in spite of the control. − The products were sufficiently active for 14 days. In the case of permanent protection (e.g. in potato) the products should be changed after this period (VADICELL is replaced by VADÓC). The results of the experiment carried out in forestries are shown in Fig. 2. As seen from the data of Fig 2 the technology elaborated by us was less efficient in forests the effect of VADÓC was a mere 70%. In forestry the products need be regularly changed which is not an economical procedure. − In the case of acorn sowings the method is ineffective, so it is not recommended. − The wild animals give different responses to out technology, as seen in Fig. 3. Accordingly: − The best results was obtained for hare in autumn and for deer and wild-hog in spring. − In autumn the effect of our method was low on deer (owing to the troating of hart) and on wild-hog (damages done by game came near to 60%). In that season good results can therefore be attained only by the joint application of several methods (regulation of the number of wild animals, mechanical techniques, use of electrical fence). The size of the area influences the success of control (Fig. 4 ). The smaller the area the better result can be attained by the olfactory effect of our area protection technology. The optimum size of area is 5 ha. In the case of areas larger than 10 ha we suggest a mosaic-like arrangement of the bags put on the plants inside the area. The data of the tables show that the technology and products (VADICELL, VADÓC) of game repellency developed by us considerably decreased the extent of damages done by game both in Hungary and Slovenia and Austria. Our method has, however, minor deficiencies (change of products, amount materials). Therefore to eliminate them we set the following tasks 1. to develop a new carrier 2. to develop a new game repellent. 98

Fig. 1. Effectiveness of Vadicell and Vadóc on the 14th day in the average of the past 10 years (1986 - 1996) experiments.

Out of the carriers used so far the production of MAVICELL has ceased in Hungary, the perlite, on the other hand, has left much to be required (absorbing capacity). We therefore decided to elaborate a new carrier. One of the possibilities is to use a wooden plate, of which we gave account last year at the Gent conference (Nádasy & Bürgés, 1997). 99

Fig. 2. Effectiveness of VADICELL and VADÓC on the 14th day in forestry of the past 10 years' (1986-1996) experiments

Fig. 3. Percentage damage of various game species on the 14th day in spring and autumn

Development of a new game repellent After 14 days the game repellents need be changed. The species of game give different responses to the game repellents. It is therefore necessary to put as many game repellents as possible in circulation. Our Institute has recently succeeded in developing a new product which in 1998 may be commercially available in Hungary under the name VADUK. The results of experiments carried out with VADUK are contained in Fig. 5. 100

The data of Fig. 5. show that the VADUK displays a good repelling effect (80 to 90 per cent on the 14th day). Its effect is similar to that of VADÓC, its use in the future is therefore definitely recommended.

Fig. 4. Trend of damages done by game on areas of different size on the 14th day of control

Put-up of game repellents The game repellents stored in plastic sheet have an unpleasant odour, therefore they cannot be stored but must be immediately put out on the area. From 1998 on the Keszthely company VAD BT. puts the product in circulation in aluminium foil whereby these disadvantages can be eliminated. Each foil contains 10, 30 or 100 plastic bags according to demand: Finally, it must be noted that the success of game repellency is fundamentally influenced by the human attitude. Success can be attained only by the observance of the technological discipline, the cooperation of foresters and agriculturists and the joint application of the different methods.

References

Köhalmy, T. (1994): Vadászati enciklopédia. Mezögazdasági Kiadó, Budapest, 47-80. Kölüs, G. (1986): Vadgondozás, élöhelygazdálkodás. Mezögazdasági Kiadó, Budapest. Nádasy, M. & Bürgés, Gy. (1997): New technology of game repellency in Hungary. Mededelingen 49th International Symposium on Crop Protection Gent, II. 523-531. Nádasy, M., Szabolcs, J., Bozai, J., Baár, J. & Gimesi, 1. (1990): Új környezetkimélö vadriasztó technológia a vadkárok mérséklése céljából. Növényvédelem, 26: 215-216. Nádasy, M., Szabolcs, J., Rábai, J. & Takács, A. (1992): A new environment protective wild reppelent technology. Med. Fac. Landbouww. Univ. Gent, 57-62. Nádasy, M., Szabolcs, J., Takács, A. & Rábai, J. (1994): Új perspektivikus környezetkimélö vadriasztó készitmények: Vadicell és Vadóc alkalmazási lehetöségei erdö- és mezögazdasági területeken. Növényvédelem, 3: 138-144. 101

Fig. 5. Results of experiments with the game repellents VADÓC and VADUK in 1995-1997 102

Nagy, I. (1990): A nagyvad által okozott károk és elháritási lehetöségeik. Diplomadolgozat, Keszthely. Walterné, Illés V. (1991): A vadkár II. Venatus Lap- és Könyvkiadó Kereskedelmi Kft. Szentendre, 13-56.

103

Ecology of Pest Insects

104

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 103-108

Host-plant selection by insects – the “Missing Link”

S. Finch & R. H. Collier Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK

Abstract: Characteristic plant odours (volatile chemicals) are credited with the major role of guiding phytophagous insects to their host plants. Studies indicated that the central “missing” link in host-plant selection depends on visual, not chemical, stimuli, and is regulated by "appropriate/inappropriate" landings in which the insects land indiscriminately on green, but avoid brown, surfaces. Hence, more insects accumulate on host-plants surrounded by bare soil than on plants surrounded by green non-host plants. Five earlier mechanisms of host-plant selection, and two general hypotheses are discounted. The current mechanism explains also why host-plants growing amongst natural vegetation are not decimated by phytophagous insects.

Key words: Undersowing, visual stimuli, diverse backgrounds, volatile stimuli

Introduction

Many researchers have shown that the numbers of phytophagous insects found on crop plants are reduced considerably when the background of the crop is allowed to become weedy (Dempster, 1969; Smith, 1969; Dempster & Coaker, 1974; Smith, 1976), when the crop is intercropped with another plant species (Ryan et al.,1980; Tukahirwa & Coaker, 1982; Altieri, 1994), or when the crop is undersown with a living mulch (Theunissen & Den Ouden, 1980; Theunissen et al., 1995). It has been suggested that diverse backgrounds prevent insects from finding otherwise- acceptable host plants, i) by the non-host plants physically impeding the searching insects (Perrin, 1977), ii) by visual camouflage (Feeny, 1976; Smith, 1976); iii) by root exudates from the non-host plants altering the physiology of the host-plant ( Theunissen et al., 1995); iv) by odours of the non-host plants directly deterring the searching insect (Uvah & Coaker, 1984); or v) by the odours of the non-host plants "masking" those of the host plant (Tahvanainen & Root, 1972). Two general hypotheses, have also been proposed to explain these reductions in insect numbers. The "resource concentration hypothesis" (Root, 1973), which proposes that more insects are found where the "resource" (host plants) is most concentrated and the "enemies hypothesis" (Root, 1973), which proposes that fewer phytophagous insects are recovered from host-plants growing in diverse backgrounds, because many of the pest-insects are eaten by the higher numbers of predators also arrested at such sites.

Experimental work

Laboratory and field experiments were done to determine how growing cabbage plants (Brassica oleraceae var. capitata Alep.) (Cruciferae) in backgrounds of bare soil and subterranean clover (Trifolium subterraneum L.) (Papilionaceae), affected host-plant finding by eight pest species belonging to four insect orders (Kienegger & Finch, 1996). The insects tested were the small white butterfly (Pieris rapae), the large white butterfly (P. brassicae), the cabbage root fly (Delia radicum), the mustard beetle (Phaedon cochleariae), the diamond-back moth (Plutella xylostella), the garden pebble moth (Evergestis forficalis), the cabbage moth (Mamestra brassicae) and the cabbage aphid (Brevicoryne brassicae) (Kienegger & Finch, 1996).

103 104

All insects were produced in the Insect Rearing Unit at HRI Wellesbourne. 30-200 insects were used per replicate in each experiment. The cabbage plants were grown in 7.5cm pots, tested at the "five true-leaf" stage, and left in their pots throughout the experiments. The laboratory experiments were done in a large rotating cage or in smaller Perspex® cages. The rotating cage (160 cm x 160 cm x 63 cm high) contained a 145 cm diameter turntable, which rotated once every four minutes (Ellis & Hardman, 1975). The rotation ensured that all treatments placed on the turntables were exposed equally to the insects, which aggregated near the strip lights used to illuminate the test chamber. The Perspex® cages were sufficiently large (80 cm x 48 cm x 54 cm) to house one seed-tray of clover and one of soil. Field experiments were done in large (600 cm x 315 cm x 180 cm high) cages and in the open field. In each laboratory test, a pot containing a test plant was inserted in the centre of each seed- tray of clover or bare soil. In each field-cage, 32 host plants were arranged, at 50 cm spacing, in four rows of eight plants; alternate plants being surrounded by either clover or bare soil. Most experiments lasted five to ten days and involved at least 10 replicates. The insect eggs were counted daily. To reduce bias, host-plants removed from one background were placed into the opposite background when re-introduced into a test cage. The field experiments were done using sixteen 25m2 plots, arranged as a 4x 4 Latin square. The four treatments, each replicated 4 times, were undersowing with two species of clover and two bare soil treatments, one subjected to the full pesticide schedule and the other without pesticide. In all experiments, fewer (P=0.05) insect eggs were laid on cabbage plants (15-20 cm tall) surrounded by green clover (10-12 cm tall) than on similar plants surrounded by bare soil (Finch & Kienegger, 1997). The percentage reductions for all eight test species ranged from 39±5% for the diamond-back moth to 94±3% for the cabbage moth (Finch & Kienegger, 1997). When the small white butterfly was presented with cabbage plants of different sizes, the clover (10-12cm tall) only reduced the numbers of eggs laid by 48±4% around 25 cm tall cabbage plants and had no effect around 35 cm tall plants. In addition, the numbers of eggs laid by the cabbage root fly, the diamond-back moth and the large white butterfly on host plants growing in brown (dead) clover (230±33, 87±9 & 98±15, respectively) did not differ (P=0.05) from those laid (255±46, 81±9 & 94±14, respectively) on host-plants growing in bare soil (Finch & Kienegger, 1997).

Discussion of earlier hypotheses

Although several authors have indicated that diverse backgrounds affected host-plant selection in the ways described earlier, from the above results and published data (Cromartie, 1981; Andow, 1991; Altieri, 1994), it is hard to refute the view that all species are affected similarly. Of the earlier mechanisms, "visual camouflage" implied "concealing an object" (Feeny, 1976; Smith, 1976), whereas our proposed mechanism (see later) is dependent on all surfaces being clearly visible to the searching insect. Physical interference (Feeny, 1976; Smith, 1976) does not appear to make a great contribution, since the brown clover had the same plant architecture as the green clover but did not deter the searching insects. Similarly, as the test plants were left in their pots throughout the experiments, root exudates from the non-host plants could not cause physiological changes in the host plants (Theunissen et al., 1995). In addition, no evidence has been produced during the last 13 years to show that the non-host plants produce their effects through chemical deterrence (Uvah & Coaker, 1984). Even background plantings of sage (Dover, 1985), thyme (Dover, 1985) and onions (Uvah & Coaker, 1984), selected for their pungent odours, failed to deter insects from landing on host plants. The host-plant odour being "masked" by that of the non-host plant (Tahvanainen & Root, 1972) is also untenable, as similar effects were produced in the case of the cabbage root fly when its host plants were surrounded by weeds (Feeny, 1976; Smith, 1976), spurrey (Spergula arvensis) (Theunissen & Schelling, 1996), 105

peas (Pisum sativum) (Kostal & Finch, 1994), or clover (Theunissen et al., 1992 & 1995; Finch & Kienegger, 1997), all of which have different odour profiles. Furthermore, the same effect was produced when host plants were surrounded by green plant models (Finch & Kienegger, 1997), or sheets of green paper (Ryan et al., 1980; Kostal & Finch, 1994; Finch & Kienegger, 1997), neither of which release plant odours. The observed differences cannot be explained by the "resource concentration hypothesis" (Root, 1973), as the host plants are at the same density in both situations. Similarly, the "enemies hypothesis" (Root, 1973) is difficult to suppport, as it would be against established principles, for more predators to be found on host-plants in clover when most prey were on host-plants in bare soil. Contrary to earlier claims, differences in colonization alone (Cromartie, 1981; Dover, 1986; Altieri, 1994) can explain why fewer pest- insects are arrested when host plants are grown in diverse backgrounds.

New hypothesis

We propose that a mechanism based on "appropriate/inappropriate landings" (Finch, 1996) is the “missing (central) link” in host-plant selection. The complete system consists of a chain of actions in which volatile plant chemicals indicate to receptive insects that they are flying over host-plants. As such chemicals are not released in amounts sufficient to provide accurate directional information (Finch, 1980), they simply stimulate the insects to land. Two types of visual stimuli then determine where the insect lands. The first is a directed response to the colour of the plant, or phototaxis (Moericke 1952), and the second an optomotor response, in which landing is provoked by plants “looming up" along the path of the flying insect (Kennedy et al., 1961). The overall system is much simpler than the previous hypotheses, as the first directed response is merely to the colour green and the optomotor reaction is to any silhouettte, not just a living plant. The component required to complete the system is that pest insects rarely land on soil (Prokopy et al., 1983; Kostal & Finch, 1996; Finch & Kienegger, 1997). Consequently, when insects flying over plants growing in bare soil are stimulated to land, the only green objects are host plants, and hence most landings are "appropriate". Once on a leaf surface, chemical cues become important (Fraenkel, 1959; Dethier, 1970) and, provided the insect receives appropriate stimulation through its tarsal receptors or mouthparts, it will remain on the plant. If the insect is not arrested, the process is repeated. In the contrasting situation, insects flying over host plants surrounded by other plants land in proportion to the relative areas occupied by the two plant types, as phytophagous insects land on any green surface (Kennedy et al., 1961; Prokopy et al., 1983; Kostal & Finch, 1996). Consequently, many landings are "inappropriate" and the insects then fly off. Even insects that make "appropriate" landings are not guaranteed success, as many insects move from leaf-to-leaf to accumulate sufficient positive stimuli before accepting the plant as a suitable oviposition site. If at any stage during this process the leaves are not sufficiently stimulating, or the insect lands on a non-host leaf, the insect leaves the area. Of 100 landings made by female cabbage root flies, only 7% of the females laid on the brassica plants in the clover, because of the frequent loss of contact with the host plant, compared to 36% on the brassica plants in the bare soil (Kostal & Finch, 1994). The proposed mechanism applies also to host-plant selection by night-flying insects, as if such insects land mainly in response to silhouettes (Kennedy et al., 1961), even dead clover should reduce the number of "appropriate" landings. As a result of this simple mechanism, more insects accumulate on host-plants growing in bare soil than on those growing in diverse backgrounds. This mechanism also explains why relatively few pest-insects are found on wild host-plants growing amongst natural vegetation.

106

General discussion

The evidence to support volatile chemicals being involved during the central link is weak. The maximum distance recorded for insect orientation to host-plant volatiles in the field is only a few metres (Hawkes, 1974; Hawkes & Coaker, 1979; Finch, 1980). The amounts of volatile chemical needed to induce directed responses are invariably several orders of magnitude greater than those released naturally (Finch, 1980). For example, in wind tunnel experiments, cabbage root fly flew upwind when host-plant odour was released at 2.5g/day (Hawkes & Coaker, 1979), an amount at least 105 times higher than that given off by a healthy brassica plant (Finch, 1980). Furthermore, although the receptive flies moved towards the odour source, the results were unexpected (Hawkes & Coaker, 1979), as more than 90% of the "flights" were shorter than 50cm (Hawkes & Coaker, 1979). Such behaviour suggests that the cue from volatile plant chemicals is to stimulate the insects to land. Finally, even when large amounts of volatile host-plant chemicals are released from insect traps in the field, many of the insects miss the trap on landing (Finch, 1980; Prokopy et al., 1983) and do not enter subsequently (Prokopy et al., 1983, Finch, 1995; Kostal & Finch, 1996), a further indication that such chemicals are arrestants rather than attractants. The proposed hypothesis, which includes the "appropriate/inappropriate landings" mechanism, seems more convincing than those based solely on chemical cues. In addition, disruptive air movements around host plants (Wilson, 1970; Murlis et al.,1992), the small amounts of volatile chemical released (Finch, 1980), the short distance over which the insect responds (Finch, 1995), the closing speed of the flying insect (Finch, 1980), and the fact that many receptive insects miss the "target" (Finch, 1980; Prokopy et al., 1983; Kostal & Finch, 1996), all suggest that the central link in host-plant finding is not governed by volatile chemicals. The great selective and exploitable advantage of the proposed hypothesis is that once an insect lands, it has circumvented the major difficulty of obtaining directional cues from plant odours while still in flight (Wilson, 1970; Murlis et al.,1992). Therefore, as visual stimuli appear to be critical to the central link of host-plant selection, there should be an infinite number of plant combinations that could be used to reduce the numbers of pest insects arrested in cultivated crops. To ensure that a high proportion of the searching insects land on non-host plants under field situations, the foliage of both plant types must be in the insects' field of vision at the time it lands. Hence, the relative height of the two plant types is crucial if intercropping/undersowing is to be used as a method of crop protection. When the silhouette of the host plant is made obvious, by mowing the intercrop (non-host plant) to reduce plant competition (Theunissen & Den Ouden, 1980; Theunissen et al., 1995; Finch & Kienegger, 1997) or by allowing the host plants to protrude well above the background crop (Finch & Kienegger, 1997), any crop protection benefit will be lost.

Acknowledgement

We thank the UK Ministry of Agriculture, Fisheries and Food (Contact: Dr Sue Popple) for supporting this work as part of Project HH1815SFV

References

Altieri, M.A., 1994. Biodiversity and Pest Management in Agroecosystems. Haworth Press Inc., New York, 185 pp. Andow, D.A., 1991. Vegetational diversity and arthropod population response. Annual Review of Entomology 36: 561-586. 107

Cromartie, W.J.Jr., 1981. The environmental control of insects using crop diversity. In: D. Pimentel (ed.), CRC Handbook of Pest Management in Agriculture, Volume 1. CRC Press Inc., Boca Raton, Florida: 223-251. Dempster, J.P., 1969. Some effects of weed control on the numbers of the small cabbage white (Pieris rapae L.) on Brussels sprouts. Journal of Applied Ecology 6: 339-345. Dempster, J.P. & T.H. Coaker, 1974. Diversification of crop ecosystems as a means of controlling pests. In: D. Price Jones & M.E. Solomon (eds.), Biology in Pest and Disease Control. John Wiley & Sons, New York: 106-114. Dethier, V.G., 1970. Chemical interactions between plants and insects. In: E. Sondheimer & J.B. Simeone (eds.), Chemical Ecology. Academic Press, New York & London: 83-102. Dover, J.W., 1985. The responses of some Lepidoptera to labiate herb and white clover extracts. Entomologia Experimentalis et Applicata 39: 177-182. Dover, J.W., 1986. The effect of labiate herbs and white clover on Plutella xylostella oviposition. Entomologia Experimentalis et Applicata 42: 243-247. Ellis, P.R. & J.A. Hardman, 1975. Laboratory methods for studying non-preference resistance to cabbage root fly in cruciferous crops. Annals of Applied Biology 79: 253-264. Feeny, P.P., 1976. Plant apparency and chemical defence. In: J. Wallace & R. Mansell (eds.), Biochemical Interactions Between Plants and Insects. Recent Advances in Phytochemistry 10: 1-40. Finch, S., 1980. Chemical attraction of plant-feeding insects to plants. In: T.H. Coaker (ed.), Applied Biology V, Academic Press, London & New York: 67-143. Finch, S., 1995. Effect of trap background on cabbage root fly landing and capture. Entomologia Experimentalis et Applicata 74: 201-208. Finch, S., 1996. "Appropriate/inappropriate landings", a mechanism for describing how undersowing with clover affects host-plant selection by pest insects of brassica crops. IOBC WPRS Bulletin 19(11): 102-106. Finch, S. & M. Kienegger, 1997. A behavioural study to help clarify how undersowing with clover affects host-plant selection by pest insects of brassica crops. Entomologia Experimentalis et Applicata 84:165-172. Fraenkel, G.S., 1959. The raison d’être of secondary plant substances. Science 129, 1466-1470. Hawkes, C. 1974. Dispersal of adult cabbage root fly (Erioischia brassicae (Bouché)) in relation to a brassica crop. Journal of Applied Ecology 11: 83-93. Hawkes, C. & T.H. Coaker, 1979. Factors affecting the behavioural responses of the adult cabbage root fly, Delia brassicae, to host-plant odour. Entomologia Experimentalis et Applicata 25: 45-58. Kennedy, J.S., Booth, C.O. & W.J.S. Kershaw, 1961. Host finding by aphids in the field. III. Visual attraction. Annals of Applied Biology 49: 1-21. Kienegger, M. & S. Finch, 1996. The effect of undersowing with clover on host-plant selection by pest insects of brassica crops. IOBC WPRS Bulletin 19(11): 108-114. Kostal, V. & S. Finch, 1994. Influence of background on host-plant selection and subsequent oviposition by the cabbage root fly (Delia radicum). Entomologia Experimentalis et Applicata 70: 153-163. Kostal, V. & S. Finch, 1996. Preference of the cabbage root fly, Delia radicum (L), for coloured traps: influence of sex and physiological status of the flies, trap background and experimental design. Physiological Entomology 21: 123-130. Moericke, V. 1952. Farben als Landereize für geflügelte Blattläuse (Aphidoidea). Zeitschrift für Naturforschung 7: 304-324. Murlis, J., Elkington, J.S. & Cardé, R.T., 1992. Odour plumes and how insects use them. Annual Review of Entomology 37: 505-532. 108

Perrin, R.M., 1977. Pest management in multiple cropping systems. Agro-ecosystems 3: 93-118. Prokopy, R.J., Collier, R.H. & Finch, S. 1983. Visual detection of host plants by cabbage root flies. Entomologia Experimentalis et Applicata 34: 85-89. Root, R.B., 1973. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monograph 43: 95-124. Ryan, J., M.F. Ryan & F. McNaeidhe, 1980. The effect of interrow plant cover on populations of cabbage root fly, Delia brassicae (Wied.). Journal of Applied Ecology 17: 31-40. Smith, J.G., 1969. Some effects of crop background on the populations of aphids and their natural enemies on Brussels sprouts. Annals of Applied Biology 63: 326-330. Smith, J.G., 1976. Influence of crop backgrounds on aphids and other phytophagous insects on Brussels sprouts. Annals of Applied Biology 83: 1-13. Tahvanainen, J.O. & R.B. Root, 1972. The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta crucifera (Coleoptera: Chrysomelidae). Oecologia 10: 321-346. Theunissen, J. & H. Den Ouden, 1980. Effects of intercropping with Spergula arvensis on pests of Brussels sprouts. Entomologia Experimentalis et Applicata 27: 260-268. Theunissen, J. & G. Schelling, 1996. Undersowing crops of white cabbage with strawberry clover and spurrey. IOBC WPRS Bulletin 19(11): 128-135. Theunissen, J., C.J.H. Booij & L.A.P. Lotz, 1995. Effects of intercropping white cabbage with clovers on pest infestation and yield. Entomologia Experimentalis et Applicata 74: 7-16. Theunissen, J., C.J.H. Booij, G. Schelling & J. Noorlander, 1992. Intercropping white cabbage with clover. IOBC WPRS Bulletin 15 (4): 104-114. Tukahirwa, E.M. & T.H. Coaker, 1982. Effects of mixed cropping on some insect pests of brassicas; reduced Brevicoryne brassicae infestations and influences of epigeal predators and the disturbance of oviposition behaviour in Delia brassicae. Entomologia Experimentalis et Applicata 32: 129-140. Uvah, I.I.I. & T.H. Coaker, 1984. Effect of mixed cropping on some insect pests of carrots and onions. Entomologia Experimentalis et Applicata 36: 159-167. Wilson, E.O., 1970. Chemical communication within animal species. In: E. Sondheimer & J.B. Simeone (eds.), Chemical Ecology. Academic Press, New York & London: 133-155. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 109-112

Oviposition preference of carrot psyllid (Trioza apicalis) on different carrot varieties

A. Nissinen,1 P. Kainulainen,2 A. Piirainen,3 K. Tiilikkala,1 & J.K. Holopainen2,1

1 Agricultural Research Centre of Finland, Plant Protection, 31600 Jokioinen, Finland 2 Department of Ecology and Environmental Science, University of Kuopio, P.O. Box 1627, 70211 Kuopio, Finland 3 University of Helsinki, Mikkeli Institute for Rural Research and Training, Lönnrotinkatu 3-5, 50100 Mikkeli, Finland

Abstract: Especially in northern Europe carrot psyllid (Trioza apicalis Förster), which is a carrot specialist, can cause serious damage to carrot cultivations. Adult psyllids cause curling of the leaves by injecting saliva to carrot during feeding. Nymphal feeding results in reduction of root growth. Oviposition preference of the carrot psyllid was studied on four different carrot varieties: Napoli, Panther, Parano, and Splendid. In both oviposition experiments the number of eggs laid per variety varied greatly thus no significant differences was found between the varieties. However, the least preferred variety in both experiments was Splendid. There was a negative linear correlation between limonene concentration in the leaves and total number of eggs laid on carrot variety. Our observations are in agreement with the earlier findings that limonene may act as repellent against the carrot psyllid.

Keywords: Daucus carota, Trioza apicalis, host-plant selection, oviposition behaviour

Introduction

The carrot psyllid is a severe pest in northern Europe. It overwinters on conifers, especially on Norway spruce (Picea abies) (Láska 1976, Rygg 1977, Valterová et. al. 1997). In early summer adult psyllids migrate from spruce to carrot fields. The damage caused by overwintered adults is considered to be the most severe. Adult psyllids inject phytotoxic saliva, which causes the curling of the leaves, to the carrot while feeding. Symptoms become visible on average within two days after infestation. If the seedlings are young one carrot psyllid per plant is enough to cause a total loss of yield. The damage of nyphal feeding is nonsystemic, but it results in reduction of root growth (Markkula et. al. 1976). Burckhardt (1985) mentions carrot (Daucus carota), parsley (Petroselinum crispum), and caraway (Carum carvi) as host plants of the carrot psyllid. According to Nehlin et. al. (1996) caraway belonged however to unfavoured group of host plants even though curling of the leaves occurred in those plants and carrot psyllids were able to develop into adults on them. Valterova et. al. (1997) showed that carrot psyllid prefers carrots, both cultivated varieties and wild carrot, among umbelliferous plants. They also showed that high limonene concentration in leaves might contribute to the host plant selection of carrot psyllid. The aim of this study was to find out whether carrot psyllid has any host plant preference among commonly cultivated carrot varieties.

109 110

Materials and methods

Four carrot varieties: Napoli, Panther, Parano and Splendid were tested in two oviposition experiments. For the first experiment seedlings of the carrots were grown on an organic farm in sandy soil, under polypropene fleece. Four seedlings of each variety per pot were potted in pots of 1.1 litres and moved to greenhouse. Four pots representing different varieties were placed in each cage in randomised order. Number of cages included in this experiment was ten. Carrot psyllids were collected from the same farm as the carrot seedlings. Seedlings were five weeks old when the experiment was started. Two pairs (two females and two males) of carrot psyllids were released in the middle of each cage. The psyllids were allowed to lay eggs for four days after which the eggs were counted under a microscope. The second oviposition test was conducted with the same varieties than the first test, but this time the plant material was grown in greenhouse under natural light period (22 hours light, 2 hours dark). Carrot seed were sown in slightly fertilised peat-sand mixture (Kekkilä TH1) in pots of 1.1 litres. All the four carrot varieties were sown in each pot. One variety was sown in each corner of the pot in randomised order. Three seedlings per variety were allowed to grow in each pot. The carrot seedlings were four weeks old when the experiment started. In the second experiment 18 replicates were included. Carrot psyllids were from the same origin as in the previous experiment. Two carrot psyllids (one female and one male) were released in each cage from an eppendorf tube, which was placed in the middle of each pot. Similarly to the first experiment, carrot psyllids were allowed to lay eggs for four days before the eggs were counted. For the chemical analyses about 20 seeds per variety were sown per pot (1.1 L). Seedlings were grown under natural light period (16 hours light, 8 hours dark) in greenhouse. Six-week-old carrot leaflets were collected for analysis. After hexane extraction samples were analysed with GC-MS as earlier (Kainulainen et. al. 1998).

Results

In the first oviposition test Parano was the most preferred variety and Splendid the least preferred variety (Table 1). In the second experiment the highest number of eggs was laid on Napoli and again the lowest number of eggs on Splendid. The number of eggs laid per variety varied greatly in both experiments, thus no significant difference (p>0.05) was found between varieties.

Table 1. The mean number of eggs of Trioza apicalis laid on different carrot varieties in two oviposition tests.

Variety Number of eggs, Number of eggs, 1st experiment (n=10) 2nd experiment (n=18) Napoli 9,95 7,48 Pather 9,15 5,65 Parano 13,15 4,09 Splendid 2,28 2,26

111

The essential oil composition was typical for each carrot variety and there was a significant difference in concentrations of some individual monoterpenes between varieties (Kainulainen et. al. in preparation). The total concentration of some terpenoids was highest in Parano and Splendid. The main monoterpene in all the varieties was myrcene. Sabinene was typical compound for Parano, and limonene concentration was highest in Splendid In both experiments a linear negative correlation was found between limonene concentration of the leaflets and the number of eggs laid per variety. In first experiment also sabinene-limonene ratio and sabinene-alfa-pinene ratio highly explained the number of eggs laid, but in second experiment no such correlations was found.

Discussion

According to observations made during the experiments oviposition behaviour of the carrot psyllid is aggregated. When the female has chosen a suitable host plant it can spend a few days on the same plant laying several dozens eggs on that plant before moving to next plant. Thus the number of eggs per single plant ranged from 0 to 137. This distribution pattern of eggs makes the statistical analyses difficult because of high standard deviation. Thus more replicates would have needed to obtain reliable differences between varieties. However, the fact that Splendid remains the least preferred variety in both experiments may suggest that the carrot psyllid has host plant selection not only among umbelliferous plants but also among cultivated carrot varieties. Kainulainen et. al. (1998) showed that there is a high variation in secondary compound composition among different carrot varieties which might affect the host plant selection of carrot psyllid. Both the Norway spruce and the carrot release large amounts of monoterpenes, but in different proportions (Borg-Karlson et. al. 1993, Persson et. al. 1996, Nehlin et. al. 1996, Valterova et. al. 1997, Kainulainen et. al.1998). Thus, most probably, the taxon specific combination of terpenes is the essential host recognition cue for the carrot psyllid (Valterová et. al. 1997). The negative linear correlation found between limonene concentration and number of eggs laid supports earlier findings of Nehlin et. al. (1994) and Valterová et. al. (1997) which suggest that limonene in high concentration is a repellent to the carrot psyllid. Valterová et. al. (1997) showed that carrots, which were the most attractive species of Apiacea to carrot psyllids, had high concentration of sabinene and alfa-pinene. Controversially, in this study concentrations of alfa-pinene and sabinene were relatively low compared to myrcene concentarion in the studied varieties. Even though it seems that limonene is a repellent to carrot psyllid the role of sabinene and alfa-pinene remains unclear. Thus, further research should clarify the role of other terpenoids and their relative proportions in the host plant selection of the carrot psyllid. Our earlier observations have shown that the damage of carrot psyllid is concentrated at the field edges (Nissinen et. al. unpublished). Because of this distribution of the damage, it might be possible to control carrot psyllids by providing them with a susceptible carrot variety first at the field edge and using the least preferred varieties as crop plants further inside the field. Before this push and pull strategy could be utilised as a control method, several carrot varieties should be screened to find the most susceptible and the most resistant carrot varieties to the carrot psyllid.

112

References

Borg-Karlson, A.-K., Lindsröm, M., Norin, T. Persson, M. & Valterová, I. 1993: Enantiomeric composition of monoterpenehydrocarbons in different tissues of Norway spruce, Picea abies (L.) Karst. A multi-dimensional gas chromatography study. Acta Chem. Scan. 47: 138-144. Burckhard, D. 1985: Taxonomy and host plant relationships of the Trioza apicalis Förster complex (Hemiptera, Homoptera: Triozidae) Ent. Scand. 47:138-144. Láska, P. 1974: Studie über den Möhrenblattfloh (Trioza apicalis Först.) (Triozidae, Homoptera). Acta Sc. Nat. Brno 8(1):1-44. Kainulainen, P.; Tarhanen, J.; Tiilikkala, K.; Holopainen, J.K. 1998: Foliar and emission composition of essential oil in two carrot varieties. J. Agric. Food Chem. 46: 3780-3784. Markkula, M., Laurema, S. & Tiittanen, K. 1976: Systemic damage caused by Trioza apicalis on carrot. Symp. Biol. Hung. 16: 153-155. Nehlin, G., Valterová, I. & Borg-Karlson 1994: Use of conifer volatiles to reduce injury caused by carrot psyllid, Trioza apicalis, Förster (Homoptera, Psylloidea) J. Chem. Ecol. 20: 771-783. Nehlin, G.; Valterova, I.; Borg-Karlson, A.-K. 1996: Monoterpenes released from Apiaceae and the egg-laying preferences of the carrot psyllid, Trioza apicalis. Entomol. Exp. Appl. 80: 83-86. Persson, M., Sjödin, K., Borg-Karlson, A.-K., Norin, T. & Ekberg, I. 1996: Relative amounts and enentiomeric composition of monoterpene hydrocarbon in xylem and needles of Picea abies. Phytochemistry 42: 1289-1297. Rygg, T. 1977: Biological investications on the carrot psyllid Trioza apicalis Förster (Homoptera, Triozidae). Meld. Nor. Landbrukshogsk.56: 1-20. Valterová, I., Nehlin, G., Borg-Karlson, A. K. 1997: Host plant chemistry and preferences in egg-laying Trioza apicalis (Homoptera, Psylloidea) Biochem. Syst. Ecol. 25: 477-491.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 113-119

Diptera occurring on vegetables in Poland

J. Szwejda Research Institute of Vegetable Crops, ul. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland

Abstract: Twenty thousand and six hundred twenty six species and genera representing 21 families and 139 specimens identified only to 6 families were collected in the larval and pupal stage on white cabbage (roots), brussels sprouts (heads), onion (bulbs) and garlic (leaves and bulbs) plantations situated in Skierniewice, Gdańsk, Kalisz and Rzeszów districts between 1972-1994. The following number of species were found during 3 - 5 years observations on each crop : white cabbage – 26 (the dominant species – Delia radicum), brussels sprouts – 53 (Fannia spp. and Delia radicum), onion – 27 (Delia antiqua) and garlic – 16 (Suillia lurida). The species: Delia platura, D. florilega, Drosophila busckii, Bradysia paupera, Fannia canicularis, F. scalaris, Muscina assimilis, and M. stabulans associated with the four crops under investigations.

Key words: Diptera, cabbage, brussels sprouts, onion, garlic

Introduction

The order of Diptera is one of the largest group of insects occurring in the vegetable agrocenosis. Among them, the dipteran pests constitute an essential part of phytophagous insects occurring on vegetables in Poland. As my critical analyses of literature shows, the percentage of harmful Diptera species oscillated between 15-25% of all vegetable pests in Poland (Tab. 1). Up to now however, the faunistic and bionomic information about polyphagous species occurring in the vegetable agrocenosis is still poorly known. Publications on this topic are mostly scarce and outdated back to the old times. A number of species described as a sapro- or coprophagous can show phytophagous properties and vice versa. This paper summarizes data on the species composition and the trofic level of Diptera specimens collected on four vegetable crops between 1972-1994 in four regions of Poland (Szwejda, 1974, 1980, 1987).

Material and methods

The pre-imaginal stages of Diptera were collected from roots of white cabbage, heads of brussels sprouts, bulbs of onion and leaves or bulbs of garlic. The selected plantations were located in two central – Skierniewice and Kalisz, one nothern – Gdańsk and one southern – Rzeszów district, known of the concentrated production of vegetables in Poland. The larvae and pupae were collected during three seasons from white cabbage and garlic plantations, four seasons from onion, and five growing seasons from brussels sprouts. Once in the two-three week period, injured plants or their parts with larvae or pupae inside, were systematically collected throughout the whole growing season up to the harvest time. The collected insects were immediately transferred into rearing cages placed in a field and kept to the emergence of adults. They were later identified to species, genus or only family. In the 90’s, some of bionomic observations on these species were carried out during the growing season.

113 114

Table 1. Participation of Diptera species in the total number of vegetable pests in Poland (modified after, Szwejda, 1988).

Number of species Plants % Diptera Others Brassicae crops 8 35 18.6 Onion, garlic 6 19 24.0 Carrot, parsley, celery 3 13 18.8 Cucumber, pumpkin 3 10 23.1 Bean, pea, broadbean 4 19 17.4 Tomato, eggplant, pepper 4 11 26.7 Red beet, spinach 1 4 20.0 Other vegetables (with soil pests) 4 20 16.7 Total 33 131 20.1

Results and discussion

The collected 20,626 specimens from four different vegetable crops:: white cabbage, brussels sprouts, onion and garlic, were identified to 63 species, genera and representing 28 families together (table 2). The majority of collected species were recorded for the fist time on the above mentioned vegetables in Poland and elsewhere. From the economical point of view, the most important are the phytophagous and the zoophagous species. The first group was dominant in my studies and commonly considered to be important pests in many countries on: cabbage and brussels sprouts - Delia radicum (Szwejda, 1977, 1980), onion – Delia antiqua (Loosjes, 1976; Szwejda, 1982), garlic – Suillia lurida (noticed as the new pest from the end of 70's in Poland; Szwejda, 1987) and D. antiqua (Nikolova, 1953, Szwejda, 1987). Nine zoophagous species was identified between 20.626 specimens collected. They composed 4.16% of the total number of dipterous insects associated with onion; 1.57% with white cabbage; 0.99% with brussels sprouts and 0.17% with garlic. A large number of the following species occurred on all three or four crops: Delia platura and D. florilega, Drospophila busckii, Bradysia paupera, Fannia canicularis, F. scalaris, Muscina assimilis, M. stabulans, Phaonia trimaculata and Hydrotaea occulta. The seed corn maggot complex: Delia platura and D. florilega known as the important pests of cucumber, bean and pea, were always present on all four crops studied. Most of the larvae of the above mentioned both species, were collected from injured plants of cabbage and garlic just before harvest time. This circumstance indicates, that they were rather the secondary pests performing the role of saprophagous insects and occasionally, they were also observed in the bulbs of onion and heads of brussels sprouts. They can be therefore classified as polyphagous species injuring many other crops, e.g. feeding on the infested or decaying matter of: asparagus, cabbage, cauliflower and onion (Brooks, 1951; Dušek, 1969; Kuwayama et al.; Hill, 1973; Loosjes, 1976, Szwejda, 1980; Jonasson et al., 1995). Larvae of D. platura can also be a pest of onion seedlings (Larrain, 1994), or they may infest edible parts of asparagus growing in the soils rich in the organic matter (Szwejda, 1999). Delia fugax was always numerous on cabbage and brussels sprouts, often feeding in corridors tunneled by D.radicum (Szwejda, 1980). D. fugax can be also sapro- or zoophages 115

(Brooks, 1951; Crowell, 1959). Drosophila busckii was also collected from all four crops. This fly belongs to the cosmopolitan species and is common in different environments, mainly as a saprophagous (Hennig, 1953; Collins, 1956; Szwejda, 1980; Band, 1995). In my opinion, D. busckii can be a very serious pest under some circumstances. During winter time of 1993-1994, I found feeding larvae of D.busckii inside the seeds in some of onion storages. After feeding, they pupated between empty seeds. This species can also be an important pest of the heads of brussels sprouts. The larvae were found between the outer leaves injuring them in August and September. Other drosophilids as: D. funebris, D. limbata and Scaptomyza pallida were observed in the injured or decaying vegetables and fruits, in fermenting substances or dead animals (Hennig, 1953; Merril & Hutson 1953; Pond, 1956; Szwejda, 1980; Nartchuk & Kirvokhatsky, 1996). Larvae of Bradysia paupera were present each year, particularly in the bulbs of onion on the above mentioned plantations. This species and other specimens of Sciaridae family are widespread in the agrocenosis, living and injuring underground parts of many crops in greenhouses and field. They were identified among others on: cucumber, tomato, garlic, poinsettia, carnation, cyclamen, begonia (Burdajewicz, 1974; Szwejda, 1987; Szot, 1990). They can also injure the seedlings of some ornamental plants (Duso & Vettorazzo, 1996). Specimens belonging to the Muscidae family – Fannia canicularis and F. scalaris were always found occurring in abundance on all studied plantations. These species were often collected from the decaying parts of cabbage, brussels sprouts, onion and garlic. They are known as a commonly occurring sapro-, copro-, necro-, and mycophagous in decaying plants, animal debris, mushrooms, human and animals excrements (Brooks, 1951; Finlayson, 1956; Hennig, 1964; Szwejda, 1974, 1980; Nartchuk & Kirvokhatsky, 1996). Muscina assimilis, M. stabulans , Hydrotaea occulta and some other species, were found in the injured and decaying parts of plants and mostly collected in harvest time (table 2). Their larvae are omnivores, including zoophages, and were observed in large numbers in different habitats (Brooks, 1951; Pond, 1956; Bogdanov, 1959; Hennig, 1964). The larvae of Phaonia trimaculata, which were found in association with larvae of other species are known as common predators (Brooks, 1951; Ciampolini, 1960). Other species presented in the table 2 were associated with one or two above mentioned crops. Some of them occurred occasionally, other species were more numerous. In the onion bulbs, the population of Eumerus strigatus was very high, reaching almost 10% of all collected specimens. The larvae of E.strigatus are known as a pest of onion seedlings (Mulin, 1990), but they also occur on infested or rotten plants, among others, onion (Loosjes, 1976) and cabbage (Szwejda, 1974). The bionomics and host range of Stetisquamolonchae fumosa is poorly known up to now. A large number of larvae of this species was in the injured parts of garlic plants (almost 5% of all collected specimens), just before the harvest time (Szwejda, 1987). The larvae of this fly species were found in many plants, among others in: parsley, asparagus, cabbage and thorn-apple (Hering, 1954, Smith, 1957). On the end of garlic vegetation, the larvae of Elachiptera cornuta composed almost 8% of all collected larvae (Szwejda, 1987). E. cornuta is probably the secondary pest of garlic, injuring also some other crops as: rye, barley, oats, wheat, tomato (Hennig, 1953) or glandavian cornflag (Czyżewski, 1975). Before the harvest time of brussels sprouts, above 7% of all collected larvae belonged to the Tephrochlamys tarsalis species and were observed in association with other species inside the ripe heads (Szwejda, 1980). The larvae of T. tarsalis are known as the copro- and necrophages in decaying substances and nests of wasps and birds (Collin, 1943). This species is still expanding into new territories (Speight et al., 1990).

116

Table 2. The occurrence and trophic label of Diptera species on some vegetable crops in Poland.

Participation in percent Species/Genus/Family White Brussels Onion Garlic and trophic position of larvae* cabbage sprouts (bulbs) (leaves (roots) (heads) & bulbs) Trichocera hiemalis (De Geer) (Trichoceridae) – S, C 3.72 T. maculipennis Meig.( Trichoceridae) – C, N 0.43 T. relegationis (L.) (Trichoceridae) – S, C 2.05 Limoniidae 0.58 Psychodidae 0.01 0.24 1.43 Xylomyidae 0.17 Aphiochaeta rufipes Meig.(Phoridae) – S, P 8.12 Leptocera spp.(Sphaeroceridae) – S, C 0.16 Leptocera heteroneura (Hal.)(Sphaeroceridae) – C,N 0.04 L. luteilabris (Rond.)(Sphaeroceridae) – C, N 0.04 Ceroxys urticae (L.) (Otitidae) – S 0.08 Docosia gilvipes (Hal.) (Psychodidae) – S, C, M 0.04 Leia bimaculata (Meig.) (Psychodidae) – M, C 0.03 Dolichopus longitarsis Stann (Dolichopodidae) – Z 0.12 Thereva nobilitata (Fabr.) (Therevidae) – Z 0.12 Sciaridae 0.46 0.16 4.43 1.86 Chloromyia formosa Scop. (Stratiomyidae) – C, N 0.04 Scatopse notata (L.) (Scatopsidae) – C, M 0.05 Empididae 0.02 Phoridae 0.02 Elachiptera cornuta (Fall.) (Chloropidae) – S, P 7.89 Nemopoda nitidula (Fall.) (Sepsidae) – S, C, N 1.02 0.08 Themira leachi Meig.(Sepsidae) – C, N 0.01 Calliopum aeneum (Fall.) (Lauxaniidae) – S 0.45 0.02 Piophila vulgaris Fall. (Piophilidae)- C, N 0.03 Lonchaeidae 0.12 Siphona geniculata Deg. (Tachinidae) – Z 0.04 Phytomyza rufipes Meig.(Agromyzidae) –P 0.74 Drosophila busckii Coqu. (Drosophilidae) – S, P, M 0.18 15.00 0.20 0.85 D. funebris (Fabr.) (Drosophilidae) – S 0.12 0.72 D. limbata v.Ros. (Drosophilidae) – S 0.81 D. phalerata (Rond.) (Drosophilidae) – S 0.04 Scaptomyza pallida (Zett.) (Drosophilidae) – S, P 3.20 0.24 Suillia lurida (Meig.) (Heleomyzidae) – P 15.74 S. bicolor (Zett.) ((Heleomyzidae) – S, C 0.03 Heleomyza modesta Meig. (Heleomyzzidae) –S, C, N 0.44 Tephrochlamys tarsalis (Zett.) (Heleomyzidae) – C, N 0.51 7.15 Stetisquamolonchea fumosa (Egger) (Lonchaeidae) – S 0.20 4.91 Eumerus strigatus (Fall.) ((Syrphidae) – P, S 0.34 9.96 Syritta pipiens L. (Syrphidae) – Z 0.08 Delia antiqua Meig. (Anthomyiidae) – P 46.50 14.80 D. radicum (L.) (Anthomyiidae) – P 82.80 9.49 D. florilega (Zett.) + 4.81 0.02 0.87 13.79 D. platura (Meig.) (Anthomyiidae) – P D. fugax (Meig.) (Anthomyiidae) – S, P, C, Z 2.98 16.65 Anthomyia pluvialis (L.) (Anthomyiidae) – P, S, C 0.10 0.04 117

Tab. 2 cont.

Ceonosia tigrina F. (Muscidae) – Z 0.40 Fannia canicularis (L.) (Muscidae) – S, C, N 1.25 17.59 13.83 2.59 F. leucostica (Meig.) (Muscidae) – C, S, Z 0.03 F. manicata (Meig.) (Muscidae) – C, N, S 0.02 F. scalaris (Fabr.) (Muscidae) – S, C, N 1.31 9.79 8.58 0.42 Helina calceata Rond. (Muscidae) – Z 0.06 0.04 H. duplicata Meig. (Muscidae) – Z 0.12 Hebecnema affinis Mall. (Muscidae) – Z 0.12 Hydrotaea armipes (Fall.) (Muscidae) – C 0.06 0.05 0.04 H. dentipes (Fabr.) (Muscidae) – S, C, N, Z 0.34 0.56 H. occulta (Meig.) (Muscidae) – S, M 0.23 0.68 0.08 Ophyra leucostoma (Wied.) (Muscidae) S, C, N 0.23 0.26 0.47 Phaonia trimaculata (Bché) (Muscidae) – Z 1.03 0.97 3.60 Muscina assimilis (Fall.) (Muscidae) – S, P, C, M, N, Z 1.49 7.55 9.92 13.95 M. stabulans (Fall.) (Muscidae) – S, P, M, N, Z 0.06 0.27 1.19 13.45 Stomoxys calcitrans (L.) (Muscidae) – S, C 0.01 Bellieria melanura Meig. (Muscidae) – C, N, Z 0.02 Others 0.12 No. of collected larvae 1747 15168 2529 1182 No. of species 26 53 27 16 *Trophic characteristic of larvae: P – phytophages, S – saprophages, C – coprophages, N – necrophages, M – mycophages, Z - zoophages

The collected and identified Diptera specimens presented in Table 2, were found to be of a group of very diverse biotical and ecological habitats, representing all terrestrial and vegetation strata. Most of them overwinter in the pre-imaginal stage. The spring peak emergence of adults was observed in Aril and May in every year under studies. Up to the time of appearance on plants, the adults profited from nutrition accessible in the other parts of biotope or other parts of the host plants. In the initial period of the growing season the larvae of phytophagous and zoophagous species appear first on growing plants in the agroecosystem, later are found on the disintegrated plant tissues, the increased amount of animal remains (dead insects and spiders mostly) and their excrements, followed by other trophic groups of Diptera: sapro-, copro-, necro- and mycophagous species. The adults of non-phytophagous species were attracted not only by plants, but also by the associated phyto- and zoofauna, decaying tissue and the metabolic products. Many of the species are effective carriers of pathogenic microorganisms. Among them, Delia radicum or Drosophilidae can transmit some bacterial or fungal diseases (Hennig, 1953; Doane & Chapman, 1964).

References

Band, H.T. (1995). Frassy substrates as oviposition breeding sites for drosophilid. Virginia J.Science 46(1): 11-23. Bogdanov, V.T. (1959). Bothynoderes punctiventris Germ. Cz.1, Biologia I gospodarcze znaczenie w Bułgarii. [B. punctiventris Germ., part 1, Biology and economic importance in Bulgaria]. Ann.UMCS, Univ.Libr. Lublin 13(3): 41-83. 118

Brooks, A.R. (1951). Identification of the root maggot (Diptera: Anthomyiidae) attacking cruciferous garden crops in Canada, with notes on biology and control. Can. Ent. 83(5): 109-120. Burdajewicz, S. (1974). Ziemiórkowate (Sciaridae) – szkodniki roślin uprawianych pod szkłem.[Sciaridae – pests of crop plants grown in glasshouses]. Ochrona Roślin 1: 15-16. Ciampolini, M. (1960). Phaonia trimaculata Bouché (Diptera: Anthomyiidae) a parasite of the larvae of Temnorrhinchus mendicus Gyll. Redia 45: 245-263. Collin, J.E. (1943). The British species of Heleomyzidae (Diptera). Ent. Monthly Mag. 79: 234-251. Collins, W.E. (1956). On the biology and control of Drosophila on tomatoes for processing. J. Econ. Ent. 49(5): 607-610. Crowell, H.H. (1959). Biology and economic status of Hylemya fugax (Meigen) in Oregon. J. Econ. Ent. 52(3): 503-505. Czyżewski, J.A. (1975). Choroby i szkodniki roślin ozdobnych. [Ornamental plants diseases and pests]. PWRiL, Warszawa: 408 pp. Doane J.F. & Chapman R.K. (1964). The relation of the cabbage maggot, Hylemyia brassicae (Bouché) to decay in some cruciferous crops. Ent. Exp.& Appl. 7: 1-8. Duso, C. & Vettorazzo, E. (1996). Observations on the behaviour and harmfulness of Bradysia paupera Tuomikoski (Diptera, Sciaridae) in glasshouses. Boll. Zool. Agr. Bachicolt. 28(1): 23-40. Dušek, J. (1969). Kvĕtilky (Anthomyiidae, Diptera) škodici na obilovinách. [Anthomyiidae species (Diptera) causing damage to cereal crops]. Acta Univ. Agric., Brno 17(1): 127- 137. Finlayson, D.G. (1956). Maggots and puparia in stems and balbs of onion at harvest. J. Econ. Ent. 49(4): 460-462. Hill, D.S. (1973). Damage to pea seedling and Brussels sprout transplants by larvae of bean seed fly (Delia platura (Meig.)). Plant Pathology 22(1): 49. Hennig, W. (1953). Diptera, Zweiflügler (Chloropidae: 111-121). In: P. Sorauer (ed.), Handbuch der Pflanzenkrankheiten, P.Parey, Berlin, Hamburg. Hennig, W. (1964). 63b. Muscidae. In: E. Lindner (ed.), Die Fliegen der Paläarktischen Region, Stuttgart, 72 (63b): 1110 pp. Hering, E.M. (1954). Lebensweise und Larven – Morphologie von Lonchaea flavidipennis Zett. (Dipt.). Dtsch. Ent. Ztschr. N.F. 1: 86-89. Jonasson, T., Ahlström-Olsson, M., Johansen, T.J. (1995). Aleochara suffusa and A. bilineata (Col., Staphylinidae) as parasitoids of brassicae root flies in nothern Norway. Entomophaga 40(2): 163-167. Kuwayama, S., Hori, M., Takizawa, M., Endo, K., Sakurai, K., Tsutsumi, M. (1970). Studies on the biology and control of the seed-corn maggot in Flakkaidi. Hokk. Nat. Agric. Exp. Sta.: 96 pp. Larrain, S.P. (1994). Fluctuation poblacional y daň de Delia antiqua (Meigen) y Delia platura (Meigen) (Diptera: Anthomyiidae) an almacigos de ceballas (Allium cepa L.) de la zona centro-norte de Chile. Agricultura Técnica (Santiago) 54(1): 60-64. Loosjes, M. (1976). Ecology and genetic control of the onion fly (Delia antiqua (Meigen). Agric. Res. Reports, Inst.Phytopathological Res., Wageningen: 179 pp. Merrill, L.G. & Hutson, R. (1953). Maggots attacking Michigan onions. J. Econ. Ent. 46(4): 678-680. Mulin, Y.I. (1990). [A dangerous pest of onion.], Zashchita Rastenii 3: 31-32. Nartchuk, E.P. & Kivokhatsky, V.A. (1996). [Unusual substratum for development of Diptera larvae – pests of biological collections]. Entomologicheskoe Obozrenie 75(1): 1214- 1219. 119

Nikolova, W. (1953). Jedin nov neprijatel po cecna – cesnokova mucha Suillia lurida Meig. [A new pest of garlic – S. lurida]. Zemizdat. Biul. Rast. Zasc. II, 2: 17-1. Pond, D.O. (1956). Annotated list of insects found in or near roots of cultivated crucifers in New Brunsick. J. Econ. Ent., 49(3): 336-338. Smith, K.G.V. (1957). Notes on the immature stages of four British species of Lonchaea Fln. Dipt., Lonchaeidae). Ent. Monthly Mag. 92: 262-265. Speight, M.C.D., Blackith, R.E., Blackith, R.M. (1990). Antichaeta brevipennis, Leucophenga maculata, Polyporivora picta and Teprochlamys tarsalis (Diptera), a insect new to Ireland. Bull. Irish Biogeographical Society, 13(2): 200-212. Szot, H. (1990). Szkodliwość ziemiórek (Sciaridae) na roślinach warzywnych i ozdobnych. [Harmfulness of Sciaridae on ornamental and vegetable crops]. Report, Res. Inst. Veg. Crops, Skierniewice: 30 pp. Szwejda, J. (1974). Muchówki (Diptera) występujące na roślinach kapustnych. [Diptera occurring on cabbage crops]. Pol. Pismo Ent. 44: 381-392. Szwejda, J. (1977). Biological and ecological studies in light of previous and recent research on the cabbage root fly (Hylemya brassicae Bouché) (Diptera: Anthomyiidae). Biul. Warzywniczy, Res. Inst. Veg. Crops 20: 275-288. Szwejda, J. (1980). Diptera occurring on Brussels sprouts. Pol. Pismo Ent. 50: 569-597. Szwejda, J. (1982). Dynamika populacji i szkodliwość śmietki cebulanki (Hylemya antiqua Meig.) (Dipt.: Anthomyiidae) na cebuli. [Population dynamics and harmfulness of onion maggot on onion]. Roczn. Nauk Roln. 12(1/2): 57-71. Szwejda, J. (1987). Diptera of garlic and ecological observations on dominant species – Suillia lurida Meig. (Dipt., Helomyzidae). Acta Horticulturae 219: 99-108. Szwejda, J. (1988). Znaczenie i szkodliwość muchówek (Diptera) w warzywnictwie. [Harm- fulness of Diptera in vegetable crops]. Wiad. Entomol., Warszawa 8 (1-2): 27-34. Szwejda, J. (1999). Stan i potrzeby badań entomologicznych w zakresie ochrony roślin warzywnych przed szkodnikami. [Status of entomolgy researches for vegetable crops protection in Poland]. Progress in Plant Prot. / Post .Ochr. Roślin 39(1): 43-51.

120

Predators and Parasitoids

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp.121-126

Role of beneficial mirid bugs in control of tomato pests in open fields

E. B. Ceglarska Szeged University, Faculty of Agriculture, Hodmezovasarhely, Andrassy 15, 6800, Hungary Veszprem University, Georgikon Faculty of Agriculture, Keszthely, Deak F. 16, 8360, Hungary, E-mail: [email protected]

Abstract: Predaceous mirid bugs are important control agents of tomato pests. Several European species occuring in open field have been reported to colonise the crop in fields and to migrate into greenhouses, and effectively control tomato pests. Dicyphus hyalinipennis Burm., a newly discovered species of Hungarian fauna was studied from the view of its potential to control noxious insects in tomato. In order to determine some biological parameters and consumption rates of the beneficial experiments were performed in controlled circumstances. Surveys of wild flora were conducted in places of mass occurrence of D. h. with the aim of finding out the range of host plants potentially suitable as hosts. The paper below presents the results.

Key words:. biological control, predators, Miridae, Dicyphus hyalinipennis

Introduction

In Europe and particularly in the Mediterranean basin several predaceous mirid bugs have been successfully used in biological control of tomato pests. One of them Macrolophus caliginosus is widely applied in greenhouse growing, others, like Dicyphus tamanini, D. errans or Cyrtopeltis tenuis (Albajes et al., 1996; Benuzzi & Mosti, 1994), are important components of beneficial fauna in open fields. Although parasitoids are the dominating ones in biological control, predatory beneficials deserve more attention. In Hungary mirid bugs compose 1/3rd part of the heteropteran fauna. Quite a number of them are considered as pests (Benedek, 1988; in: Jermy & Balázs, 1988). Predators occur in different field crops but their role in pest control is not significant, probably due to wide application of chemicals. In 1995 first spontaneous mass occurrence of a mirid predatory bug, unknown before for Hungarian insect fauna, was observed. The predator moved into greenhouse tomato crop, reproduced in a high level and reduced the whitefly population without any additional chemical treatments. Since that time the bug, later identified as Dicyphus hyalinipennis Burm. (Heteroptera: Miridae), has been reported from many places of South Hungary. According to Melber et al. (1990) the predator is present in fauna of North-East Austria. Putshkov & Putshkov (1996) reported it from Carpathians, Sub-Carpathia and Crimea. The beneficial occurs in open fields on areas rich in weed-flora. Adults of its 1st generation enter greenhouses and they reproduce at a high range. Nymphs as well as adults prey on greenhouse whiteflies (Trialeurodes vaporariorum, Bemisia tabaci) and aphids (Myzus persicae, Aphis gossypii), but feeding on spider mites, lepidopterous eggs (Helicoverpa armigera) and thrips was also reported (Ceglarska et al., 1998). Studies on biology and predation capacity of D. hyalinipennis showed that the beneficial possesses features qualifying it as a potential biological control agent. All the European experience coming from study and practice on predatory mirids as well as the increasing

121 122

complexity of IPM, creates motivation for further work on the whole group of Dicyphinae in order to clear their role in control of noxious pests either in greenhouses or in open fields.

Material and methods

Composition of flora in sites of mass occurrence of Dicyphus hyalinipennis Burm. Surveys of composition of wild plants were conducted in places of mass introduction of D. h. in order to determine the range of plants potentially suitable for maintenance of population in open field.

Insect rearing The rearing of D. h. was maintained in glasshouse conditions (temp. 25 +2 0C, 60 % RH, 16/8 D/L regime) on tomato and tobacco, on Trialeurodes vaporariorum as a prey.

Main biological features The tests, replicated six times, were conducted under laboratory conditions in climate regime as indicated above. The daily production of viable eggs was determined on tomato, cucumber and tobacco. Fifteen couples of two weeks old adults were placed on host-plants for 48 hours. After two weeks incubation the plants were checked for the presence of nymphs. For determining of nymphal development time just hatched individuals were maintained on leaf-discs infested with T. v. premature stages, until eclosion. Adult longevity was determined using just hatched individuals, which were kept on tomato and tobacco plants with T. vaporariorum as a prey, until death. To avoid the interference of a new born insects, the host plants were changed fortnightly.

Potential daily consumption rates In order to obtain an uniform level of hunger before the establishment of feeding tests, 4th-5th instar nymphs and adult females of D. hyalinipennis were isolated for 24 hours and supplied only with water. The tests were carried out in plastic containers containing fresh host plants leaves, on which the prey was offered for 24 hours (no-choice test): on tomato - various stages of T. vaporariorum, Bemisia tabaci, Tetranychus urticae, on cucumber - winged and wingless forms of Aphis gossypii.

Evaluation of data All the data obtained was statistically evaluated using one-way ANOVA test, with the separation of appropriate means by Tuke’s HSD (SPSS 6.1).

Results and discussion

Composition of flora in sites of mass occurrence of Dicyphus hyalinipennis Burm. The surveys on composition of flora in sites of occurrence of D. h. showed that the beneficial prefers places rich in weed plants (Table 1). It is still to clear, which are the potential hosts providing winter shelter and what stage is the overwintering one. In greenhouses the bugs colonised flowering tops of goosefoot, when the tomato crop was finished (Table 2). From among Dicyphinae occurring in Mediterranean Dicyphus tamaninii, closely related to D. h., has the widest range of host plants (23 species), suitable for overwintering (Alomar et al., 1994). Most of the studied weeds, e.g., Atriplex, Amaranthus, Galium, Solanum, Sonchus, Urtica spp. occur in Hungarian flora and might have an importance as host plants for D. h..

123

Table 1. Composition of flora from the place of mass occurrence of Dicyphus hyalinipennis Burm.(Hodmezoevasarhely, 1997)

Family Species Amaranthaceae Amaranthus spp. Caryophillaceae Stellaria media Compositae Ambrosia elatior Artemisia spp. Bidens tripartitum Cichorium intibus Cirsium arvense, C. vulgaris Onopordon acanthium Sonchus arvensis Taraxacum officinale Xanthium strumaria Convolvulaceae Calistegia sepium Convolvulus arvensis Chenopodiaceae Atriplex patula Equisetaceae Equisetum arvensis Gramineae Agropyron repens Cynodon dactylon Echinochloa crus-galli Setaria viridis, S. verticillata Sorghum halepense Labiatae Salvia sp. Linaceae Linum sp. Moraceae Morus sp. Onagraceae Epilobium sp. Oxalidaceae Oxalis sp Plantaginaceae Plantago major, P. lanceolata Polygonaceae Polygonum aviculare Rumex obtusifolia Portulacaceae Portulaca oleracea Rosaceae Malus sp. Rubus caesius Salicaceae Populus sp. Salix sp. Scrophulariaceae Digitaria sanguinalis

Solanaceae Datura stramonium Solanum nigrum, Solanum spp. Umbelliferae Daucus carota

Urticaceae Urtica spp. Verbenaceae Verbena sp.

124

Table 2. Weeds providing a shelter for Dicyphus hyalinipennis Burm. after destruction of tomato crop in glasshouse (Hodmezoevasarhely, 1997)

Number of Plant Dicyphus hyalinipennis Burm. individuals per plant Adults Nymphs Wilting tomato 20 9 Goosefoot Chenopodium album - flowering 13 4 shoot-tops Bristle-grass Setaria 2 0 Prickly lettuce Lactuca seriola 2 0 Stinging nettle Urtica dioica - flowering tops 1 0

Main biological features The results are presented in Table 3. The daily production of viable eggs differs significantly by the host-plant: the highest rates were obtained on tobacco, the lowest ones on cucumber. Concerning nymphal development time the 1st instar nymphs have longer development time on tomato, while 2nd and 3rd instar - on cucumber. The period of 4th instar did not differ significantly between host plants. In the case of 5th instar nymphs significant differences were experienced between all three host plants. According to the data the longevity of adults does not depend on examined plants.

Table 3. Main biological parameters of predatory bug Dicyphus hyalinipennis Burm. (Wageningen, 1998)

Daily Adults Host-plant Nymphal development time, days production longevity, of viable 1st instar 2nd instar 3rd instar 4th instar 5th instar days eggs Tomato 1.46 + 3.3 + 2.7 + 3.3 + 4.7 + 5.5 + 60.0 + 0.36 0.51 0.51a 0.51a 0.51a 0.55 6.7 Cucumber 0.33 + 2.8 + 3.3 + 4.3 + 4.5 + 6.2 + n.a. 0.14 0.41a 0.51 0.51 0.55a 0.75 Tobacco 4.75 + 2.5 + 2.7 + 3.5 + 4.5 + 4.5 + 55.3 + 0.47 0.55a 0.51a 0.54a 0.55a 0.55 2.7 Means indicated with letter "a" show no significant differences between treatments

Potential daily consumption rates Table 4 contains the potential daily predation rates of D. hyalinipennis. All offered kinds of prey were accepted by the predator, some of them - like spider mites and cotton aphid - were consumed in a high rates. Comparing the data obtained from related species of D. tamaninii by Alvarado et al. (1997), D. h. nymphs consumed much more wingless aphids on cucumber, while females - less. In the case of tobacco whitefly on tomato the predator exhibited higher predation than that of D. t., reported by Barnadas et al. (1998). According to synthetic 125

evaluation of D. t. given by Albajes et al. (1996), feeding on glasshouse whitefly larvae occurs to be approximate. Amounts of consumed prey do not differ significantly between examined stages, except for those of aphids and mites: D. h. nymphs ate more than females.

Table 4. Potential daily prey consumption by the predatory bug Dicyphus hyalinipennis Burm. (Wageningen, 1998)

Number of consumed individuals per 24 hours Dicyphus Tetra- hyalini- Trialeurodes vaporariorum Bemisia tabaci nychus Aphis gossypii pennis urticae stage wingless winged Eggs Larvae Adults Larvae Adults Adults form form

Nymphs 18.7 13.3+1.9 9.5+1.0 9.8+0.6 4.1+0.3 48.7+3.2 41.2+2.9 35.1+1.4

Females n.a. 12.1+1.4 12.6+0.8 10.3+0.6 3.6+0.4 36.3+1.8 31.8+1.9 28.5+1.4

Conclusions

Predatory bug Dicyphus hyalinipennis Burm. (Heteroptera: Miridae), spontaneously migrating into Hungarian greenhouses from fields, possesses features qualifying it as potential biological control agent. The beneficial is able to colonise tomato crop in protected cultivation and to control its noxious pests. Growers, for whom the commercially distributed Macrolophus caliginosus is too expensive, prefer to collect D. h., usually together with host insects. This may lead to spreading of virus diseases. As for open field tomato growing Dicyphus hyalinipennis may potentially play an important role, especially in conditions of cultivation on supporting system. Positive Spanish experience gained on relative species Dicyphus tamaninii proved that conservation is the right way to save the field populations of beneficial mirids.

References

Albajes, R., Alomar, O. Riudavets, J. Castane, C. Arno, J. & Gabarra, R. 1996: The mirid bug Dicyphus tamaninii: an effective predator for vegetable crops. IOBC WPRS Bulletin 19 (1): 1-4. Alomar, O., Goula, M. & Albajes, R. 1994: Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonization of tomato fields. IOBC WPRS Bulletin 17 (5):217-223. Alvarado, P., Balta, O. & Alomar, O. 1997: Efficiency of four heteroptera as predators of Aphis gossypii and Macrosiphum euphorbiae (Hom.: Aphididae)., Entomophaga 42: 215- 226. 126

Barnadas, I., Gabarra, R. & Albajes, R. 1998: Predatory capacity of two mirid bugs preying on Bemisia tabaci. Entomologia Experimentalis et Applicata 86: 215-219. Benuzzi, M. & Mosti, M. 1994: I miridi predatori di aleurodidi [Mirid predators of aleyrodids]. Informatore Fitopatologico 44 (11): 25-30 (in Italian). Ceglarska, E., Budai, Cs., Kondorosy, E., Deme, J. & Moravszky, G. 1998: Dicyphus hyalinipennis Burm. (Heteroptera: Miridae) ragadozo mezei poloska hazai elõfordulasa és szerepe a növényházi növényvédelemben [Occurrence of indigenous predatory bug Dicyphus hyalinipennis Burm. (Heteroptera: Miridae) and its role in biological control in greenhouses]. Plant Protection Scientific Days, 24-25 Feb., 1998 ( in Hungarian). Benedek, P. (1988): Rend: Poloskak (Heteroptera).[Order: Bugs (Heteroptera)] Chapter 12. In: T. Jermy and K. Balázs (eds.) A novenyvedelmi allattan kezikonyve [Manual of plant protection zoology]. Akademiai Kiado, Budapest: 306-423. Melber, A., Günther, H. & Rieger, C. (1990): Die Wanzenfauna des Österreichischen Neusiedlerseegebietes (Insecta, Heteroptera). Wiss. Arbeiten Bgld., Eisenstadt 89: 63- 192. Пучков, В.Г. & Пучков, П.В. (1996): Полужесткокрылые Насекомые Украины: Список Видов и Распространение, Зоологический институт РАН, С. Петербург

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 127-133

Releasing the rove beetle Aleochara bilineata in the field as a biological agent for controlling the immature stages of the cabbage root fly, Delia radicum

C. Hartfield & S. Finch Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK

Abstract: The predatory rove beetle Aleochara bilineata Gyllenhal was released inundatively as part of a study to determine whether biological control of a pest species using a predator could be achieved in ephemeral field crops in the UK. Different numbers of A. bilineata were released under semi-field conditions (covered plots) to quantify the number of predatory beetles required to control cabbage root fly (Delia radicum L.) larvae on the roots of artificially-infested cabbage plants (Brassica oleracea var. capitata Alef.). The release of between two and eight A. bilineata/plant reduced the number of fly pupae recovered by about 60%. Releasing more than eight beetles/plant did not improve the level of control. By calculating the mean percentage reduction in the number of D. radicum pupae/plant that could be attributed to each A. bilineata released, it was apparent that the beetles were most effective when released at the rate of two beetles/plant. The release of A. bilineata under open field conditions, and the constraints that could prevent its success as a biological agent for controlling cabbage root fly, are discussed.

Key words: Aleochara bilineata, Delia radicum, predation, biological control.

Introduction

At present, UK growers spend more than £ 9 million/year on insecticides to control populations of the cabbage root fly (Delia radicum). However, the majority of these chemicals are anti-cholinesterase insecticides (organophosphorus and carbamate compounds) and many are due shortly to be withdrawn from use (Finch et al., 1999). In their place, a competitively-priced, environmentally-acceptable alternative to insecticides would be a welcome addition to the methods available currently for controlling this pest. Work is underway at HRI Wellesbourne to try and answer the broad fundamental question of whether biological control of a pest species using a predator can be achieved in short-term cropping systems under open field conditions. The pest-predator system used in this study is that of the pest fly D. radicum and the predatory rove beetle Aleochara bilineata. The concept of controlling field populations of the cabbage root fly biologically by releasing A. bilineata has been discussed for more than 75 years (see Tomlin et al., 1992). However, no one to date has used beetles successfully in this way. Until now, many of the proposed ways of using A. bilineata to control root fly have been based on the beetle’s ability to eat fly eggs and so lower the overall level of pest infestation in the first wave of fly attack (Bromand, 1980; Hertveldt et al., 1984; Tomlin et al., 1992). However, the results of recent laboratory experiments at HRI Wellesbourne cast serious doubt upon the effectiveness of A. bilineata as an egg predator (Finch et al., 1999). Individual beetles were shown to be capable of destroying about 12 fly eggs/day. However, the beetles only found eggs on the soil surface, not those in the soil. As further experiments showed that less than 15% of fly eggs were laid exposed to predators on the soil surface (Finch et al.,

127 128

1999), egg predation by A. bilineata is not likely to contribute greatly to the overall levels of cabbage root fly control. The ineffectiveness of A. bilineata as a predator of the eggs of the cabbage root fly has two major implications; 1) the value of mass-releasing this predatory beetle will depend on whether it can destroy enough fly larvae to reduce damage to acceptable levels on the roots of crop plants, and 2) following on from this, it is clear that any mass-release strategy could only be used in leafy brassica crops, where limited root damage can be tolerated. This paper describes a study to determine whether cabbage root fly larvae can be controlled under semi-field conditions by an inundative release of the predator A. bilineata.

Materials and methods

Insects All insects used in the experiment were obtained from cultures maintained in the Insect Rearing Unit at HRI Wellesbourne. The cabbage root fly eggs were obtained from the continuous culture maintained using the method developed by Finch & Coaker (1969). The fly eggs used to inoculate the experimental plants were less than 24 hours old. Adult rove beetles, obtained from both a continuous culture and field-collected fly pupae, were maintained using the method described in Hartfield et al. (1999). Mixed ages of beetle adults were released into field cages (see below). The number of beetles released/test plant ranged from 0-16.

Plants Cabbage (Brassica oleracea var. capitata (L.) Alef., cv. Derby Day) was used as the test brassica plant for the experiments. The brassica plants were grown from seed in Hassy 308 plastic modular trays (Erin Planter Systems Ltd., Baldock, Herts., UK) in a glasshouse. Once the plants reached the three-leaf stage, they were removed from the modules and planted directly into the field plots. The test plants were then left for seven days to establish prior to being inoculated with 40 fly eggs; washed onto the soil surface around the base of the stem of each plant. This number of eggs/plant would represent a ‘worst case’ scenario for a grower. Based on the forecasting model, sufficient time was allowed for the fly maggots to develop to the target stage before the beetles were released into the plots.

Field cages and experimental design Beetles were released at two separate field sites at Wellesbourne during 1998. Experiment 1 lasted from late-April to early-June, and Experiment 2 from early-July to early-October. Each experiment consisted of 25 plots, arranged in a 5 x 5 Latin square design. The plots were 1.8 m wide x 3.6 m long and spaced 1.2 m apart. The plants were spaced 0.6 m apart, both within and between the rows, so that each plot contained three rows of five cabbage plants. As soon as they had been planted, each plot was covered with a cage made from 0.5 mm mesh polyester netting, supported internally by metal arches (1 cm gauge steel wire, 80 cm x 45 cm high). The skirting of each cage wall was covered with soil to make the cages insect-proof. Three of the cabbages in each plot were not inoculated with fly eggs. These were for the control treatment used to assess plant growth in the absence of fly larvae. The A. bilineata were taken into the cage in 7.5 x 2.5 cm glass tubes and released at the base of each plant at the following rates: 0, 2, 4, 8 and 16 beetles/infested plant. If released too early, the pest would still be in the egg-stage or the newly-hatched larvae would be too

129

young to produce the chemical cues that attract adult A. bilineata. In either situation, the beetles would find insufficient food and disperse from the area. If released too late, the fly larvae would have caused unacceptable amounts of damage to the crop. The cabbage root fly forecasting model (Collier et al., 1995) was used to predict precisely the developmental stages of the fly larvae in the field and thereby time the release of the beetles to ensure maximum impact. The time for 50% pupation, calculated from the forecasting model, was used to determine when to harvest the cabbage plants and to take the soil samples. At harvest, the shoot weight and the root weight were recorded for each plant. A 10 cm core of soil was then taken from around the roots of each plant. Fly pupae were washed-out from the soil by flotation. The level of parasitism was determined either by direct dissection of the fly pupae or by maintaining the pupae under controlled environmental conditions and recording the relative numbers of flies and beetles that eventually emerged. Both experimental plots were irrigated daily throughout the course of the experiments.

Data analysis The numbers of pupae recovered and the shoot and root weights were analyzed using ANOVA. As the numbers of A. bilineata released were based deliberately on a logarithmic scale, it was possible to use orthogonal polynomial contrasts to examine the shape of various responses, i.e. changes in shoot weight or number of fly pupae recovered, relative to the number of beetles released.

Results and discussion

The linear equation y = yo + ax was fitted separately for shoot and root weights using the data from Experiment 1. The parameters associated with the resulting regression lines are shown in Table 1. Figure 1 shows clearly that there was a linear trend (P < 0.05) between the weights of harvested shoots and roots of fly-infested and the number of predatory beetles released/plant. Both shoot weight and root weight increased as the numbers of A. bilineata increased. Releasing eight beetles/ inoculated plant resulted in an increase in shoot and root weight at harvest of 88% and 100%, respectively, when compared with the inoculated control plants (Table 2). There was no linear relationship between the weight of inoculated plants in Experiment 2 and the numbers of A. bilineata released/plant.

Table 1. Parameters arising from the linear regression of shoot weight and root weight on number of A. bilineata released. Experiment 1.

Yo A r2 N s2

Shoot weight 28.69 2.811 0.88 5 1231 Root weight 2.77 0.232 0.92 5 2.966

130

80 1 Shoot 60

20 Root 0 Mean shoot or root weight (g) weight shoot or root Mean

024 8 16

Number of A. bilineata released

Fig. 1. Relationship between the root (●) or the shoot (○) weights of fly-infested plants and the number of A. bilineata released. 1 Means taken from Table 2. The straight lines are the linear regression lines fitted for shoot, y = 28.69 + 2.81x (r2 = 0.88, n = 5), and root, y = 2.77 + 0.23x (r2 = 0.92, n = 5), respectively.

