Biological Control Programmes in 2001–2012 This page intentionally left blank Biological Control Programmes in Canada 2001–2012

Edited by

P.G. Mason1 and D.R. Gillespie2

1Agriculture and Agri-Food Canada, , , Canada; 2Agriculture and Agri-Food Canada, Agassiz, British Columbia, Canada

iii CABI is a trading name of CAB International

CABI Head Offi ce CABI Nosworthy Way 38 Chauncey Street Wallingford Suite 1002 Oxfordshire OX10 8DE Boston, MA 02111 UK USA

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Chapters 1–4, 6–11, 15–17, 19, 21, 23, 25–28, 30–32, 34–36, 39–42, 44, 46–48, 52–56, 60–61, 64–71 © Crown Copyright 2013. Reproduced with the permission of the Controller of Her Majesty’s Stationery. Remaining chapters © CAB International 2013. All rights reserved. No part of this publication may be reproduced in any form or by any means, electroni- cally, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners.

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

Library of Congress Cataloging-in-Publication Data Biological control programmes in Canada, 2001-2012 / [edited by] P.G. Mason and D.R. Gillespie. p. cm. Includes bibliographical references and index. ISBN 978-1-78064-257-4 (alk. paper) 1. pests--Biological control--Canada. 2. Weeds--Biological con- trol--Canada. 3. Phytopathogenic microorganisms--Biological control- -Canada. 4. Biological pest control agents--Canada. I. Mason, P. G. (Peter G.) II. Gillespie, David Roy.

SB933.32.C2B57 2013

632’.7--dc23 2013002768

ISBN-13: 978 1 78064 257 4

Commissioning editor: Rachel Cutts Editorial assistant: Alexandra Lainsbury Production editor: Shankari Wilford

Typeset by Columns Design XML Limited, Reading Printed and bound in the UK by CPi Group (UK) Ltd, Croydon, CR0 4YY Contents

Contributors xi Foreword xix Preface xxiii Acknowledgements xxv

1 Regulation of Biological Control in Canada 1 Peter G. Mason, J. Todd Kabaluk, Brian Spencer and David R. Gillespie 2 Access and Benefi t Sharing and Biological Control 6 Peter G. Mason and Jacques Brodeur 3 Climate Change and Biological Control in Canada 12 David R. Gillespie, Owen O. Olfert and Matthew J.W. Cock 4 New Tools in Biological Control: Molecular Markers and Mathematical Models 22 Tara D. Gariepy and Bernie D. Roitberg 5 A Novel Approach for Developing Microbial Biopesticides 37 Susan M. Boyetchko and Antonet M. Svircev 6 Reproductive Parasites: Symbiotic Bacteria for Potential Use in Biological Control 43 Kevin D. Floate and George K. Kyei-Poku 7 Acantholyda erythrocephala L., Pine False Webworm (: Pamphiliidae) 54 D. Barry Lyons 8 assectella (Zeller), (: ) 56 Peter G. Mason, Wade H. Jenner, Andrea Brauner, Ulrich Kuhlmann and Naomi Cappuccino 9 Agrilus planipennis Fairmaire, Emerald Ash Borer (Coleoptera: Buprestidae) 62 D. Barry Lyons 10 spp. L., Wireworms and Click (Coleoptera: Elateridae) 72 Todd Kabaluk, Alida Janmaat, Claudia Sheedy, Mark Goettel and Christine Noronha

v vi Contents

11 Anoplophora glabripennis (Motschulsky), Asian Longhorned (Coleoptera: Cerambycidae) 82 Jean J. Turgeon and Michael T. Smith 12 Aphis glycines Matsumura, Soybean (: Aphididae) 93 Jacques Brodeur 13 Aphis gossypii Glover, Melon/Cotton Aphid, Aulacorthum solani (Kaltenbach), Foxglove Aphid, and Other Pests in Greenhouse Crops 98 Rosemarije Buitenhuis, Graeme Murphy and Les Shipp 14 Bactericera cockerelli (Sulc), Tomato/Potato Psyllid (Hemiptera: Triozidae) 107 Robert R. McGregor 15 Cephus cinctus Norton, Wheat Stem Sawfl y (Hymenoptera: ) 112 Héctor Cárcamo and Brian Beres 16 Ceutorhynchus obstrictus (Marsham), Cabbage Seedpod (Coleoptera: ) 119 Tim Haye, Peter G. Mason, Lloyd M. Dosdall, Dave R. Gillespie, Gary A.P. Gibson and Ulrich Kuhlmann 17 Choristoneura rosaceana (Harris), Obliquebanded Leafroller (Lepidoptera: ) 130 Joan Cossentine, Charles Vincent, Mike Smirle and Jean-Charles Côté 18 Contarinia nasturtii Kieffer, Swede Midge (Diptera: Cecidomyiidae) 134 Paul K. Abram, Guy Boivin, Tim Haye and Peter G. Mason 19 Cydia pomonella (L.), (Lepidoptera: Tortricidae) 139 Joan Cossentine and Charles Vincent 20 Delia radicum (L.), Cabbage Maggot (Diptera: Anthomyiidae) 142 Neil J. Holliday, Lars D. Andreassen, Peggy L. Dixon and Ulrich Kuhlmann 21 Drosophila suzukii (Matsumura), Spotted Wing Drosophila (Diptera: Drosophilidae) 152 Howard M.A. Thistlewood, Gary A.P. Gibson, David R. Gillespie and Sheila M. Fitzpatrick 22 formosana Scopoli, Cherry Bark Tortrix (Lepidoptera: Tortricidae) 156 Wade H. Jenner, Emma J. Jenner, Ulrich Kuhlmann, Andrew M. Bennett and Joan E. Cossentine 23 ochrogaster (Guenée), Redbacked Cutworm, Euxoa messoria (Harris), Darksided Cutworm, and Euxoa auxiliaris (Grote), Army Cutworm (Lepidoptera: ) 164 John Gavloski and Vincent Hervet 24 pumila Leach, , (Konow), Ambermarked Birch Leaf Miner (Hymenoptera: ) 175 Chris J.K MacQuarrie, David W. Langor, Scott C. Digweed and John R. Spence 25 Haematobia irritans L., Horn , Musca domestica L., House Fly, and Stomoxys calcitrans (L.), Stable Fly (Diptera: Muscidae) 182 Kevin D. Floate, Tim J. Lysyk and Gary A.P. Gibson 26 Harmonia axyridis (Pallas), Multicolored Asian Ladybeetle (Coleoptera: Coccinellidae) 192 Charles Vincent and Gary Pickering Contents vii

27 (Klug), European Sawfl y (Hymenoptera: Tenthredinidae) 198 Charles Vincent, Dirk Babendreier, Ulrich Kuhlmann and Jacques Lasnier 28 Lambdina fi scellaria (Guenée), Hemlock Looper (Lepidoptera: Geometridae) 203 Christian Hébert and Jacques Brodeur 29 Lilioceris lilii (Scopoli), Lily Leaf Beetle (Coleoptera: Chrysomelidae) 208 Naomi Cappuccino, Tim Haye, Lisa Tewksbury and Richard Casagrande 30 Listronotus oregonensis (LeConte), Carrot Weevil (Coleoptera: Curculionidae) 214 Guy Boivin 31 Lygus lineolaris (Palisot), Tarnished Plant Bug (Hemiptera: Miridae) 221 A. Bruce Broadbent, Tim Haye, Tara D. Gariepy, Owen Olfert and Ulrich Kuhlmann 32 Mamestra confi gurata Walker, Bertha Armyworm (Lepidoptera: Noctuidae) 228 Martin A. Erlandson 33 Oulema melanopus (L.), Cereal Leaf Beetle (Coleoptera: Chrysomelidae) 233 Swaroop V. Kher, Lloyd M. Dosdall and Héctor Cárcamo 34 Panonychus ulmi (Koch) European Red (Trombidiformes: Tetranychidae) 238 Howard M.A. Thistlewood, Noubar J. Bostanian and J. Michael Hardman 35 Phyllonorycter blancardella (Fabricius), Spotted Tentiform Leafminer (Lepidoptera: Gracillariidae) 244 Charles Vincent, John T. Huber, Gary A.P. Gibson, and Henri Goulet 36 Phyllotreta cruciferae (Goeze), Crucifer Flea Beetle and P. striolata (Fabricius), Striped Flea Beetle (Coleoptera: Chrysomelidae) 248 Juliana J. Soroka 37 Plutella xylostella (L.), Diamondback Moth (Lepidoptera: Plutellidae) 256 Sadia Munir, Lloyd M. Dosdall, Juliana J. Soroka, Owen Olfert and Ruwandi Andrahennadi 38 Sirex noctilio Fabricius (Hymenoptera: Siricidae) 263 Kathleen Ryan, Sandy M. Smith and Jean J. Turgeon 39 Sitodiplosis mosellana (Géhin), Orange Wheat Blossom Midge (Diptera: Cecidomyiidae) 272 John F. Doane, Owen O. Olfert, Robert H. Elliott, Scott Hartley and Scott Meers 40 Sitona spp. Germar, Broad Nosed (Coleoptera: Curculionidae) Héctor Cárcamo and Mehgan Vankosky 277 41 Synanthedon myopaeformis (Borkhausen), Apple Clearwing Moth (Lepidoptera: Sesiidae) 285 Joan Cossentine, V. Marius Aurelian and Gary J.R. Judd 42 Trichoplusia ni Hübner, Cabbage Looper (Lepidoptera: Noctuidae) 291 Martin A. Erlandson 43 Ambrosia artemisiifolia L., Common Ragweed (Asteraceae) 296 Alan K. Watson and Miron Teshler 44 Centaurea diffusa Lamarck, Diffuse Knapweed, and Centaurea stoebe subsp. micranthos (S.G. Gmel. ex Gugler) Hayek, Spotted Knapweed (Asteraceae) 302 Rob S. Bourchier and Brian H. Van Hezewijk viii Contents

45 Convolvulus arvensis L., Field Bindweed (Convolvulaceae) 307 Alec S. McClay and Rosemarie A. De Clerck-Floate 46 Cynoglossum offi cinale (L.), Houndstongue (Boraginaceae) 309 Rosemarie A. De Clerck-Floate 47 Euphorbia esula L., Leafy Spurge (Euphorbiaceae) 315 Rob S. Bourchier and Brian H. Van Hezewijk 48 Fallopia japonica (Houtt.) Ronse Decraene, Japanese Knotweed, Fallopia sachalinensis (F. Schmidt) Ronse Decraene, Giant Knotweed, Fallopia × bohemica (Chrtek & Chrtková) J. P. Bailey, Bohemian Knotweed (Polygonaceae) 321 Rob S. Bourchier, Fritzi Grevstad and Richard Shaw 49 Galium spurium L., False Cleavers, and G. aparine L., Cleavers (Rubiaceae) 329 Alec S. McClay 50 Lepidium draba L., L. chalepense L., L. appelianum Al-Shehbaz, Hoary Cresses (Brassicaceae) 332 Hariet L. Hinz, Robert S. Bourchier and Mark Schwarzländer 51 Leucanthemum vulgare Lam., Oxeye Daisy (Asteraceae) 337 Alec S. McClay, Sonja Stutz and Urs Schaffner 52 Linaria dalmatica (L.) Miller, Dalmatian Toadfl ax (Plantaginaceae) 342 Rosemarie A. De Clerck-Floate and Susan C. Turner 53 Linaria vulgaris Mill., Yellow Toadfl ax (Plantaginaceae) 354 Rosemarie A. De Clerck-Floate and Alec S. McClay 54 Lythrum salicaria L., Purple Loosestrife (Lythraceae) 363 Jim Corrigan, Dave R. Gillespie, Rosemarie De Clerck-Floate and Peter G. Mason 55 Malva pusilla Smith, Round-leaved Mallow (Malvaceae) 367 Paul D. Hildebrand, Cheryl Konoff and Klaus I.N. Jensen 56 Setaria viridis (L.) Beauvois, Green Foxtail (Poaceae) 370 Susan M. Boyetchko, Gary Peng, Russell K. Hynes and Paul Y. de la Bastide 57 Tanacetum vulgare L., Common Tansy (Asteraceae) 378 Alec S. McClay and André Gassmann 58 Taraxacum offi cinale F.H. Wigg, Dandelion (Asteraceae) 383 Alan K. Watson and Karen L. Bailey 59 Tripleurospermum inodorum (L.) Sch. Bip., Scentless Chamomile (Asteraceae) 391 Alec S. McClay, Gary Peng, Karen L. Bailey, Russell K. Hynes and Hariet L. Hinz 60 Vincetoxicum nigrum (L.) Moench, V. rossicum (Kleopow) Barbar., Swallow-Worts, Dog Strangling Vine (Apocynaceae) 402 Rob S. Bourchier, Aaron Weed, Richard Casagrande, André Gassmann, Sandy M. Smith and Naomi Cappuccino 61 Erwinia amylovora (Burrill) Winslow et al., Fire Blight (Enterobacteriaceae) 408 Antonet M. Svircev, Julie Boulé, Peter Sholberg and Alan J. Castle 62 Fusarium graminearum Schwabe (teleomorph Gibberella zeae (Schwein.) Petch.), Fusarium Head Blight Disease (Nectriaceae) 412 Jianwei He, Greg J. Boland and Ting Zhou Contents ix

63 Heterobasidion irregulare Garbel. & Otrosina, Annosus Root Rot (Bondarzewiaceae) 420 Gaston Lafl amme and Mike T. Dumas 64 Monilinia vaccinii-corymbosi (Reade) Honey, Mummy Berry (Monilinia Blight) (Sclerotiniaceae) 424 James A. Traquair, Paul D. Hildebrand, Donna H. Langdon and Greg J. Boland 65 Plasmodiophora brassicae Woronin, Clubroot of Crucifers (Plasmodiophoraceae) 429 Gary Peng, Rachid Lahlali, Russell K. Hynes, Susan M. Boyetchko, Bruce D. Gossen, Sheau-Fang Hwang, Denis Pageau, Mary Ruth McDonald and Steven E. Strelkov 66 Pythium aphanidermatum (Edson) Fitzpatrick and Pythium ultimum Trow (Pythiaceae), Seedling Damping-off and Root and Crown Rot 438 Pervaiz A. Abbasi 67 Rhizoctonia solani Kühn (Anamorphic State of Thanatephorus cucumeris (A.B. Frank) Donk), Damping-off, Root and Crown Rot, Blight, Leaf Spot, Stem Canker and Tuber Scurf (Ceratobasidiaceae) 446 James A. Traquair, Russell K. Hynes, Siva Sabaratnam and Pervaiz A. Abbasi 68 Streptomyces scabies Lambert and Loria, Common Scab or Potato Scab (Streptomycetaceae), and Verticillium dahliae Klebahn, Verticillium albo-atrum Reinke and Berthhold, Verticillium Wilt (Plectosphaerellaceae) 453 Pervaiz A. Abbasi 69 Taphrina deformans (Berk.) Tul., Peach Leaf Curl (Taphrinaceae) 463 James A. Traquair and Antonet M. Svircev 70 Xanthomonas euvesicatoria Jones et al., Xanthomonas perforans Jones et al., Xanthomonas vesicatoria (ex Doidge) Vau terin et al., Xanthomonas gardneri (ex Šuticˇ ) Jones et al., Bacterial Spot of Tomato and Pepper (Xanthomonadaceae) 466 Diane A. Cuppels and Pervaiz A. Abbasi 71 Invasive Alien and Future Biological Control Targets 474 Dave R. Gillespie and Peter G. Mason