Table 2. The effect of the numbers of A. bilineata released on the shoot and root weights of fly-infested plants and on the number of fly pupae recovered.

Experiment 1 Experiment 2 No. A. bilineata Shoot Root Mean no. pupae Mean no. pupae released weight (g) weight (g)1 recovered/plant recovered/plant 0 32 a 2.6 a 0.72 a 5.17 a 2 26 a 2.8 a 0.26 b 3.50 b 4 41 a 4.0 ab 0.20 b 2.83 bc 8 60 a 5.2 b 0.18 b 2.02 c 16 70 a 6.2 b 0.16 b 2.10 c SED (P = 0.05, 12 d.f.) 22 1.1 0.14 0.62

1 Means followed by the same letter are not significantly different (P>0.05).

Releasing the predator A. bilineata onto plants infested with cabbage root fly had a considerable impact on the number of fly pupae recovered from the plants in both experiments 1 and 2 (Table 2). In both experiments, there was a linear relationship (P < 0.05) between the numbers of pupae recovered and the numbers of A. bilineata released. The numbers of pupae decreased as numbers of beetles released increased. In Experiment 1, releasing A. bilineata reduced the number of fly pupae recovered by at least 64% (Figure 2). However, the low numbers of fly pupae recovered from this experiment were not sufficient to enable differences to be found between the four levels of A. bilineata released (Table 2). In Experiment 2, the numbers of fly pupae recovered were higher (Table 2) and although the

131

maximum reduction in the number of pupae recovered (59%) was slightly lower than in Experiment 1 (Figure 2), the differences between the various treatments were significant. Fewer pupae were recovered (c. 41% less) when eight or 16 beetles were released/plant compared to when just two beetles were released (P < 0.05) (Table 2). Therefore, the maximum reduction in the size of the cabbage root fly infestation was obtained when two to eight beetles were released/plant. However, when the % reduction in the number of fly pupae recovered was calculated on a ‘per beetle released’ basis, the optimum number of beetles to release was two/plant (Figure 3). At present, the reasons for this are unclear and so it will require further study.

100 Experiment 1 Experiment 2 80

% reduction in number of fly pupae of fly number in reduction % 0 0 2 4 6 8 1012141618 Number A. bilineata released/plant

Fig. 2. Relationship between the % reduction in the mean number of fly pupae recovered from fly-infested plants and the number of A. bilineata released in experiments 1 and 2. % reductions obtained by calculating the difference between the control (where no A. bilineata released) and the other treatment means shown in Table 2.

The major criticism of experiments done in field cages, to exclude the natural population of pest flies, is that the cages prevent the released A. bilineata from dispersing. The primary reason for dispersal would be if there was an inadequate food supply at the release site. Therefore, the beetles are only ever likely to disperse from areas that contain too few fly maggots, i.e. if such areas are essentially pest-free. The behaviour of A. bilineata after their release in open field plots is being investigated currently at HRI Wellesbourne. The aim of this work is to answer the questions regarding the dispersal of released beetles, their effectiveness in controlling aggregated fly infestations, their interaction with other invertebrates and the impact upon them of any pesticides applied to the crop. The study will determine whether the tendency for A. bilineata to disperse is innate or not. If it is innate, then it may be limited to only a restricted period of time and so it may be practical to retain the beetles during this period and only release them once their dispersal phase is over. However, if the dispersal phase occurs over a protracted period, it may be necessary to look for other options. One such option could be the selection of flightless beetles, as a proportion of every beetle population is flightless.

132

Once we can answer these behavioural and ecological questions we should be nearer to defining the attributes a predatory insect needs if it is to control pest insects in ephemeral field crops.

Experiment 1 Experiment 2 40

20 beetle released

% reduction in number of fly pupae of fly number in % reduction 0 024681012141618

Number A. bilineata released/plant

Fig. 3. Relationship between the mean % reduction in the number of fly pupae recovered/ A. bilineata released and the number of A. bilineata released in experiments 1 and 2. % reductions obtained by calculating the difference between the control (where no A. bilineata released) and the other treatment means shown in Table 2.

Acknowledgements

The authors thank colleagues at HRI for technical support, and the UK Ministry of Agriculture, Fisheries and Food (Contact: Dr S Popple) for supporting this work as part of Project HH1830SFV.

References

Bromand, B. (1980). Investigations on the biological control of the cabbage rootfly (Hylemya brassicae) with Aleochara bilineata. IOBC WPRS Bulletin 3 (1): 49-62. Collier, R.H., Finch, S. & Phelps, K. (1995). Forecasting attacks by insect pests of horticultural field crops. Integrated Crop Protection: Towards sustainability? BCPC Symposium Proceedings 63: 423-430. Finch, S & Coaker, T.H. (1969). A method for the continuous rearing of the cabbage root fly Erioischia brassicae (Bouché) and some observations on its biology. Bulletin of Entomological Research 58: 619-627. Finch, S., Collier, R.H. & Jukes, A. (1999). Ultimate challenge. Grower 132 (3): 51-52. Finch, S., Elliott, M.S. & Torrance, M.T. (1999). Is the parasitoid staphylinid beetle Aleochara bilineata an effective predator of the egg stage of its natural host, the cabbage root fly? IOBC WPRS Bulletin 22(5): 109-112.

133

Finch, S., Skinner, G. & G. H Freeman (1975). The distribution and analysis of cabbage root fly egg populations. Annals of Applied Biology 79: 1-18. Hartfield C.M., Nethercleft M. & Finch, S. (1999). The effect of undersowing brassica crops with clover on host finding by Trybliographa rapae and Aleochara bilineata, two parasitoids of the cabbage root fly, Delia radicum. IOBC WPRS Bulletin 22(5): 117-124. Hertveldt, L., Van Keymeulen, M. & C. Pelerents (1984). Large scale rearing of the entomo- phagous rove beetle Aleochara bilineata (Coleoptera: Staphylinidae). Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft 218: 70-75. Tomlin, A.D., McLeod, D.G.R., Moore, L.V., Whistlecraft, J.W., Miller, J.J. & J.H. Tolman (1992). Dispersal of Aleochara bilineata (Col.: Staphylinidae) following inundative release in urban gardens. Entomophaga 37: 55-63.

134

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 135-140

Effect of the host-plant on the biological characteristics of Trybliographa rapae W. (Hymenoptera: Figitidae), endoparasitoid of the cabbage root fly Delia radicum L. (Diptera: Anthomyiidae)

N. Kacem-Haddjel-Mrabet & J.-P. Nenon Laboratoire d'Ecobiologie des Insectes Parasitoïdes -Université de Rennes 1. Campus de Beaulieu, Avenue du Général Leclerc. 35042 Rennes Cedex, France

Abstract: The present work was undertaken to evaluate the effect of two Cruciferous host plants, cauliflowers Brassica olearaceraL.and swede Brassica napus L. on the developmental time, pupae recovered per female, weigth of parasitised pupae, size of adults (length of tibia P3), sex-ratio (% of females) and percentage of parasitism of the parasitoid Trybliographa rapae W. (Hymenoptera: Figitidae) on its host Delia radicum L. (Diptera: Anthomyiidae). The developmental time, sexe-ratio and size of males progeny of T. rapae was not influenced by host plants at all. However, host plants significantly influenced size of females progeny, number of pupae recovered, weigth of parasitised pupae and the percentage of parasitism, it was 50,5 % on cauliflowers and 28,5 % on swede. The findings established a direct relationship between the host plants and the parasitoids and therefore, the importance of the host plants as a factor in the success of a bioagent should also be considered.

Keys words: tri-trophic system, cabbage root fly, D. radicum, Diptera, Hymenoptera, T. rapae cruciferae, Brassica oleracea L., Brassica napus L., Brassica rapa L.

Introduction

Natural enemies of phytophagous insects function and develop in multitrophic systems. Their behaviour and physiology, determine their fitness wich are influenced by the plant (1st trophic level) and host (2nd trophic level) (Vinson, 1976; Takabayashi et al., 1991). The interaction between phytophagous insects and their parasitoids can be quite complex. Much research has focused on the relationships between plants and pests (Maxwell & Jenning, 1980) and between pests and natural enemies in attempt to estimate parasitoids efficiency in biological control (Price et al., 1980; Waage & Hassell, 1982; Rosen, 1985). The plant influence host habitat location, host searching and oviposition on behaviour of parasitoids. Effects of plants on parasitoids may be directly through physical (silhouette, contrast, colour) and chemical characteristics (volatile compounds) or indirectly, chemical cues derived from the activity of the host though not actually from the host itself (frass, honeydew) (Godfray, 1994). Trybliographa rapae W. (Hymenoptera: Figitidae) is a specialist Figitidae parasitoid of several species of Hylemya (syn. Delia) (Wishart, 1954; Hertvelt, 1970) including the cabbage root fly, Delia radicum, a species which is distributed throughout the entire north temperate region of the world. T. rapae also attacks the closely related turnip root fly Delia floralis (Fall) (Jones et al., 1993), D. Platura (Meig.), D. Antiqua (Meig.) ((Lundbald, 1913; Hammond, 1924; Wishart & Monteith, 1954; Lahmar, 1982).

135 136

The estimation of parasitoid efficiency in biological control it should be necessary to integrating the first level trophic system (Tingle & Copland, 1988; Van Emden, 1991). The tritrophic system cultivated cruciferous - cabbage root fly - parasitoid was studied under laboratory conditions in attempt to determine the effect of plants eaten by Dipteran on ecobiological carachteristics of T. rapae in order to select the best plant for masss rearing of parasitoid.

Material and methods

Plants The plants used were cauliflowers Brassica olearaceraL. and swede Brassica napusL. cultivated in a glasshouse at Rennes, watered twice a week and transeferred to the controlled insect rearing room, when reached seven leaf stage at 20 ± 1°C, 60 ± 10 % HR and L 16: 8 D for the experiment.

Insects The strain of D. radicum and T. rapae used in this study came from field in Brittany (INRA Le Rheu). T. rapae was reared in a climate controlled room, on larvae of D. radicum which fed on roots of swede. Adults were fed on droplets of accacia honey spread on cardboard support. The rearing method was described by Neveu et al., (1996).

Experimental procedure Ten females have been isolated individually at the emergence in a petri dishes with one male for mating and feeding with honey and water. Twenty four hours before the experiment, 10 second instar larvae of cabbage root fly were put on lower stem of each plant. The plants were introduced into a muslin pocket (24cm breadth, 25cm long) with one female parasitoid for 48 hours of parasitism. Every 48 hours, the females were transferred in the same muslin pocket to a new plant infested with 10 unparasitized second instar larvae of cabbage until 14 days. For each plant species, 10 replicates were respectively made. The larvae that had been exposed to the parasitoid carried on their development in controlled room until pupation about 20 to 25 days. The pupae were collected with a sieve (10 mesh/cm2) and then the pupae were kept in damp vermiculite in small plastic boxes. At the emergence of parasitoids, adults were sexed, developmental time, size (length of tibia) of males and females offspring was measured by an ocular micrometer, number of pupae recovered per female, weight of parasitised pupae, sex ratio and percentage of parasitism on each host plant were noted. The data obtained on the different parameters like, percent values, developmental time, size of offspring, number of pupae recovered and weight were subjected to Anova or to Chi-Square test. were subjected to Mean (± S.E) were separated by Fischer's PLSD multiple range test at a confidence level of 5%.

Results Developmental time The developmental time of parasitoid is the period from oviposition to emergence. On cauliflowers, the duration of males varied from 37 to 73 days and females from 38 to 59 days. On

137

Swedes, the duration of males varied from 36 to 54 days and females from 40 to 52 days. The developmental time of both sexes is not significantly affected by host plants (Tab. 1).

Table. 1. Effect of the host-plant on developmental time, the size, sex ratio and percentage of parasitism (± s.e.m)

Developmental time Length of tibia (p3) sex-ratio parasitism Host Host plants (days) (mm) (% females) (%) instar males females males females Cauliflower 44,6 ± 1,1 a 46,4 ± 1,0 a 0,83 ± 0,18 a 0,85 ± 0,13 a 53,6 ± 6,6 a 50,5 ± 6,9 a Swede L2 43,3 ± 0,7 a 45,8 ± 0,4 a 0,87 ± 0,30 a 0,92 ± 0,02 a 66,3 ± 6,4 a 28,4 ± 4,7 b test-F F = 0,333 F = 0,823 F = 2,307 F = 9,759 F = 2,148 F = 7,059 P = 0,5660 P = 0,3675 P = 0,1461 P = 0,0059 P = 0,1641 P = 0,0161 Ns Ns Ns Ns Ns S

Size of offspring The length of leg P3 tibia of two sexes emerged on two host plants was measured. For males, the size was not significantly different between 2 host plants (F = 2,30; P = 0,1461). But, the it was significantly different between 2 host plant for females (F = 9,75; P = 0,0059) (Tab. 1). The size was higher on swede.

Number of pupae recovered and weight of parasitised pupae The number of recovered pupae per female per plant and the weight of parasitised pupae were significantly different between two plants. The number of pupae recovered is 33,5 ± 5,06 on cauliflowers and 21,10 ± 5,11 on swede (Tab. 1). The weight of parasitised pupae is 0,012 g ± 0,001 g on cauliflowers and 0,007 ± 0,001 g on swede (Tab. 1). The higher number of pupae and weight was obtained on cauliflowers.

Sex ratio The sex ratio (proportion of females in the population ) of the emerging parasitoid was not significantly different between two plants 53,6 ± 6,0 % on cauliflowers and 66,3 ± 6,4 % on swede (Tab. 1).

Percentage of parasitism The percentage of parasitism is 50,5 ± 6,9 % on cauliflowers and 28,4 ± 4,8 % on swede. It was significantly higher on cauliflowers than on swede (Tab. 1).

Discussion

The developmental time of parasitoids was not influenced by host plant. T. rapae is a koinobiont parasitoid which larvae continuous to feeding and developing after parasitism (Waage, 1982). Contrary to idiobiont parasitoids which kill their hosts at the moment of infestation. This results showed a bimodal emergence, it perhaps caused by two early and late phenotype of cabbage root fly (Biron, 1998; Collier et al., 1989).

138

Neveu Bernard-Griffiths (1998) has shown that developmental time is shorter when oviposition had occurred in a third stage rather than in a first or second larval stage of cabbage root fly. The first stage of T. rapae remain at this stage until the host has reached its final developmental pupal stage of Dipteran. The total developmental time depends on host stage at the moment of parasitism (Kacem et al., 1996). The size of males was not significantly different between two host plants. But, a significant difference appears for size of females. Othors factors can influence the size and particularly the host stage at the moment of infestation; in T. rapae, the size of males and females offspring obtained on turnip (Brassica rapa L.) increase significantly when the third host stage is parasitised (Neveu Bernard-Griffiths, 1998). Many parasitoids Hymenopteran namely arrhenotokous, have a direct control of the sex ratio of their offspring produce females whereas unfertilized eggs produce males. In recent years some reviews have discussed that the parasitoid decisions taken in regard to the adaptative response influenced by many environmental and physical stimuli (Charnov, 1982; Waage, 1986; Strand, 1979; Cate et al., 1973; Kfir & Luck, 1979; Werren, 1980). The sex ratio can be influenced by many factors: a) parental age, duration of mating, genetics factors, size of females. b) The abiotics factors like photoperiod, relative humidity, and temperature. c) sex, size and host stage (King, 1987). d) differential mortality of both sexes during the developmental time (Flanders, 1956; King, 1987), superparasitism and local mate competition between larvae (Hamilton, 1967). This results showed in standardized conditions that the sex ratio is in favour of females and there is a significant absence of effect of host plants on the sex ratio of T. rapae. The sex ratio of T. rapae was not significantly different among three host stage fed on turnip roots (Neveu Bernard-Griffiths, 1998). In T. rapae, host stage and host plant have no effect on sex ratio. Nevertheless, the effect of host plant has been reported in other Hymenopterans: Trioxys indicus (Aphidiidae) (Kumar & Tripathi, 1987; Tripathi & Shukla, 1991) and Diadegma insulare (Ichneumonidae) (Idris & Grafius, 1996). Many factors can influence the parasitism rate: host size (Strand & Vinson, 1983b), chemical composition of hemolymph (Kainoh & Tatsuki, 1988), contact chemicals stimuli and plant foliar structure (Copland et al., 1993; Heinz & Parella, 1994). This results demonstrate that the parasitism rate obtained on cauliflowers was higher than on swede. This can be explained by the vegetables bark, in our observations was less hardness than on swede and perhaps the parasitoid may be attracting by the volatils compounds of host plants. In fact, Yaman (1960) and Coaker & Williams (1963) suggested that the host plant play an important role in host searching by T. rapae. Whereas, the chemicals compounds in roots and ingested by larvae of D. radicum may be different in two host plants. This can lead host survival and/or parasitoid more important on cauliflowers. In conclusion, this study shows that a direct relationships exist between host plant and parasitoid, the cultivated Brassicae have an effect on size of females offspring, number of recovered pupae, weight of parasitised pupae and parasitism rate. Cauliflowers seems to be the best host plant for mass production of parasitoids. It would be interesting to carry on this study on others cultivated and wild Cruciferae and on several generations because this results were provided by the first generation offspring obtained on swede. It is important to understand the tritrophic interaction between Brassicaceae plants, cabbage root fly and its parasitoids, especially T. rapae. This will enable us to effectively combine of host plant, variety or cultivar selection and

139

planting of wild Brassicaceae, and use T. rapae to suppress cabbage root fly populations and reduce pesticide dependence.

Acknowledgments

This work was funded by the G.I.S. «Lutte Biologique et Integrée en Cultures Légumières dans l’Ouest de la France». We thank " Conseil régional" for the financial support.

References

Biron D., 1998. Génétique des populations de Delia radicum L. (Diptera: Anthomyiidae). Thèse de Doctorat en Sciences de l'Environnement. Université du Québec à Montréal. 130 pp. Boulétreau M., 1988. Parasitisme et génétique dans le monde des insectes. La Recherche 123: 78-87. Cate R.H., Archer T.L, Eikenbary R.D, Starks K.J. & Morrison R.D., 1973. Parasitization of the greenbug by Aphelinus asychis and the effect of feeding by the parasitoid on aphid mortality. Environ. Entomol. 2: 549-553. Coaker T.H. & Williams D.A., 1963. The importance of some carabidae and Staphylinidae as predators of the cabbage root fly, Erioischia brassicae (Bouché). Entomol. Exp. Appl. 6: 156-164. Copland M.J.W, Perera H.A.S. & Heidari M., 1993. Influence of host plant on the biocontrol of glasshouse mealybug. IOBC wprs Bulletin 16 (8): 44-47. Flanders S.E., 1965. On the sexuality and sex ratio of Hymenopterous populations. Am. Nat. 909: 489-494. Godfray H.C.J., 1994. Parasitoids behavorial and evolutionary ecology. Princeton University Press, Princeton, New-Jersey: 473 pp. Hamilton W.D., 1967. Extraordinary sex ratios. Science 156: 477-488. Heinz K.M. & Parella M.P., 1994. Poinsettia (Euphorbia pulcherrima Wild. Ex Koltz.) cultivar- mediated differences in performance of five natural enemies of Bemisia argentifolii Bellows and Perring, n. sp. (Homoptera: Aleyrodidae). Biol. Cont. 4: 305-318. Hertveldt L., 1970. Incidence of Trybliographa rapae Westwood, a parasitic wasp of the cabbage root fly, Delia brassicae Bouché. Med. Fakult. Landbouww. Wetenschap. Gent. 35 (1): 105- 117. James H.C., 1928. On the life-histories and economic status of certain cynipid parasites of dipterous larvae, with descriptions of some new larval forms. Ann. Appl. Biol. 15: 287-316. Kacem N., Neveu N. & Nénon J.P., 1996. Larval development of Trybliographa rapae (Hymeno- ptera: Eucoilidae). IOBC wrsp Bulletin 19 (11): 156-161. Kainoh Y. & Tatsuki S., 1988. Host egg kairomones essential for egg-larval parasitoid, Asco- gaster reticulatus Watanabe (Hymenoptera: Braconidae). Internal and external kairomones. J. Chem. Ecol. 14: 1475-1485. King B.H., 1987. Offspring sex-ratio in parasitoid wasp. Q. Rev. Biol. 62: 367-396. Kfir R. & Luck R.F., 1979. Effects of constant and variable temperature extremes on sex ratio and progeny production by Aphytis melinus and A. lingnanensis (Hymenoptera: Aphelin- idae). Ecol. Entomol. 4: 335-344.

140

Kumar A. & Tripathi C.P.M., 1987. Parasitoid-host relationship between Trioxys indicus Subba Rao and Sharma (Hymenoptera: Aphidiidae) and Aphis craccivora Koch (Hemiptera: Aphididae): Effect of host plants on the sex-ratio of the parasitoid. Z. Angew. Entomol. 12: 95-99. Maxwell F.G. & Jenning P.R., 1980. Breeding plants resistant to insects. New York, John Wiley. Neveu N., Kacem N. & Nénon J.P., 1996. A method for rearing Trybliographa rapae W. on Delia radicum L. IOBC wprs Bulletin 19 (11): 173-178. Neveu Bernard-Griffiths N., 1998. Sélection de l'hôte chez Trybliographa rapae W. (Hymeno- ptera: Figitidae), parasitoïde de la mouche du chou Delia radicum L. (Diptera: Anthomyiidae); perspectives d'application en lutte biologique. Thèse Université de Rennes 1, 131 pp. Price P.W., Bouton C.E., Gross P., McPheron B.A., Thompson J.N. & Weis A.E., 1980. Inter- actions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann. Rev. Ecol. Syst. 11: 41-65. Rosen D., 1985. Biological control. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology. Kerkut, G.A. & Miller, M.C. (eds.), Pergamon Press, Oxford, New York. 12: 413-463. Sandlan K., 1979. Sex ratio regulation in Coccygomimus turionella Linnaeus (Hymenoptera: Ichneumonidae) and its ecological implications. Ecol. Entomol. 4: 365-378. Takabayashi J., Dicke M. & Posthumus M.A., 1991. Variation in composition of predator- attracting allelochemicals emitted by herbivore-infested plants: relative influence of plant and herbivore. Chemoecology 2: 1-6. Tingle C.C.D. & Copland M.J.W., 1988. Effects of temperature and host-plant on regulation of glasshouse mealybug (Hom: Pseudococcidae) population by introduced parasitoids (Hym: Encyrtidae). Bull. Entomol. Res. 78: 135-142 Tripathi C.P.M. & Shukla A.N., 1991. Influence of plant quality of parasitoid's fitness. In: Proceedings of the National Symposium on "Emerging Trends in the Biological Control of Phytophagous Insects" held at Madras, January, 19-21, T.N. Annanthakrishnan (ed.): 32-34. Van Emden H.F., 1991. The role of host plant resistance in insect pest mis-management. Bull. Entomol. Res. 81: 123-126. Vinson S.B., 1975. Biochemical coevolution between parasitoids and their hosts. In: Evolutionary strategies of parasitic Insects and mites. Price, P.W. (ed.), Plenum press, New York: 14-48. Vinson S.B., 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21: 109-133. Waage J.K., 1986. Family planning in parasitoids: adaptative patterns of progeny and sex allocation. In: Insects parasitoids. Waage J.K. & Greathead D.J. (eds.), Acad. Press, London: 63-95 Waage J.K. & Hassell M.P., 1982. Parasitoids as biological control agents. A fundamental approach. Parasitology 84: 241-268. Werren J.H., 1980. Sex ratio adaptation to local mate competition in a parasitic wasp. Science 208: 1157-1159. Wishart G. & Monteith A.E., 1954. Trybliographa rapae (Westw.) (Hymenoptera: Cynipidae), a parasite of Hylemya spp. (Diptera: Anthomyiidae). Can. Entomol. 86: 145-154. Yaman I.K.A, 1960. Natural control in cabbage root fly populations and influence of chemicals. Med. Landbouw. Wageningen 60: 1-57.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 141-147

Observations on the composition and effectiveness of diamondback moth (Plutella xylostella L.) parasitoids

K. Wiech & J. Kalmuk Agricultural University, Chair of Plant Protection, Al. 29 Listopada 54, 31-425 Krakow, Poland

Abstract: 11 species of parasitoids and hyperparasitoids were recovered from Plutella xyllostella cocoons collected in 1998-1999 in Mydlniki Experimental Station near Krakow. Diadegma fenestralis was the most numerous among parasitoids followed by Gelis nigricornis. Mean parasitization of Plutella caterpillars was in 1998 and in 1999. Covering early cabbage with flees decreased the number of Plutella larvae and pupae. Undersowing cabbage with white clover did not however influence the number of Plutella development stages as well as the parasitization level.

Key words: Plutella xylostella, diamondback moth, Diadegma fenestralis, parasitoids, undersowing, white clover pheromone traps

Introduction

The diamondback moth (Plutella xylostella L.) is one of the most severe pest of cabbage and other related cruciferous crops in Poland as well as in many other countries (Abraham, Padmanagan,1968; Hamilton, 1979; Kempczynski, 1983; Sastrosiswojo 1996). Chemical and biological control of this pest has been the subject of intensive research in different parts of the world (Iga, 1997; Pell, Wilding, 1994; Sastrosiswojo, 1996; Shelton et al., 1993). Caterpillars feed on leaves making small holes and „windows”, but may also destroy the growing point which stops from cabbage forming heads (Kempczynski, 1983). Numerous studies have shown that the population of diamondback moth can be reduced by parasitoids belonging to genus Diadegma (Ali, Karim, 1995; Iga, 1997; Harcourt, 1960; Lagowska, 1981; Rahn, Chevallereau, 1996; Wiech, Jankowska, 1999). However, not too much attention has been paid to the role of other parasitoids as well as to the effect of undersowing cabbage with white clover and other cultural methods on the effectiveness of diamond-back parasitoids.

Materials and methods

Observations were carried out at the Agricultural University Experimental Station in Mydlniki near Krakow. We used a randomised block design with four replications. In 1998 two cultivars of white cabbage were used: early - Pierwszy Zbior and late - Kamienna Glowa. On the next year only late cabbage was applied. The brassica plants were grown from seeds in plastic modular trays in a greenhouse and then planted in the field. Early cabbage was covered with flees (for 4 weeks), and late cabbage was undersown with white clover (local cultivar Podkowa). Clover was sown on the beginning of April and early cabbage was planted on 21 April. Late cabbage was planted on 18 May between the rows of white clover.

141 142

IPO-DLO pheromone traps were used to observe the population dynamics of Plutella xylostella. Two traps were placed inside the experimental area in 1998 and 1999. Each trap was examined every 3 days and all captured Plutella males were counted. Observations of the occurrence of diamond-back larvae have been carried out weekly through the whole season. Each time, all larvae and pupae were counted on 10 randomly selected cabbage plants. Moreover the last stage larvae and all pupae were placed in separate vials and reared to recover moths or parasitoids and to find the percentage of parasitization. The recovered parasites were identified by DR B. Miczulski from the Agricultural University in Lublin.

Results

Observations on the occurrence of Plutella xylostella moths, larvae and pupae The first diamond-back adults were captured into pheromone traps in the beginning of June (1998) and in the second half of July (1999). Twice as much moths were captured in 1998 than in 1999 and the last adults were observed in the traps one week longer in 1998 than in 1999 (Fig. 1). Graphs of Plutella population dynamics showed the presence of three generations of Plutella and are the useful tool in monitoring this pest population.

9 8 7 6 5 4 3 2 1 0 21. 28. 04. 11. 18. 25. 02. 09. 16. 23. 30. Mai Mai Jun Jun Jun Jun Jul Jul Jul Jul Jul

Fig. 1: Number of Plutella xylostella adults captured in pheromone traps in Mydlniki (1998)

The mean number of diamondback larvae and pupae per one plant was much higher in 1998 than in 1999 (Fig. 2 and Tab. 1) In 1999 we had to search all plants on plots to find scarce larvae which occurred on the plants. The artificial cover (flees) didn’t significantly decreased the infestation of early cabbage in comparison with the control (Tab. 1). The infestation of cabbage occurred after removing cover from the plants. No effect on diamond-back moth population was also observed in case of undersowing cabbage with white clover.

143

9 8 7 6 5 4 3 2 1 0 30. 06. 13. 20. 27. 04. 11. 18. 25. 01. Mai Jun Jun Jun Jun Jul Jul Jul Jul Aug

Fig. 2: Number of Plutella xylostella adults captured in pheromone traps in Wegrzce (1999)

Table 1. Number of Plutella xylostella larvae and pupae collected from cabbage according to the type of cultivation (Mydlniki, 1998)

early cabbage late cabbage cabbage covered cabbage cabbage with white cabbage date with flees clover larvae pupae larvae pupae larvae pupae larvae pupae 1 July 30 2 43 24 27 2 26 6 8 July 62 73 72 67 15 8 23 11 16 July 37 84 16 100 13 11 16 19 22 July – – – – 3 7 8 10 29 July – – – – 3 3 6 1 total 129 159 131 191 61 31 79 47

Table 2. The results of rearing Plutella xylostella pupae (1998)

number of decade of collected recovered parasitoids recovered moths dead pupae the month pupae number % number % number % II/June 15 4 93.3 0 0 1 6.7 III/June 241 187 77.6 23 9.5 31 12.9 I/July 408 360 88.2 8 2.0 40 9.8 II/July 434 387 89.2 2 0.5 45 10.3 III/July 191 147 77.0 4 2.1 40 20.9 total 1289 1095 37 156 144

The composition of parasites and hyperparasites recovered from Plutella cocoons In 1998, 1095 specimens of parasitic wasps belonging to 11 species were reared out from 1289 diamond-back moth cocoons (Tab. 2). The most numerous of all obtained specimens was Diadegma fenestralis – 90.22% (Tab. 4). The second numerous species was Gelis nigricornis which is the parasite of D. fenestralis larvae. Other species both Plutella parasites and second stage parasites (hyperparasitoids) occurred much less numerous (about 5% of all recovered). In 1999 only 208 larvae and pupae and empty Plutella cocoons were collected from the plots with late cabbage. Only 5 moths of Plutella xylostella were recovered from the cocoons. Among 133 parasitoids which were reared out in laboratory 127 were Diadegma fenestralis. Most of the parasitoids, in two years of observations were reared out in July. In 1999 the last parasitoids were reared out in the laboratory in the last days of August.

Table 3. Number of parasitoids and diamond-back moths recovered from the collected cocoons (Mydlniki, 1999)

Date Number of Number of parasitoids Plutella moths no. % % 21 June 3 100.0 – 0 6 July 1 100.0 – 0 14 July – 0 – 0 22 July 56 96.6 2 3.4 29 July 13 92.9 1 7.1 5 August 10 83.3 2 16.7 11 August 2 100.0 – 0 25 August 7 100.0 – 0 Total 92 5 % 94.8 5.2

Table 4. The composition of parasitoids recovered from Plutella xylostella L. cocoons (1998)

Species Number of % Kind of parasitization speciments Diadegma fenestralis 988 90.22 Parasite of dbm larvae Gelis nigricornis 46 4.20 parasite of D. fenestralis larvae Diadromus collaris 18 1.64 Parasite of dbm pupae Mesochorus spp. 17 1.55 hyperparasitoid Diadegma semiclausum 5 0.45 Parasite of dbm larvae Cotesia fuliginosus 9 0.82 Parasite of dbm larvae Cotesia rubecula 3 0.27 Parasite of dbm larvae Cotesia longipalpis 2 0.18 Parasite of dbm larvae Eupteromalus sp. 3 0.27 hyperparasitoid Habrocytus sp. 2 0.18 hyperparasitoid Macroneura vesicularis Retzims 1 0.09 hyperparasitoid Total 1094 100.00 145

Table 5: The composition of parasitoids recovered from Plutella xylostella L. cocoons (1999)

Species Number of % speciments Diadegma fenestralis 81 92.0 Diadegma semiclausum 2 2.3 Diadromus collaris 2 2.3 Gelis nigricornis 3 3.4 Total 88 100.0

Preliminary studies on the development simple key for recognizing parasitoid cocoons All parasite cocoons were compared, photographed and drawn to show the differences in their appearance (Figure 3). In case of Diadegma the cocoons are brown, black whitish or gray with a white narrow strip in the middle part. The hole left after leaving cocoon by the parasitoid is placed in the top part of it. The holes left by Gelis, Mesochorus and Hemiteles were in the under- top part of the cocoon. In case of Habrocytus, Eupteromalus and Macroneura the holes were found in the middle part of the cocoon.

Fig. 3: Pictorial key to parasitsed cocoons of Plutella xylostella and the parasitoid species emerging 146

Cocoons left by Cotesia species are white or yellowish. The hole left by parasite is placed in top part of the cocoon with the characteristic cap-shaped cover connected with the rest of the cocoon. Diadromus collaris is the parasite of Plutella pupae. The diamond-back pupae cover in case of parasitization is brown and in case of unparasitised white/semitransparent.

Discussion

Until recently in Poland, little attention has been paid either to Plutella xylostella or its parasitoids. Studies on the biology of the diamond-back moth were carried out only by Kempczynski (1983) and the composition as well as the effectiveness of Plutella parasitoides were studied by Lagowska (1981) and Wiech, Jankowska (1999). The obtained results confirmed that Plutella xylostella is one of the most numerous cabbage pests in Krakow region and its abundance fluctuates from one year to another. Similarly to the former studies, Diadegma fenestralis was the most abundant and the most effective among all recovered parasitoids. The parasitoid composition differed from the results obtained in former years. More parasitoids were reared out in 1998 than in former years. Only Oomuzus sokolovskii was not recovered from Plutella cocoons in 1998. Until now no studies were carried out on the appearance of Plutella parasitoid cocoons. The simple key presented in this paper (in some cases based on a very scarce material) is the first trial of preparing simple tool for farmer advisers and vegetable producers.

Acknowledgments

We thank Dr. Bartlomiej Miczulski from the Agricultural University of Lublin for his identification of the parasitoids of Plutella xylostella L.

References

Abraham, E.V. & Padmanagan, M.D. 1968. Bionomics and control of the Diamond-back moth, Plutella maculipennis Curtis. Indian J. Agric. Sci. 38: 513-519. Ali, M.I. & Karim, M.A. 1995. Host range abundance and natural enemies of diamond-back moth in Bangladesh. Bangladesh Journal of Ent. 5(1-2): 25-32. Harcourt, D.G. 1960. Biology of Diamond-back moth, Plutella maculipennis (Curt.) (Lepidoptera, Plutellidae), in Eastern Ontario, III. Natural Enemies. Canadian Entomologist 92: 419-428. Hamilton, J.F. 1979. Seasonal abundance of Pieris rapae (L.), Plutella xylostella (L.) and their diseases and parasites. Gren. Appl. Ent. 11:59-66. Idris, A.B. & Grafius E. 1993. Pesticides affect immature stages of Diadegma insulare (Hymenoptera: Ichneumonidae) and its host, the diamond-back moth (Lepidoptera: Plutellidae). J. Econ. Ent. 86(4): 1203-1212. Iga, M. 1997. Effect of release of the introduced ichneumonid parasitoid Diadegma semiclausum (Hellen) on the diamond-back moth, Plutella xylostella (L.) in an experimental cabbage field. Jap. J. Appl. Ent. Zool. 44(4): 195-199. Kempczynski, L.S. 1983. Badania nad szkodliwoscia tantnisia krzyzowiaczka (P. maculipennis Curt.) (Lepidoptera: Plutellidae). Roczniki Nauk Roln. 13(1-2): 62-72. 147

Lagowska, B. 1981. Ichneumonidae and Braconidae (Hymenoptera) parasites of Plutella maculipennis Curt. (Lepidoptera, Plutellidae) in Poland. Polskie Pismo Ent. 51: 355-362. Pell, J.K. & Wilding, N. 1994. Preliminary field caged trial, using the fungal pathogen Zoophthora radicans Brefeld (Zygomycetes: Entomophtorales) against the diamond-back moth, P. xylostella L. (Lepidoptera: Yponomeutidae) in the UK. Biocontrol Science Technology 4(1): 71-75. Rahn, R. & Chevallereau, M. 1996. Brassica Lepidoptera and their parasitoids in Brittany. IOBC wprs Bull. 19(11): 179-183. Sastrosiswojo, S. 1996. Biological control of diamond-back moth in IPM systems: case study from Asia (Indonesia). BCPC Symposium Proc. 67: 15-32. Shelton, A.M., Robertson, J.L. Tang, J.D. Perez, C., Eigenbrode, S.D., Priesler, H.K., Wilsey, W.T., Colley, R.J. 1993. Resistance of diamond-back moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the field. J. Econ. Ent. 83(3): 697-705. Wiech, K. 1993. The influence of intercropping late cabbage with white clover and French bean on the occurrence of pests and beneficial insects. Agric. Univ. of Krakow, habilitation desert. No. 177. Wiech, K. & Jankowska B. 1999. Preliminary observations on Diadegma fenestralis a parasitoid of the diamond-back moth, Plutella maculipennis. IOBC wprs Bull. 22(5): 145-149.

148

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 149-153

Biological control with Chrysoperla lucasina against Aphis fabae on artichoke in Britany (France)

J.C. Maisonneuve 1 , N. Hugon 2 & F. Lolivier 2 : Plant Protection Service (SRPV) Brittany, Brest (France) 2 FE.RE.DEC

Abstract: The black aphid, Aphis fabae (Scop.) (Hom., Aphididae) is with the green aphid Capitophorus horni (Börner) the main pest on artichoke crop. Flowerheads with aphids can not be sold. That’s why, since 1994, open field experiments have been taken on to settle a strategy of Integrated Pest Management (IPM) against this pest with Chrysoperla lucasina (Lacroix) (Neur., Chrysopidae). Green lacewing larvae eat aphids. In 1996, the results are the most significant ones. These experiments show up the action of the green lacewing on the black aphid, the need of defining an adapted strategy of releases and interactions with the beneficial fauna, particularly with lady birds.

Keywords: Biological control, artichoke, Chrysoperla lucasina (Lacroix), green lacewing, Aphis fabae, Capitophorus horni, Coccinella septempunctata, lady bird.

Introduction

In Britanny, the climate is particularly favourable to the artichoke crop (Cynara scolymus L.). 50.000 metric tons are produced in a year on 11.000 hectares. The black aphid, Aphis fabae (Scop.) (Hom., Aphididae) is with the green aphid Capitophorus horni (Börner) the main pest on this crop (Maisonneuve et al. 1981; Collet, 1997). It colonizes flowerheads which can not be sold. Since 1994, open fields experiments have been taken on to settle a strategy of Integrated Pest Management (IPM) against this pest with Chrysoperla lucasina (Lacroix) (Neur., Chrysopidae). The interest of the green lacewing is its carnivorous larvae (Malet, 1994). A larva can eat 300 to 500 aphids during its development. The aim of these experiments is to work out a strategy of releases in order to hold the populations of black aphids below the intervention thresholds. In 1996, the results are the most significant ones.

Materials and methods

Experimental conditions In 1996, the experiment takes place on a second-year artichoke crop. The variety is called “Camus de Bretagne”. Located at the CATE (Comité of Technical and Economical Action) experimental station in Saint-Pol-de-Léon (France), the area of 1728m² has been divided in 24 elementary plots of 6m x 12m. Each one includes 72 plants. The experiment has 4 modalities, 6 replications each: CU: Control Untreated, CT: Control Treated, ethiophencarb (24/04) and pyrimicarb (07/06), C3x7: 3 releases of 7 larvae/m², each 15 days, 09/05, 22/05 and 05/06, C5x4: 5 releases of 4 larvae/m², each 15 days, 18/04, 02/05, 15/05, 29/05 and 13/06.

149 150

Chemical treatments are done with active ingredients chosen according to their compatibilities with C.lucasina. Table I sum up those registrated against aphids on artichoke crop.

Table 1: Active ingredient: compatibilities with C. lucasina (1 no toxic ⇒ 4 very toxic).

Active ingredient Compatibility with B.C. Persistence (in weeks) Dichlorvos 4 0.5 Rotenone 2-4 2 Ethiophencarb 3-4 0.5 Deltamethrin 2-4 8 Heptenophos 4 1 Omethoate 3-4 8 Pirimicarb 1-2 1 Lambda-cyhalothrin 4 8-12 Acephate 4 > 6 Endosulfan 1-4 2 Source: Biobest, Koppert, ACTA

Strategy of releases C. lucasina are mass reared and supplied by the laboratory of the Plant Protection Service (SRPV) in Brest. The larvae are fed with eggs of Ephestia kuehniella, the adults are fed with a mixture of yeast, pollen and honey. Late first stage-early second stage larvae are wrapped up in plastic boxes with husk of buckwheat and some eggs of E. kuehniella. They are spread by hand, as homogeneously as possible. The quantity of release is 20L/m², two strategies: 3 releases of 7 L/m² or 5 releases of 4 L/m².

Assessment procedure Weekly counts allow to follow the evolution of the populations of black aphids and of the beneficial fauna. On each elementary plot, 8 marked plants are totally examined (leafs and flowerheads). The 72 plants of each elementary plot are twice examined: first time on the 07/06 (beginning harvesting), second time on the 09/07 (half harvesting). Absence or presence of the black aphid is recorded on flowerheads.

Results

Figure 1 presents the evolution of the population of black aphids. The arrival of the first black aphids is observed in the beginning of may on control plots (CU). Six weeks later, they are present on plots with C. lucasina releases. Treated plots sustain a very weak infestation. The infestation by A. fabae is greater on control plots than on the others where a regulation probably took place. On the 07/06, the notations on the whole plants did not give any significant result. At this date, there were few aphids. Figure 2 presents the percentages of infested plants on the 09/07 for the 4 modalities.

151

90 80 70 CU 60 CT 50 C5*4 40 C3*7

on a plant 30 20 10 Number of black aphids 0 28.3 4.4 12.4 18.4 25.4 2.5 9.5 15.5 22.5 29.5 5.6 13.6 20.6 4.7 11.7 Dates

Fig. 1: Evolution of the populations of black aphids for the 4 modalities.

10 8 A 6 AB 4 2 B B 0 CT C5*4 C3*7 CU Percentages of infested plants Fig. 2: Percentages of infested plants for the 4 modalities on the 09/07.

7 6 A 5 4 3

on a plant 2 BBB 1

Means of lady bird larvae 0 CU C 3*7 C5*4 CT Fig. 3: Means of lady bird larvae on a plant for the 4 modalities.

The two modalities with releases of green lacewings present intermediate rates of infestation between treated plots (2.8%) and untreated plots (8.8%). A statistic analysis (Newman-Keuls test, 5%) allows to define 3 groups as indicated on Fig.2: Group A: CU, 8.8% of infested plants, Group AB: C3x7, 6.7% of infested plants, Group B: C5x4, 3.8% of infested plants and CT, 2.8% of infested plants. There is no 152

significant difference, concerning rates of infestation, between treated plots and those with 5 releases of 4 L/m². Furthermore, these two modalities present a lower infestation in comparison with the control plots. During the weekly observations, lady bird larvae are recorded on the 8 marked plants on each elementary plot. Figure 3 indicates the means of Coccinella septempunctata L. larvea counted on a plant for the 4 modalities. Higher numbers of lady bird larvae have been recorded on control plots (CU). A Newman-Keuls test (5%) indicates two homogeneous groups: Group A: CU, 6.5 larvae on a plant, Group B: C3x7, 2.2 larvae; C5x4, 0.5 larvae and CT, 0.2 larvae on a plant. Lady bird larvae are significantly more numerous on the plants of the control plots.

Discussion

Figure 1 shows up the capacity of green lacewings to delay the settle of black aphids on artichoke crop and to regulate the infestation. The percentages of infested plants on the 09/07 are statistically homogeneous on treated plots and on the plots with 5 releases of 4 L/m². This strategy of releases is as effective as the chemical treatment. The rate of infestation is significantly lower than in the control plots. The C5x4 strategy is more effective than the other. In the first one, the releases begin earlier, green lacewing larvae are better fixed when black aphids arrive. Figure 2 and statistic test show an incompatibility between chemical treatment with ethiophencarb and lady birds on the one hand, and an antagonism between green lacewings and lady birds on the other hand. Table 1 indicates a strong toxicity of ethiophencarb against C.lucasina, and for lady bird larvae. At the time of the first releases of the C3x7 modality, earlier fixed lady bird larvae probably ate the green lacewing larvae. Earlier C.lucasina releases increase their installation to the detriment of lady bird larvae. From 1994 to 1998, 11 experiments have been taken on. They have confirmed the action of green lacewing, two of them were very significant.

Conclusion

C.lucasina larvae are able to delay the installation of black aphids and to regulate the infestations on an artichoke crop in open fields, until the natural beneficials settle. An adapted strategy may be as effective as a chemical treatment. The C5x4 strategy is improved by early releases which increase the installation of green lacewings. When a population of lady birds is yet installed on a crop, releases of C.lucasina are ineffective because of the competition between lady birds and green lacewings.

Resumé

Le puceron noir, Aphis fabae (Scop.) (Hom., Aphididae) est avec le puceron vert Capitophorus horni (Börner) le principal ravageur de la culture d’artichaut. Sa présence au niveau des capitules empêche la commercialisation des produits. C’est pourquoi, depuis 1994, des expérimentations de plein champ sont menées afin de mettre au point une stratégie de Protection Biologique Intégrée (PBI) contre ce ravageur à l’aide de Chrysoperla lucasina (Lacroix) (Neur., Chrysopidae). Les larves de cette chrysope sont aphidiphages. Parmi les résultats obtenus, ceux de 1996 sont les plus significatifs. 153

Ces expérimentations ont mis en évidence l’action de la chrysope sur le puceron noir, la nécessité de définir une stratégie d’apport adaptée ainsi que des interactions avec la faune auxiliaire, en particulier avec les coccinelles.

References

Canard, M., Semeria, Y., New, T.R. 1984: Biology of Chrysopidae. Dr W.Junk Publishers. 294 pp. Collet, J.M. 1997: Puceron de l’artichaut en Bretagne: plus de trente ans d’histoire. Aujourd’hui et demain 53: 9-13. Maisonneuve, J.C., Collet, J.M. 1995: Un nouveau prédateur contre les pucerons: Chrysopa lucasina. Aujourd’hui et demain 47: 5-6. Malet, J.C., Noyer, C., Maisonneuve, J.C. & Canard, M. 1994. Chrysoperla lucasina (Lacroix) (Neur., Chrysopidae), prédateur potentiel du complexe méditerranéen des Chrysoperla Steinmann: premier essai de lutte biologique contre Aphis gossypii Glover (Hom., Aphididae) sur melon en France méridionale. J. Appl. Ent. 118: 429-436. 154

155

Undersowing or Intercropping Crops

156

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 155-161

Detailed studies of how undersowing with clover affects host-plant selection by the cabbage root fly

K. Morley & S. Finch Horticulture Research International, Wellesbourne, Warwick CV35 9EF, UK

Abstract: Detailed experiments were done to try to explain the lack of consistency in some of the published data concerning how undersowing affects host-plant selection by pest insects. The results showed that host-plant selection by the cabbage root fly was affected considerably by 1) the distance of separation between the host-plant and the surrounding non-host plants. Host-plant selection was affected also by 2) the difference in height between the host and non-host plants; and by 3) the leaf area (overall size) of the host plant. In contrast, host plant selection by the fly was not affected by the orientation of the leaves of the host-plant. Therefore, the relative condition of the crop plants and the undersown background at the time of fly infestation governs the level of control that can be achieved from undersowing. The present results help to explain why some of the conclusions published by earlier authors were not always consistent.

Key words: Undersowing, clover, cabbage root fly, Delia radicum,

Introduction

Conclusions published on how diverse backgrounds affect host-plant selection by pest insects have not always been consistent (see Andow, 1991; Altieri, 1994), primarily because many data have been collected in the field where it is difficult to ensure that only one factor varies at a time (Finch & Kienegger, 1997). It appears that many of the anomalies described by earlier authors can be attributed to the different visual images produced by the host or the non-host plants. For instance, in many experiments no mention was made of the relative heights of the host plants and the surrounding vegetation. However, Finch & Kienegger (1997) showed that it was necessary to have part of the vertical profile of the host plant covered by clover, for the clover to reduce the levels of infestation by this fly. Similarly, O’Donnel & Coaker (1975) found that, to reduce fly infestations, it was necessary to cover at least 60% of the bare soil in the interrow spaces. This ‘critical’ level may not have been achieved by some of the earlier authors. In addition, it is well known (Vandermeer, 1989) that competition from clover affects the height, the combined leaf area (or size) and the leaf orientation of the brassica plants. Hence, considerable detailed work is still needed if we are to obtain a better understanding of how undersowing produces the effects that are beneficial for crop protection. This paper describes experiments to show how host-plant selection by the cabbage root fly is affected by 1) the distance from the surrounding clover to the brassica plants, 2) the difference in height between the brassica plants and the clover, 3) the size of the host plants, and 4) the orientation of the leaves on the host plants.

Materials and methods

Insects The cabbage root flies were obtained from a continuous laboratory culture (Finch & Coaker, 1969). The 50 or 100 female flies, used in each test cage, were of a similar age and always

155 156

more than 5 days old. The flies were denied an oviposition site for 2 days prior to the start of each test. All of the laboratory experiments were done in a constant environment room maintained at 24 ± 2°C during the light period and 16 ± 1°C during the dark period, and with a L16:D8 photoperiod.

Plants Cauliflower (Brassica oleracea var. botrytis L.) plants grown from seed were kept under glasshouse conditions in Hassy 308 plant modular trays (Erin Planter systems Ltd., Baldock, Herts, England, UK). Two weeks prior to the start of each experiment, the numbers of plants required for the tests were transplanted into 7.5 cm diameter pots. Subterranean clover (Trifolium subterraneum, L.), cv. Goulburn., was used as the plant for the non-host background. For the field experiment, the clover was sown as three 40m long x 2m wide beds during April 1998. The experiment was done in July 1998, to allow sufficient time for the clover to grow to the required height. For the laboratory experiments, trays of clover were sown each week during the test period, to produce clover of different heights

Pre-selection of test plants Results indicated that although the visual appearance of the individual plants within a batch appeared similar, the plants varied greatly in their ability to stimulate flies to lay. Therefore, 20-25 plants were screened in preliminary tests and four plants, on which similar numbers of eggs were laid, were chosen for the main tests. Each plant selected was presented in a different background during the four repeats of each experiment

Models and artificial backgrounds Artificial brassica leaves were made by photocopying all of the leaves pulled from a living plant and then using the outlines obtained to cut the appropriate shapes out of green cardboard. By wiring the artificial leaves to a green carnation cane, the leaves could be assembled into the shape of an ‘artificial plant’. The photocopier was used also to reduce or enlarge the size of the individual leaves so that test plants could be constructed that were 0.25, 1, 2.25 or 4 times as large as those of the original plant. Green cardboard was used also as one of the backgrounds for the leaf area and leaf orientation experiments. The cardboard was cut to cover the surface of each test tray and then a hole was made in the centre of each card to accommodate a square 7.5 cm plant pot.

Experimental arena This consisted of a metal framed test chamber made of two equal-sized compartments (1.1 m x 1.1 m x 1.1 m) positioned one above the other. Each compartment contained a 95 cm diameter turntable that made one revolution/minute. The rotation ensured that everything placed on the turntables was exposed equally to the flies which aggregated near to the strip lights used to illuminate the cage.

The experimental set-up In all laboratory tests, a brassica plant was inserted into the centre of a seed tray that contained 1) clover, 2) an artificial background, or 3) bare soil. For the experiments in which fly eggs were counted, the compost surrounding the plants was spread with a layer of silver sand, about 1cm thick, and then covered with sieved field soil (2mm mesh). The eggs were separated from the soil by flotation, (Kostal & Finch, 1994).

157

Experimental

1. Distance of separation between the test plant and the surrounding clover Instead of making the circular bare soil areas by digging up the clover, heavy wooden discs were pressed down firmly on top of the clover to de-limit the test areas. Discs measuring 1 m, 60 cm, 30 cm and 15 cm in diameter were cut from sheets of 9 mm plywood. A 7.5 cm square hole was cut in the centre of each disc to accommodate a test plant growing in a square 7.5 cm plant pot. Two further treatments, 7.5 cm and 0 cm diameter, were made by digging holes at the appropriate positions within the 40m long beds of clover and placing a potted plant in each hole. In the 0cm treatment, foliage from the adjacent clover plants was pulled across the pot to cover the soil directly beneath the plant. Once the discs were in position, the test plants were inserted and the top of each plant pot was made level with the surface of the board. The wood was then covered with sieved field soil. The treatments were arranged as a 6 x 6 randomised Latin square, which had to be split into two to accommodate the narrow (40m x 6m) shape of the field plot. Each plot was 1 m2 and was separated from adjacent treatments by a 1 m wide ‘guard’ area. Every 3-4 days, the plants were replaced and the eggs in the soil around the base of the test plants were counted. The experiment was replicated through time on four occasions. A robust (r2 =0.93) linear relationship was found between the numbers of cabbage root fly eggs recovered and the distance the brassica plants were from the surrounding clover. The relationship between numbers of fly eggs laid and distance of separation is given by ‘loge mean egg numbers = 0.0493 (radial distance in centimeters) + 1.491’.

2. Effect of height of clover on egg-laying and landing by the cabbage root fly Four test plants were surrounded by backgrounds of 1) bare soil; 2) tall clover; 3) medium clover; and 4) short clover and then placed into the test arena. The experiment was repeated four times for each of three different periods of exposure; 24h, 12h and 6h. Eggs were recovered by flotation and counted. The numbers of flies that landed on the host plants and on the four test backgrounds were recorded during the last 30 minutes of each experiment. More eggs were laid around the test plants presented in backgrounds of bare soil than around those presented in clover (P<0.001) . The number of eggs laid alongside the test plants decreased (P<0.001) as the height of the surrounding clover was raised (Fig.1). The length of time (6,12 or 24 hours) the brassica plants were exposed to the flies also had a pronounced effect on the numbers of eggs laid (P<0.001). Flies landed more frequently on the plants in the bare soil background than on the plants surrounded by clover (P<0.001). Flies also landed more frequently on the clover backgrounds than on the bare soil (P<0.001). In addition, there was an inverse linear relationship between the log transformed number of flies that landed on the brassica plant and the height of the clover background (P<0.001) (Fig. 1). Most (P<0.001) landings were recorded on the highest clover background and fewest (P<0.001) on the bare soil (Fig. 1). There was also an interaction between the duration of the experiment (6-24h) and the number of landings made on the host plants presented in the clover and bare soil backgrounds (P<0.05). As this interaction accounted for only a small amount of the overall variation, the order of preference for plants in the different backgrounds did not change between the three exposure periods. Therefore, the relative numbers of landings, shown for the 12h exposure in Fig. 1, appear representative for all clover treatments.

158

100

o .

f l

80 y

l a

40 n d

60 i

n g

60 s

40 o

80 l o

20 v e 100 r No.fly landingson brassica 0

Tall Medium Short Bare soil

Clover background Fig. 1. The relative numbers of fly landings recorded on the brassica plants and the corresponding clover or bare soil background.

3. The effect of leaf area and plant size on the number of fly landings Artificial plants of four different leaf areas were presented against a background of either green card or bare soil. The two backgrounds were each tested for 15 minutes during the 30 minute duration of each experiment. The numbers of flies that landed on the model plants and backgrounds during this period were counted. The experiment was repeated on three occasions for both backgrounds.

3 fly landings on plant

e 2 log

1 012345 Relative plant area Fig. 2. The number of fly landings recorded on four different sizes of artificial plants presented against backgrounds of either bare soil (ο) or green card (•).

There was a positive (P=0.001) linear relationship between the numbers of fly landings and the areas of the plant leaves when the models were presented against backgrounds of both green card and bare soil (Fig. 2). As leaf size was increased, more (P=0.001) fly landings were recorded on the models and fewer on the backgrounds. In addition, as in the earlier experiments, more (P=0.01) flies landed on the green card than on the bare soil background.

159

4. Effect of leaf orientation on the numbers of fly landings on the host plant Pots containing model leaves, aligned at 0°, 30°, 60° and 90° to the vertical, were presented to the flies against backgrounds of both green card or bare soil. The numbers of flies that landed on the various leaves were counted for 15 minutes against the bare soil backgrounds and 15 minutes against the green card backgrounds. To avoid any possible bias arising from exposing the flies initially to either the green or the bare-soil background, the order in which the backgrounds were presented was alternated between runs. The experiment was repeated 5 times for each background. Similar numbers of fly landings were recorded on all model leaves irrespective of the angles at which the individual leaves were presented. Changing the background from green card to brown soil did not affect the results (P=0.05).

Discussion A clear relationship exists between the proximity of the surrounding clover to the host brassica plant and the numbers of eggs laid by the cabbage root fly. Prokopy et al. (1983a) found that visual stimuli became important in host-plant finding by the cabbage root fly once the insects were within 40- 60 cm of a host plant. The current results showed that the response of the flies to visual stimuli from the host plant was disrupted when other green objects were positioned within 0-50cm of the host plant. The extent of this disruption, however, was related directly to the distance of separation between the host and non-host plants and it was the lack of information on such details that gave rise to many of the earlier inconsistent results. Linear relationships were found also between the height of the clover background and the numbers of landings made on both the host plants and on the clover. The present results indicate that a relationship may exist also between the relative height of the host-plant above the clover background and the numbers of eggs laid on the specific host plant. This again indicates how precise the information has to be if the effects of undersowing on pest insect species are to be determined accurately. In many of the earlier studies, the relative heights of the crop and the undersown plants were never recorded. In the experiments concerning the height of the clover background, more flies landed on host plants surrounded by bare soil backgrounds than on plants surrounded by clover. This confirms earlier findings (e.g. Kostal, 1991; Kostal & Finch 1994) which showed an increased number of fly landings on objects which contrasted greatly with their background. The number of fly landings on the model leaves and the model plants was not affected when the background was changed from brown to green. This result appears to contradict earlier findings (Ryan et al., 1980; Kostal & Finch, 1994; Finch, 1995) which showed that when brassica plants were presented in any green background both the number of landings on the brassica plants and the numbers of eggs laid were reduced considerably. The present result confirms the findings of Liburd et al. (1998) who applied a green hydromulch, a treatment that involved spraying wood fibre plus adhesive onto the surface of the soil, providing a background which was low in comparison to the height of the host plant. These authors recovered similar numbers of fly pupae at harvest from around the roots of brassica plants sprayed with hydromulch as from around the roots of plants growing in bare soil. A similar situation had been noted in 1992 by Finch & Edmonds (unpublished data) when they tried to reduce damage from this fly by growing Brussels sprout plants in ‘Astroturf’, a plastic artificial turf used as a surface for field sports. In this case, more fly pupae were recovered from around the plants growing in the green Astroturf than from around those growing in bare soil. However, such results may not all arise solely from differences solely in fly oviposition, as both materials are highly effective mulches. Hence, when compared to bare soil, both 160

coverings would reduce considerably the numbers of fly larvae that died from desiccation. Finch & Kienegger (1997) noted that in undersown crops, more than 50% of the vertical profile of the plant needed to be covered to reduce oviposition by the cabbage root fly. Similarly, the present results indicate that it is the “contrast” in height and not colour that is the important factor in reducing fly landings on plants in living backgrounds. The results from the present experiments showed that there was a linear relationship between model plant area and the number of flies that landed on the plants. This confirms previous findings (Roessingh & Stadler, 1990; Kostal, 1993) and indicates that plant height is not the only factor that contributes to “plant apparency” (Feeny, 1976). In the experiment involving clover of different heights, it was often necessary to move the clover foliage to expose similar areas of the brassica plants in each background. In many cases, this changed the angles of orientation of the leaves on the host plants, a change that is induced often by undersown crops (Vandermeer, 1989). Hence, it was thought that the orientation of the leaves might influence the number of fly landings, as previous studies had shown that the orientation at which sticky traps were angled had a pronounced effect on the number of flies that landed (Finch & Collier, 1989). The horizontal and vertical components of leaf models and traps have been found also to make such objects more apparent to flies (Roessingh & Stadler, 1990; Kostal, 1993). Therefore, changes in leaf orientation might have been expected to alter the attractiveness of plants to flies. In the current experiments the differences between landings on the leaves presented at various angles were not significant. The different leaf orientation of brassica plants growing amongst clover is therefore not a major factor influencing fly landings in undersown crops. It is clear from the present results that if the full benefits from undersowing are to be obtained against this fly, the proximity of the clover to the crop plants and the height of the clover background relative to that of the crop plants will need to be regulated carefully.

Acknowledgement

We thank Marian Elliott and Martin Torrance for help with the experimental work.

References

Altieri, M.A., 1994. Biodiversity and Pest Management in Agroecosystems. Haworth Press Inc., New York: 185 pp. Andow, D.A., 1991. Vegetational diversity and arthropod population response. Annual Review of Entomology 36: 561-586. Feeny, P.P., 1976. Plant apparency and chemical defence. In: J. Wallace & R. Mansell (eds.), Biochemical Interactions Between Plants and Insects. Recent Advances in Phytochemistry 10: 1-40. Finch, S.,1995. Effect of trap background on cabbage root fly landing and capture. Entomologia Experimentalis et Applicata 74: 201-208. Finch, S. & T.H. Coaker, 1969. A method for the continuous rearing of the cabbage root fly Erioischia brassicae (Bouche) and some observations on its biology. Bulletin of Biological Research 58: 619-627. Finch, S., & Rosemary H. Collier, 1989. Effects of the angle of inclination of traps on thenumbers of large Diptera caught on sticky boards in certain vegetable crops. Entomologia Experimentalis et Applicata 52: 23-27. Finch, S. & M. Kienegger, 1997. A behavioural study to help clarify how undersowing with clover affects host-plant selection by pest insects of brassica crops. Entomologia 161

Experimentalis et Applicata 84:165-172. Kostal, V., 1991. The effect of colour of the substrate on the landing and oviposition behaviour of the cabbage root fly. Entomologia Experimentalis et Applicata 59: 189-196. Kostal V., 1993. Oogenesis and oviposition in the cabbage root fly, Delia radicum (Diptera: Anthomyiidae), influenced by food quality, mating and host plant availability. European Journal of Entomology 90: 137-147. Kostal, V. & S. Finch, 1994. Influence of background on host-plant selection and subsequent oviposition by the cabbage root fly (Delia radicum). Entomologia Experimentalis et Applicata 70: 153-163. Liburd, O.E., Casagrande, R.A. & S.R. Alm, 1988. Evaluation of various color hdromulches and weed fabric on broccoli insect populations. Journal of Economic Entomology 91(1): 256- 262. O'Donnell, M.S. & T.H. Coaker, 1975. Potential of intracrop diversity for the control of brassica pests. Proceedings of the 8th British Insecticide and Fungicide Conference 1975: 101-107. Prokopy, R.J. & R.D. Owens, 1983. Visual detection of plants by herbivorous insects. Annual Review of Entomology 28: 337-364. Prokopy, R.J., Collier, R.H. & S. Finch, 1983. Visual detection of host plants by cabbage root flies. Entomologia Experimentalis et Applicata 34: 85-89. Roessingh, P. & E. Städler, 1990. Foliar form, colour and surface characteristics influence oviposition behaviour in the cabbage root fly Delia radicum. Entomologia Experimentalis et Applicata 57: 93-100. Ryan, J., Ryan, M.F. & F. McNaeidhe, 1980. The effect of interrow plant cover on populations of the cabbage root fly, Delia brassicae (Wied.) Journal of Applied Ecology 17: 31-40 Vandermeer, J., 1989. The Ecology of Intercropping. Cambridge University Press: 237 pp.

162

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 163-166

Performance of the aphid Myzus persicae on intercropped and monocropped cabbages in glasshouse experiments

Z. Seress1, R.G. McKinlay2, B. Pénzes1 1 Saint István University, Faculty of Horticultural Science, 44 Ménesi út, Budapest, 1118, Hungary; email: [email protected] 2 Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK

Abstract: To investigate the mechanism that causes less attack by aphids on cabbages intercropped with clover, the mean relative growth rate, fecundity and the delay in maturity were studied of the peach potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae) on intercropped and monocropped cabbages, where roots were allowed to grow together and separated. The ‘intercropping, roots together’ treatment showed the smallest mean relative growth rate, delayed the maturity and slowed down the growth of cabbages. The ‘monocropping, roots separated’ treatment showed the highest the mean relative growth rate and the maturity was reached earlier. These results may indicate that intercropping delays the growth of settled aphid populations and this effect is via the roots by competition.

Keywords: aphid performance, host plant quality, intercropping

Introduction

Reviews based on more than hundred experiments show that pests tend to be less abundant in intercrops, although not always (Vandermeer, 1989; Andow, 1991). Even nowadays an ethnically isolated minority in Rumania, the ‘Ceangău’ [tsangou] people still produce their food in polyculture with minimum input, without occasional food shortages (Seress, 1997). The most researched polyculture in temperate zones is the white cabbage undersown by clovers, which suffers much less damage by Brevicoryne brassicae, Mamestra brassicae, Delia brassicae and Thrips tabaci than non-intercropped cabbage (Wiech & Wnuk, 1991; Theunissen et al., 1992; Finch & Edmonds, 1994). The mechanism for the above pest reducing observation is not clear exactly. Most researchers noticed smaller number of aphids settling on intercropped cabbages. Some has noted that the rate of increase of aphid numbers was the same between intercropped and monocropped Brassicas (Vidal & Bohlsen, 1994), but it was still promising to see whether in laboratory the quality of cabbages changes the performance of a Brassica pest, the peach potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae).

Material and methods

Glasshouse grown white cabbages (Minicole F1) with white clover (Trifolium repens ssp. sylvestre “Rivendel”) plants were arranged and / or transplanted in a glasshouse according to the following treatments (Fig. 1): 1) intercropping, roots allowed to grow together: 3 cabbage plants and 14 x 10 clover plants transplanted to a seedling tray 2) monocropping, roots allowed to grow together: 3 cabbage plants transplanted to a seedling tray

163 164

3) intercropping, roots separated: 3 pots of cabbage and 8 pots of clover (10 plants in each pot) 4) monocropping, roots separated: 3 pots of cabbage and 8 pots of peat

Fig. 1. Treatments

M. persicae larvae and pre-reproducing nymphs were raised in clip-cages placed on the same position of the same leaf considering the level above the ground on the middle cabbage plants of each treatment. The aphid performance was evaluated using three methods: a) mean relative growth rate b) fecundity c) delay in maturity (no. of adults / no. of all forms were counted every 5 hours). The plants were arranged and / or transplanted one day before the experiment started, then the first measurements took 9 days, and repeated again for 9 days on the same plants. Four replicates were used in each test. The aphids were derived form a genetic clone.

Results

On the 18th day of the experiment the cabbages in the treatment ‘intercropping, roots together’ had one leaf less as in all the other treatments. The slower growth was probably by the competition between the cabbage and the clover. On the second 9 days of the experiment (by the time the roots grew together) the mean relative growth rate became the smallest in the treatment ‘intercropping, roots together’. The fastest was the weight increase in the treatment ‘monocropping, roots separated’ (Fig. 2).

165

0,24 intercropped, roots together 0,22 intercropped, 0,2 roots separated (µg/day) 0,18 monocropped, roots together 0,16 monocropped, 14-23 Aug 25 Aug - 3 Sept roots separated

Fig. 2. Mean relative growth rate of M. persicae

The fecundity did not show differences. The maturity was reached last always in the treatment ‘intercropping, roots together’, however, this became significant only in the second 10 days of the experiment. The maturity was reached first always in the treatment ‘monocropping, roots separated’ (Fig. 3).

80% intercropped, roots together 60% intercropped, roots separated 40% moncropped, 20% roots together adults / all forms (%) 0% monocroppd, 14-23 Aug 25 Aug - 3 Sept roots separated

Figure 3. Delay in maturity of M. persicae

Discussion

Theunissen experienced that if the competition is reduced between the plants by planting clover only between every second cabbage row than the positive plant protection effect is reduced, too (pers. comm.). Therefore we expected that the model of the observed pest- population reducing growing method, the ‘intercropping, roots together’ treatment will differ from the other treatments. The data supported our hypothesis. The ‘intercropping, roots together’ treatment showed the smallest mean relative growth rate, delayed the maturity and slowed down the growth of cabbages. The ‘monocropping, roots separated’ treatment showed the highest the mean relative growth rate and the maturity was reached earlier. The treatments with medium competition gave intermediate results. 166

These results may indicate that intercropping delays the growth of settled aphid populations and this effect is via the roots by competition.

References

Andow, D.A. 1991: Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36: 561-586. Finch, S. & Edmonds, G.H. 1994: Undersowing cabbage crops with clover - the effects on pest insects, ground beetles and crop yield. IOBC wprs Bulletin 17 (8): 159-167. Seress, Z. 1998: Köztestermesztés a moldvai csángók veteményeskertjeiben. (In Hungarian: Intercropping in the self-subsisting gardens of the ceangau people in Moldva.) Biokultúra 9 (1): 7. Theunissen, J., Booij, C.J.H., Schelling, G. & Noorlander, J. 1992: Intercropping white cabbage with clover. IOBC wprs Bulletin 15 (4): 104-114. Vandermeer, J.H. 1989: The Ecology of Intercropping. Cambridge, Cambridge University Press. Vidal, S. & Bohlsen, W. 1994: What makes intercropped cauliflower plants less susceptible to Brevicoryne brassicae? IOBC wprs Bulletin 17 (8): 173-182. Wiech, K. & Wnuk, A. 1991: The effect of intercropping cabbage with white clover and French bean on the occurrence of some pests and beneficial insects. Folia-Horticulturae 3 (1): 39-45. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26( 3) 2003 pp. 167-176

The effects of undersowing (Brussels sprouts – black mustard) on population density of Brevicoryne brassicae and natural enemies of aphids

T. Bukovinszky 1,2, V. Rasztik 3, J.C. van Lenteren 1, L.E.M. Vet 1 & G. Bujáki 2 1 Wageningen University, Binnenhaven 7, 6709PD Wageningen, The Netherlands 2 Szent István University, Páter K. út 1., 2100 Gödöllő, Hungary 3 Szent István University, Villányi út 29-43., 1118 Budapest, Hungary

Abstract: The changes of population sizes of the cabbage specialist aphid Brevicoryne brassicae and its parasitism by the specialist Diaeretiella rapae were followed in undersown plots (Brussels sprouts – black mustard) and monocultures of sprouts in 1998. The effects of undersowing on the parasitoid complexes of aphids and on the syrphid communities organised in the mixed and monocropped stands were also investigated. Mustard was mown to promote a uniform 2nd flowering period, thus we could test the effects of flowering and the disturbance of mowing. Significantly lower incidence and densities of B. brassicae populations were observed in the undersown plots. The densities of all observed natural enemy groups of aphids were positively affected by undersowing. Rate of parasitism of B. brassicae by D. rapae was significantly higher during flowering periods. Members of Neuropteroidea were also more frequent in the undersown stands. Removal of flowers (to induce second flowering) adversely affected the populations of D. rapae and the syrphid species. No differences were found in the diversity and similarity of aphid parasitoid complexes between the treatments. However, different syrphid communities were organised in the undersown culture due to flowering with higher species richness and diversity. Mowing of mustard was followed by decline in the number of species till the next flowering period.

Key words: Brevicoryne brassicae, Diaeretiella rapae, predatory insects, diversity, undersowing, black mustard;

Introduction

Population densities of herbivorous insects are frequently lower in vegetationally diverse habitats than in simple ones (Risch et al. 1983). Diverse vegetation can affect herbivore populations directly, through limited resources and interfering with host plant searching behaviour (e.g. disruptive crop hypothesis). Growing different plant species together can lead to decreased herbivore populations through increasing the success of natural enemies. This has placed greater emphasis on how factors such as resource enrichment, disturbance and vegetational diversity affect arthropod species richness and population abundance. The role these factors play in affecting community structure will help to explain agricultural problems including the development of herbivores and pests and stimulate the development of effective biological control programs, especially in annual crops (Herzog and Fundenburk, 1985 in Murphy et al. 1998). The purpose of this study was to investigate the effects of intercropping on pest populations and their natural enemies. As the subject of our investigations we chose the distinctive entomofauna of cruciferous plants with regard to aphid populations and the communities of their natural enemies.

167 168

The comparison of densities of Brevicoryne brassicae populations and density changes of natural enemies of aphids were carried out in monocropped and undersown plots in 1998. Community structures of aphid parasitoid complexes and syrphid communities were also analysed in relation to cropping system.

Materials and methods

The experiment was carried out in the experimental field of the Wageningen Agricultural University in 1998. Monocropped fields of Brussels sprouts (Brassica oleracea cv. gemmifera) (coded as S) and the undersown culture of Brussels sprouts and black mustard (Brassica nigra) (coded as Sm) were compared. The black mustard was chosen because it is an intensively flowering species presumably providing pollen and nectarine sources for natural enemies. In an earlier study it was found that the presence of wild mustard has considerably increased the parasitism of Pieris brassicae by Cotesia glomerata (Telenga 1957 in Altieri 1994). Three plots of each treatment were embedded in a barley field in a randomised Latin block design, about 30 m distance to each other (Fig.8). Each plot was surrounded by a 4 m wide boundary of Lolium multiflorum. Mowing of the grass was carried out when it was necessary. The spacing of Brussels sprouts plants was 75 cm. No pesticide was applied. After the first flowering (14.07.) the mustard was cut back to promote a uniformly dense second flowering of mustard. During the experiment, the mustard flowered two times. Flowering started at approximately the same time (1-2days difference between plots). The mowing provided the uniform removal of flowers for about 20 days. The fields were surrounded by barley, except the eastern side where an orchard was situated. Individual plant observations were carried out to estimate the incidence and relative population densities of Brevicoryne brassicae. Whole Brussels sprouts plants (20 plants/plot in each week, the last week the sample size was reduced to 15 plants/plot) were chosen as sample units and the total numbers of B. brassicae individuals/plant were counted or estimated in case of high population densities. The density changes of Neuropteroid eggs and larvae and the larvae and pupae of syrphids were also monitored. Primary parasitism of aphids was determined by counting the number of intact mummies per plant on each week. The community structures of aphid parasitoid complexes and syrphid communities were compared between the treatments by using yellow dishes (1dish/each plot, with 14 cm diameter). Differences in species richness, diversity and similarity were calculated.

Data analysis

The Univariate Analysis of Variance (ANOVA) and t-test for independent samples were used to compare the population densities of the observed species and rates of parasitism of aphids within and between the treatments. Statistical data analysis was carried out by use of SPSS 8.0. All differences were calculated with 95% confidence interval. The species composition of communities and complexes was compared by the similarity index of Jaccard (Southwood, 1984) and Morosita (Morosita, 1959 in Krebs 1989). The diversity of complexes and communities was calculated by using the Shannon-Weaver- (Southwood, 1984), Williams-α (Williams, 1943), and Berger Parker indexes (Southwood, 1984). To compare the structure of the communities, hierarchical clustering and PCoA analysis were applied based on Horn- index (Podani, 1997; Krebs 1989). For the multivariate data analysis, Syntax 5.1 program package was applied.

169

Results and discussion

Lower incidence and population levels of B. brassicae were found in the undersown culture (Fig. 1, 2). This indicates the slower colonisation of plants and progress of population by B. brassicae in the undersown plots. The numbers of individuals were not corrected according to the different plant size. The use of a planimeter was not possible because of lack of time and because aphids were counted on all plant parts. This might have influenced the accuracy of the data to a certain extent.

100 500

Sm1 400 * Sm2 300 2nd flowering 10 Sm3 mowing 200 S1 *** 100 *** S2 individuals/plant 0

(log transformed) S3 1 27 28 29 30 31 32 33 % of plants colonized weeks 25 26 27 28 29 30 31 32 33 mono undersown weeks

Fig. 1. The incidence of B. brassicae in the treatments. Sm-undersown; S-monocropped. 2 2 2 2 2 R (logS1) = 0.823; R (logS2) = 0.75 R (logS3) = 0.83; R (logSm1) = 0.9; R (logSm2) 2 = 0.87; R (logSm3) = 0.76; Difference between the slopes P = 0.006 (independent sample t-test). Fig. 2. The changes in density of Brevicoryne brassicae in the monocropped and undersown cultivated plots. Error bars are standard error of the mean. *= significant difference; 0.01

It is possible that aphids were not able to find Brussels sprouts plants due to high vegetation density, so the relative number of individuals/plant could have been smaller in the undersown than in the monocropped fields. The contrast between the vegetation and its background has a basic influence on the host-plant finding byspecialist herbivores (Kostal and Finch, 1994). This contrast was totally different in the two systems. In intercropping experiments with Brussels sprouts B. brassicae was found to react strongly to the contrast of background and crop plants (Theunissen and Den Ouden, 1980 in Theunissen, 1989). Because Brussels sprouts plants were smaller in the undersown culture, herbivores which react to plant size (aphids as well) might have difficulties in finding crop-plants. Since B. brassicae is a crucifer specialist, the presence of another host plant in high densities might have hindered the colonisation of B. sprouts plants. Black mustard contains sinigrin and some related compounds in higher concentrations than other crucifer plants (Kjaer in Read et al. 1970), which are feeding stimulants to crucifer specialists. However, this does not mean necessarily that B. brassicae prefers black mustard above Brussels sprouts, it might have hindered host plant finding of this species. Aphids on mustard tend to aggregate on the germinative plant parts thus by mowing this part of the population was removed. The huge differences in plant growth parameters (data are not shown) indicate the presence of interspecific competition, so poor host plant quality could inhibit the progress of aphid populations. B. brassicae prefers sites of high protein synthesis, like growing parts of 170

plants (Van Emden, 1966). This preference behaviour corresponds with different reactions of the species to water budget of tissues. B. brassicae suffers adversely from a decrease of turgor, which affects reproduction and longevity of females (Van Emden, 1966). The presence of interspecific competition between plants implies the adverse effects of plant quality on development of B. brassicae.