Taxonomic index 485 This page intentionally left blank Contributors

Abbasi, Pervaiz A., Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sanford Avenue, London, Ontario N5V 4T3, Canada. Email: [email protected] Abram, Paul, Département de sciences biologiques, Université de Montréal, Montréal, Québec H1X 2B2, Canada. Email: [email protected] Andrahennadi, Ruwandi, Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Ruwandi. [email protected] Andreassen, Lars, Department of Entomology, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada. Email: [email protected] Aurelian, V. Marius, Biological Sciences Department, CW405 Biological Sciences Building, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. Email: aurelian@ ualberta.ca Babendreier, Dirk, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: d. [email protected] Bailey, Karen L., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Karen.Bailey@agr. gc.ca Bennett, Andrew M., Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: [email protected] Beres, Brian L., Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: [email protected] Boivin, Guy, Agriculture et Agroalimentaire Canada, Centre de recherches et de dévelop- pement en horticulture, 430 boulevard Gouin, Saint-Jean-sur-Richelieu, Québec J3B 3E6, Canada. Email: [email protected] Boland, Greg, J., Ontario Agricultural College, School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada. Email: gboland@uoguelph. ca Bostanian, Noubar, Agriculture et Agroalimentaire Canada, Centre de recherches et de développement en horticulture, 430 boulevard Gouin, Saint-Jean-sur-Richelieu, Québec J3B 3E6, Canada. Email: [email protected]

xi xii Contributors

Boulé, Julie, Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Highway 97, Summerland, British Columbia V0H 1Z0, Canada. Email: Julie.Boule@agr. gc.ca Bourchier, Rob, Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403-1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: [email protected] Boyetchko, Susan, Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Sue.Boyetchko@agr. gc.ca Brauner, Andrea, Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: [email protected] Broadbent, A. Bruce, Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sandford Street, London, Ontario N5V 4T3, Canada. Email: [email protected] Brodeur, Jacques, Département de sciences biologiques, Université de Montréal, Montréal, Québec H1X 2B2, Canada. Email: [email protected] Buitenhuis, Rosemarije, Vineland Research and Innovation Centre, 4890 Victoria Ave. N., Box 4000, Vineland Station, Ontario L0R 2E0, Canada. Email: Rose.Buitenhuis@ vinelandresearch.com Cappuccino, Naomi, Department of Biological Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada. Email: naomi_cappuccino@ carleton.ca Cárcamo, Héctor, Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: Hector.Carcamo@agr. gc.ca Casagrande, Richard, University of Rhode Island, CELS-PLS, Woodward Hall, Kingston, Rhode Island 02881, USA. Email: [email protected] Castle, Alan, Department of Biological Sciences, Brock University, 500 Glenridge Avenue, St Catharines, Ontario L2S 3A1, Canada. Email: [email protected] Cock, Matthew J.W., CABI, Bakeham Lane, Egham, Surrey TW20 9TY, UK. Email: m. [email protected] Corrigan, Jim, British Columbia Ministry of Forests, Lands and Natural Resource Operations, 3401 Reservoir Road, Vernon, British Columbia V1B 2C7, Canada. Email: [email protected] Cossentine, Joan E., Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Hwy 97, Summerland, British Columbia V0H 1Z0, Canada. Email: Joan. [email protected] Côté, Jean-Charles, Agriculture et Agroalimentaire Canada, Centre de recherches et de développement en horticulture, 430 boulevard Gouin, Saint-Jean-sur-Richelieu, Québec J3B 3E6, Canada. Email: [email protected] Cuppels, Diane, Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sandford Street, London, Ontario, N5V 4T3 Canada. Email: [email protected] De Clerck-Floate, Rosemarie A., Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: [email protected] de la Bastide, Paul Y., University of Victoria, Biology Department, PO Box 3020 STN CSC, Victoria, British Columbia V8W 3N5, Canada. Email: [email protected] Digweed, Scott C., Midwinter Consulting Inc., 14423 – 78 Avenue NW, Edmonton, Alberta T5R 3C2, Canada. Email: [email protected] Dixon, Peggy L., Agriculture and Agri-Food Canada, Building 25, 308 Brookfi eld Road, St John’s, Newfoundland A1E 0B2, Canada. Email: [email protected] Contributors xiii

Doane, John F., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: [email protected] Dosdall, Lloyd M., University of Alberta, 4-16B Agriculture/Forestry Centre, University of Alberta, Edmonton, Alberta T6G 2P5, Canada. Email: [email protected] Dumas, Mike T., Natural Resources Canada, Canadian Forest Service, Great Lake Forestry Centre, 1219 Queen Street East, Sault Ste Marie, Ontario P6A 2E5, Canada. Email: [email protected] Elliott, Robert H., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: [email protected] Erlandson, Martin A., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Martin. [email protected] Fitzpatrick, Shiela, Agriculture and Agri-Food Canada, Pacifi c Agriculture Research Centre, PO Box 1000, Agassiz, British Columbia V0M 1A0, Canada. Email: Shiela. [email protected] Floate, Kevin D., Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: [email protected] Gariepy, Tara D., Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sandford Street, London, Ontario N5V 4T3, Canada. Email: [email protected] Gassmann, André, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: a. [email protected] Gavloski, John, Manitoba Agriculture, Food and Rural Initiatives, Crops Branch, Box 1149, 65-3rd Ave NE, Carman, Manitoba R0G 0J0, Canada. Email: John.Gavloski@gov. mb.ca Gibson, Gary A.P., Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: Gary. [email protected] Gillespie, Dave R., Agriculture and Agri-Food Canada, Pacifi c Agriculture Research Centre, PO Box 1000, Agassiz, British Columbia V0M 1A0, Canada. Email: Dave. [email protected] Goettel, Mark, 1618 – 178 Ave S., Lethbridge, Alberta T1K 1A6, Canada. Email: bstedit@ telusplanet.net Gossen, Bruce D., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Bruce.Gossen@agr. gc.ca Goulet, Henri, Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: Henri.Goulet@ agr.gc.ca Grevstad, Fritzi, Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331, USA. Email: [email protected] Hardman, J. Michael, Agriculture and Agri-Food Canada, Atlantic Food and Horticulture Research Centre, 32 Main Street, Kentville, B4N 1J5, Canada. Email: [email protected] Hartley, Scott, Saskatchewan Ministry of Agriculture, Walter Scott Building, 125 - 3085 Albert Street, Regina, Saskatchewan S4S 0B1, Canada. Email: [email protected] Haye, Tim, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: [email protected] He, Jianwei, School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada. Email: [email protected] Hébert, Christian, Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 rue du P.E.P.S., Québec, Québec G1V 4C7, Canada. Email: [email protected]

xiii xiv Contributors

Hervet, Vincent A., Biological Sciences, WE1077, University of Lethbridge, Lethbridge, Alberta T1K 3M4, Canada. Email: [email protected] Hildebrand, Paul D., Atlantic Food and Agriculture Research Centre, Agriculture and Agri-Food Canada, 32 Main Street, Kentville, Nova Scotia B4N 1J5, Canada. Email: [email protected] Hinz, Hariet, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: h.hinz@cabi. org Holliday, Neil J., Department of Entomology, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada. Email: [email protected] Huber, John T., Natural Resources Canada, Canadian Forest Service, c/o Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: [email protected] Hwang, Sheau-Fang, Alberta Agriculture and Rural Development, 17507 Fort Road NW, Edmonton, Alberta T5Y 6H3, Canada. Email: [email protected] Hynes, Russell K., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Russell.Hynes@agr. gc.ca Janmaat, Alida, University of the Fraser Valley, Department of Biology, 33844 King Road, Abbotsford, British Columbia V2S 7M8, Canada. Email: [email protected] Jenner, Emma J., CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: e.jenner@ cabi.org Jenner, Wade H., CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: [email protected] Jensen, Klaus I.N., Box 110, Coldbrook, Nova Scotia B4R 1B6, Canada. Email: kjensen@ xcountry.tv Judd, Gary J.R., Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Hwy 97, Summerland, British Columbia V0H 1Z0, Canada. Email: Gary.Judd@agr. gc.ca Kabaluk, J. Todd, Agriculture and Agri-Food Canada, Pacifi c Agriculture Research Centre, PO Box 1000, Agassiz, British Columbia V0M 1A0, Canada. Email: Todd. [email protected] Kher, Swaroop, University of Alberta, 1-20E Agriculture/Forestry Centre, University of Alberta, Edmonton, Alberta T6G 2P5, Canada. Email: [email protected] Konoff, Cheryl, Environment Canada, Environmental Enforcement Directorate, Enforcement Branch, 45 Alderney Drive, 16th Floor, Queen Square, Dartmouth, Nova Scotia B2Y 2N6, Canada. Email: [email protected] Kuhlmann, Ulrich, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: [email protected] Kyei-Poku, George K., Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen St East, Sault Ste Marie, Ontario P6A 2E5, Canada. Email: [email protected] Lafl amme, Gaston, Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., Québec, Québec G1V 4C7, Canada. Email: Gaston. Lafl [email protected] Lahlali, Rachid, Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Rachid.Lahlali@agr. gc.ca Langdon, Donna, 1 Eagleridge Drive, Brampton, Ontario L6R 1G6, Canada. Email: [email protected] Langor, David W., Natural Resources Canada, Canadian Forest Service, Northern Forestry Centre, 5320 122 Street, Edmonton, Alberta T6H 3S5, Canada. Email: David.Langor@ NRCan-RNCan.gc.ca Contributors xv

Lasnier, Jacques, Co-Lab R&D, Division de Ag Cord Inc., 655 Delorme, Granby, Québec, J2J 2H4, Canada. Email: [email protected] Lyons, D. Barry, Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen St East, Sault Ste Marie, Ontario P6A 2E5, Canada. Email: [email protected] Lysyk, Tim J., Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: [email protected] MacQuarrie, Chris J.K., Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen St East, Sault Ste Marie, Ontario P6A 2E5, Canada. Email: [email protected] Mason, Peter G., Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, 960 Carling Avenue, Ottawa, Ontario K1A 0C6, Canada. Email: Peter.Mason@ agr.gc.ca McClay, Alec S., McClay Ecoscience, 5 Greenbriar Crescent, Sherwood Park, Alberta T8H 1H8, Canada. Email: [email protected] McDonald, Mary Ruth, University of Guelph, Kettleby Muck Crops Research Station, 1125 Woodchoppers Lane, RR#1 Kettleby, Ontario L0G 1J0, Canada. Email: [email protected] McGregor, Robert, Department of Biology, Douglas College, PO Box 2503, New Westminster, British Columbia V3L 5B2, Canada. Email: [email protected] Meers, Scott, Alberta Agriculture and Rural Development, 301 Horticulture Station Road, Brooks, Alberta T1R 1E6, Canada. Email: [email protected] Munir, Sadia, University of Alberta, 4-10 Agriculture/Forestry Centre, University of Alberta, Edmonton, Alberta T6G 2P5, Canada. Email: [email protected] Murphy, Graeme, Ontario Ministry of Agriculture, Food and Rural Affairs, Box 7000, 4890 Victoria Avenue North Vineland Station Ontario, L0R 2E0, Canada. Email: [email protected] Noronha, Christine, Agriculture and Agri-Food Canada, Crops and Livestock Research Centre, 440 University Avenue, Charlottetown, C1A 4N6, Canada. Email: [email protected] Olfert, Owen O., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Owen.Olfert@agr. gc.ca Pageau, Denis, Agriculture and Agri-Food Canada, 1468 St-Cyrille Street, Normandin, Québec G8M 4K3, Canada. Email: [email protected] Peng, Gary, Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: [email protected] Pickering, Gary, Department of Biological Sciences, Cool Climate Oenology and Viticulture Institute, Department of Psychology, Environmental Sustainability Research Centre, Brock University, St Catharines, Ontario L2S 3A1, Canada. Email: [email protected] Roitberg, Bernie D., Simon Fraser University, Department of Biological Science, Burnaby, British Columbia V5A 1S6, Canada. Email: [email protected] Ryan, Kathleen, Silv-Econ Ltd, 913 Southwind Court, Newmarket, Ontario L3Y 6J1, Canada. Email: [email protected] Sabaratnam, Siva, Abbotsford Agriculture Centre, British Columbia Ministry of Agriculture, 1767 Angus Campbell Road, Abbotsford, British Columbia V3G 2M3, Canada. Email: [email protected] Schaffner, Urs, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: [email protected] Schwarzländer, Mark, University of Idaho, Agricultural Science 237, Moscow, Idaho 83844-2339, USA. Email: [email protected] xvi Contributors