Parasitoids 4700 mummies of B. brassicae were collected and reared out (92% emerged, the others were dissected). Among the primary parasitoids Diaeretiella rapae was the dominant (more than 99%), and a few individuals were parasitised by a Praon sp. (very few specimens emerged from these mummies). Percent parasitism of B. brassicae by Diaeretiella rapae was significantly higher in the undersown culture than in the monocropped plots (Figure 3). Percent of parasitism was higher in the undersown lots during the first flowering, and a week after the onset of the second flowering of the black mustard. This tendency was observed in the yellow dish material as well. Mowing was followed by a decline in rates of parasitism approximately a week later. Therefore the changes in rates of parasitism in time were compared in the two plots. Within treatments the fraction of two weeks were taken and compared. Significantly greater changes in percent of parasitism were found in the undersown plots than in the monocropped ones. These changes were observed after mowing (t=-3.81, P=0.019) and a week after the onset of the 2nd flowering period (t=3.826, P=0.019). Higher rates of parasitism in the mixed culture could occur as a result of a different response of parasitoids to the different host densities in the two cultures. However, the better response of parasitoids to equal host densities in the undersown plots is also possible. Point estimation was done to investigate whether the different responses of parasitoids at equal host density categories resulted in the higher rates of parasitism by D. rapae in the undersown plots. According to the 3 distinctive periods of the flowering, data were divided into three groups. D. rapae parasitised B. brassicae at higher rates both at low and higher population densities during flowering periods in the undersown plots than in the monocropped ones (Figure 4).

60 mowing 50 40 * 2nd flowering 30 20 ** ** 10

% of parasitism % of 0 27 28 29 30 31 32 33 weeks mono undersown

Fig. 3. Rate of parasitism of B. brassicae by Diaeretiella rapae in the mono- and undersown cultures. Error bars are standard error of the mean. *= significant difference; 0.01

171

50 1st flowering after mowing 2nd flowering 40

20 ** * ** 10 % of parasitism 0 <30123412341234 <70<200 >200 <30 <70 <200 >200 <30 <70 <200>200 S Sm host density/plant

Fig. 4. Point estimation of parasitism at different density categories during 1st and 2nd flowering and mowing. Error bars are standard error of the mean. *= significant difference; 0.01

Percent of parasitism was higher at lower host density categories than at higher ones. After mowing, rate of parasitism in undersown plots showed significantly lower value in the undersown plots than in the monocropped ones or no difference was found at other density categories. Although it is not known whether D. rapae feeds on mustard flowers in nature or not, it might have been attracted to undersown plots by flowering, either by the colour or by the presence of additional (pollen/nectarine) resources. Diaeretiella rapae has an innate response to infochemicals (mustard oil allyl isothiocyanate) emitted by cruciferous plants which is the most important cue in its habitat selection, followed by visual searching for the host (Read et al. 1970). In some species of Brassicaceae, especially in B. nigra, the major mustard oil component is allyl isothiocyanate (Kjaer, 1960 in Read et al. 1970). Chemical stimuli together with a more suitable, shady moist microenvironment could accumulate individuals and increased tenure time of this parasitoid species in the undersown stands. The increase in rate of parasitism was probably the outcome of higher density of D. rapae populations and the response to generally lower host density/plant in the undersown plots. However, responses to different plant sizes of sprouts in the mixed culture might have led to higher success of individuals during their host searching. It is probable that huge numbers of active primary parasitoids were removed from the plots by mowing. Also other factors may have contributed to the experienced differences, like the change in microclimatic conditions in the undersown stands, differences in composition and concentration of secondary plant metabolites within the treatment.

Comparison of aphid parasitoid complexes Plant variation could influence the primary- and hyperparasitoid densities of B. brassicae. The effects of undersowing were further investigated at the level of aphid parasitoid complexes. 439 specimens were collected which belonged to 13 genera. Designation to species level was not always possible. The composition and the dominance order of the species caught by yellow dish were very similar to that reared from the mummies of B. brassicae. The overall comparison of the species composition of the two habitats showed high similarity (Jaccard- index: 86.7%), and the comparison based on the species they had in common and their 172

frequency also suggested that aphid parasitoid complexes were highly similar (Morosita’s index: 83.4%) in the treatments. Cluster analysis and ordination based on Horn-index showed high similarity values. Differences in organisation of aphid parasitoid complexes were independent of treatment effects (Figure 5, 6). The diversity indexes of aphid parasitoid complexes showed rather low values, which was due to the low species richness (Table 1). There were no differences found between the treatments.

4 6 5

Fig. 5-6. Hierarchical clustering and PCoA for the comparison of structure of aphid parasitoid complexes in the mono and undersown plots based on Horn-index (1,2,3,7 monocropped plots; 4,5,6 undersown plots).

Table 1. The diversity of the parasitoid complexes of aphids in the treatments.

Berger-Parker Shannon- Williams-α Weaver Undersown 0,34 1,95 3,35 Monocropped 0,34 2,03 3,49

Certain disadvantages must be considered when using the yellow dishes for sampling in this case. The results of observations through using yellow dish are affected by the selectivity of the traps. A prerequisite to use such traps is differences between habitats should not affect the efficiency of traps (Southwood, 1984). This case the catches by the traps in the undersown plots were expected to be relatively smaller than those in the monocropped plots, due to the lack of contrast with the background. The vegetation characteristics (height and density) made the application of other techniques (sweep netting or D-Vac sampling) impossible. Habitat characteristics may exert a basic influence on the occurrence and dominance order of parasitoid species in a particular system. We discuss the possibility that adding another plant species to the system did not enhance higher species diversity of parasitoid complexes. It is possible that the relative abundance of certain species (D. rapae) was higher in the undersown stands, but overall species richness was hardly influenced. It seems that species diversity was not affected by undersowing, and highly similar complexes were organised in the stands. However, differences in similarity were found between the plots 173

independently to treatment effect, which suggests that more data is needed to underpin this theory. It is possible that adding black mustard as flowering plant to the system did not provide any additional resource to be utilized by other aphid parasitoid species. However, tourists of other species could have arrived from e.g. cereal aphid-parasitoids, they might have problems to settle due to lack or rarity of suitable host(s).

Predatory populations All observed predatory populations were favoured by applying undersowing. Significantly higher numbers of eggs and larvae of lacewings were found in the intercropped culture, although their populations were very low (Fig. 7). In most cases only eggs were found, in some cases larvae were observed as well. Adults were recovered neither from individual plant observations nor from yellow dishes. Maredia et al (1992) found that Chrysoperla carnea predominantly preferred yellow colour and to a less extent green and red. This species is one of the most common cosmopolitan chrysopid species. Although no Neuropteroidea species was found in the yellow dish material, it is possible, that flowering attracted them, or they preferred the shady, more humid mesoclimate of the undersown culture. Significantly more syrphid larvae and pupae/plant were found in the undersown culture (Fig. 8). Their density declined after mowing, to a significantly lower level than that in the monocropped plots. After the onset of 2nd flowering their density increased again, their numbers seemed to fluctuate as a consequence of mowing. They seemed to respond to the flowering; not only by visiting the flowers in higher numbers, they also laid more eggs on the undersown Brussels sprout plants, though prey densities were considerably lower in these stands. The total number of species found was significantly higher in the undersown treatment than in the monocropped one. In the monocropped plots the predator guild was dominant, while in the undersown plots the saprophyte guild occurred most frequently, though members of predatory guild was also more abundant in the undersown plots (Table 2). The higher species richness, due to flowering apparently declined after mowing, and the second flowering was followed by subsequent increase in species number (Fig. 9). Characteristically different communities were structured in the undersown plots when compared to monocultures. Similarity based on the extent to which the two habitat had species in common (Jaccard-index) was low (41.6%). If we consider the abundance of the common species (Moroshita-index) the similarity was higher, 80.1%. Similarity of communities based on hierarchical clustering and ordination revealed differences between the structures of syrphid communities organised in the two treatments (Fig. 10, 11). Differences between the undersown plots were less than between the monocropped plots. Estimations of diversity based on the moderately abundant species (Williams-α) showed higher values for syrphid assemblages in the undersown treatment (Table 3).

Table 2. The proportions of different guilds of syrphids in the treatments. Numbers in brackets represent mean number of individuals/dish.

Undersown Monocropped Phytophagous 2(23) 6(2) Predatory 21(23.3) 52(16) Saprophyte 77(87.3) 42(13)

174

2 mowing 2nd flowering 3 -1 -1 2,5 1,5 mowing 2nd flowering * 2 ** * 1 1,5 1 * *** 0,5

egg/larva plant 0,5 * larvae/pupae plant 0 0 27 28 29 30 31 32 33 25 27 28 29 30 31 32 33 mono undersown week mono undersown week

Fig. 7-8. Changes in densities of Neuropteroidea and syrphid larvae and pupae in the treatments. Error bars are standard error of the mean. *= significant difference; 0.01

mowing 12 10 8 6 4 2 No. of species 0 25 26 27 28 29 30 31 32 33 34 mono undersown weeks

Fig. 9. Changes in syrphid species richness of the two treatments. Error bars are standard error of the mean.

Fig. 10-11. Hierarchical clustering and PCoA for the comparison of structure of syrphid communities in the mono and undersown plots based on Horn-index(1,2,3= monocropped plots; 4,5,6= undersown plots). 175

Table 3. The diversity of Syrphid communities in the treatments.

Berger- Shannon- Williams-α Parker Weaver Undersown 0.25 2.4 8.67 Monocropped 0.16 2.56 7.23

It is well known that pollen and nectarine resources are essential for syrphids as the only protein staple (Kevan and Baker, 1983). Their high densities and species richness in the yellow traps during flowering prove this suggestion. The preference of different syrphid species to flower colours is mentioned by several authors (Cowgill et al., 1993; Haslett, 1989, Kevan and Baker, 1983). These observations revealed the influence of physiological and ecomorphological characteristics on flower selectivity of syrphids. Nectarine/pollen sources and the colour of flowers together can shape the species composition of syrphids visiting a certain habitat. It is very likely that in our experiment both pollen/nectarine sources and the colour of flowers structured syrphid communities. The species composition in the undersown plots was quite different to those of monocultures. Larger population size, higher species richness and diversity of syrphids were concomitant to flowering. An additional effect of intercropping might have been the alteration of microclimatic conditions, which resulted in larger populations of syrphids in the diverse stands. Tenhumberg and Poehling (1995) mentions that besides aphid density, the egg-laying behaviour of syrphids is affected by temperature (Ankersmit et al., 1986), humidity (Wahbi, 1967), light, aphid species, and plant density (Chandler, 1968). The oviposition by gravid females in the undersown plots might have been enhanced by the different mesoclimate as well. The effect of floral density on foraging decisions is not known. It is probable that the combined effects of additional pollen/nectarine resources and the altered mesoclimatic conditions led to the experienced differences. Further conclusions cannot be drawn in this context because of the non-mechanistic approach of the work. Species diversity largely depends on the relative abundance of species. Diversity patterns of natural communities follow certain seasonal dynamics. In agroecosystems cultivation practices might cause changes in the diversity of communities. It should be mentioned that calculated overall diversity values might reflect the differences between the treatments, they are not dynamic, and could eliminate the differences caused by disturbance to a certain extent (mowing). However, the dynamics of species richness could be followed in this case, suggesting that species diversity also declined after mowing. This proves that mowing disturbed syrphid populations and led to temporal extinction of several species from the stands. Unfortunately the degree of efficiency of syrphids in the suppression of developmental rate of aphid populations to lower levels in this case is not known because of the complexity of interacting factors in pest regulations. We conclude that undersowing Brussels sprouts with black mustard effectively reduced the populations of B. brassicae and it is likely that direct effects of vegetation (disruptive crop hypothesis) was mostly responsible to this phenomenon. The presence of black mustard enhanced the efficiency of natural enemies. The application of flowering non-crop plants species seems to be a perspective way to increase efficiency of biological control. It would be worthwhile to search for more efficient flowering species compatible with the demand of vegetable production. It is important to find and quantify the sources of disturbance because they can lead to temporal extinction of species from the system, so population interactions are disrupted. Since natural enemies are often more susceptible to disturbances originating from e.g. cultural practices, these situations can lead to increase in pest population sizes. It is 176

important to know how fast communities of natural enemies are able to recover following disturbances.

References

Altieri, M.A. 1994. Biodiversity and Pest Management in Agroecosystems. Food Products Press, The Haworth Press Inc.: 185 pp. Ankersmit, G.W., Dijkman, H., Keuning, N.J., Mertens, H., Sins, A. & Tacoma, H.M. 1986. Episyrphus balteatus as a predator of the aphid Sitobion avenae on winter wheat. Entomol. Exp. Appl. 42: 271-277. Chandler, A.E.F. 1968. Some factors influencing the occurrence and site of oviposition by aphidophagous Syrphidae (Diptera). Ann. Appl. Biol. 61: 435-446. Cowgill, S. E., Wratten, S.D. & Sotherton, N.W. 1993. The selective use of floral resources by the hoverfly Episyrphus balteatus (Diptera: Syrphidae) on farmland. Ann. appl. Biol. 122: 223-231. Haslett, J.R. 1989. Interpreting pattterns of resource utilization: randomness and selectivity in pollen feeding by adult hoverflies. Oecologia. 78: 433-442. Kevan, P.G. & Baker, H.G. 1983. Insects as flower visitors and pollinators. Ann. Rev. Entomol. 28: 407-453. Kjaer, A. 1960. Naturally derived isothiocyanates (mustard oils) and their parent glucosides. Fortschr. Chem. Org. Naturst. 18: 122-176. Kostal, V. & Finch, S. 1994. Influence of background on host-plant selection and subsequent oviposition by the cabbage root fly (Delia radicum). Entomol. exp. appl. 70: 153-163. Krebs, C.J. 1989. Ecological Methodology. HarperCollinsPublishers, Inc.: 654 pp. Maredia, K.M., Cage, S.H., Landis, D.A. & Wirth, T.M. 1992. Visual response of Coccinella septempunctata (L.), Hippodamia parenthesis (Say), (Coleoptera: Coccinellidae), and Chrysoperla carnea (Stephens), (Neuroptera: Chrysopidae) to colors. Biological Control 2: 253-256. Murphy, B.C. et al. 1998. Habitat diversification tactic for improving biological control: parasitism of the western grape leafhopper. Entomol. Exp. Appl. 87: 225-235. Podani, J. 1997. Bevezetès a többváltozós biológiai adatfeltárás rejtelmeibe. [Introduction to the multivariate analysis of biological data.] Scientia Kiadó, Budapest: 412 pp. Read, D.P. et al. 1970. Habitat selection by the aphid parasite Diaeretiella rapae (Hymeno- ptera: Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 102: 1567-1578. Risch, S.J., Andow, D. & Altieri, M.A. 1983. Agroecosystem diversity and pest control: Data, tentative conclusions, and new directions. Environ. Entomol. 12, 625-29. Southwood, T.R.E. 1984. Ecological Methods with particular reference to the study of insect populations. Chapman & Hall. University Printing House, Cambridge: 524 pp. Tenhumberg, B. & Poehling, H-A. 1995. Syrphids as natural enemies of cereal aphids in Germany: Aspects of their biology and efficacy in different years and regions. Agric. Ecosyst. & Environ. 52: 39-43. Theunissen, J., 1992. Cabbage-clover intercropping: oviposition of Delia radicum. Proc. Exp. Appl. Entomol., N.E.V. Amsterdam 3: 191-96. Van Emden, 1966. Studies on the relations of insects and host plant. III. A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae (Hemiptera: Aphididae) on brussels sprout plants supplied with different rates of nitrogen and potassium. Entomol. Exp. Appl. 9: 444-60. Wahbi, A.A. 1967. Untersuchungen über den Einfluß der Temperatur und der relativen Luftfeuchtigkeit auf das Fraßvermögen von Syrphidenlarven (Diptera, Syrphidae). Ph.D. Thesis, University of Göttingen. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 177-182

Thrips species in leeks and their undersown intercrops

H. Legutowska1 & J. Theunissen2. 1 Department of Applied Entomology, Warsaw Agricultural University, Warsaw 2 PolandResearch Institute for Plant Protection (IPO), Wageningen, The Netherlands

Abstract: The thrips faunas of leeks and their undersown intercrops have been determined in a number of intercropping trials during one growing season. In the leeks, Thrips tabaci and Frankliniella tenuicornis were the dominant species, with females, males and larvae found within the leek plants. In the undersown intercrops, clovers and Medicago lupulina, these two species were part of a broader spectrum of thrips species. No larvae of both species were found. It is concluded that T. tabaci and F. tenuicornis are not specifically attracted to and do not reproduce on clovers. These intercrops do not sustain Thysanopterous leek pest populations. The pest status of F. tenuicornis in leek needs closer investigation.

Key words: thrips, Thysanoptera, leek, intercropping, undersowing, Trifolium

Introduction

Within the concepts of IPM (Integrated Pest Management) measures have to be developed to prevent infestation and infection of field vegetable crops by pests and diseases. The growing dislike of consumers and markets of pesticide use on fresh products and the resulting legislation of national and European authorities require a certain urgency in finding alternatives for pesticides. Among the approaches which have recently received some attention are the pest and disease suppressing effects of intercropping (Altieri, 1994; Andow, 1991; Vandermeer, 1989). In field vegetables intercropping effects, using clover species as undersown crops, were demonstrated in cabbage and leek (Theunissen et al., 1995; Theunissen and Schelling, 1996, 1997). A number of theories have been formulated to explain, at least partially, the observed intercropping effects. The most prominent hypotheses are: the resource concentration hypothesis, the enemies hypothesis (Risch, 1981) and the host-plant quality hypothesis (Theunissen, 1994). Associated with the resource concentration hypothesis is the interference with the orientation and behaviour of pest insects. Kostal and Finch (1994) found that undersowing disturbed the oviposition behaviour of the cabbage root fly, Delia radicum, explaining the drastical reduction of eggs laid in undersown cabbage. For other cabbage pests, Finch (1996) proposed the mechanism of appropriate/ inappropriate landings to explain the delayed crop colonization observed at undersowing. Undersowing clover in leek, Allium porrum L., leads to induced resistance to Thrips tabaci Lindeman (Theunissen and Schelling, 1996). But, in addition to this, one of the reasons of a very reduced thrips population on intercropped leeks could be a deflection of the pest from the leek crop towards the undersown crop, usually a clover species. If a preference of the pest species, Thrips tabaci, for the intercrop would exist, then the intercrop would act as a sink for invading thrips adults. To check whether this is the case in the leek-clover-thrips system, thrips were sampled and identified in both the undersown and the leek crops. In this paper the results are presented.

177 178

Material and methods

The experiments and fields from which the crop samples were taken were situated at the experimental farm ‘de Grebbedijk’ of IPO-DLO in Wageningen. The soil type was river clay. Some of the experiments have been described elsewhere (Theunissen and Schelling, 1998), some fields were laid out especially for the purpose of making this inventory, named Hanna’s fields. In the latter case the plots were 4 * 6 m, containing 7 rows of 43 plants each. The row distance between the leeks was 65 cm. Sowing date of intercrops was 4 June, planting date of leeks cv Albana 3 July. The plots were separated by 1 m of grass and situated in a row with a randomly assigned undersown broadcasted intercrop or monocrop of leek as a check. No replicates were used. As intercrop the following species were used: Trifolium repens cv Asterix (white clover), T. subterraneum cv Nungarin (subterranean clover), T. fragiferum cv Palestine (strawberry clover), Medicago lupulina and a plot with assorted weeds. In the same experimental field we had summer leeks cv Rami, in monocrop and undersown with T. fragiferum cv Palestine and weeds (‘Early leeks’). The clover was sown on 7 May and the leeks were planted the same day. The weeds emerged spontaneously, as usual. Other experiments were laid out with autumn leeks cv Tadorna, also in monocrop and undersown with T. fragiferum cv Palestine. One in various patterns of undersowing to study the effects of these patterns on thrips infestation and yield, named ‘Patterns’. The treatments were: monocrop, broadcasted full field undersowing, between rows and within rows (Theunissen and Schelling, 1998). The clover was sown on 7 April, the leeks planted on 18 June. The second experiment dealt with sowing times of the clover relative to the planting of leek, which also were planted on 18 June. The treatments were: monocrop, broadcasted sowing of clover prior to the planting of leeks, and broadcasted sowing of clover at the time of leek planting (Theunissen and Schelling, 1998). In none of the experiments pesticides were used. From the beginning of the growing period of the crops, samples were collected from thrips in different fields. From the intercrop foliage was cut with a scissor and put in a plastic bag. The bags were stored in a cold storage room until the thrips could be retrieved. Prior to opening the bags they were weighted to establish the fresh biomass of the crop samples. The bags were opened inside a white plastic box with a more or less transparent bottom which was illuminated from the underside. The material was carefully checked on the presence of thrips, which were picked up with a soft brush and stored in small plastic vials containing a 60% methylalcohol-water mixture. Thrips could easily been found on the opaque illuminated underside of the box and picked up. They showed a tendency to stay on the lighter underside when separated from the plant material. The vials were labeled to show the date and the kind of intercrop. From the leeks, thrips were catched during the regular observations while counting the thrips in the field. The trips were stored in similar plastic vials and labeled for future use. Because of the sometimes large numbers of thrips in leeks (in the monocrops) we made sure to have sufficient numbers of individuals without collecting them quantitatively. When small numbers of thrips were found attempts were made to catch them all. The inventory is therefore of a qualitative, rather than quantitative nature. The species and numbers per vial were checked by the first author.

Results

A variety of Thrips species were found on leek and the undersown crops, albeit in different proportions. The species found were: Thrips tabaci Lindeman, Thrips atratus Haliday, Thrips fuscipennis Haliday, Thrips angusticeps Uzel, Thrips major Uzel, Limothrips cerealium 179

Haliday, Limothrips denticornis Haliday, Frankliniella tenuicornis (Uzel), Frankliniella intonsa (Trybom), Aeolothrips intermedius Bagnall, Anaphothrips obscurus Muller, Iridothrips spp. To maintain an overview of our findings we present the material per experiment or collection of fields which belong together, in a chronological sequence.

Early leeks In samples of flowers of T. fragiferum, collected in the ‘Early leeks’ plots, the following species were found at two dates in July, 2 months after planting of the leek. 16 July: T. tabaci 1 ♀; T. fuscipennis 12 ♀, 1 ♂; T. angusticeps 1 ♀, 1 ♂; T. major 2 ♀♀; L. cerealium 2 ♀♀ 23 July: T. tabaci 1 ♀; T. fuscipennis 24 ♀♀, 2 ♂♂, 2 larvae; T. angusticeps 2 ♀♀, 1 larva; L. denticornis 3 ♀♀; F. tenuicornis 1 ♂; F. intonsa 1 ♀, 1 ♂, 2 larvae; A. intermedius 1 ♀. In the foliage of this clover no thrips were found. Early leeks; in leeks; 16 July: T. tabaci 1 ♀, 1 larva; F. tenuicornis 1 ♀, 1 ♂, 2 larvae (monocrop); T. tabaci 1 ♀; F. tenuicornis 5 ♀♀ (clover intercrop); F. tenuicornis 1 ♀; T. angusticeps 1 larva (weed intercrop). Early leeks; in leeks; 23 July: T. tabaci 6 ♀♀; T. atratus 1 ♂; F. tenuicornis 7 ♀♀, 13 larvae (monocrop); T. angusticeps 1 larva; F. tenuicornis 7 ♀♀ (clover intercrop); F. tenuicornis 4 ♀♀ (weed intercrop). Early leeks; in intercrop; 5 August: none (clover intercrop); T. atratus 4 ♀, 1 larva (weed intercrop). Early leeks; in leeks; 7 August: T. tabaci 8 ♀♀; F. tenuicornis 2 ♀♀, 1 larva; L. cerealium 3 ♀♀ (monocrop); F. tenuicornis 7 ♀♀, 3 ♂♂ (clover intercrop); T. tabaci 6 ♀♀; F. tenuicornis 8 ♀♀, 2 ♂♂ (weed intercrop). Early leeks; in intercrop; 20 August: none (clover intercrop); none (weed intercrop). Early leeks; in leeks; 21 August: T. tabaci 79 ♀♀, 4 ♂♂, 4 larvae; F. tenuicornis 2 ♀♀, 4 ♂♂, 4 larvae; A. intermedius 3 larvae (monocrop); T. tabaci 24 ♀♀, 1 ♂; F. tenuicornis 3 ♀♀, 7 ♂♂, 2 larvae (clover intercrop); thrips found but data missing (weed intercrop). Early leeks; in intercrop; 3 September: F. tenuicornis 1 ♀ (clover intercrop); T. fuscipennis 1 ♀; T. atratus 2 ♀♀ (weed intercrop). Early leeks; in leeks; 3 September: T. tabaci 65 ♀♀, 9 ♂♂, 4 larvae; F. tenuicornis 2 ♀♀ (monocrop); T. tabaci 31 ♀♀, 1 ♂, 4 larvae; F. tenuicornis 3 ♀♀ (clover intercrop); T. tabaci 20 ♀♀; F. tenuicornis 1 ♀, 2 ♂♂ (weed intercrop).

Hanna’s fields Hanna’s fields; in the leeks, 16 July: F. tenuicornis 1 ♀ (monocrop); T. tabaci 1 ♀; F. tenuicornis 5 ♀♀, 6 larvae (Asterix); F. tenuicornis 2 larvae (Nungarin); F. tenuicornis 1 larva (Palestine); none (Medicago); F. tenuicornis 3 ♀♀, 1 larva; L. cerealium 1 ♀ (weeds) Hanna’s fields; in the leeks, 23 July: F. tenuicornis 1 ♀; L. cerealium 1 ♀ (monocrop); F. tenuicornis 4 ♀♀, 1 ♂, 1 larva (Asterix); F. tenuicornis 8 ♀♀, 1 ♂ (Nungarin); F. tenuicornis 2 ♀♀, 3 larvae (Palestine); F. tenuicornis 1 ♀ (Medicago); F. tenuicornis 3 larvae (weeds). Hanna’s fields; in intercrops; 5 August: no thrips were found in any of the intercrops. Hanna’s fields; in intercrops; 20 August: no thrips found in intercrops, except in Palestine F. tenuicornis 1 ♂; T. atratus 2 ♂♂. Hanna’s fields; in intercrops; 3 September: T. atratus 3 ♀♀; F. intonsa 1 ♀ (Asterix); none (Nungarin); none (Palestine); T. fuscipennis 1 ♀ (Medicago). Hanna’s fields; in intercrops; 16 September: none (Asterix); F. intonsa 1 ♀ (Nungarin); none (Palestine); none (Medicago). 180

Hanna’s fields; in leeks; 17 September: T. tabaci 24 ♀♀, 1 ♂, 3 larvae (monocrop); T. tabaci 8 ♀♀, 2 ♂; F. tenuicornis 2 ♀♀ (Asterix); T. tabaci 9 ♀♀, 2 ♂♂ (Nungarin); T. tabaci 10 ♀♀, 2 larvae (Palestine); T. tabaci 8 ♀♀ (Medicago). Hanna’s fields; in leeks; 28 October: T. tabaci 252 ♀♀, 13 ♂♂, 2 larvae (monocrop); T. tabaci 110 ♀♀, 9 ♂♂ (Asterix); T. tabaci 9 ♀♀, 2 ♂♂ (Nungarin); T. tabaci 10 ♀♀, 2 larvae (Palestine); T. tabaci 61 ♀♀, 1 ♂; F. tenuicornis 1 ♀ (Medicago).

Patterns Patterns; in leeks; 2 August: T. tabaci 76 ♀♀, 1 ♂, 11 larvae; F. tenuicornis 4 ♀♀, 6 ♂♂ (monocrop); none in other treatments. Patterns; in intercrop; 5 August: F. tenuicornis 1 ♀; L. cerealium 2 ♀♀ (full field); F. tenuicornis 1 ♀ (between rows); none (within rows). Patterns; in leeks; 7 August: T. tabaci 7 ♀♀; F. tenuicornis 3 ♀♀, 2 ♂♂; L. cerealium 1 ♀ (monocrop); F. tenuicornis 12 ♀♀, 1 ♂ (full field); T. tabaci 1 ♀, F. tenuicornis 3 ♀♀, 2 ♂♂ (between rows); F. tenuicornis 2 ♀♀ (within rows). Patterns; in intercrop; 20 August: F. tenuicornis 2 ♀♀ (full field); none (between rows); F. tenuicornis 2 ♀♀ (within rows). Patterns; in leeks; 21 August: missing data (monocrop); T. tabaci 7 ♀♀; F. tenuicornis 11 ♀♀ 13 ♂♂, 2 larvae (full field); T. tabaci 12 ♀♀; F. tenuicornis 1 ♀, 12 ♂♂; A. intermedius 2 larvae (between rows); missing data (within rows). Patterns; in intercrop; 3 September: T. atratus 2 ♀♀, 1 larva (full field); none (between rows); none (within rows). Patterns; in leeks; 4 September: T. tabaci 21 ♀♀; F. tenuicornis 1 ♀, 1 ♂; Iridothrips 1 ♀ (monocrop); T. tabaci 7 ♀♀, 1 ♂, 1 larva; F. tenuicornis 2 ♀♀, 2 Γ (full field); T. tabaci 24 ♀♀, 2 ♂♂, 1 larva; F. tenuicornis 4 ♀♀ (between rows); T. tabaci 4 ♀♀, 1 ♂; F. tenuicornis 4 ♂♂ (within rows).

Late sowing Late sowing; in leeks; 7 August: T. tabaci 3 ♀♀; F. tenuicornis 4 ♀♀, 2 larvae; L. cerealium 3 ♀♀ (monocrop); T. tabaci 2 ♀♀; F. tenuicornis 5 ♀♀ (prior sowing); T. tabaci 3 ♀♀; F. tenuicornis 6 ♀♀, 1 ♂ (sowing at planting). Late sowing; in intercrop; 20 August: F. tenuicornis 1 ♀ (prior sowing); F. tenuicornis 1 ♂ (sowing at planting). Late sowing; in leeks; 21 August: T. tabaci 50 ♀♀, 1 ♂; F. tenuicornis 6 ♀♀, 3 ♂♂; L. cerealium 2 larvae (monocrop); T. tabaci 16 ♀♀, 2 ♂♂; F. tenuicornis 14 ♀♀, 19 ♂♂, 1 larva; T. fuscipennis 1 ♀ (prior sowing); T. tabaci 13 ♀♀; F. tenuicornis 11 ♀♀, 3 ♂♂ (sowing at planting). Late sowing; in intercrop; 3 September: T. tabaci 1 ♀; F. tenuicornis 2 ♂♂ (prior sowing); none (sowing at planting). Late sowing; in leeks; 4 September: T. tabaci 61 ♀♀, 2 ♂♂; F. tenuicornis 2 ♀♀; F. intonsa 1 ♀ (monocrop); T. tabaci 18 ♀♀; F. tenuicornis 1 ♀ (prior sowing); T. tabaci 16 ♀♀; F. tenuicornis 1 ♀, 2 ♂♂ (sowing at planting). Late sowing; in intercrop; 16 September: F. tenuicornis 1 ♀ (prior sowing); T. tabaci 1 ♀; F. tenuicornis 1 ♀ (sowing at planting). Late sowing; in leeks; 4 December: data missing (monocrop); T. tabaci 31 ♀♀, 2 ♂♂; F. tenuicornis 1 ♀; A. obscurus 1 ♀ (prior sowing); T. tabaci 24 ♀♀, 1 ♂; F. tenuicornis 2 ♀♀ (sowing at planting). Late sowing; in leeks; 13 January: T. tabaci 79 ♀♀ (monocrop); other treatments not sampled.

181

In a well established field of white clover, T. repens cv Asterix, which was in its second year, we sampled the clover foliage once, on 4 August: F. tenuicornis 1 ♀; L. cerealium 1 ♀; T. fuscipennis 2 ♀♀; T. angusticeps 1 ♀; F. intonsa 1 ♂. The relative abundance of the main thrips species in the leeks and the various intercrops is indicated by the incidence of thrips in plant samples. In leeks this incidence was 100%, consisting mainly of T. tabaci and F. tenuicornis. In the intercrops the incidence was lower: T. fragiferum 50%, T. repens and T. subterraneum 25%, M. lupulina 75%. The role of T. tabaci and F. tenuicornis in samples of leek and intercrops is given in Fig.1, where their dominant presence in leeks is illustrated.

Discussion

Thrips tabaci is considered a major pest of leeks because the species is able to reproduce on this host-plant. However, during summer till well into August F. tenuicornis is relatively abundant in the leek plants. Females , males and larvae were found in many samples. Thus the question rises whether F. tenuicornis is also a major pest during the first half of the growing period of leek crops. Feeding symptom expression is economically relevant shortly after planting and at harvest time. Heavy thrips infestation at a moment just after planting can damage the young leek plants severely, leading to stunted or killed plants. When thrips populations decline sharply during the second half of the growing season the symptoms fade and newly formed leaves are undamaged. Earlier feeding symptoms are then irrelevant. The role of F. tenuicornis in these situations would need more detailed investigation. Although unlikely, feeding symptom development could be different for both species and thus their economic importance from a practical point of view. T. tabaci and F. tenuicornis are the dominant species within the sampled leek plants.The presence of other thrips species in leeks seems to be quite variable and of little practical consequence in terms of feeding damage symptoms.

Fig. 1. Relative abundance of adults of two major thrips species in leeks and in the associated undersown intercrops. Note the logarhitmic ordinate. 182

The presence of populations of T. tabaci and F. tenuicornis within leeks can be followed throughout the winter. Added to more quantitative observations during the winter months (Theunissen, unpubl. data) this makes clear that overwintering crops of leek are a major source of infection for young crops during spring. The thrips fauna of clover and other undersown crops seems to be more varied when compared to that in leek plants. T. tabaci and F. tenuicornis are present but as a part of a broad scala of species and not in dominant numbers. Larvae of both species were not found in the intercrops, which makes it unlikely that these species are attracted to and can reproduce on the clovers. Sampling of the weeds in the ‘weed’ plots was abandoned in an early stage because the species composition of the weeds would also determine the thrips species composition. The variety of weeds in place and time would be reflected in the thrips species composition and would need a separate investigation. From the obtained data it can be concluded that clovers do not act as crops which sustain populations of T. tabaci and F. tenuicornis. The undersown intercrops sampled do not act as a sink for these species and show their own species composition which differs partly from the thrips species composition in the leek plants. The role of F. tenuicornis as a pest of leek has to be investigated in more quantitative detail.

Acknowledgements

The authors wish to express their appreciation for the supervision of the fields and cooperation with the collection of the material by Gijs Schelling.

References

Altieri, M.A. 1994: Biodiversity and Pest Management in Agroecosystems. Food Products Press, Haworth, London: 185 pp. Andow, D.A. 1991: Vegetational diversity and arthropod population response. Annual Review of Entomology 36: 561-586. Finch, S. 1996: “Appropriate/inappropriate landings”, a mechanism for describing how undersowing with clover affects host-plant selection by pest insects of brassica crops. IOBC WPRS Bulletin 19(11), 102-106. Kostal, V. and Finch, S. 1994: Influence of background on host-plant selection and subsequent ovipositon by the cabbage root fly (Delia radicum). Entomologia Experimentalis et Applicata 70: 153-163. Risch, S.J. 1981: Insect herbivore abundance in tropical monocultures and polycultures: an experimental test of two hypotheses. Ecology 62: 1325-1340. Theunissen, J. 1994: Intercropping in field vegetable crops: pest management by agosystem diversification – an overview. Pesticide Science 42: 65-68. Theunissen, J. & Schelling, G. 1996: Pest and disease management by intercropping: suppression of thrips and rust in leek. International Journal of Pest Management 42 (4): 227-234. Theunissen, J. & Schelling, G. 1997: Damage threshold for Thrips tabaci (Thysanoptera: Thrip- idae) in monocropped and intercropped leek. European Journal of Entomology 94: 253- 261. Theunissen, J. & Schelling, G. 1998: Infestation of leek by Thrips tabaci as related to spatial and temporal patterns of undersowing. BioControl 43: 107-119. Theunissen, J., Booij, C.J.H. and Lotz, L.A.P. 1995; Effects of intercropping white cabbage with clovers on pest infestation and yield. Entomologia Experimentalis et Applicata 74: 7-16. Vandermeer, J. 1989: The ecology of intercropping. Cambridge University Press, Cambridge, 237 pp.

183

Insecticidal Control

184

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 183-187

Light oil based pesticides as an effective mean for IPM

Z. Ilovai1, I. Kajati1 & E. Kiss2 1 Plant Health and Soil Conservation Station of Budapest Capital, 1519 Budapest, P.O. Box 340 (Hungary) 2 Plant Health and Soil Conservation Station of Csongrad County, 6800 Hodmezovasarhely, P.O. Box 110 (Hungary)

Abstract: Studies on effectiveness of paraffin oil itself and combined with fatty acid copper salt against virus vectors, mainly aphids, and also its role in inhibition of virus transmission have been conducted for almost twenty years. Experiments were carried out in open field pepper as well as in greenhouse paprika. Mortality of aphids, virus infection of crop, and influence on bacterial and fungal infection were determined in order to judge the biological efficacy of two commersialised products Vektafid A® and Vektafid R®. Side effect on three natural enemies was also checked. The pesticides performed a high activity in killing aphids. Virus-transmission inhibitory effect of paraffin oil varied by years. Results obtained from application of oil-copper soap combination proved more stabile. Both preparations were safe for natural enemies tested. Oil-based natural pesticides may play an important role in IPM in vegetables.

Key words: natural pesticides, virus transmission, vector control, side-effect, Aphidus colemani, Cyrtopeltis tenuis, Encarsia hispida, paraffin oil, fatty acid copper salt

Introduction

Virus diseases are one of the most serious problems in plant protection, particularly in open field vegetables. Virus infections cause considerable quantitative and qualitative losses of valuable and often expensive to grow crops. An effective protection against viruses is always a case of effective management of their vectors. In Hungary the most important aphidophil viruses of vegetables are the following CMV, PVY, AMV. Currently the TSWV, transmitted by thrips, appeared (Ilovai et al, 1996; Kiss, 1998). From among different ideas formed about inhibition of virus transmission the use of light summer oils have been proved to be a reasonable solution for control of not persistent „stylet borne” viruses, transmitted mostly by aphids. The mechanism of action is based on a fine film layer of oil sprayed out on the surface of plant, which interfere with virus retention in aphid stylet (Bradley, 1963; Vanderveken, 1977). During the probing a hydrophobic layer of oil forms in the stylet, which hinders virus retention (Wang & Pirone, 1996). In effect spreading of viruses significantly decrease. Experiments carried out in Hungary with oil-based products proved decreasing of virus infection by 60-80 % (Basky, 1983; Basky et al, 1987; Kajati et al., 1989; Kiss et al. 1988). Experience with foreign products stimulated research work initiated in 1980’s aimed at developing home products and technologies of their application in the practice. At first testing of paraffin oil took place. In result a new oil-based preparations were made, one containing the oil itself and another one with content of fatty acid copper salt. The copper component opened a new perspectives for application: it widened the spectrum of action by possibility of

183 184

control of bacterial and fungal diseases, and on the other hand the oil strengthened the effect of copper (Ilovai et al, 1995; Kajati, 1997). Most of the application work was done on pepper (Capsicum annuum L. spice and delicate varieties), the crop of high importance in Hungarian open filed and greenhouse vegetable growing. Sprayings against aphid vectors were harmonised with their flight activity recorded by yellow water traps. Judgement of the efficacy of treatments included assessments of mortality of aphids, visual and laboratory assessment (ELISA test) of virus infection, and quantitative and qualitative measurements of yield. Results showed that the products significantly decreased the virus infection of pepper (Huszka et al., 1998). Besides open field application a range of experiments was carried out on side-effect of oil-based products on beneficial fauna (Ilovai et al., 1998) and also some trials were done in order to determine the effect on dangerous exotic whiteflies: Bemisia tabaci (Carnero et al., 1998), Aleurodicus dispersus, Lecanoideus floccissimus (Zoltan et al., 1996; Kajati et al., 1997). Experience gained during years of work with oil-based pesticides shows that these products are suitable mean for integrated management of virus vectors and in consequence of virus diseases, both in open field and in greenhouse pepper. Presently a number of oil-based natural pesticides are registered in Hungary and available for growers.

Material and methods

The experiments were carried out in open field and in greenhouse pepper, either in spice or delicate varieties, according to Hungarian official methods of testing zoocides, based on EPPO standards and Zoocide testing methods, 1984 (Herzig, 1997). Main characteristics of experimental product: Name: ...... Vektafid A® (Rogator Ltd., HU), Reg. number: 24.199/1997 HU Active ingredient: ...... paraffin oil, 83% + Atplus 300 F, 17% Application dose: ...... 3-6 l/ha Spray concentration: ...1% Name: ...... Vektafid R® (Rogator Ltd., Hu.), Reg. number: 27.401/1998 HU Active ingredient: ...... paraffin oil, 79% + fatty acid copper salt, 6% + Atplus 300 F, 15% Application dose: ...... 3-6 l/ha Spray concentration: ...1% In order to prevent the virus infection sprayings against aphid vectors were harmonised with their flight activity recorded by yellow water traps. Sprayings were done 1-4 times, in series of treatments repeated weekly during the main period of aphid invasion. Judgement of the efficacy of treatments included assessments of mortality of aphids, visual and laboratory assessment (ELISA test) of virus infection (CMV, PVY, AMV, TSWV). In greenhouse the treatments were started after planting and repeated 4-6 times. The side effect of oil-based preparations was studied in laboratory conditions. Leaves infested by Bemisia tabaci were infected with Encarsia hispida. When the pupae turned black, the leaves were immersed in Vektafid solutions. Water served as a control. The mortality of the parasitoid was calculated on the basis of emerged adults, using Schneider-Orelli formula. In the case of Cyrtopeltis tenuis adults and nymphs were placed on sprayed leaves in small insect cages. The mortality was assessed after six days using the formula mentioned before. Effect on Aphis gossypii an Aphidius colemani was evaluated in nethouse experiment, on pepper, on naturally occured populations. Assessments were carried out after the series of 185

tretment. Aphids were counted by Bank’s scale. The parasitism was expressed in percent of leaves with mummies. After the treatment mummies were collected from the plots and placed into laboratory conditions with the aim of determining the emergence of adults.

Results

Summarised results of experiments on biological efficacy of Vektafid products performed in period of 1984-1998 years are presented in Table 1. Recently it was also proved that besides aphidophil viruses these substances are also able to decrease the dangerous tomato spotted wilt virus infection, transmitted by thrips. The copper compound in addition completes the oil with preventive bactericide and fungicide effect, but according to Huszka et al. (1998) only in conditions of low infection pressure. It is important to emphasise that paraffin oil does not have curative effect, that is why series of treatments are necessary to maintain the prevention. Experience shows that in general Vektafids control aphids well but the decrease of virus infection depends on composition of viruses infecting the crop and on the infection pressure. The efficacy varies by years, due to weather conditions; rainy seasons or strong insolation influence it negatively. The paraffin oil itself is suitable for integrated virus management. In the case of fatty acid copper salt (Cu-oleate) containing product the results proved to be more stabile as the copper soap strengthens the oil’s effect. Compare to copper containing pesticides the oleate form increases the efficacy and in the same time the content of copper is decreased, this way the product suits better the requirements of IPM.

Table 1. Efficacy of oil-based pesticides on pepper diseases and virus vectors in open field and greenhouse experiments, Hungary, 1984-1998

Efficacy interval, % Active ingredient, Number (in comparison with untreated control) product, of Pepper Viruses Bacterial – crop experiments Aphids powdery leaf spot Aphidophil TSWV* mildew Paraffin oil, Vektafid A

– field spice pepper 7 36,9-77,8 n.a. 47,0-70,0 33,9 n.a. – field sweet pepper 3 34,7-54,3 n.a. 86,0-96,3 6,1-8,3 n.a. – greenhouse pepper 3 83,0 77,0 90,6-97,4 n.a. n.a. Fatty acid copper salt + paraffin oil Vektafid R

– field spice pepper 1 43,0 n.a. 97,0 59,0 n.a. – field sweet pepper 2 61,4 n.a 95,7 57-61,3 n.a. – greenhouse pepper 3 69,0-92,0 82,5. 84,8-98,2 n.a. 96,9 * thrips transmitted virus

186

The tests carried out on beneficial insects showed quite a positive picture: the bioagents did not suffer from the treatments (see Table 2, 3). On the basis of obtained data the products according to IOBC principles, might be classified as harmless, risk category 1. With the propagation of IPM ideas more data will be necessary, particularly on the side effect on natural enemies widely applied in greenhouses and also on natural populations, specific for certain agroecosystems.

Table 2. Side effect of natural pesticides on beneficial insects in laboratory test, Tenerife, 1995

Mortality, % Beneficial insect Vektafid A, 1% Vektafid R, 1% Encarsia hispida parasitic wasp (black pupae) -5,0 -12,8 -5,8 10,0 Cyrtopeltis tenuis predatory bug Adults 15,9 9,6 Nymphs 0,0 2,7

Table 3. Effect of natural pesticides on Aphis gossypii and its parasitoid Aphidius colemani (after 3 times application on sweet pepper), Tenerife, 1995

Aphidius colemani Treatment, Number of aphids Percentage of leaves with Emergence of adults concentration per leaf parasitised aphids from mummy, % Vektafid A, 1% 1,18 100,0 68,0 Vektafid R, 1% 1,03 42,5 63,3 Untreated control 45,6 82,5 59,1

Oil-based natural pesticides have been developed from products originally used as surfactants. Hungarian experience proved their indisputable role in inhibiting virus infections in pepper. According to preliminary studies these preparations performed hopefully in controlling aphid activity in potato and tomato, which may gain importance in suppressing so- called necrotic strain of potato virus Y (PVY) and other potato viruses spreading in Europe. Favourable toxicological parameters make these active ingredients environment safe, thus they are suitable for development of integrated technologies for ecological farming as well.

References

Basky, Zs. 1983: A new way to use paraffin oil – surfactant blends “Atplus 411 F” in seed cucumbers to decrease stylet-borne virus infections. XXXV Intern. Symp. on Crop Prot., 03 May, 1983. Med. Fac. Landbow Rijksuniv., Gent, Belgium 3: 839-846. Basky, Zs. Kajati I., Kiss F., Kölber M., Nasser M.A.K. 1987: Inhibition of aphid transmission of plant viruses by light summer oils. Med. Fac. Landbow., Gent 52(3a): 1027- 1031. Bradley, R.H.E. 1963: Some ways in which a paraffin oil impedes aphid transmission of potato virus Y. Can. J. Microbiol. 9: 369-380. 187

Carnero A., Hernandez-Suarez E., Torres R., Hernandez-Garcia M., Ilovai Z. & Kiss F.E. 1998: Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) and its natural enemies: possibilities for integrated pest management. Proceedings of International Workshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hodmezővásárhely, Hungary, 10-14 June 1996: 53-61. Herczig, B. (ed.) 1997: Official methods for testing zoocides. Budapest, Hungarian Min. of Agric. Huszka, T., Ocsko, I. &Kiss, F. 1998: Pepper viruses and the ways of their control. Proceedings of International Workshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hodmezővásárhely, Hungary, 10-14 June 1996: 104-108. Ilovai, Z., Budai, Cs., Carnero, A., Kajati, I., Kiss, E.F., Hernandez-Garcia, M., Hernandez- Suarez, E. & Torres, R. 1998: Development of integrated pest management for protected paprika with particular attention to beneficial arthropods. Proceedings of InternationalWorkshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hodmezővásárhely, Hungary, 10-14 June 1996: 109-114. Ilovai, Z., Budai, Cs., Dormanns-Simon, E. & Kiss, F.E. 1996: Implementation of IPM in Hungarian greenhouses. IOBC wprs Bulletin 19(1): 63-66. Ilovai, Z., Kajati, I., Kiss, E.F. 1995: Oily fatty acid copper salt as a new pesticide. Poster Abstracts of European Conference on Chemistry and Environment Budapest, Hungary, 15-18 May, 1995: 35. Kajati, I., Budai, Cs., Ilovai, Z., Torres, R., Hernandez-Garcia, M., Hernandez-Suarez, E., Carnero, A. & Hatala-Zsellér, I. 1997: Natural pesticides to control the spiralling whiteflies Aleurodicus dispersus and Lecanoideus floccissimus (Homoptera: Aleyrodidae) Poster Palm 97 Symposium, Tenerife, Canary Islands, 28 February 1997. Kajati, I., Kiss, E.F., Kölber, M., Basky, Zs., Nasser, M.A.K. 1989: Effect of light summer oils on aphid transmission of viruses in bell pepper and red pepper fields. Proceedings of 40th Intern. Symp. on Crop Protection, Gent, Belgium Kajati, I., Kiss, F. & Molnar, J. 1997: Vektafid A: uj kornyezetkimelo (IPM “Zold Kategorias”) konnyu nyari olaj, egyes, sulyos karokat okozo kartevok lekuzdesere. [Vektafid A: a new environment friendly (of IPM “Green category”) light summer oil for control of certain pests, causing hard losses]. Novenyvedelem 33(5): 245-249 (in Hungarian). Kiss, E.F., Kajati, I., Kölber, M., Basky, Zs.,& Nasser, M.A.K. 1988: The effect of Atplus 411 F on virus infection of red pepper and bell pepper. Med. Fac. Landbouw. Rijksuniv. Gent 53(2a): 479-486. Kiss, E.F. 1998: Virus diseases of greenhouse pepper in South Hungary. Proceedings of International Workshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hodmezővásárhely, Hungary, 10-14 June 1996: 119-131. Vanderveken, J. 1977: Oils and other inhibitors of non-persistent virus transmission. In: Aphids as virus vectors. K.F. Harris & K. Maramorosch (eds.), Academy Press, New York: 435-454. Zoltan, I., Kiss, E.F., Kajati, I., Budai, Cs., Torres, R., Hernandez-Garcia, M., Hernandez- Suarez, E. & Carnero, A. 1996: Laboratory toxicity test of several natural pesticides on Aleurodicus dispersus Russel (Hom. Aleyrodidae) the spiralling whitefly. Proceedings of XX International Congress of Entomology Firenze, Italy, 25-31 Aug. 1996: 608. 188

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 189-192

Field trials with lambda-cyhalothrin against carrot flies in Norway

T.J. Johansen The Norwegian Crop Research Institute, Holt Research Centre, 9292 Tromso, Norway

Abstract: The effect of using pyrethroids in carrot fly (Psila rosae Fabr.) control was investigated in two seasons (1998-1999) in Norway. Lambda-cyhalothrin proved to be effective in 1999, probably because the spray was applied before egglaying, while it failed to control the flies in 1998, when application took place after the onset of egglaying. The results demonstrated a need for a new control strategy when changing from organophosphorous to pyrethroid insecticides. It becomes crucial to apply the spray before the onset of egglaying.

Key words: carrot flies, lambdacyhalothrin, control strategy

Introduction

An integrated strategy for controlling carrot flies in Norway includes non-chemical methods like crop rotation and selecting suitable growing sites. Adjusting sowing and harvest times is not an option in the northern part of the country, as the carrots need the relatively short and cool growing season to complete growth. Most growers have to apply insecticides to achieve a sufficient reduction in larval damage. In Norway, like many other countries, insecticides are applied when trap catches of adult flies have exceeded a certain threshold. Recently, high insecticide residues was found in carrots sprayed with the organophosphorous (OP) insecticide fenthion, and diazinon is currently the only approved insecticide against carrot flies in Norway (Johansen 1999). Pyrethroids are not known to be environmentally friendly insecticides as they also affect beneficial organisms. On the other hand, use of pyrethroids instead of OP`s reduces the risk of insecticide residues in the carrots. This is due to small dosages and spraying on foliage instead of more or less drenching the soil. In previous studies, lambda-cyhalothrin proved to be effective against carrot flies in laboratory cage tests (Johansen et al. 1999). These experiments indicated that chemical residues on the carrot foliage might kill flies up to two weeks after spraying. Such a residual effect comes in addition to the ”knock down” effect when the spray hits the flies directly. Unfortunately, little is known about the effect of pyrethroids against the carrot fly under field conditions. The aim of the current studies was to test the effect of lambda-cyhalothrin compared to the current sprays with diazinon in small scale trials.

Material and methods

Field trials with small plots (10 m²) in a latin square design with four replicates were established within growers fields at two locations in Norway (Valnesfjord, 67°N, and Rygge, 59°N). Sprays were targeted against the first generation flies (first and only generation in the northernmost trials) and were applied when the trap catches (Rebel®) reached four or more flies/trap/week. The plots were sprayed two or three times with 14 days intervals. Diazinon (Basudin 600 EW, 600 g.a.i./l) was applied in 1000 l of water/ha while lambda-cyhalothrin (Karate 2,5 WG, 25 g.a.i./kg) was applied in 250 l/ha.

189 190

Results and discussion

In two trials in 1998, both lambda-cyhalothrin and diazinon failed to reduce damage compared to unsprayed plots (Table 1). In the field surrounding the strongest attacked trial this year, however, diazinon performed well, probably due to application as a soil drench. In 1999, carrot fly attack was noticeable in only one trial. This year lambda-cyhalothrin reduced the percentage of damaged roots substantially and fully demonstrated the potential of using pyrethroids (Table 1).

Table 1. Effect of lambda-cyhalothrin against carrot flies. a) Valnesfjord 1998. Carrots sown 3 June, sprayed 13 July, 27 July and 14 August and lifted 16 September

Total yield % damaged roots Treatment g.a.i./ha t/ha 1. Unsprayed – 55.4 36 2. Diazinon 1500 49.5 41 3. Lambdacyhalothrin 7.5 50.8 41 4. Lambdacyhalothrin 15 56.0 38 n.s n.s n.s. = not significant (p=0.05)

Table 1. b) Jeløy1998. Carrots sown 25 March, sprayed 2 and 18 June and lifted 10 July

Total yield % damaged roots Treatment g.a.i./ha t/ha 1. Unsprayed – 65.8 10 2. Diazinon 150 67.7 8 3. Lambdacyhalothrin 0,75 66.0 6 4. Lambdacyhalothrin 1,5 65.6 11 P (%) n.s. n.s. n.s. = not significant

Table 1 c) Valnesfjord 1999. Carrots sown 22 May, sprayed 30 June, 14 July and 28 July, and lifted 23 September

Treatment Total yield % damaged roots g.a.i./ha t/ha 1. Unsprayed – 26.0 15 2. Diazinon 1500 26.7 25 3. Lambdacyhalothrin 7.5 29.3 2 4. Lambdacyhalothrin 15 29.2 3 P (%) n.s. 1.36 n.s. = not significant 191

Valnesfjord 1998

20 flies/trap/week

0 24.6. 1.7. 8.7. 15.7. 22.7. 29.7. 5.8. 12.8. 19.8. 26.8. 2.9. 9.9.

Jeløy 1998

10 flies/trap/week 5

0 22.5. 28.5. 4.6. 11.6. 18.6. 25.6. 2.7.

70 Valnesfjord 1999 60

flies/trap/week 20

0 15.6. 22.6. 29.6. 6.7. 13.7. 20.7. 27.7. 3.8. 10.8.

Fig. 1: Carrot fly catches on yellow sticky traps. Arrows indicate the first spraying dates in the field trials

The reason for the unsuccessful pyrethroid spraying in 1998 is probably wrong application time. According to the fly activity graphs, both trials were sprayed too late and 192

probably after the onset of egglaying this year (Figure 1). I 1999, when a significant impact of spraying was observed, the first application was earlier (Figure 1). It is important to remember that pyrethroids mainly affect adult flies, and it becomes crucial to apply the first spray before egglaying starts to prevent larval damage. This change in control strategy when using pyrethroids instead of OP`s makes it necessary to study the traps more than once a week to establish the time for first fly appearance. The results in this investigation originate from field trials with small plots and a large “bank” of carrot flies in the surrounding fields. What happens when whole fields are sprayed with pyrethroids? Can one optimal spray be sufficient to keep the population of flies below the economic threshold throughout the season? Obviously, by spraying whole fields, many flies are “knocked down” and many of the surviving flies are eventually killed by insecticide residuals on the carrot foliage. New experiments including monitoring carrot flies and spraying whole fields may give further knowledge, although many growers already have made their conclusion and have started to use pyrethroids in carrot fly control.

Acknowledgement

Thanks to Salten and Jeløy & Omland Agricultural Research and Extension Groups for hosting the field trials.

References

Johansen, T.J. 1999: Monitoring and control of the carrot fly (Psila rosae Fabr.) in northern Norway. Acta. Agric. Scand., Sect. B, Soil and Plant Sci. 49. In press (accepted August 99). Johansen, T.J., S. Finch & A. Jukes 1999: Effectiveness of insecticides applied to carrot foliage in killing carrot fly. IOBC wprs Bulletin 22 (5): 197-205. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 193-200

Efficacy of insecticide seed treatments of dwarf French bean to control bean seed fly, Delia platura (Meig.)

A. Ester, E. Brommer, J.J. Neuvel & M.T. van Ijzendoorn Applied Research for Arable Farming and Field Production of Vegetables, P.O. Box 430, 8200 AK Lelystad, The Netherlands

Abstract: Field experiments were carried out in 1995, 1996 and 1997 to assess the control of the bean seed fly (Delia platura (Meig.)) in dwarf French bean crop (Phaseolus vulgaris (L.)) by film-coating the seeds with insecticides. The treatment with the insecticides was compared with the standard seed treatment of dichlofenthion and untreated seeds. Coating the seeds with chlorpyrifos in the formulations 75 WG, 250 g/l CS, LOS720 and fipronil 500 FS gave sufficiently good protection against the bean seed fly, but furathiocarb and novaluron were not effective. The fipronil and chlorpyrifos formulations 25 CS and LOS 275, did not cause phytotoxicity.

Key words: Delia platura, Phaseolus vulgaris, seedcoating, chlorpyrifos and fipronil.

Introduction

The bean seed fly (Delia platura (Meig.)) is a commonly, occurring species in countries from Scandinavia to North Africa, India, Japan, Australia, New Zealand and from North America to the temperate areas of South America, (Montecinos et al., 1986; Eckenrode, et al., 1976; Goffau de, 1985). Its hostplants are bean, cabbage, beetroot, spinach, lettuce, lupin, corn, asparagus, melon, celery, radish, soybean, cereals, clover, freesia, gladiolus, onion, broad bean, pea, cauliflower and other brassicas. This insect can cause severe damage in a relatively short period to especially dwarf French and runner beans (Phaseolus vulgaris & P. cocineus) (Hubbeling, 1955; Funderburk et al., 1984). The bean seed fly affects the germination of the bean seeds and development of the plants, consequently reducing the yield. This process takes place particularly in the spring under cool and wet conditions, when germination is slow, thus causing serious reduction of plant stands. Bean seeds for the processing industry are sown chiefly from mid-June till the beginning of July, a period prone to the most severe bean seed fly attack in Belgium as found by Steene, v.d. & Vulsteke (1995). Larrain (1994) monitored the densest population in September by using sticky white traps. A high content of organic matter in the soil increases the probability of an infestation. Namely, the adult flies are attracted to volatilised substances released by the decomposition of organic material from living cover crops or when previous crops like spinach or beans are incorporated into the soil in the spring. Additional observations indicate that the risk of bean seed fly infestation is potentially less when these cover crops or residue from the previous crops remain on the soil surface. Once the growing seedlings are above the soil surface they are less likely to be seriously injured. Since 1968, this pest has been controlled by treatment of the seeds with insecticide 1.5 g. a.i. (dichlofenthion/thiram (37.5%/25%) per unit seed, trade name AAtifon,

193 194

registered in The Netherlands for Delia platura control of bean seeds until 200l only. In several European countries the use of this product is not longer allowed anymore. Moreover, as the compound is usually added to the seeds using a slurry method, the dosage is inaccurate because much of the compound gets lost as the seeds rub against each other. The chemical dust drops to the bottom of the bags with seeds and is discarded by the farmer. Over the past few years a new generation of insecticide for seedtreatment have become available together with a new application techniques for coating of seeds with insecticdes. The objectives of this study were to determine the efficacy of insecticides for the control of D. platura, applied by film-coating bean seeds (Phaseolus vulgaris L.). Additional, on evaluation of the possible toxicity on the germination of the seeds has been done.

Materials and methods

Seed treatments In 1995, the experiments were performed with the dwarf French bean variety, Saranda, provided by Seminis/Royal Sluis B.V., Enkhuizen, which has a thousand kernel weight (tkw) of 276 gram and a germination of 85 %. Seeds of the variety Forum used in the second year, 1996, have a tkw of 256 gram and a germination of 90% and were provided by Novartis Seeds BV, Enkhuizen. In the third year, 1997, the variety Masai provided by Novartis Seeds BV, Enkhuizen were used, with a tkw of 256 gram and a germination of 92%. The seeds used in all experiments were film-coated by Novartis Seeds BV, Enkhuizen using an angled drum mixer technique (Clarke, 1987). The film-coating contained polymeres that gave rise to a dust-free product. To obtain the same amount of insecticide per seed, rates were expressed as per unit of seed, one unit equalling 5,000 (Table 1). All the treatments contained the fungicide thiram at 1.3 g. a.i. per unit of seed. The “untreated” seeds were film-coated with fungicide only. The insecticide fipronil (EXP80415A) was chosen because of its systemic action, and was applied before film-coating the leek seeds, sufficient for the controlling of the onion thrips (Ester et al., 1997). Ester and Jeuring (1992) determined the effect of furathiocarb applied as a seed treatment to control the pea and bean weevil by seed. Chlorpyrifos adequately controls the Delia platura treatment (Montecinos, 1986). The insecticide Novaluron (MCW-275) was chosen because of its inhibitory effect on chitin synthesis formation, thus interferering with the formation of the insect cuticle (acts at time of insect moulting, or at hatching of eggs) and belongs to insect growth regulator (IGR) group, which controls the onion fly larvae well (Eck, van, 1981). The compound dichlofenthion was formulated as a mixure with thiram, containing 1.9 and 1.3 g thiram a.i. per unit seed, respectively. This compound is standard in our experiments.

Efficacy trials Trials were carried out in 1995, 1996 and 1997 at two locations, in Lelystad (in the centre of The Netherlands) and in Westmaas (in the south of the country). Both have a clay soil with 24% silt (Lelystad) and 31% silt (Westmaas). The trials consisted of 15 treatments in 1995, five in 1996 and six in 1997 each, with four replicates. Each plot comprised two 10 m rows 50 cm apart, covering an area of 10 m2. The seeds were sown 6 cm apart in the rows (17 seeds per metre row) at a depth of 6 cm, with

195

a Nodet precision sowing machine as used by Dutch growers of French beans. Sowing periods were mid-May in 1995 and 1996 and the end of May in 1997. Prior to sowing with beans, a spinach crop had been grown and ploughed in shallowly to make the field attractive to bean seed fly. Immediately after sowing, 250 g fishmeal was scattered per row on the soil, to attract the bean seed fly as it is known to find the smell of fishmeal organic material or the organic material itself irresistible.

Table 1. Summary of insecticides and doses [g. a.i. per unit (5,000 seeds) of seed] used to film-coat dwarf French bean seed to control bean seed fly.

Insecticides Formulation 1995 1996 1997 Chlorpyrifos 75 WG 0.25 – – 0.50 – – 1.00 – – 2.00 – – Chlorpyrifos 250 g/l CS – – 0.5 Chlorpyrifos LOS720 0.25 – – 0.50 – 0.5 1.00 – – 2.00 – – Furathiocarb 400 CS 0.4 – – 0.8 – – 1.6 – – 2.0 – – Fipronil (EXP80415A) 500 FS – 0.5 – 1.0 1.0 – – 2.0 – Novaluron (MCW-275) 10 EC – – 0.25 – – 0.50 Dichlofenthion/thiram 37.5%/25% 1.5 1.5 1.5

Statistical analysis The experimental layout consisted of randomised blocks. Data were analysed using analysis of variance (ANOVA) in Genstat 5. Least significant differences (LSD) and F. probabilities were obtained form the ANOVA mean. The student’s t distribution was used to calculate the LSD.

Assessment Field emergence was determined (four weeks after sowing), by counting the number of plants (with or without damage) in a two metre strip of row in 1996 and 1997. The data of emergence of 1995 not being relevant are not presented in this paper. Crop damage by the bean seed fly was assessed in the beginning of June 1995 and mid June in 1996 and 1997. Assessment took place by digging up eight metres of row (divided over two rows) The beans were assigned to one of the following categories: − healthy plants; − ‘snake heads’, i.e. seedlings whose growing point has been damaged, leaving only the hypocotyl and the two cotyledons; − normal-sized plants with a hole in the hypocothyl; − plants with a hole in the hypocothyl, with stunted growth; − ungerminated seeds with larval damage;

196

− germinated seeds that had not emerged and − abnormal plants e.g. with one leaf only, or ‘snake heads’ that had sprouted from a lateral bud.

Results

Field emergence Table 2 gives the relative field emergence, i.e. the ratio of plants to seeds. All plants (including damaged ones) were counted. In 1996 the emergence was strongly influenced by the location and the treatment. At both locations the effect of the treatment revealed that percentage of plants from the untreated seeds was lower than from the treated seeds. Significant differences in field emergence were revealed in 1997 at both locations. In Lelystad, the field emergence of seeds treated with dichlofenthion and chlorpyrifos 250 g/l was significantly higher than from the untreated seeds. The novaluron treatment also produced a lower field emergence. In Westmaas, the field emergence after treatments with dichlofenthion and both chlorpyrifos formulations was significantly higher than from the untreated seeds and the lower doses of the novaluron treatment.

Table 2. The relative field emergence of dwarf French bean (plants as % of seed sown) at Lelystad and Westmaas in, 1996 and 1997.

g. a.i. 1996 1997 Insecticide per unit Lelystad Westmaas Lelystad Westmaas of seed Untreated 0 63 91 88 81 Dichlofenthion 1.5 88 98 97 100 Chlorpyrifos (25CS) 250 g/l 0.5 – – 99 100 Chlorpyrifos LOS720 0.5 – – 94 100 Fipronil 0.5 92 100 – – 1.0 93 100 – – 2.0 92 100 – – Novaluron 0.25 – – 82 71 0.50 – – 89 88 LSD (α = 0.05) 7.2 3.8 7.1 13.7

Efficacy of the insecticides In both locations, the percentage of plants attacked was significantly higher from the untreated seeds than from the treated seeds (table 3). Furthermore, there were more damaged plants in Westmaas than in Lelystad. In Westmaas in 1995, treated seeds with chlorpyrifos at doses of 0.5, 1 and 2 g. a.i. per unit of seed in both formulations as well as the fipronil treatment produced a significantly lower percentage of affected plants than the standard treatment. The lowest dose of chlorpyrifos and the furathiocarb treatment provided the same level of protection as the standard. The results of the field trial shows the same tendency. Table 4 shows that in 1996 the damage to plants produced from the treated seeds was significantly less than those from the untreated seeds. In Lelystad, there was a significant difference between the number of damaged plants following the standard treatment with dichlofenthion and the fipronil treatments of 0.5 and 1 gram. Strikingly, 2 gram fipronil produced results similar to the dichlofenthion.

197

Table 3. Efficacy of the insecticides applied as a film-coat for controlling bean seed fly in dwarf French bean crops. Percentages of damaged plants three weeks after sowing at Lelystad and Westmaas, 1995.

Insecticides g. a.i. per Lelystad Westmaas unit of seed Untreated 0 21 49 Dichlofenthion 1.5 5 28 Chlorpyrifos 75 WG 0.25 5 19 0.50 5 11 1.00 3 7 2.00 0 3 Chlorpyrifos LOS720 0.25 5 18 0.50 2 7 1.00 3 6 2.00 2 6 Furathiocarb 0.4 10 34 0.8 9 24 1.6 10 30 2.0 7 25 Fipronil 1.0 5 8 LSD (α=0.05) 6.2 12.2

Table 4. Efficacy of the insecticides applied as a film-coat for controlling bean seed fly in French bean crops. Number of plants damaged by bean seed fly per metre row, four weeks after sowing in 1996 and two weeks after sowing in 1997.

g. a.i. per 1996 1997 Insecticide unit of seed Lelystad Westmaas Lelystad Westmaas Untreated 0 10.5 10.2 13.2 15.1 Dichlofenthion 1.5 4.0 2.6 11.3 12.3 Chlorpyrifos (25CS) 250 g/l 0.5 – – 9.9 9.8 Chlorpyrifos LOS720 0.5 – – 11.8 7.8 Fipronil 0.5 2.7 2.4 – – 1.0 2.1 2.7 – – 2.0 3.0 1.6 – – Novaluron 0.25 – – 13.7 14.2 0.50 – – 13.9 14.0 LSD (α=0.05) 1.1 1.4 2.38 2.32

In 1997, the table shows that the damage caused by the bean seed fly was so severe that some of the beans had rotted and it was not always possible to recover 17 seeds. In Westmaas, dichlofenthion and both chlorpyrifos treatments resulted in markedly fewer damaged plants compared with the untreated control. In Lelystad, only the chlorpyrifos 25CS treatment produced significantly fewer damaged plants than the untreated control. In Westmaas, the damaged plants following the treatment with chlorpyrifos 720LOS was far less than after the standard treatment with dichlofenthion. Both doses of novaluron produced results similar to the untreated seeds.

198

Discussion

Film-coating of leek seeds with fipronil was successful in controlling the onion fly (Ester, 1999), as was the film-coating of cauliflower seeds with chlorpyrifos in controlling the cabbage root fly (Ester, et al., 1994). The aim of this research was to develop an alternative for the standard bean seed fly control compound dichlofenthion/thiram using film-coating of seeds instead to better protect the plants. In both locations used in the field trials in 1995, 1996 and 1997 the basic population was different. Tables 3 and 4 show an indication of the damage caused by the bean seed fly (untreated row) dependent on the quick emergence of the bean seedlings. High average temperatures in spring result in rapid germination. Of the six insecticides including formulation tested, only fipronil and chlorpyrifos controlled bean seed fly significantly (Tables 3 and 4). In both the location, the beans were sown in a fine tilth. The Nodet sowing-machine compressed the soil well after sowing, thereby creating a better physical barrier against the egg-laying flies than was would have been the case on the loose sandy soils. In both locations there was sufficient residual organic matter from the previous crop to attract the flies. Hammond (1991) found that the bean seed fly population increased when green living cover crops were incorporated into the soil, often resulting in increased bean seed fly injury to young plants. This corresponded with our field trials with beans and a prior crop of spinach. Fishmeal acts as an attractant to the bean seed fly, the use of which resulted in a severe attack at several sites. The organic material itself or its odour is responsible for the attraction (Vulsteke et al., 1989). Eckenrode et al., (1975) mentioned to use of bone meal applied on the soil (after sowing) as a attractand to ensure an adequate bean seed fly infestation. Strikingly, the number of seedlings decreased after every sowing, probably attributable to the bean seed fly before emerging. Field emergence was clearly better in the treatments with dichlofenthion, chlorpyrifos 25 CS and chlorpyrifos 720LOS than in the untreated control. This contradicts of the results of King and Biddle (1973) who found that chlorpyrifos seed treatment produced some phytotoxicity in a certain percentage of the emerged plants. Sparrow et al. (1973) reported that chlorpyrifos, applied as a seed dressing to bean seeds, provided good control of bean seed fly larvae without any phytotoxicity. The phytotoxicity is not a problem when the chemical is applied using correct dosages and methods of application (Montecinos et al., 1986). The field emergence in the treatments with novaluron (0.25 and 0.5 g a.i.) was worse than following the treatments with dichlofenthion and both formulations of chlorpyrifos. Treating seed by coating it with the insecticides dichlofenthion, chlorpyrifos (both formulations) fipronil ensured good protection against the larvae of the bean seed fly. Coating seed with the insecticides chlorpyrifos 75 WG, 25CS and chlorpyrifos 720LOS and fipronil is as effective - and often even more effective – in protecting against attack by bean seed fly larvae than the standard treatment with dichlofenthion (Tables 3 and 4). The results of treatments with novaluron (0.25 g and 0.5 g a.i.) and furathiocarb (0.4, 0.8, 1.6 and 2.0 g a.i.) were similar to the untreated control, from which a conclusion can be drawn that these compounds do not control bean seed fly (Tables 3 and 4). Quiroz (1987) found similar results from the application of chlorpyrifos and furathiocarb as a seed treatment against the bean seed fly attack. Bateman, et al. (1997) reported that field trials with furathiocarb treated lupin seeds produced a partial effect against Delia platura (Trotus & Ghizdavu, 1996 (a and b).

199

The use of a supervised control system may also be considered as a solution. Funderburk et al. (1984) monitored with a cone trap the bean seed fly and predicted the emerge of the first and second flight of the bean seed fly with the number of day degrees (Trotus & Ghizdavu, 1996 (c)). Another way in controlling the bean seed fly is the use of resistant varieties, Vea and Eckenrode (1976) mentioned collored seeded resistant and moderately resistant lines and a commercial variety of Phaseolus vulgaris against the bean seed fly. These lines and variety emerged 2-3 days earlier after sowing than the susceptible varieties, which emerged in 7-8 days. This rapid emergence might render the seedlings less susceptible to bean seed fly attack. In most cases, fipronil and chlorpyrifos 720LOS, 75 WG and the 25CS formulation at a dose of 0.5 gram active ingredient per 5,000 seeds gave statistically significant better protection against bean seed fly than treating seed with dichlofenthion.

Acknowledgements

We thank H.P. Versluis and P.W.V. Bakker, for technical assistance of the field experiments. We are also grateful to Ir. S.B. Hofstede of the seed company Novartis Seeds BV for supplying the seeds and the seed coating. Rhône Poulenc Agro BV and AAKO BV for supplying the chemical compounds.

References

Bateman, G.L., Ferguson, A.W. & Shield, J., 1997: Factors affecting winter survival of the florally determinate white lupin cv. Lucyane. Annals of Applied Biology 130: 349-359. Clarke, B., 1987: Seed coating techniques. In: Application to seeds and soil. T. Martin (ed.), BCPC Monograph 39: 205-211. Eck, W.H. van, 1981: Possible mechanisms of the difference in sensitivity of caterpillars of Adoxophyes orana and Laspeyresia pomonella to diflubenzuron. Entomol. Exp. Appl. 29: 60-68. Eckenrode, C.J., Robbins, P.S. & Webb, D.R., 1975: 1974 insecticide research report on cabbage maggot, seedcorn maggot, aphids on lettuce, and phytotoxicity in cucumbers. New York’s Food and Life Sciences Bulletin 56: 1-6. Eckenrode, C.S., Robbins, P.S. & Webb, D.R., 1976: Control of seedcorn maggot, cabbage maggot and black cutworm (1975 insecticide research report). New York’s Food and Life Sciences Bulletin 6: 1-5. Ester, A. 1999. Controlling of the onion fly (Delia antiqua (Meig.)) with insecticides applied to leek seed. IOBC wprs Bulletin 22(5): 189-195. Ester A. & Jeuring, G., 1992: Efficacy of some insecticides used in coating faba beans to control pea and bean weevil (Sitona lineatus) and the relation between yield and attack. Fabis Newsletter 3: 32-41. Ester, A. de Vogel, R. & Bouma, E., 1997: Controlling Thrips tabaci (Lind.) in leek by film-coating seeds with insecticides. Crop Protection 1: 673-677. Ester, A., Hofstede, S.B., Kosters, P.S.R. & de Moel, C.P., 1994: Filmcoating of cauliflower seed (Brassica oleracea L. var. Botrytis L.) with insecticides to control the cabbage root fly (Delia radicum). Crop Protection 1: 14-19. Funderburk, J.E., Higley, L.G. and Pedigo, L.P., 1984: Seedcorn Maggot (Diptera: Anthomyiidae) Phenology in Central Iowa and Examination of a Thermal-Unit

200

System to Predict Development under Field conditions. Environmental Entomology 13: 105-109. Goffau, de L.J.W., 1986: Inventarisatie van insecten en mijten. In: Jaarboek 1985, Plantenziekten-kundige Dienst Wageningen: 41-44. Hammond, R.B., 1991: Seedcorn Maggot (Diptera: Anthomyiidae) Populations on Ohio Soybean. Journal of the Kansas Entomological Society 64: 216-220. Hubbeling, N. 1955. Ziekten en beschadigingen van bonen. Mededeling nr. 3, Instituut voor Plantenziektenkundig Onderzoek 63 pp. King, J.M. and Biddle, A.J., 1973: Field tests of insecticides for the control of bean seed fly (Delia cilicrura). Proceedings 7th British Insecticide and Fungicide Conference. 567-572. Larrain, P.S., 1994: Population variation, and damage of Delia antiqua (Meigen) and Delia platura (Meigen) (Diptera: Anthomyiidae) on onions seedlings (Allium cepa L.) in north-central area of Chile. Agricultura Tecnica 54: 60-64. Montecinos, M.T., Arretz, P.V. & Araya, J.E., 1986: Chemical control of Delia platura in Phaseolus vulgaris with seed and soil treatments in Chile. Crop Protection 5: 427- 429. Quiroz, C.E., 1987: Chemical control of the seedcorn maggot, Delia platura (Meig.) (Dip.: Anthomyiidae) on beans. Agricultura Tecnica Chile 47: 372-377. Saito, O., 1994: Difference of seasonal prevalence of the seedcorn fly, Delia platura (Diptera: Anthomyiidae), between surveys using a kairomone trap and a fish meal trap in Sapporo, Hokkaido. Annual Report of the Society of Plant Protection of North Japan 45: 147-149. Sparrow, P.R., Huraux, M.J., Komblas, K.N. & Huisman, A.H. 1973: Chlorpyrifos a broud spectrum soil insecticide. Proceedings 7th British Insecticide and Fungicide Conference: 545-556. Steene, van de F. & Vulsteke, G., 1995. Biologische waarnemingen omtrent de bonevlieg, Delia platura (Meigen) in West-Vlaanderen gedurende 1988-1993. Parasitica 51: 123-129. Trotus, E. & Ghizdavu, I., 1996(a): Prevention of Delia platura Meig. Attack at bean crops by seed treatment. Cercetari Agronomice in Moldova 29: 111-114. Trotus, E., Ghizdavu, I. & Guran, M., 1996(b): Experimental results concerning the compatibility among different fungicides, insecticides and bacterial preparations (Rhizobium spp.) used for treating bean seeds. Cercetari Agronomice im Moldova. 29: 105-109. Trotus, E. & Ghizdavu, I. 1996(c): Research on evolution of Delia platura Meig. (Diptera-Anthomyiidae) in the Moldavian forest steppe. Probl. Prot. Plant 24 (1): 13- 18. Vea, E.V. & Eckenrode, C.J., 1976: Resistance to seedcorn maggot in snap bean. Environmental Entomology 5: 735-737. Vulsteke, G., Seynnaeve, M. & Calus, A., 1989: Bonevliegbestrijding (Delia platura). Onderzoek- en voorlichtingscentrum voor land- en tuinbouw. Beitem-Roeselare. 107- 121.