Shaw, Richard, CABI, Bakeham Lane, Egham, Surrey TW20 9TY, UK. Email: r.shaw@ cabi.org Sheedy, Claudia, Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 1st Avenue South, Lethbridge, Alberta T1J 4B1, Canada. Email: Claudia.Sheedy@agr. gc.ca Shipp, Les, Agriculture and Agri-Food Canada, Research Centre, 2585 County Road 20, Harrow, Ontario N0R 1G0 Canada. Email: [email protected] Sholberg, Peter, Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Highway 97, Summerland, British Columbia V0H 1Z0, Canada. Email: Peter. [email protected] Smirle, Michael, Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Highway 97, Summerland, British Columbia V0H 1Z0, Canada. Email: Michael. [email protected] Smith, Michael T., Department of Agriculture, Agricultural Research Service, Benefi cial Insect Introduction Research Unit, 501 S Chapel Street, Newark, Delaware 19713, USA. Email: [email protected] Smith, Sandy M., Faculty of Forestry, University of Toronto, 33 Willcocks Ave., Toronto, Ontario M5S 3B3, Canada. Email: [email protected] Soroka, Juliana J., Agriculture and Agri-Food Canada, Saskatoon Research Centre, 107 Science Place, Saskatoon, Saskatchewan S7N 0X2, Canada. Email: Julie.Soroka@agr. gc.ca Spence, John R., University of Alberta, Faculty of Agricultural, Life and Environmental Sciences, Department of Renewable Resources, 751 General Services Building, Edmonton, Alberta T6G 2H1, Canada. Email: [email protected] Spencer, Brian, Applied Bionomics, 11074 West Saanich Road, North Saanich, British Columbia V8L 5P5, Canada. Email: [email protected] Strelkov, Steven E., University of Alberta, Department of Agriculture, Food and Nutritional Sciences, Agriculture/Forestry Centre, Edmonton, Alberta T6G 2P5, Canada. Email: [email protected] Stutz, Sonja, CABI, Rue des Grillons 1, 2800 Delémont, Switzerland. Email: s.stetz@cabi. org Svircev, Antonet, Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, Vineland Research Farm, 4902 Victoria Avenue North, PO Box 6000, Vineland, Ontario L0R 2E0, Canada. Email: [email protected] Teshler, Miron, McGill University, 21111 Lakeshore Road, Ste Anne de Bellevue, Québec H9X 3V9, Canada. Email: [email protected] Tewskbury, Lisa, University of Rhode Island, CELS-PLS, Woodward Hall, Kingston, Rhode Island 02881, USA. Email: [email protected] Thistlewood, Howard M.A., Agriculture and Agri-Food Canada, Pacifi c Agri-Food Research Centre, 4200 Highway 97, Summerland, British Columbia V0H 1Z0, Canada. Email: [email protected] Traquair, James A., Agriculture and Agri-Food Canada, Southern Crop Protection and Food Research Centre, 1391 Sandford Street, London, Ontario N5V 4T3, Canada. Email: [email protected] Turgeon, Jean J., Natural Resources Canada, Canadian Forestry Service, Great Lakes Forestry Centre, 1219 Queen Street East, Sault Ste Marie, Ontario P6A 2E5, Canada. Email: [email protected] Turner, Susan C., British Columbia Ministry of Forests, Lands and Natural Resource Operations, Regional Offi ce, 441 Columbia Street, Kamloops, British Columbia V2C 2T3, Canada. Email: [email protected] Van Hezewijk, Brian, Natural Resources Canada, Canadian Forest Service, 506 West Burnside Road, Victoria, British Columbia V8Z 1M5, Canada. Email: bvanheze@nrcan. gc.ca Contributors xvii

Vankosky, Meghan, University of Windsor, Room 119 Biological Sciences Building, 401 Sunset Avenue, Windsor, Ontario N9B 3P4, Canada. Email: [email protected] Vincent, Charles, Agriculture et Agroalimentaire Canada, Centre de recherches et de développement en horticulture, 430 Boulevard Gouin, Saint-Jean-sur-Richelieu, Québec J3B 3E6, Canada. Email: [email protected] Watson, Alan K., McGill University, 21111 Lakeshore Road, Ste Anne de Bellevue, Québec H9X 3V9, Canada. Email: [email protected] Weed, Aaron S., Department of Biological Sciences, Dartmouth College, 78 College Street, Hanover, New Hampshire 03755, USA. Email: [email protected] Zhou, Ting, Agriculture and Agri-Food Canada, Guelph Food Research Centre, 93 Stone Road W., Guelph, Ontario N1G 5C9, Canada. Email: [email protected] This page intentionally left blank Foreword

Biological control of , weeds and plant diseases in Canada has a long and success- ful record in terms of both research results and implementation. A period of gradual suc- cesses and continued acceptance in the 1970s and 1980s led to initial criticism and debate in the early 1990s following concern over the potential negative impact of biologi- cal control on . Many countries however, including Canada, have developed and adopted stringent policies and procedures for ensuring risk and benefi t analysis in importation and release of biological control agents. This has addressed any public con- cerns and, at the same time, strengthened the scientifi c basis for its use. Over the last two decades the overwhelming scientifi c evidence from science groups worldwide has emphasized the past, current and future opportunities in enhancing the agricultural and forestry sectors and the natural environment through the study and use of biological con- trol practices and principles. Biological control is expected to contribute directly to recent renewed interest and action by international organizations to increase food pro- duction and provide sustainable solutions for an ever increasing world population to pre- vent loss of habitat, crop, food and forest reserves. Canada’s federal and provincial governments and universities, in partnership with other countries, non-government organizations and the industry sector itself, have supported biological control pro- grammes for over one hundred years. This work has in turn been highly recognized and appreciated by a Canadian public whose ever-increasing focus and scrutiny of the use of public funds has made it even more necessary for the biological control research com- munity to articulate the need for continued support of this work. The enormous volume of information in this review is evidence of the extent of work and success in biological control programmes in Canada over an 11 year period from 2001–2012. This volume, the fi fth in a series documenting biological control programmes in Canada, presents new information on specifi c insect, weed or plant diseases, some of which are updates of on-going studies on historical biological control projects while other chapters report on biological control efforts for new emerging invasive alien species. In each case information is presented in a consistent and logical manner, starting with the pest status in Canada, followed by a comprehensive background on previous studies, review of the use of biological control in these programmes, an evaluation of the biologi- cal control efforts and future needs in research or implementation activities. A compre- hensive reference list is also provided for each case study. A total of 64 chapters is

xix xx Foreword dedicated to biological control case studies; 36 on insect pests of agricultural importance and forestry or ornamental pests; 18 on control of weeds for crops, rangeland, pastures, ‘rights-of-way’ or aquatic areas; and 10 on biological control of plant disease causal agents. The case studies have been chosen to fully represent all major work in biological control in Canada over the past 11 years and therefore range from reports on work in bio- logical control for pests that cause major economic loss such as head blight of wheat to work on and nuisance public health concerns such as housefl y and stablefl y bio- logical control. Invited authors for this volume are each expert in their fi eld and collec- tively represent the very best team in the country working in biological control research. Depending on the particular programme, as to when work may have started or degree of effort across the country, the reports are single or multi-authored, of varying length and the described programmes are at different stages of completion. Readers not familiar with the capacity or on-going activities in biological control work in Canada will fi nd a wealth of information on current studies in a format that can be easily understood and refer- enced. Of particular interest to researchers in this fi eld will be the fi rst six chapters of the vol- ume that are dedicated to describing emerging and transformational issues or needs in the area of biological control research and implementation. The fi rst chapter on regulation of biological control in Canada addresses the aforementioned area of concern by the public that this tool is carefully regulated in terms of sound risk assessment in order to make informed science-based decisions. The need for regulatory overview, the various acts of legislation, and the agencies or departments with jurisdiction in this area and the process for complying with Canadian government law are fully explained. Linkages and cross compliance with international organizations are also described. In the second chapter the authors have been both bold and forthcoming by addressing the impact of the Access and Benefi t Sharing (ABS) objective of the treaty on Convention of Biological Diversity on bio- logical control. The chapter explains the complexity of this objective and the need for Canada to develop an ‘informed policy’ in order that collection and sharing of biological control agents may continue in a way that benefi ts all parties. The third chapter in this section identifi es the recent issue of climate change on pest populations and its impact on use of biological control. The three remaining chapters describe new tools or approaches such as the use of molecular techniques in identifying biological control agents and use of non-traditional biological control agents such as reproductive symbiotic bacteria for con- trol of reproductive functions in pests. Together this overview section provides a fi rm foundation and framework for the case study chapters by clearly identifying the chal- lenges and working environment that the researchers had to consider in their work over the past 11 years, be it national or international policy changes, advances in science or new external environmental drivers of change. The last (71st) chapter in the volume addresses the ever increasing threat of invasive alien species (IAS) and draws attention to the fact that the majority of the key insect, weed and plant disease pests of Canadian agriculture are considered to be exotic. They have been introduced accidentally in terms of arthropod and diseases or intentionally in the case of weeds through plant global trade activities. Many of the agricultural and for- estry pests described in the preceding chapters are in fact invasive alien species and the authors describe current and future needs for biological control of IAS in Canada. This volume reviews and presents new insights, information or evidence of past and current successes in employing biological control and future needs or opportunities to expand this work. The authors and contributors have made a major contribution to this fi eld in Canada over the past 11 years and are to be complimented in their tenaciousness to persevere in a climate of inconsistent or reduced funding and increased public scrutiny of public-good research. The benefi ts and return on investment from these studies are Foreword xxi clearly presented. Like the other four volumes that preceded this publication, it is expected that this work will draw attention to the benefi cial use of biological control and the excellent work that has been done in this area in Canada.

G.H. Whitfi eld PhD Research and Development Director, Agriculture and Agri-Food Canada Chair of CABI International Executive Council (2006–11) Chair of the WHO/FAO Expert Committee on Pesticide Management-JMPM (2009–11) This page intentionally left blank Preface

Biological control programmes in Canada continue to provide solutions for pest prob- lems that affect the food supply, our natural resources and the environment. These pro- grammes are aimed primarily at invasive alien species, which are increasingly disrupting the ability of Canadians to produce food, manage resources and enjoy their environment. This is the fi fth volume in the series that summarizes the work on the many target species identifi ed as important pests in Canada and covers the period 2001– 2012. During this time, studies on new pests have been initiated and studies on existing pests have continued. Most importantly, several projects are demonstrating clear suc- cess in reducing target pest numbers. The target species are primarily in agro-ecosys- tems, where activity has increased, while biological control activities in forest ecosystems have declined in the last 12 years. Biological control programmes against plant pathogens and annual weeds of crops continue to strengthen as our understanding of the complexities of plant–pathogen interactions increases. Great strides have been made in the development of inundative biological control agents that can be registered and used as commercial products. Several overview chapters are included in this volume to inform readers about emerging issues that will have an impact on biological control programmes in Canada. New research tools, such as molecular techniques, modelling and symbionts, and new approaches to organizing research that maximize resource investment, are beginning to facilitate biological control research as never before. Our understanding of how large- scale climate change will affect biological control is still in its infancy, but it is clear that there will be effects and that biological control programmes will have to adapt to these. In the past decade, greater regulatory constraints and implementation of inter- national agreements have presented new challenges, and by better understanding these, biological control programmes can continue to meet the needs of Canadians. , systematics and an evolutionary framework are critical to clearly, and unambiguously, understanding the target species and biological control agents. Recent changes to plant classifi cation and impending changes to fungal classifi cations infl u- ence research programmes by clarifying phylogenetic relationships and stabilizing nomenclature. In this volume, names for plants and fungi follow the ‘Tropicos’ and the ‘Species Fungorum’ databases (http://www.tropicos.org/ and http://www.indexfungo- rum.org/, respectively). To as great a degree as possible, names for follow the

xxiii xxiv Preface

most current catalogues available and, where available, authoritative databases, e.g. the ‘Universal Chalcidoidea Database’ (http://www.nhm.ac.uk/research-curation/research/ projects/chalcidoids/database) and ‘Taxapad’ (http://www.taxapad.com), have been used. Errors in species and higher group names that may have crept into the work are the responsibility of the editors. The stories of insects, , weeds and plant diseases written by the 120 contributors clearly show their passion for the science of biological control and their concern for Canadian agriculture, forestry and the environment.

Peter Mason and Dave Gillespie, December 2012 Ottawa, Ontario and Agassiz, British Columbia, Canada. Acknowledgements

We thank the many chapter authors (120 contributors!) who have written so clearly and enthusiastically about their study insects, mites, weeds and plant diseases. Several indi- viduals have contributed to completion of this project. Andrea Brauner assisted in the editing at various stages of the process. The advice of Fred Beaulieu, Andrew Bennett, John Bisset, Patrice Bouchard, Stephen Darbyshire, Gary Gibson, Jean-François Landry, André Levesque, Owen Lonsdale and Qing Yu on taxonomic names is greatly appreci- ated. We thank the funding agencies and organizations, which are acknowledged in the individual chapters, for the support that has enabled the research that is summarized here. Finally, we thank the managers who have provided encouragement to contributors to complete these projects. Funding to publish this work was provided by Agriculture and Agri-Food Canada. Previous volumes of this book are available on the Entomological Society of Canada website at http://www.esc-sec.ca/cabi.php.

xxv This page intentionally left blank Chapter 1 1

1 Regulation of Biological Control in Canada

Peter G. Mason,1 J. Todd Kabaluk,2 Brian Spencer3 and David R. Gillespie2 1Agriculture and Agri-Food Canada, Ottawa, Ontario; 2Agriculture and Agri-Food Canada, Agassiz, British Columbia; 3Applied Bionomics, Saanich, British Columbia

1.1 Introduction 1991; Follett et al., 2000; Louda et al., 2003) challenged the claim that introduction of Biological control of pests, including natural enemies had little or no impact on weeds, and pathogens, has a the environment. These challenges to long history in Canada. The earliest conventional thinking led to calls for attempts, dating from the late 1800s, greater scrutiny of importation and uses of consisted of moving natural enemies from biological control (see Ehler, 2000; Messing, a source location to the habitat where the 2000; Simberloff, 2011). Regulatory target pest occurred. The modern approach agencies in Canada responded by including encompasses: introduction of exotic BCA oversight in the interpretation of their natural enemies that self-propagate to respective Acts governing pest control regulate pest populations (classical); agents. Canada is seen as one of the world periodic introduction of mass-produced leaders in developing regulatory oversight natural enemies into specifi c environments of BCAs (Hunt et al., 2008, 2011). In recent to reduce pest populations (inundative); years the regulatory oversight itself has application of formulations containing changed and the following attempts to whole natural enemies or toxic com- provide an overview of the regulatory ponents of natural enemies to reduce pest process for biological control. populations (biopesticides); and manipu- lation of habitats to encourage survival and increase of natural enemies to regulate pest 1.2 Legislation populations (conservation). Government regulation of biological control agents has The government of Canada has the become essential in fostering good responsibility to provide the framework for practices that help ensure the protection of ensuring that its borders are protected for human and environmental health. For the health and well-being of Canadians. example, the need for oversight of The framework is provided through importation and release of exotic biological legislative Acts passed in the Canadian control agents (BCAs) has become in- Parliament. Organisms used as biological creasingly apparent because of concerns control agents are regulated under the about unintended effects, particularly after Plant Protection Act (1990) and the Pest several publications (e.g. Howarth, 1983, Control Products Act (2002). Under these