201

Disease Control

202

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 201-210

Pepper pathogen viruses and their control by resistance breeding and light summer oils

E.F. Kiss1, T. Huszka2 & I. Ocskó2 1 Csongrád County Plant Health and Soil Conservation Station, 6800 Hódmezövásárhely, Rárosi str. 110., Hungary 2 Szegedi Paprika Foodprocessing and Trading Co., 6725 Szeged, Szövetkezeti str. 1., Hungary

Abstract: In Hungary, viruses endanger spice pepper plantations every year. The dimension of virus infections is influenced by joint actions of several factors (i.e. viruses, vectors, weather conditions, host plants). We have been surveying the virus infection of spice pepper plantations continuously since 1968. Independently from the examined variety, the rate of virus infected plants was very high (80-100 %) in some years (for example epidemic years were in 1973-1976, 1984, 1986, 1987 and 1989). Concerning virus epidemics: from the beginning of 90s we observed a tendency for improving, thanks to spreading of less virus susceptible varieties. In case of virus epidemic, almost always, relatively early, the aphid vector activity was found strong, because the weather favoured to multiplication of aphids. Capability of resistance to natural and artificial virus infection (TMV, CMV, PVY and AMV complex) of basic breeding materials (lines, candidate varieties and varieties) of Szeged Paprika Co., was determined every year, since 1980, in identical circumstances. Identification of viruses - beside visual survey - is carried out by the help of DAS-ELISA serological method as well. On the basis of examinations of last 2 years, can be established, that half of tested breeding materials tolerated better than the average, the high, complex virus infection. From among varieties of Szeged Paprika Co., Bibor and Viktória showed the best virus resistance, followed by Fesztivál and Mihályteleki. Variety Napfény proved to be medium virus susceptible. Integrated control of viruses is a complex, difficult task. Healthy, virus-free, plate-marked seeds must be used for sowing for the prevention of virus infections. If possible, resistant or tolerant varieties must be grown. Insecticide applications usually do not provide proper protection against virus vector aphids. Instead of less effective insecticide treatments, paraffin oils, inhibiting virus transfer, could be taken into consideration; from among what Vektafid A, Vektafid R, Sprayprover and Agrol- Plus are registered in Hungary.

Key words: viruses, diseases, epidemic, pepper, integrated control

Introduction

Some of most important diseases of spice pepper are caused by viruses. The degree of virus infection is influenced by several factors together. From among these factors the following ones have determining role: • Occurrence of infection sources in the surroundings • Activity of virus spreading vectors • Weather factors • Susceptibility of pepper varieties

201 202

Material and methods

Survey of virus infection of spice pepper plantations continuously since 1968 The epidemics graph is made yearly from survey data of 4-6 plantations in Szeged region, where the situation in the last third period of vegetation was represented. Based on several- year survey and Hungarian literature ( Szirmai, 1941; Horváth, 1966 a, b, 1967 a, b, 1969, 1979 a, b, 1980; Kádár and Kajati, 1974; Burgyán, Beczner and Gáborjányi, 1978; Beczner,1979; Kiss, 1980, 1996; Csilléry, Tóbiás and Ruskó, 1982; Salamon, 1993, 1996). The aphid vector activity was determined by the observation of flight (yellow traps) and plant survey (Horváth, 1972: Basky and Kiss, 1996).

Effect of weather factors on virus infection In 1980-1999 from daily average temperature and precipitation and from spice pepper virus infection data, the weather factors significantly influencing the infection were determined by the help of regression analysis (Kiss et al., 1983).

Study of virus resistant ability of spice pepper varieties and breeding basic materials In every year since 1980, the virus susceptibility of spice pepper lines, candidate varieties and varieties has been tested in identical circumstances with natural and artificial virus infection: tobacco mosaic tobamovirus (TMV), cucumber mosaic cucumovirus (CMV), potato Y potyvirus (PVY) and alfalfa mosaic alfamovirus (AMV) complex. Every year, testing and selection of many hundreds of basic breeding materials is going on (Kiss, Kajati and Schmidt, 1986; Schmidt and Kiss, 1989; Huszka and Kiss, 1995; Huszka, Kiss and Ocskó, 1996).Determination of viruses was carried out by visual examination and by DAS-ELISA serological method (Clark and Adams, 1977). In case of visual assessment an evaluation scale and formula was applied, according to the severity of symptoms:

Infection index equation: ∑i ( ai x fi ) In = N where: In = infection index ai = scale value equivalent to the severity of virus symptoms, 0-5 (0 = symptomless, …, 5 = severe symptoms) fi = frequency belonging to the scale value N = total number of examined plants

Resistance grade (%) equation: ∑ n ( b - 1 ) x 100 RG = N ( B - 1 ) where: RG = resistance grade n = frequency belonging to the scale value b = scale value equivalent to the severity of virus symptoms, 1-4 ( 1 = severe, 2 = moderate, 3 = weak symptoms, 4 = symptomless ) N = total number of examined plants B = the maximum scale value 203

In case of natural virus infection the In (infection index) value, while in case of artificial infection the RG (degree of resistance) was determined.

The inhibiting effect of light summer oils on transfer of viruses by aphid vectors The observation of the flight of aphids was carried out by the help of Moericke yellow bowl traps from the end of May till the end of August. Series of sprayings were carried out in 7-10 days frequency, by 1 % emulsion of preparates with paraffin oil active ingredient, in the period critical for virus infection (from the settling of first winged aphids till the end of the flight). The virus infection on experimental plots was determined at the end of vegetation period, by visual survey and DAS-ELISA test (Basky et al., 1987; Kiss et al., 1988; Ilovai, Kajati and Kiss, 1995; Kajati et al., 1996; Carnero et al., 1997).

Results and discussion

Virus infection of spice pepper plantations since 1968 Independently from the examined variety, the rate of virus infected plants was extremely high (80-100 %) in some years (epidemics years: 1973-1976, 1984, 1986, 1987 and 1989). On the basis of last 30 years, a tendency similar to sinus curve was observed: in the middle of 70s, 80s and 90s years' period (with the exception of few years) generally the virus infection was higher, than in the beginning or at the end of the mentioned periods (Table 1 and Figure 1). Till the 80s, the variety Szegedi-20 was overwhelming, then the number of chosen varieties was gradually increasing. Concerning virus epidemics: from the beginning of 90s we observed a tendency for improving, thanks to spreading of less virus susceptible varieties (for example Mihályteleki, Bíbor, etc.) and to the results of breeding for virus resistance. In case of virus epidemic, almost always, relatively early (at the beginning of June), the aphid vector activity was found strong, because the weather favoured to multiplication of aphids (Table 2).

Table 1: Most important viruses of pepper in Hungary

Transmission Virus name Group Acronym

soil/seed/ Tobacco mosaic virus TOBAMO TMV mechanical Tomato mosaic virus TOBAMO ToMV

by aphids/ mechanical Cucumber mosaic virus CUCUMO CMV Potato virus Y POTY PVY Alfalfa mosaic virus AMV AMV

204

Table 2.Virus incidence and aphid activity in field pepper (Csongrád County, 1984-1999.)

Virus infection of Time of swarming No of Years plants at the end of of aphids winged aphids/ vegetation period (decade) yellow trap in (%) beginning peak time of peak 1984 99 3.d. May 2.d. June 4 500 1985 43 2.d. June 3.d. June 193 1986 96 3.d. May 3.d. June 2 000 1987 86 1.d. June 1.d. July 531 1989 99 3.d. May 2.d. June 13 000 1991 54 3.d. May 2.d. June 340 1992 24 3.d. June 3.d. June 200 1993 50 3.d. May 3.d. June 780 1994 10 3.d. May 3.d. June 130 1995 80 3.d. May 2.d. June 2 600 1996 42 3.d. May 3.d. June 170 1997 15 1.d. June 2.d. June 180 1998 24 2.d. June 3.d. June 380 1999 18 1.d. June 2.d. June 70

Infected plants (%) 120

100

1 2 3 4 5 6 7 8 9 1011121314151617181920212223242526272829303132 1968 Studied years 1999

Fig. 1. Average virus infection of spice pepper at the end of vegetation period (Csongrád County, 1968-1999.) 205

Effect of weather factors on virus infection Three times was found close correlation by regression analysis (Figure 2): • too much of precipitation in May decreased the virus infection of pepper plantations, while an optimal quantity probably favoured to multiplication of aphid vectors and increased the danger of virus infection • extreme heat in June decreased the infection, and • the infection was low in case of very rainy (cool) weather in July too.

100

Infected plants % 0 0 20 40 60 80 100 120 140 Precipitation in May (mm)

100 80

60 40

20 Infected plants % 0 15 17 19 21 23 25 Average daily temperature in June (oC)

100

20 Infected plants %

0 0 30 60 90 120 150 Precipitation in July (mm)

Fig. 2. Connection in-between weather factors and virus infection of spice pepper (Hódmezővásárhely, 1980-1999)

206

Virus resistant ability of spice pepper varieties, basic breeding materials On the basis of last two years, can be established, that about 60 % of spice pepper basic breeding materials examined in the vegetation garden, showed a field tolerance better than the average to natural virus infection. CMV was the dominant virus in infections (Table 3 and Figure 3).

Table 3. Natural virus infection of spice pepper plantations at the end of vegetation period, on the basis of DAS-ELISA tests (Hódmezővásárhely, 1998.)

Examined Virus infection on the basis of DAS-ELISA tests* variety (plant %) Toba- CMV PVY AMV TSWV CMV+ Total mo PVY Sz-20 3,3 16,7 8,3 3,3 0,0 6,7 38,3 Viktória 0,0 26,6 0,0 0,0 0,0 0,0 26,6 Bíbor 3,3 3,3 10,0 0,0 0,0 0,0 16,6 Napfény 0,0 18,3 10,0 0,0 0,0 0,0 28,3 Mihályteleki 0,0 8,3 0,0 0,0 0,0 0,0 8,3 Fesztivál 0,0 20,0 0,0 0,0 0,0 6,6 26,6 Average: 1,1 15,3 4,7 0,6 0,0 2,2 24,1 * on the basis of tests of 60 plants / variety, Tobamo = TMV+ToMV +PMMV, TSWV = tomato spotted wilt tospovirus

4. 5 4 Average of breeding 3. 5 materials 3 Bíbor 2. 5 2 Viktória 1. 5 Infection index Susceptible control 1 0. 5 0

0 2 88 96 98 9 99 9 9 1 1 199 1994 1 1 Studied years

Fig. 3. Natural virus susceptibility of spice pepper varieties (Hódmezővásárhely, 1988-1998)

207

Half of examined basic materials tolerated more than the average, even the severe complex provocative virus infection. Bíbor and Victoria had the best virus resistant abilities, followed by Fesztivál and Mihályteleki varieties (Figure 4). Viktória is a TMV resistant variety carrying the L1 gene (Table 4).

Sz20 Mihályteleki Bíbor

20 Tolerant 10

-10

-20 average -30

-40 Susceptible -50 Alternation of RG values from the 1990 1991 1992 1993 1994 1995 1996 1997 1998

Sz20 Viktória Napfény

60 50 40 30 Tolerant 20 10 0

average -10 -20 -30 -40 Susceptible -50 Alternation of RG values from the 1990 1991 1992 1993 1994 1995 1996 1997 1998

Fig. 4. Infection resistance level (RG* value) of spice pepper varieties (Hódmezővásárhely, 1990-1998) (*RG = ability for resistance to complex (TMV, CMV, PVY, AMV) virus infection)

208

Table 4. Resistance / susceptibility of Capsicum species against tobamoviruses

Capsicum species/varieties Patotype of tobamoviruses isolates* (genes of resistance) TMV-U1 PTMV-U2 DYFV-Sd PMMV-P8 ( P0 ) ( P1 ) ( P1 ) ( P1,2 ) C. annuum cv.Szegedi 20 (L+) S** S S S C. annuum cv. Fehérözön (L1) R S S S C. frutescens cv. Tobasco (L2) R R R S C. chinense P.I. 159236 (L3) R R R R C. annuum cv. Viktória (L1) R R/S R/S S (L2?) RG=100 RG=93,3 RG=84,6 RG=25 * : TMV = tobacco mosaic virus, PTMV = para tobacco mosaic virus, DYFV = dulcamara yellow flack virus, PMMV = pepper mild mottle virus **: S = susceptible, R = resistant, RG = resistance grade (%)

Table 5. Effect of Vektafid preparates on virus infection

Experiment Name of Efficacy %* years place preparate 1984 Bokros Vektafid A 34,7 1985 Mintszent Vektafid A 36,0 1986 Szeged-Mihálytelek Vektafid A 53,0 1987 Hódmezővásárhely Vektafid A 27,4 Szeged-Mihálytelek Vektafid A 77,8 1988 Hódmezővásárhely Vektafid A 75,3 Szeged-Mihálytelek Vektafid A 74,3 1990 Hódmezővásárhely Vektafid A 54,3 Vektafid R 61,4 Felgyő Vektafid A 50,6 Vektafid R 61,1 1991 Sóshalom Vektafid R 43,0 * against aphidofil viruses: CMV, PVY and AMV

The inhibiting effect of light summer oils on transfer of viruses by aphid vectors Vektafid preparates decreased the virus infection of open field spice pepper plantations by 30- 60 % and had a thinning effect on aphids too (Table 5.).

Conclusion

Main steps of preventive integrated control of viruses are: • crop rotation • utilisation of healthy seeds and seedlings • if possible, growing of resistant or tolerant varieties • well timed control by observation of flight of aphid vectors • application of paraffin oils for the inhibition of virus transmission • providing weed-free conditions and proper growing technologies. 209

References

Basky, Zs., Kajati, I., Kiss, E.F., Kölber, M. & Nasser, M.A.K. (1987): Inhibition of aphid transmission of plant viruses by light summer oils. Med. Fac. Landbauww. Rijksuniv. Gent 52/3a: 1027-1031. Basky, Zs. & Kiss, E.F. (1996): Aphid virus vectors in pepper. Int.Workshop on Biological and Integrated Pest Management in greenhouse pepper, Hódmezővásárhely, Hungary, 10- 14 June 1996: 10-13. Beczner, L. (1979): Virus diseases of pepper. In: Zatyko, L. (ed.): Paprikatermesztés. Mezőgazdasági Kiadó, Budapest (in Hungarian): 140-151. Burgyán, J., Beczner, L. & Gáborjányi, R. (1978): Relationship among some tobamo viruses. Act. Phyto. Hung. 13: 75-85. Carnero, A., Hernandes-Garcia, M., Torres, R., Hernandes-Suares, E., Kajati, I., Ilovai, Z., Kiss, E.F., Budai, Cs., Hataláné-Zsellér, I. & Dancsházi, Zs. (1997): Possibilities of aplication of preparates on natural basis in the environment saving pest management (IPM) of greenhouse paprika. IOBC wprs Bulletin 20 (4): 297. Clark, M.F. & Adams, A.N. (1977): Characteristics of the microplate method of enzyme- linked immunosorbent assay for the detection of plant viruses J. Gen. Virol. 34: 574-586. Csilléry, G., Tóbiás, I. & Ruskó, J. (1982): A new pepper strain of tomato mosaic virus. Acta Phytopath. Acad. Sci. Hung. 18: 195-200. Horváth, J. (1966 a): Studies of strains of potato virus Y. 1. Strain C. Acta Phytopath. Hung. 1: 125-138. Horváth, J. (1966 b): Studies of strains of potato virus Y. 2. Normal strain. Acta Phytopath. Hung. 1: 333-352. Horváth, J. (1967 a): Studies of strains of potato virus Y. 3. Strain causing browning of midribs in tobacco. Acta Phytopath. Hung. 2: 95-108. Horváth, J. (1967 b): Studies of strains of potato virus Y. 4. Anomalous strain. Acta Phytopath. Hung. 2: 195-210. Horváth, J. (1969): Information on virus sensitivity of pepper varieties and on differentation of pepper pathogen viruses. (in Hungarian). Növénytermelés 18: 79-88. Horváth, J. (1972): Növényvírusok, vektorok, vírusátvitel. [Plant viruses, vectors, virustrans- mission]. Akadémiai Kiadó, Budapest: 515 pp. (in Hungarian). Horváth, J. (1979 a): New artificial hosts and non-hosts of plant viruses and their role in the identification and separation of viruses. IX. potyvirus group (subdivision-III). Acta Phytopath. Hung. 14: 157-173. Horváth, J. (1979 b): New artificial hosts and non-hosts of plant viruses and their role in the identification and separation of viruses. X. Cucumovirus group: Cucumber mosaic virus. Acta Phytopath. Hung. 14: 285-295. Horváth, J. (1980): Viruses of lettuce. II. Host ranges of lettuce mosaic virus and cucumber mosaic virus. Acta Agronomica 29: 333-352. Huszka, T. & Kiss, E.F. (1995): Recent results in virus resistance breeding of spice pepper (Capsicum annuum L.). Eucarpia IXth. Meeting on genetics and breeding on Capsicum and Eggplant, Budapest, 21-25 Aug. 1995., in summary of proceedings. Huszka, T., Ocskó, I. & Kiss, E.F. (1996): Pepper viruses and the ways of their control. Int. Workshop on Biological and Integrated Pest Management in Greenhouse Pepper. Hódmezővásárhely, Hungary, 10-14 June 1996: 104-108. Ilovai, Z., Kajati, I. & Kiss, E.F. (1995): Oily fatty acid copper salt as a new pesticide. 5 th. European Conference on Chemistry and the Environment, Budapest, 15-18. may. 1995: 35. 210

Kajati, I., Kiss, E.F., Ilovai, Z., Budai, Cs., Kovács, G. & Varga, I. (1996): Role of light summer oils in the integrated control of protected crops. Int.Workshop on Biological and Integrated Pest Management in greenhouse pepper, Hódmezővásárhely, Hungary, 10-14 June 1996: 169. Kádár, A. & Kajati, I. (1974): Results of experiments concerning pepper cultivation problems in Szentes region, in 1972 years. Növényvédelem 10: 20-31. (in Hungarian). Kiss, E.F. (1980): Observation on infection dinamics of pepper pathogen viruses. Növényvédelem 16: 550-555 (in Hungarian). Kiss, E.F. (1996): Virus diseases of greenhouse pepper in South-Hungary. P. Int. Workshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hódmezővásárhely, Hungary, 10-14 June 1996: 119-131. Kiss, E.F., Ilovai, Z., Surányi, R. & Gombos, J. (1983): The effect of ecological factors on the virus infection of pepper. P. Int. Conf. Integr. Plant. Prot., Budapest, 4th - 9th July 1983, 3: 58-64. Kiss, E.F., Kajati, I., Kölber, M., Basky, Zs. & Nasser, M.A.K. (1988): The effect of Atplus 411 F on virus infection of red pepper and bell pepper. Med. Fac. Landbauww. Rijksuniv. Gent 53/2a: 479-486. Kiss E.F., Kajati, I. & Schmidt, H.E. (1986): Methods for evaluation of resistance of condiment pepper plants to several viruses occurring in Hungary. Symp. Recent Results in Plant Virology. Reinhardsbrunn, GDR, 23rd - 27th March 1986: 42-43. Salamon, P. (1993): Resistance genes against Tobamoviruses in the genus Capsicum and the results of resistance breeding in Hungary. Integrált Termesztés a Kertészetben (14.), Budapest, 30. Nov. 1993, 14: 104-113 (in Hungarian). Salamon, P. (1996): Some little-known and newly- emerged viral diseases in pepper (Capsicum annuum L.) produced under cover in Hungary. P. Int.Workshop on Biological and Integrated Pest Management in Greenhouse Pepper, Hódmezővásárhely, Hungary, 10-14 June 1996: 145-151. Schmidt, H. & Kiss E.F. (1989): Use of interferance as base for preselection of pepper plants in the formation of multiple virus resistance. Symp. Recent Results in Plant Virology. Eberswalde, GDR, 18-23 Sept. 1989: in summary of proceedings. Szirmai, J. (1941): Occurrence of a new viral disease "újhitűség" on spice pepper. Növényegészségügyi Évkönyv 1: 109-133 (in Hungarian).

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 211-215

The role of the fungicide resistance examination system in the Integrated Plant Protection of vegetables in Hungary

I. Aponyi & Z. Vendrei Plant Health and Soil Conversation Station, Budapest Capital, Budaörsi út 141 – 145, 1118 Budapest, Hungary

Abstract: According to the wording of IOBC (1973) under the conditions of integrated pest management, every method acceptable from economic, ecological and toxicological aspects shall be applied in order to maintain the harmful organisms below the economic threshold, giving priority to the deliberate use of natural controlling factors. Therefore, in order to answer the questions of when and which pesticide (in our case fungicide) to choose, not only the target pathogen, the developed level of infection, the economic threshold, the efficacy of the fungicide to be applied and its environmental impact shall be taken into consideration, but also the possibility of including the fungicide in the resistance management strategy. On the bases of the system worked out in 1996, in case of poor efficiency of fungicides we not only revise the pest management program, the application technique and the active ingredient content, but test the susceptibility of the given pathogen to the given fungicide at least at two study bases as well. In Hungary we have been working out tests of monitoring resistance to fungicides in five topics, one out of the ten, which is the most important one, is made up by the sensitivity tests of Phytophthora infestans, isolated from tomatoes and potatoes, to phenylamides. By intoducing a new group of active ingredients we have got the tasks to determine the initial sensitivity to fungicides, because with fungicides of specific mode of action resistance does not always appear according to the principle „it’s hit or miss!” („everything or nothing”), but the changes occurring in the sensitivity of the individuals will come out in the form of a gradual shift at population level. This shift in the initial sensitivity can be distinguished from the standard deviation only by testing sufficient number of samples. Initial sensitivity of wild populations to fungicides can move within a wide range. Therefore it is reasonable to determine the order of the range for each fungicide – fungus relation before introducing a new active ingredient to avoid false reasoning during resistance studies. Before intoducing a new group of active ingredients, during the time of registration process, initial sensitivity of wild populations originating from the agroecological districts (at least from 20 places ) of Hungary shall be determined.

Key words: diseases, integrated control, fungicide resistance examination system

Introduction

Soon after the introduction of the fungicides of specific action sites – in the late sixties and early seventies – it became known that the fungicides which used to be efficient, have lost a part of their efficiency. Studies were begun to clear the doubtful cases occuring in the practice in several countries, thus in Hungary, too. These studies have unambiguously confirmed that regular use of fungicides of specific mode of action for longer or shorter times can provoke development of resistant populations in phytopathogenic populations of fungi of the most different taxonomic places. In Hungary benzimidazole resistant populations of Venturia inaequalis and Botrytis cinerea were observed for the first time in the late 1970s and 1981, respectively (Tóth & Vajna 1980 a; Tóth & Vajna 1980 b; Kaptás & Dula 1981; Enisz 1987).

211 212

During study of problems occuring in the practice, the pertinent authority got to the conclusion that it was not enough to clear such cases afterwards, but – as much as possible – these problems shall be prevented. The results obtained in researches of fungicide resistance also stimulated the pertinent authority to establish forecasting of fungicide resistance by conducting monitoring studies in several agro-ecological areas. On the basis of the above mentioned, in 1989 fungicide resistance monitoring inquest started.

Material and methods

Fungicide resistance monitoring and poor efficacy studies having been conducted in Hungary since 1978 indicated that a scheme has to be worked out for the study of fungicide resistance allowing uniform determination of tasks related to the poor efficacy of fungicides, monitoring of fungicide resistance and the introduction of new active substances of fungicides. The object of task to be performed in case of poor efficacy of fungicides is to clear the question of reduced and very poor biological efficiency of fungicides causing problems in practice. The object of monitoring of resistance to fungicides is to clear the question of reduced and very poor biological efficiency of fungicides causing problems in practice, thus to forecast reduction of sensitivity to fungicides for the practice, answering to the question, how long we can count on the good efficacy of the introduced fungicide(s), when we shall replace them by other ones suitable for the control of the population having meanwhile become resistant to them. Forecasting of resistance by a national monitoring system is mainly done in such crops, where specific fungicides have been used since their placing on the market or are used several times during a season, and at the same time a characteristic feature of these fungicides, beside high level of efficiency, is the risk of building up of a resistance. Subjects of monitoring of resistance to fungicides: studies of sensitivity of B. cinerea, isolated from grapes and sunflowers, to benzimidazole and dicarboximide; Phytophthora infestans, isolated from tomatoes and potatoes, to phenylamide; V. inaequalis to benzimidazole and SBI fungicides, Plasmopara viticola to phenylamide fungicides were started. Determination of initial sensitivity to fungicides has become important, because with fungicides of specific mode of action resistance does not always appear according to the principle „it’s hit or miss” (everything or nothing”), but the changes occuring in the sensitivity of the individuals will come out in the form of a gradual shift at population level. This shift in the initial sensitivity can be distinguished from the standard deviation only by testing sufficient number of samples.

Results

Tasks to be performed in case of poor efficacy of fungicides is beside revising the pest management program, application technique and active ingredient content, to test the susceptibility of the given pathogen to the given fungicide at least at two study bases. Scheme of the study, tasks of participants and their connection points are shown in figure 1. In the given period of time (1989-1999) sensitivity of Pseudoperonospora cubensis to phenylamides was studied to clear the problem of poor fungicide efficacy. As a result of tests with 16 isolates of P. cubensis, it was concluded that the lowest efficient rate ranged between 500 and 1000 mg a. i. /l with one third of the isolates, while with two third of them similar results could be achieved only with 2,5 times as much as the practical rate or even by several times more. During the study no isolate of P. cubensis with known initial sensitivity was available,

213

thus, for lack of comparability, it cannot be decided whether sensitivity of cucumber powdery mildew to phenylamides is originally of this kind or we are facing the problem of resistance (Dula et al. 1989).

Fig. 1. Study scheme for resistance to fungicides: poor efficacy of fungicides

Fig. 2. Study scheme for resistance to fungicides: monitoring studies

214

The tasks of monitoring of resistance (Fig. 2) to fungicides is mapping of fungicide- sensitivity, involving each important growing district to provide a basis for preparing a recommendation for pest control according to the state of resistance characteristic of the district. Fungicide-sensitivity of the pathogen shall be monitored during the cycle of vegetation by repeated samplings started at the beginning of the season.The results can inform on timing and frequency of application of the given substance. Relationship among pest management program, field efficiency and fungicide sensitivity shall be searched for. Strategies shall be worked out to prevent building up of resistance and to control the already developed resistance. Management programmes shall be recommended for the practice to prevent and manage resistance problems. Determination of time and type of resistance shall also be covered by the study. Test shall be extended to study cross or double resistance within and among groups of active ingredients. It is necessary to study phenylamide (metalaxyl) sensitivity of the Phytophthora infestans populations of host plants too, because fungicide sensitivity of the mating types can differ among the host plants, as well. According to ten years' results of the Hungarian monitoring metalaxyl resistance exists in potato. Average EC 50 values of the studied populations were above the resistance limit of 10 mg/l every year except 1998. Considering the share of populations, the proportion of resistant ones was similar, about 30% except in 1997 outstanding for the high incidence of late blight. A smaller part of the populations can be considered absolute sensitive (Aponyi & Dula 1994, 1998). In tomato fields metalaxyl sensitivity is characteristic. Symptoms of resistance were found for the first time in 1999 in greenhouses. Before introducing a new group of active ingredients, during the time of the registration process, initial sensitivity of wild populations originating from the agroecological district ( at least from 20 places ) of Hungary shall be determined (Fig. 3 ).

Fig. 3. Study scheme for resistance to fungicides: Determination of basic sensitivity of pathogens to fungicides before introducing new active ingredients or groups of active ingredients

215

Discussion

Agriculturists need a certain level of knowledge and practical experience so that they can understand and use the IPM. Through the already worked out fungicide resistance examination system we can give help to the farmers in such questions as: how they should choose fungicide, in witch the followings have the greatest importance, how effective it is against the pathogen; if it is user and environment – friendly; if it is specifically againnst of the pathogen; how it is included in the strategy of protection against the development of resistance.

References

Aponyi, I. & Dula, T. 1994: Fungicid rezisztencia monitoring vizsgálatok 1992-1994-ben. Scientific Report of OMFB: 12-23. Aponyi, I. & Dula, T. 1998: Fungicid rezisztencia – új védekezési technológiák. Scientific Report of OMFB: 8-16. Dula, T., Kaptás, T., Tóth, B. & Aponyi, I. 1989: Fungicid hatékonysági vizsgálatok uborkaperonoszpóra (Pseudoperonospora cubensis Brk. et Curt.) esetében. Növényvédelem 25: 307. Enisz, J. 1987: Néhány kórokozó gomba fungicid rezisztenciája Magyarországon. Növényvédelmi Tudom. Napok ’87: 58 (Budapest) Kaptás, T. & Dula, T. 1981: Botrytis cinerea benzimidazol típusú szerekkel szemben kialakult rezisztenciája Magyarországon. Heves Megyei Növényvédelmi és Agrokémiai Állomás Jelentése, Eger: 1-10. Tóth, B. & Vajna, L. 1980a: Növénykórokozó gombák fungicidekkel szembeni rezisztenciája. I. A fungicid rezisztencia kérdésének irodalmi áttekintése. Növényvédelem 16: 97-104. Tóth, B. & Vajna, L. 1980b: A Venturia inaequalis (Cooke) Winter rezisztenciája a benzimidazol típusú szisztemikus hatású fungicidekkel szemben. Növényvédelem 16: 151-158.

216

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 p. 217

Parsnip Yellow Fleck Virus in carrots: Development of a disease management strategy

R. H. Binks1, D. Morgan2, N. Spence3 & J. Blood-Smyth1 1 ADAS Consulting Ltd, Kirton, Boston, Lincolnshire, PE20 1EJ, UK 2 Central Science Laboratories, Sand Hutton, York, YO4 1LZ, UK 3 Horticulture Research International, Wellesbourne, Warwick, CV9 9EF

Abstract: Recently the anthriscus strain of parsnip yellow fleck sequivirus (PYFV) has become epidemic in UK grown carrot crops. The virus is transmitted semi-persistently by the willow-carrot aphid (Cavariella aegopodii) but vectors can only successfully transmit PYFV to carrots after acquiring a co virus Anthriscus yellows waikavirus (WYV), from cow parsley (Anthriscus sylvestris). Very little is known about the epidemiology of PYFV/AYV and the relative importance of plant hosts and insect vectors in viral spread. Furthermore, from recent observations of filed infestations of PYFV it is evident that pesticides have no success in controlling spread of the disease; that is because some pesticides are not sufficiently fast acting and do not prevent the relatively short aphid feeding probes which are sufficient for virus transmission. The project aims to close major gaps in our understanding of the complex PYFV/AYV complex. It will undertake strategic research to investigate the dynamics and behaviour of the vector and the role of known and alternative hosts for both vector and virus. The ultimate aim of the project will be to develop diagnostic techniques to improve virus detection and the epidemiology of the disease in carrot crops with the aim of developing sustainable strategies for the management of both vectors and virus.

Key Words: Willow carrot aphid (Cavariella aegopodii), Parsnip Yellow Fleck Virus (PYFV), Anthriscus Yellows waikavirus (AYV), carrots, decision support, monitoring, diagnostics

Acknowledgements

We thank the Ministry of Agriculture, Fisheries and Food (MAFF/LINK scheme No. 248), Horticultural Development Council (HDC), ACRS, Coe House Farms Ltd and DMA Crop Consultants Ltd for providing funding for this work. Thanks also go to Horticultural Research International (HRI), Central Science Laboratories (CSL) and ADAS Research Division for providing academic input into the project.

217 218

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 219-228

Virus disease problems on field cucumber in Hungary

E.F. Kiss1, G. Kazinczi2, J. Horváth2, S. Kobza3, T. Baranyi4, M Varga5, B. Havasréti5 & A. Fehér5 1 Plant Health and Soil Conservation Station of County Csongrád, Hódmezővásárhely, Hungary 2 University of Veszprém Georgikon Faculty of Agriculture, Institute for Plant Protection, Dept. Plant Pathology and Virology, Keszthely, Hungary 3 Plant Health and Soil Conservation Station of Ministry Agriculture, Budapest, Hungary 4 Ministry of Agriculture and Rural Development, Department of Plant Protection and Agro- Environment Management, Budapest, Hungary 5 Plant Health and Soil Conservation Station of Ccounty Győr-Moson-Sopron, Győr, Hungary

Abstract: Viruses caused severe yield losses of field cucumber in Hungary last years. Field surveys have been carried out on field cucumber to evaluate virus infection in the region of Győr-Moson- Sopron county. Virus infection was determined on the basis of symptoms, biotest and with DAS ELISA serological method for the presence of 15 viruses. The virus vector aphid flight was monitored by Moericke yellow water pan. On the basis of field surveys 100% virus infection has been observed in cucumber fields. Virus symptoms were various, depending on varieties, environmental factors, viruses and strains. Out of the viruses investigated only three [cucumber mosaic cucumovirus (CMV) (DTL serotype); zucchini yellow mosaic potyvirus (ZYMV) and watermelon mosaic 2 potyvirus (WMV-2)] have been occurred on cucumber samples. Biological tests confirmed the results of DAS ELISA. There was much difference, regarding the frequency of viruses. ZYMV was dominant in 1998, while CMV was dominant in 1999. The proportion of the complex infection was very high. Till now, besides CMV other viruses can not be detected from weeds in cucumber ecosystems. The peak of aphid flight was in the middle of June and later a secondary peak was observed at the beginning of July, which coincided with the appearance of the first virus symptoms. Regarding, that cucumber production occurs in fields at the same place year by year, soil borne virus vectors may play important role in virus infection. To reduce virus infection we can suggest using of light summer oils, which prevents virus transmission by aphids. It is concluded, that team work of virologists, pathologists, growers, technologists and the breeders is necessary to solve virus problems of field cucumber in Hungary.

Key words: field cucumber, virus diseases

Introduction

Cucumis species originated in tropical and subtropical Africa, which is the primary center of diversity. The secondary centres of diversity are China, Iran and Community of Independent States (Kallo 1988). In Hungary the area of field cucumber is about 4200 ha. The most important parts of the country, where the little-sized conserve cucumber production occur are the following: Győr-Moson-Sopron county – it is the most important part regarding conserve cucumber production –, southern part of Zala and Somogy, Nyírség, Békés, Jász-Nagykun- Szolnok, Bács-Kiskun and Heves counties. Conserve cucumber is one of our most important export goods. Hungary exports 8-10000 tons conserve cucumber a year, mainly to Germany, less to Switzerland, Italy, Benelux States and Austria.

219 220

From virological point of view, cucumber belongs to the virophilous plants. Cucumber (Cucumis sativus L.) is the best known species, susceptible -to our knowledge- to more than 60 viruses (Lovisolo 1980, Horváth 1985). Recent investigations cleared up the behaviour of several Cucumis species to 12 viruses and 16 new host-virus relations were described (Horváth 1985). On the basis of the literature the number of viruses infecting cucurbit plants is nearly forty, belonging to 17 virus genus. Most of them belong to the potyvirus genus. Great part of this viruses can be transmitted by different vectors, mainly by aphids. Several of them can be transmitted by other vectors, like beetles, whiteflies and soil borne nematodes (Table 1).

Table 1. Viruses infecting cucurbit crops, grouped by the vectors

Vector Virus Year reported Other modes of transmission*

Aphids Bryonia mottle potyvirus (BryMV) Lockhart and Fischer (1979) M Clover yellow vein potyvirus (ClYVV) Hollings (1965) M Cucumber mosaic cucumovirus (CMV) Price (1934) M, S Melon vein-banding mosaic potyvirus Huang et al. (1993) M (MVBMV) Muskmelon vein necrosis carlavirus Freitag and Milne (1970) M (MuVNV) Papaya ringspot potyvirus type W (PRSV) Webb (1965) M [syn. watermelon mosaic 1 potyvirus (WMV-1)] Telfairia mosaic potyvirus (TeMV) Nwauzo and Brown (1975) M, S Watermelon mosaic 2 potyvirus (WMV-2) Webb and Scott (1965) M Watermelon Moroccan mosaic potyvirus Fischer and Lockhart (1974) M (MWMV) Zucchini yellow fleck potyvirus (ZYFV) Martelli et al. (1981) M Zucchini yellow mosaic potyvirus (ZYMV) Lisa et al. (1981) M, S Beetles Melone rugose mosaic tymovirus (MRMV) Jones (1981, cit.: Brunt et al. M 1996) Squash mosaic comovirus (SqMV) Freitag (1956) M, S Wild cucumber mosaic tymovirus (WCMV) Freitag (1952) M, S Cucumber green mottle mosaic tobamovirus Ainsworth (1935) M, S, W (CGMMV) Fungi Cucumber necrosis tombusvirus (CuNV) McKeen (1959) M, W Melon necrotic spot carmovirus (MNSV) Kishi (1966) M, S Tobacco necrosis necrovirus (TNV) Smith and Bald (1935, cit.: M Brunt et al. 1996) Cucumber leaf spot carmovirus (CLSV) Weber et al. (1982) M, S Nematodes Tobacco ringspot nepovirus (TRSV) Van Koot and Van Dorst M, S, P (1955, cit.: Lovisolo 1980) Tomato ringspot nepovirus (ToRSV) Provvidenti and Schroeder M, S, P (1970) Arabis mosaic nepovirus (ArMV) Hollings (1963) M, S Tomato black ring nepovirus (TBRV) Forghani et al. (1965) M, S, P Tobacco rattle tobravirus (TRV) Böning (1931, cit.: Brunt et M, S al. 1996) Thrips Tomato spotted wilt tospovirus (TSWV) Samuel et al. (1930, cit.: Brunt M et al. 1996) Whiteflies Beet pseudo-yellows closterovirus (BPYV) Duffus (1965) not known Cucurbit yellow stunting disorder virus Célix et al. (1996) not known (CYSDV) 221

Table 1. cont. Cucumber vein-yellowing virus (CVYV) Cohen and Nitzany (1963) M Lettuce infectious yellows closterovirus Duffus et al. (1986) not known (LIYV) Squash leaf curl bigeminivirus (SLCV) Cohen et al. (1983) not known Watermelon curly mottle bigeminivirus Brown and Nelson (1984, cit. M (WmCMV) Brunt et al. 1996)

Watermelon chlorotic stunt bigeminivirus Jones et al. (1988, cit.: Brunt G (WmCSV) et al. 1996) Leafhoppers Beet curly top hybrigeminivirus (BCTV) Freitag and Severin (1936, cit.: G, C. Lovisolo 1980) Unknown Melon Ourmia ourmiavirus (OuMV) Lisa et al. (1988) M Tobacco mosaic tobamovirus (TMV) Foster and Webb (1965) M Tomato bushy stunt tombusvirus (TBSV) Schmelzer (1958, cit.: Brunt et M, S, P al. 1996) Cucumber soil-borne carmovirus (CuSBV) Koenig et al. (1982) M Melon variegation cytorhabdovirus (MVV) Rubio-Huertos and Pena- not known Iglesias (1973) * C, Cuscuta spp.; G, grafting; M, mechanically; P, pollen; S, seed; W, water

Until know out of them only three aphid borne viruses [cucumber mosaic cucumovirus (CMV), zucchini yellow mosaic potyvirus (ZYMV) and watermelon mosaic potyvirus (WMV)] are known to have economic importance in Hungary (Szirmai 1941, Horváth and Szirmai 1973, Tóbiás et al. 1996). Among cucumber varieties parthenocarp ones: Amber, Accordia, Ringo and Harmonie are the most often grown which has high resistance to viruses on the basis of descriptions (Mártonffy 1999). In spite this fact, severe virus disease has been occurred on field cucumber in Hungary last years, which pay attention to the growers, researchers and breeders (Basky 1983, 1985, Tóbiás et al. 1996, Salamon et al. 1998, Kiss and Fehér 1998, Basky and Tóbiás 1998). Therefore field surveys have been carried out on field cucumber to evaluate virus infection last two years.

Materials and methods

Nearly hundred samples of different cucumber varieties (Accordia, Ringo, Amber, Harmonie, NU8105, Etűd), squash and other species from cucumber ecosystem from different places of Győr-Moson-Sopron county (Csorna, Rábatamási, Kapuvár, Farád, Szárföld) were collected in 1998 and 1999 years. First half of the samples was mechanically transmitted to cucumber (Cucumis sativus L. cvs Delicatess and Amber) in vector free virological glasshouse. The other half of the samples was investigated by DAS ELISA serological method after Clark and Adams (1977) for the presence of 15 viruses [CMV(DTL and ToRS serotype), watermelon mosaic 1 potyvirus (WMV-1), watermelon mosaic 2 potyvirus (WMV-2), zucchini yellow fleck potyvirus (ZYFV), ZYMV, Arabis mosaic nepovirus (ArMV), tomato black ring nepovirus (TBRV), tomato ringspot nepovirus (TRSV), tomato spotted wilt tospovirus (TSWV), squash mosaic comovirus (SqMV), melon necrotic spot carmovirus (MNSV), tobacco necrosis necrovirus (TNV), tobacco rattle tobravirus (TRV) cucumber green mottle mosaic tobamovirus (CGMMV), tomato bushy stunt tombusvirus (TBSV)]. Substrate absorbance was measured two hours after adding the substrate at 405 nm wavelength on Labsystems Multiskan RC ELISA Reader. Test samples were considered positive if their absorbance values exceeded twice those of the healthy control samples. 222

Possibility of seed transmission of viruses was examined in preliminary studies, too. The virus vector aphid flight was monitored by Moericke yellow water pan from the beginning of June to the beginning of August.

Results and discussions

During field surveys, 100% virus infection was observed in cucumber fields. Symptoms were various; depending on cucumber varieties, environmental factors, viruses and virus strains. The most often symptoms were the following: yellow and green mosaic, malformation, blistering, vein banding, necrotic spots, growth reduction, chlorotic rings, leaf deformation and vein clearing on the leaves; reduced growth of the internodes on the stem; severe deformations on the fruits. On the basis of the symptoms it was impossible to distinguish the different viruses because the same viruses can produce different symptoms and oppositely; different viruses could produce the same symptoms. Due to the complex infections more severe symptoms have been occurred. We have confirmed the results of earlier surveys on cucumber in Hungary (Kiss and Fehér 1998). On the basis of serological tests, three viruses (CMV DTL serotype, WMV-2, ZYMV) have been occurred in cucumber samples. ZYMV was first described in Italy (Lisa et al. 1981) and became widespread all over the world (Lisa and Lecoq 1984, Sammons et al. 1989, Schrignwerkers et al. 1991, Perring et al. 1992, Grafton-Cardwell et al. 1996, Alhudaib 1997). In Hungary ZYMV was isolated by Tóbiás et al. (1996) at first time, and became one of the most serious viruses of cucumber. Since 1996 the biology of ZYMV has been intensively studied in Hungary. Tóbiás et al. (1998) reported, that nucleotid sequence of coat protein region of ZYMV-10 strain showed 86-98.6% homology with other ZYMV strains, while amino acid homology are between 91.7-98.2%. ZYMV-10 strain has the highest nucleotid sequence homology with strain isolated in Israel (98.6%) and amino acid homology with California strain (98.2%). Studies on epidemiology of ZYMV were carried out as well (Basky and Tóbiás 1998). Besides CMV, ZYMV and WMV-2, other countries have another viral problems in cucumber, e.g. beet pseudo-yellows closterovirus (BPYV) and cucurbit yellow stunting disorder virus have been associated with yellowing diseases of cucumber in Spain (Berdiales et al. 1999). All cucumber and squash samples were infected by one or more viruses in 1998. 100, 63 and 33% of the cucumber, squash and weed samples were infected with viruses in 1999. In 1998 CMV alone did not occur, while in 1999 WMV-2 alone did not occur on cucumbers. The proportion of the complex infections in both years was very high (Fig. 1). On the basis of our surveys among weeds from cucumber ecosystem five species (Malva neglecta, Ambrosia elatior, Chenopodium album, C. hybridum and Solanum nigrum) were infected with CMV. Besides CMV, other cucurbit viruses can not be isolated from weeds in cucumber ecosytem. Woody plants (Prunus spp.) were not infected by cucurbit viruses. There was much difference between the two years, regarding the frequency of cucurbit viruses. In 1998 the occurrence of ZYMV was dominant, while in 1999 CMV was dominant on cucumber (Fig. 2). The peak of virus vector aphid flight was in the middle of June, and later a secondary peak was observed at the beginning of July, which coincided with the appearance of the first virus symptoms in fields. In spite of the regular spraying with different insecticides, the protection was not effective. Treatments with insecticides are effective only in case, when viruses are transmitted in persistent (circulative) manner. All of the detected cucumber 223

viruses (CMV, ZYMV, WMV-2) can be transmitted by non persistant manner. Therefore effective technology need against aphid vectors, including the use of light summer oils. Bradley et al. (1962) first reported that mineral oil has an inhibitory effect on transmission of a virus transmitted aphids in a nonpersistent manner. Since then, there have been many reports of mineral oil use in laboratory and field applications, alone and in combination with insecticides, on a wide variety of crops (Bell 1980, Basky 1983, 1985, Gibson and Rice 1986, Webb 1993). The mechanism by which mineral oil prevents aphid transmission of viruses is still not understood (Peters and Lebbink 1973, Simons et al. 1977, Qiu and Pirone 1989, Powell 1991, Powell et al. 1992, Wang et al. 1996). Wang and Pirone (1996) support the hypothesis that mineral oil interferes with the retention of virions in aphid stylets.

100 90 80 70 60 50 40 30

virus infection ratio (%) 20 10

0 Total Complex ZYMV 1998 Squash CMV Cucumber 1999 Squash Cucumber Weeds WMV-2 Prunus spp. Prunus

Fig. 1. Virus infection ratio of cucumber and other plants from cucumber ecosystem

Our preliminary studies did not prove seed transmission. In spite this fact and confusing data available in literature (Lecoq et al. 1981, Wang et al. 1984, Nameth et al. 1986, Gleason and Provvidenti 1990, Schrijnwerkers et al. 1991) we can not exclude the possibility of transmission of cucurbit viruses by seeds of cucumber varieties. On the basis of our surveys virus resistant varieties (Harmonie, Ringo etc.) were susceptible to viruses so it is presumed that these varieties have low level of resistance (or tolerance). On the other hand, it can be presumed that new, resistance breaking strain of CMV appeared. Remarkable are the investigations concerned with the virus resistance of various Cucumis species (Webb 1979, Bohn et al. 1980, Pitrat and Lecoq 1984, Weber et al. 1985, Lebeda et al. 1996, Lebeda and Kristková 1996). In an earlier experiments C. myriocarpus have been found to be resistant to CMV (Horváth 1975, 1983). Horváth (1993) studied the reactions of 67 accessions of 12 Cucumis species to seven viruses. From the point of view of resistance to viruses examined C. africanus G1. 2302 proved the best, being immune to five viruses [cucumber leaf spot carmovirus (CLSV), CGMMV, CMV, WMV-2, ZYMV]. Good resistance qualities were shown by Cucumis melo PI 217974, which was immune to four 224

viruses (CLSV, CMV, WMV-2, ZYMV) and hypersensitive resistant to two viruses [Melandrium yellow fleck bromovirus (MYFV), MNSV]. Due to resistance research, today a number of Cucumis cultivars possess resistance to CMV, WMV-1, WMV-2 and ZYMV (Cohen et al. 1971, Provvidenti et al. 1983, Wang et al.1984). It is possible for cucumber breeders to combine genes for resistance to four viruses. No doubt, however, that investigations on resistance to some important viruses (e.g. CGMMV, CLSV, MNSV) are still very deficient (Horváth 1993).

CMV % 70 60 50 40 30 20 a b 10 0

ZYMV WMV-2

Fig. 2. The frequency of occurrence of viruses (%) on cucumber (a, 1998; b, 1999 years)

Regarding, that severe, unsolved viral problems are on field cucumber growing in Hungary, we have to continue investigations to the following directions: (a) from the point of virus epidemiology it is very important to find primary infection sources and virus reservoirs from cucumber ecosystem, with special regard to perennial plants, (b) regarding that field cucumber production occurs in field year by year at the same place, we can not exclude the presence of other, soil borne nematode and fungi transmitted viruses, (c ) natural waters used for irrigation may contain plant viruses and play a vector role in the epidemiology of viruses, (d) effective technology against aphid vectors is necessary, including light summer oils, (e) future studies are necessary about transmission of viruses by seeds of cucumber varieties, (f) until know there are no exact surveys regarding the susceptibility or resistance of cucumber varieties to viruses, (g) identification of sources of resistance is of great importance that could be used for cucumber breeding programs. We should hope, that team work of virologists, pathologists, entomologists, growers, technologists and breeders help us to solve virus problems of field cucumber in Hungary.

Acknowledgements

We should like to thank the Office for Academy Research Groups Attached to Universities and Other Institutes for their financial support.

225

References

Ainsworth, G.C. 1935: Mosaic diseases of the cucumber. Ann. Appl. Biol. 22: 55-67. Alhudaib, K.A. 1997: Studies on zucchini yellow mosaic virus isolated from squash in Al- Hassa Oasis. M.Sc. Thesis. Al-Hassa. Basky, Zs. 1983: A new way to use paraffinic oil-surfactant blends ‘ATPLUS 411 F’ in seed cucumbers to decrease stylet-borne virus infections. Med. Fac. Landbouww. Rijksuniv. Gent 48/3: 839-846. Basky, Zs. 1985: The effect of nutrient supply and oil treatments on the virus incidence in seed cucumber field. Med. Fac. Landbouww. Rijksuniv. Gent 50/3b: 1271-1276. Basky, Zs. and Tóbiás, I. 1998: Studies on epidemiology of zucchini yellow mosaic virus in Hungary. Növényvédelem 34: 477-484. Bell, A.C. 1980: The use of mineral oil to inhibit aphid transmission of potato veinal necrosis virus: A laboratory and field experiment. Rec. Agric. Res. 28: 13-17. Berdiales, B., Bernal, J.J., Sáet, E., Woudt, B., Beitia, F. and Rodriguez-Cerezo, E. 1999: Occurrence of cucurbit yellow stunting disorder virus (CYSDV) and beet pseudo-yellows virus in cucurbit crops in Spain and transmission of CYSDV by two biotypes of Bemisia tabaci. Eur. J. Plant Pathol. 105: 211-215. Bohn, G.W., Kishaba, A.N. and McCreight, J.D. 1980: WMR 29 muskmelon breeding line. HortSci. 15: 539-540. Bradley, R.H., Wade, C.V. and Wood, F.A. 1962: Aphid transmission of potato virus Y inhibited by oils. Virology 18: 327-329. Brunt, A.A., Crabtree, K., Dallwitz, M.J., Gibbs, A.J. and Watson, L. 1996: Viruses of Plants. Descriptions and Lists from the VIDE Database. CAB International University Press, Cambridge 1996: 1484 pp. Célix, A., López-Sesé, A., Almarza, N., Gómez-Guillamón, M.L. and Rodrigez-Cerezo, E. 1996: Characterization of cucurbit yellow stunting disorder virus, a Bemisia tabaci- transmitted closterovirus. Phytopathology 86: 1370-1376. Clark, M.F. and Adams, A.N. 1977. Characteristics of the microplate method of enzyme- linked immunosorbent assay for the detection of plant viruses. J. Gen. Virol. 34: 475-483. Cohen, S. and Nitzany, F.E. 1963: Identity of viruses affecting cucurbits in Israel. Phyto- pathology 53: 193-196. Cohen, S., Duffus, J.E., Larsen, R.C., Liu, H.Y. and Flock, R.A. 1983: Purification, serology and vector relationships of squash leaf curl virus, a whitefly transmitted geminivirus. Phytopathology 73: 1669-1673. Cohen, S., German, E. and Kedar, N. 1971: Inheritance of resistance to melon virus in cucumbers. Phytopathology 61: 253-255. Duffus, J.E. 1965: Beet pseudo yellows virus, transmitted by the greenhouse whitefly (Trialeurodes vaporariorum). Phytopathology 55: 450-453. Duffus, J.E., Larsen, R.C. and Liu, H.Y. 1986: Lettuce infectious yellows virus – A new type of whitefly transmitted virus. Phytopathology 76: 97-100. Fischer, H.U. and Lockhart, B.E. 1974. Serious losses in cucurbits caused by watermelon mosaic virus in Morocco. Pl. Dis. Reptr. 58: 143-146. Forghani, B., Sänger, H.L. and Grossmann, F. 1965: Übertragung des Tomaten-Schwarzring- flecken-Virus an Ölkürbis durch Longidorus attenuatus Hooper in Deutschland. Nematologica 11: 450-451. Foster, R.E. and Webb, R.E. 1965: High-temperature masking of mosaic symptoms on muskmelon. Phytopathology 55: 981-985. 226

Freitag, J.H. 1952: Seven virus diseases of cucurbits in California. Phytopathology 42: 8. Freitag, J.H. 1956: Beetle transmission, host range and properties of squash mosaic virus. Phytopathology 46: 73-81. Freitag, J.H. and Milne, K.S. 1970: Host range, aphid transmission, and properties of muskmelon vein necrosis virus. Phytopathology 60: 166-170. Gibson, R.W. and Rice, A.D. 1986: The combined use of mineral oils and pyrethroids to control plant viruses transmitted non- and semi-persistently by Myzus persicae. Ann. Appl. Biol. 109: 465-472. Gleason, M.L. and Provvidenti, R. 1990: Absence of seed transmission of zucchini yellow mosaic virus from seed of pumpkin. Plant Dis. 74: 828. Grafton-Cardwell, E.E., Perring, T.M., Smith, R.F., Valencia, J. and Farrar, C.A. 1996: Occurrence of mosaic viruses in melons in the Central Valley of California. Plant Disease 80: 1092-1097. Hollings, M. 1963: Cucumber stunt mottle, a disease caused by a strain of Arabis mosaic virus. J. Hort. Sci. 38: 139-149. Hollings, M. 1965: Anemone necrosis, a disease caused by a strain of tobacco ringspot virus. Ann. Appl. Biol. 55: 447-457. Horváth. J. 1975: Cucumis myriocarpus Naud., Gomphrena decumbens Jacq. and Solanum rostratum Dun. as new virus-susceptible and -immune plants. Ann. Inst. Prot. Plant Hung. 13: 189-197. Horváth, J. 1983: New artificial host and non-hosts of plant viruses an their role in the identification and separation of viruses. XVIII. Concluding remarks. Acta Phytopath. Acad. Sci. Hung. 18: 121-161. Horváth, J. 1985: New artificial host-virus relations between cucurbitaceous plants and viruses. II. Cucumis and Cucurbita species. Acta Phytopathol. Acad. Sci. Hung. 20: 253- 266. Horváth, J. 1993: Reactions of sixty-seven accessions of twelve Cucumis species to seven viruses. Acta Phytopathol. Entomol. Hung. 28: 403-414. Horváth, J. and Szirmai, J 1973: Untersuchungen über eine Virose der Wildgurke (Echino- cystis lobata [Michx.] Torr. et Gray). Acta Phytopath. Acad. Sci. Hung. 8: 329-346. Huang, C.H., Chang, L. and Tsai, J.H. 1993: The partial characterization of melon vein- banding mosaic virus, a newly recognized virus infecting cucurbits in Taiwan. Pl. Pathol. 42: 100-107. Kalloo 1988: Vegetable Breeding. Vol. I-III. CRC Press Boca Raton, Florida. Kishi, K. 1966: Necrotic spot of melon, a new viral disease. Ann. Phytopath. Soc. Japan 32: 138-144. Kiss, F. and Fehér, A. 1998: New data to the virus diseases of cucurbit plants. Kertészet és Szőlészet 52-53, 44-46. Koenig, R., Lesemann, D.E., Huth, W. and Makkouk, K.M. 1982: A new cucumber soil-borne virus compared with tombus-, diantho-, and other similar viruses. Phytopathology 72: 964. Lebeda, A. and Kristková, E. 1996: Resistance in Cucurbita pepo and Cucurbita maxima germplasms to cucumber mosaic virus. Genetic Res. Crop Evol. 43: 461-469. Lebeda, A., Kozelská, S., Kristková, E. and Novotny, R. 1996: The occurrence of viruses on Cucurbita spp. in the Czech Republic and resistance of squash cultivars to CMV and WMV-2. Z. PflKrankh. PflSchutz 103: 455-463. Lecoq, H., Pitrat, M. and Clément, M. 1981: Identification et caractérisation d’ un potyvirus provoquant la maladie du rabougrissement jaune du melon. Agronomie 1: 827-834. 227

Lisa, V. and Lecoq, H. 1984: Zucchini yellow mosaic virus. CMI/AAB Description of Plant Viruses. 282: 1-4. Lisa, V., Boccardo, G., D’Agostino, G., Delavalle, G. and D’Aquilio, M. 1981: Characteri- zation of a Potyvirus that causes zucchini yellow mosaic. Phytopathology 71: 667-672. Lisa, V., Milne, R.G., Accotto, G.P., Boccardo, G. and Caciagli, P. 1988: Ourmia melon virus, a virus from Iran with novel properties. Ann. Appl. Biol. 112: 291-302. Lockhart, B.E. and Fischer, H.U. 1979: Host range and some properties of Bryonia mottle virus, a new member of the potyvirus group. Phytopath. Z. 96: 244-250. Lovisolo, O. 1980: Virus and viroid diseases of cucurbits. Acta Horticulturae 88: 33-82. Martelli, G.P., Russo, M. and Vovlas, C. 1981: Ultrastuctures of zucchini yellow fleck virus infections. Phytopathol. Medit. 20: 193-196. Mártonffy, B. 1999: Conserve cucumber. Mezőgazda Kiadó, Budapest. McKeen, C.D. 1959: Cucumber necrosis virus. Can. J. Bot. 37: 913-925. Nameth, S.T., Dodds, J.A., Paulus, A.O. and Laemmlen, F.F. 1986: Cucurbit viruses in California: an ever-changing problem. Plant Disease 70: 8-12. Nwauzo, E.E. and Brown, W.M. 1975: Telfairia (Cucurbitaceae) mosaic virus in Nigeria. Pl. Dis. Reptr. 59: 430-432. Perring, T.M., Farrar, C.A., Mayberry, K. and Blua, M.J. 1992: Research receals pattern of cucurbit virus spread. California Agriculture 46: 35-40. Peters, D. and Lebbink, G. 1973: The effect of oil on the transmission of pea enation mosaic virus during short inoculation probes. Entomol. Exp. Appl. 16: 185-190. Pitrat, M. and Lecoq, H. 1984: Inheritance of zucchini yellow mosaic virus resistance in Cucumis melo L. Euphytica 33: 57-61. Powell, G. 1991: Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Ann. Appl. Biol. 119: 313-321. Powell, G., Harrington, R. and Spiller, N.J. 1992: Stylet activities and potato virus Y vector efficiences by the aphids Brachycaudus helichrysi and Drepanosiphum platanoidis. Entomol. Exp. Appl. 62: 293-300. Price, W.C. 1934: Isolation and study of some yellow strains of cucumber mosaic. Phytopathology 24: 743-761. Provvidenti, R. and Schroeder, W.T. 1970: Epiphytotic of watermelon mosaic among Cucurbitaceae in Central New York in 1969. Pl. Dis. Reptr. 54: 744-748. Provvidenti, R., Gonsalves, D. and Humaydan, H.S. 1983: Occurrence of zucchini yellow mosaic virus in the United States. Cucurbit. Genet. Coop. 6: 99. Qiu, J.Y. and Pirone, T.P. 1989: Assessment of the effect of oil on the potyvirus aphid transmission process. J. Phytopathol. 127: 221-226. Rubio-Huertos, M. and Pena-Iglesias, A. 1973: Bacilliform particles in cortex cells of Cucumis melo fruits. Pl. Dis. Reptr. 57: 649-652. Salamon, P., Salánki, K., Szilassy, D. and Balázs, E. 1998: Pathological characterization of necrotic isolate of cucumber mosaic virus (CMV-N). Növényvédelem 34: 583-591. Sammons, B., Barnett, O.W., Davis, R.F. and Mizuki, M.K. 1989: A survey of viruses infecting summer squash in South Carolina. Plant Disease 73: 401-404. Schrijnwerkers, C.C., Huijberts, F.M. and Bos, L. 1991: Zucchini yellow mosaic virus; two outbreaks in the Netherlands and seed tarnsmissibility. Netherlands J. Plant Pathol. 97: 187-191. Simons, J.N., McLean, D.L. and Kinsey, M.G. 1977. Effects of mineral oil on probing behavior and transmission of stylet-borne viruses by Myzus persicae. J. Econ. Entomol. 70: 309-315. 228

Szirmai, J. 1941. About the virus disease, called ”újhitűség”, causing pepper decline. Növényegészségügyi Évkönyv, Budapest (1937-1939). 1: 109-133. Tóbiás, I., Basky, Zs. and Ruskó, J. 1996: Zucchini yellow mosaic virus is a new pathogen on cucurbitaceous plants in Hungary. Növényvédelem 32: 77-79. Tóbiás, I., Palkovics, L. and Balázs, E. 1998: Characterization of Hungarian strain of zucchini yellow mosaic potyvirus causing severe damage on cucurbit plants. Növényvédelem 34: 613-616. Wang, R.Y. and Pirone, T.P. 1996: Mineral oil interferes with retention of tobacco etch potyvirus in the stylets of Myzus persicae. Phytopathology 86: 820-823. Wang, R.Y., Ammar, E.D., Thornbury, D.W., Lopez-Moya, J.J. and Pirone, T.P. 1996: Loss of potyvirus transmissibility and helper component activity correlates with non-retention of virions in aphid stylets. J. Gen. Virol. 77: 861-867. Wang, Y. J., Provvidenti, R. and Robinson, R.W. 1984: Inheritance of resistance to watermelon mosaic virus 1 in cucumber. HortSci. 19: 587-588. Webb, R.E. 1965: Luffa acutangula for separation and maintance of watermelon mosaic virus 1 free from watermelon mosaic virus 2. Phytopathology 55: 1379-1380. Webb, R.E. 1979: Inheritance of resistance to watermelon mosaic virus 1 in Cucumis melo L. HortSci. 14: 265-266. Webb, R.E. and Scott, H.A. 1965: Isolation and identification of watermelon mosaic virus 1 and 2. Phytopathology 55: 895-900. Webb, S.E. 1993: Effetc of oil and insecticide on epidemics of potyviruses in watermelon in Florida. Plant Dis. 77: 869-874. Weber, I., Döring, U., Meyer, U. and Richter, J. 1985: Ein Beitrag zur Bewertung der Resistenz von Gurken-Genotypen gegenüber dem Gurkenmosaik-Virus (cucumber mosaic virus) anhand der Virusvermehrung. Arch. Phytopathol. PflSchutz 21: 251-257. Weber, I., Proll, E., Ostermann, W.D., Leiser, R,.M., Stanarius, A. and Kegler, H.. 1982: Charakterisierung des Gurkenblattflecken-Virus (cucumber leaf spot virus), eines bisher nicht bekannten Virus an Gewächshausgurken (Cucumis sativus L.). Arch. Phytopathol. PflSchutz 18: 137-154. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 229-232

Experiences of the use of Coniothyrium minitans based biofungicide against Sclerotinia diseases

G. Bohár1, L. Vajna1, I. Aponyiné Garamvölgyi2, S. Csete, K. Kerényiné Nemestóthy, P. Balogh, G. Illés & Z. Becsey 1 Plant Protection Institute, Hungarian Academy of Sciences, 1022 Budapest, Herman O. 15, Hungary 2 Plant Health and Soil Conservation Station, 1118 Budapest, Budaörsi út 141-145, Hungary

Abstract: Sclerotinia diseases cause serious loss in vegetable, field and ornamental plants world-wide. Besides of their harmful environmental effect, chemical control methods provide only limited control. Coniothyrium minitans is an effective hyperparasitic fungus of Sclerotinia species. Commercial biocontrol products of C. minitans for greenhouse use have been existed for a few years. Experimental applications of a registered product and an experimental formulation proved practical usefulness of C. minitans even in open field situations but revealed a relative insufficiency in extremely Sclerotinia infested soils.

Keywords: Coniothyrium minitans, Sclerotinia spp., white rot, biological control, biofungicide

Introduction

Sclerotinia species (white mould) cause white rot diseases of different vegetable, field and ornamental plants, e.g. paprika, tomato, cucumber, carrot, lettuce, sunflower, beans, soybean, petunia, etc. world-wide. The main infection sources are the sclerotia in the soil. These tough sustaining bodies partly tolerate even soil fumigation. Spraying with chemicals results of considerable environmental threat and is hardly effective against this type of disease. Coniothyrium minitans is a highly specialised, effective hyperparasitic fungus with a host fungus range of Sclerotinia sclerotiorum, S. trifoliorum, S. cepivorum and S. minor in the nature (Whipps and Gerlach 1992). This fungus has a distribution in the temperate zone (Sandys-Winsch 1993). In 1997, two C. minitans based biofungicides were registered, one in Germany and another in Hungary for greenhouse use. Contans and Koni products contain living conidia of the hyperparasitic fungus and are intended to be used for the destruction of living, dormant sclerotia in the soil. During the previous years, several experiments were carried out with the meanwhile registered Hungarian Coniothyrium preparation and an experimental formulation of it in various environmental situations in Hungary in order to elucidate the potential use of this kind of biofungicide in greenhouse and field production and to determine its usefulness against Sclerotinia diseases.

Material and methods

The registered Hungarian C. minitans strain (K1) was used in the registered formulation (Koni) and in an experimental formulation (Koni WP). Koni is a granule for direct spread while Koni WP is a wettable powder for spraying with water to the ground. Both C. minitans preparations has to be applied uniformly to the soil surface and incorporated into the upper

229 230

soil layer 2-4 weeks before planting or sowing. Best biological efficiency of the active agent might be achieved by 60-70 % water saturation and 10-25 °C temperature of the treated soil. Dose of the applied C. minitans conidia varied from 2 x 1012 to 1 x 1013 living conidia/hectare with soil incorporation to 5-20 cm depth. Sclerotinia infestation of the soil was characterised by the disease incidence on the area.

Results

Crop: Cucumber Area: 600 m² plastic tent, Horticultural Research Institute, Budapest History: 65-70% of Sclerotinia infection ratio and plant death by the end of the season during the previous three years Treatment: The same area was treated in three consecutive years. The granule formulation (8x1012 living conidia per hectare) was applied once in 1992 and spray application was used (the same dose) in 1993 and 1994 once a year, incorporated 10 cm deep one month before planting. Results: Decrease of the disease to 33% in 1992, to 5% in 1993 and to 3% in 1994. The disease situation did not get worst during the following years without additional treatments.

Crop: Lettuce Area: 2x300 m² plastic tents, SZESZIKO Ltd., Szigetvár History: Overall presence of Sclerotinia disease during the previous years Treatment: One spray application (8x1012 living conidia per hectare) one month before planting in 1996, incorporated 10 cm deep. Control tents were sprayed every two weeks with chemical fungicides. Results: Disease incidence reached 0.2-2.0 % infection rate in KONI treated tents while it was 20-30 % in control tents.

Crop: Paprika in 1998 and lettuce in 1999 Area: 2000 m² plastic tents, Becsey farm, Balástya History: 10 years long presence of Sclerotinia disease with a continuos 5-10% plant loss exploding up to 40-45 % from 1996 Treatment: Koni spray application (6x1012 living conidia per hectare), incorporated 10 cm deep one month before planting in June of 1998 and a repeated application in October of 1998. Control tents were sprayed regularly with chemical fungicides. Results: At the beginning of October, disease incidence in paprika was under 5 % in Koni WP treated tents while it was almost 30 % in untreated ones. By the end of the production cycle at the end of October, infection rate reached 30 % in Koni WP treated tents while it was over 70 % in control. Complete plant death on account of mycelial infection reached 10 % in control tents while it was almost not present on treated area. In February of 1999, lettuce was planted on the previously treated area. It showed 25 % loss on 400 m2 while the remaining 1600 m² was free of the disease.

Crop: Annual flowers (Petunia, Tagetes and Cosmos spp.) Area: Altogether 8000 m² flower beds in Budapest common parks, Horticultural Company of the Capital (FŐKERT), Budapest History: 30-45 % plant loss due to Sclerotinia disease during the preceding consecutive years. Treatment: KONI granule application (1x1013 living conidia per hectare), incorporated 20 cm deep one month before planting in early spring in 1998 and 1999. 231

Results: Disease ceased already in the first year in Tagetes and Cosmos while it decreased to 3-5 % in Petunia. The second year gave similar results.

Crop: Sunflower Area: 25 m² plots in 4 replications, Gesztely, Plant Health and Soil Conservation Service History: Sclerotia were placed to the soil artificially Treatment: Koni WP treatment with doses of 4x1012 and 2x1012 living conidia per hectare incorporated 5 cm deep. Control was untreated. Results: In control, 35 % of the sclerotia died 60 days after placing sclerotia to the soil. 100 % of sclerotia died in 4x1012 and 2x1012 living conidia per hectare dose experiments after 50 and 60 days of experiment respectively. Sclerotinia rot occurred in control but not in the treated area.

120

100 Control

80 2x10 to12

60 4x10 to12

0 01020405060 days after putting sclerotia to the soil Fig. 1. Dying rate of sclerotia due to Koni WP treatment with dose of 2x1012 and 4x1012 living conidia per hectare

Discussion

• The C. minitans products had considerable control effect on Sclerotinia disease in all cases. In moderate disease situations, even the first application could reduce disease occurrence under practically acceptable level. However, one of the most important evidence of the experiences with C. minitans is that the effectiveness depends very much on measure of soil infestation by Sclerotinia. Higher the number of sclerotia in the soil is, lower the efficiency of C. minitans will be. Probably, a very simple model might be used for this situation, namely: C. minitans always kills the same proportion of sclerotia, about 90-98 %. But the forthcoming disease situation will depend on the absolute number of the escaping sclerotia. Repeated application or higher dose may solve this problem. • C. minitans provides a long lasting control effect at least for a whole vegetation period. • Appearance of Sclerotinia disease is influenced also by the sensitivity of the plant species grown. 232

• The dose to be applied should depend on the degree of sclerotia pollution of the soil. Lower dose is able to exert similar sclerotia destruction but longer time period is needed. • Different formulations did not show significant difference in effectiveness. • C. minitans preparations were proved to provide effective and environmentally friendly control of Sclerotinia diseases. C. minitans seems to be one of the most promising biocontrol agent and this kind of biofungicide might be competitive with chemical products on the world market.

References

Sandys-Winsch, C., Whipps, J. M., Gerlach, M. and Kruse, M. (1993): World distribution of the sclerotial mycoparasite Coniothyrium minitans. Mycological Research 97: 1175- 1178. Whipps, J. M. and Gerlach, M. (1992): Biology of Coniothyrium minitans and its potential for use in disease biocontrol; Review. Mycological Research 96: 897-907.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 233-238

Characterisation of Hungarian Phytophthora infestans isolates in the 1990’s

T. Dula1, I. Aponyi2, K. Varga2, G. Bohár3, J. Bakonyi3 & T. Érsek3 1 Plant Health and Soil Conservation Station of County Heves, H-3300 Eger, P.O. Box 218, Hungary 2 Plant Health and Soil Conservation Station, Budapest Capital, H-1519, Budapest, P.O. Box 340, Hungary 3 Plant Protection Institute, Hungarian Academy of Sciences, H-1525 Budapest, P.O. Box 102, Hungary

Abstract: During characterisation of the Hungarian Phytophthora infestans populations it was proved that both (A1 and A2) mating types are present in Hungary, ensuring generative reproduction. The share of A2 is higher, but on potato the rate of the two types is almost 1:1. Metalaxyl sensitivity of the populations differs year by year, resistance problems shall be faced on potato fields, especially with the mating type A1. In populations infecting tomato the mating type A2 and metalaxyl sensitivity is dominant. The Hungarian populations are also characterised by complex races.

Key words: late blight, tomato, potato, mating types, fungicides, resistance, metalaxyl, race structure

Introduction

Since the mass outbreak of potato blight in Ireland in 1845, the most dangerous disease of potato and tomato is late blight caused by Phytophthora infestans. Two genotypes of P. infestans are distinguished. One of them is the so-called genotype "non-infecting tomato" with more intensive sporulation and causing larger lesions on potato than on tomato, the other one is the genotype "infecting tomato" being similarly aggressive on both host plants (Legard et al., 1995). This specialisation has importance from the point of view of crop protection. The pathogen can reproduce in generative and vegetative ways. Generative process takes place only if the two mating types, A1 and A2 are present at the same place and time. Until the 1970s it was believed that only the mating type A1 is wide-spread in the world and type A2 is present only in Mexico. Nowadays it is already known that mating type A2 is also distributed in the world (Fry et al., 1993), in Europe it has been occurring since the middle of the 1980s. It has been present in Hungary at least from 1991 (Bakonyi et al., 1998). The common presence of the two mating types, with the establishment of the generative processes, results in faster and higher variability, the multiple effects of which fundamentally changes the control of the disease. Among the agronomic methods, crop rotation does not offer a solution due to the several year-long survival of spores originating from the generative reproduction. The previous forecasting methods worked out for the vegetative reproduction cannot be applied either. Great problem is caused by the resistance built up against the systemic active substances (phenylamides) introduced in the late 1970s for chemical control, presenting a breakthrough and widely used all over the world.

233 234

No completely reliable method exists for the control of P. infestans. Breeding for vertical resistance is made more difficult by the high variability of the fungus and the appearance of new races. In this radically changed situation success can be ensured only by a well-based integrated programme. However it needs basic, exact knowledge on the Hungarian populations of P. infestans. Therefore the objective was set out to study the distribution of mating types and races of the Hungarian population as an activity joined to fungicide resistance monitoring studies having been carried out since 1991.

Material and methods

During collection of representative samples, leaves showing symptoms, in some cases greater part of tomato were collected in the field, some tomato samples were taken in greenhouse. Tomato leaves of cultivar Zömök were used for isolation and the in vivo test. The in vitro test and determination of the mating type were done on pea-agar medium containing ampycillin and pymaricin (Érsek and Bakonyi, 1997). Mating type of the Hungarian isolations was determined using races of known mating type. The isolate producing high amount of oospores with the race A1 was qualified as type A2 and the one acting similarly with A2 was specified as A1. Metalaxyl sensitivity of the pathogen was studied in vivo (on leaf discs) and in vitro (culturing in Petri-dishes). The isolate, the growing of which was inhibited by 50% applying at least 10 mg/l rate of the active substance (EC 50) was qualified as resistant. Sensitive was the isolate, for which the determined EC 50 value was not more than 0,01 mg/l (in the regular annual monitoring: 0,1 mg/l). The isolates in the range of 0,01 and 10 mg/l were considered intermediate sensitivity. Races were determined by inoculating potato genotypes carrying different resistance genes. Among the known 11 genotypes R5 and R9 were not available. Tubers of genotypes R 1,2,3,4,6,7,10,11 were obtained from Poland, R8 from Scotland. Medium- old leaves of the same age taken from plants grown from material stored as meristem culture were inoculated. The genotypes on which the fungus provoked rapidly spreading, soaked lesions were qualified as sensitive. In numbering of the races, the number of R genes is indicated which could be overcome by the virulence genes of the pathogen, provoking disease in the plant cultivars, lines carrying the particular genes.