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 2 Chapter 1

Acts BCAs introduced for classical bio- eradicating pests in Canada.’ The PPA logical control, inundative biological governs the importation and approval of control, including commercial products, BCAs and decisions are based on assess- and formulated microbial-based bio- ment of risk. A request to import a new pesticides are regulated to ensure safety IBCA for fi rst release into the environment and quality (Parker and Gill, 2002; Mason or as a commercially sold species is and Parker, 2006; Kabaluk et al., 2010; submitted to the CFIA and must be Canadian Food Inspection Agency, 2012). accompanied by a document (petition) that Introduction of classical biological control includes information on the target species, agents may also be regulated under one or the biological control agent and potential more Provincial Acts. For example, in impacts. Guidance on preparation of a Newfoundland and Labrador Section 7.1 petition is provided by De Clerck-Floate et (dd) of the Wild Life Act applies ‘to al. (2006). Importation of candidate and prohibit or control the importation of approved BCAs from outside of Canada wildlife into the province’ and a permit is requires an import permit (CFIA, 2012). required (Newfoundland and Labrador Microbial biological control agents Wild Life Act, 1990). In British Columbia, (MBCAs), e.g. fungi, bacteria, viruses and ‘Once insects have been approved for microsporidia, that are formulated as release in Canada, the Biocontrol Com- biopesticides are regulated under the Pest mittee of the British Columbia Plant Control Products Act (PCPA). The purpose Protection Advisory Council has a fi nal of the PCPA is ‘to protect human health review of the screening report before and safety and the environment by insects are introduced into the province’ regulating products used for the control of (British Columbia Weed Control Act, pests’ and is administered by Health 1996). In Ontario, the Fish and Wildlife Canada’s Pest Management Regulatory Conservation Act, Section 54. (1) Release Agency (PMRA). Microbial biological con- of imports, applies: ‘Except with the trol organisms are considered to be authorization of the Minister, a person ‘biopesticides’ but this defi nition also shall not release wildlife or an invertebrate includes semiochemicals, biochemicals that has been transported into Ontario or and other non-conventional pest control has been propagated from stock that was products (Kabaluk et al., 2010). Sub- transported into Ontario’ (Fish and missions are made to the PMRA and must Wildlife Conservation Act, 1997), although include a covering letter, application form, the Act is not binding on the Crown (D. fees, a product specifi cation form, letters of Wales, Peterborough, 2012, pers. comm.). support and authorization, a draft label and There is no provincial legislation for BCA supporting scientifi c data (Kabaluk et al., introductions in Alberta, Saskatchewan, 2010). MBCAs that are not formulated and Manitoba, , Nova Scotia and Prince released into the environment are regulated Edward Island. These provinces rely solely under the PPA (CFIA, 2012). on federal oversight of BCAs. Costs to conduct the research to provide Invertebrate biological control agents the information in support of approval/ (IBCAs), i.e. insects, mites, and registration are high, thus harmonization nematodes, that are released into the with other jurisdictions is strongly en- environment or sold commercially are couraged, not only to offset costs but to regulated under the Plant Protection Act strengthen the assurance of BCA safety (PPA), which is within the mandate of the while hastening their entry into the market Canadian Food Inspection Agency (CFIA). as alternatives to synthetic pesticides. The purpose of the PPA ‘is to protect plant Harmonization of information requirements life and the agricultural and forestry for IBCAs has been achieved through the sectors of the Canadian economy by North American Plan Protection Organi- preventing the importation, exportation zation (NAPPO). For MBCAs, harmoni- and spread of pests and by controlling or zation has been achieved through the North Chapter 1 3

American Free Trade Agreement (NAFTA) the Biological Control Review Committee and the Organisation for Economic Co- (BCRC). This process was outlined by operation and Development (OECD). Mason and Parker (2006) and De Clerck- Floate et al. (2006); however, some changes have taken place since. A submission is 1.3 Harmonization sent to the CFIA who forward it to the BCRC with a request to conduct a review. Information requirements for IBCAs in Individual reviews are done by scientists have been developed by the with expertise in taxonomy, ecology and NAPPO Biological Control Panel, which biological control, and specialists at the includes members from the regulatory and PMRA and CFIA. The comments are sum- research arms of Canada, Mexico and the marized and a recommendation is pro- USA (http://www.nappo.org). These vided to the CFIA Plant Health Directorate regional requirements are based on those where a fi nal decision is made. The developed under the International Plant Director of the Plant Health Directorate Protection Convention of the Food and informs the applicant in writing of the Agriculture Organization of the United CFIA decision. Nations, in particular International For MBCAs, a pre-registration con- Standards for Phytosanitary Measures No. sultation with the PMRA is encouraged. 3 (IPPC, 2005). The NAPPO requirements Along with the allowance for tiered testing are outlined in two Regional Standards for and data waivers in advance of submitting Phytosanitary Measures (RSPMs), RSPM an application for registration, registrants No. 7 for phytophagous IBCAs and RSPM can avoid the collection of unnecessary or No. 12 for entomophagous IBCAs (NAPPO, redundant information for inclusion in the 2008a, b). As well, guidelines for certifi - fi nal submission package. The process for cation for movement of commercial IBCAs reviewing MBCAs is outlined by Kabaluk between NAPPO countries (RSPM No. 26) et al. (2010), and while similar to the have been developed with industry par- process for synthetic pesticides, tiered ticipation (NAPPO, 2006). Furthermore, in testing and advanced consultation make the case of phytophagous IBCAs, input is the process for MBCAs faster – around 12 sought, during the review process, from the months, and possibly shorter for PMRA- USDA Animal and Plant Health Inspection EPA joint reviews. Following an initial and Service (APHIS) technical advisory group thorough review for completeness, sub- (TAG) to ensure that IBCA approvals in mission packages received by the PMRA Canada are in line with those in the USA. are scientifi cally reviewed by specialists in The basis for harmonized information environmental toxicology, human health requirements for MBCAs is the Data Code and safety, and effi cacy. Depending on the (DACO) and its use is outlined by Kabaluk origin and intended use of the MCPA, e.g. et al. (2010). Essentially, the DACO new to Canada, registered in Canada but itemizes and codes the information, data with a proposed new use etc., different and other documentation required for review streams are followed. The highest registration and associates this information level review is for a ‘Category A’ MCPA, i.e. with similar codes used by OECD and the a technical grade active ingredient that is US Environmental Protection Agency new to Canada. The active ingredient and (EPA) whose data submissions are accept- end-use product require separate appli- able for review in Canada. cations, although the latter is greatly supported by the prior registration of the active ingredient. The regulatory decision 1.4 The Review Process on the MCPA is posted on PMRA’s website for public comment, and pending a Submissions made to the CFIA for IBCAs favourable review and the absence of are reviewed by an arms-length committee, challenges, the fi nal regulatory decision is 4 Chapter 1

made. A Certifi cate of Registration and a by several companies producing them. Of Pest Control Product (PCP) number is then the IBCAs released into nature, 22% are issued, legalizing the use and marketing of phytophagous species and the remainder the MCPA in Canada. are entomophagous. It is not known how many of these species have established. Kabaluk and Gazdik (2011) provide a 1.5 Approved Products and Agents list of microbial pesticides registered in member countries of the OECD. For Invertebrate species released in Canada as Canada, there are 85 products listed in the biological control agents number more than database with active ingredients based on 400 species. Among these, 74 are fungi, bacteria, viruses, microsporidia and ‘approved’ for commercial use and are sold nematodes.