Results and discussion

Mating type In the Hungarian population of P. infestans there are more isolates belonging to the mating type A2, 67% of all the isolates, and only 33% of them is considered A1. Among the isolates originating from potato, the share of the two isolates was almost the same (1:1), mating type A2 made out 52%, 48% of the isolates belonged to A1. Among the isolates taken from tomato, the majority (80%) of the isolates were considered A2 mating type. In our studies several places were found where both mating types of the pathogen were present at the same time, in case of two potatoes: H-3/98 Inke in county Somogy, H-12/98 in county Szabolcs and with one tomato isolate H-14/98 Buj in county Szabolcs (Table 1).

235

Table 1: Characteristics of P. infestans isolates collected in Hungary between 1991 and 1998.

Isolates a Collected area Original b Mating Sensitivity to Pathotyped place/county host type metalaxyl c In vitro In vivo H-3,1/93 Monor/Pest Potato A1 IS NT 1,3,4,7(8)10,11 H-2a/96 Zirc/Veszprém Potato A2 R R 1,2,3,4,7,8,11 H-4/97 Őrhalom/Nógrád Potato A1 R R 1,3,4,7,(8)10,11 H-6/97 Őrhalom/Nógrád Potato A1 R NT NT H-8/97 Cserkeszőlő/Jász-N-Sz. Potato A1 R R 1,3,4,7,10,11 H-1-1/98 Inke/Somogy Potato A2 NT IS NT H-1/2/98 Inke/Somogy Potato A2 NT S NT H-3/1/98 Inke/Somogy Potato A2 IS S 1,3,4,7,11 H-3/2/98 Inke/Somogy Potato A1 R IR 1,3,4,7,10,11 H-3/3-98 Inke/Somogy Potato A2 NT IS 1,2,3,4,7,11 H-4/2/98 Zirc/Veszprém Potato A2 NT S 1,3,4,7,11 H-4/3/98 Zirc/Veszprém Potato A2 NT S NT H-5/1/98 Zirc/Veszprém Potato A2 NT S NT H-5/2/98 Zirc/Veszprém Potato A2 NT S 1,3,4,7 H-2a/98 Forráskút/Csongrád Potato A1 IS NT NT H-12/1/98 ?/Szabolcs-Szatmár-B. Potato A1 NT IS NT H-12/2/98 ?/Szabolcs-Szatmár-B. Potato A2 IS S 1,2,3,4,(7) H-12/3/98 ?/Szabolcs-Szatmár-B. Potato A1 S S 1(2)3,4,7,8,10,11 H-15/98 Kisvárda/Sz.-Sz.-B. Potato A1 R R 1,3,7,11 H-K/91 Kerecsend /Heves Tomato A2 NT S 1,2,3,4,7,10,11 H-2/97 Heves/Heves Tomato A2 S IS 1,3,4,7,(8)10,11 H-12/2/98 Nagycserkesz/Sz.Sz.B. Tomato A2 IS S 1,3,4,7,(10)11 H-13/3/98 Nagycserkesz/Sz.Sz.B. Tomato A2 IR S 1,3,4,7,10,11 H-14/1/98 Buj/Sz.-Sz.-B. Tomato A1 IS S 1,7 H-14/2/98 Buj/Sz.-Sz.-B. Tomato A1 IS IS 1,3,4,7,(10)11 H-14/3/98 Buj/Sz.-Sz.-B. Tomato A2 IS S 1,3,4,7,11 H-16/98 Debrecen/Hajdú-Bihar Tomato A1 R R 1,3,7,11 H-17/98 Heves /Heves Tomato A1 IS S NT H-18/98 Hatvan /Heves Tomato A2 IS IS 1,3,4,7 H-19/98 Szomolya/B.-A.-Z Tomato A1 R S 1,3,4,7,11 H-20/98 Heves/Heves Tomato A2 IS IS 1,(3)4,10,11 H-22/98 Orosháza/Békés Tomato A2 NT IR 1,3,4,7,10,11 H-23/98 Orosháza/Békés Tomato A2 IS S NT H-24/98 Orosháza/Békés Tomato A2 NT S NT H-26/98 Szabadkígyós/Békés Tomato A2 IR S NT H-29/98 Mezőmegyer/Békés Tomato A2 IR S NT f H-30/98 Budapest Tomato A2 R NT NT f H-31/98 Bölcske/Tolna Tomato A2 IR NT 1,3,4,7 f H-32/98 Budapest Tomato A2 IS NT NT a “H” and the first number: a Hungarian isolate and its number: “/number” means origin from the same plot: the last two digits refer two the year of collection. b If not indicated otherwise, the isolate was taken from leaves, f fruits. c S: sensitive (EC 50 < 0,01 mg/l a.i.), R: resistant (EC 50 > 10 mg/l a.i.), IS: intermediate sensitive (EC 50 > 0,01< 1 mg/l a.i.), IR: intermediate resistant (EC 50 > 1 < 10 mg/l a.i.), NT: not tested. d Numbering of virulence genes is in accordance to the number of R gene suppression. 236

Sensitivity to metalaxyl It is necessary to study metalaxyl sensitivity of the populations also per host plants, because fungicide sensitivity of the mating types can differ among the host plants, too (Gisi and Cohen, 1996). This observation was confirmed by our results. According to five years' results of the Hungarian monitoring metalaxyl resistance exists in potato. Average EC 50 values of the studied populations were above the resistance limit of 10 mg/l in every year except 1998. Considering the share of populations, the proportion of resistant ones was similar, about 30% except in 1997 outstanding for the high incidence of late blight. A smaller part of the populations can be considered absolute sensitive. In tomato fields metalaxyl sensitivity is characteristic. Symptoms of resistance was found for the first time in 1999 in greenhouses (Table 2, 3).

Table 2: Sensitivity to metalaxyl (EC 50 values) in populations of P. infestans collected from tomato and potato fields in Hungary between 1995 and 1999

Number of population EC 50 a mg/l a.i. metalaxyl Year Total Potato Tomato Potato Tomato 1995 31 26 5 10,56 0,03 (< 0,01 – 39) b (0,01 – 0,039) b 1996 37 27 10 21,38 0,005 (0,0032 – 320) b (0,0032 – 1,5) b 1997 98 77 21 53,96 0,0019 (0,0032 – 320) b (0,0032 – 0,27) b 1998 33 16 17 2,43 0,0087 (0,0032 – 29) b (0,003 – 0,025) b 1999 50 37 13 16,7 0,81 (< 0,001 - > 100) b (0,004 - > 10) b a mean values b minimum – maximum values, reference strain: EC 50 0,016 mg/l a.i.

Table 3: Proportion (% of total) of P. infestans isolates collected from tomato and potato fields in Hungary between 1995 and 1999 showing a sensitive, intermediate and resistant response to metalaxyl.

Year Number of Proportion of isolates % tested isolates Sensitive Intermediate Resistant Potato 1995 26 15 50 35 1996 27 44 26 30 1997 77 29 22 49 1998 16 50 19 31 1999 37 43 30 27 Tomato 1995 5 20 80 0 1996 10 100 0 0 1997 21 100 0 0 1998 17 65 35 0 1999 13 84 8 8 Reference strain: EC 50 = 0,016 mg/l a.i. 237

Metalaxyl sensitivity of mating types Analysing metalaxyl sensitivity by mating types it can be concluded that majority (70%) of isolates with mating type A2 originating from potato is sensitive. The situation is reverse with the mating type A1, with it the proportion of the resistance are higher (66%). On tomato plants metalaxyl sensitivity is characteristic for both mating types (Table 4).

Race structure Analysing virulence phenotypes of the populations it can be concluded that the Hungarian P. infestans populations are characterised by complex race character, independently from the origin of the isolates. Majority of the isolates is able to suppress at least 4-8 resistance genes, all of them contains a virulence gene of higher number 7-11 (Table 1).

Table 4: Mating type distribution and sensitivity to metalaxyl of P. infestans collected from tomato and potato fields in Hungary.

Isolates (number) Proportion of mating type %

Original host A2 A1 Percentage of total (39) 67 33 Percentage of potato (19) 52 48 Percentage of tomato (20) 80 20

Sensitivity to metalaxyl a Potato Sensitive b 70 17 Intermediate c 20 17 Resistant d 10 66

Tomato Sensitive b 69 50 Intermediate c 31 50 Resistant d 0 0 a in vivo results b Sensitive EC 50 < 0,1 mg/l a.i. c Intermediate EC 50 0,1 - 10 mg/l a.i. d Resistant EC 50 > 10 mg/l a.i.

Acknowledgements

This work was supported by the US-Hungarian Science and Technology Joint Fund, No. 521 and the Hungarian Scientific Research Fund, No. T 022850, and National Committee for Technological Development (OMFB) No. 96-97-44-1195. Authors wish to thank all collegues for collecting the blight samples from the fields.

References

Bakonyi, J. and Érsek, T. 1997: A burgonyavész fenyegető jelei Magyarországon. Növényvédelem 33: 221-228. Bakonyi, J., Láday, M., Dula, T. and Érsek, T. 1998: Characterization of Phytophthora infestans isolates from Hungary. Acta Phytopath. Entom. Hung. 33: 49-54. 238

Bohár, Gy., Bakonyi, J., Dula, T., Garamvölgyi, I. and Érsek, T. 1999: A Phytophthora infestans új populációi Magyarországon. Növényvédelem 35: 301-306. Érsek, T. and Bakonyi, J. 1997: A burgonyavész és kórokozója: a Phytophthora infestans. Növényvédelem 33: 353-382. Fry, W.E., Goodwin, S.B., Dyer, A.T., Matuszak, J.M., Drenth, A., Tooley, P.W., Sujkowszki, L.S., Koh, Y.J., Cohen, B.A., Spielman, L.J., Deahl, K.L., Inglis, D.A. and Sandlan, K.P. 1993: Historical and recent migrations of Phytophthora infestans: chronology, pathways and implications. Plant Dis. 77: 653-661. Gisi, U. and Cohen, Y. 1996: Resitance to phenylamide fungicides: A case study with Phytophthora infestans involving mating type and race structure. Annu. Rev. Phyto- pathology 34: 549-572. Legard, D.E., Lee, T.Y. and Fry, W.E. 1995: Pathogenic specialization in Phytophthora infestans: Agressiveness on tomato. Phytopathology 85: 1356-1361. Sozzi, D., Schwinn, F.J. and Gisi, U. 1992: Determination of the sensitivity of Phytophthora infestans to phenylamides: a leaf disc method. EPPO Bull. 22: 306-309. 239

Krakow Meeting

Monitoring Pest Populations

240

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 239-244

Cutworm (Agrotis segetum) forecasting Two decades of scientific and practical development in Denmark

P. Esbjerg Department of Ecology, Royal Veterinary and Agricultural University, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark

Abstract: Forecasting of attacks is one a main issues of IPM. Threat of sudden attacks as those of A. segetum in Denmark 1975-76-77 is a driving force. Therefore sex traps were employed for monitoring from 1980. However, the interpretation of catch into risk levels was as a problem because of information only about occurrence in time and because of the number of instars between catch and damage. Over the first decade the forecasts improved step by step due to the revealing of soil moisture and temperature as two major factors behind survival/mortality of larvae supplemented with density- >damage studies and numerous field recordings. The first control thresholds were 1988-89. During the next decade DD-values for phenological stages and a refined set of control thresholds opened for special forecasts for control with virus and/or irrigation or with chemicals. Electronic recording of climatic data at farm level combined with modeling made a promising start in 1997 but was terminated by the company involved. Growers reactions to new technical steps versus rutine and negative warnings were noted. The latter tended to erode attention. This example of forecasting shows that in some cases the difficult gab from relative estimate to reliable forecast of subsequent damage risk may be bridged. However, long-time research in collaboration with advisory service and farmers who need ongoing informative “nursing” are prerequisites.

Key words: Agrotis segetum, cutworm, forecasting, sex traps, Integrated Pest Management

Introduction

Forecasting of insect attacks is a central part of IPM (Integrated Pest Management) and IP (Integrated Production) strongly linked to the principle of using economic injury levels to optimize control actions economically as well as environmentally. Obviously the requirement for forecasting increases with increasing variability in attack levels of the particular insect species. Cutworm (Agrotis segetum Schiff., Lep., Noctuidae) are known for certain extremes like the attack level in NW Europe in 1976 (Crüger, 1978, Zethner, 1977). However, a high proportion of years with only moderate attacks or even practical abscence has been demonstrated in Denmark on the basis of a unique historical recording 1906-76 systematized by Stapel (1977). The variation in density of fully grown cutworms has a range from 50-200 cutworms / m2 in 1976 to only 0.2 / m2 in e.g. 1981 and 2000 (pers.obs.). This degree of variation, the very severe losses in 1975, 1976 and 1977 (Zethner & Joergensen, 1976, Esbjerg, unpublished) and the growing interest for IPM made the request for a modernized and reliable forecasting system very clear . Untill that time 8 light traps delivered the input into a thumb rule type of forecasting (Thygesen, 1968). After promising experiments with a prototype sex trap 1977-78 (Esbjerg et al., 1980) this type of trapping with an improved trap version became the source of biological information ever since.

239 240

The problem of forecasting over stages and time

Moth Egg L1 L2 L3 L4 L5-6

Fligth Eggs Practical Cut stalks in some Deep holes in even in 400/& invisible, crops (soil 1-3 cm) roots and tubes cold feeding on (soil 1-10 cm) windy foliage Tiny Roots nigths (soil 1-3 mm) roots holes holes

Very Highly Sensi- Some sensitivity Very robust, robust sensitive tive to low temp. pathogens at rare to low temp. occasions and moist soil

> 3 ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ %%/trap ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ /nigth ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ ⊥ 5 days 83 DD 50 DD 53 DD 80 DD >10oC >12.5oC >10.5oC >8oC

Virus or Synthetic irrigation Pyrethroid

Fig. 1: Illustration of the major part of the life cycle of Agrotis segetum and its crop related activity. The text section further explains activity and which stages are more or less sensitive. The upper bottom part indicate the most important mortalities and below is given the forecasting relevant thermal requirements to be calculated 5 days after catch in excess of the minimum threshold of 3 males/ trap/ week.

241

Materials and methods

The basic tool for monitoring of A. segetum, since 1980, is the ”tray trap” (Esbjerg et al., 1981) with a rubber dispenser loaded with 100 µg of Z5-10Ac, Z7-12Ac and Z9-14Ac in a 1:1:1 blend (Arn et al., 1983) mounted on the sticky bottom. On each trapping site three of these traps are placed as corners of triangle with all sides 50 metres long. Catches are recorded 2-5 times a week depending on catch levels. The sticky cardboard is replaced at least once a week or as soon as the catch exceeds 20-25 moth. The dispenser is replaced after 5-6 weeks. The interpretation of the obtained catches into damage risk first includes the dilemma of handling a relative estimate (occurrence of turnip moths in time). Secondly it, however, also includes the problem of forecasting over developmental stages and time. As indicated on figure 1, this step involves the questions about duration and survival of each of 5 stages in between the moth and the economically significant 5ht and 6th larval instars. To meaningfully ”step over” the younger stages in between catch of moth and possible damage of large larvae a crack-down of ecological details is necessary. This crack-down has taken place in some major steps. A first step was the presentation of historical data by Stapel (1977). Analyses of these data revealed importance of the May-June- July-precipitation (Zethner & Esbjerg, 1978) which was further refined into focusing on June- July-precipitation and July-temperature (Mikkelsen & Esbjerg, 1981) as key factors for the levels of damaging attacks. Second step was the experimental demonstrations of detrimental effect of moist soil on 1st and 2nd instar larvae (Esbjerg et al., 1988) and of no such effect on 3rd and elder larval instars (Esbjerg, 1989). The third step was the experimental demonstration of low temperature as a most important mortality factor to 1st and 2nd larvae and the determination of thermal development requirements for eggs and the three first larval instars (Esbjerg , 1992), which appear on figure 1 together with a summary of the above steps (right figure). The descriped steps haven taken place along with the practical use of traps throughout 20 years and as shown in table 1, the number of participating growers has first increased gradually but later levelled out. Since 1983 the participating growers have payed a fixed seasonal amount per three traps (to be returned) This also included the necessary sticky bottoms, 2 dispensers per trap and printed cards for the recording of catch. In the price was also included issuing of forecasts (recommending no treatment or treatment and time of this). In order to step-wise produce control tresholds some of the growers to whom treatment was recommended were requested to leave untreated field parts for subsequent recording of injuries.

Results and discussion

In table 1 all the milestones in development the forecasting of cutworm attacks are listed. The very first was the issuing of thumb-rule advice to the few participating growers. This advice was before 1986 based on the average catch per night, modulated by soil type precipitation and temperature so that high soil moisture during the roughly estimated period of L1 and L2 would cause a high mortality and subsequently a low risk. It was, however, obvious from damage records in untreated plots, that in 1984 and 1985 the risk-levels predicted for a proportion of the fields were much too high. By the end of 1985 pilot results of temperature influence indicated mortality of young larvae at low temperature as the underlying factor. This was stepwise included in forecasts 1986-93 but from 1994 a more precise Day Degree – based calculation of development times of eggs and the first three larval instars was ready for 242

use (Esbjerg et al., 1995, 1996). As a result both a more precise estimation of age dependent mortalities and optimal timing of treatment (virus spraying or irrigation against L1 and L2 or treatment with synthetic pyrethroid against larvae moulting from L3 into L4) could be worked out. Table 1. Steps in the development of cutworm forecasting in Denmark. *years are years with combinations of moth abundance and weather favorable for cutworm attacks. The grower numbers 1996 and onwards include both Danish (left) and Swedish (right) growers. Ref.s: 1: Mikkelsen & Esbjerg (1981), 2: Esbjerg et al. (1986), 3: Esbjerg (1989a), 4: Esbjerg (1989b), 5: Esbjerg (1992), 6: Esbjerg et al. (1995), 7: Esbjerg et al. (1996), 8: Nilars & Esbjerg (1998).

1978 sex traps with virgin fem. Replaced light 1991 (age dependent mortality, ref. 5) traps. 8 growers 55 growers 1980 ”new” sex trap, thumb rule advice *1992 13 gowers 68 growers 1981 analysis of old records (ref.1) *1993 13 growers 65 growers 1982 early experiments on soil moisture -> 1994 mortality 17 growers 65 growers *1983 initial use of soil moisture in forecasting *1995 adjusted control thresholds DD’s for L1 and L2 (ref.6) 18 growers 71 growers *1984 1996 further threshold and DD details (ref.7) 32 growers 67+33 growers 1985 unexpected natural mortality 1997 introduction of HARDI METPOLE® 30 growers 63+28 growers 1986 intial use of temp. -> mortality in forecasting 1998 Trapping + Metpole for forecasting (ref.8) 51 growers 62+33 growers 1987 1999 43 growers 53+30 growers 1988 (soil moisture , ref.2) 2000 37 growers 48+31 growers

1989 pop.density -> damage, L3+4 mortality 2001 (ref.3), first thresholds (ref.4) 39 growers 40+27 growers 1990 age dependent mortality, first approach 1980-2001 More than 150 untreated reference plots for the assessment of the 47 growers trap-catch/damage relationship.

The full utilization of this possibility was somewhat limited because of the need for sufficient recording of soil temperature and precipitation. Therefore the introduction in 1997 of the Hardi Metpole® (a farm weather station) and a program designed for cutworm 243

forecasting (Nilars & Esbjerg, 1998) appeared as a much desired possibility. This possibility, however, disappeared again already in 2000 because the production of the metpole was stopped by Hardi. Seen in retrospect the effect of the sex trap based forecasting has been high. Since 1978 there has not been any case of important damage (> 2 % non marketable carrots, red beets, leeks or onions, Esbjerg unpublished) at farms formally linked to and following the advice of the forecasting system. As already mentioned this included over-estimation of damage risk in 1984 and 1985, which was subsequently explained on the background of lacking information about mortality of the early larval instars due to low temperatures. It is, however, worth to notice that the damage recordings show that 1983, 1984, 1992, 1993 and 1995 (marked with asterisks in table 1) were years of locally high risk. E.g. in 1983 damage levels of up to 68% unmarketable roots were registered (Esbjerg, 1985). Parallel with this the field recordings of damages since 1995 show examples of 1% damaged roots after recommendation of no treatment and 3-4% damaged roots in untreated plots within fields where treatment were recommended. This demonstrates very clearly that the combination of an array of experimental inputs in combination with ongoing trial-and-error work has enabled a successful covering of the almost impossible gap of variation between sex trap catch and subsequent damage of the late larval instars (cf. Figure 1). Along with this the growers changed their problem perception towards a high confidence to the forecasts, which is also the background for the collaboration with Sweden since 1996 (Table 1). However, the situation is not automatically durable since 2-3 years of ongoing no- treatment forecasts tend to erode the attention of growers. Thus a small proportion of the growers tend to neglect setting up of traps and the current servicing and recording of catch, and in the worst case they later treat in a headless way.

The over-all conclusions are: • Even to insect pest insects wich are in principle difficult to forecast, reliable forecasting may be developed but a sytematic and often long lasting procedure is necessary. • Even a very well functioning forecasting system requires a current catalytic information follow-up to prevent erosion, particularly among growers experiencing longer periods of no treatment actions.

References

Arn, H., Esbjerg, P., Bues, R., Toth, M., Szöcs, G., Guerin, P. & Rauscher, S., 1983: Field attraction of Agrotis segetum males in four European countries to mixtures containing three homologous acetates. J. Chem. Ecol. 9 (2): 267-276. Crüger, G., 1978: Beobachtungen zum starken Erdraupenauftreten (Agrotis spp.) im Jahre 1976. Nachrichtenbl. Dtsch. Pflanzenschutzd. 30: 17-19. Esbjerg, P., 1985: Cutworm (Agrotis segetum) – Forecastings and damages in 1983 and 1984. Proc. 2. Danske planteværnskonf. 1985: 249-260. Esbjerg, P., 1989a: The influence of soil moisture on mortality and the damaging effect of 2nd to 6th instar cutworms (Agrotis segetum Schiff., Lep., Noctuidae). Acta Oecologica, Oecol. Applic. 10: 335-347. Esbjerg, P., 1989b: Knoporme – en risiko, der kan imødegås. Grøn Viden 32: 1-8. Esbjerg, P., 1992, Temperature and soil moisture – two major factors affecting Agrotis segetum Schiff. (Lep., Noctuidae) populations and their damage. IOBC wprs Bull. 15 (4): 82-91. Esbjerg, P., Philipsen, H. & Zethner, O. 1980: Monitoring of flight periods of Agrotis segetum using sex traps baited with virgin females. Danish J. Plant Soil Sci. 84: 387-397. 244

Esbjerg, P., Nielsen, J.K. & Zethner,O., 1981: Influence of trap design on catch of turnip moth (Agrotis segetum, Lep., Noctuidae) males in traps baited with virgin females. Les Mediateur chimiques, Versailles, 16-20 nov. 1981. Les colloques de l’INRA 7: 315-323. Esbjerg, P., Nielsen, J.K., Philipsen, H., Zethner, O. & Øgaard, L., 1986: Soil moisture as a mortality factor for cutworms, Agrotis segetum Schiff. (Lep., Noctuidae). J. Appl. Ent. 102: 277-278. Esbjerg, P., Ravn, H.P. & Percy-Smith, A., 1995: Knoporme i økologiske grønsager. Grøn Viden 87: 1-6. Esbjerg, P., Ravn, H.P. & Percy-Smith, A., 1996: Feromonfælder til agerugler – behovs- bestemt bekæmpelse af knoporme. Grøn Viden 96: 1-8. Mikkelsen, S. & Esbjerg, P., 1981: The influence of climatic factors on cutworm (Agrotis segetum) attack level, investigated by means of linear regression models. Danish J. Plant & Soil Sci. 85: 291-301. Nilars, M.S. & Esbjerg, P., 1998: PC forecasting model for cutworm (Agrotis segetum) in organic farming, based on sex trap catches and data collected with Hardi Metpole®. Proc.15. Danish Plant Prot. Conf., Pests and Diseases 1998: 183-192 . Stapel, C., 1977: Den økonomiske betydning af plantesygdommenes og skadedyrenes bekæmpelse i jordbruget. Ugeskr. f. agron. hort. & lic. 122 (35): 735-746. Thygesen, T., 1968: Iagttagelser over biologien samt resultater af bekæmpelsesforsøg 1959- 1966. Danish J. Plant & Soil Sci. 71: 429-443. Zethner, O., 1977: Losses caused by cutworms (Agrotis segetum) and approaches to their control in Denmark. Proc. British Crop Prot. Conf., Pests & Diseases: 271-277. Zethner, O. & Joergensen, A.S., 1976: Angreb af knoporme i 1975, skader, tab og bekæmpelsesmuligheder. Ugeskr. f. agron., hort., forst. & lic. 121 (25): 530-534. Zethner, O. & Esbjerg, P., 1978: Cutworm attacks in relation to rainfall and temperature during 70 years. Klimatologiske Meddr. 4: 103-108.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 245-252

Survey of aphids on outdoor lettuce and strategies for their control

F. Van de Steene 1, L. Tirry 1 & R. Driessen 2 1 Department of Crop Protection, Laboratory of Agrozoology, Ghent University, Coupure Links 653, 9000 Ghent, Belgium 2 Rijk Zwaan Zaadteelt en Zaadhandel B.V., Postbus 40, 2678, ZG De Lier, The Netherlands

Abstract: Lettuce is sensitive to aphid infestations during the complete production period, from April to mid October. Periodic observations in outdoor lettuce during the 1998 and 1999 growing seasons allowed us to identify all species feeding on in lettuce in the Flanders region. In both years, Nasonovia ribisnigri (Mosley) was the most common leaf aphid species, followed by Macrosiphum euphorbiae (Thomas). Myzus persicae (Sulzer) and Aulacorthum solani (Kalt) were also found but were of minor importance. The root aphid Pemphigus bursarius (L.) was not found in this survey. Aphids in lettuce are mainly controlled by routine insecticide applications with organophosphates, carbamates or pyrethroids. However, problems in the control can increase, due to the decreasing number of registered insecticides and the development of insecticide resistance in aphids. Also, the use of routine insecticide applications is being heavily criticized by consumers and environmentalists. For that reason, 2 alternative and approved control measures were tested in the 1999 and 2001 growing seasons: a seed treatment with imidacloprid and the use of NAS-resistant cultivars. Seed treatment at the rate of 80 g a. i. imidacloprid /kg seed protected lettuce plants until 3 weeks after planting; 1 extra treatment with lambda-cyhalothin + pirimicarb at 7,5 + 150 g a. i./ha provided complete control until harvest. In the NAS-resistant lettuce cultivars, the levels of resistance were not sufficiently high to obviate the need for insecticides.

Key words: aphids, lettuce, host plant resistance, seed pelleting

Introduction

Leaf aphids cause serious problems in lettuce crops. Infested plants often show deformation and head rot. This decreases the percentage of marketable heads and may result in great financial losses for lettuce growers. Furthermore, aphids transmit virus diseases and cause reduced or abnormal growth. Lettuce (Lactuca sativa L) is a suitable host for many aphids species (Blackman & Eastop, 1984). However, a survey carried out under the auspices of the International Organisation of Biological Control (IOBC) in outdoor lettuce during two years at 11 sites in six European countries (Czechoslovakia (1), England (1), France (2), Germany (1), The Netherlands (4) and Switserland (2)) showed that only three species predominated: the lettuce root aphid (Pemphigus bursarius L), the lettuce aphid (Nasonovia ribisnigri Mosley) and the potato aphid (Macrosiphum euphorbiae Thomas). In the Netherlands, Uroleucon sonchi L was also frequently found in high numbers on lettuce (Reininck & Dieleman, 1993). In Belgium, no data about aphid species are available. With the aim to develop supervised control programs in the future, a survey of aphid species on butterhead an iceberg lettuce was carried out in 1998 en 1999. Lettuce growers frequently apply insecticides to avoid damage in periods favourable to development of aphids. Frequent spraying is detrimental to the quality of the product and undesirable for the environment. Sprayings also increase production costs. Even after

245 246

intensive crop treatments, heads are frequently reject at the auctions because of aphids contamination. Host plant resistance and seed treatment with an insecticide may substantially reduce the amount of insecticides in lettuce production. These have the additional advantage of protecting the plants from the moment of sowing. Our objective was to compare the effects of seed pelleting with imidacloprid and resistant butterhead and iceberg lettuce cultivars on aphid populations in two field experiments during 1999 and 2001. Imidacloprid had a wide range of activity against many economically important insect pests such as aphids, whiteflies and trips. (Elbert at al., 1990).

Material and methods

Survey of aphid species A total of 13 experiments (7 in 1998 and 6 in 1999) were carried out to determine which aphid species are most important in Belgium on outdoor butterhead and iceberg lettuce. The experiments were done at the Vegetable Research Station at Sint-Katelijne-Waver. The plants were planted at different times during the year: spring, summer and autumn plantings. Each experiment consisted of 4 rows of 200 plants of the surveyed lettuce. Cultural methods were applied according to local practice with the exception of insecticides, which were not used. Cultivar, sowing, planting and harvestable date of the experiments are presented in table 1. A week before harvest, at harvest and a week after the harvest ten plants were lifted and the roots were evaluated for root aphids. At the laboratory the numbers of winged leaf aphids were counted and determined by peeling off the leaves.

Table 1. Cultivar, sowing, planting and harvestable date of the experiments

Experi- Cultivar Sowing date Planting date Harvestable date ments 1998 1999 1998 1999 1998 1999 1998 1999 Sprinter (butter) Sprinter 18 13 1 23 Feb 7 Apr 6 May 25 May Sesam (iceberg) (butter) March March Sunny 23 2 Sunny (butter) 14 Apr 16 Apr 4 May 26 May 15 June (butter) March Newton (butter) 3 Libuta (butter) 10 Apr 17 May 5 May 3 June 9 June 13 July Roxette (iceberg) Newton (butter) Libusa 4 15 May 18 June 4 June 7 July 14 July 17 Aug Roxette (iceberg) (butter) Newton (butter) 5 Libusa (butter) 15 June 15 July 2 July 4 Aug 4 Aug 14 Sept Roxette (iceberg) Newton (butter) Plenty 6 15 July 18 Aug 30 July 2 Sept 15 Sep 19 Oct Roxette(iceberg) (butter) Plenty 7 21 Aug 9 Sept 20 Oct (butter)

247

Control strategies Two field trials were carried out in 1999 and 2001. In 1999, the seeds were sown on 15 July and the seedlings were planted out on 4 August and harvested on 14 September. In 2001, the seed was sown on 23 July and the seedlings were planted out on 7 August and harvest on 18 September. The experiments were done with susceptible and resistant butterhead and iceberg lettuce cultivars and lettuce of which the seed was treated with imidacloprid at 80 or 120 g.a.i./ kg seed. Each experiment was a randomised complete black design, consisted of 9 (1999) and 8 (2001) objects, each replicated three times. The different objects are presented in table 2. Each plot consisted of 60 plants of 30 x 30 cm planting distance. Cultural methods were applied according to local practice, foliar sprayings with insecticides were not done, except in the trial of 2001: the plants of object 5 (seed treatment with imidacloprid 80 g.a.i./ kg seed) were sprayed on 3 September with lambda-cyhalothrin + pirimicarb. Every week, from planting on, the numbers of leaf aphids (both alate and apterous) on 6 plants were counted in the laboratory by peeling off the leaves. At planting, 2, 3 and 5 weeks after planting the amount of imidacloprid in the lettuce plants was assessed by Fytolab, Technologiepark, RUG, 3, GENT.

Table 2. Objects of the two experiments of 1999 and 2001

Object 1999 2001 untreated butterhead lettuce untreated butterhead lettuce 1 cv. Newton cv. Remus untreated iceberg lettuce seed treatment 80 g.a.i./ kg seed 2 cv. Roxette cv. Remus seed treatment 80 g.a.i./ kg seed seed treatment 120 g.a.i./ kg seed 3 cv. Newton cv. Remus seed treatment 80 g.a.i./ kg seed untreated butterhead lettuce 4 cv. Roxette cv. Nadine Resistant butterhead lettuce seed treatment 80 g.a.i./ kg seed 5 cv. LM9130 cv. Nadine Resistant butterhead lettuce resistant iceberg lettuce 6 cv. LM9131 cv. Fortunas resistant iceberg lettuce and seed treatment 80 Resistant butterhead lettuce 7 g.a.i./kg seed cv. LM9136 cv. Fortunas Resistant iceberg lettuce resistant Batavia-lettuce 8 cv. Vetonas cv. Elenas Resistant iceberg lettuce 9 cv. Fortunas

Results and discussion

The results from the 13 experiments carried out in 1998 and 1999 are presented in table 3 and 4. The spring and autumn experiments were heavily infestated. Most summer and the two late autumn experiments had low infestation levels. These tables show clearly that N. ribisnigri and M. euphorbiae were the most common aphid species on butterhead and iceberg lettuce. Myzus spp. and Aulacorthum solani were found in low frequencies, less then 1 species/plant. 248

Uroleucon sonchi seems to be a Dutch problem: this species did not occur in our experiments. Pemphigus bursarius was also absent in these experiments.

Table 3: Mean number of alate aphids observed in the experiments of 1998

Species N. ribisnigri M. euphorbiae Aulacorthum Myzus spp. Experi- Date Cultivar solani ment mean % mean % mean % mean % no. no. no. no. (n=10) (n=10) (n=10) (n=10) 28/4 Sprinter 0,4 40 0,2 20 0,2 20 0,2 20 Sesam 0,2 50 0,2 50 5/5 Sprinter 1 50 0,8 40 0,2 10 1 Sesam 0,8 58 0,4 28 0,2 14 12/5 Sprinter 5,8 72,5 2,2 27,5 Sesam 13,2 66 6,6 33 0,2 1 19/5 Sunny 10,4 84 2 16 2 26/5 Sunny 45,6 92 3,8 8 2/6 Sunny 50,2 99 0,4 1 2/6 Libuta 3,2 84 0,6 16 3 9/6 Libuta 4,8 86 0,4 7 0,4 7 16/6 Libuta 13,8 96 0,6 4 7/7 Newton 11,2 98 0,2 2 Roxette 1,2 100 4 14/7 Newton 0,2 50 0,2 50 Roxette 3,4 100 22/7 Newton 0,6 75 0,2 25 Roxette 2 100 28/7 Libusa 0,8 80 0,2 20 5 4/8 Libusa 0,4 50 0,4 50 11/8 Libusa 0,2 100 8/9 Newton 6,6 100 Roxette 0,6 100 6 15/9 Newton 14,4 91 0,8 5 0,6 4 Roxette 0,2 33 0,2 33 0,2 33 22/9 Newton 61,8 87 6,2 9 2,6 4 Roxette 8,8 64 4,8 36 13/10 Plenty 0,6 60 0,4 40 7 20/10 Plenty 0,2 33 0,4 66 27/10 Plenty 0,4 50 0,4 50 249

Table 4: Number of alate aphids observed in the experiments of 1999

Species

N. ribisnigri M. euphorbiae Aulacorthum Myzus spp. Experi- Date Cultivar solani ment mean % mean % mean % mean % no. no. no. no. (n=10) (n=10) (n=10) (n=10) 18/5 Sprinter 2,4 24 6,8 70 0,2 2 0,4 4

25/5 Sprinter 38,8 69 17,6 31 1 2/6 Sprinter 50,4 63 28,4 37

8/6 Sunny 8,8 78 2,4 21 0,2 1

15/6 Sunny 6,8 92 0,6 8 2 22/6 Sunny 4,4 83 1,2 17

6/7 Newton 2,6 100 Roxette 1 100 3 13/7 Newton 0,6 60 0,4 40 Roxette 0,2 100 20/7 Newton 2 90 0,2 10 Roxette 0,2 100 10/8 Libusa 0,1 100

17/8 Libusa 0,4 66 0,2 33 4 24/8 Libusa 1 100

7/9 Newton 3,4 100 Roxette 4,6 96 0,2 4 5 14/9 Newton 16,6 86 2,6 14 Roxette 7,4 90 0,8 10 21/9 Newton 9,4 61 4,2 23 2,6 16 Roxette 6,4 66 3,8 34 12/10 Plenty 0,2 50 0,2 50

19/10 Plenty 0,2 25 0,4 50 0,2 25 6 26/10 Plenty 0,6 30 0,6 30 0,8 40

250

The results concerning the recovered amount of imidacloprid at planting date (13 August), 1, 2 and 3 weeks after planting and the weight of lettuce plants are presented in table 5.

Table 5: Mean weight and amount of imidacloprid recovered in the lettuce plants after seed pelleting.

Dose Cultivar Mean weight (n=20) Residu (ppm) g.a.i./kg seed 13/8 20/8 27/8 3/9 13/8 20/8 27/8 3/9 10/9 Remus 80 4,9 16,41 69,9 201,6 0,32 0,20 ------Remus 120 3,7 14,11 61,05 180,9 0,66 0,76 ------Nadine 80 3,4 15,49 50,88 158,6 0,69 0,20 0,06 0,05 --- Fortunas 80 3,9 13,82 60,2 194,4 0,47 0,16 ------

These results show that two weeks after planting few imidacloprid was recovered in the lettuce plants even when 80 or 120 g.a.i. kg/seed were applied. This can be explained by the fact that the volume of the lettuce plants strongly increased from two weeks after planting. The number of aphids also increase from 3-4 weeks after planting. The results from the experiment of 1999 and 2001 are presented respectively in table 6 and 7. The aphid populations in the untreated plots quickly colonised the plants and began rapid growth about two weeks after planting. Thereafter, population densities continued to increase until harvestable date. More than 200 aphids were count at the end of the culture. There was a difference in aphid colonisation in these experiments between the Nas-resistent and the susceptible cultivars short after planting. Aphids in the plots with Nas-resistant cultivars did not begin rapid population growth until 3 weeks after planting. Only few M. euphorbiae were found the first weeks after planting. The levels of resistance at the tested butterhead and iceberg lettuce were in these experiments not sufficiently high to obriate the need for insecticides. At harvestable date, there was no difference between the numbers of aphids on the susceptible and Nas-resistant lettuce cultivars. On the other hand, these experiments clearly show that with Nas-resistant lettuce cultivars it may be possible to reduce the number of sprayings with insecticides. Generally, in regular lettuce growing in Belgium the number of insecticide applications on lettuce ranges from about 4 to 6. The use of the resistant cultivars will depend on the suitability of these cultivars for the growers and the consumers. For instance, the resistant butterhead cultivar Dynamite is not appreciated by the growers at this moment. Three weeks after planting 2 to 5 aphids were found on the lettuce in the seed treated plots with imidacloprid. There was no effect between the 2 doses: 80 or 120 g.a.i/plant. From four weeks on, aphids colonisation begins and at harvestable date there was no differences in number of aphids on the treated and untreated lettuce plants. Imidacloprid seed pelleting does not provide complete control throughout the full lettuce crop. At least 1 or 2 insecticide applications of an are necessary at the end of the growing seasons. However, in the experiment of 2001, one insecticide application with lambda-cyhalothrin + pirimicarb clearly reduced the number of aphids at harvest. The mean numbers of aphids per plant were consistently low throughout the season (table 7) in the plots with the Nas-resistant iceberg cultivar Fortunas and seed treatment with imidacloprid. Differences in head size and weight were not observed in the two field experiments. In the plots with one insecticide application of lambda-cyhalothrin + piricarb, the lettuce was 251

free of aphid infestation at harvest and all plants were marketable. In Belgium, auctions refuse a lettuce plant with five or more aphids.

Table 6: Mean number of aphids per lettuce plant on ten dates at the experiment of 1999

Date Object Aphids 10/8 17/8 24/8 31/8 7/9 14/9 21/9 28/9 5/10 12/10 Untrated apterous 8 13 29,2 44,4 >20 91,4 67,6 124 >200 >200 cv. Newton alate 0,4 0,2 0,2 0,5 2 4,5 2 3,4 19 Untrated apterous 2,2 7,4 18,4 17,4 88,8 36 78 >200 >200 >200 cv. Roxette alate 0,1 0,5 0,5 0,5 7,5 4,7 8 Imidacloprid apterous 0,4 2,4 3,2 10,2 8,4 >200 131 67 68 cv. Newton alate 0,2 0,2 0,8 9,6 12,2 5,2 8,6 Imidacloprid apterous 1,6 5,2 15,6 11,8 84,6 >200 >200 >200 cv. Roxette alate 0,2 0,2 0,8 35,2 6,2 5,4 Resistant apterous 0,2 1,4 8,4 10,2 13,8 25 65 156,5 >200 >200 cv. LM9130 alate 0,1 0,2 0,2 1,2 0,2 7,4 6,6 9,6 Resistant apterous 0,8 4,6 15,4 18 20,4 17,8 35,8 64 >200 >200 cv. LM9132 alate 0,2 0,4 Resistant apterous 1,8 2,4 4,6 14,4 21,4 24 114 >200 >200 >200 cv. LM9136 alate 0,2 0,2 0,1 0,5 23,6 16 3,1 Resistant apterous 1,6 2,5 10,2 9,4 15,4 20,4 47,2 104,4 37 21 cv. Vetonas alate 0,2 0,2 0,2 0,6 0,6 0,5 2 Resistant apterous 1,4 1,6 6,4 11,4 20,8 32 78 128,6 48,7 21 cv. Fortunas alate 0,3 0,2 0,2 6,8 3,6 4

Table 7: Mean number of aphids per lettuce plant on eight dates at the experiment of 2001

Date Object Aphids 13/8 20/8 27/8 3/9 10/9 17/9 24/9 1/10 Untrated Apterous 3,3 16,1 40,4 >100 >200 >200 >200 cv. Remus Alate 0,1 1,4 2,8 3,2 8,4 49,2 Imidacloprid (80 g.a.i) Apterous 0,2 19,4 48,4 180,6 >200 cv. Remus Alate 0,1 0,9 2,6 13,4 Imidacloprid (120 g.a.i.) Apterous 5,3 11,2 15,4 68,3 26,4 cv. Remus Alate 0,1 0,2 0,6 0,6 2,4 Untreated Apterous 2,4 14,4 28,6 >100 >200 >200 >200 cv. Nadine Alate 0,1 0,1 0,2 3,2 4,8 34,7 Imidacloprid (80 g.a.i.) Apterous 0,4 1,2 4,6 12,8 cv. Nadine (1) Alate 0,1 Resistant Apterous 2,4 24,4 21,2 164,2 >200 cv. Fortunas Alate 1,4 0,5 10,6 Resistant + Imidacloprid Apterous 4,3 2,4 25,4 cv. Fortunas Alate 1,8 Resistant Apterous 3,5 45,6 23,4 43,6 >200 cv. Elenas Alate 0,1 0,2 0,2 6,2 (1) Treatment with lambda-cyhalothrin + pirimicarb on 3 september 252

Conclusions

N. ribisnigri (Mosley) in the most common leaf aphid species, followed by M. euphorbiae (Thomas) in Belgium. Resistant cultivars and seed treatment with imidacloprid may provide a more suitable and practical approach to aphid management on lettuce than is currently available with foliar insecticides. In addition, the use of resistant cultivars and pelleted seeds reduced in the amount of insecticides necessary to control and control aphids directly from sowing and a reduce the risk of starting control measures to late.

Acknowledgements

We thank the Belgian Ministry of Agriculture, Traders and Small Enterprises Administration for Research and Development for supporting this research project.

Résumé

Evaluation des Pucerons en Culture Exterieure de la Laitue et Strategies pour leur Controle La laitue est sensible aux attaques des pucerons durant toute la période de production, depuis avril jusqu’ à la moitié d’ octobre. Des observations périodiques faites durant les saisons de culture de laitues en extérieur de 1998 et 1999 ont permis d’ identifier toutes les espèces de pucerons se nourrissant sur la laitue dans la région de Flandres. Durant les deux années, Nasonovia ribisnigri (Mosley) a été l’ espèce de puceron la plus répandue, suivie par Macrosiphum euphorbiae (Thomas). Myzus persicae (Sulzer) et Aulacorthum solani (Kalt.) ont également été observées, mais sont d’ une importance mineure. Le puceron des racines Pemphigus bursarius (L.) n’ a pas été observé. Les pucerons en laitue sont généralement contrôlés par des applications en routine d’ insecticides organosphorés, carbamates ou pyréthroïdes. Toutefois, le contrôle des pucerons peut poser de plus en plus de problèmes, suite au nombre décroissant d’insecticides agréés, et suite au développement de résistances par les pucerons. En outre, les applications répétéés d’ insecticides sont fortement critiquées par les consommateurs et les enviromentalistes. Pour ces raisons, deux techniques alternatives de lutte ont été essayées durant les saisons de culture de 1999 et 2001: un traitement des semences par l’imidacloprid et l’utilisation de variétés dont le feuillage est résistant aux pucerons. Le traitemnt des semences par 80 g d’ imidacloprid par kg de semence protège les laitues durant les 3 semaines qui suivent la plantation. Un traitement supplémentaire par lambda- cyhalothrin + pirimicarb à 150 + 7,5 g de m.a./ ha donne une protection complète jusqu à la récolte. Concernant les variétés résistantes aux pucerons, les niveaux de résistances ne sont pas suffisamment élevés que pour supprimer le besoin d’ insecticides. L’ utilisation de varietés résistantes dépendra de ce que celles- ci conviennent aux cultivateurs et aux consommateurs. Par exemple, la variété résistante « butterhead » Dynamite n’ est pas appréciée actuellement par les cultivateurs.

References

Blackman, R.L. and Eastop, V.F., 1984. Aphids on the World’s Crops: An Identification Guide. Chickester, U.K.: John Wiley & Sons: 115-117. Elbert, A., Overbeck, H., Iwaya, H. and Tsuboi, S. 1990. Imidacloprid, a novel systemic nitromethylene analogue insecticide for crop protection. Proceedings, Brighton Crop Protection Conference, Pests and Diseases, Brighton, England: 21-28. Reinick, K. and Dieleman, F.L. 1993. Survey of aphid species on lettuce. IOBC wprs Bulletin 16 (05): 56-68 Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 253-258

Evaluation of 9 years supervised carrot fly control in the Netherlands

M. Loosjes De Groene Vlieg b.v., Duivenwaardsedijk 1, 3244 LG Nieuwe Tonge, The Netherlands

Abstract: Since supervised control of the carrot fly was carried out commercially in the Netherlands, it was observed that in the main region where this method was applied on a large scale, numbers of carrot flies increased in the course of years. Theoretically, supervised control will lead to an increase of fly numbers, until a certain level is reached. Analysis of second flight data showed no clear difference in control level between fields with seed coating and fields with supervised control as the first generation control method. Dispersal of flies does not seem to conceal possible differences. So both control strategies, second flight supervised control combined with either first generation seed coating or with first flight supervised control, result in control of carrot fly populations, also in the long run.

Key words: Carrot fly, Psila rosae, supervised control

Introduction

De Groene Vlieg (the Green Fly) is an independent company offering environmentally friendly pest control services to farmers. The main activities are: 1. application of the sterile insect technique against the onion fly Delia antiqua (2001: 3300 ha), 2. supervised control of the carrot fly Psila rosae (2001: 4000 ha), 3. research using the staphilinid beetle Aleochara bilineata as biological control agent against onion fly (2001: 40 ha) and 4. soil sampling for different species of nematodes, for certificates and cropping advices preventing soil disinfection (2001: 14000 ha). The effect of supervised control of the carrot fly on its population level in the course of years is evaluated, depending on the first generation control method. It has to be taken into account that the data were not obtained in a research project, but as spin off of commercial application of supervised control.

Materials and methods

Supervised control of the carrot fly in the Netherlands is carried out with a Goudval® (goldtrap). This is an orange-yellow (ICI 229) PMMA holder containing a polyester sheet coated with insect glue (Tanglefoot®), fixed at an inclination of 45º to an iron rod. It is constructed to permit easy adjustment of trap height to be just above the vegetation. The trap top is always pointing eastward. At each supervised carrot field, at least one group of four traps is placed at a site favourable to the flies. The sticky sheets are changed weekly, advices to spray with dimethoate are given next day. Supervised control is applied either during the second flight, or during both first and second flight. Farmers should only spray shortly after a spraying advice. Information about their real spraying behaviour was very limited and incomplete.

253 254

Farmers not using supervised control by de Groene Vlieg, generally use chlorfenvinfos coated seed as first generation control and spray blind during the second flight. Because our largest group of customers is situated in Flevoland, that region was chosen for a first analysis. In Flevoland, some 1500 – 2000 ha of carrots are grown, representing about 2 % of the local arable area. Only fly catches were used of fields with carrots, grown by conventional farmers. Moreover, the analysis was restricted to data from series of at least 9 catches in the weeks 30 – 40. Week 30 was chosen because the second flight never starts before this week. The end at week 40 was chosen because most farmers did not need any more supervision with the harvest approaching. The catch data were averaged per week. As relative size of the second flight was used the sum of these averages over the eleven weeks involved. No corrections were made for any effect of insecticide treatments on the catches. As this preliminary analysis indicated an increase in population in the course of years, data from all other regions were analysed similarly. The data were treated separately, as there are important differences between the regions, a.o. in number of customers per year, in their distribution over the control methods, and in frequency and method of carrot cropping.

Fig. 1. Carrot fly control in the region Flevoland: distribution of control methods applied in the first / second flight

Figure 1 shows the distribution of control methods in Flevoland. Control activities not mentioned, e.g. supervised control not carried out by de Groene Vlieg or soil treatment at sowing, are estimated at less than 5%. Fly catches are only available of fields under supervised control. During the first flight in 2000, temporary no insecticide was admitted for carrot fly control. Some of the farmers, using supervised control, may not have sprayed in that period. Several farmers must have had not-coated seed, planning to use supervised control. Surprised as they were by the temporal illegality of dimethoate, they may have applied not any first flight control at all. Such farmers are included in the category seed coating/supervised in fig.1.

Results and discussion

For the region Flevoland, second flight catches of fields with supervised control during the first flight were compared with those of seed coated fields (fig. 2). The general shape of the 255

second flight curve is independent of the first flight control method used. In 2001 more flies were caught after supervised control of the first flight than after seed coating.

Fig. 2. Second flight curves of the Carrot flies under supervised control, region Flevoland. Continuous line: first flight seed coating; dotted line: first flight supervised 256

Figure 3a shows the relative size of the second flight in the region Flevoland. After supervised control, the population increases from year to year. However, only in 2001 it clearly differs from the population level on seed coated fields. Theoretically, supervised control will lead to an increase in fly numbers, because no insecticide treatment is applied as long as fly catches remain below a certain threshold. With carrot flies, it is quite common that on a field this threshold is never reached during the whole growing season. In that situation populations may increase freely, until a level is reached at which control by one or more sprayings will keep the population theoretically at an equilibrium level. Of course in practice such a level will be rather variable.

Fig. 3. Relative size of the second flight. Continuous line: first flight seed coating; dotted line: first flight supervised; a: Region Flevoland, b/d: other regions. Dot size is in proportion th the square root of underlying trap group number; vertical scales are identical.

Figure 3 b/d shows the relative sizes of the second flight in three different regions, of which data were available of both seed coated fields and fields with the first flight supervised. Between the two control strategies no clear difference is found. Within each region, the fluctuations look rather similar, but the curves are not identical among the different regions. The causes of the fluctuations are not clear. The following cases of population increase can be due to actually no control in the first flight of 2000: in figs. 3a and 3b in 2000 the fields supposed having had coated seed in the first flight, and in fig. 3b in 2001 the fields under supervised control. 257

Fig. 4. Relative size of the second flight; dots and scales as in Fig. 3. a: first flight supervised control in 2 regions where the strategy dominates; n 0 11-47; b: first generation seed coating in 6 regions where that strategy dominates, n = 10-69

Figure 4 a/b shows the relative sizes of the second flight in regions where one first generation control strategy dominates. Again, there is no indication that one control strategy has a better effect than the other. In both cases, high population levels can be reduced. The variations in second flight population levels in the course of years do not suggest a general equilibrium range. Other information indicates that higher population levels may be related to more common carrot cropping. Dispersal might conceal any difference between the two control strategies, so one could suppose it to be the cause of the similarity of fluctuations per region in fig. 3. In spring, at the start of the first flight, there is necessarily dispersal to the new carrot fields. Often this will cause an exchange between populations under different first generation control treatments. The same effect will occur when farmers change their control method, which is more common than can be concluded from fig. 1. So in all regions there will be some exchange between populations under different control treatments. However, this dispersal takes place before the effect on the first generation of either seed coating or supervised control. Independent of such dispersal, any difference between these two control methods would become clear in the second flight on these fields. Only a considerable dispersal of emerging second flight flies would be able to conceal a difference in effect between the first flight control methods. Now, in a group of neighbouring biological growers, some carrot fields had very high numbers of flies trapped during both flights. On some other fields of these growers, at less than one to two kilometres distance, the numbers of flies remained low in the second flight also. This indicates that emerging second flight flies do not disperse in relevant numbers. So dispersal does not seem to conceal any difference that might exist between the first flight control methods. In conclusion, the difference between the control strategies as observed in Flevoland, fig. 3a, is not supported by other data. It can be assumed that both control strategies, second flight supervised control combined with either seed coating or supervised control against the first generation, result in control of carrot fly populations, also in the long run. A considerable part of the spraying advices was given after mid September (fig.5). Dimethoate is now the only chemical allowed for carrot fly control in the Netherlands. It is not certain whether in the near future it will be allowed after mid September. In that case, the farmers would be without any control measure during a risky part of their cropping period.

258

Fig. 5. Cumulative frequencies of advices for spraying, per week, averaged over 1995-2001, n = 373-1687.

Acknowledgements

I gratefully acknowledge the discussions with Tjarda Everaarts, her critical comments on the manuscript and her presentation at Krakow.

259

Integrated Pest Management

260

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 259-264

Economies in transition and integrated pest management on vegetables: The case studies in Poland

Z.T. Dąbrowski1 & K. Wiech2 1 Department of Applied Entomology, Warsaw Agricultural University, Nowoursynowska 166, 02-787 Warsaw, Poland 2 Department of Plant Protection, Kraków Agricultural University, 29 Listopada 54, 31-425 Cracow, Poland

Abstract: The political and economic changes implemented during the last twelve years in central and eastern European countries (including Poland) has significantly affected both research and practice of plant protection of horticultural and agricultural crops. In the meantime the concept of Integrated Pest Management as the intelligent pesticide management has evolved into the ecologically based pest management. The Integrated Pest Management (IPM) is the core of the integrated management of vegetable crops with the objective to produce healthy crop. Because of the low average use of pesticides in Poland (0.6 - 0.7 kg a.c./ha) and mineral fertilisers in comparison to the EU countries, the Polish authorities should explore this unique opportunity and support a wide implementation of IPM on vegetables by involving all stakeholders in participatory approach: producer groups, commerce and industry, researchers, extensionists, governmental agencies and parliament. The concept and priority of such programmes in Poland should be the yield increase in regard to quality and quantity, however avoiding pesticide dependency as a pre-condition for this sustainable intensification of vegetable production. Only wide implementation of integrated production systems by vegetable farmers would allow them to meet international standards on product quality. The role of the National Committee on Science and Research (KBN) and the private sector in supporting integrated crop and pest management is emphasised.

Key words: Integrated crop management, integrated pest management, participatory approach, vegetables, sustainable agriculture

Introduction

There is a common belief among farmers that vegetables like other horticulture crops have to be grown under high input production systems, which will guarantee high yields and quality of their products. Unfortunately, as a rule, intensification of their production has led to a reduction of rotation in the specialised farms, frequent usage of higher doses of synthetic fertilisers and intensive application of a variety of pesticides. These practices have led to negative externalities associated with such systems including: direct public health risks, the destruction of natural enemies and emergence of secondary pests, the development of pesticide resistance, increasing soil and water contamination and other environmental liabilities. Vegetable crops grown under protection or open field in addition to orchards and ornamental plants became the benchmark for these environmental negative impacts. Two different strategies has been proposed to reduce the negative health and environmental externalities created by the high input production systems: the organic farming and integrated crop management. The previously neglected organic (ecological) production systems considered to be a hobby of a small group of producers has gained more public

259 260

attention, first from pro-ecological groups, later from a wider part of the society and finally from researchers. The presently growing demand for pro-ecological products attracted attention of large commercial enterprises in addition to small specialised shops offering organic farming products in a number of the European Union countries. However, the present experience with marketing organic products in Poland shows that there are some constraints and the organic production of vegetables does not secure the economic sustainability of farmers. Therefore it is our conviction that the integrated crop management may link the public demand for better quality products with guaranteeing the economic sustainability of vegetable farmers. The integrated pest management (IPM) is the core of the integrated management of vegetable crops with the objective to produce healthy crop. The concept of IPM has been developed by scientists since the middle of 60-ties, but only recently has been successfully implemented by farmers in a number of countries. The field studies and observations carried out in the 80-ties in the USA and the EU countries have clearly showed that developing IPM recommendations by researchers does not mean that they will be accepted and implement by farmers on a wider scale (Wearing 1988). It has also been identified that the methodology of its implementation in practice is as important as the development of its scientific content.

Lessons learnt from slow adoption of IPM in the past

In spite of attractive and solid theoretical bases of IPM programmes prepared by research institutions since the70-ties their adoption by farmers was slow and unsatisfactory in both developed and developing countries. Based on the authors’ personal experience in developing IPM technologies in Poland and in the international programmes as well as literature review, the following factors may affect common acceptance of IPM tactics and strategies by farmers: * it must be recognised that the implementation of IPM strategies and tactics is more difficult than using traditional methods based exclusively on chemical pest control, therefore fundamental changes are needed in the relations between researchers-farmers- extensionists and politicians; * selection of priorities in developing IPM programmes should be based on the real needs of farmers and socio-economic parameters of farms; * a participatory approach and the main role of a farmer („Farmer first approach”) must be recognised in developing and implementation of an IPM programme according to the principles of the Agriculture Knowledge and Information System; * necessity of replacing present model of mass training of farmers in classrooms into smaller education groups using active participation of farmers and informal education methods under field conditions in implementation of IPM principles; * stronger role and influence of farmer production groups and co-operatives practising IPM on marketing and governmental regulations. Only in the 80-ties was it realised with the help of social scientists that IPM as a knowledge-intensive approach requires strong and innovative education and training components, and technology-generating (research) backup oriented to meet farmers’ needs. Many authors emphasised that IPM is not a technology and is therefore, not something that can be transferred using conventional approaches. Instead, it is a process ideally catalysed and supported by extensionists and researchers - that engages farmers in experimental learning and dynamic local research that continuously reshapes solutions to their problems of the moment (Dąbrowski 1999, 2000). The fundamental message is that IPM is implemented by farmers. Researchers and extension agents provide the essential support to the IPM enterprise,

261

usually through training or technology development projects. Successful IPM programmes involve a continuous and dynamic interaction of farmer-trainer initiative and research response. The recently developed concept of Agriculture Knowledge and Information Systems gives methodological guidance to involve all stakeholders in the development and implementation of new technologies (Drygas et al. 1996, Dąbrowski 2000).

Factors responsible for the successful implementation of IPM programmes in Poland

The critical analysis of factors responsible for the development and implementation of two successful IPM programmes introduced recently in Poland should be used as a model to provide guidance for other vegetable crops. One programme has been introduced for carrot grown under open field conditions and the other for cucumber and tomato grown under protection. The research activities forming the base of both programmes started in the70-ties and implementation on a large scale in the 90-ties. The methodology used in developing IPM strategy and tactics for the carrot fly, Psila rosae (Fabr.) is presently defined as an holistic approach. Their implementation as a common practice was only made possible by the demand by the large food processing industry, e.g. Alima Gerber (Rzeszów) and Nutricia Ovita (Opole). The IPM programme includes the following recommendations: selection of fields non-preferable for the oviposition by the fly females; seed coating with degradable insecticides; planting of less preferable cultivars and supervised chemical treatment with insecticides (Dąbrowski and Legutowska 1976a, b). Pest monitoring is being used to determine the incidence and timing of carrot fly activity and to target chemical treatments more accurately. Altogether about 20% of the carrot growers practice carrot fly monitoring and use sticky traps covering 15,000 - 20,000 ha/year. Participation of the Polish researchers in international projects on integrated control of the carrot fly has allowed to build the IPM recommendation parallel to current achievements in other European countries (Ellis and Ester 1999, Finch et al. 1999). Alima Gerber contracts approx. 10 000t of carrots annually from 70 farmers. The company extension officers have trained farmers and the governmental extension inspectors in the integrated crop production and monitoring of the carrot fly appearance. Residues of nitrites, cadmium and pesticides in carrot roots are regularly monitored. The company is also processing other vegetables as: potatoes, celery, parsley (including leaves), chive, celery and broccoli. The protocol for product quality and safety for consumers is the same as for carrots. Nutricia Ovita (Opole) process 2 500t of carrot annually for juice and has the same high requirements for quality as Alima Gerber. Some blocks of IPM programmes on cabbage and Brussels sprouts have been proposed to farmers by the Research Institute of Vegetable Crops and other vegetable crops by an interdyscyplinary team from the Cracow Agricultural University (PHARE 1995). Our meetings with farmers have indicated that there it is necessary to develop appropriate methods allowing them to optimise pesticide use on the following crops: green peas, broad bean and especially field tomatoes used for processing. The second successful IPM programme on protected vegetables has been implemented efficiently by all large greenhouse enterprises (previously government owned) manages by well trained and experienced managers. They had access to bank loans and advanced greenhouse technologies. Private advisers of the Polish distributors of natural enemies (ROLEKO and BIO PARTNER) provide them and the governmental extension service with information on the newest production techniques. They do not restrict their obligation to sell and

262

distribute required species of predators, parasitoids and bumble bees to producers. Their agents respond immediately to any new plant health problems occurring in the enterprise. The practical IPM programme on protected vegetables has been developed in Poland by researchers through close and regular exchange of information, workshops and joint project with leading research institutions in the EU countries. The expert system developed recently by the inter-institutional team of researchers from the Research Institute of Vegetable Crops (Skierniewice) and the Warsaw Agricultural University (Warsaw) offers information on the integrated production and protection of tomato crops grown under protection (Nawrocka et al. 2000). However, the introduction of new techniques (including biological control agents) by small sale farmers is slow and unsatisfactory. There are objective and relative factors hampering the introduction of IPM into these small family enterprises (mostly plastic-covered tunnels). Unfortunately, researchers did not yet develop a satisfactory IPM programme for this group of farmers using mostly low input technologies because of their limited financial resources. A diminishing number of specialised horticulture extensionists in the regional extension service and the low budget allocated by the government for their activities restricts their role as facilitators of information on new recommended cultivars and pesticides obtained from seed and pesticide private companies. The same problems are faced by the majority of small scale farmers growing vegetables under open field conditions.

Participatory approach in the IPM development and implementation

The comparison of both programmes with other attempts to introduce IPM strategies on other vegetable crops in Poland shows that in order to implement integrated pest management, effective and practical strategies should be available for the diversified farmer’s community in Poland. The strategies should fit to the target group needs. Particularly in the first decades of IPM concept development, research institutions were given the task to develop IPM packages that were brought to the farmer through the extension service. Experience from Poland and many countries in the region shows that this approach was not very effective. The development of the package often takes a long time because of the human tendency first to develop „the optimal package” before it is given to the farmer. Another serious drawback of this approach is that the package in the end may not meet the farmer’s needs. There is no „ideal farmer” who will implement „the package” (Schulten 1994, Dąbrowski 2000). The farming community consists of a large number of individuals who all have their specific problems in producing a healthy crop and making their living. In developing IPM for vegetables, a holistic approach should be used with due attention to production and protection in various regions. IPM development should be done in close collaboration with farmers. Their needs should be well known and appropriate recommendation be available (Dąbrowski 1997, Wiech 2000). Research activities need to be constantly monitored for their appropriateness in solving farmers’ problems (Szwejda 2001). The present preference for small disciplinary orientated sub-projects does not stimulate the development of IPM programmes in Poland nor in the rest of the region. The necessity of changes in identification of research priorities for IPM development and application of studies on single pest/crop relations to large on-farm multi-institutional and multidisciplinary research and development projects should be considered by the National Committee for Research and Science. Some approaches previously used in the development of the holistic IPM programmes (e.g. for carrot crops) should be used more widely for other crops. Recent changes in the financing of multi-institutional IPM projects in the USA and some EU

263

countries should serve as examples to generate farmer-orientated research according to the recommendation of the Agenda 21, chapter 14 - Promoting sustainable agriculture and rural development. The present weak and mainly unofficial problem solving co-operation between scientists representing agricultural education, extension, institutional building and communication and plant protection in Poland delays the implementation of the newest methods and techniques in the technical and social disciplines. The importance of the participatory approach as the base of the Agriculture Knowledge and Information System in the IPM implementation in Poland should be put into practice.

References

Bednarek A. & Goszczyński W. 1997. [The actual state and perspective of integrated and biological plant protection in greenhouses]. Prog. Plant Protection/Post.Ochr. Roślin 37 (1): 123-130 (in Polish with English summary). Dąbrowski Z.T. 1997. Integrated Pest Management in Vegetables, Wheat and Cotton in the Sudan: A Participatory Approach. The ICIPE Science Press, Nairobi, Kenya. Dąbrowski Z.T. 1999. [The importance of partnership relations in developing and implementation of IPM programmes]. Prog. Plant Protection/Post. Ochr. Roślin 39 (1): 190-200 (in Polish with English summary). Dąbrowski Z.T. 2000. [The necessity of changes in the methodology of development and implementation of integrated pest management]. Prog. Plant Protection/Post. Ochr. Roślin 40 (1): 334-342 (in Polish with English summary). Dąbrowski Z.T. & Legutowska H. 1976a. [Basis of integrated control of carrot fly (Psila rosae F.)]. Mater. XVI Sesji Naukowej Instytutu Ochrony Roślin, Poznań: 201-219 (in Polish with English summary). Dąbrowski Z.T. & Legutowska H. 1976b. [The effect of field location and cultural practices on the occurrance of the carrot fly (Psila rosae F.)]. Wiadomości Ekologiczne 22 (3): 265-277 (in Polish with English summary). Drygas M., Duczkowska-Małysz K. & Wiatrak A.P. 1996. Agricultural Extension as a Link of the Agricultural Knowledge System in the Process of Modernizing Rural Areas and Agriculture in the Integration Process with the European Union. Centrum Doradztwa i Edukacji w Rolnictwie, Poznań. Ellis P.R. & Ester A. 1999. Possible reasons for the decline in carrot fly (Psila rosae (F.)) infestation in western Europe. IOBC wprs Bulletin 22 (5): 83-87. Finch S., Freuler J. & Collier R.H. 1999. Monitoring Populations of the carrot fly Psila rosae. International Organization for Biological Control of Noxious Animals and Plants, West Palearctic Regional Section, Dijon, France. Nawrocka B., Kropczyńska D., Owczarek-Wysocka M. & Derda M. 2000. [A decision support system for protection and production of greenhouse tomato]. Prog.Plant Protection/ Post.Ochr.Roślin 40 (2): 973-976 (in Polish with English summary). PHARE 1995. [Integrated System of Vegetable Production]. Fundacja Programów Pomocy dla Rolnictwa – Regionalny Ośrodek w Rzeszowie. Małopolskie Stowarzyszenie Doradztwa Rolniczego z s. w Akademii Rolniczej w Krakowie. Kraków (in Polish). Schulten G.G.M. 1994. The need for integrated pest management and its implementation. In: Integrated Vegetable Crop Management in the Sudan. Z.T. Dąbrowski (ed.), The ICIPE Science Press, Nairobi, Kenya: 20-23.

264

Szwejda J. 2001. [Estimation of the present threat of field vegetable crops by pests]. Mater. Ogólnokrajowej Konferencji „Szkodniki, Choroby i Chwasty w Warzywach Polowych”, Instytut Warzywnictwa, Skierniewice, 2nd August 2001: 5-15. Wearing C.H. 1988. Evaluating the IPM implementation process. Ann. Rev. Entomol. 33: 17- 38. Wiech K. 2000. [Integrated crop production and its chances for development]. Wieś i Doradztwo. Special Issue: Gospodarka Zasobami Przyrody w Polsce w Aspekcie Integracji z Unią Europejską, 2 (22): 1-4. Foundation of Assistance Programmes for Agriculture (in Polish).

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 265-270

The influence of cabbage whitefly (Aleyrodes proletella L., Aleyrodidae) abundance on the yield of Brussels sprouts

S. Trdan, Š. Modic & A. Bobnar University of Ljubljana, Biotechnical Faculty, Agronomy Department, Institute of Phytomedicine, Jamnikarjeva 101, SI – 1111 Ljubljana, Slovenia

Abstract: In 2000 a study on the bionomics of a cabbage whitefly (Aleyrodes proletella L.) was conducted. Various control methods against the pest were tested in order to find the most adequate way of its control. In the field block experiment on Brussels sprouts the efficacy of the systemic insecticide Confidor SL 200 (imidacloprid), the contact insecticide Actellic–50 (pirimiphos-methyl) and the yellow sticky boards were tested. The problem was how to plan a systematic pest control in comparison to a treatment where no agents were used. By using the yellow sticky boards it was noticed, that in the continental part of Slovenia the highest number of the cabbage whitefly is found from the second decade of September to the second decade of October. Spraying with Actellic-50 was established as the most effective way of pest (A. proletella L.) control. When comparing other treatments, no statistically significant differences were determined. Therefore the assumption about effectiveness of the yellow sticky boards in order to control the cabbage whitefly on the cultivated Brassica plants cannot be confirmed.

Key words: cabbage whitefly, Aleyrodes proletella, Brussels sprouts, control methods

Introduction

The cabbage whitefly (Aleyrodes proletella L.) is one of the most noticeable pests on the cultivated Brassica plants in Slovenia. Usually it is found on kale (Brassica oleracea L. convar. acephala (DC.) Alef. var. sabellica L.) and Brussels sprouts (B. oleracea L. convar. oleracea L. var. gemmifera DC.) while savoy cabbage (B. oleracea L. convar capitata (L.) Alef. var. sabauda L.) and cabbage (B. oleracea L. convar. capitata (L.) Alef. var. capitata L.) are less affected. In Slovenia it was first mentioned in 1961 under the name of Aleurodes brassicae Walk. (Janežič, 1961). In the mid nineties the scientific paper was written that exposed its bigger meaning in the last decade in our country (Gomboc and Celar, 1997). A larger economic importance is usually given to the bugs of the Eurydema genus, flea beetles (Phyllotreta spp.), cabbage aphid (Brevicoryne brassicae L.) and some other insects that are continually or periodically found on the cultivated Brassica plants. So far, the cabbage whitefly has been given less attention as it generally appears in the higher numbers only in the second part of the growing period. Besides, the attention has mostly been given to the indirect damage that is connected to the secretion of the whitefly honeydew, where the sooty moulds appear. As the result, the photosynthesis is less efficiant. Also, the aestetic view of yield loses some of its market value. Under such circumstances A. proletella L. has not been studied enough, either in Slovenia or in its neighboring countries. However, in the last years, the numbers of the insect have been increasing rapidly, therefore it was expected the whitefly to carry a direct impact on the yield amount as well. So, the bionomics of the A. proletella L. and the efficacy of various control methods were put to the test, in order to develop the most adequate method of pest control.

265 266

Materials and methods

The bionomics (life cycle and development) and the adequate control methods of the cabbage whitefly were studied in the Laboratory field of the Biotechnical Faculty in Ljubljana. This region had been chosen because the pest culminates in Ljubljana and its surroundings. On March 30 the coated seed of Brussels sprouts (B. oleracea L. convar. oleracea L. var. gemmifera DC.) cv. “boxer F1” were planted. They were chosen because in contrast to the kale (B. oleracea L. convar acephala (DC.) Alef. var. sabellica L.) the yield of Brussels sprouts is easier to evaluate. The seedlings grew in the greenhouse without any extra nourishment. After a month (May 03) the seedlings were transplanted in the open air in a black plastic mulch, under which a drop irrigation system was placed. The field experiment was organized in four blocks and each of them included four treatments. First, spraying with a systemic insecticide Confidor SL 200 (imidacloprid). Second, spraying with a contact insecticide Actellic-50 (pirimiphos-methyl). Third, placing the yellow sticky boards in order to reduce the pest intentionally. Fourth, no agents whatsoever were used. Each treatment was repeated once. 12 plants were planted on 3,2 m long and 1 m wide parcels (this surface was used for an individual treatment). The distance among the plants was 45 cm, and among the rows it was 75 cm. The plants were growing 20 cm away from the border of the parcel. Due to a heavy attack of the flea beetles (Phyllotreta spp.), on May 05 the seedlings were sprayed with the insecticide radotion E–50 (25 ml/10 l). Five days later, the limacide Mesurol granulat against slugs (Gastropoda) (40 g/100 m2) were used. On June 01 three sticky boards were placed on each parcel in the treatment of »yellow boards« and were changed in 10 to 14 days long intervals. On June 06 the weeds among the rows were sprayed with the herbicide Cidokor (70 ml/100 m2). The first spraying against cabbage whitefly took place approximately a month later (August 02). At each treatment both insecticides were used, each in 0,1% concentration (10 ml/10 l water). The same method was used on September 08. On October 05 Brussels sprouts was only sprayed (for the third time) with the contact insecticide. The preliminary tests were done on September 05 and September 29 on the efficacy of the control methods in the experiment. The leaves were chosen randomly and on the upper third of each plant the whitefly larvae were counted. On December 04 the yield of Brussels sprouts in various treatments of the experiment was estimated. For this purpose the heads of the plants were picked and weighted. Therefore, an average weight was established and by using of the Newman-Keuls multiple range test it was determined whether any statistically significant differences in the yield of the cultivated Brassica plants among the individual treatments appear.

Results

Testing the efficacy of various cabbage whitefly control methods on Brussels sprouts and the influence on the yield of the vegetable In both evaluations the lowest number of the cabbage whitefly larvae was found on the plants sprayed with Actellic–50. This number was statistically significantly lower than the number of the larvae found in the other three treatments, where the statistically significant differences in the number of larvae among the randomly chosen leaf in the upper third of the the plants in the other three treatments were not found (Table 1). The highest average yield per plant that also included a statistically significant difference from the yield in the other treatments was found on Brussels sprouts sprayed with the contact 267

insecticide Actellic–50. In the plants used in other treatments (the ones sprayed with systemic insecticide Confidor SL 200, the ones where yellow sticky boards were placed in order to reduce the number of the imogoes of A. proletella L., and the plants, that were not controlled by any agent), no differences in the average yield were found (Table 2).

Table 1: An average number of the cabbage whitefly larvae (Aleyrodes proletella L.) on a randomly chosen leaf and the homogenity of groups (counted with 95% probability using the Neuman-Keuls multiple range test) after two terms of evaluation

Date of evaluation Treatment Average number of Homogenity of larvae/ leaf groups Actellic-50 27.1 a September 05, 2000 Confidor SL 200 46.3 b Control 53.8 b Yellow boards 55.0 b Actellic-50 46.8 a September 29, 2000 Confidor SL 200 94.4 b Control 104.5 b Yellow boards 115.0 b

Table 2: An average yield of Brussels sprouts per plant and the homogenity of the treated groups (counted with 95% probability using the Newman–Keuls multiple range test) on December 04, 2000

Treatment Average Homogenity yield/plant of groups Actellic–50 780,4 g b Confidor SL 200 611,1 g a Control 625,1 g a Yellow boards 535,2 g a

Studying a part of the cabbage whitefly bionomics on Brussels sprouts with the yellow sticky boards The first imogoes of the cabbage whitefly were found on the lower side of the Brussels sprouts leaves by the visual examination on June 30. In the same period, the first flying forms were found on the yellow sticky boards. From that time on the number of the whiteflies caught on the yellow boards was increasing and it culminated in the period from the second decade of September to the second decade of October, when an average number of the imogoes caught daily exceeded 130 (Figure 1).

Discussion

In the last period of ten years the numbers of the cabbage whitefly (A. proletella L.) on the cultivated Brassica plants, more explicitely on Brussels sprouts (Brassica oleracea L. convar. oleracea L. var. gemmifera DC.) and kale (Brassica oleracea L. convar. acephala (DC.) Alef. var. sabellica L.) were evidently increasing. Until now, an indirect damage was mostly emphasized. The suspicion, that the pest also causes a direct damage, was the subject of this

268

35000 31162 30000 25000 20000 16214 15000 9945

L.) caught on the yellow yellow on the L.) caught 10000 3456 4411 5000 2991 sticky boards sticky 00185 123 266 1343 0

0 0 0 0 0 0 0 0 00 00 000 00 00 2 2 2 2 20 2 2000 4 3 2000 0 0 -10 2 1 2

Number of the cabbage whitefly imogoes imogoes whitefly cabbage of the Number 1-09 1 0-20 g 1 4- p 0- 0 1 u 1 1 ec 04 Aleyrodes proletella Aleyrodes 0-Jul 01 20 A Se D ( un un 09-20 22000 Jul 0 Jul Jul 20-30 2000 - ep - J J - Aug Aug 23-300 2000 S 0 un 30 3 20 - Oct 10 2000 J p ct 1 Jul Aug Se O Period of placing the yellow sticky boards in the experiment

Fig. 1. Review of the total amount of the cabbage whitefly imogoes (Aleyrodes proletella L.) caught on 12 yellow sticky boards in 2000

Temperature (oC) Precipitation (mm)

30 180 160 25 140 20 120 100 15

80 (mm) 10 60 40 5 20 Average temperature (oC)

0 0 Total amount of precipitation

I II I II II I II I II I I I n Jul ug ct May Ju Jul Sep I O Nov I May A Sep III Nov Monthly decade

Fig. 2. Review of an average decade temperatures and total decade amount of precipitation in the period from the first decade of May to the first decade of December 2000

research. It focused on two main points. First, studying the life cycle and development (bionomics) of the cabbage whitefly. Second, finding the most adequate control methods against pest. The emphasis was on the comparison of various agents with various modes of action. The contact insecticide Actellic–50, that is found on the list of environmental friendly phytopharmaceutical agents was used. Apart from that, the systemic insecticide Confidor SL 200 was used, although it is less environmental friendly as Actellic–50. As the third method 269

the yellow sticky boards (one of the biotechnical plant protection methods) were added to the experiment; their usage is linked to monitoring the whitefly (Aleyrodidae) (Abdel-Megeed et al., 1994; Gorski, 1999; Razvi et al., 1999). So far, the efficacy of boards and their influence on the yield of the cultivated plants have been not studied enough (Edigaryan et al., 1988; Rui and Zheng, 1990). The first spraying took place approximately a month after the flying forms were first noticed; that was when daily more than 2 imagoes were found on a board. The second spraying took place when the number was approximately 40 times higher. The insecticide Actellic-50 can be used up to three times in the growing period of the vegetables, therefore it was used three times in this experiment. By then, the number of the cabbage whitefly imagoes daily caught on each board reached 130 (Figure 1). The results show that the most effective control method against the cabbage whitefly on Brussels sprouts is a threefold usage of Actellic-50. The number of pest larvae on plants sprayed with this insecticide was (in both cases) halfed, compared to the plants at the other three treatments which did not show any statistically significant differences in the number of the larvae on a randomly chosen plant leaf. In accordance with these results the highest average yield of Brussels sprouts (780,4 g/plant) was determined after using Actellic-50. It was approximately 20-30% higher than the yield in the other treatments. The yellow sticky boards have proven to be less successful. However this result does not diminish their significance at an early detection and at counting insects during the growing period. The systemic insecticide Confidor SL 200 has proven to be less efficiant than expected. This result is probably due to its quite early usage in the experiment. Still, it can not be fully confirmed, as it showed an unsatisfactory efficacy already in the preliminary estimation (an average number of the larvae/leaf). It was observed, that the cabbage whitefly mostly attacks younger leaves, as it was most commonly found on the upper third of the plants. Also, the pest protects itself by sucking the plant juices on the lower part of the leaves in its preimaginal development stages as well as in the imaginal stages. It can be stated that more abundant precipitation in some decades in the autumn of 2000 did not have the significant impact on the number of the pest found on Brussels sprouts. On the other hand, higher average decade temperatures almost certainly led to the quicker appearance of the pest as it would be expected in a »normal year« (Figure 2). This resulted in the shorter development cycle of the cabbage whitefly and in the larger number of generations. The higher temperatures in the second and in the third decade of August were probably the reason for a fast increase of the pest imagoes on the yellow boards in the second part of September and in the first part of October. During the mild winter 2000/2001 the active imogoes of cabbage whitefly were found on the Brussels sprouts plants in the open air. In the last years, such changes of climate often occurred in Europe and this probably influences the bionomics of these and other insects that are of a larger economic importance a great deal. Knowing these facts, the insects will have to be given more attention in the future as they were given up to this time.

References

Abdel-Megeed, M.I., Zidan, Z.H., Dahroug, S.M.A., Salem, M. & Daoud, M.A. 1994. Factors influencing the performance of yellow sticky traps for monitoring whitefly, Bemisia tabaci on cucumber in Egypt. Ann. Agric. Sci. Cairo 39 (2): 823-828. Edigaryan, S.E., Vardanyan, L.O. & Eritsyan, D.A. 1988. The use of colour traps for control of the greenhouse whitefly Trialeurodes vaporariorum Westw. Biol. Zhurnal Armen. 41 (6): 498-503. 270

Gomboc, S. & Celar, F. 1997. Some news concerning pests in Slovenian horticulture. Lect. and Pap. present. at the 3rd Slov. Conf. on Plant Prot., Portorož, March 4-5, 1997, Plant Prot. Soc. of Slov., Ljubl.: 241-245. Gorski, R. 1999. Monitorowanie szkodnikow roslin szklarniowych. Progress Plant Prot. 39 (1): 321-326. Hydrometeorological Institute of Slovenia. 2000. Mesečni bilten (ed. Hrček, D. and Cegnar T.). Ljubl., Minist. Environ. Phys. Plan., Vol. VII, No. 5-12. Janežič, F. 1961. Kmetijski tehniški slovar. 1. knjiga, 3. zvezek. Varstvo rastlin. Ljubl., Univ. Ljubl., Fak. agron., gozd. vet.: 6. Razvi, S.A., Azam, K.M. & Al Raeesi, A.A. 1999. Monitoring of sweet potato whitefly, Bemisia tabaci (Gennadius) with yellow sticky traps. Sultan Qaboos Univ. J. Sci. Res. Agr. Sci. 4 (1): 11-16. Rui, C.H. & Zheng, B.Z. 1990. Yellow sticky traps combined with a mixture of insecticides for the integrated control of glasshouse whitefly. Acta Agric. Univ. Pekin. 16 (4): 429- 435. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 271-276

Connection between herbicide treatments and nitrate accumulation of green onion

E. Nádasy University of Veszprém Georgikon Faculty of Agriculture Keszthely, Institute for Plant Protection, Department of Herbology and Pesticide Chemistry, 8360 Keszthely, Hungary

Abstract: Nitrate accumulation of vegetables is one of the most important environmental problems recently. There are huge differences among plant species and varieties in nitrate accumulation because of their biological and genetical caracteristics. It’s known that some herbicides can influence the quantity of nitrate in the plants. The aim of our experiment was to study the effect of nitogen fertilizer doses and two preemergent herbicides: Dual 960 EC (metolachlor) and Stomp 330 (pendimethalin) on nitrate accumulation of onion. We have only a few datas about nitrate content of this vegetable, but this plant closely related to the leek which accumulate a lot of nitrate. Weed controll of onion is very important because it has a bad weed competition. We examined changing of fresh matter production, dry matter production, nitrogen and nitrate concentration of onion influenced by nitrogen fertilizer doses and applying herbicides. We established, that Dual and Stomp herbicides could influence nitrate accumulation of onion: they decreased the nitrate concentration in the bulbs and contrary increased in the leaves. Green onion accumulated maximum medium quantity of nitrate even if had excessive nitrogen supply.

Key words: nitrate accumulation, onion, herbicides

Introduction

Nitrate accumulation during the N-cycle of the plants, particularly in vegetables, is one of the most important environmental problems recently. Plants take up nitrogen as nitrate or ammonium. Taken up ammonium incorporates into the organic compounds because it is toxic for the plants. Contrary the plants can store a lot of nitrate without any problems. But high nitrate content in plants are harmful for people especially for babies. Nitrate accumulation is a typical physiological characteristic of plants which is the result of consecutive processes and influenced by many factors. There are huge differences among plant species and varieties in nitrate accumulation because of their biological and genetically characteristics (Prugar et al., 1991). Leafy vegetables have the highest nitrate content but other species also may store large amount of nitrate. We have only a few dates about nitrate content of onion, but it is closely related to leek which accumulate a lot of nitrate. There are great inequality in nitrate content of plant parts affected also by their age (Maynard et al., 1976; Nádasyné & Debreczeniné, 1995; Nádasyné, 1996 a; Pashold & Hundt, 1986). Usually nitrate concentration of the young plants are higher than that of the older. Among the environmental factors there are soil characteristics, quantity and intensity of light, temperature, and water supply. Their modifying effects are significant. Factors of plant production are very important from the point of view of nitrate accumulation.

271 272

Nutrition of plants mainly the nitrogen supply plays an important role in nitrate accumulation where the quantity and form of nitrogen are determinants (Barker & Maynard, 1971; Lehmann, 1977; Nádasyné , 1996 a; Nádasyné, 1996 b.). A lot of herbicides have effect on N-sources of soil, in the first place the soil incorporated herbicides which kill a part of microbe population and this makes trouble in transformation of nitrogen forms. It’s known that different herbicides hinder different processes such as nitrification, denitrification and N-fixation. Weed control of onion is an important question because of its bad weed competition. In this experiment were applied two pre-emergent herbicides, Dual 960 EC (metolachlor) and Stomp 330 (pendimethalin). On the base of former researches pendimethalin hinders the first step of nitrification in the soil, namely the oxidation of ammonium to nitrite (Goring & Laskowski, 1982). The aim of our experiment was to study the effect of nitrogen supply and two preemergent herbicides: Dual 960 EC (metolachlor) and Stomp 330 (pendimethalin) on nitrate accumulation of onion.

Material and methods

The method of pot experiment was chosen to observe nitrate accumulation of onion. Experiments were carried out in soil culture to study soil-plant-fertilizer interactions. It were set up in the greenhouse in 2000. March in four replications. The pots contained 2 kg air dried soil (Table 1.).

Table 1. Characteristics of the experimental soil

Soil characteristics Humus 1,13 % Total nitrogen: 709,88 mg/kg soil Mineral nitrogen 12,28 mg/kg soil NH4-N 7,40 mg/kg soil NO3-N 4,88 mg/kg AL-P2O5 109,06 mg/kg AL-K2O 111,73 mg/kg Maximal water holding 325,20 g/kg capacity

We used ammonium-nitrate as N-fertilizer. It was dosed six days before planting in water solution with rising doses. N-treatments were 0, 15, 30, 60 and 120 mg N/kg soil. Beside control we used two preemergent herbicides: Stomp 330 (pendimethalin), and Dual 960 EC (metolachlor). Herbicides were sprayed by in field suggested doses: Dual 2 l/ha, Stomp 3 l/ha, counted to the surface of the pot, one day after planting. Water was dosed by weight using irrigation until the level of 60% of maximal water holding capacity. A Hungarian onion variety “Makói” was included in this study. We planted 10 bulbs per pots. Leaf and bulb samples of onion were collected at the seventh week after planting. So we examined the young green onion.

273

Methods of plant analysis The plant material were digested according to the Kjeldahl method. From the digestion the total nitrogen was determined by dead-stop indication (Füleki, 1970). Nitrate content of dried and grounded plant samples was determined photometricaly from the 1:8 rate water extract using hydrazine-sulphate as reducing agent and N-(1-naphthyl)-ethylene-diamine plus sulphanilamide as color producing reagents (Thammné, 1990).

Methods of statistical analysis The statistical analysis was carried out by SPSS 7.5 software. The statistical procedure of multifactorial variance analysis was employed.

Results and discussion

Fresh mass production In our experiment a 30 mg N/kg soil fertilizer dose proved to be optimal for the bulb fresh mass production. The yield-growing effect of the N-fertilizer did not come to prevail applying Dual in consequence of its protein synthesis and the root growing hindering effect. The fresh mass of bulbs in these treatments remained the same as that of control, and decreased in the 120 mg N-treatment significantly, producing the lowest quantity of fresh mass. Stomp decreased the fresh mass production only with higher nitrogen doses (Figure 1).

25 20 Control 15 Dual 10 5 Stomp

Fresh mass (g) 0 0153060120 N-doses (mg/kg soil)

Fig. 1. Fresh mass of onion bulbs

60 50 40 Control 30 Dual 20 Stomp 10

Fresh mass (g) 0 0 15 30 60 120 N-doses (mg/kg soil)

Fig. 2. Fresh mass of onion leaves 274

The fresh mass of leaves was lowest also using Dual, and highest at Stomp treated samples. The fresh mass increased up to 60 mg/kg nitrogen without herbicides but with Dual. In the case of Stomp, the leaf mass grew continuously even if treated with 120 mg N (Figure 2). It is to be mentioned that the leaves of the plants grown on a soil treated with Dual presented symptoms of sensitivity as the leaves became wavy.

Nitrogen concentration Effected by the rising N-fertilizer doses the N-concentration of the bulbs of onion increased almost fivefold. Compared the effect of Stomp with the Dual but without herbicides we established that Stomp decreased under lower N-conditions and increased over a 30 mg/kg soil dose. The Dual has decreased the N-content significantly (Figure 3). The N-concentration of the leaves was in the unfertilized control three times and using a maximal N-dose twice higher than that of the bulb. The nitrogen contents increased continuously as the N-doses were getting higher and higher. Increase remained lower than that of the N-concentration of bulb. Effected by Stomp, the N-content of leaves changed in the same way as that of the bulbs, i.e. the less nitrogen supplied the less N-content there was, and vice versa. In the plants on a soil treated with Dual the N-concentration increased continuously. As contrasted with the bulb, the highest values were found in the Dual treatments (Figure 4).

2,5 2 Control 1,5 Dual 1 0,5 Stomp

Total nitrogen (%) 0 0 15 30 60 120 N-doses (mg/kg soil)

Fig. 3. Nitrogen concentration of onion bulbs

4 3 Control 2 Dual 1 Stomp

Total nitrogen (%) 0 0153060120 N-doses (mg/kg soil)

Fig. 4. Nitrogen concentration of onion leaves

275

Nitrate concentration The nitrate-nitrogen contents were stated in the dry mass and converted into the N-content of fresh mass in sense of the international suggestions relating to the limits of nitrate contents. Effected by the control N treatments and the 15 mg N/kg soil fertilizer, no measurable nitrate quantities in the bulb of onion were stored. Even if treated with 30 mg N, only a very little quantity of nitrate could be found. The nitrate concentration increased rapidly if treated with 60 and 120 mg N, respectively. Thus, the 30 mg N/kg dose of fertilizer can be considered as optimal as for nitrate accumulation as for fresh mass production. The highest nitrate values were found in the treatments without herbicides. This fact is probably caused by the root developing inhibitory effects of Dual and the nitrification inhibitory effect of Stomp. In consequence of this the plants could find or take up less nitrate. The effect of Dual was stronger as the lowest nitrate quantities were accumulated in the samples treated with it (Figure 5).

500 400 Control 300 Dual 200 Stomp 100 (mg/kg) 0 0 153060120 nitrate in fresh mass N-doses (mg/kg soil)

Fig. 5. Nitrate concentration of onion bulbs

800 600 Control 400 Dual 200 Stomp (mg/kg) 0 0 153060120 nitrate in fresh mass N-doses (mg/kg soil)

Fig. 6. Nitrate concentration of onion leaves

As for nitrate concentration of leaves it could be established that no measurable quantities of nitrate there were in the leaves without N fertilizer given, and only a very little concentration has been measured in one treatment dosed with 15 and 30 mg/kg nitrogen. Similarly to the bulb, the nitrate concentration of the leaves also increased strongly by treating 276

with 60 mg/kg soil nitrogen, and it became higher and higher by dosing with 120 mg/kg N. The nitrate accumulation of bulb was higher than that of leaves. Effected by the herbicides, the nitrate concentration in the leaves in contrast to the bulb increased except when treated together with 120 mg/kg N and Dual (Figure 6.). We established, that Dual and Stomp herbicides could influence nitrate accumulation of onion: they decreased the nitrate concentration in the bulbs and contrary increased in the leaves. Green onion accumulated maximum medium quantity of nitrate even if had excessive nitogen supply.

References

Barker, A.V. & Maynard, D.N. 1971: Nutritional factors effecting nitrate accumulation in spinach. Commun. Soil Sci. Plant Anal. 2 (6): 471-478. Füleky, Gy. 1970: A dead-stop végpontjelzéses nátriumhipobromitos titrálás alkalmazása növényi anyagok és műtrágyák nitrogén tartalmának meghatározására. Agrokémia és Talajtan 19: 339-345. Goring, C.A.I. & Laskowski, D.A. 1982: The effects of pesticides on nitrogen transformations in soils. USA Agronomy Monograph 22: 689-720. Lehmann, K. 1977: Die Wirkung hoher Mineraldüngung auf die wichtigsten Stickstoff- fraktionen, insbesondere Nitrat-N in Futterpflanzen. Arch. Acker- Pflanzenbau Bodenk. 21: 191-199. Maynard, D.N., Barker, A.V., Minotti, P.L. & Peck, N.H. 1976: Nitrate accumulation in vegetables. Adv. Agron. 28: 71-118. Nádasy, E. & Debreczeni, K. 1995: Study on NO3-N content of green pea. Fourth International Symposium on Inorganic Nitrogen Assimilation. Darmstadt, Germany 1995. 87. Nádasy, E. 1996 a: Study on the effect of N-fertilizers on total nitrogen and nitrate content of green pea and garlic. European Society for Agronomy Fourth Congress Veldhoven and Wageningen, Netherlands 1996. 2: 578-579. Nádasy, E. 1996 b: Changing of the total nitrogen and nitrate content in green pea and lettuce using rising rates of N-fertilizers. IX.International Colloquium for the Optimization of Plant Nutrition 8th-15th September 1996 Prague, Czech Republic.: 205-208. Paschold, P.J. & Hundt, I. 1986: Produktion von Spinat und Möhren mit reduziertem Nitrat- gehalt. 24: 4. Prugar, J., Vanek, V., Sokolov, O.A. & Semenov, V.M. 1991: Nitrates in plants. In: Nitrogen Cycles in the Present Agriculture. Bielek, P. & Kundeyarov, V.N. (eds.), Priroda Bratislava, Czecho-Slovakia. 140: 127-167. Thamm, F-né. 1990: Növényminták nitráttartalmának meghatározását befolyásoló tényezők vizsgálata. Agrokémia és Talajtan 39: 191-206. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 277-299

The role of banker plants in the enhancement of the action of Diaeretiella rapae (M’Intosh) (Hymenoptera, Aphidiinae) the primary parasitoid of the cabbage aphid Brevicoryne brassicae (L.)

J. Freuler1, S. Fischer1, C. Mittaz2 & C. Terrettaz3 1 Swiss Federal Research Station for Plant Production, Changins, CH-1260 Nyon, Switzerland 2 Swiss Federal Research Station for Plant Production, Les Fougères, CH-1964 Conthey, Switzerland 3 Office of Plant Protection of the Canton of Valais, CH-1950 Châteauneuf, Switzerland

Abstract: Since 1972, the cabbage aphid Brevicoryne brassicae has been known as a pest in the west of Switzerland and, since 1981, has reached economic thresholds in oilseed rape and Brassica vegetables. Up until 1991, applied research concentrated on developing visual scouting methods and tolerance thresholds based on the "first event" method. From 1987 to 1999, the relative efficacy of several insecticides available against the pest was checked and from 1996 to 1998, trials were carried out to further investigate the action of the aphid parasitoids and hyperparasitoids. The present article describes these latter experiments. A experimental plot of approximately 30 m x 40 m on the estate of "Les Fougères" in the Valais was planted with cauliflower. Rows of Savoy cabbage and turnip, which act as banker plants for aphids and their parasitoids, were sown across the middle of the field. The populations of healthy aphids and parasitised aphids (unhatched mummies) are estimated in situ or by plant sampling. The aphids concerned are: the cabbage aphid Brevicoryne brassicae, the green peach aphid Myzus persicae, and the potato aphid Macrosiphum euphorbiae. The latter two species being called "green aphids". The parasitoids and hyperparasitoids were allowed to emerge from the collected mummies. The parasitoids found all belong to the sub-family of Aphidiinae: Diaeretiella rapae, Aphidius matricariae, Aphidius ervi and Praon sp. and the hyperparasitoids to the families of Charipidae: Alloxysta sp. and Pteromalidae: Asaphes suspensus and Pachyneuron aphidis. The turnip is a banker plant of inferior quality; aphid populations are low in general, cultivation time is short and the nutritive quality of the plant diminishes rapidly. Moreover, it is possible that the leaves covered in hairs impede insect movement. On the other hand, Savoy cabbage is capable of holding large aphid host populations for parasitoids, even early in the season. Up until June, parasitoids are made available for neighbouring crops. After this time, the multitrophic system also becomes a source of hyperparasitoids, undesirable in biological control. Because of its host specificity for the cabbage aphid, D. rapae largely dominates the parasitoid population and generally accounts for >90% of individuals on Savoy cabbage. Indeed, the numerically weaker green aphids often arrive later than the cabbage aphids and are unable to establish large populations of A. matricariae, A. ervi and Praon sp. In the slightly continental climate of the Valais, the cabbage aphid is typically holocyclic, alternating between parthenogenesis and a compulsory winter diapause at the egg stage. D. rapae has adapted well to this prolonged absence of its host by a long diapause which it spends inside the mummified aphid. At the end of winter, emergence is spread out over quite a long period so that generations are not clearly separated. D. rapae action is severely hampered by the hyperparasitoids, by Alloxysta sp. in particular. Although the former emerges in the spring 2 to 4 weeks before the latter, this advance cannot be used in biological control since, at this time, the host plants are not yet established. As soon as the hosts are in place, the hyperparasitoids also begin to emerge. Furthermore, hyperparasitoids live longer than parasitoids which helps them to cope better with the temporary absence of hosts. The efficacy of D. rapae is reduced when the "escape" phenomenon on Savoy cabbage occurs late in the season under

277 278

the effect of increased honeydew quantities, when, in a given plot, the number of parasitised aphids increases and there is a rise in hyperparasitoid numbers. The density of hyperparasitoids can become so high that D. rapae is locally exterminated which then leads to the disappearance of hyperparasitoids. Under such conditions, it is advisable to destroy the banker plants and remainders of the primary crop directly after its harvesting in order to prevent hibernation of hyperparasitoids. Given that the host-foraging behaviour of D. rapae is efficient when hosts are widely spread and few and that its area of discovery is larger than that of Alloxysta sp., sowing banker plants in an environment free from overwintering host plants gives D. rapae the chance to settle safely on new aphid colonies before the arrival of hyperparasitoids and to then leave for new neighbouring crops. The resulting high level of parasitism could prevent the establishment of aphid colonies. Banker plants which are sown a month before cauliflower planting carry their first mummies 2 to 3 weeks before the latter. On the cauliflower, parasitism triumphs over pests. Indeed, the cauliflower heads are generally free from B. brassicae and any traces found are of no economical consequence. According to our observations in the Valais over a longer period from 1992 to 1999, the cauliflower heads were free from aphids at harvesting when planting took place between the second half of May and the beginning of June with a length of cultivation < 70 days. Indeed, within these limits, D. rapae is still in its ascending phase and B. brassicae in a descending phase.

Key words: Banker plants, Savoy cabbage, turnip, cauliflower, Brevicoryne brassicae, parasitoids, Diaeretiella rapae, Aphidius matricariae, Aphidius ervi, Praon, hyperparasitoids, Alloxysta, Asaphes suspensus, Pachyneuron aphidis

Introduction

The cabbage aphid Brevicoryne brassicae (L.) a pest of Brassica crops has posed, since the beginning of the eighties, an economic threat to Brassica vegetables (Freuler et al., 2001a). The main antagonist of this aphid is Diaeretiella rapae (M'lntosh), a small hymenopteran wasp of the Aphidiinae sub-family. The endoparasitic lifestyle of this primary solitary parasitoid during its immature stages leads to the destruction of its aphid host (Vinson, 1976). Its high host- specificity, its short generation span, its excellent synchronisation with the host together with its high potential fertility all combine to make this parasitoid an attractive method of control. Its own enemies, however, called hyperparasitoids or secondary parasitoids (Borgemeister and Poehling, 1990) reduce its usefulness. In the slightly continental climate of the Valaisthe cabbage aphid is typically holocyclical alternating between parthenogenesis and a compulsory winter diapause at the egg stage. During this prolonged absence of its host, D. rapae has adapted by hibernating inside the mummified aphid (Krespi et al., 1997). At the end of winter, there is a good coincidence between the host and the parasitoid (Hafez, 1961), when the latter develops all its qualities for the quest of a host, still widely scattered and poorly populated (Lopez et al., 1990; Höller et al., 1993). The resulting high parasitism may prevent the establishment of aphid colonies (Bradburne and Mithen, 2000). Hafez (1961) and Sedlag (1964) had already envisaged a strategy for favouring the presence of D. rapae at the beginning of the season which consisted of planting overwintered Brassica with a high level of parasitism at the edges of new cultivations. This proximity between old and new crops facilitated localisation of the new host's habitat by the parasitoids. Given that the hyperparasitoids emerge after D. rapae, the overwintered Brassica can be destroyed after the latter have emerged and the majority of the former are still in the mummies. 279

In this study, the evolution of parasitism in the cabbage aphid was followed during a 3 year period in a system where cauliflower was cultivated side by side with rows of Brassica plants which served as banker plants for D. rapae.

Material and methods

1996 The experimental plot measuring 30 m wide and 40 m long is situated in the canton of Valais, on the estate of the Horticultural Centre "Les Fougères" in Conthey. Two rows of Savoy cabbage (Brassica oleracea L. convar. capitata var. sabauda L.), run through the middle of the plot, flanked on either side by a row of turnip (Brassica rapa L. var. rapifera subvar. Majalis). The remainder of the plot is cultivated with cauliflower (Brassica oleracea L. convar. botrytis (L.) Alef. var. botrytis (L.)). Four varieties of Savoy cabbage were utilised, differing according to their precocity and thus length of culture: Cvs ‘Promasa” F1 (58 days), ‘Famosa’ F1 (75 days), ‘Darsa’ F1 (110 days) and ‘Wirosa’ F1 (140 days). The latter variety resisted the cold well and could be left in the field over the winter. The half-long, early, white Vertus turnip (marteau race) has numerous leaves, rather short and rough. Its period of growth lasts two and a half months in the spring and two months in the summer. The variety of cauliflower 'Fremont' F1 is semi-early. Its leaves are partly erect, with feeble swellings on its summit and a weak folding near the principal nervure. Seeds from the four varieties of Savoy cabbage were mixed and sown in four rows per strip directly into the ground on the 23.4 using a manual sower, Sembdner Kombi. A density of plants of approx. 20 per m2 was aimed for (approx. 30 cm x 15 cm). Monitoring of the cabbage aphid Brevicoryne brassicae (L.) populations, the green peach aphid Myzus persicae Sulz. and the potato aphid Macrosiphum euphorbiae Thos. – the latter two species being called hereafter "green" aphids – , and parasitised aphids (unhatched mummies) were made once a week from 15.5 to 25.7. After this date populations were monitored every two weeks until 13.11. During these 11 controls, a certain number of plants were sampled according to their phenological stage. That is, 50 plants were sampled randomly from both strips of cabbage at about the 9-leaf stage and 20 at more developed stages. The insects found were either counted or estimated using a class system with appropriate multiplication factors (class O = 0 aphid or unhatched mummies, class 1 = 1 to 5 aphids or unhatched mummies (factor 3), class 2 = 6 to 20 aphids or unhatched mummies (factor 10), class 3 = 21 to 100 aphids or unhatched mummies (factor 50), and class 4 = > 100 aphids or unhatched mummies (factor 300). From the 18.9, unhatched mummies found during the controls were placed in emergence boxes by date of sampling in the insectarium at Changins. Each week, until 5.12 and from 26.2 to 20.6.1997, the parasitoids and their hyperparasitoids were thus collected. As the Savoy cabbage crop overwintered, samples from 20 plants were taken in the spring 1997 on 4 and 20.3 and on 1.4, in order to further investigate the evolution of the cabbage aphid from the time of hatching of winter eggs, of parasitism and hyperparasitism at the end of winter, and of the formation of new mummies. On 1.4 the first winged cabbage aphids appeared and the proportion of old to new mummies was about 1. On 8.4, some of the overwintered plants were harvested and laid down alongside the experimental plot in order to supply the new crops with parasitoids. Emergence boxes were installed on the spot on 8 and 15.4 containing 10 and 30 plants so that the study of parasitism and hyperparasitism could be continued at the end of winter. The overwintered crop was destroyed immediately afterwards. 280

The turnips were also sown on the 23.4 in five rows per strip. The density of plants aimed for was about 40 per m2 (about 25 cm x 10 cm). Monitoring of insect populations were made every week from 15.5 to 17.7. During these 10 controls, a certain number of plants were sampled randomly from the two strips according to their phenological stage, i.e., 100 up to the 5 or 6-leaf stage, 50 up to the 10 to 11-leaf stage, and 20 plants at a more developed stage. The insects found were either counted or estimated according to the same scale of classes O to 4, as above. The cauliflowers were planted mechanically on 22.5 in the northern part of the field and a week later in the southern half. The density of plants was about 3 per m2 (70 cm x 50 cm). Monitoring of insect populations were made weekly from 4.6 to 25.7 and at harvest on 8.8. Monitoring was made in situ with the exception of the final inspection when whole plants were harvested. The first 3 controls were made on 60 plants over the whole of the two parts of the plot before insecticide treatments, whereas the following 6 controls concerned 40 plants in an 8m strip on the untreated west side of the plot. The length of the cultivation period was 78 days.

1997 The experimental plot was the same as that used in 1996 and the lay-out of crop strips identical. Only two Savoy cabbage varieties, 'Famosa' F1 and 'Wirosa' F1 were sown directly in the ground on 5.5. From 3.6 to 10.12, the 14 visual controls were made separately according to variety. From 24.6, unhatched mummies were placed in emergence boxes by date of sampling in order to collect parasitoids and hyperparasitoids until 29.10 and again from 25.2 to 24.9.1998. The Savoy cabbage crop having overwintered, sampling was continued from spring 1998, on 11 and 25.3 and on 1 and 8.4. After hatching of the cabbage aphid winter eggs and at the start of the formation of new mummies, the 1.4 samples and some of the 8.4 samples were placed in emergence cages at "Les Fougères". On 8.4, after setting up the emergence boxes, the remaining overwintered Savoy cabbages were harvested and laid down near the experimental plot so that the new crop could be supplied with parasitoids. As the heads dried up, so aphid development stopped. The turnips were sown on 6.5. Six visual controls were made between 27.5 and 22.7. The cauliflowers, var. 'Fremont' F1 were mechanically planted on 20.5. Eight visual controls were made between 27.5 and 30.7, the final one taking place at harvesting. The first 3 controls were made before insecticide treatments over the whole of the south block and the 5 following ones in an 8 m untreated strip on the west. The length of the cultivation period was 71 days.

1998 The experimental plot was a little further to the south and measured 46 m in width and 36 m in length. On the west of the plot, a 24 m long strip was sown directly with Savoy cabbage, cvs. 'Famosa' F1 and 'Wirosa' F1, on 27.4. From 27.5 to 9.12, 15 visual inspections were made separately according to variety. From the 10.6 control, unhatched mummies were placed in emergence boxes by date of sampling and the hymenoptera parasitoids and hyperparasitoids were collected until 30.12 and from 3.2 to 30.6.1999. As the 'Famosa' F1 variety suffered from winter frost and because no mummies were found after the controls on 25 and 31.3.1999 at the end of winter on the 'Wirosa' F1 due to rapid multiplication of the cabbage white fly during the 1998 season, the trial was stopped. Turnip cultivation as a banker plant for parasitoids was abandoned due to its poor host plant qualities for the green aphids and the cabbage aphid. 281

The cauliflowers cv. 'Fremont' Fl were mechanically planted on 27.5. Of the six visual controls carried out between 2.6 and 30.7, two took place before insecticide treatments over the whole of the plot and the remaining controls in the 8 m untreated west strip. The length of the cultivation period was 94 days. A crop of cauliflower was planted on 2.6, i.e. one week later, at the cantonal School of Agriculture at Châteauneuf (ECA) and was used as a comparison. Monitoring took place on the same dates. In order to present results of monitoring, the average number of aphids, i.e. cabbage aphid, green aphids and mummies, was calculated. Parasitoid activity was estimated by determining the rate of mummification M = (unhatched mummies/unhatched mummies + aphids) * 100 (Kuo-Sell et al., 1989). The hymenoptera collected in the emergence boxes were identified according to species, where possible. The number of parasitoids and hyperparasitoids per plant and the percentage of hyperparasitism were calculated.

Results

During experimentation, the following parasitoids, all of which belong to the Aphidiinae sub- family, appeared in the emergence boxes: D. rapae, Aphidius matricariae Haliday, A. ervi Haliday, Aphidius sp. and Praon sp. Aphidiinae are endoparasitoids and lay their eggs inside the host's body. Their hyperparasitoids are represented by small hymenoptera wasps of the Charipidae family: Alloxysta sp. and the Pteromalidae family: Asaphes suspensus (Nees), Asaphes sp. and Pachyneuron aphidis (Bouché). Alloxysta sp. is an endohyperparasitoid, that is, a secondary parasitoid which lays its egg inside the primary parasitoid larva which is itself inside the live aphid. It is relatively specific (Müller and Godfray, 1998) and shows a preference for the Aphidiinae (Krespi et al., 1997). The Alloxysta genus is undergoing taxonomic revision (Grasswitz and Reese, 1998). The following names can be found in the literature which attack D. rapae: Alloxysta brassicae (Ash.), A. victrix (Westwood), A. fuscicornis (Hartig, 1841), Allotria victrix var. infuscata Kieff. and Charips brassicae (Ash.). On the other hand, P. aphidis and A. suspensus are ectohyperparasitoids, that is, secondary parasitoids which lay their egg once the aphid has been mummified by the primary parasitoid during the final larval stage or in the pupa of D. rapae or Alloxysta sp. (Vater, 1971; Müller and Godfray, 1998). In France, P. aphidis is also associated with parasitoids of the pear-tree psylla (Nguyen et al., 1984; Armand et al., 1991), an unknown phenomenon in Switzerland (M.Hächler, pers. comm.).

1996 The green aphids colonised the Savoy cabbage at the 2-leaf stage and the turnips at the 3-5 leaf stage on 15.5 or 22 days after sowing, and before the cauliflower had been planted. The cabbage aphid infested all three host plants at least two weeks later, between 29.5 and 4.6, at similar phenological stages. Evolution of the cabbage aphid, the green aphids, the mummies and mummification percentage in the banker plants and in the cauliflower can be followed in figure 1. A maximum of 37 green aphids per Savoy cabbage plant was reached on 17.7. On the turnip green aphid presence remained discrete throughout cultivation reaching a maximum of 17 aphids per plant, also on 17.7. This was the last inspection as the crop was ripe. Green aphid presence on cauliflower was insignificant with a small peak of 4 individuals per plant on 19.6. The cabbage aphid was the most prolific on Savoy cabbage where there were two maxima: around mid-July with 173 aphids per plant and at the beginning of October with 184 aphids per plant. At the end of the season there was a large population. On the turnip, the

282

200 Savoy cabbage 100 180 90 160 80 140 70 120 60

100 50 % 80 40 60 30 40 20 Average number per plant 20 10 0 0

4.6 4.7 8.8 5.9 15.5 22.5 29.5 12.6 19.6 26.6 10.7 17.7 25.7 20.8 18.9 2.10 16.10 30.10 13.11 Date

Turnip 200 100 180 90 160 80 140 70 cabbage aphid 120 60

100 50 % green aphids 80 40 60 30 mummy 40 20 Average number per plant % mummification 20 10 0 0

15.5 29.5 12.6 26.6 10.7 Date

Cauliflower

200 100 180 90 160 80 140 70 120 60

100 50 % 80 40 60 30 40 20 20 10 Average number per plant 0 0

6 8 .6 9.6 0.7 5.7 . 4 12. 1 26.6 4.7 1 17.7 2 8 Date

Fig. 1. Development of cabbage aphid, green aphids, mummies and mummification percentage on banker plants and cauliflower at "Les Fougères" in 1996. 283

cabbage aphid's presence was insignificant and never rose above 3 individuals per plant. On the cauliflower, populations rose to 41 aphids per plant on 10.7 and fell back to 2 at harvesting. The first mummies were found on Savoy cabbages on 29.5 or 36 days after sowing, followed by turnips on 4.6 or 42 days after sowing and, finally, on cauliflowers on 19.6 or 24 days after planting. A maximum of mummies was reached on 25.7 in the Savoy cabbage with 37 mummies per plant. As from the 25.7 the number of mummies decreased, in spite of a large presence of the cabbage aphid. As far as the turnip and cauliflower are concerned, the maximum occurred around the time of crop maturity, with 3 mummies per plant on 10.7 and 12 mummies per plant on 8.8. The maximum rate of mummification was obtained in the cauliflower at harvesting, on 8.8, with 75 %, in Savoy cabbage on the same date with 42%, and in the turnip on 10.7 at crop maturity with 33%. The frequency of parasitoids and hyperparasitoids on the banker plant, Savoy cabbage, is presented in figure 2. The results of parasitoid emerging in the Savoy cabbage samples were partial, since mummy sampling covered the period from mid-September to mid-November only.

D.rapae Savoy cabbage A.matricariae 10 Praon sp. 9 Alloxysta sp. t 8 A.suspensus 7 6 P.aphidis 5 4 3 Number per plan 2 1 0

0 0 7 3 .4 .4 4 .10 11 1 8 996 2 3. 20. 15. 16.1 30.1 1 9.1 8. 4.3.199 1 Date

Fig. 2. Frequency of parasitoids and hyperparasitoids on the banker plant Savoy cabbage according to dates of mummy sampling at "Les Fougères" in 1996.

There was a distinct domination of D. rapae which accounted for 97.6% to 100% of individuals. A. matricariae never exceeded 2.4%. In 1997, in the overwintered Savoy cabbage crop, the number of D. rapae individuals accounted for 84.6% to 100%, that of A. matricariae 13.5% and that of Praon sp. 2.2%. In 1996, Alloxysta sp. was the most frequently occurring hyperparasitoid at 73.3% to 100%. A. suspensus reached a frequency of 12.5% and P. aphidis 20%. Alloxysta sp. remained dominant at the beginning of 1997, but then lost ground to A. suspensus which reached a frequency of 41.4% on 15.4. P. aphidis, however, remained rare with 2.7%. If the number of parasitoids and hyperparasitoids which emerged from the last sampling in 1996 (13.11) is compared with that of the first sampling in 1997 (4.3), a winter loss of 284

67.5% is noted for D. rapae (from 2 to 0.65 per plant) and 66.7% for Alloxysta sp. (from 1.35 to 0.45 per plant). The populations of D. rapae and Alloxysta sp. were amply built up again by 8.4.1997 following the formation of new mummies. On 15.4 the 3 parasitoids and the 3 hyperparasitoids were all present. In 1996 and in 1997 on the overwintered crops, the rate of hyperparasitism did not vary greatly, from 33.3% to 53.9% and from 43.2% to 68.1 %. Figure 3A and 3B demonstrates how emergence of D. rapae and Alloxysta sp. from mummies collected at the end of 1996 and the beginning of 1997 is staggered. 63.3% of D. rapae and 81.8% of Alloxysta sp. collected on 18.9 still emerged in 1996. There were few mummies in the sample of 2.10, of which all the D. rapae and Alloxysta sp. emerged in 1996. Of the mummies sampled on 16.10, 100% D. rapae and 50% Alloxysta sp. emerged in 1996. Only 13.3% of the D. rapae emerged from mummies collected on 30.10 in 1996 and aIl the Alloxysta sp. emerged only in 1997. From the final sampling on 13.11, 2.5% of the D. rapae still emerged in 1996. From the first samplings in 1997, D. rapae emerged before AIloxysta sp. whereas, at the end of the season 1996, emergences of both hymenoptera were mixed. No new mummies were found on 4.3.1997 and the first were observed on 20.3. By 1.4 the proportion between new and old mummies was estimated to be about 1.

1997 Savoy cabbage and turnips were sown almost 2 weeks later than in 1996, whereas the cauliflower was planted at about the same time. Green aphids and cabbage aphids colonised turnips at the 3-4 leaf stage on 27.5 or 21 days after sowing. Colonisation of the Savoy cabbage is thought to take place at a slightly earlier phenological stage. In this year the cabbage aphid was no later than the green aphids which reached its maximum on 8.7 on the cabbage with 21 aphids per plant, 64 days after sowing (fig. 4). The presence of these aphids was insignificant on the turnip, and weak on the cauliflower. Development of the cabbage aphid on the Savoy cabbage took place in 4 successive waves with 3 distinct peaks on 24.6, 19.8 and 18.9 with 89, 63 and 49 aphids per plant, respectively. The cabbage aphid was more active than in 1996 on the turnip but was still, nevertheless, feeble with no more than 13 aphids per plant. On the cauliflower the population rose high with a maximum of 128 aphids per plant on 17.6, exceeding for this year the peaks in Savoy cabbage. By harvesting, only traces of the pest population remained with 0.5 aphids per plant. The first mummies appeared on the 3 host plants on 10.6, which corresponds to 36 days after sowing of cabbage, 35 days after turnip sowing and 21 days after cauliflower planting. The maximum number of mummies was reached on 22.7 in the Savoy cabbage with 51 mummies per plant. Very few mummies developed on the turnip with a maximum of 0.6 mummies per plant on 24.6, whereas the number of mummies on the cauliflower rose to 18 per plant on 15.7. 285

Fig. 3A. Staggering of D. rapae and Alloxysta sp. emergence from mummies collected at "Les Fougères" at the end of 1996. 286

Fig. 3B. Staggering of D. rapae and Alloxysta sp. emergence from mummies collected at "Les Fougères" at the beginning of 1997. 287

Savoy cabbage

140 100 120 80 100 80 60

60 % plant 40 40 20 20

Average number per per number Average 0 0

6 6 7 7 7 8 9 9 3. 1. 8.7 5. 2. 12 27.5 10.6 17. 24.6 15. 22.7 30. 19.8 18.9 30. 14.10 29.10 11.11 25.11 10. Date

Turnip

140 100 cabbage aphid 120 80 100 80 60 green aphids %

plant 60 40 40 20 20 mummy Average number per 0 0

6 3. 1.7 8.7 5.7 2.7 27.5 10.6 17.6 24.6 1 2 % mummification Date

Cauliflower

140 100 90 120 80 100 70 80 60 50 % 60 40

40 30 20

Average number per plant 20 10 0 0 5 6 6 6 7 7 7 . 3.6 . . . 1.7 8.7 . . . 27 10 17 24 15 22 30 Date

Fig. 4. Development of cabbage aphid, green aphids, mummies and mummification percentage on banker plants and cauliflower at "Les Fougères" in 1997. 288

D.rapae Savoy cabbage Aphidius spp. 10 9 Praon sp. 8 Alloxysta sp. 7 6 Asaphes spp. 5 4 P.aphidis 3

Number per plant 2 1 0

0 0 1 1 2 5.8 2.9 1.4 8.4 19.8 18.9 2.10 25.3 .1997 16.1 30.1 13.1 25.1 10.1 .1998 22.7 11.3 Date

Fig. 5. Frequency of parasitoids and hyperparasitoids on the banker plant Savoy cabbage according to dates of mummy sampling at "Les Fougères" in 1997.

The highest rate of parasitism was obtained in the cauliflower with 83% on 30.7 at harvesting, followed by the Savoy cabbage with two peaks of 76% and 50% on 22.7 and 2.9 (corresponding to the periods between the two first maxima of the cabbage aphid) and finally the turnip with only 4% on 24.6. The emergence boxes containing mummies on Savoy cabbage leaves (var . 'Famosa' F1 and 'Wirosa' F1) sampled on 24.6 and 8.7 were abandoned after two weeks because mould developed on the foliage. Parasitoid emergence showed that there was a clear domination of D. rapae throughout the year 1997, accounting for 98.8% to 100% of individuals (fig. 5 ). A. ervi and Praon sp. were found only in the sample of 22.7. From 18.9 to 25.11, there were very few unhatched mummies or even none at all. On the overwintered Savoy cabbage, the frequency of D. rapae rose in 1998 from 88% to 100%, leaving a little more room from the month of April for Aphidius spp. (Aphidius sp., A. ervi and A. matricariae, maximum 9%) and for Praon sp. (maximum 6.4%). During the months of July and the beginning of August, the hyperparasitoids A. suspensus and P. aphidis were well represented. For the remainder of the season, however, Alloxysta sp. dominated with frequencies between 90.9% and 100%. On the overwintered crop, in 1998, Alloxysta sp. was first to arrive. Its frequency rate varied between 71.2% and 86%. Asaphes spp. (Asaphes sp. and A. suspensus) reached a rate of 14% to 27.4%. P. aphidis did not exceed 5.2%. The rate of hyperparasitism varied between 46% and 91.7%, the maximum being reached on 19.8. On the overwintered crop, in 1998, it varied from 37.4% to 43.4%. If the number of parasitoids and hyperparasitoids emerging from the final sample in 1997 (10.12) is compared with that of the first in 1998 (11.3) before the appearance of new mummies, a winter loss of 95.7% is noted for D. rapae (from 2.35 to 0.1 per plant), and of 97.5% for Alloxysta sp. (from 2 to 0.05 per plant). With the formation of new mummies, on 1.4, the D. rapae population had built up to 76.6% (1.8/2.35*100) and the AIloxysta sp. population to 43.5% (0.87/2*100). 289

On 22.7 all 3 genera of parasitoids and hyperparasitoids were present. As from 5.8, the hyperparasitoids caused the disappearance of Aphidius spp. and of Praon sp., and from 18.9 of D. rapae also. The latter made a timid reappearance from 11.11 but was caught up again by Alloxysta sp. at the end of the year. From 1.4.1998 the 3 genera of parasitoids and hyperparasitoids were again all present and on 8.4.1998 all species of parasitoids and hyperparasitoids. From mummies collected up to 2.9, all the D. rapae and Alloxysta sp. emerged in 1997. After which, there were no mummies until the end of October. Mummies placed in emergence boxes on 11.11 and 10.12 all emerged in 1998, the majority of D. rapae emerging before Alloxysta sp.

1998 Savoy cabbage was sown and cauliflower planted at the same time as in 1996. Together, green aphids and cabbage aphids colonised Savoy cabbages at the 2-5 leaf stage of growth on 27.5, or 30 days after sowing, and cauliflower on 2.6 or 6 days after planting at "Les Fougères" and on 10.6 or 8 days after planting at the ECA. Continuing development was affected by a population explosion of the cabbage white fly Aleyrodes proletella (L.) which created strong space competition on the plant. Green aphids reached a maximum on the Savoy cabbage on 1.7 with 30 aphids per plant 65 days after sowing (fig. 6). On the cauliflower, green aphids presence was weak with a peak of 13.4 aphids per plant on 24.6 at "Les Fougères" (28 days after planting), but strong at the ECA with a peak also on 24.6 of 162 aphids per plant (22 days after planting). On 1.7, a maximum of 300 cabbage aphids per plant was measured on the Savoy cabbage (highest possible with our system of estimation) with a smaller peak again on 24.9 with 65.8. Large populations of this aphid were also found on the cauliflower although not as high as on the Savoy cabbage: at "Les Fougères" a maximum was found on 24.6 with 170 aphids per plant (28 days after planting) and at the ECA on 1.7 with 285 (29 days after planting). As usual, at harvesting time only traces of all aphids species were found on cauliflower (0.15 - 4 aphids per plant). The first mummies appeared on Savoy cabbage on 27.5 or 30 days after sowing, i.e. at the same time as the first aphids were found by monitoring. In both cauliflower fields, the first mummies appeared on 17.6 or 21 days after planting at "Les Fougères" and 15 days at the ECA. A maximum number of mummies was reached on 1.7 in Savoy cabbage, 65 days after sowing, with 142 mummies per plant, corresponding to the period when aphids were also arriving at its maximum. Parasitism was similar for cauliflower at the ECA and for Savoy cabbage; however, on the cauliflower at "Les Fougères", the maximum was measured at harvesting on 29.7, 63 days after planting with 81 mummies per plant. For the other years, the maximum had also been found at or around harvesting time. The highest rate of parasitism was obtained with cauliflowers at harvest-time: 99.1% at "Les Fougères" and 91.7% at the ECA, followed by the Savoy cabbage with a high point of 84.0% on 15.7 and a smaller one of 16.2% on 8.10. Parasitoid emergence from the Savoy cabbage samples (var. 'Famosa' F1 and 'Wirosa' F1 together) showed that D. rapae clearly dominated all year long in 1998 with 90% to 100% of individuals (fig. 7). Aphidius spp. (Aphidius sp. and A. matricariae) progressively lost ground from 10% on 10.6 to 0.05% on 1.7. Praon sp. did not exceed 1 %. There were very few unhatched mummies after 27.8. As for hyperparasitoids, Alloxysta sp. was the first to arrive on 10.6 and remained dominant until 1.7 (51.2%). After 15.7, A. suspensus and P. aphidis took its place (16.4%), finishing at 7.1 % on 30.7. A.suspensus rose to 100% on 12.8 and P.aphidis to its maximum on 30.7 with 28.6%. 290

Savoy cabbage 300 100

250 80 200 60

150 %

plant 40 100 50 20 Average number per 0 0

5 7 7 8 8 9 9 0 0 1 1 .7 ...... 1 1 1 1 2.6 1.7 8 5.7 9 0 2 7 0 4 . 2. . 6. 27. 10.6 17.6 24.6 1 2 3 1 2 1 2 8 2 3 1 Date

Cauliflower Les Fougères cabbage aphid

300 100 90 green aphids 250 80 200 70 60

150 50 % mummy 40 100 per plant 30 50 20

Average number 10 0 0 % mummification

6 7 7 7.6 5.7 . 2. 1 1. 1 30 Date

Cauliflower ECA

300 100 90 250 80 200 70 60

150 50 %

plant 40 100 30 50 20 Average number per 10 0 0

6 6 6 7 7 7 1.7 8.7 10. 17. 24. 15. 29. 30. Date

Fig. 6. Development of cabbage aphid, green aphids, mummies and mummification percentage on banker plants and cauliflower at "Les Fougères" and at the ECA in 1998.

291

Savoy cabbage

20 112,1 D.rapae 18 Aphidius spp. 16 14 Praon sp. 12 Alloxysta sp. 10 A.suspensus 8

Number per plant 6 P.aphidis 4 2 0

8 7 .9 0 99 17.6 1.7 15. 30.7 12.8 2.9 18 24.9 .10 16.10 22.1 30 13.11 10.12 6.1 0. 1 Date Fig. 7. Frequency of parasitoids and hyperparasitoids on the banker plant Savoy cabbage according to dates of mummy sampling at"Les Fougères" in 1998.

The frequency of hyperparasitism varied from 3.5% to 100%, a maximum being reached on 12.8. All mummies collected between 10.6 and 24.9 emerged in 1998 in the 2 to 4 weeks following sampling, Alloxysta sp. emerging a little later than D. rapae. From 12.8 to 10.9 and from 8.10 to 9.12, there were no mummies; an invasion of the cabbage white fly left little room for other insects. Even though, on 8.4, all species of parasitoids and hyperparasitoids were present on the overwintered crop, only D. rapae was present on the new crop from the beginning of the season (10.6), accompanied by a few rare specimens of Aphidius spp. and Alloxysta sp. After that, D. rapae developed rapidly attaining 112 individuals per plant by 1.7. The hyperparasitoid complex increased during the same period, Alloxysta sp. reaching a maximum before A. suspensus and P. aphidis. A. suspensus was the dominant hyperparasitoid for this year. The hyperparasitoids caused Aphidius spp. to disappear as from 15.7, Praon sp. from 30.7 and D. rapae from 12.8. There was a certain resemblance between the situations on 15.7 and 30.7.1998 and those of 22.7 and 5.8.1997.

Discussion

In our trial, D. rapae and A. matricariae emerged from mummies of B. brassicae and M. persicae, in addition to A. ervi from M. euphorbiae. Nevertheless, the outstanding predominance of D. rapae is due, above all, to the parasitoid's specificity. D. rapae has a particularly cosmopolitan distribution with over 60 host species listed (Pike et al., 1999). However, there is such a difference between values of the biological parameters of the various parasitoid populations that biotypes are thought to exist (Bernai and Gonzalez, 1993, 1997), whose genetic subdivisions would correspond to the host profile (Vaughn and Antolin, 1998). In central Europe, D. rapae uses the cabbage aphid as principal host, on which its genetic diversity is the greatest, and other aphids as spare or occasional hosts. This capacity to pass from one aphid to another contributes to keeping a relatively 292

stable population of D. rapae and counterbalances adverse events, such as pesticide treatments, harvesting or disturbed habitats (Pike et al., 1999). The cabbage aphid B. brassicae, the Boat gall aphid Hayhurstia atriplicis (L.), the European asparagus aphid Brachycorynella asparagi (Mordvilko), the Russian wheat aphid Diuraphis noxia (Mordvilko) (not present in Switzerland; G. Goy, pers. comm.) and, under certain conditions related to the spatial distribution of plant hosts, cereal aphids are all frequently cited as D. rapae hosts. D. rapae, on the other hand, does not seem to parasitise M. euphorbiae (Hafez, 1961; Vater, 1971; Gabrys et al., 1997; Nemec and Stary, 1984; Elliot et al., 1994; Pike et al., 1999). A. matricariae parasitises 40 aphid species (Giri et al., 1982). M. persicae is well accepted as a host, which is not the case for M. euphorbiae (Quentin et al., 1995). In the palaearctic region, A.ervi is evenly distributed and also shows a wide genetic variability which may lead to geographic sub-species (Takada and Tada, 2000). Its centre of genetic diversity is represented by the pea aphid Acyrthosiphon pisum Harris. On the nettle aphid Microlophium carnosum (Bckt.) and the grain aphid Sitobion avenae L., this parasitoid shows much less polymorphism. This centre is unintentionally upkept by man's activities (Nemec and Stary, 1983a, b, 1984). The different parameters contributing to parasitoid competitivity, such as the zero threshold of development, the number of degree-days necessary for one generation, fertility, the sex-ratio, and the capacity for finding a host, do not allow A. matricariae, A. ervi and Praon sp. to gain ground in relation to D. rapae. In the relations between different parasitoids, superparasitism and multiparasitism cannot be excluded. The former concerns descendants of the same parasitoid species and is rarely of importance except during short periods when hosts are few. When it occurs, only one single adult emerges from each aphid attacked. Multiparasitism concerns descendants of different parasitoid species and may lead to the elimination by competition of one species by another and have long term effects on parasitoid composition (Chow and Mackauer, 1984 ). As far as banker plant quality is concerned, the turnip would not appear to be a avourable host plant for aphids in general. As the cultivation period is short, plant quality diminishes rapidly and leaf pilosity may also be unfavourable to aphid development. Savoy cabbage, on the other hand, is capable of supporting large populations of aphids which are already hosts to parasitoids at the start of the season. Up until June, parasitoids are made available for surrounding crops. Later, the multitrophic system evolves in a different way according to the year and also provides a source of hyperparasitoids, undesirable for biological control. The cabbage aphid seems to be a better coloniser than green aphids. This can be expressed by the number of cabbage aphids/green aphids at certain times of the year, such as the start of colonisation and at peak populations. The host plant gradient is the following: cauliflower > Savoy cabbage >turnip. When banker plants are sown one month before cauliflower planting, mummies are obtained on the former two to three weeks earlier than on the latter (1996 and 1998). A difference of 15 days is insufficient since mummies appear on the banker plants and on the cauliflower at the same time (1997). In the first case, banker plants play the role of supplying parasitoids to the aphids which then invade the cauliflower. This benefit is, however, relative since hyperparasitoids were found in the first emergences of 10.6.1998 from Savoy cabbage.

293

Aphid-parasitoid evolution

1996 Parasitism peaks on the Savoy cabbage closely followed those of the cabbage aphid. The number of mummies fell off after 25.7 and the rate of mummification from 8.8, in spite of an increase in the cabbage aphid. In the cereal agrosystem, this lack of D. rapae is described as an "escape" phenomenon: there are several reasons for this. Aphid honeydew acts as kairomone for D. rapae, directing it towards aphid colonies (Budenberg, 1990; Du et al., 1996, 1997, 1998; Green and Ayal, 1998; Guerrieri et al., 1999; Birkett et al., 1000). D. rapae's foraging time can be positively correlated with honeydew quantity and, consequently, the number of aphids attacked increases. Nevertheless, whenever the number of aphids in a colony exceeds a certain level, the absolute number of aphids attacked stops increasing and the parasitoid leaves the colony or even the plant. Thus, parasitism rates in small colonies can be extremely high (90%), but decrease rapidly to only 15% in larger colonies. Moreoever, each contact with aphids which have already been attacked has a negative effect on foraging time (Shaltiel and Ayal, 1998; Green and Ayal, 1998). In addition, as soon as hyperparasitoids become abundant, parasitoids also leave the area (Höller et al., 1993). This dispersion is induced by the production of a pheromone by the female of Alloxysta victrix (Micha et al., 1993). By dispersing to other habitats containing less hyperparasitoids, the parasitoids have more chance of reproducing. This behaviour is partly responsible for its limited effectiveness in the control of aphids when hyperparasitoid density rises (Höller et al., 1994 ). On the cauliflower, aphid presence was overwhelmed by D. rapae and remained relatively discrete. Although at harvest-time traces of B. brassicae were found on 5% of cauliflower heads, this was of no economic consequence. D. rapae develops more slowly than B. brassicae. However, the parasitoid has a better reproduction potential than the cabbage aphid (Hafez, 1961; Sedlag, 1964; Akinlosotu, 1977).

1997 In spite of B. brassicae's earlier activity on the Savoy cabbage, parasitism still managed to haIt the first two population risings of the pest. The number of mummies decreased from 22.7 and the rate of mummifaction fell off sharply from 2.9 until the end of the season. At this moment, the cabbage aphid’s presence was lower than in 1996, probably due to the increasing presence of the cabbage white fly which invaded plants. A gradual build-up of B. brassicae on the cauliflower around mid-June was progressively contained by D. rapae. At harvest-time, no B. brassicae were found on the vegetable heads.

1998 On the overwintered Savoy cabbage plants, cabbage aphid presence was already high and continued on the new crop. From 1.7, parasitism struck out at the rapid multiplication so that aphids began to decline together with the number of mummies. After 15.7, a decrease in the rate of mummification was also seen. After this, development was disturbed by the cabbage whitefly domination. At "Les Fougères", the situation in cauliflowers was similar to that of 1997: there were even more mummies and parasitism was higher at the end of the season. The limited length of the crop growth period resulted in a loss of vigour in the aphid colonies, due mainly to diminishing nutritive qualities of the plant, so that there was no second build-up to threaten the vegetable market value. At harvest-time, there were no B. brassicae on the cauliflower heads. In the cauliflower crop at the ECA, and in spite of larger aphid populations, parasitism coped with the pests and plant heads were free from B. brassicae at harvesting. 294

Parasitoid-hyperparasitoid evolution Hyperparasitoid density can become so high that D. rapae is locally exterminated. Such an extinction of parasitoids and also of hyperparasitoids took place from mid-September to the end of October 1997 on the Savoy cabbage. D. rapae returned around mid-November and was caught up by Alloxysta sp. around mid-December. In 1998, parasitoids had already been exterminated on 12.8, followed by hyperparasitoids about two weeks later. After this time, development was perturbed by the cabbage whitefly's omnipresence.

1996 In its final larval stage inside the aphid mummy, D. rapae goes into diapause. Probably at about the same time, in September, Alloxysta sp. also begins to go into diapause on the Savoy cabbage. Nevertheless, in the 13.11 sampling of mummies, there was still 2.5% of D. rapae emerging in the same year whereas Alloxysta sp. entered into 100% diapause from the end of October. During the observed period, Alloxysta sp. was the most successful of hyperparasitoids and appears to be the best adapted to D. rapae. Observations of a few hyperparasitoid individuals showed that, by mid-October at the latest, A. suspensus was already in diapause, whereas P.aphidis hibernated from September. On the whole, hyperparasitoids were in total diapause before D. rapae which could then take advantage of this situation by continuing to parasitise aphids to the end of the season. The sexual female of the cabbage aphid represents the final stage of the year where D. rapae can lay its egg (Hardie et al., 1994). In order to attract winged male aphids, the female emits a sexual pheromone of which the major composant is (4aS, 7S, 7aR) - nepetalactone (a cyclopentanoid terpene). D. rapae is equally attracted by this pheromone which may then be used as a supplementary signal in finding a host for the winter when it is dispersed in small colonies across the field (Gabrys et al., 1997). Similar phenomena are known with A.ervi (Glinwood et al., 1999a, b) and P. volucre (Lilley et al., 1994a, b). Late in the season, parasitism takes on a practical importance insomuch as the parasitoid larva reach their final larval stage and transform the host into mummy before the bad weather to avoid perishing with the host during the winter. In effect, D. rapae is active above temperatures of 12.7°C and lays eggs from 14°C (Sedlag, 1964). Under conditions in the Valais and if the autumn weather were clement sexual forms could appear at the end of September and the beginning of October allowing D. rapae to develop up to a stage capable of hibernating. Reference to the literature (Bernal and Gonzalez, 1995) can be made for thermal requirements of development. Emergence of D. rapae and Alloxysta sp. is staggered out over quite a long period so that generations are not well separated. The difference in emergence between the first and the second was two weeks for hibernating mummies stocked in emergence boxes, and about three weeks on plants at the end of winter. Thus, the first parasitoids appeared as from 6.3 at a time when crops are not yet established which means that this advance over hyperparasitoids cannot be exploited. Once crops are in place, hyperparasitoids have also begun to emerge from the mummy stocks. Wintering banker plants close to future crops would thus tend to have a negative effect.

1997 Diapause began for D. rapae and Alloxysta sp. after 2.9 and was complete from 11.11. The lack of mummies for the period between these two dates prevents greater precision. Alloxysta sp. was the most commonly occurring hyperparasitoid. The difference in emergence between D. rapae and Alloxysta was about 4 weeks for overwintered mummies stocked in emergence boxes. The first parasitoids appeared as from 295

25.2. On plants, however, there were not enough emergences at the end of winter to establish a clear difference.

1998 Because plants were overrun by the cabbage whitefly leaving little room for other insect species, there were no data for this year concerning the diapause. The first valid emergence data came from the first samples which showed a rapid progression of D. rapae which, in turn, was rapidly hampered by hyperparasitoids. At one point, A. suspensus and P. aphidis outnumbered Alloxysta sp. Development continued, however, in spite of the latter, up to the end of June or early July at the latest. In some Aphidiinae, induction of the diapause may be influenced by length of day, temperature or even host plant quality, and can be stronger in host aphids which are oviparous than in those which are virginiparous. This would permit the parasitoid to adapt to his host's cycle (Polgar et al., 1991; Hardie et al., 1993; Polgar et al., 1995; Christiansen-Weniger and Hardie, 1997, 1999). The longevity of the Aphidiinae is shorter than that of hyperparasitoids. It is about 2 weeks at the beginning of spring and about 1 week in mid-summer for D. rapae (Hafez, 1961); about 7 to 8 days (Giri et al., 1982) or 13.9 days under optimal conditions in the laboratory in the presence of hosts for A. matricariae (Shalaby and Rabasse, 1979); and no more than 5 days for A.ervi (Ives and Settle, 1996). Charips sp., on the other hand, can live 34 days and P. aphidis can live about 60 days (Vater, 1971). To give a further idea, Asaphes vulgaris males can live about 43 days at 20°C and the females about 92 days (Brodeur and McNeil, 1994 ). This difference in longevity gives an advantage to hyperparasitoids, giving them greater independance to cope with a temporary loss of host. Synchronisation between parasitoids and hyperparasitoids proved to be good in the studied agroecosystem which meant that hyperparasitism could establish itself and progress quickly. Given that ecto-hyperparasitoids parasitise the Aphidiinae at a more advanced stage, they appeared after endohyperparasitoids. On the overwintered Savoy cabbages left in the field, both parasitoids and hyperparasitoids were found right at the start of the growing season (4.3.1997; 11.3.1998). This leads to the question of whether it would not be better to completely destroy crop remains in the autumn so as not to facilitate hibernation of hyperparasitoids. Since D. rapae has good host-prospecting faculties and its foraging zone is greater than that of Alloxysta brassicae (Chua, 1979), sowing banker plants in an environment free from overwintered host plants would allow it some time to safely establish new colonies on aphids before the arrivaI of hyperparasitoids. Active dispersion by flight is of importance to D. rapae and Alloxysta sp. and probably also to P. aphidis and Asaphes spp. D. rapae has an advantage over hyperparasitoids because it can be transported at the egg and L1 stage by winged, parasitised aphid hosts whose flying capacity is not reduced. This passive transport is doubly advantageous for the parasitoid since finding a host becomes unnecessary and a spatial coincidence with the aphid is assured (Vater, 1971 ).

Conclusions (Freuler et al., 2001b)

– D. rapae largely dominates the aphid parasitoid community with > 90% in general on Savoy cabbage. Green aphids do not arrive regularly before B.brassicae to be able to favour A.matricariae, A.ervi and Praon sp. 296

– The Savoy cabbage presents attractive qualities as a banker plant on condition that it is sown a month before cauliflower planting. In this way, mummies are obtained on the cabbage 2 to 3 weeks before the cauliflower. – D. rapae activity is hindered from the beginning of July by hyperparasitoids by which it is rapidly overrun. It is therefore important to destroy banker plants at the same time as ploughing the cauliflower field after harvesting, so that hyperparasitoid populations are not perpetuated. – D. rapae has good prospecting faculties and its foraging zone is greater than that of Alloxysta sp. At the beginning of the season, this means that it is temporarily safe from hyperparasitoids while exploring new crops with growing aphid colonies. – According to observations made in central Valais from 1992 to 1999, cauliflower heads are free from aphids at harvest-time when planting takes place between the second half of May and the beginning of June with a length of growing period < 70 days. Indeed, within this time period, D. rapae is still in its ascending phase while B.brassicae is in a descending phase.

References

Akinlosotu T.A., 1977. Effect of temperature on some biological activities of the cabbage aphid Brevicoryne brassicae (Homoptera: Aphididae) and its primary parasite Diaeretiella rapae (Hymenoptera: Aphidiidae). Nigerian Society for Plant Protection: NSPP 7th Annual Conference Proceedings: 41. Armand E., Lyoussoufi A. & Rieux R., 1991. Evolution du complexe parasitaire des psylles du poirier Psylla pyri et Psylla pyrisuga (Homoptera: Psyllidae) en vergers dans le Sud- Est de la France au cours de la période hivernale, printanière et estivale. Entomophaga 36(2): 287-294. Bernal J. & Gonzalez D., 1993. Temperature requirements of four parasites of the Russian wheat aphid Diuraphis noxia. Entomol. exp. appl. 69: 173-182. Bernal J. & Gonzalez D., 1995. Thermal requirements of Diaeretiella rapae (M'Intosh) on Russian wheat aphid (Diuraphis noxia Mordwilko, Hom., Aphididae) host. J. Appl. Ent., 119: 273-277. Bernal J. & Gonzalez D., 1997. Reproduction of Diaeretiella rapae on Russian wheat aphid hosts at different temperatures. Entomol. exp. appl. 82: 159-166. Birkett M.A., Campbell C.A.M., Chamberlain K., Guerrieri E., Hick A.J., Martin J.L., Matthes M., Napier J.A., Pettersson J., Pickett J.A., Poppy G.M., Pow E.M., Pye B.J., Smart L.E., Wadhams G.H., Wadhams LK.J. & Woodcock C.M., 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proceedings of the National Academy of Sciences of the United States of America 97(16): 9329-9334. Borgemeister C. & Poehling H.-M., 1990. Einfluss von Primär- und Hyperparasitoiden auf die Populationsdynamik von Getreideblattläusen – Ergebnisse zweijähriger Untersuchungen im Raum Hannover. Mitt. Dtsch. Ges. allg. angew. Ent. 7(4-6): 555-562. Bradburne R.P. & Mithen R., 2000. Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica. Proc. R. Soc. Lond. B 267: 89-95. Brodeur J. & McNeil J.N., 1994. Life history of the aphid hyperparasitoid Asaphes vulgaris Walker (Pteromalidae): possible consequences on the efficacy of the primary parasitoid Aphidius nigripes Ashmead (Aphidiidae). Can. Ent. 126: 1493-1497. Budenberg W.J., 1990. Honeydew as a contact kairomone for aphid parasitoids. Entomol. Exp. appl. 55(2): 139-148. 297

Chow F.J. & Mackauer M., 1984. Inter- and intraspecific larval competition in Aphidius smithi and Praon pequorum (Hymenoptera: Aphidiidae. Can. Ent. 116, 1097-1107. Christiansen-Weniger P. & Hardie J., 1997. Development of the aphid parasitoid, Aphidius ervi, in asexual and sexual females of the pea aphid, Acyrthosiphon pisum, and the blackberry-cereal aphid, Sitobion fragariae. Entomophaga 42(1/2), 165-172. Christiansen-Weniger P. & Hardie J., 1999. Environmental and physiological factors for diapause induction and termination in the aphid parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae). Journal of Insect Physiology 45(4): 357-364. Chua T.H., 1979. A comparative study of the searching efficiencies of a parasite and a hyperparasite. Res. Popul. Ecol. 20: 179-187. Du Y.J., Poppy G.M. & Powell W., 1996. Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. Journal of Chemical Ecology 22(9): 1591-1605. Du Y.J., Poppy G.M., Powell W. & Wadhams L.J., 1997. Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). Journal of Insect Behavior 10(4): 509-522. Du Y.J., Poppy G.M., Powell W., Pickett J.A., Wadhams L.J. & Woodcock C.M., 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of Chemical Ecology 24(8): 1355-1368. Elliot N.C., French B.W., Reed D.K., Burd J.D. & Kindler S.D 1994. Host species effects on parasitization by a syrian population of Diaeretiella rapae M'Intosh (Hymenoptera: Aphidiidae). Can. Ent 126: 1515-1517. Freuler J., Fischer S., Ançay A. & Mittaz C., 2001a. Efficacité comparée de quelques insecticides contre le puceron cendré du chou. Revue suisse Vitic. Arboric. Hortic. 33(2): 89-97. Freuler J., Fischer S., Mittaz C. & Terrettaz C., 2001b. Le rôle des plantes relais pour renforcer l'action de Diaeretiella rapae principal parasitoide du puceron cendré du chou. Revue suisse Vitic. Artboric. Hortic. 33(6): in print. Gabrys B., Gadomski H.J., Klukowski Z., Pickett J.A., Sobota G.T., Wadhams L.J. & Woodcock C.M., 1997. Sex pheromone of cabbage aphid Brevicoryne brassicae: identification and field trapping of male aphids and parasitoids. Journal of Chemical Ecology 23(7): 1881-1890. Giri M.K., Pass B.C., Yeargan K.V. & Parr J.C., 1982. Behavior, net reproduction, longevity, and mummy-stage survival of Aphidius matricariae (Hym. Aphidiidae. Entomophaga 27(2): 147-153. Glinwood R.T., Smiley D.W.M., Hardie J., Pickett J.A., Powell W., Wadhams L.J. & Woodcock C.M., 1999a. Aphid sex pheromones: manipulation of beneficial insects for aphid population control. 9th International congress of pesticide chemistry, London, UK, 2-7 August 1997; Pesticide Science 55(2): 208-209. Glinwood R.T., Du Y.-J. & Powell W., 1999b. Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi. Entomol. exp. appl. 92: 227-232. Grasswitz T.R. & Reese B.D., 1998. Biology and host selection behaviour of the aphid hyperparasitoid Alloxysta victrix in association with the primary parasitoid Aphidius colemani and the host aphid Myzus persicae. BioControl 43: 261-271. Green R.F. & Ayal Y., 1998. A simple Markov model for the assessment of host patch quality by foraging parasitoids. Oecologia 116(4): 456-466. Guerrieri E., Poppy G.M., Powell W., Tremblay E. & Pennacchio F., 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. Journal of Chemical Ecology 25(6): 1247-1261. 298

Hafez M., 1961. Seasonal fluctuations of population density of the cabbage aphid, Brevicoryne brassicae (L.), in the Netherlands, and the role of its parasite, Aphidius (Diaeretiella) rapae (Curtis). T. Pl.-ziekten 67: 445-548. Hardie J., Hick A.J., Höller C., Mann J., Merritt L., Nottingham S.F., Powell W., Wadhams L.J., Witthinrich J. & Wright A.F., 1994. The responses of Praon spp. parasitoids to aphid sex pheromone components in the field. Entomol. Exp. appl. 71(2): 95-99. Höller C., Borgemeister C., Haardt H. & Powell W., 1993. The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. Journal of Animal Ecology 62(1), 12-21. Höller C., Micha S.G., Schulz S., Francke W. & Pickett J.A., 1994. Enemy-induced dispersal in a parasitic wasp. Experientia 50(29): 182-185. Ives A.R. & Settle W.H., 1996. The failure of a parasitoid to persist with a superabundant host: the importance of the numerical response. Oikos 75(2): 269-278. Krespi L., Dedryver C.-A., Creach V., Rabasse J.-M., Le Ralec A. & Nenon J.-P., 1997. Variability in the Development of Cereal Aphid Parasitoids and Hyperparasitoids in Oceanic Regions as a Response to Climate and Abundance of Hosts. Environ. Entomol. 26(3): 545-551. Kuo-Sell H.-L., Holtusen C., Quentin M., Wieduwilt A. & Wilhelms A., 1989. Wechsel- wirkungen zwischen Getreideblattläusen (Homoptera: Aphididae) und Parasitoiden (Hymenoptera: Aphidiidae) und ihre Bedeutung für die Blattlaus-Bekämpfung in Winter- weizen. Med. Fac. Landbouww. Rijksuniv. Gent 54/3a: 883-893. Lilley R., Hardie J. & Wadhams L.J., 1994a. Field manipulation of Praon populations using semiochemicals. Norwegian Journal of Agricultural Sciences, supp. 16: 221-226. Lilley R., Hardie J., Powell W. & Wadhams L.J., 1994b. The aphid sex pheromone: a novel host location cue for the parasitoid Praon volucre. Proceedings Brighton Crop Protection Conference, Pests and Diseases 3: 1157-1162. Lopez E.R., Van Driesche R.G. & Elkinton J.S., 1990. Rates of parasitism by Diaeretiella rapae (Hymenoptera: Braconidae) for cabbage aphids (Homoptera: Aphididae) in and outside of colonies: why do they differ? J. Kans. Entomol. Soc. 63: 158-165. Micha S.G., Stammel J. & Holler C., 1993. 6-methyl-5-heptene-2one, a putative sex and spacing pheromone of the aphid hyperparasitoid, Alloxysta victrix (Hymenoptera: Alloxystidae). European Journal of Entomologgy 90(4): 439-442. Müller C.B. & Godfray H.C.J., 1998. The response of aphid secondary parasitoids to different patch densities of their host. BioControl 43: 129-139. Nemec V. & Stary P., 1983a. Genetic polymorphism in Aphidius ervi Hal. (Hym., Aphidiidae), an aphid parasitoid on Microlophium carnosum (Bckt.). Z. ang. Ent. 95: 345-350. Nemec V. & Stary P., 1983b. Electro-morph differentiation in Aphidius ervi Hal. (Hym., Aphidiidae) biotypes on Microlophium carnosum (Bckt.) related to parasitization on Acyrthosiphon pisum (Harr.). Z.ang.Ent. 95: 524-530. Nemec V. & Stary P., 1984. Population diversity of Diaeretiella rapae (M'Int.) (Hym., Aphidiidae), an aphid parasitoid in agroecosystems. Z. ang. Ent. 97: 223-233. Nguyen T.X., Delvare G. & Bouyjou B., 1984. Biocénose des psylles du poirier (Psylla pyri L. et Psylla pyrisuga Forster) dans la région Toulousaine, France. IOBC wprs Bulletin 7(5): 191-197. Pike K.S., Stary P., Miller T., Allison D., Graf G., Boydston L., Miller R. & Gillespie R., 1999. Host Range and Habitats of the Aphid Parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) in Washington State. Environ. Entomol. 28(1): 61-71.

299

Polgar L., Mackauer M. & Völkl W., 1991. Diapause induction in two species of aphid parasitoids: the influence of aphid morph. J. Insect Physiol. 37: 699-702. Polgar L., Darvas B. & Völkl W., 1995. Induction of dormancy in aphid parasitoids: implications for enhancing their field effectiveness. Agriculture, Ecosystems and Environment. 52(1): 19-23. Quentin U., Hommes M. & Basedow T., 1995. Untersuchungen zur biologischen Bekämpfung von Blattläusen (Hom., Aphididae) an Kopfsalat im Unterglasanbau. J. Appl. Entomol. 119(3): 227-232. Sedlag U., 1964. Zur Biologie und Bedeutung von Diaeretiella rapae (McIntosh) als Parasit der Kohlblattlaus (Brevicoryne brassicae L.). Nachrichtenbl. Pflanzenschutzd. DDR 18(4): 81-86. Shalaby F.F. & Rabasse J.M., 1979. On the biology of Aphidius matricariae Hal. (Hymeno- ptera: Aphidiidae), parasite on Myzus persicae (Sulz.) (Homoptera. Aphidae). Annals of. Agricultural Science, Moshtohor 11: 75-97. Shaltiel L. & Ayal Y., 1998. The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations. Ecol. Entomol. 23(3): 319-329. Takada H. & Tada E., 2000. A comparison between two strains from Japan and Europe of Aphidius ervi. Entomol. Exp. Appl. 97(1): 11-20. Vater G., 1971. Über Ausbreitung und Orientierung von Diaeretiella rapae (Hymenoptera, Aphidiidae) unter Berücksichtigung der Hyperparasiten von Brevicoryne brassicae (Homoptera, Aphididae). Zeitschrift für Angewandte Entomologie 68(2): 187-225. Vaughn T.T. & Antolin M.F., 1998. Population genetics of an opportunistic parasitoid in an agricultural landscape. Heredity 80(2): 152-162. Vinson S.B., 1976. Host selection by insect parasitoids. Annual Review of Entomology 21: 109-133. 300

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 301-305

The use of onion sets as „trap plants” to protect onion seed against insect pest

I. Wiewióra & I. Łuczak Department of Plant Protection, Agricultural University of Cracow, Al. 29 Listopada 54, 31-425 Krakow, Poland

Abstract: Three cultivars of onion sets (Armstrong F1, Wolska, Hyton F1) differing in the attractiveness to Lilioceris merdigera, Ceutorrhynchus suturalis, Acrolepiopsis assectella, and Thripidae were tested as „trap plants” planted around of the plots of onion grown from seed. The applied cultivars of onion grown from seed (Red Baron, Sochaczewska, Wolska) also differed in a degree of infestations by the same pests. Each plot of the onion from seed was surrounded by a single row of onion sets (9 plots x 2 replications). The plots of onion from seed without surrounding rows of onion sets were estimated, too. The present experiment showed that the use of onion sets as „trap plots” always reduced number of L. merdigera, C. suturalis, and Agromyzidae. The highest reduction in the number of these pests (80% for Lilioceris and 50% to 70% for Ceutorrhynchus and Agromyzidae) was found on onions from seed surrounded by onion sets of cv. Hyton F1. The use of onion sets as „trap plots” did not decrease the percentage of infestation of onion seedlings by Acrolepiopsis assectella and Thripidae.

Key words: onion sets, cultivars, „trap plots”, protection, onion seed, pests

Introduction

Insect pests feeding on above-ground onion parts includes such species as leek moth (Acrolepiopsis assectella), onion weevil (Ceutorrhynchus suturalis), thrips (Thripidae) and Agromyzidae. Since 1980 the onion crops in southern and south-eastern Poland are being increasingly deteriorated from onion beetles Lilioceris merdigera L. (Łuczak, 1997; 1993 b). Under field conditions onion grown from sets is attacked by beetles and larvae of Lilioceris considerably earlier (end of May – beginning of June) and to larger extent than onion grown from seed (Łuczak, 1993 b). This allows onion sets to be used as “trap plants” to protect onion grown from seed (Łuczak, 1993 c). An advantageous effect of onion sets on reducing degree of infestation for Lilioceris has been shown by Łuczak (1993 a). In further investigations (Wiewióra & Łuczak, 2001) the differences in attractiveness (to Lilioceris) have been found for various onion set cultivars. The same authors (unpublished data) have indicated similar differences in attractiveness to Ceutorrhynchus, Acrolepiopsis i Tripidae. One can conclude that reduction in L. merdigera and other onion pests resulting from using onion sets as “trap plants” should depend on attractiveness to insects a given cultivar of onion sets. The problem has been discussed in detail in this paper.

Material and methods

The investigations have been carried out at the Experimental Station in Mydlniki near Kraków in 2001. The three cultivars of onion sets, namely Armstrong F1, Wolska and Hyton F1) , which differ in attractiveness to L. merdigera, C. suturalis, A. assectella and Thripidae have been tested as “trap plants” on seedling onion fields (Table 1). There were differences in

301 302

degree of infestation by the same pests for onion cultivars grown from seed (Red Baron, Sochaczewska, i Wolska) (see Table 2).

Table 1. The cultivars of onion sets tested in 2001 as ″trap plants″. Degree attractiveness to L. merdigera was defined on the basis of the results published by Wiewióra & Łuczak (2001). The attractiveness to another pests (C. suturalis, A. assectella and Thripidae ) was defined from study of the same author′s (unpubl. data ).

Degree of attractiveness ∗ to: Cultivar L. C. A. Thripidae merdigera suturalis assectella

Armstrong F1 1 1 2 1 Wolska 2 2 1 2 Hyton F1 3 3 3 3 ∗ 1 – low, 2 – average, 3 – high

Table 2. The cultivars of onion grown from seed tested in 2001. Degree of infestation was defined on the basis of the results published by Łuczak & Wiewióra (2001).

Degree of infestation ∗ by : Cultivar L. C. A. Thripidae merdigera suturalis assectella Red Baron 1 1 2 3 Sochaczewska 2 2 3 2 Wolska 3 3 1 1 ∗ 1 – low, 2 – average, 3 – high

Each seedling onion field was of 8,4 m2 (4 m length x 2,1m width) in surface area and included plants grown in 6 rows. 9 test fields (x 2 repetitions) of onion grown from seed protected with a single row of onion sets were used. 80 onion sets (spaced every 15 cm) were planted around each test field. Observations have included also 3 fields (x 2 repetitions) of onion grown from seed with no protection. Occurrence of Lilioceris merdigera was observed in June and July. Field plants were inspected twice a week. The presence of eggs, larvae and adult Lilioceris was recorded. The frequency of pest occurrence on onion grown from seed (without sets) and protected with sets was compared. Occurrence of C. suturalis and A. assectella as well as Thripidae and Agromyzidae was based on percentage (%) of seedlings infested by pests. To do it every week (in June and July) the plant samples were taken to perform laboratory analysis of leaf interiors with a binocluar. Each analysis included 30 onion seedlings for any cultivar.

303

Results and discussion

In 2001 Lilioceris was most often (i.e. 6 times) recorded on seedlings of Wolska cultivar – without onion sets (Table 3). The population of Lilioceris was always reduced by using onion sets as “trap plants”. The largest reduction in occurrence of this pest was observed on onion seedlings protected with sets of Hyton F1 (found to be of high attractiveness to L. merdigera). The results presented in Table 3 support an introductory hypothesis mentioned above that reduction in population of Lilioceris on onion grown from seed by using “trap plants” depends on attractiveness to this insect for onion set used for protection purposes. The use of onion sets of high attractiveness to L. merdigera (specified by Wiewióra & Łuczak, 2001) can provide effective seedling protection as shown by Łuczak (1993 a).

Table 3. Occurrence of Lilioceris merdigera on onions grown from seed (without onion sets) and with use of onion sets as „ trap plants ” in 2001.

Frequency of occurrence of Lilioceris ∗ with onion sets Onion seed without onion cv. cv. cv. sets Armstrong F1 Wolska Hyton F1 ( 1 ) ( 2) ( 3 ) Red Baron ( 1 ) 2 0 0 0 Sochaczewska ( 2 ) 4 3 2 0 Wolska ( 3 ) 6 4 3 1 ∗ - Number of records of Lilioceris during 12 inspections Legends: (1), (2), (3) – as in Tables 1 and 2

In the year under investigation very large numbers of Ceutorrhynchus suturalis were observed. The seedling onion fields (without onion sets) were infested up to 33,3% (Wolska) to 13,3% (Red Baron) (Table 4). It has been found that seedling infestation was reduced considerably (i.e. by 50%) only if onion sets of Hyton F1 were used as “trap plants”. The use of Armstrong F1 set had no significant effect on population of Ceutorrhynchus.

Table 4. Occurrence of Ceutorrhynchus suturalis on onions grown from seed (without onion sets) and with use of onion sets as ″trap plants″ in 2001.

Maximum % of seedlings with Ceutorrhynchus with onion sets Onion seed without onion cv. cv. cv. sets Armstrong F1 Wolska Hyton F1 ( 1 ) ( 2 ) ( 3 ) Red Baron ( 1 ) 13.3 13.3 6.7 6.7 Sochaczewska ( 2 ) 26.7 20.0 13.3 10.0 Wolska ( 3 ) 33.3 26.7 20.0 16.7 Legends: (1), (2), (3) – as in Tables 1 and 2

304

Table 5. Occurrence of Acrolepiopsis assectella on onions grown from seed (without onion sets) and with use of onion sets as „ trap plants” in 2001.

Maximum % of seedlings with Acrolepiopsis with onion sets Onion seed without onion cv. cv. cv. sets Wolska Armstrong F1 Hyton F1 ( 1 ) ( 2 ) ( 3 ) Wolska ( 1 ) 0 0 0 0 Red Baron ( 2 ) 13.3 6.7 6.7 6.7 Sochaczewska ( 3 ) 13.3 13.3 10.0 10.0 Legends: (1), (2), (3) – as in Tables 1 and 2

Table 6. Occurrence of Thripidae on onions grown from seed (without onion sets) and with use of onion sets as „trap plants” in 2001.

Maximum % of seedlings with Thripidae with onion sets Onion seed without onion cv. cv. cv. sets Armstrong F1 Wolska Hyton F1 ( 1 ) ( 2 ) ( 3 ) Wolska ( 1 ) 0 0 0 0 Sochaczewska ( 2 ) 0 0 0 0 Red Baron ( 3 ) 6.7 6.7 6.7 6.7 Legends: (1), (2), (3) – as in Tables 1 and 2

Table 7. Occurrence of Agromyzidae on onions grown from seed (without onion sets) and with use of onion sets as „trap plants” in 2001.

Maximum % of seedlings with Agromyzidae with onion sets Onion seed without onion sets cv. cv. cv. Wolska Armstrong F1 Hyton F1 Sochaczewska 13.3 10.0 6.7 6.7 Wolska 20.0 20.0 13.3 6.7 Red Baron 33.3 26.7 20.0 23.3 Legends: (1), (2), (3) – as in Tables 1 and 2

Onion seedlings were rarely infested by Acrolepiopsis assectella. The Wolska cultivar remained untouched by this pest (Table 5). The use of onion sets as “trap plants” had only minute effect on population of Acrolepiopsis. Thrips occurred in large numbers on Red Baron only (Table 6). The onion set protection had no effect on these insects.

305

In 2001 onion seedlings were highly infested by larvae of Agromyzidae (Table 7). The largest infestation was observed for Red Baron (33,3% - on unprotected fields and slightly lower on fields protected with sets). It should be concluded that an application of onion sets for protecting onion grown from seed reduces population of Lilioceris merdigera, Ceutorrhynchus suturalis and Agromyzidae on onion seedlings. The largest reduction (80% for Lilioceris, and from 50% to 70% for Ceutorrhynchus suturalis and Agromyzidae) has been found for onion set of Hyton F1 of high attractiveness to Lilioceris, Ceutorrhynchus and Agromyzidae. In addition it has been indicated that the use of onion sets as “trap plants” have no effect on population of leek moth and thrips.

References

Łuczak, I. 1992: Noxiousness of onion beetle (Lilioceris merdigera L.) to onion (Allium cepa L.). Folia Hort. 6 (1): 83-93. Łuczak, I. 1993 a: The effect of growing methods and onion (Allium cepa L.) cultivars on the occurrence of the onion beetle (Lilioceris merdigera L.). Folia Hort. 5 (2): 33-41. Łuczak, I. 1993 b: The threat of onion beetle Lilioceris merdigera L. (Coleoptera, Chrysomelidae) to onion grown from seed and sets in Southern Poland. Roczn. Nauk Roln., ser. E 23 (1/2): 61-66. Łuczak, I. 1993 c: The protection of onion grown from seed against Lilioceris merdigera L. (Coleoptera, Chrysomelidae) by the use of the onion sets. Roczn. Nauk Roln., ser. E 23 (1/2): 67-73. Łuczak, I. & Wiewióra, I. 2001: Susceptibility of different cultivars of onion grown from seed to pest infestations. Veg. Crops Res. Bull. 54/1: 163-167. Wiewióra, I. & Łuczak, I. 2001: The attractiveness of different cultivars of onion (Allium ssp.) grown from sets to onion beetle (Lilioceris / Crioceris / merdigera L.). Veg. Crops Res. Bull. 54/1: 159-162.

306

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 307-314

T. Bukovinszky1, M.J. Brewer2, K. Winkler1, H. Trefas1,3, L.E.M. Vet1,4 & J.C. van Lenteren1

1 Wageningen University and Research Centre, Laboratory of Entomology, Wageningen 6700 EH, The Netherlands. 2 University of Wyoming, Renewable Resources-Entomology 3 Szent István University, Department of Crop Protection, Gödöllõ, Hungary 4 Netherlands Institute of Ecology, Centre for Terrestrial Ecology, Heteren, The Netherlands

Abstract: We studied the effects of flowering field margins on flight activity of the diamondback moth (Plutella xylostella L.) and its parasitoids Diadegma spp. in Brussels sprout fields (Brassica oleracea cv gemmifera var. Icarus), twice during the summer of 2000. We also compared the effect of vertical position of traps on insect counts, to investigate movement of insects within the field margin and field. Diamondback moth adults were attracted to flowering field margins. There was an increase in moth counts with increasing distance from the field edge. Flowers adjacent to the field influenced this pattern in the second observation period; as overall density of the moths inside the field was higher when flowering margins were present. Traps at higher position within the margin (level of flowers), caught more moths, than traps at lower position, whereas within-field field catches were higher in traps placed lower (canopy of plants) than in traps just above the canopy. However, this tendency changed to the opposite in the second observation period. Spatial patterns in catches of Diadegma spp. were in general similar to those of the diamondback moth. Although there was an increase in counts with increasing distance from the field edge, parasitoid counts over distance were not significantly influenced by the flowering field margin. Within the fields, traps at a lower position caught consistently more individuals then traps at a higher position. This finding suggests that this species is indeed a specialist in cruciferous habitats and its flight activity within the crop is restricted to the plant canopy. Results show that flowering field margins may act as trap crops by attracting populations of specialist herbivores, a reason to this might have been the high abundance of Sinapis alba in the margin. Field margins also increased pest densities in adjacent fields. Vertical position of traps affects efficiency of catches, and may influence the reliability of detection and estimation of herbivore and parasitoid populations.

Keywords: Plutella xylostella, Diadegma spp., Sinapis alba, flowering field margin, habitat manipulation

Introduction

Diamondback moth Plutella xylostella (L.) is the most important insect pest of cruciferous crops throughout the world (Talekar and Shelton, 1993). The costs of chemical control and the increasing resistance against pesticides urges the development of alternative control methods against this pest (Charleston and Kfir, 2001). Diadegma semiclausum (Hellén) and

307 308

Diadegma fenestrale (Holmgren) (Hymenoptera: Ichneumonidae) are two of its few parasitoids and can be major mortality factors of the diamondback moth (Waage, 1983). However, their efficiency is often low in newly planted cruciferous habitats, because their host is often better able to establish itself (Talekar and Shelton, 1993). The goal of habitat management is to create a suitable infrastructure within the agricultural landscape by selectively providing resources for beneficial natural enemies to enhance natural control of pests (conservation biological control). A way to provide pollen/nectar sources for parasitoids, is to establish flowering field margins. Such margins may accumulate natural enemies of pests and increase their efficiency as control agents in adjacent fields. However, when herbivores can make use of them, field margins may also increase pest problems (Landis et al., 2000), raising interest in composing field margins selectively for pest control (Baggen et al., 1999). As cyclic colonisation of annual agroecosystems by herbivores and their parasitoids is a scale dependent process, the spatial dynamics of pests and beneficials in and around fields is an important issue in the establishment of flowering field margins (Bowie et al. 1999). Our aim was to study the effects of flowering field margins on spatial distribution of the diamondback moth and its parasitoids Diadegma spp. in Brussels sprout fields (Brassica oleracea cv gemmifera var. Icarus). We compared the effect of vertical position of traps on insect counts, to investigate where insect movement took place in the field margin and within the field.

Materials and methods

Experimental design Experiments were carried out on four Brussels sprout (Brassica oleracea var gemmifera cv. Maximus) plots (50mx80m) in the vicinity of Wageningen (The Netherlands) during the summer of 2000. The experimental site was located in a woodland area dominated by oak. Plots were isolated by a path of mown grass (mixture of Lolium spp. and Poa spp.) of at least 10m at each side. Flowering field margins (4mx50m) were established on the southwestern side of two of the plots in the direction of prevailing wind. Flowering field margins were composed of 27 plant species known to be used by insects as pollen and nectar source (Frei and Manhart, 1992, Table 1.). The time of flowering and percentage of cover by each plant species were monitored once a week in 10 randomly chosen square meters per flowering margin. Control plots were surrounded by mown grass on all sides.

Sampling insect populations To monitor flight activity of the diamondback moth and its parasitoids Diadegma spp., we coated clear plastic circular traps (h=21cm, d=9cm) with transparent adhesive (Tanglefoot®), affixed them to a cane and placed them within the field margin and adjacent field. Traps were set to the height of the canopy of Brussels sprout plants (15cm above ground) and just above the canopy (50cm above ground) at four different distances from the field edge. The first trap line was placed within the field edge (0.75m from the border of the field), a second at 0.75m, a third at 6m, and a fourth line at 15m into the B. sprout field. Each trap line contained 3 traps of both vertical positions. We set the traps out in the field twice; in the periods of 5th of July - 13th of July (week 27-28) and 19th of July – 26th of July (week 29-30). Traps were collected at the end of each sampling period, and were taken to the laboratory for identification of the specimens.

309

Data analysis Before the analysis, insect counts were value + 1 transformed. A general linear model for analysis of variances was built to detect sources of significant variation between groups (SPSS 8.0). Each sampling period was analysed separately.

Results and discussion

During the observation period 5 to 11 plant species flowered in the field margins (Table 1), the dominant species were white mustard (Sinapis alba) and buckwheat (Fagopyrum esculentum).

Table 1. The period of flowering and the percentage of cover of plant species recorded within the field margin during the summer season.

Plant species % Week cover 27 28 29 30 Anthemis tinctoria 1 Arthemis arvensis 1 Borago officinalis 1 Capsella bursa-pastoris 1 X X X X Centaurea cyanus 2-5 Chenopodium album 5 Erodium cicutarium 1 X X X X Fagopyrum esculentum 10 X X X X Galeopsis sp. 1 X X X Galinsoga parviflora 1 Matricaria chamomilla 1 Matricaria inodora 1 Matricaria matricarioides 1 Medicago lupulina 1 Papaver rhoeas 1 Plantago lanceolata 1 X Plantago major 1 X X Polygonum persicaria 2-5 Sinapis alba 30 X X X X Solanum nigrum 1 X Sonchus arvensis 1 Spergula arvensis 1 X Stellaria media 1 X Trifolium incarnatum 2 Trifolium pratense 2 Veronica arvensis 1 X X X Viola arvensis 1 X X X X

X- indicates flowering

Diamondback moth adults were attracted to the flowering field margins (Table 2). Host plant allelochemicals are known to influence host location by the diamondback moth. The

310

olfactory attraction of the diamondback moth to volatiles from the white mustard (Brassica hirta) has been demonstrated earlier (Palaniswamy and Gillot, 1986).

Table 2. Statistics (General Linear Model) on the effects of type of field margin, trap position, distance from edge of field and trap line on numbers of diamondback moth (Plutella xylostella L.) adults in the first (a) and second (b) sampling periods. Non- significant interactions are omitted from the model. a) Source of variation Type III SS df MS F P Field edge 6.22 1 6.22 4.72 0.0327 Position 52.99 1 52.99 40.24 <0.0001 Distance 30.81 3 10.27 7.79 0.0001 Trap Line 4.42 2 2.21 1.68 0.1932 Field edge x Distance 27.86 3 9.29 7.05 0.0003 Position x Distance 28.32 3 9.44 7.17 0.0003 Error 108.01 82 1.32 b) Source of variation Type III SS df MS F P Field edge 126.65 1 126.65 21.01 0.0002 Position 48.64 1 48.64 8.07 0.0056 Distance 178.83 3 59.61 9.89 <0.0001 Trap Line 5.29 2 2.65 0.44 0.6463 Field edge x Position 39.17 1 39.17 6.49 0.0126 Error 524.51 87 6.03

It is known to be attracted to, and sustain feeding and reproduction on Sinapis alba (Talekar and Shelton 1993). Although the flowering field margin might have acted as a trap crop in the field, it also increased overall density of the moths inside the field. Although catches inside the fields were not different between the treatments in the first sampling period (P=0.814; Fig.1.), the number of moths in fields with flowering margin was higher than in the control plots in the second sampling period (P=0.001; Fig. 2.). Trap line did not influence abundance of the diamondback moth, whereas distance of traps from the field edge had a significant spatial effect (Table 2a.b.) in both sampling periods. More moths were caught with increasing distance from the edge both in the treatment and the control plots (Fig. 1.). Distribution of moths over distance were different in the plots with flowering margin then in the ones without, as interaction term between the type of field margin and distance was significant (Table 2a., Fig. 1.), although this tendency was not present in the second sampling period. Within the flowering margins traps at higher position (at the level of flowers, Fig. 1a., 2a.), caught more moths, than traps at lower position (Fig 1b., 2b.), which may be explained both by oviposition preference within a plant and foraging for nectar sources. The accessibility of nectar from flowers of buckwheat as food source for diamondback moth adults has been demonstrated (Winkler in prep.). Within the field lower traps caught more moths in the first week than upper ones, but this tendency changed to the opposite in the second observation period (Table 2b.).

311

Fig. 1. Mean (± SE) number of diamondback moth caught in traps placed high (above) and low (below.) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the first sampling period.

Most of the Diadegma spp. specimens caught belonged to D. semiclausum; the other, less abundant species found was D. fenestrale. Spatial patterns in catches of Diadegma spp. were similar to those of the diamondback moth (Fig.3a.b.). Within-field catches of Diadegma spp. were not different between the treatments in the first sampling period (P=0.307), but catches inside the fields with flowering margin were higher in the second sampling period (P<0.001). There was an increase in counts with increasing distance from the field edge (Table 3.). Trap line did not influence parasitoid distribution, but vertical position of traps did (Table 3.). Inside flowering margins traps at higher position (Fig. 3a.) caught more wasps, than traps at lower position (Fig 3b.). Specialist parasitoids may use infochemicals from the plant level to find their host (Vet and Dicke, 1992). Diadegma insulare prefers to search on wild cruciferous plant species over cultivated ones (Fox and Eisenbach, 1992). It is possible that Diadegma spp. were also attracted to field edges due to the presence of Sinapis alba, although this assumption needs further study. Since the nectar of buckwheat and Sinapis alba is accessible for D. semiclausum, these plant species may also provide food for these parasitoids (Winkler in prep.). Further studies are required to explain similarities in the distribution pattern of Diadegma spp. to that of its host and to see how far field margins exert their effects in adjacent crop fields.

312

Fig. 2. Mean (± SE) number of diamondback moth caught in traps placed high (above) and low (below) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the second sampling period.

Table 3. Statistics (General Linear Model) on the effects of type of field margin, trap position, distance from edge of field and trap line on numbers of Diadegma spp. in the first (above) and second (below) sampling periods. Non-significant interactions are omitted from the model.

Source of variation Type III SS df MS F P Field edge 0.08 1 0.08 0.161 0.689 Position 20.32 1 20.32 42.59 <0.0001 Distance 9.41 3 3.14 6.57 0.0005 Trap Line 2.44 2 1.22 2.56 0.0833 Position x Distance 9.85 3 3.28 6.88 0.0003 Error 40.56 85 0.48

Source of variation Type III SS df MS F P Field edge 21.69 1 21.69 33.16 <0.0001 Position 63.65 1 63.65 97.31 <0.0001 Distance 17.14 3 5.71 8.73 <0.0001 Trap Line 0.47 2 0.23 0.36 0.7016 Field edge x 5.62 1 5.62 8.59 0.0044 Position Position x Distance 23.57 3 7.86 12.01 <0.0001 Error 54.94 84 0.65

313

Fig. 3. Mean (± SE) number of Diadegma spp. caught in traps placed high (above) and low (below) in Brussels sprout fields, at different distances from the border. Grey bars are fields with flowering margin, white bars are fields without flowers in the first sampling period.

Inside the field, traps at a lower position (level of canopy) caught consistently more individuals (Table 3, Fig. 3). Within-field distribution of catches of wasps suggest that this species is indeed a specialist in cruciferous habitats and its flight activity within the crop is restricted to the plant canopy. These results show that flowering field margins may act as trap crop by attracting pest populations. However, trap crops may increase pest problems in adjacent fields when not accompanied by appropriate management practices (Hokkanen, 1991). Therefore the floral composition of field margins is an important factor to establish pest suppressive habitats, and management practices should be adjusted accordingly. Differences in the vertical position of traps have a great impact on efficiency of catches, and may influence reliability of detection and estimation of herbivore and parasitoid populations.

Acknowledgements

This project is financed by the Netherlands Organisation for Scientific Research (NWO- ALW, project number: 014-22.031). The help of Yde Jongema in the identification of insect material is acknowledged. The authors thank the experimental farm of Wageningen University and Research Centre (UNIFARM) for the maintenance of the experimental fields.

314

References

Baggen, L.R., Gurr, G.M. and Meats, A. 1999. Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol. Exp. Appl. 91: 155-161. Bowie, M.H., Gurr, G.M., Hossain, Z., Baggen, L.R. and Frampton, C.M. 1999. Effects of distance from field edge on aphidophagous insects in a wheat crop and observations on trap design and placement. Int. J. Pest Manage. 45: 69-73. Charleston, D.S. and Kfir, R. 2001. The possibility of using Indian mustard, Brassica juncea, as a trap crop for the diamondback moth, Plutella xylostella, in South Africa. Crop Prot. 19: 455-460. Fox L.R. and Eisenbach J. 1992. Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia. 89: 574-579. Frei, G. and Manhart, C. 1992. Nützlinge und Schädlinge an künstlich angelegten Ackerkraut- streifen in Getreidefeldern. Verlag Paul Haupt, Bern: 140 pp. Hokkanen, H.M.T. 1991. Trap cropping in pest management. Annu. Rev. Entomol. 36: 119- 38. Landis, D.A., Wratten, S.D. and Gurr, G.M. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45: 175-201. Palaniswamy, P. and Gillot, C. 1986. Attraction of diamondback moths, Plutella xylostella (L.) (Lepidoptera: Plutellidae), by volatile compounds of canola, white mustard, and faba bean. Can. Entomol. 118: 1279-1285. Talekar, N.S. and Shelton, A.M. 1993. Biology, ecology, and management of the Diamondback moth. Annu. Rev. Entomol. 38: 275-301. Vet, L.E.M. and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37: 141-172. Waage, J. K. 1983. Aggregation in field parasitoid populations: foraging time allocation by a population of Diadegma (Hymenoptera: Ichneumonidae). Ecol. Entomol. 8: 447-453.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 315-319

The effect of winter cover crops on occurrence of some pests in cauliflower and cabbage

S. Kotliński Research Institute of Vegetable Crops, Skierniewice, Poland

Abstract: Impact of winter cover crops mulch on pests in cauliflower and late type of white cabbage production was investigated in polish conditions. In 2000, the number of Brevicoryne brassicae L. on cauliflower, growing on plots with cover crops mulch, was significantly less than on plots with bare soil. In 2001, on late type of white cabbage, growing on plots with cover crops mulch was less aphids Brevicoryne brassicae L and caterpillars Pieris rapae L. than in bare soil. The differences in number of Pieris brassicae L. and caterpillars of Plutella maculipennis Curt. on plots with cover crops and without cover crop were not observed

Key words: sustainable agriculture, cover crops, mulch, Brevicoryne brassicae, Pieris rapae, Pieris brassicae, Plutella maculipennis

Introduction

The conventional production system of vegetables depends heavily on pesticides to control pests. Like synthetic fertilizers, pesticides have become a major source of contamination to the environment particularly to surface and ground water. Sustainable agriculture allows reducing applying of pesticides, herbicides and mineral fertilizers. Growing of vegetables in mulch of cover crops is one of the methods of sustainable agriculture. This method eliminates also ploughing soil before planting of vegetable crops. In Poland was evaluated usefulness of following plants as winter cover crops: hairy vetch (Vicia villosa Roth), rye (Secale cereale L.), crimson clover (Trifolium inkarnatum L.) These plants were sown in two kinds of mixture: rye plus hairy vetch and rye plus hairy vetch plus crimson clover. Biomass yield, expressed in tons per hectare of cover crops dry matter, was diverse in years of investigations. Yield of biomass ranged from 6,7 to 14,4 tons. In biomass yield were significant content of nitrate from 71 to 308 kg/ha, potassium from 150 to 406 kg/ha and less amounts of other macronutrients. Large amount of organic mulch inhibited development of weeds for about two months after vegetables planting (Kotliński 2000, 2001, Kotliński and Abdul-Baki 2000). During years of trials with cover crops the number of Delia radicum was variable. In the trial the cover crops were applied for three years. In the third year of trial was observed significant reduction of larvae and pupa of Delia radicum on cauliflowers grown on plots with cover crops mulch in comparison to bare soil (Kotliński at al., 2000). In another year when cauliflowers cultivated on plots, on which cover crops were applied first year, the differences were not significant (Kotliński 2001). It is known, that fertilisation, some of chemical compounds in the plants can have influence on susceptibility to pests and diseases. For example, the higher level of nitrogen fertilization applied in tomatoes production caused the increase of greenhouse whitefly (Trialeurodes vaporariorum) population (Jauset 2000).

315 316

The damages caused by Phytophthora infestans on tomato leaves were lower on plots with mulch of cover crops by 21-59 % in comparison to plots with bare soil (Kotliński and Abdul-Baki 2000). The cruciferous plant residues decreased Sclerotium cepivorum on onion and Fusarium oxysporum on tomato (Smolińska 2000). These data indicate that cultivation of vegetable crops in mulch of cover crops can have influence on damages caused by pests and diseases.

Materials and methods

The trial was carried out in four replications, using as cover crops hairy vetch, rye, crimson clover and mixture of hairy vetch plus rye and hairy vetch plus rye plus crimson clover. The combinations are given in tables 1-6. The cover crops were sown September 5 - 15. The cover crops was cutting from May 25 to June 5. After that, on plots with mulch or in bare soil the plants of cauliflower or cabbage have been planted. The field experiment with cauliflower located at Research Institute of Vegetable Crops in Skierniewice and private farm in Lubiczów near Warsaw. In both places carried out the observation of aphid Brevicoryne brassicae population on cauliflower growing on plots with cover crops mulch and bare soil (Tables 1 and 2).

Table 1. Number of Brevicoryne brassicae L. on cauliflower growing on plots with bare soil and with winter cover crops mulch. Skierniewice 2000

Aphids Aphids [number] [%] Cover crops July 7, July 21, July 7, July 21, 2000 2000 2000 2000 Bare soil 69,3 40,2 100 100 Rye + hairy vetch 30,4 19,9 43,9 49,5 Rye + hairy vetch + crimson clover 25,4 10,5 36,6 26,1 Rye + hairy vetch + crimson clover+herb. 35,1 13,2 50,6 32,8 LSD 0.05 25,9 23

Table 2. Number of Brevicoryne brassicae L. on cauliflower growing on plots with bare soil and with winter cover crops mulch. Lubiczów, July 14, 2000.

Dose Aphids Cover crops N kg/ha Number % Bare soil 100 21,6 100 Rye + hairy vetch 50 1,2 5,5 Rye + hairy vetch 100 4,7 22,8 LSD 0.05 9,2

317

In Lubiczów two levels of nitrate fertilizations (50 and 100 kg N/ha) on plots with cover crops mulch were applied. Besides that, in Skierniewice were two combinations with hairy vetch plus rye plus crimson clover. One of combinations was treated by herbicide Butisan Star 416 SC in 10 days after cauliflower planting. The trials with late type of white cabbage was carried out in 2001 at Lubiczów near Warsaw and at Breeding Company PlantiCo Strugi. In these trials were evaluated the appearance of Brevicoryne brassicae, Pieris rapae, Pieris brassica and Plutella maculipennis on cabbage plants on plots with cover crops mulch and with bare soil (Table 3-6).

Results

In the trial at Lubiczów with cauliflower growing on plots with cover crops mulch observed significantly less number of B. brassicae than on plots with bare soil (Table 2). The dose of nitrate fertilisers had not significant influence on number of B. brassicae on cauliflower growing in cover crops mulch. In spite of that on plots with cover crops, on which applied bigger dose of nitrate fertilisers observed not large increase of aphid number (Table 2). In Skierniewice stated significant decrease of B. brassicae population on cauliflower plants growing on cover crops mulch in comparison to bare soil (Table 1). The differences in the numbers of B. brassicae between the plots with mulches of rye plus hairy vetch, rye plus hairy vetch plus crimson clover and rye plus hairy vetch plus crimson clover additionally treated by herbicide Butisan Star 416 SC were insignificant (Table 1).

Table 3. Number of Brevicoryne brassicae L. on cabbage growing on plots with bare soil and with winter cover crops mulch. Strugi, July 5, 2001.

Aphids Aphids Cover crops number %

Bare soil 421,5 100 Hairy vetch 16,5 3,9 Rye + Hairy vetch 13,8 3,3 Rye 0 0 Crimson clover 26,5 6,3 Rye + Hairy vetch + Crimson 0 0 clover LSD 0.05 114,9

In both experiments with white cabbage, it was noticed significantly less numbers of B. brassicae in all plots with cover crops in comparison to plots on bare soil (Table 3 and 4). In these trials, the number of Pieris rapae caterpillars was also significantly less on cabbage plants growing on plots with cover crops (Table 5 and 6). There were insignificant differences 318

in the number of aphid B. brassicae and Pieris rapae caterpillars on cabbage plants growing on plots with mulches of different of cover crops. The differences were insignificant in case of caterpillar’s number of P. brassica and P. maculipennis independently of combinations.

Table 4. Number of Brevicoryne brassicae L. on cabbage growing on plots with bare soil and with winter cover crops mulch. Lubiczów, July 14, 2001.

Aphids Aphids Cover crops number % Bare soil 370,5 100 Hairy vetch 6 1,6 Rye + Hairy 0 0 vetch Rye 0 0 LSD 0.05 253,5

Table 5. Number of Pieris rapae L. on cabbage growing on plots with bare soil and with winter cover crops mulch. Strugi 03.08.2001

Caterpillars Caterpillars Cover Crops number % Bare soil 24.5 100 Hairy vetch 7.5 30.6 Rye + Hairy vetch 2.8 11.4 Rye 1.3 5.3 Crimson clover 1.8 7.3 Rye + Hairy vetch + Crimson 2.8 11.4 clover LSD 0.05 6.6

Table 6. Number of Pieris rapae L. on cabbage growing on plots with bare soil and with winter cover crops mulch. Lubiczów, August 1, 2001.

Caterpillars Cover crops Caterpillars % number Bare soil 26.7 100 Hairy vetch 12.0 44.9 Rye + Hairy 13.2 49.4 vetch Rye 10.5 39.3 LSD 0.05 8.0 319

References

Jauset, A.M., Sarasua M.J., Avilla, J. & Albajes, R. (2000). Effect of nitrogen fertilization level applied to tomato on the greenhouse whitefly. Crop Protection 19: 255-261 Kotliński, S. (2000). Rośliny okrywowe w produkcji warzyw a możliwości ograniczenia chemizacji. Ogólnopolska Konf. Zwalczanie chorób i szkodników warzyw polowych. 10.08.2000 (in Polish) Kotliński, S. & Abdul Baki, A. (2000). Rośliny okrywowe w uprawie pomidora a porażenie liści przez zarazę ziemniaka Phytophthora infestans. [The influence of winter cover crops in tomato production on damages caused Phytophthora infestans.] Progress in Plant Protection / Postępy w Ochronie Roślin. Poznań 40 (2) 895-898. Kotliński, S. (2001). Przydatność ozimych roślin okrywowych w uprawie warzyw. Mat.Ogólnop. Konf. Naukowej: Biologiczne i agrotechniczne kierunki rozwoju warzywnictwa. Skierniewice, 21 – 22.06.2001: 82-83. Kotliński, S., Szwejda, J., Smolińska, U. & Abdul-Baki, A. (2000). Wpływ roślin okrywowych na skład mikrobiologiczny gleby i stopień porażenia kalafiora przez śmietkę kapuścianą Hylemya brassicae Bche. [The influence of organic mulch on soil microflora and cauliflower root attack by Hylemya brassica Bche.]. Progress in Plant Protection / Postępy w Ochronie Roślin. Poznań 40 (2): 897- 900. Smolińska, U., (2000). Survival of Sclerotium cepivorum sclerotia and Fusarium oxysporum chlamydospores in soil amended with crucifeorous residues. J. Phytopathology 148: 343- 349. 320

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 321-324

Economic importance and the control method of Thrips tabaci Lind. on onion

B. Nawrocka Research Institute of Vegetable Crops, 96-100 Skierniewice, Poland

Abstract: During the last decade an increase of the population size of Thrips tabaci Lind. has been evidenced in onion crops in Poland. Onion thrips is a pest as important as onion fly and both species should be controlled obligatory every year. The control is most effective when treatments are executed on the turn of the first ten days of June (2 treatments at an interval of 7 days) and the at the stage, when 50% onion tops have folded down (2 treatments, as above).

Key words: Thrips tabaci, onion, population dynamic, control

Introduction

Since 1985 Thrips tabaci is considered as a one of a important pest of onion in Poland. Damage caused by thrips in onion crops shorten the growing season and in consequence caused losses in the yield. Recently, a tendency to the increase of density of T. tabaci populations on onion is observed and the importance of the pest is growing. The paper presents the changes in population density of T. tabaci and describes some novelties in the control on onion.

Material and methods

Population dynamics The experiments were conducted over1996 to 2001 in the Research Institute of Vegetable Crops at Skierniewice. To determine the population dynamics of T. tabaci on onion, 50 plants randomly chosen from a 200 m2 field were inspected every week for the number of trips living on each of them. The observation began at the 3-leaves stage of onion plants and lasted to the end of onion growing season.

Control of thrips The experiments of efficiency of some insecticides in controlling T. tabaci on onion were conducted on experimental fields at Skierniewice and Powiercie in 1999 and 2000. The details of the experiments for both locations were as follows: • crop – onion of Wolska cv.; no. of replications – 4; experimental design – randomized blocks; plot size – 10 m2; • evaluation of thrips density – number of living individuals from 25 plants per plot were recorded within 24 hours, as well before the treatment as 3, 7, 10, 14 and 21 days thereafter; • compounds and rates – benfuracarb 120 g ai/ha, chlorpirifos 250 g ai/ha + cypermethrin 25 g ai/ha, diazinon 210 g ai/ha, carbosulfan 150 g ai/ha and untreated plants. In 1999 the plots with onion were drilled on April 15 at Skierniewice and on April 20 at Powiercie, treatment were done in both location on June 7. In 2000 the plots were drilled on April 18 in both location and treatment were done on June 9 at Skierniewice and on June 6 at Powiercie.

321 322

Experiment tending towards determination of the right number of treatments per growing season were conducted in 2000 at Skierniewice. The following combinations were tested: 2 treatments, at an interval of 7 days, were executed on the turn of first days of June (beginning of thrips infestation); 3 treatments, one of them executed at the beginning of thrips infestation and next two, at 7 days interval, executed at the stage when 50% onion tops have folded down; 4 treatments, two of them, at 7 days interval, at the beginning of thrips infestation and next two as above.

Results and discussion

Population dynamic Investigations into the population dynamics of T. tabaci on onion conducted over 1996 to 2001 had shown that the beginning of plant infestation by thrips took place always in second ten days of May and that the pest population reached the highest level between the end of July and middle of August (Fig.1). It corresponds with the flight activity of T. tabaci reported by Richter et al. (1999). Although the population dynamic were similar in all the years examined, the population densities were different. In the peak of population dynamics the density oscillated from below 5 thrips per plant in 1996 and 1997 up to 20 in 2000 and 2001. The tendency to increase the population density of T. tabaci has been evident (Fig.1).

20 1996 1997 1998 15 1999 2000 2001

10 Avg number of living thrips/plant

0 10.5 20.5 30.5 10.6 20.6 30.6 10.7 20.7 30.7 10.8 20.8 30.8 data of observations

Fig. 1. Population dynamics of Thrips tabaci on onion in growing season. Skierniewice 1996 to 2001

Search for control efficiency The tested insecticides controlled T. tabaci very efficiently and all of them can be used to protect onion against trips (Tab.1).

323

Tab. 1. Efficiency of chemical control of Thrips tabaci on onion.

Number of living thrips Mean number of living thrips per plant Treatment per plant in days after treatment before 3 7 10 14 21 treatment Skierniewice 1999 benfuracarb 120g ai/ha 15.9 0.5a* 0.3a 0.1a 0.2a 0.0a chlorpiryfos 250g + cypermethrin 25g ai/ha 12.0 0.2a 0.8a 1.3b 0.2a 0.1a diazinon 210g ai/ha 12.8 0.5a 0.9a 0.6a 0.4a 0.2a carbosulfan 150g ai/ha 15.1 0.7a 0.5a 0.1a 0.1a 0.0a untreated 14.3 13.4b 17.5b 15.7c 17.6b 14.2b Skierniewice 2000 benfuracarb 120g ai/ha 11.4 0.5a* 0.8a 0.1a 0.0a 0.1a chlorpiryfos 250g + cypermethrin 25g ai/ha 10.5 0.6a 0.9a 0.3a 0.0a 0.0a diazinon 210g ai/ha 12.4 0.5a 0.8a 0.6a 0.2a 0.2a carbosulfan 150g ai/ha 10.7 0.2a 0.4a 0.1a 0.0a 0.0a untreated 12.6 13.7b 15.2b 13.5b 17.6b 16.2b Powiercie 1999 benfuracarb 120g ai/ha 5.8 0.3a* 0.7a 0.1a 0.0a 0.0a chlorpiryfos 250g + cypermethrin 25g ai/ha 7.0 0.2a 0.6a 1.3b 0.0a 0.0a diazinon 210g ai/ha 7.8 0.3a 0.3a 0.4a 0.2a 0.2a carbosulfan 150g ai/ha 6.2 0.1a 0.0a 0.2a 0.0a 0.1a untreated 7.3 7.5b 8.9b 10.2c 15.6b 18.4b Powiercie 2000 benfuracarb 120g ai/ha 15.9 0.5a* 0.3a 0.1a 0.2a 0.0a chlorpiryfos 250g + cypermethrin 25g ai/ha 12.0 0.2a 0.2a 0.3a 0.0a 0.1a diazinon 210g ai/ha 10.5 0.6a 0.4a 0.3a 0.2a 0.2a carbosulfan 150g ai/ha 14.7 0.4a 0.5a 0.1a 0.0a 0.1a untreated 14.3 13.4b 14.5b 15.7b 17.6b 17.5b * The number with the same letter are not significantly different

In protecting onion against thrips the most effective frequency was two couples of treatments per growing season, each couple executed at an interval of 7 days in the turn of the first ten days of June and then at the stage when 50% of tops have folded down, respectively (Fig. 2c). This number of treatments correspond with that of the supervised method of controlling thrips, reported by Richter et al. (1999) and van de Steene (1999).

References

Richter, E., Hommes, M. & Krauthausen, J.H., (1999) Investigations on the supervised control of Thrips tabaci in leek & onion crops. IOBC wprs Bulletin 22 (5): 61-72. Steene Van de, F., (1999) Monitoring and control of Thrips tabaci Lind. with furathiocarb in leek fields. IOBC wprs Bulletin 22 (5): 235-240.

324

Untreated plants 20 chlorpirifos 250g ai/ha + cypermethrin 25g ai/ha 15

10 treatment

5 Mean number of living thrips / plant A

0 10.5 20.5 30.5 10.6 20.6 30.6 10.7 20.7 30.7 10.8 20.8 30.8 Observation data

20 Untreated plants

chlorpirifos 250g ai/ha + 15 cypermethrin 25g ai/ha

Mean number of living thrips / plant B

0 10.5 20.5 30.5 10.6 20.6 30.6 10.7 20.7 30.7 10.8 20.8 30.8 Observation days

untreated plants 20 chlorpirifos 250g ai/ha hi 25 15

5 Mean number of living thrips / plant C 0 10.5 20.5 30.5 10.6 20.6 30.6 10.7 20.7 30.7 10.8 20.8 30.8 observation data

Fig 2. Efficiency of chemical control of Thrips tabaci applied at different time and with different number of treatment in growing season. Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 325-330

The effect of broad bean cultivars sowing time on the occurrence of Aphis fabae Scop. and its predators

E. Wojciechowicz-Żytko Department of Plant Protection, Agricultural University, al. 29-Listopada 54, 31 425 Kraków, Poland

Abstract: In the research on Aphis fabae Scop. and its predators the occurrence and population dynamics of A. fabae as well as the species composition of Syrphidae on broad bean cultivars from different sowing time were studied. The greatest number of aphids was recorded on beans from the first sowing time, the least plant infestation was observed on plants from the latest sowing . The number as well as species composition of syrphids collected from the beans from the first and second sowing time were similar, the least amount of Syrphidae was found on the plants from the third sowing time.

Key words: Aphis fabae Scop., Syrphidae, broad bean, sowing time

Introduction

Aphis fabae Scop. is the main pest of beetroot, poppy, broad bean and field beans regularly causing severe crop losses (Goszczyński et al. 1992; Way et al. 1954). The number of aphids depends on many factors e.g. the weather conditions, broad bean plants sowing time and the occurrence of beneficial insects in these colonies (Wojciechowicz-Żytko 2000.). Aphido- phagous syrphid larvae are the main predatory group influencing the A. fabae population (Sądej, Ciepielewska 1996; Hurej 1982, Wojciechowicz-Żytko 1998a,b;). The aim of investigation was to examine the effect of broad bean cultivars sowing time on the population dynamics of A. fabae and the occurrence of aphidophagous Syrphidae in these colonies.

Materials and methods

The experiment was carried out in the year 2000 at the Experimental Station in Mydlniki near Kraków. Broad bean seeds were sown in 14 03, 30 03 and 14 04. Four cultivars – Windsor Biały, Hangdown Biały, Bachus and Basta were compared. No insecticidal treatment was applied. On each plot (16 m²) ten plants were selected and marked at random. A. fabae colonies not larger than 100 specimens were counted while those larger were roughly estimated. Quantities and seasonal variability as well as species composition of Syrphidae were established by collecting them. Samples were taken every 5-8 days during the growing season. Collected syrphid larvae and pupae were placed in Petri dishes and kept at 20-24ºC. Larvae were daily fed on a diet of A. fabae. The emerged adults were classified based on Bańkowska key (1963).

325 326

Results and discussion

Occurrence of Aphis fabae Scop. On the control plots the appearance of first alate aphids on the broad bean plants was observed in year 2000 in late April/early May. (Fig.1). It corresponds to observations by other authors (Dunning et al. 1984; Sądej, Ciepielewska 1996; Wojciechowicz-Żytko 1999). Their more numerous appearance was observed in mid May. At that time the highest density of aphids was found on the plants from the first sowing time; aphids already established colonies from 200 (Bachus) to 400 (Windsor, Hangdown Biały, Basta) specimens/plant (Fig. 1). From this moment their population rapidly grew in number and reached the peak in late May/early June. In this period the largest aphid colonies exceeding 700-800 specimens/plant were found on the broad bean plants from the first sowing time whereas on the beans from the latest sowing, the highest density reached only 100 (Bachus) and about 200 (Windsor, Hangdown Biały, Basta) aphids/plant (Fig.1). In the end of May broad bean plants from the first sowing time were at the stage of large pods, from the second – at the beginning of pods setting whereas from the third – in full flowering. Due to the high air temperature and the decreasing rainfall resulting in the wilting and drying of plants leaves, from the mid June aphid populations were rapidly decreasing until they disappeared two weeks later. There were no distinct differences in the infestation of various broad bean cultivars by aphids, however the smallest aphid colonies were noted on the Bachus cultivar. In year 2000 the greatest number of aphids was recorded on beans from first sowing time, the least plant infestation was observed on plants from latest sowing.

Occurrence of Syrphidae During the sampling period 94 syrphids larvae belonging to 6 species were collected (Tab. 1).

Table 1. The composition of syrphid species occurred in Aphis fabae Scop. colonies on broad bean cultivars from the different sowing time

Sowing time 14.03.2000 30.03.2000 14.04.2000 Syrphid species Total % Number of syrphid larvae A B C D A B C D A B C D Episyrphus 4 2 4 6 3 3 4 6 4 1 1 2 40 42.6 balteatus Deg. Syrphus ribesii 2 1 1 1 1 1 0 1 0 0 1 0 9 9.6 (L.) Metasyrphus 1 1 2 0 1 0 0 0 2 0 0 0 7 7.4 corollae Fabr. Sphaerophoria 1 2 3 2 2 1 3 2 1 3 2 2 24 25.5 scripta (L.) Scaeva pyrastri 0 0 1 0 0 1 1 1 1 1 0 0 6 6.4 (L.) Epistrophe 2 2 1 0 1 1 1 0 0 0 0 0 8 8.5 bifasciata Fabr. Total 10 8 12 9 8 7 9 10 8 5 4 4 94 100.0 A-Windsor Biały, B-Hangdown, Biały, C-Basta, D-Bachus

327

Windsor n 800 600

400 200

number of aphids/pla 0 30 IV 5V 10 V 16 V 24 V 30 V 5 VI 13 VI 20 VI date

14.03 30.03 14.04

Basta n 800

600 400

200

number of aphids/pla 0 30 IV 5V 10 V 16 V 24 V 30 V 5 VI 13 VI 20 VI date 14.03 30.03 14.04

Bachus

n 800

600

400

200

number of aphids/pla 0 30 IV 5V 10 V 16 V 24 V 30 V 5 VI 13 VI 20 VI date 14.03 30.03 14.04

Hangdown Biały

n 800

600 400

200

number of aphids/pla 0 30 IV 5V 10 V 16 V 24 V 30 V 5 VI 13 VI 20 VI date 14.03 30.03 14.04

Fig. 1. The population dynamics of Aphis fabae Scop. on broad bean cultivars from the different sowing time 328

Syrphid species identified during the experiment were similar to those found by Wojciechowicz-Żytko (1998a; 1998c,) in previous years in A. fabae colonies on broad bean and Hurej (1982), Laska (1959) on sugarbeet. Episyrphus balteatus with percentage contribution about 40% predominated in material gathered. Sphaerophoria scripta was the second most numerous species (about 25%). The remaining species did not occur on each broad bean cultivar. According to Dusek, Laska (1966), Sądej, Ciepielewska (1996) all those species play an essential role in reducing A. fabae populations. There were no distinct differences between the cultivars with respect to number of syrphid occurring in A. fabae colonies (Tab. 2).

Table 2. The occurrence of syrphid larvae in A. fabae colonies on various broad bean cultivars

Sowing Cultivar Total time Windsor H. Biały Basta Bachus 14.03 10 8 12 9 39 30.03 8 7 9 10 34 14.04 8 5 4 4 21 Total 26 20 25 23 94

During the experiment the number of syrphids collected from the beans from the first and second sowing time was similar, the least amount of Syrphidae was found on the plants from the third sowing time (Fig. 2).

12 10 number of 8 syrphids/ 6 10plants 4 3

2 1 2 0 2 1 3 sowing time y ł Basta H.Bia Windsor Bachus broad bean cultivar

Fig. 2. Density of Syrphidae on broad bean cultivars from the different sowing time

On broad bean plants from the earliest sowing time the first syrphid individuals appeared at the beginning of May while on the others 1-2 weeks later (Fig. 3). It was from 10 to 16 days later than first aphids were noted. Afterwards syrphids appeared more numerously and their number has been increasing, reaching its maximum in late May/early June. Later the population showed a declining tendency, completely disappearing in mid June. 329

Windsor

4 3,5 3 2,5 2

plants 1,5 1 0,5 syrphids/10 number of 0 10 V 16 V 24 V 30 V 5 VI 13 VI date 14.03 30.03 14.04

Hangdown Biały

4 3,5 3 2,5 2 1,5 number of 1

syrphids/10 plants 0,5 0 10 V 16 V 24 V 30 V 5 VI 13 VI date

14.03 30.03 14.04

Basta 4 3,5 3 2,5 2 1,5 of number 1

syrphids/10 plants syrphids/10 0,5 0 10 V 16 V 24 V 30 V 5 VI 13 VI date 14.03 30.03 14.04

Bachus 4 3,5 3 2,5 2 1,5 of number 1 syrphids/10 plants syrphids/10 0,5 0 10 V 16 V 24 V 30 V 5 VI 13 VI date 14.03 30.03 14.04

Fig. 3. Number of syrphid larvae in Aphis fabae Scop. colonies on broad bean cultivars from the different sowing time 330

References

Bańkowska, R. 1963. Klucze do oznaczania owadów Polski. Część XXVII. Muchówki- Diptera. Zeszyt 24 Syrphidae, PWN, Warszawa: 236 pp. Dunning, R.A., Graham, C.W. & Light, W.I. st. G. 1984. Black bean aphid. Leaflet, Ministry of Agriculture, Fisheries and Food, UK, 54: 8 pp. Dusek, J. & Laska, P. 1966. Occurrence of syrphid larvae on some aphids. In: Hodek (ed.), Ecology of Aphidophagons Insects. Acad. Prague: 37-38 Goszczyński W., Cichocka E. & Chacińska M. 1992. Aphis fabae Scop. on field beans (Vicia faba sp. minor) – life cycle and the direct harmfulness. Aphids and Other Aphidophagous Insects, PAS, Warszawa 4: 51-57. Hurej, M. 1982. Naturalna redukcja liczebności mszycy trzmielinowo-burakowej Aphis fabae Scop. przez Syrphidae (Diptera) w uprawie buraka cukrowego. Polskie Pismo Entomologiczne 52 (3/4): 287-294. Sądej, W. & Ciepielewska, D. 1996. Occurrence of the black bean aphid (Aphis fabae Scop.) and its predators on broad bean (Vicia faba L. Major). Aphids and Other Aphidophagous Insects, PAS, Skierniewice 5:165-170. Way, M.J., Smith, P.M. & Potter, C.1954. Studies on the bean aphid (Aphis fabae Scop.) and its control on field beans. Ann. appl. Biol 41 (1): 117-131. Weismann, L. & Vallo, V. 1963. Voska makova (Aphis fabae Scop.). Vydavatel'stvo Slovenskej Akademie Vied, Bratislava: 304 pp. Wojciechowicz-Żytko, E. 1998a. Syrphids (Diptera, Syrphidae) as the predators of Aphis fabae Scop. (Homoptera, Aphidoidea) on the broad bean. Aphids and Other Aphidophagous Insects, PAS, Warszawa 6: 89-96. Wojciechowicz-Żytko, E. 1998b. Mszyca Aphis fabae Scop. i jej drapieżcy na różnych odmianach bobu (Vicia faba). Zeszyty Naukowe Akademii Rolniczej w Krakowie, nr 333, Sesja Naukowa z. 57: 329-333. Wojciechowicz-Żytko, E. 1998c. Role of syrphid larvae (Diptera, Syrphidae) in reducing population of Aphis fabae Scop. (Homoptera, Aphidoidea) on broad bean. Acta Horticulturae et Regiotecturae, The First Horticulture Scientific Conference with Foreign Participation, Nitra 23-24 Sepember, vol. 1: 199-200. Wojciechowicz-Żytko, E. 1999. Predatory insects occurring in Aphis fabae Scop. (Homoptera, Aphidoidea) colonies on broad bean (Vicia faba L.). Scientific Works of the Lithuanian Institute of Horticulture and Lithuanian University of Agriculture, Horticulture and Vegetable Growing, Babtai 18 (3): 276-284. Wojciechowicz-Żytko, E. 2000. Występowanie mszycy Aphis fabae Scop. (Homoptera, Aphidoidea) na bobie w zależności od terminu siewu i jej wpływ na plon nasion. Zeszyty Naukowe Akademii Rolniczej w Krakowie, 364, Sesja Naukowa z. 71: 373-376.

331

Ecology of Pest Insects

332

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 331-338

A strategy for the control of carrot psylla (Trioza apicalis Förster) in Switzerland

S. Fischer1 & C. Terrettaz2 1 Swiss Federal Research Station for Plant Production, Changins, 1260 Nyon, Switzerland 2 Office cantonal valaisan de protection des plantes, 1950 Châteauneuf, Switzerland

Abstract: Over the last few years, a general increase of carrot psylla (Trioza apicalis) attacks has been observed in western Switzerland, leading to severe economic losses. Growers generally reacted by intensified sprayings on the young crops. Practical experiments carried out in the lower part of the Rhone Valley over a three-year period have led to a system of supervised control. On a regional level, monitoring of the springtime arrival of the pest is done by extension services, with only 5 yellow sticky traps, placed in a carrot field situated in a reference zone. At first insects detection, growers are informed, and carry out regular visual checks on 10 series of 20 plantlets in each of their fields. The percentage of plantlets with curled leaves is calculated. A comparison of this percentage can then be made with a series of intervention thresholds which have been established, taking into account several rates of yield and expected market prices. Use of this scheme helps to avoid unnecessary chemical treatments. Trials also indicated that, when needed, a single application of λ-cyhalothrine is generally sufficient to control the pest.

Key words: carrot, Trioza apicalis, monitoring, threshold.

Introduction

Over the last few years, a general increase in the carrot psylla attacks has been observed in western Switzerland. In 1997, exceptional damage in several zones of production led to intense applications of treatments on the young crops. In order to get a better control strategy several experiments were carried out between 1998 and 2000 on commercial plots situated in the lower Rhone valley. Since about 10 years there has been a rapid rise in carrot cultivation in this area. On the other hand, the numerous coniferous forests in neighbouring mountains provide very favorable hibernating locations for psylla populations.

Biology of T.apicalis Carrot psylla is univoltine. Adults hibernate in various coniferous species (Pinus, Abies, Picea, Juniperus, etc.) and in spring they migrate towards carrot crops where mating and egg laying take place. Main economic losses are due to the females of this “post-hibernating” generation which, as they feed, inject a substance creating systemic phytotoxaemia. This causes the leaves to curl and a decrease, or even complete stoppage, of plant growth. The intensity of this effects depends on the quantity of toxins injected and thus on the duration of feeding by one or more females on the plant. The stage of host plant is also crucial: the younger the plant, the greater the risk of irreversible damage. Nevertheless, our observations have shown that beyond 4-5 leaf stage, economic risk is over, even when pest pressure remains high. Cotyledons attacked show hardly any symptoms although leaves emerging afterwards may be curled under the latent effect of the pest salivary toxins.

331 332

The nymphs and adults of the new generation cause practically no leaf curling as they feed, indicating that the toxic effect of the saliva is acquired during over-wintering. Migration of the new generation back to the winter host plants usually begins in August.

Materials and methods

Experimental sites The experiments took place in production fields of the lower Rhone valley, at Illarsaz and Colombey, near Leman Lake. Soils are sandy and loamy with water layers close to the surface, thus, carrot sowing takes place on ridges 0.75 m apart, at the rate of 1.3 to 1.5 million seeds per hectare.

Adults immigration monitoring Trapping is efficient for the monitoring of immigrating adults. A trapping post consisted of five sticky yellow plates 20 x 20 cm (Perspex® ICI acrylic glass, n° 229), identical to those used for the carrot rust fly (Psila rosae). The plates were placed vertically in a carrot field at intervals of about 20 m. Catches were counted weekly under a dissecting microscope. As the experience of 1998 showed clearly that a well-placed trapping post was perfectly representative of the pest immigration for the whole region, only one post was running in 1999 and 2000.

Evaluation of practical intervention thresholds Field monitoring method A visual method of checking leaf curling caused by the pest, easily put into practice by growers, was deliberately chosen. By this way, a direct and precise estimation of insect pressure seemed possible because of the almost immediate symptomatic reaction exhibited by the carrot leaves. Sample units consisted of a series of 20 carrot seedlings along a row, the number of plants presenting one or more curled leaves being recorded. This procedure was repeated at least 10 times at various points over the field or the experimental plots (=200 plants monitored) and the mean rate of plants with damaged leaves calculated.

Insecticide sprayings In order to determine action threshold, spraying experiments were carried out with λ- cyhalothrine (Karate®), commonly used by local growers. Commercial product was applied at a dose of 250 ml/ha (12.5 g a.i./ha.) with a brew volume of 450-500 liters/ha, at a pressure of 3 kg/cm2, using a portable compressed air apparatus. A wetting agent (Etalfix®, 0.1%) was added. The experiments took place in commercial carrot fields using ‘Puma F1’ and ‘Navarre 2 F1’ cultivars. The surface area of each unit plot varied from 85 to 500 m . Sprayings were made according to the results of visual checks of the unit plots up to the 4-5 leaf stage. Variants differed by the percentage of seedlings with curled leaves at the time of spraying, and each variant received only one treatment. For technical reasons, the 1998 and 1999 experiments were carried out without replications. In 2000, each variant included 3 replications of 200 m2, randomly disposed in blocks. Table 1 summarizes the experimental set up of the trials. Short time effect of each application has been checked by the rate of damaged plantlets observed 2 weeks after spraying compared with untreated control plots. At the end of the growth period, 5 x 1 m2 samples of roots were harvested from each unit plot, in order to establish the relation between maximum rates of attack on young plants and yield. The roots were sorted according to their size using the following simple criteria: i) marketable (> 60 grams/root), ii) non-marketable (< 60 grams/root). Each lot was counted and

333

weighed. For comparison, visual checks and harvest samplings were made in the same way in surrounding commercial fields.

Table 1. Summary of spraying experiments with lambda-cyhalothrin (Karate®)

Variants: Localities and Carrot Crop stage at Date of rate of plants with curled years cultivars spraying time spraying leaves at spraying time 15 % 2 leaves 16.06 Illarsaz 1998 ‘Puma F1’ 25 % 3 leaves 23.06 Untreated control 20 % 2 leaves 16.06 Collombey 1998 ‘Navarre F1’ 25 % 3-4 leaves 23.06 Untreated control 10 % 3 leaves 29.06 Illarsaz 1999 ‘Puma F1’ 20 % 4 leaves 6.07 Untreated control 3% 2-3 leaves 29.06 Collombey 1999 ‘Puma F1’ 10 % 4 leaves 13.07 Untreated control 10 % 1-2 leaves 20.06 15 % 2-3 leaves 27.06 Illarsaz 2000 ‘Puma F ’ 1 20 % 4 leaves 4.07 Untreated control

Results

Spring immigration During the three-year period of observation, colonization of carrot by psylla began in May, intensified in June, and even continued up to the beginning of July in 1998 (Fig. 1). Our field observations showed that the timing of the first captures coincided perfectly with the appearance of the first curled leaves, even in fields distant from trapping posts. Anyway, visual checking of damage levels is better adapted to producers’ needs than trapping, which is rather complicated and onerous, as it requires dissecting microscope and training for the pest identification. Practically, trapping should only be effected on a single field in a regionally representative zone, as a warning system for notifying producers when to begin visual checks, after which it can be stopped. However, it remains a useful tool in bio-ecological studies of T.apicalis. During the remainder of the season hardly any psylla were caught in traps which means that, once established in the plots, their movements are limited to the crop canopy. Furthermore, the designed trap system did not appear able to clearly detect the new generation flight back towards hibernating sites.

Short-term effectiveness of spraying Determination of short-term effectiveness of treatments is biased, as it concerns only the attack symptoms and not the actual pest mortality. Former unpublished data concerning chemical control trials against T. apicalis have shown that, whatever the active ingredient,

334

effectiveness of spraying on foliage damage is generally limited. These observations are consistent with results reported here. Analysis of the results from trials and from growers’ fields shows an average effectiveness of λ-cyhalothrine of 31% (30.8 ± 2.8%, n = 14; [15 days after treatment]). This poor result is due to the inertia of phytotoxaemia, since removal of the insects does not lead to immediate elimination of salivary toxins and disappearance of symptoms. It was also noted that the crop phenological stage and pest pressure had practically no influence on the effect of treatment. Furthermore, a number of observations in growers’ fields showed that a second treatment would not improve overall effectiveness.

100 Collombey 1998 90 Illarsaz 1999 80 Collombey 2000 70

30 weekly catches / 5 traps . / 5 traps catches weekly 20

0 IV IV V V VI VI VII VII VII VIII VIII IX IX X X XI months

Fig. 1. Catches of T.apicalis adults on yellow sticky traps in the lower Rhone valley, 1998- 2000.

Relationship between damage and harvest yield Table 2 presents the number and weight of marketable roots harvested from treatment experimentation. Yield in sprayed plots were generally higher, although not always significantly, than in untreated control plots, whatever the level of damage reached at spraying time. The economic impact of phytoxaemia results essentially in a reduction in the size of carrot roots. Thus the maximum level of deformations on young plants ought to be directly related to weight of yield per unit surface. This was true of individual experimentation, but no more when one considered an overall analysis of the trials, which brings out a weak relationship between attack levels on seedlings and the weight of marketable roots at harvest (r = -0.389, n = 15). This phenomenon can be explained by the fluctuation of average carrot yields according to fields and years (maturity at harvest, edaphic conditions, watering management, etc.). A much better negative correlation (r = -0.826, n = 15) between maximum damage levels on seedlings and the number of marketable carrots per surface unit is observed (Fig. 2), because of the modern sowing technique, which ensures a very homogenous density of plants.

335

Thus, for each field, evaluation of the rates of yield loss due to psylla attacks is possible (fig 3).

Table 2. Harvest sampling of marketable roots from experimental plots. The variants differed by the percentage of damaged seedlings reached at the time of treatment with λ- cyhalothrine (Karate®). Data followed by a same letter do not show statistically significant difference (p=0.05)

Locat.: Illarsaz Collombey Illarsaz Collombey Illarsaz Years: 1998 1998 1999 1999 2000 Variants: % of ] ] ] ] ] 2 2 2 2 2 damage 2 2 2 2 2 when No./m weight [kg/m weight [kg/m weight [kg/m weight [kg/m weight [kg/m treated No./m No./m No./m No./m 127,8 3% 8,69 a b 134,2 126,0 138,2 12,15 10% 9,60 a 8,85 a a b a a 135,9 12,01 15% 97,8 a 9,67 b a a 7,84 129,2 134,4 12,14 20% 73,4 a 9,85 a ab a a a 11,65 25% 94,0 a 78,4 a 8,44 a a untreated 108,4 110,6 119,8 10,23 69,8 b 7,64 c 68,0 a 6,63 b 8,51 b 6,15 b control b b a a

Proposition for action thresholds Establishing action thresholds necessitates calculating acceptable losses (Derron, 1984) which, in turn, depend on the expected net yield, the wholesale price of marketable roots, the costs of treatment application and the effectiveness of the treatment, according to the formula:

100 ⋅ C L[]% = ⎡()()a ⋅ A ⋅ 100 − e ⎤ a ⋅ A − ⎣⎢ 100 ⎦⎥ Where: L = rate of acceptable yield loss [%] a = wholesale price of marketable roots [SFr or €/kg] A = expected net yield [kg/ha] e = efficacy of spraying [%] C = spraying cost (product + application cost) (SFr or €/ha)

For carrot psylla, the best-defined factors concern treatment. The application costs of Karate® are approximately SFr 120.00 or € 80.00/ha (product: SFr 70.00 or € 45.00; machines and labour: SFr 50.00 or € 35.00). As indicated before, the mean effectiveness of the application is 31%.

336

160

140 y = -1.2218x + 139.44 120 r 2 = 0.683

2 100 80 per m 60

marketable roots 40 20 0 0 102030405060708090100 maximal rate of damaged seedlings (up to 4 leaf-stage)

Fig. 2. Relationship between the rate of seedlings damaged by T.apicalis and the number of marketable roots per sq.meter.

Accurate estimation of future net yields is more difficult. A gross yield of 90 to >100 tons/ha is usual in the lower Rhone valley. In other production regions of Switzerland, carrot yields are more often in the range of 80 tons/ha. Even so, a production of 60 tons/ha is considered satisfactory depending on soil types and root maturity. Anyhow, observations made in the lower Rhone valley indicate net commercial yields (after sorting) of 70% gross yields (mean 69.7 ± 0.4%, n = 11), for a standard “healthy” crop. Similar proportions are observed in other production areas. Greater variations exist in wholesale prices, which can differ between SFr 0.15 (€ 0.10) and SFr 0.40 (€ 0.27) per kg, according to the market demand. Fluctuations in these two latter factors directly influence acceptable losses which, of course, fall off as expected yields and selling prices rise. As standard situations example, table 3 shows admissible losses for 4 different levels of net yield and 6 wholesale price. Rate of losses is shown to fluctuate between 1.4 and 6.4% of marketable root yields.

s 10,0 9,0 8,0 7,0 6,0 5,0 4,0 3,0 2,0 1,0 % loss of marketable root 0,0 1,0 2,0 3,0 4,0 5,0 6,0 7,0 8,0 9,0 10,0

maximum rate of damaged seedlings

Fig. 3. Evaluation of marketable roots loss rate in relation with damaged seedlings.

337

Table 3 also presents a series of pre-calculated action thresholds corresponding to these admissible rates of loss. They are expressed as percentages of deformed seedlings: the less severe corresponds to 7.5% (low yield, low price) and the most severe 1.5% (high yield, high price) of injured plantlets.

Table 3. Pre-calculated acceptable losses, and corresponding action thresholds for 4 net yield and 6 price levels.

Whole sale prices per kg Expected net yield SFr 0.15 0.20 0.25 0.30 0.35 0.40 [kg/ha] € 0.10 0.13 0.17 0.20 0.23 0.27 Acceptable losses 6.4 % 4.8 % 3.9 % 3.2 % 2.8 % 2.4 % [% yield] 40 000 Economic threshold 7.5 % 5.5 % 4.5% 3.5 % 3.0 % 2.5 % [% of damaged seedlings] Acceptable losses 5.2 % 3.9 % 3.1 % 2.6 % 2.2 % 1.9 % [% yield] 50 000 Economic threshold 6.0 % 4.5 % 3.5 % 3.0 % 2.5 % 2.0 % [% of damaged seedlings] Acceptable losses 4.3 % 3.2 % 2.6 % 2.1 % 1.8 % 1.6 % [% yield] 60 000 Economic threshold 5.0 % 3.5 % 3.0 % 2.5 % 2.0 % 1.5 % [% of damaged seedlings] Acceptable losses 3.7 % 2.8 % 2.2 % 1.8 % 1.6 % 1.4 % [% yield] 70 000 Economic threshold 4.0 % 3.0 % 2.5 % 2.0 % 2.0 % 1.5 % [% of damaged seedlings]

Discussion

Our experiments have confirmed that carrot psylla is a very serious pest, requiring appropriate and close monitoring. Insect activity rapidly leads to important yield losses and, consequently, economic thresholds are rather low. Moreover, because of fluctuations in price and yield, thresholds have to be adjusted case by case. The implementation of T.apicalis supervised control in the study area has been achieved and should be tested in other carrot production areas. Local growers are satisfied and confident with the proposed scheme, and have reduced the insecticide treatments in carrot fields from now onward. In practical terms the strategy works as follows: 1. Monitoring of immigrating adults by trapping is carried out by official services. The data produced by a single trapping post (i.e.5 yellow plates) placed strategically in a field

338

known to be in a micro-area highly subject to psylla attacks is relevant for the whole region. As soon as the first catches are recorded, growers are alerted so that they can begin visual sampling in individual fields. 2. This visual sampling of 10 series of 20 successive plants per field of ≤2 ha (or 20 series of 20 plants per field of >2ha) is carried out by growers themselves. The rate of plants exhibiting curled leaves can then be compared with the chosen threshold, depending on expected yield and wholesale price. It requires usually less than 10-15 minutes to check a field. 3. Visual sampling should be done twice a week, as the sanitary situation can change dramatically in a few days because of the rapid action of female toxins. Once the crop reaches 4 leaf stage, checking ceases since the risk of damage becomes negligible. 4. Even if a grower has a “minimalist” approach of supervised control, and reluctant to strictly apply action thresholds, the described monitoring system allows avoidance of out- of-time treatments. Future experiments should include a study of real effects of attacks and control possibilities at the cotyledon stage, since cotyledons do not exhibit symptoms. The effectiveness of other insecticide groups, particularly the natural products agreed for organic farming should also be tested. Furthermore, a better knowledge of the biology and behaviour of T. apicalis, especially concerning migration distances and overwintering locations, would be important particularly in evaluating the pest potential of a new carrot production area.

Résumé

Stratégie de lutte contre le psylle de la carotte (Trioza apicalis) en Suisse

Au cours des dernières années, une augmentation générale des attaques de Trioza apicalis a été constatée dans l’ouest de la Suisse, induisant parfois de graves pertes économiques. En réaction, les maraîchers ont généralement multiplié les traitements insecticides sur leurs jeunes cultures. Des expérimentations pratiques conduites en basse vallée du Rhône, près du lac Léman, ont abouti à leur proposer une stratégie de lutte raisonnée. Au niveau régional, la surveillance de l’immigration printanière du ravageur est effectuée par les services officiels, au moyen d’un seul poste de piégeage (soit 5 plaques engluées jaunes) placé dans un champ de carotte localisé au sein d’une zone de référence. Dès les premières captures, les cultivateurs sont avertis et effectuent des contrôles visuels bihebdomadaires de leurs parcelles, jusqu’à ce que les plantes atteignent le stade phénologique de 4-5 feuilles. Ces contrôles consistent à observer 10 séries de 20 plantules par champ, et permettent de calculer le taux de plantes ayant une ou plusieurs feuilles déformées. Ce pourcentage de dégâts est ensuite comparé à un seuil d’intervention, établi d’après le rendement visé et le prix de vente escompté de la récolte. L’usage de ce schéma permet d’éviter les traitements superflus. Les essais ont également montré que, si nécessaire, une seule application à base de λ-cyhalothrine est généralement suffisante.

References

Derron, J.O. 1984: Seuil de tolérance et techniques intensives. Revue suisse Agric. 16: 59-63.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 339-343

Phytophagous entomofauna of horseradish

J. Szwejda & M. Rogowska Research Institute of Vegetable Crops, ul. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland

Abstract: The studies on the on the qualitative and quantitative composition of phytophagous insects on horseradish crops were carried out in the 1997 and 1999 growing seasons in two different cropping regions in Poland. The experimental field of the Research Institute of Vegetable Crops in Skierniewice was located in the region of intensive cultivation of other cruciferous vegetable crops, such as brassica plants. On the contrary, plantation located around Lipnik village, 150 km from Skierniewice, Sieradz region represented an area of high concentration of horseradish cultivation as the sole cruciferous crop. In total, 5.061 insect specimens were caught, over 90% of all collected insects were as follows: Phyllotreta atra, Ph. undulata, Delia radicum, Athalia rosae, Brevicoryne brassicae and Aphis fabae.

Introduction

The horseradish crop is cultivated in Poland on the largest area in the world reaching recently ča 2100 ha. The tradition of horseradish cultivation is very old and reaching more than 100 years. The largest area (above 95%) is concentrated in the Sieradz district, central part of Poland. Its production has recently been injured by a number of insect pests. Their harmfulness is very high, and it can reach 60 - 70% of lost yield. In the Sieradz region no cruciferous crops other than horseradish are cultivated. In the Skierniewice region on the contrary, brassica vegetables are grown on a large area. Up to the present, field observations on the entomofauna occurring on horseradish have not been regularly carried out not only in Poland but also in other countries with intensive horseradish production.

Materials and methods

Detailed regular field observations were carried out on the experimental field of the Research Institute of Vegetable Crops in Skierniewice and on plantations located near Lipnik village, Sieradz region. Basic information on the methodology used in our studies is presented in the table 1.

Table 1. The agrotechnical details of the field experiments carried out in the 1997 and 1999 growing seasons

No. Specification Skierniewice Lipnik Experimental field Production fields 1. Type of horseradish cultivar Creamy Creamy 2. Length of root seedlings 30cm 30cm 3. Spacing between rows 67.5cm 67.5cm 4. Planting period 2nd decade of April 1st decade of April 5. No. of replications and plot size 4 x 10m2 4 x 15 running m of row 6. Harvest period October October 7. Type of soil Sandy soil Sandy soil

339 340

During the growing period all larvae feeding on the leaves, stems or roots of horseradish plants were collected, and later (besides Homoptera, Heteroptera and Lepidoptera species) reared to adults and identified to species.

Results

In total, 5.061 specimens were collected from horseradish crops: on the Skierniewice plantation - 2967 and the Lipnik plantations – 2094 insects during the vegetation seasons of 1997 and 1999. Twenty species of pests were identified together with other 29 specimens which could not be identified to species (Ceutorhynchus – 15 and Elateridae – 14). The dominants were flea beetles (Phyllotreta spp.) on all plantations, composing 36% (Lipnik) to 83% (Skierniewice) of all collected phytophagous insects. The dominants were also two species: Phyllotreta atra and P. undulata. The subdominants were determined as the following species: Aphis fabae, Brevicoryne brassicae, Pieris brassicae, Plutella xylostella, Athalia rosae and Delia radicum. The flea beetles (Phyllotreta spp.) occurred on the field during the emerging period of plants and feeding in all cases until August always. The peak appearance of aphids (Aphis fabae and Brevicoryne brassicae) took place in June and July; caterpillars of Pieris brassicae and Plutella xylostella were feeding from July to September. Larvae of Athalia rosae were noticed on horseradish plants from August to October. The larvae of cabbage root fly (Delia radicum) were observed feeding on the roots from May to the end of vegetation. Other species as: Thrips tabaci, Lygus rugulipennis, L. punctatus, Eurydema oleracea, Phaedon cochleariae, Pieris rapae, Mamestra brassicae and Plusia gamma occurred in lower numbers during both studied seasons.

Discussion

The above presented species belong to the phytophagous insects commonly occurring not only on horseradish but also on wild and other cultivated cruciferous plants. Both species as: Aphis fabae and Lygus rugulipennis are polyphagous and known to be important pests of many crops. Some of the observed insect species as Phyllotreta armoraciae and Phaedon cochleariae are monophagous. The rest of collected species are oligophagous, feeding on plants belonging to the Brassiceae family. The first species of horseradish pests were recorded in the beginning of 1860, and there were: Pieris brassicae, P. rapae, P. napi, Mamestra brassicae, Plusia gamma and Anthomyia brassicae (Belke, 1861). To the present time the above mentioned species are still important pests occurring every year on horseradish plantations in Poland. The characteristics of collected species is giving below.

Phyllotreta spp. Flea beetles are known as horseradish pests since many years in Poland (Ruszkowski, 1933), and also in other countries of Europe and North America (Balachowsky & Mensil, 1936; Davidson, 1966; Crüger, 1991). Usually one generation per year is observed in central Poland (Boczek, 1988). Phyllotreta armoraciae Koch. Distribution: Europe, North America (Heikertinger et al., 1954). Adults feeding on leaves, larvae in leaf petioles. Common pest in Poland (Rogowska, 1999). This species can also feed on mustard plants (Davidson, 1966). Phyllotreta atra F. Distribution: Europe to Caucasus, north Africa, Siberia (Balachowsky & Mensil, 1936). In Poland, the most numerous species on horseradish among all mentioned species (Rogowska, 1999, 2001). 341

Phyllotreta undulata (Kutsch). Distribution: Europe, north Asia and Africa (Heikertinger et al., 1954). Very common species and numerous on horseradish in Poland (Rogowska, 1999, 2001). Phyllotreta nemorum L. Distribution: Europe, north Africa, western Asia (Balachowsky & Mensil, 1936). In some years, this species can occur in large numbers, severely injuring horseradish in Poland (Wojtaszek, 1980 & 1981; Rogowska, 2001). Phyllotreta nigripes F. Distribution: like Ph. atra. Phyllotreta flexuosa Ill. Distribution: Europe, North America (Balachowsky & Mensil, 1936). This species occurred only sporadically in Poland up to now (Rogowska, 2001).

Chrysomelidae Phaedon cochleariae F. Distribution: Europe, Asia, North America (Heikertinger et al., 1954; Szwejda, 1985). At present, the least numerous species in the Coleoptera order in both regions: Skierniewice and Sieradz (Rogowska, 2001). One generation per year in Poland (Szwejda, 1985).

Curculionidae Ceutorrhynchus spp. Distribution: Europe to Caucasus, south Asia, north Africa, North America (Dosse, 1954; Szwejda, 1985). In Poland, these beetles are very common and feeding on different Brassicaceae plants (Wojtaszek (1981). Obarski (1962) was noticed 17 species on cabbages and rape, among others: C. napi Gyll., C. quadridens (Panz), C. rapae Gyll., C. sulcicollis (Payk.), C. nigrinus (Marsh.), C. erysimi (F.), C. pleurostigma (Marsh.). This last species was found in horseradish roots (Wojtaszek, 1981). Crüger (1991) found larvae of C. cochleariae in leaf petioles. One generation/year (Szwejda, 1985).

Elateridae Distribution: Cosmopolitan family, more than 120 species. Very common in Europe. Some of these species were found on horseradish crops (Blunck & Mühlmann, 1954). The most common on Brassiceae plants are: Agriotes obscurus L., A. lineatus L., A. sputator L., Alhous niger L., Selatosomus aeneus L. (Tischler, 1965; Kagan, 1985) In Poland, the most injured by wireworms is horseradish cultivated in the humus soil (Rogowska, 2001).

Thripidae Thrips tabaci Lind. Distribution: Europe, Asia, Africa, Australia, North America (Blunck, 1925). Polyphagous species. In both years: 1997 and 1999, Th. tabaci occurred in all developmental stages on horseradish (Rogowska, 2001). In Poland, from 4 to 6 generations per year were observed on cabbage and cauliflower (Boczek, 1988), but on horseradish only from 3 to 4 generations per year (Rogowska, 2001).

Miridae Lygus rugulipennis Popp. Distribution: Palearctic zone (Kagan, 1985). Polyphagous species (Korcz, 1994). It was found in all developmental stages on horseradish (Rogowska, 2001). Two generations per year occur in Poland (Romankow, 1959; Rogowska, 2001). L. punctatus Zett. Distribution: Europe and Asia (Korcz, 1994). Sporadic occurrence on Polish horseradish plantatios (Rogowska, 2001).

Pentatomidae Eurydema oleracea L. Distribution: Europe, north Asia with Siberia (Otten, 1956). In Poland, very common on Brassiceae plants, one generation/year (Szwejda, 1985). Sporadic occurrence on horseradish (Rogowska, 2001).

342

Aphididae Two species of aphids feeding on horseradish leaves were identified on experimental horseradish crops. Brevicoryne brassicae L. Distribution: Palearctic zone (Nawrocka, 1985). It is a very common species occurring on Brassiceae crops (Szwejda, 1985). Noted also on horseradish in Poland by Lipa et al. (1977); Wojtaszek (1980) and Rogowska (2001). From 6 to 8 generations per year commonly observed (Boczek, 1988). Aphis fabae Scop. Distribution: the cosmopolitan species (Balachowsky & Mensil, 1936). As a poliphagous pest is occurring on many wild and cultivated plants including horseradish (Rogowska, 2001). In Poland, from 7 to 10 generations per year occur (Nawrocka, 1985).

Pieridae Pieris brassicae L. Distribution: Europe, Asia with India, north Africa, North America (Szwejda, 1985). One of the oldest pest of horseradish in Poland (Belke, 1861) occurring every year (Szwejda & Rogowska, 2000). Two generations per year on cabbage or cauliflower (Szwejda, 1985) and horseradish were noted in Poland (Rogowska, 2001). Pieris rapae L. Distribution: Palearctic zone (Heddergott, 1953). Another oldest pest of horseradish noted in Poland (Belke, 1861), occurring regularly every year (Szwejda & Rogowska, 2000). Two generations per year on cabbage or cauliflower (Szwejda, 1985) and horseradish (Rogowska, 2001) are observed in central Poland.

Plutellidae Plutella xylostella L. Distribution: the cosmopolitan species (Blunck, 1925, Heddergott, 1953), important on all Brassiceae plants on the world (Szwejda, 1985), including horseradish (Szwejda & Rogowska, 2000; Rogowska, 2001). In Poland, from 3 to 4 generations on cabbage and cauliflower (Boczek, 1988), but from 2 to 3 generations on horseradish (Rogowska, 2001).

Noctuidae Mamestra brassicae L. Distribution: Europe, Asia, north Africa (Balachowsky & Mensil, 1936, Heddergott, 1953). The poliphagous species. Besides cruciferous plants, it can also feed on pea, tomato, lettuce, sugar beet, flax and tobacco (Szwejda, 1985). In Poland, two generations per year on cabbages (Szwejda, 1985), noted since 1860 (Belke, 1861). Caterpillars of M. brassicae are not so numerous on horseradish as Pieris species and occur in 1 or 2 generations (Rogowska, 2001). Plusia gamma L. Distribution: Palearctic zone (Heddergott, 1953). Polyphagous species occurring in 2 generations per year (Balachowsky & Mensil, 1936). As the pest of horseradish is noted since 1860 in Poland (Belke, 1861).

Anthomyiidae Delia radicum L. Distribution: Europe, Asia, Africa, Australia, south America, North America (Henning, 1953; Szwejda, 1977). In Poland, one of the most important pests of horseradish roots (Rogowska, 2001), noted since 1860 (Belke, 1861). In Poland, two generations on cabbages (Szwejda, 1977) and from one to two generations on horseradish observed (Rogowska, 2001).

Tenthredinidae Athalia rosae L. Distribution: Europe, Asia, Africa, south America, North America (Balachowsky & Mensil, 1936; Francke-Grosman, 1953). This pest occurred always in high numbers from the beginning of August to the end of September in Poland (Rogowska, 2001).

343

Table 2. The population composition of entomofauna collected on horseradish in two regions in central Poland

Species Species composition (in%) Skierniewice Lipnik 1997 1999 1997 1999 Thrips tabaci 1.2 0 0 0 Lygus rugulipennis 1.6 0 1.3 1.8 L. punctatus 0 0 0.2 0 Eurydema oleracea 0 0.4 0 0 Aphis fabae + 20.5 13.3 7.7 14.1 Brevicoryne brassicae Phyllotreta armoraciae 4.8 4.3 3.3 5.1 Ph. nemorum 9.1 3.2 5.4 6.6 Ph. undulata 13.9 42.5 20.3 45.0 Ph. atra 57.7 16.6 6.5 10.3 Ph. nigripes 0 2.7 0 0 Ph. flexuosa 0 11.2 0 0 Phaedon cochleariae 0 0 0.3 0 Ceutorhynchus spp. 0.2 0 0.5 0.9 Elateridae 0 0 1.2 0 Pieris brassicae 5.6 0.3 7.6 2.8 P. rapae 1.3 0.4 7.1 0.8 Plutella xylostella 2.0 3.7 3.1 0 Mamestra brassicae 0 0 4.5 0 Plusia gamma 0.1 0 0 0 Athalia rosae 0.7 0.2 19.9 0 Delia radicum 1.3 1.2 11.1 12.6 Total number of trapped 1577 1390 1214 880 insects

The above listed insect species were collected from horseradish crops only in two growing seasons, therefore they do not probably include all phytophagous species which may occur in other years. But the most important pest species are certainly presented in this paper. Our studies are confirming data mentioned in other publications, among others by: Belke (1861); Balachowsky & Mensil (1936); Lipa et al. (1977); Crüger (1991). In Poland, Lipa et al. (1977), showed other species which were not noticed by us in the growing seasons of 1997 and 1999. They were: Phyllotreta cruciferae (Gz.), Baris laticollis (Marsh.), Meligetes aeneus F., Psylliodes chrysocephala (L.), four species of Ceutorhynchus spp., Lygus pratensis (L.), Thrips fuscipennis Hal. and Macroletes laevis (Rib.). According to Lipa et al. (1977), this last mentioned species was very commonly occurring every year in large numbers on horseradish plantations. It is a migrating species, very numerous in different environments, transmitting phytoplasmatic diseases but not on cruciferous plants (Soika, Kamińska, 2000). These studies on the phytophagous entomofauna species composition and population of dominant species (Rogowska, 2001), shall become the base of our future work to develop a precise and effective programme to control pests on horseradish plantations in Poland.

344

References

A list with references could be sent by the senior author upon request.

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 345-353

Occurrence of bean aphid (Aphis fabae Scop.) on red beet in relation to different coverage of soil by weeds

M. Pobożniak Deparment of Plant Protection, Agricultural University,Al. 29 Listopada 54, 31-425 Cracow, Poland

Abstract: In 1998- 2000 author investigated the occurrence of Aphis fabae Scop.in red beet in relation to differrent coverage of soil by weeds. It was found that the number of aphids and the number of red beet plants colonized by aphids decreases with the lower weeding frequency i.e. with the greater coverage of the soil by weeds, reaching its minimum on the plots where weeds were not removed. Keeping plots weed-free, which is the present practice in market gardening can create a better environment for pest occurrence. In 1998 the total number of aphids per plant on plots kept weed free was twice as big as on plots weeded three times and nearly five times as big as on plots which were not weeded. In 1999 and 2000 the differences between the plots without the weeds and weeded three times were not so distinct while they were significant between plots without the weeds and plots weeded twice and not weeded

Key words: Aphis fabae, weeds, red beet

Introduction

In view of economic and environmental concerns the trends to reduce the use of pesticides (including herbicides and insecticides) and introduce integrated methods (IPM) can be observed. One of the IPM methods is to use weeds as natural and main component of the agricultural environment. Andow (1991) and McKinlay & McCreath (1995) treat weedy culture as one of the method of cultivation of two or more species together along with intercropping, undersowing or using living mulch. The variety of plants in agroecosystems influences both the number of pests and stability of their population (Bach 1980, Emden & Willams 1974, Root 1973). The research on many specialized plant pests shows that they are more numerous in monoculture than in more complex systems (Altieri & Whitcomb 1980, Dempster & Coaker 1974, Rish et al. 1973). The aim of the research was to evaluate how the presence of weeds in red beet cultivation (Beta vulgaris L.) influences the occurrence of bean aphid (Aphis fabae Scop.).

Material and methods

Experiments were carried out on red beet plots (cv. Czerwona Kula) at the Experimental Station, Dept. of Plant Protection, Mydlniki near Cracow in 1998-2000. The method of randomised blocks with four replications was apllied including the following combinations: A-plots continuously kept weed-free during the whole vegetation season, B-removed three times, C-weeds removed twice, D-weeds not removed, but topped to the high of red beet. Until to the end of thinning of beet plants, all plots were kept weed-free in order to protect the crop (Tab. 1). The infestation rate and population dynamics of aphids were regularly observed on 25 plants randomly selected per plots. The analyses were started when the first winged forms

345 346

were observed and continued until the disappearance of the population of aphids. The percentage of plants infested by aphids was also determined. During the observation, the analyses of weeds were carried including their species and soil coverage according to the methods applied by Rola (1964). For this reason four areas of 0,25 m 2 were selected at random. In the experiments, the yield from the individual combinations as well as the percentage decrease of yield were compared to the combination A consisting of plots kept weed-free. In 2000 because of mistake, the weeds from combination D were removed. As a result of this, the presentation of yield do not cover the data from this combination.

Result and discussion

The development and the number of aphids on the red beet were different in the individual years. (Fig. 1-3). The highest number of aphids was noticed in 1998. In this year the first aphid colonies were recorded on 25 May on all plots. The fastest development of aphids was noticed on the plots kept weed-free, reaching its maximum on 18 June (207 aphids/plant). Aphids were less numerous on plots weeded three times and twice and a small number of aphids was observed on plots, where weeds were not removed. The mean number of aphids per plant during the period of the highest infestation in combination kept weed-free was nearly four times as high as in combination where weeds were not removed. In 1999 and 2000, because of the bad weather conditions, the number of aphids was smaller than in the previous year. The first aphids were noticed on 29 May in 1999 and on 23 May in 2000. Similarly to the results achieved in 1998, the highest occurrence of aphids was noticed on the plots kept weed-free, and the lowest -on the plots where weeds were not removed. On the plots, where weeds were not removed the aphids colonies lasted only to the second half on June in 1998 and to the end of June in 2000 i.e for a much shorter period than on plots of other combinations. By comparing the percentage of plants infested by bean aphid it may be stated that percentage increased proportionally to the number of aphids on plants. The number of infested plants correlates with the number of aphids and in all years of observations the greatest number of infested plants was observed on weed- free plots and the smallest in combination where weeds were not removed (Fig. 1-3). In each period of observations the number of A. fabae and the percentage of colonized plant did not depend on the fact whether weeding was carried out before the analysis (combination B and C) or not. The reduction of weeding frequency causing greater soil coverage by weeds decreased the number of aphids as well as percentage of infested plants. (Fig. 1-3). In 1998 the total number aphids per plant on plots kept weed free was twice as big as on plots weeded three times and nearly five times as big as on plots which were not weeded. In 1999 and 2000 the differences between the plots without the weeds and weeded three times were not so distinct while they were significant between plots without the weeds and plots weeded two times and not weeded (Tab 2). In all years of observations the average level of infestation of plants indicates that the greater number of colonized plants was on weed-free plots and in 1999 it was three times, in 1998 and 2000 nearly twice as big as on plots where weeds were not removed (Tab 2). Also the negative result of the correlation coefficient indicates that along with the increase of the coverage of soil by weds the number of aphids and the percentage of infested plants is decreasing (Tab 3).

347

Combination A Combination A % 100 210 % 100 100 %

80 175 80 80 140 60 60 60 105 40 40 40 70

20 35 20 20

0 0 0 0 5-06 2-07 9-07 5-06 2-07 9-07 28-05 10-06 18-06 25-06 28-05 10-06 18-06 25-06 Combination B Combination B % 100 210 % 100 100 %

80 175 80 80 140 60 60 60 105 40 40 40 70

20 35 20 20

0 0 0 0 5-06 2-07 9-07 5-06 2-07 9-07 28-05 10-06 18-06 25-06 28-05 10-06 18-06 25-06 Combination C Combination C % 100 210 % 100 100 %

80 175 80 80 140 60 60 60 105 40 40 40 Soil coverage by weeds [%] [%] weeds by coverage Soil 70 plant per aphids of Number [%] weeds by coverage Soil aphids by plants of Infestation

20 35 20 20

0 0 0 0 5-06 2-07 9-07 5-06 2-07 9-07 28-05 10-06 18-06 25-06 28-05 10-06 18-06 25-06 Combination D Combination D % 100 210 % 100 100 %

80 175 80 80 140 60 60 60 105 40 40 40 70

20 35 20 20

0 0 0 0 5-06 2-07 9-07 5-06 2-07 9-07 28-05 10-06 18-06 25-06 28-05 10-06 18-06 25-06 Soil coverage by weeds Number of aphids per plant Infestation of plants by aphids

Fig. 1. Influence of weeds on occurrence of bean aphid and plants infestation (Mydlniki 1998).

348

Combination A Combination A % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 30 40 40 30 20 20 20 20 10 10 0 0 0 0 5-06 6-07 5-06 6-07 29-05 11-06 17-06 25-06 30-06 14-07 29-05 11-06 17-06 25-06 30-06 14-07 Combination B Combination B % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 30 30

40 40 20 ] 20 % 20 [ 20 10 10 0 0 0 0 weeds weeds 5-06 6-07 5-06 6-07 y 29-05 11-06 17-06 25-06 30-06 14-07 29-05 11-06 17-06 25-06 30-06 14-07

Combination C e b Combination C

% 100 60 g % 100 70 % 60 80 50 80 50 40 60 60 40 30 30 Soil coverage by weeds [%] [%] weeds by coverage Soil 40 plant per aphids of Number covera Soil 40 aphids by plants of Infestation 20 20 20 20 10 10 0 0 0 0 5-06 6-07 5-06 6-07 29-05 11-06 17-06 25-06 30-06 14-07 29-05 11-06 17-06 25-06 30-06 14-07 Combination D Combination D % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 30 40 40 30 20 20 20 20 10 10 0 0 0 0 5-06 6-07 5-06 6-07 29-05 11-06 17-06 25-06 30-06 14-07 29-05 11-06 17-06 25-06 30-06 14-07

Soil coverage by weeds Number of aphids per plant Infestation of plants by aphids

Fig. 2. Influence of weeds on occurrence of bean aphid and plants infestation (Mydlniki 1999). 349

Combination A Combination A % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 30 40 40 30 20 20 20 20 10 10 0 0 0 0 4-06 4-06 28-05 14-06 21-06 30-06 12-07 28-05 14-06 21-06 30-06 12-07 Combination B Combination B % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 30

] 30 40 t 40

20 % [ 20 20 20 10 10 0 0 0 0 weeds y 4-06 4-06 28-05 14-06 21-06 30-06 12-07 28-05 14-06 21-06 30-06 12-07 e b

Combination C g Combination C % 100 60 % 100 70 % 60 80 50 80 50 40 60 60 40 Number of aphids per plan per aphids of Number covera Soil aphids by plants of Infestation

Soil coverage by weeds [%] [%] weeds by coverage Soil 30 40 40 30 20 20 20 20 10 10 0 0 0 0 4-06 4-06 28-05 14-06 21-06 30-06 12-07 28-05 14-06 21-06 30-06 12-07 Kombinacja Combination D 100 60 100 70 60 80 50 80 50 40 60 60 40 30 40 40 30 20 20 20 20 10 10 0 0 0 0 4-06 4-06 28-05 14-06 21-06 30-06 12-07 28-05 14-06 21-06 30-06 12-07

Soil coverage by weeds Number of aphids per plant Infestation of plants by aphids

Fig. 3. Influence of weeds on occurrence of bean aphid and plants infestation (Mydlniki 2000).

350

Table 1. Agricultural treatments.(Mydlniki 1998-2000).

Combination B Combination C Date of Date of Year Date of sowing thinning weeding I II III I II 1998 7 IV 16 V 19 V 14 VI 10 VII 8 VI 17 VII 1999 6 IV 18 V 24 V 17 VI 12 VII 11 VI 19 VII 2000 10 IV 20 V 27 V 20 VI 19 VII 14 VI 26 VII

Table 2. Selected information concerning the occurrence of bean aphid plants infestation (Mydlniki 1998-2000)

Combinations Selected information A B C D 1998 Mean number of aphids /plant in period of 207.3c 127.3b 8..7ba 53.9a maximum infestation Percent of plants infested by aphids in period of 94,0b 79,0a 75,0a 70,0a maximum infestation Total number of aphids 1177.1c 616.4b 325.7a 262.5a Mean percent of plants infested by aphids 53.8b 48.0ba 34.1a 31.6a 1999 Mean number of aphids /plant in period of 57.4c 38.8bc 20.1ba 13.1a maximum infestation Percent of plants infested by aphids in period of 64.0b 54.0b 33.0a 26.0a maximum infestation Total number of aphids 135.9c 106.2cb 57.7b 28.9a Mean percent of plants infested by aphids 28.3c 23.9cb 16.3b 9.5a 2000 Mean number of aphids /plant in period of 56.7b 43.1ab 21.6a 23.2a maximum infestation Percent of plants infested by aphids in period of 63.0b 50.0b 34.0a 36.0a maximum infestation Total number of aphids 213.4b 173.1ab 92.4a 84.6a Mean percent of plants infested by aphids 32.0b 25.9ab 16.3a 15.0a *Values in one row with the same letter do not differ statistically from each other

The weed composition was almost the same on all plots. The most frequent were: Galinsoga parviflora Cav., Chemopodium album L., Cirsium arvense (L.) Scop. Echinochloa crus-gali L., Agropyron repens L., Amaranthus retroflexus L. and Equisetum arvense L. The less frequent were: Polygonum persicaria L., Lamium purpureum L., Veronica arvensis L. and Plantago lanceolata L.. Despite of the presence of some species of weeds which can be host- plants for A. fabae, the population of aphids on the weeding plots was not increased. The analysis showed that weeds in the cultivation of red beet during the summer infestation caused the reduction of percentage of plants infested by A. fabae. and the population of 351

aphids. It seems that aphids were attracted to the crop without any weeds due to clear contrast between cultivated plants and soil and the plots kept weed free ensured better condition for development of A. fabae. It corresponds with the results obtained by Smith (1976), who observed a small number of Brevicoryne brassicae L. on weed infested Brussels sprouts, despite the presence of cruciferous weeds. Also Horn (1981) and Wnuk & Pobożniak (1999) noticed that the number aphids decreased with the greater coverage of soil by weeds, reaching its minimum on the plots where the weediness was higher.

Table 3. Correlation coefficients (for average values, 1998-2000)

Analyzed dependencies Correlation Coefficient r Coverage of soil by weeds/ -0.270* Number of aphids Coverage of soil by weeds/ -0.328* Percent of plants infested by aphids Rteor.p=0.05=0.204 Rteor. P=.,01=0.265 *Dependence significant at p=0.05 and p=0.01

Table 4. Yield and reduction of root yield of red beet in relation to weeding frequency (Mydlniki 1998-2000).

Combinations A B C D Yield Yield Reduction Yield Reduction Yield Reduction Yield Reduction [kg] [%] [kg] [%] [kg] [%] [kg] [%] 1998 29.1c 0.0 27.8c 4.5 20.7b 28.9 9.6a 67.0 1999 35.5b 0.0 31.2b 12.1 22.6ba 36.6 10.1a 71.5 2000 43.0d 0.0 37.3c 13.2 28.2b 34.4 - - Average 35.8 0.0 32.1 9.9 23.8 33.3 9.8 69.2

The suggestion that weeds can protect cultivated plants from pests was also made by Altieri (1981), Altieri et al. (1977), Altieri & Whitcomb (1980), Emden (1970), Emden & Williams (1974), Shelton & Edwards (1983) but the reason behind this phenomenon are very complex and requires further experiments to be carried out. Some authors indicate that weeds, which usually are higher than cultivated plants restrict the access of aphids to the crop (Perrin 1977) or can influence microclimate among plants Emden (1965), Levis (1965) The presence of weeds within a crop may be misleading by creation the visual camouflage or even discouraging the pest thus the plant is more difficult to find (Fenny 1976, Smith 1976). Uvah, Coaker (1984) suggested that diverse backgrounds reduce host- plant colonization by pest insects through the volatile chemicals released by the non -host plants directly deterriing the pest species. The odours of host-plants being masked by those of the non host-plants and this misleads the pest during the host-plant finding (Tahvanainen & Root 1972). Finch (1996) and Finch & Collier (2000) put forward a theory based on “appropriate / inappropriate landings” 352

by pests to explain why fewer specialist insects are found on host-plants growing in diverse backgrounds than on similar plants growing in bare soil. In all years, the greatest yield was achieved in combination without weeds and a bit smaller in combination weeded free times, where the average crop decrease was 9,9 %. The smallest crop was in combination weeded twice and in combination where weeds were not removed. The average crop decrease was 33,3 % and 69,2 % respectively (Tab. 4) Based on the comparison of the occurrence of aphids, the degree of weedinees and the crops from individual combinations it can be state that maintaining the certain level of weediness can be used as a treatment in integrated protection of the red beet against the bean aphid.

References

Altieri, M.A. 1981: Weeds may augment biological control of insects. Calif. Agric. 5-6: 22- 24. Altieri, M.A., Schoonhoven, A. & Doll, J. 1977: The ecological role of weeds in insect pest management systems: a review illustrated by bean (Phaseolus vulgaris) cropping systems. PANS 23: 195-205. Altieri, M.A. & Whitcomb, W.H. 1980: Weed manipulation for insect pest management in corn. Envir. Manag. 4: 483-489. Andow, D.A. 1991 Vegetational diversity and arthropod population response. Ann. Rev. Ent. 36: 561-586. Bach, C.E. 1980: Effects if plant diversity and time of colonization on an herbivore – plant interaction. Oecologia 44: 319-326. Dempster, J.P.& Coaker, T.H. 1974: Diversification of crop ecosystems as a means of controlling pests. Biology in Pest and Diseases Control. Blackwell, Oxford: 106-114. Emden, H.F. 1965: The role of uncultivated land in the biology of crop pests and beneficial insects. Sci. Hort. 17: 121-136. Emden, H.F. 1970: Insects, weeds and plant health. Proceedings 10th British Weed Control Conference, Brighton: 953-957. Emden, H.F.& Williams G.F. 1974: Insect stability and diversity in agro-ecosystems. Ann. Rev. Entomol. 19: 455-475. Fenny, P.P. 1976: Plant appearance and chemical defense. In: J. Wallace & R. Mansell (eds.), Biochemical Interactions Between Plants and Insects. Recent Advances in Phytochemistry 10: 1-40. Finch, S. 1996: “Appropriate / inappropriate landings”, a mechanism for describing how undersowing with clover affects host plant selection by pest insects of brassica crops. IOBC wprs Bulletin. 19 (11): 102-106. Finch, S.& Collier R.H. 2000: Host-plant selection by insects-a theory based on “appropriate / inappropriate landings” by pest insects of cruciferous plants. Ent. Exp. Appl. 96: 91-102. Horn, D.J. 1981: Effect of weedy backgrounds on colonization of collards by green peach aphid, Myzus persicae, and its major predators. Environ. Entomol. 10: 285-289. Lewis, T. 1965: The effects of shelter on the distribution of insects pests. Scientific Horticulture 17: 74-84. McKinlay, R.G.& McCreath, M. 1995: Some biological alternatives to synthetic insecticides for sustainable agriculture. Pesticide Outlook 6: 31-35. Perrin, R.M. 1977: Pest management in multiple cropping systems. Agro-ecosystems 3: 93- 118. 353

Rish, S.J.D. Andow, D. & Altieri, M.A. 1983: Agroecosystems diversity and pest control: Data, tentative conclusions and new research directions. Environ. Entomol. 12: 625-629. Rola, J. 1964: Metodyka szacunkowej analizy agrofitosocjilogicznej dla obserwacji polowych doświadczeń herbicydowych. In: Materiały do metodyki badań biologicznej oceny środków ochrony roślin, Vol. II: 25-33. Root, R.B. 1973: Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Monograph 43: 95-125. Smith, J.G. 1976: Influence of crop background on aphids and other phytophagous insects on Brussels sprouts. Ann. Appl. Biol. 83: 1-13. Shelton, M.D. & Edwards C.D. 1983: Effects of weeds on the diversity and abundance of insects in soybeans. Environ. Entomol. 12: 296-298. Tahvanainen, J.O.& Root, R.B. 1972: The influence of vegetational diversity on the population ecology of a specialized herbivore Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10: 321-346. Uvah, I.I.I. & Coaker, T.H. 1984: Effect of mixed cropping on some insects pests of carrots and onions. Ent. Exp. Appl. 32: 159-167. Wnuk, A. & Pobożniak, M. 1999: Influence of weeds on occurrence og bean aphid (Aphis fabae Scop.) and aphidophagous Syrphidae on red beet (Beta vulgaris L.). Scientific works of the Lithuanian Institute of Horticulture and Lithuanian University of Agriculture 18 (3): 266-275. 354

355

Undersowing or Intercropping Crops

356

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 355-359

The effect of intercropping leek with clover and carrot on thrips infestation

H. Legutowska1, H. Kucharczyk2 & J. Surowiec1 1 Department of Applied Entomology, Warsaw Agricultural University, Nowoursynowska 166, 02-787 Warsaw, Poland, 2 Department of Zoology, Maria Curie-Skłodowska University, Akademicka 19, 20-033 Lublin, Poland

Abstract: The effect of intercropping leek with clover and carrot was demonstrated by a decrease of the number of adults and larvae of the onion thrips (Thrips tabaci Lindeman). On the leek plants grown in a monoculture occurred from 55-70.9 % of all thrips collected in the two experimental sites in the 1999 growing season. From 9 to 25.2% of thrips occurred on the leek plants intercropped with carrot and av. 20% on the leek intercropped with strawberry clover. It was also found that the intercropped leek plants demonstrated lower damage symptoms caused by Thrips tabaci.

Key words: Thrips tabaci Lindeman, Thysanoptera, onion thrips, leek, intercropping

Introduction

The onion thrips, Thrips tabaci Lindeman (Thysanoptera, Thripidae), is the most important insect pest of leek (Allium porrum L.) in Poland (Legutowska, 1997) and in Western Europe (Crüger and Hommes, 1990; Ester et al., 1997; Van de Steene, 1999). Thrips damage leek by sucking out juice from the cells, which results in the appearance of white-silvery spots on leaves and leaf sheaths (Theunissen and Legutowska, 1991). Such damage can lead to lower prices or even rejection of injury crop at market. Chemical control of thrips is difficult due to the continuous invasion of mature insects originating from other plants. Thus, frequent pesticide treatments are necessery which not only increase the cost sof production but also increase the danger for the environment and human health. In the last years there was a tendency to limit the use of insecticides by introducing non-chemical and integrated methods of pest management. One proposed method was the intercropping of crop plant with other plant species. Some attempts to find non- chemical methods for controlling thrips in leek have been made in the Netherlands by Theunissen and Schelling (1993). Intercropping could be a promising method for reducing insect pest populations in vegetable crops in which applications of insecticide are relatively ineffective. The aim of our field studies was to demonstrate whether there is a significant reduction of thrips population on leek plants intercropped with other plant species. A positive effect of intercropping may lead to maintaing the quality of yield without carrying intensive insecticide treatments.

355 356

Materials and methods

The investigations were carried out during the 1999 growing season in two experimental sites. A commercial production field was selected in Ożarów Mazowiecki, near Warsaw in the region of intensive cultivation of field vegetables. The second site was located in the experimental field of the Applied Entomology Department of Warsaw Agricultural University at Ursynów. Leek (cv. Jolant) was intercropped with strawberry clover (Trifolium subterraneum, cv. Palestine), carrot (cv. Jaguar) and was grown as the monocrop. T. subterraneum and carrot were sown in the rows of 80 cm apart and leeks were planted in the middle of the rows of these plants. A random complete block design with four replications was used in these experiments. Every 7-10 days samples of 10 plants were randomly collected from each field for the whole period of vegetation. Each plant was individualy examined and assessed on a quality class regarding symptoms of thrips damage. The scale consisted of four classes: 1= no symptoms (clean), 2 = slight, 3 = moderate and 4 = heavy infestation symptoms. Thrips were collected from each plant, later counted and put into separate test tubes with 70% ethyl alcohol in order to identify them to a species.

Results

In the 1999 growing season the appearance of the first onion thrips was observed on the July 7 in Ożarów. The most numerous were in the monocrop plots (13.1 adult and larvae/ one plant) and the least on the leek intercropped with carrot (2.5 adult and larvae/1 plant) (Fig.1). In the monocrop treatment the highest number of thrips was observed on the 24th August (229.2 adult and larvae/ one leek) while in the intercropped with carrot and clover, there were 109.2 and 80.8 onion thrips specimens, on that day, respectively.

250

200

150 Th. tabaci 100 /1plant 50

Mean no. of 0 7.7 13.7 20.7 28.7 4.8 10.8 17.8 24.8 31.8 12.9 22.9 30.9

Fig. 1. The dynamics of Thrips tabaci Lind. population on leek in the Ożarów Mazowiecki experimental site, 1999.

In the Ursynów experimental site, the first Th. tabaci insects appeared only on some plants in all combinations of leek on July 30 (Fig. 2). The mean number of thrips/plant in the monocrop was 1.0 adult and larvae while the smallest number (0.3 adult and larvae/ plant) was observed on leek intercropped with carrot. 357

An increase of the pest population was noted at the end of August in the monocrop where, on the average, there were 36.6 adult and larvae/one plant. At the same time there were 7.5 and 22.6 specimens/plant, respectively on leek intercropped with carrot and clover. The largest number of thrips was noted at the end of September on leek in the monocrop, equal to to 90.8 adult and larvae. At the same time the number of thrips in the intercropped plots ranged from 8.2 to 15.1 adult and larvae/plant.

250

0 7.7 13.7 20.7 28.7 4.8 10.8 17.8 24.8 31.8 12.9 22.9 30.9 200 mmonocroponocrop leek w withith carrot carrot leek w withith clover clover 150 Th.tabaci 100 /1plant

50 Mean no.of 0 30.7 6.8 13.8 20.8 30.8 10.9 20.9 30.9 12.10

Fig. 2. The dynamics of Thrips tabaci Lind. population on leek in the. Ursynów experimental site, 1999.

On the Ożarów experimental site 55,668 adults and larvae of Th. tabaci were colledted during the whole growing season of 1999. Th. tabaci comprised up to 54.9% of the total number of thrips collected in all treatments (Fig. 3,4).

50000

40000 Ożarów Mazowiecki Ursynów L. 30000 adults 20000 larvae Th. tabaci 10000 No of 0 monocrop leek with leek with monocrop leek with leek with carrot clover carrot clover

Fig. 3. A total number of Thrips tabaci Lind. adults and larvae collected frorm leek, 1999.

In the Ursynów experimental site 11,503 adults and larvae of Thrips tabaci were collected in the monocrop plots during the entire period of the 1999 growing season.This number represents 70.9% of the total number of thrips collected in the Ursynów experiment. In the intercropped plots, the highest number of thrips was recorded on leeks grown with 358

clover and was equal to 3,254 specimens, comprosong 20% of all insects collected. The smallest number was collected on leeks intercropped with carrot – 1,475 speciments, comprising 9.1% of all insects collected (Fig. 3 and 4).

Ożarów Mazowiecki Ursynów 19,9 54,9 20 70,9

9,1

25,2

monocrop leek with carrot leek with clover Fig. 4. The percentage of Thrips tabaci Lind. collected from leek grown as a monocrop and intercropped with carrot and clover during the 1999 vegetative season.

Ożarów Mazowiecki 100 90 80 70 60 50 40 30 20 10 0

Plants per damage class [%] monocrop leek with carrot leek with clover

Ursynów 100 90 80 70 60 50 40 30 20 10 0 monocrop leek with carrot leek with clover Plants per damage class [%]

100708090 405060 clean slight moderate 2030100 heavy mo noc leek with

Fig. 5. Feeding symptoms of Thrips tabaci Lind. on the leek plants expressed in damage classes in the 1999 vegetative season.

359

Our regular observations on the infestation level of leek plants by thrips carried out in the Ożarów experiment showed the highest damages on leek grown as the monocrop. The whole leaf surface shown the 4th degree of infestation on 85.8% plants in the 1999 growing season. The crop did not present no commercial value. In the case of leek intercropped with carrot and clover 13.1 and 17.1% of plants showed heavy damage of the thrips feeding, respectively (Fig. 5). In the site Ursynów the symptoms of intensive thrips feeding was obseved on 24% leek plants grown as the monocrop. On leek intercropped with clover only 1.4% plants showed heavy damages and presented no commercial value (Fig. 5).

References

Crüger G. and Hommes M. 1990. Krankheiten und Schädlinge an Porree. Gemüse 2: 130-135. Ester A., de Vogel R. and Bourma E. 1997. Controlling Thrips tabaci (Lind.) in leek by film- coating seeds with insecticides. Crop Prot. 16: 673-677. Legutowska H. 1997. [The occurrence of onion thrips (Thrips tabaci Lindeman) on leek plants.] Prog. Plant Protection/ Post. Ochr. Roślin 37(2): 57-60.(In Polish with English summary). Theunissen J. and Legutowska H. 1991. Thrips tabaci Lindeman (Thysanoptera: Thripidae) in leek: symptoms, distribution and population estimates. J. Appl. Ent. 112: 163 -170. Theunissen J. and Schelling G. 1993. Suppression of Thrips tabaci population in intercropped leek. Mededelingen Faculteit Landbouww. University Gent 58 (2a): 383-390. Van de Steene F. 1999. Monitoring and control of Thrips tabaci Lind. with furathiocarb in leek fields. IOBC wprs Bulletin 22(5): 235-240. 360

361

Insecticidal Control

362

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 361-369

Effects of film-coating flax seeds with various insecticides on germination and on the control of flea beetles.

A.Ester, H.F. Huiting & J.H. Nijënstein* Applied Plant Research, P.O. Box 430, 8200 AK Lelystad, The Netherlands *Cebeco Seeds B.V., P.O. Box 10,000, 5250 GA Vlijmen, The Netherlands

Abstract: Field experiments were carried out in 1999, 2000 and 2001 to assess the control of the flax flea beetles Longitarsus parvulus (Payk.) and the large flax flea beetle Aphthona euphorbiae (Schrank) in fibre flax crop (Linum usitatissimum L.) by film-coating the seeds with insecticides. The treatment with the insecticides was compared with the standard spray application of parathion and with untreated seeds. Film-coating the seeds with imidacloprid 70 % WS, fipronil 500g/l FS and thiamethoxam 350 g/l FS gave sufficiently protection against flea beetle, but spinosad was not effective to control the flea beetles. The fipronil, spinosad and thiamethoxam at rates of 2.5 g and 5.0 g per kg seed did not cause phytotoxicity. Imidacloprid at a rate of 8.75 g and 17.5 g and thiamethoxam at rates of 10 g and 20 g resulted in a lower number of emerged plants.

Key words: Flax flea beetles, Longitarsus parvulus, Aphthona euphorbiae, Flax, Linum usitatissimum, seed film coating.

Introduction

Flax flea beetles are of great economic importance. Longitarsus parvulus (Payk.) and Aphthona euphorbiae (Schrank) are known as serious pests of flax and linseeds crops in Europe, Hungary, Romania, North Africa, West Siberia and Bulgaria as well as Egypt (Vig, 1997; Oakley et al., 1996; Gruev et al., 1993; Beaudoin, 1988). To obtain optimum yields of oil production or straw and fibre production of flax, crop growth without any pests as flea beetles or thrips is necessary. Flea beetles are small black coleopterans with green metal glints. The attack begins as soon as the soil splits before the emerging during dry and sunny weather in spring. This can continue until the end of the vegetation, but it is detrimental to flax until the flax plants reach a height of 7 cm. The insect attacks the seedlings, cotyledons, stems and leaves. Attacks made before emerging eliminate the plants. After emerging, the plant population can still sometimes be reduced but above all the vegetation will be retarded and damaged (Beaudoin, 1988). These insects are responsible for the attack of the top of the seedlings, which results in branching of the stem. This is unacceptable for the flax fibre industry. To protect the crop against flea beetles several spray applications with parathion are needed, particularly in the seedling stage of the crop. This method of treatment appears not to be fully effective and also has a poor environmental profile. Using insecticides as seed treatment could be a more convenient and more effective way of controlling flea beetles and would be less injurious to other organisms and predators. This paper deals with further field trials of some compounds for the final introduction in practices.

361 362

Materials and methods

Seed treatments The experiments were performed with the fibre flax variety, Escalina. In 1999 the seed lot had a thousand kernel weight (tkw) of 6.2 gram and a germination of 99 %, 2000, having a tkw of 6.0 gram and a germination of 94 %. In 2001, the variety Escalina was also used, with a tkw of 6.0 gram and a germination of 95 %. The seeds used in all experiments were film-coated by Cebeco Seeds BV, using an angled drum mixer technique (Clarke, 1987). All the treatments contained the fungicide prochloraz at a rate of 0.2 g. a.i. per kg seed. Two types of ‘untreated’ seeds were tested: one without a film-coating and one with a film- coating. Both types were treated with the fungicide. Untreated film-coated seeds were drilled in the plots for the parathion applications. The insecticide imidacloprid was chosen because of the systemic action. It was applied in pellets of iceberg lettuce seeds and proved effective in controlling of aphids (Ester and Brandjes, 1998). Ester and Huiting (2001) confirmed the effectiveness of fipronil (EXP80415A), applied as a seed treatment, in controlling the onion thrips by seed. Spinosad was chosen for its biological action. The active ingredient is composed of two metabolites from the fungus Saccharopolyspora spinosa, namely Spinosyn A and Spinosyn D (Miles and Dutton, 2000). The compound thiamethoxam was chosen because it belongs to the same group of insecticides as imidacloprid that are known of the systemic action. Until 1999, the recommendation for flea beetle control in linseeds and flax crop was to spray post-emergence parathion-ethyl. In 2000 and 2001 only parathion-methyl was allowed in practice in The Netherlands, as parathion-ethyl lost its registration.

Table 1. Summary of insecticides and doses (g. a.i. per kg of seed) used to film-coat flaxseed to control flea beetle.

Insecticides Formulation 1999 2000 2001 Imidacloprid 70 % WS 8.75 8.75 8.75 17.5 17.5 – Fipronil 500 FS 2.5 2.5 – – 6.25 – 12.5 12.5 12.5 Spinosad 480 SC 24 – – 48 – – 96 – – Thiamethoxam 350 g/l FS – – 2.5 – – 5.0 – – 10.0 – – 20.0 Parathion-ethyl 25 % 0.15 l/ha 1) – – Parathion-methyl 240 g/l CS – 144 g/ha 2) 144 g/ha 3) 1) one spray application 27/5; 2) two spray applications 27/4 and 2/5; 3) three spray applications 25/4, 3/5 and 10/5, – = not used

363

Efficacy trials Trials were carried out in 1999, 2000 and 2001 at one location, in Lelystad (in the centre of The Netherlands). The soil was a marine loam with 21 % silt. Infestations of flea beetle could be expected each year, because flax crop is cultivated intensively. The seeds were drilled with an Øyord drilling machine, which is also favoured by Dutch growers of flax. In 1999, plots consisted of 12 rows (12.5 cm between rows) each 12 m long, covering an area of 18 m2, the number of seeds were 2000 per square meter. In 2000, plots consisted of 20 rows of 8 m long with an area of 21 m2 with 1600 seeds per m2. In 2001, the plots consisted also of 20 rows with 10 metre long, this means an area of 26.5 m2 with 1660 seeds per m2. The seeds were drilled 0.5 cm apart in the rows (20 seeds per metre row) at a depth of 1 cm. The seeds were drilled at the end of April in 1999, in mid-April in 2000 and begin of April in 2001. The experimental layout consisted of a randomised block design with each treatment being replicated four times, in 1999 and 2000. In 2001, six replicates were drilled.

Assessment Field emergence was determined (two and four weeks after drilling, 2000 and three and five weeks in 2001). The number of plants (with and without damage) were counted in a ten metre strip of rows, totalling 1.25 m2. The data of emergence of 1999 not being relevant are not presented in this paper, because the optimise effectively doses were not known in this phase of the research. Crop damage by the flea beetle was assessed in the end of May and the first week of June in 1999 and the end of April and end - May in 2000 and begin of May in 2001. Assessment took place by counting eight metres of row (divided over eight rows) totalling 1 m2 in 1999 and six metres over six rows, totalling 0.75 m2 in 2000 and 2001. The flax plants were assigned to one of the following categories: – Normal plants – Deformation of the cotyledons – Chlorosis of the cotyledons and /or leaves – Necrosis of the cotyledons and/or leaves – Attacked leaves, with a hole in the leaves. Assessment on leaf damage per plant, took place by pulling out fifteen plants from three rows of each plot. The first 14 leaves (1999) and 30 leaves (2001) per plant were examined on the number of attacked leaves per plant.

Statistical analysis Data were analysed using analysis of variance (ANOVA) in Genstat 5. From the ANOVA means, least significant differences (LSD) and F-probabilities were obtained. LSD's were calculated with Student’s distribution.

Results

Field emergence Two weeks after drilling the field emergence of seeds treated with imidacloprid was significantly lower compared to untreated seeds (Table 2). The imidacloprid 17.5 g resulted in a lower field emergence than the 8.75 g, which indicates a doses response effect. The fipronil treatment with a dose of 12.5 g also produced a lower field emergence than the 2.5 g. a.i. per kg seed. Four weeks after drilling, the field emergence after treatments with imidacloprid and fipronil at a dose of 12.5 g a.i. per kg seed was significantly lower compared to the untreated 364

seeds plus film-coating. Untreated seeds plus film coating had an equal emergence as the plots without a film coating. In 2001, after three and five weeks, imidacloprid at a rate of 8.75 g and thiamethoxam 10 g. and 20 g. a.i. per kg seed lowered the number of emerged plants, per square metre.

Table 2. Emergence of flax seedlings in the field trial. Number of seedlings per m2 two and four weeks after drilling in 2000 and three and five weeks in 2001.

Insecticides g. a.i. / kg seed 2000 2000 2001 2001 Two weeks Four weeks Three weeks Five weeks Imidacloprid 8.75 857 979 573 1022 17.5 748 893 – – Fipronil 2.5 1034 1106 – – 6.25 986 1062 – – 12.5 938 1022 907 1202 Thiamethoxam 2.5 – – 956 1230 5.0 – – 876 1207 10.0 – – 798 1076 20.0 – – 471 894 Parathion-methyl 144g/ha 932 1012 1047 1296 Untreated + coat 0 1010 1102 949 1241 Untreated - coat 0 990 1074 – – LSD (α = 0.05) 80 78 111 86 F-probability < 0.001 < 0.001 < 0.001 < 0.001

Efficacy of the insecticides In 1999, the percentage of plants attacked was significantly higher from the untreated seeds without film coating than from the film-coated seeds with or without insecticide treated (Table 3). The treatments with fipronil and spinosad provided the same level of protection as untreated plus film-coat and the standard parathion-ethyl treatment. The percentage of plants damaged was higher in 2000 and 2001 than in 1999. In 2000, table 3 shows that the damage to ‘untreated’ caused by flea beetles was not influenced by the film-coat. Even the parathion-methyl treatment two times (standard) did not show any controlling effect on the flea beetles five weeks after drilling. Table 3 shows that the damage to plants produced from treated seeds was significantly less than those from untreated seeds and the standard parathion-methyl treatments in 2000. Two weeks after drilling the imidacloprid treatments were significantly less attacked than the fipronil at the dose of 2.5 gram only. Furthermore, the percentage of damaged plant doubled in the period of three and five weeks after drilling. In 2001, the insecticide seed treatments resulted in markedly fewer damaged plants compared with the untreated control and the parathion application. Parathion-methyl applied two times produced results similar to the untreated seeds. Thiamethoxam treatments, at rates from 2.5 up to 20 g a.i. per kg seed, did not show any significantly dose response effect. Treated seeds with imidacloprid at doses of 8.75, 17.5 g. a. i. per kg of seed produced significantly lower number of leaves per plant than the plants of the untreated seeds and the 365

standard (Table 4). Seeds treated with a film-coat produced a significantly lower percentage of affected plants than the untreated seeds without a coating.

Table 3. Efficacy of the insecticides applied as a film-coat for controlling flea beetle in flax crop. Number of damaged plants per m2 and percentage four weeks after drilling in 1999 and two and five weeks after drilling in 2000 and five weeks drilling in 2001.

Insecticides g. a.i. /kg seed 1999 1999 2000 2000 2001 No. plants % 2 weeks 5 weeks 5 weeks Imidacloprid 8.75 55 3.3 15.7 39.1 34.0 17.5 30 1.9 13.1 20.2 – Fipronil 2.5 68 4.2 38.1 45.1 – 6.25 – – 24.8 63.0 – 12.5 74 4.6 26.2 56.8 33.8 Spinosad 24 132 8.1 – – – 48 129 8.0 – – – 96 74 4.9 – – – Thiamethoxam 2.5 – – – – 30.5 5.0 – – – – 23.9 10.0 – – – – 21.6 20.0 – – – – 24.9 Parathion-ethyl 0.15 l/ha 134 8.2 – – – Parathion-methyl 144 g/ha – – 63.6 83.3 62.8 Untreated + coat 0 135 8.2 61.2 77.9 62.9 Untreated - coat 0 284 17.7 68.2 84.8 – LSD (α=0.05) 107 7.0 18.7 27.0 15.0 F-probability 0.004 0.007 < 0.001 < 0.001 < 0.001

Table 4. Average number of leaves per plant and the percentage of attacked leaves per plant five weeks after drilling in 1999

Insecticides g. a.i. / kg seed No leaves per plant Attacked leaves per plant Imidacloprid 8.75 21.4 18.7 17.5 21.0 12.9 Fipronil 2.5 23.8 15.9 12.5 22.9 11.5 Spinosad 24 25.4 23.2 48 24.5 24.0 96 23.9 17.2 Parathion-ethyl 0.15 l/ha 24.0 24.9 Untreated +coat 0 23.9 22.8 Untreated - coat 0 24.4 37.6 LSD (α = 0.05) 1.7 11.8 F-probability < 0.001 0.006 366

Parathion-ethyl treatments had no effect on the percentage damaged leaves per plant. The treatments with imidacloprid at a dose of 17.5 g and fipronil 12.5 g a.i. per kg seed resulted in far less damaged leaves than after the standard treatment with parathion-ethyl.

Percentage of attacked leaves per leaf number, 1999 60 untreated

50 1 x parathion-ethyl 17.5 g imidacloprid 12.5 g fipronil 40 96 g spinosad

10 Percentage of attacked leaves

0 1234567891011121314

Leaf stage (counted from the stem basis)

Fig. 1. Percentage of leaves attacked by the flea beetles per leaf number five weeks after drilling.

Figure 1 shows the percentage of leaves attacked by the flea beetles per leaf number five weeks after drilling. Results are shown for leaf stage 1 to 14, and for the highest dose of each insecticide only. The results of the field trial shows the same tendency, the attack during crop growth is increasing. Imidacloprid and fipronil seed treatment showed a lower percentage of attacked leaves up to the leaf number five. In figure 2 the percentage of attacked leaves by the flea beetles per leaf number for leaf stage 1 to 30 are shown. Results for insecticides at the optimised doses, five weeks after drilling are given. Figure 2 indicates that the three insecticides used as a seed treatment give an excellent protection against flea beetle attack. At the rates tested, thiamethoxam was significantly better compared to the other ones. This insecticide has an effect up to leaf stage 30. Parathion- methyl spray application has no effect on flea beetle attack.

Discussion

Film coating of leek seeds with fipronil was successful in controlling the onion fly (Ester and Huiting, 2001), as was the pelleting of iceberg lettuce seeds with imidacloprid in controlling aphids (Ester and Brantjes, 1998). The aim of this research was to develop an alternative (seed treatment) for the standard flea beetle control compound parathion-ethyl or parathion- methyl used as a spray application. Seed treatment places the insecticide precisely where it is

367

Percentage of attacked leaves per leaf number, 2001 100

untreated 80 3 x parathion-methyl 8.75 g imidacloprid 12.5 g fipronil 60 5.0 g thiamethoxam

20 Percentageleaves of attacked

0 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 Leaf stage (counted from the stem basis)

Fig. 2. Percentage of attacked leaves by the flea beetles per leaf number for leaf stage 1 to 30

needed to control flea beetles and so should be more effective and less injurious to predators than many spray applications. Often field sprayings are applied after the first attacks of the beetles have become visible, whereas a seed treatment protects the seedling from the very beginning of the germination. In the location used in the field trials in 1999, 2000 and 2001, the basic population was different. Tables 3 and 4 indicate the damage caused by the flea beetle (untreated plots). High average temperatures in spring resulted in rapid germination and more activity of flea beetles Of the four insecticides tested, imidacloprid, thiamethoxam and fipronil significantly controlled the flea beetle (Tables 3 and 4 and Fig.2). Similar trials on a location in the Southwest Netherlands resulted in similar results (not published). All doses of imidacloprid and thiamethoxam at rates of 10 g and 20 g a.i. seed treatment resulted in a lower number of plants in 2000 and 2001 and a lower number of leaves per plant in 1999, (Tables 4 and 2). The crop development of the imidacloprid treated seeds showed a delay in flowering and ripening of about one week. The results of spinosad treatments (24 g, 48 g and 96 g a. i.) were similar to those for the untreated control. It can therefore be concluded that this compound does not control flea beetle (Tables 3 and 4). Cullis et al.(1999) found similar effectiveness for fipronil and imidacloprid applied as a seed treatment against flea beetle attack of linseed crop. Although imidacloprid at a dose of 3.9 g a.i. per kg seed shows excellent protection in his experiments 10 days after drilling, whereas this dose was less effective in our experiments after a longer period of two and five weeks after drilling. In the field trial only in 1999, the untreated seeds without a coat show a higher percentage of attacked plants or leaves than the untreated seeds including the film coat. Ester and Neuvel (1990) found that untreated carrot seeds without a film coating had a significantly higher percentage of attacked carrot plants caused by the carrot root fly than plants of untreated seeds with a film coat in one year (1986). In the following years 1987, 1988 and 1989 the percentage of attacked carrots was significant higher in the plants of seeds treated with a film 368

coat. Ester and Jeuring (1992) found similar results in the control of the pea and bean weevil in film coated field beans. At present, no clear reason for this is known. One possibility is that the coating influences the water uptake during the germination. Another is the smell of the polymers in the coating material could have an effect as a kind of attractant or repellent to the insects. Flea beetles, pea and bean weevils as well as the carrot root fly are present at the moment of plant emergence. Field emergence was at the same level in the treatments with fipronil and spinosad as the untreated control. Cullis et al. (1999) reported that populations of the large flax flea beetle A. euphorbiae and the flax flea beetle L. parvulus, had increased considerably with the expansion of the area of linseed grown in the UK. Howard and Parker (2000) found that using trap crops drilled up to four weeks in advance of swede were most attractive to flea beetles. This could be a solution for organic farmers as well as for conventional farmers. Further work is needed to investigate the role of trap cropping in flea beetle management. Another way in controlling the flea beetle is the use of flea beetle-resistant varieties of false flax (Camelina sativa) and crambe, which may also be considered a solution to prevent flea beetle damage. Flea beetles fed little (0 - 10% consumption) on cotyledons or true leaves, and fed more (59 - 100% consumption) on cruciferes (Pachagounder, et al., 1998; Lamb Palaniswamy, 1990). Franssen and Mantel (1962) mentioned that flax varieties with blue flowers are resistant against thrips. Film-coating the seed has the additional advantage of protecting the plants from the moment of drilling, whereas the conventional spray treatment is applied after the first flea beetles have been detected, which might be too late for adequate control. Because parathion-methyl is not allowed as a spray application in flax crops, a seed treatment with an insecticide should be the best alternative. This method of control is recommended as part of the integrated pest management strategy of flax crops. In most cases, imidacloprid 8.75 g, fipronil 12.5 g active ingredient per kg seed and in one field trial the thiamethoxam 5 g. a.i. per kg seed only gave statistically better protection against flea beetles than spraying with parathion-ethyl or parathion-methyl

Acknowledgements

We thank Mrs L.J.W. de Goffau of the Crop Protection Service, Wageningen for the determination of the flea beetle samples, Mr. R. Gruppen, and Mrs M. Huisman-de Lange for their assistance in the field experiments.

References

Beaudoin, X. 1988: Disease and pest control. In: G. Marshall. (ed.), Flax: Breeding and Utilisation. Kluwer Academic Publishers, Dordrecht / Boston / London: 81-88. Clarke, B. 1987: Seed coating techniques. In: T. Martin (ed.), Application to seeds and soil. BCPC Monograph 39: 205-211. Cullis, A.G., Finch, S., Jukes, A.A. & Hartfield, C.M. 1999: Evaluation of insecticidal seed treatments for the control of flax flea beetles in spring drilled linseed. Tests of Agrochemicals and Cultivars No. 20. Ann. Appl. Biol. 134: 6-7. Ester, A. & Neuvel, J. 1990: Protecting carrots against carrot root fly larvae (Psila rosae F.) by filmcoating the seeds with insecticides. Proceedings Exper. & Appl. Entomol., N.E.V. Amsterdam. 1: 49-56. 369

Ester, A. & Jeuring, G. 1992: Efficacy of some insecticides used in coating Faba beans to control pea and bean weevil (Sitona lineatus) and the relation between yield and attack. Fabis Newsletter 30: 32-41. Ester, A. & Huiting, H.F. 2001: Filmcoating the seed of leek with fipronil to control onion thrips, onion fly and leek moth. Proceedings No 76: Seed Treatment: Challenges and Opportunities.: 159-166. Ester, A. & Brandjes, N.B.M. 1998: Pelleting the seed of iceberg lettuce (Lactuca sativa L.) and butterhead lettuce (Lactuca sativa L.var. Capitata L.) with imidacloprid to control aphids. Med. Fac. Landbouww. Univ. Gent 63/2b: 563-570. Franssen, C.J.H. & Mantel, W.P. 1962: Tripsen in vlas en hun betekenis voor de vlascultuur. Mededelingen no.300.van het IPO te Wageningen: 1-77. Gruev, B., Merkl, O. & Vig, K. 1993: Geographical distribution of Alticinae (Coleoptera, Chrysomelidae) in Romania. Annales Historico-naturales Musei Nationalis Hungarici, 85: 75-132. Howard, J.J. & Parker, W.E. 2000: Evaluation of trap crops for the management of Phyllotreta flea beetles on brassicas. In: The BCPC Conference – Pests & Diseases: 975- 980. Lamb, R.J. & Palaniswamy, P. 1990: Host discrimination by a crucifer-feeding flea beetle, Phyllotreta striolata (F.)(Coleoptera: Chrysomelidae). Canadian Entomologist 122: 817- 824. Miles, M. & Dutton, R. 2000: Spinosad – a naturally derived insect control agent with potential for use in integrated pest management systems in greenhouses. In: The BCPC Conference – Pests & Diseases: 339-344. Oakley, J.N., Corbett, S.J., Parker, W.E. & Young, J.E.B. 1996: Assessment of risk and control of flax flea beetles. In: Brighton crop protection conference – Pests & Diseases: 191-196. Pachagounder, P., Lamb, R. & Bonnaryk, R.P. 1998: Resistance to the flea beetle Phyllotreta cruciferae (Coleoptera: Chrysomelidae) in false flax, Camelina sativa (Brassicaceae). The Canadian Entomologist 130: 235-240. Vig, K. 1997: Leaf beetle collection of the Matra Museum, Gyöngyös, Hungary (Coleoptera, Chrysomelidae sensu lato). Folia Historico Naturalia Musei Matraensis 22: 175-201. 370

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 p. 371

Effects of chemical control programs against cabbage pests on ground dwelling fauna

J. Freuler1, G. Blandenier2, H. Meyer3 & P. Pignon1 1 Swiss Federal Research Station for Plant Production, Changins, 1260 Nyon, Switzerland 2 Groupe d'arachnologie, Musée d'histoire naturelle, Avenue L.-Robert 63, 2300 La Chaux- de-Fonds, Switzerland 3 Chemin des Vignes 13, biologiste, 1027 Lonay, Switzerland

Abstract: Present agricultural policies seek to revitalise agricultural landscapes, and at the same time maintain a healthy, economically viable agriculture. The creation of areas removed from agricultural production aims not only to preserve but also to enrich biodiversity. Epigeal fauna play an important role in these schemes. It is thought that some of their arthropod members possess bioindicator characteristics permitting an evaluation of the quality of the environment. For this reason, over the last few years, the number of studies on this subject has increased. The present study highlights the species richness of certain elements of the epigeal fauna in a white cabbage field. Furthermore, the experiment compared effects of two different insecticide programmes on the arthropods. From the 8.6 to the 21.9.1994 the activity density of spiders, carabids, staphylinids and ants in a field of white cabbage was estimated by means of pitfall traps. The field was divided into three equal plots, one of which was treated with broad spectrum insecticides (fonofos, dimethoate and cypermethrin), another with selective insecticides (pirimicarb and Bacillus thuringiensis), while the third plot remained untreated. 31 species of spiders, 35 species of carabids, and 22 species of staphylinids were found. Insecticide treatment did not fundamentally modify the composition of species. However, a reduction in the number of catches of web spiders, dominated by Oedothorax apicatus of the Linyphiidae family, was observed following treatment with broad spectrum insecticides. The same was true for carabid beetles, dominated by Bembidion quadrimaculatum. This species is proposed as an indicator of springtime surface treatment effects on beneficial fauna. Staphylinids are sensitive to fonofos as an early soil treatment. Ants did not appear to be a suitable measurement of pesticide side effects.

Key words: Epigeal fauna, vegetable agroecosystem, side effects, insecticides, cabbage pests.

References

Freuler J., Pignon P., Blandenier G., Meyer H., 2000. Effets sur la faune épigée de programmes de lutte insecticide dans une culture de chou blanc. Revue suisse Vitic., Arboric., Hortic. 32(4): 199-204. Freuler J., Blandenier G., Meyer H., Pignon P., 2001. Epigeal fauna in a vegetable agroecosystem. Bull Soc. Ent. Suisse 74: 17-42.

371 372

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 373-375

Efficiency of Proagro 100 SL (imidacloprid) in controlling of cabbage aphid Brevicoryne brassicae L on cauliflower cv. Berliński

J. Narkiewicz-Jodko1, B. Nawrocka1 & J. Świętosławski2 1 Research Institute of Vegetable Crops, 96-100 Skierniewice, Poland. 2 Pest Control News Laboratory, ul. Forteczna 10, 32-513 Jaworzno, Poland.

Abstract: Two field experiment were carried out at the Research Institute of Vegetable Crops in Skierniewice on the efficiency of Proagro 100 SL in the control of cabbage aphid. Proagro 100 SL was applied in the rate of 0.25 l/ha. The standard treatment were: Pirimix 100 PC in dosage of 0.6 l/ha and Nurelle D 550 EC in dosage 0.6 l/ha. The experiments included four replicates in a randomized block desing. Treatments were applied with a knapsack sprayer using 600 litters of liquid per 1 hectare. In the both experiments Proagro 100 SL gave a very good effect in control of aphids.

Key words: cabbage aphids, Proagro 100 SL, cauliflower.

Introduction

The cabbage aphid is the most important pest of cauliflower and late cultivar of head cabbage. Heavy infestation can destroy up to 50 % of potential yield. The beginning of cauliflower and cabbage plant infestation by cabbage aphids take place in the second ten days of June. The pest population reach the first pick between the end of July and first ten days of August and second in September. Intensive use of insecticides in controlling of cabbage aphids have effectively accelerated resistant strains of aphids development. Searching for new insecticides and methods of controlling the pest are required. Proagro 100 SL belongs to the new nitroguanidine group of active ingredients. This product is a low toxicity, systemically acting insecticide with broad spectrum of activity. The active ingredient imidacloprid, act also as a stomach and contact insecticide. Proagro 100 SL permits the effective control of insect strain which have developed resistance to organophosphorus compounds, carbamates and pyrethroids. Experiments on the efficiency of some new insecticides and methods in controlling of cabbage aphids were carried out among others by: Freuler et al. (2003), Richter et al. (2001), Wojciechowicz-Żytko (2003), Wauters (1993), Puiggres et al. (1997), Narkiewicz-Jodko (1995, 1966, 1966a &1999), Epperlein et al. (1993), Schoonejans et al. (1993) and Bay et al. (1991).

Materials and method

Two field experiments were carried out by the Research Institute of Vegetable Crops in Skierniewice and in Miedniewice to control the cabbage aphid Brevicoryne brassicae L. by applying the Proagro 100 SL. The experiment were done in randomized block design in four replications. The Proagro 100 Sl was applied in the rate of 0.25 l/ha. Pirimix 100 PC at the rate of 0.6 l/ha and Nurelle D 550 EC at the rate 0.6 l/ha were used as the standard chemical treatment. Sprays were applied from the knapsack sprayer at the rate of 600 l of liquid per 1 hectare. To determine the efficiency of Proagro 100 SL in cabbage aphid control, the number of living aphids were recorded from 5 plants on each plot at 24 hours before treatments and 3, 7 and 14 days after.

373 374

Results and discussion

The results of the experiments are presented in tables 1 and 2. Proagro 100 SL applied at the rate of 0.25 l/ha performed very well in the control of cabbage aphid in experiment done at Skierniewice and killed 100% of the pests 3 days after treatment. Proagro100 SL was as good as standard treatment (Tab.1) Also in the second experiment done in Miedniewice, Proagro 100 SL in the rate of 0.25 l/ha was very effective and destroyed over 99% of the pests in 3 days after treatment (Tab. 2). Proagro 100 SL was as effective as standard insecticide. On the base of this experiments it can be concluded that Proagro 100 SL is very effective in cabbage aphid control. The number of experiments done in Poland showed a very good efficiency of imidacloprid also in control of black bean aphid, carrot fly, onion fly and other pests.

Table 1. The efficiency of Proagro 100 SL in control of cabbage aphid Brevicoryne brassicae L. on cauliflower. Field experiment, Skierniewice 2001.

mean numbers of living aphids per plant Combinations before days after treatment treatment 3 7 14 Proagro 100 SL – 0.25 l/ha 58.1 0.0a* 0.0a 0.0a Pirimix 100 PC – 0.6 l/ha 42.5 0.0a 0.0a 0.0a Control 140.8 191.4b 272.5b 256.5b *Newman-Keleus test α = 0.05

Table 2. The efficiency of Proagro 100 SL in control of cabbage aphid Brevicoryne brassicae L. on cauliflower. Field experiment, Miedniewice 2001.

mean numbers of living aphids per plant Combinations before days after treatment treatment 3 7 14 Proagro 100 SL – 0.25 l/ha 51.0 0.3a* 0.3a 0.0a Nurelle D 550 EC – 0.6 l/ha 31.3 0.3a 0.3a 0.0a Control 41.3 49.5b 32.6b 29.5b *Newman-Keleus test α = 0.05

References

Bay D., Luminis S.C.R., Leicht W., Breer H. & Sattelle D.B. 1991. Actions of imidacloprid and a related nitromethylene on cholinergic receptors of an identified insect motor neurone. Pesticide Science 33: 197-204. Epperlein K. & Schaberlein W. 1993. Zum Einfluss von Imidacloprid am Rübensaatgut auf Schädlinge und Nützlinge der Zuckerrübe. 105. VOLUFA Kongress, Hamburg. Kurzfass. d. Vorträge: 99 Freuler J., Fischer S., Mittaz C., H. & Terrettaz C. 2003. The role of banker plants in the enhancement of the action of Diaeretiella rapae (M’Intosh) (Hymenoptera, Aphidiinae) 375

the primary parasitoid of the cabbage aphid Brevicoryne brassicae (L.). IOBC wprs Bulletin 26(3): 277-299. Narkiewicz-Jodko J. 1995. Preliminary trials on the efficiency of chemical control of cabbage aphids (Brevicoryne brassicae L.). Med. Fac. Landbouww. Univ. Gent. 60/36: 941-943. Narkiewicz-Jodko J. 1996. Gaucho 350 FS do ochrony warzyw przed szkodnikami. Hasło Ogrodnicze 3: 22. Narkiewicz-Jodko J. 1996. Gaucho 350 FS nowa skuteczna zaprawa. Owoce Warzywa Kwiaty: 5 Narkiewicz-Jodko J. 1999. Confidor 200 SL zwalczanie mączlika szklarniowego. Hasło Ogrodnicze: 5 Puiggros I.M., Margues X., Mansanet V. & Sanz J.V.1997. Confidor un nuevo concepto de protection contra el minador de los citricos. Phytoma Espana No 92, October. Schoonejans T., De Maeyer L., Tossen H., Dhollander R., Sysmans J., Baets S. & Vicinaux C. 1991. Etude de l’insecticide systemique imidacloprid en betteraves cereales cultures maraicheres et ornementales en Belgique. Med. Fac. Landbouww. Rijksuniv. Gent. 56/36: 1161-1179. Wauters A. 1993. Raport de l’imidacloprid comme traitment de semences en culture betteraviere en Belgique. Med. Fac. Landbouww. Univ, Gent 58/2a: 249-255. Wojciechowicz-Żytko E. 2003. The effect of broad bean cultivars sowing time on the occurrence of Aphis fabae Scop and its predators. IOBC wprs Bulletin 26(3): 325-330.

376

Integrated Control in Field Vegetable Crops IOBC wprs Bulletin 26 (3) 2003 pp. 377-379

Preliminary trials on the efficiency of the Pirimix 100 PC (pirimicarb) in controlling of black bean aphid (Aphis fabae Scop.) on broad bean cv. Hangdown biały

J. Narkiewicz-Jodko1, M. Rogowska1 & J. Świętosławski2 1 Research Institute of Vegetable Crops, ul. Konstytucji 3 Maja 1/3, 96-100 Skierniewice, Poland 2 Pest Control News Laboratory, ul. Fortuna 10, 32-513 Jaworzno, Poland

Abstract: Two field experiment were carried out at the Research Institute of Vegetable Crops in Skierniewice on the efficiency of Pirimix 100 PC in the control of black bean aphids. Pirimix 100 PC was applied at the rate of 0.6 l/ha. The standard treatment was Pirimor 25 WG – 0.6 kg/ha. In the both experiments Pirimix 100 PC gave very goog effect and killed 100 % of the aphids.

Key words: Black bean aphid, Pirimix 100 PC ( pirimicarb)

Introduction

Pirimix 100 PC – Polish insecticide from carbamate group. contains 100 g of active ingredient of pirimicarb in one liter and non harmful additives. which stimulate action of Pirimicarb. The experiments carried out in the Institute of Vegetable Crops. Institute of Plant Protection, Institute of Pomology and Floriculture in Poland. has showed a good results of Pirimix 100 PC in different species of aphids control. In 1998 two field experiments were carried out on control of the black bean aphids by applying the Pirimix 100PC. The black bean aphids is the most important pest of broad bean in Poland. In case of heavy infestation she can destroyd up to 80% of potencial crop. Mass flieght of black bean aphids to the bean plantation take place generaly at the beginning of June. Permanet use of the some insecticides to aphids control have effectiveli accelerate resistand strains development. Under these circumstances searching for new insecticides and methods of control are required. The experiments on the control of aphids using some new natural and chemicals methods were carried out among others by Freuler et al (2001), Gadomska (1994), Jaworska (1996), Kelm (1994), Malinowski et al. (1996), Narkiewicz-Jodko (1992, 1995, 1997), Narkiewicz-Jodko et al. (1996), Richter et al. (2001), Ridel (2001), Wojciechowicz-Żytko (2001).

Materials and method

Field experiments were carried out at the Research Institute of Vegetable Crops in Skierniewice for control the black bean aphid (Aphis fabae Scop.) by applying the Pirimix 100 PC. The experiments were conducted in a randomized block design. Each treatment being replicated four times. The Pirimix 100 PC was applied in the rate of 0.6 l/ha. Pirimor 25 WG was used as the standard chemical treatment at the rate of 0.6 kg/ha. Sprays were applied from a knapsack sprayer at the rate of about 600 liters of liqud per one hectare. To determine the efficiency of Pirimix 100 PC the numbers of living aphids were recorded on 5 plants on each plot before and indifferent times after treatment.

377 378

Results and discussion

The results of the experiments are presented in table 1 and 2. As seen in table 1 Pirimix 100 PC applied at the rate of 0.6 l/ha gave very good results in the control of black bean aphid and killed 100 % of the pest one day after treatment. Also in the second experiment Pirimix 100 PC – 0.6 l/ha was effective and killed one day after treatment 94 % of the aphids. Hundred % of control was obtained six days after treatment (table 2). The above experiment showed that Pirimix 100 PC performed very well in black bean aphid conrol Pirimix 100 PC has high insecticidal activity, provides quick killing action and long lasting effect. Pirimix 100 PC was as effective as standard – Pirimor 25 WG which contains 2.5 times more of active ingredient. At present Pirimix 100 PC is registered in Poland for aphids control on all of the more important: agricultural. horticultural and ornomentals plants.

Table 1. The efficiency of Pirimix 100 PC in controlling of black bean aphid (Aphis fabae Scop.) on broad bean cv. Hangdown biały. Skierniewice 1998

Mean no. of living aphids per plant Combination Before Number days after treatment treatment 1 4 6 Pirimix 100 PC – 0.6 l/ha 182.5 0.0 0.0 0.0 Pirimor 25 WG – 0.6 kg/ha 209.0 0.0 0.0 0.0 Control 179.5 216.5 261.0 231.5 Treatment – 01.06.1998 LSD (α=0.05) – 01.06 - 93.11 05.06 - 102.56 08.06 - 171.80

Table 2. The efficiency of Pirimix 100 PC in controlling of black bean aphid (Aphis fabae Scop.) on broad bean cv. Hangdown biały. Powiercie 1998

Mean no. of living aphids per plant Combination Before Number days after treatment treatment 1 4 6 Pirimix 100 PC – 0.6 l/ha 235.5 13.0 5.5 0.0 Pirimor 25 WG – 0.6 kg/ha 168.3 10.3 1.6 0.0 Control 198.0 224.0 260.0 275.0 Treatment – 04.06.1998 LSD (α=0.05) – 05.06 - 4.90 08.06 – 12.36 10.06 – 5.97

References

Freuler J., Fischer S., Mittaz C. H. & Terrettaz C., (2001). Enhancement of Diaeretiella rapae to control the cabbage aphid Brevicoryne brassicae. IOBC wprs Bulletin 26(3): 277-299. 379

Gadomski H. (1994). The effectiveness of Diaeretiella rapae (McIntosh) in the reduction of the cabbage aphid Brevicoryne brassicae L. on cruciferous crops. Aphids and other hemopterous insects 4. PAS. Skierniewice: 41-46. Jaworska T. (1996). The role of Carabidae in controlling Aphis fabae (Scop.). Aphids and other hemopterous insects 5. PAS. Skierniewice: 83-88. Kelm M. (1994). Effect of nitrogen fertilization on the cabbage aphid (Brevicoryne brassicae L.) in oilseed rape crop. Aphids and other hemopterous insects 4. PAS. Skierniewice: 27- 32. Narkierwicz-Jodko J. (1992). The effectiveness of Marshal 25 EC (Carbosulfan) in control of some vegetable pests. Med. Fac. Landbouww. Univ. Gent. 57/3a: 801-803. Narkierwicz-Jodko J., Rogowska M. (1996). The effectiveness of Aztec 140 EW (Triazamate) in the control of cabbage aphid (Brevicoryne brassicae L.) and black bean aphid (Aphis fabae Scop.) Aphids and other hemopterous insects 5. PAS. Skierniewice: 131-136. Narkierwicz-Jodko J. (1997). The effectiveness of Orion 30 EC (Alanycarb) in controlling of cabbage aphid (Brevicoryne brassicae L.). Biuletyn Warzywniczy XLV. Instytut Warzywnictwa: 105-107. Narkierwicz-Jodko J. (1995).Preliminary trials on the efficiency of the chemical control of cabbage aphids (Brevicoryne brassicae L.). Med. Fac. Landbouww. Univ. Gent. 60/3b: 941-943. Richter E. & Hommes M. (2001). Can flower strips support the natural control of aphids in vegetable crops. IOBC wprs Working Group on Integrated Control of Field Vegetables. Kraków Agricultural University 14.10-17.10.2001 (Oral presentation). Riedel W. (2001). Distribution of Hover flies (Diptera: Syrphidae) and aphids (Hemiptera: Aphididae) in Lettuce Field with Flowering Strips. IOBC wprs Working Group on Integrated Control of Field Vegetables. Kraków Agricultural University 14.10- 17.10.2001 (Oral presentation). Wojciechowicz-Żytko E. (2001). The effect of broad bean cultivars sowing time on the occurance of Aphis fabae Scop. and its predators. IOBC wprs Bulletin 26(3): 325-330.