References

British Columbia Weed Control Act (1996) Weed Control Act [RSBC 1996] CHAPTER 487, Chapter 11 Weed Containment and Control. Available at: http://www.for.gov.bc.ca/hfp/ publications/00005/Ch11.pdf (accessed 15 March 2012). Canadian Food Inspection Agency (CFIA) (2012) Plant Protection Import Requirements for Living Organisms Other than Plants (Micro-organisms and Invertebrates including Bio logical Control Agents, Tropical Butterfl ies, Earthworms, Pollinators, Snails and Slugs). D-12-02 Available at: http://www.inspection.gc.ca/plants/plant-protection/imports/eng/1324569244509/ 1324569331710 (accessed 18 December 2012). De Clerck-Floate, R.A., Mason, P.G., Parker, D.J., Gillespie, D.R., Broadbent, A.B. and Boivin, G. (2006) Guide for the Importation and Release of Arthropod Biological Control Agents in Canada. Agriculture and Agri-Food Canada A42-105/2006E. Ehler, L.E. (2000) Critical issues related to nontarget effects in classical biological control of insects. In: Follett, P.A. and Duan, J.J. (eds) Nontarget Effects of Biological Control. Kluwer Academic Publishers, Norwell, Massachusetts, pp. 3–13. Fish and Wildlife Conservation Act (1997) Service Ontario 1997, Chapter 41. Available at: http:// www.e-laws.gov.on.ca/html/statutes/english/elaws_statutes_97f41_e.htm# (accessed 28 March 2012). Follett, P.A. and Duan, J.J. (eds) (2000) Nontarget Effects of Biological Control. Kluwer Academic Publishers, Norwell, Massachusetts. Howarth, F.G. (1983) Classical biological control: panacea or Pandora’s box. Proceedings of the Hawaiian Entomological Society 24, 239–244. Howarth, F.G. (1991) Environmental impacts of classical biological control. Annual Review of Entomology 36, 485–509. Hunt, E.J., Kuhlmann, U., Sheppard, A., Qin, T.-K., Barratt, B.I.P., Harrison, L., Mason, P.G., Parker, D., Flanders, R. and Goolsby, J. (2008) Review of invertebrate biological control regulation in Australia, New Zealand, Canada and the USA: recom mendations for a harmonized European system. Journal of Applied Entomology 132, 89–123. Hunt, E.J., Loomans, A.J.M. and Kuhlmann, U. (2011) An international comparison of invertebrate biological control agent regulation: What can learn? In: Ehlers, R-U. (ed.) Regulation of Biological Control Agents. Springer, Dordrecht, the Netherlands, pp.79–112. IPPC (International Plant Protection Convention) (2005) Guidelines for the export, shipment, import and release of biological control agents and other benefi cial organisms. International Standards for Phytosanitary Measures No. 3. Available at: https://www.ippc.int/fi le_uploaded/ 1146657660135_ISPM3.pdf (accessed 6 February 2012). Kabaluk, J.T. and Gazdik, K. (2011) Directory of Biopesticides for Agricultural Crops in OECD Countries. Available at: https://www4.agr.gc.ca/MPDD-CPM/search-recherche.do?lang=eng (accessed 6 February 2012). Chapter 1 5

Kabaluk, J.T., Brooks, V.R. and Svircev, A.M. (2010) Canada. In: Kabaluk, J.T., Svircev, A.M., Goettel, M.S. and Woo, S.G. (eds) The Use and Regulation of Microbial Pesticides in Representative Jurisdictions Worldwide, pp. 59–73. Available at: http://www.iobc-gobal.org/download/ Microbial_Regulation_Book_Kabaluk_et_%20al_2010.pdf (accessed 6 February 2012). Louda, S.M., Pemberton, R.W., Johnson, M.T. and Follett, P.A. (2003) Nontarget effects – the Achilles’ Heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annual Review of Entomology 48, 365–396. Mason, P.G. and Parker, D.J. (2006) Ensuring the Safety of Biological Control in Canada. Newsletter of the Biological Survey of Canada (Terrestrial Arthropods) 25, 14–16. Messing, R.H. (2000) The impact of nontarget concerns on the practice of biological control. In: Follett, P.A. and Duan, J.J. (eds) Nontarget Effects of Biological Control. Kluwer Academic Publishers, Norwell, Massachusetts, pp. 45–55. NAPPO (North American Plant Protection Organisation) (2006) Guidelines for certifi cation of commercial arthropod biological control agents moving into NAPPO member countries. Regional Standards for Phytosanitary Measures No. 22. Available at: http://www.nappo.org/en/ data/fi les/download/PDF/RSPM26-15-10-06-e.pdf (accessed 6 February 2012). NAPPO (North American Plant Protection Organisation) (2008a) Guidelines for petition for fi rst release of non-indigenous phytophagous biological control agents. Regional Standards for Phytosanitary Measures No. 7. Available at: http://www.nappo.org/en/data/fi les/download/PDF/ RSPM7-Rev20-10-08-e.pdf (accessed 6 February 2012). NAPPO (North American Plant Protection Organisation) (2008b) Guidelines for petition for fi rst release of non-indigenous entomophagous biological control agents. Regional Standards for Phytosanitary Measures No. 12. Available at: http://www.nappo.org/en/data/fi les/download/ PDF/RSPM12-Rev20-10-08-e.pdf (accessed 6 February 2012). Newfoundland and Labrador Wild Life Act (1990) RSNL1990 CHAPTER W-8, An Act Relating to Wild Life. Queen’s Printer, St John’s, Newfoundland and Labrador, Canada. Available at: http:// www.assembly.nl.ca/legislation/sr/statutes/w08.htm (accessed 14 March 2012). Parker, D.J. and Gill, B.R. (2002) and biological control. In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 1–4. Pest Control Products Act (2002) Department of Justice, Ottawa, Canada. Available at: http://laws. justice.gc.ca/PDF/P-9.01.pdf (accessed 6 February 2012). Plant Protection Act (1990) Department of Justice, Ottawa, Canada. Available at: http://laws-lois.justice. gc.ca/eng/acts/P-14.8 (acces sed 6 February 2012). Simberloff, D. (2011) Risks of biological control for conservation purposes. BioControl 57, 263–276. 6 Chapter 2

2 Access and Benefi t Sharing and Biological Control

Peter G. Mason1 and Jacques Brodeur2 1Agriculture and Agri-Food Canada, Ottawa, Ontario; 2Université de Montréal, Montréal, Québec

Biological control is a pest management 2.1 Convention on Biological Diversity strategy used primarily against invasive and the Nagoya Protocol alien species that have become pests in regions where they have newly invaded. The Convention on Biological Diversity Biological control can also be used in (CBD) resulted from the 1992 ‘Earth confi ned environments where pest out- Summit’ conference in Rio de Janeiro, breaks occur. Classical biological control Brazil. The CBD is an international, legally relies on natural enemies from the area of binding treaty signed by 168 countries origin being introduced into the invaded (Convention on Biological Diversity, 2012). region to suppress populations of the The CBD has three main objectives: target pest. Inundative biological control • Conservation of biological diversity; involves the mass production of natural • Sustainable use of its components; enemies, often from the area of origin, • Fair and equitable sharing of benefi ts which are released in high numbers into arising from genetic resources. an environ ment where the target pest is present at economic levels. Historically, Although the CBD is one of the most exploration for natural enemies, their important treaties in the history of capture and preservation for identifi cation, humanity as it concerns the diversity of life and culture for studies on biology and host on earth (Prathapan and Rajan, 2011), specifi city have been achieved through specifi c methods of implementation, initiatives sponsored by the countries enforcement etc. were not provided. Thus, where the alien species has caused eco- participating countries were left to nomic or environ mental damage. Access to determine how to comply with the these genetic resources, specifi cally, agreement using whatever resources they biological control agents, was only limited had available. by funding levels or political confl icts that The third objective on Access and presented safety issues. However, in the Benefi t Sharing (ABS) came into effect in last 20 years geo-political developments 2010. After years of negotiation, the 10th such as the Con vention on Biological Conference of Parties to the CBD met in Diversity have presented new challenges Nagoya, Japan in October 2010 to fi nalize with the potential to impede biological an agreement that will contribute to the control. conservation and sustainable use of

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 2 7

biodiversity – the ‘Nagoya Protocol on agents (Cock, 2010). As with other areas of access to genetic resources and the fair and non-commercial research, such as equitable sharing of benefi ts arising from taxonomy, ecology and general biodiversity their utilization’. (see Feit et al., 2005), biological control is The Nagoya Protocol is an agreement caught between the intent to prevent between the signatory countries of the CBD biopiracy and the need to understand and as to how access and benefi t sharing of preserve biodiversity. The result is that genetic resources will be handled in future prior informed consent and mutually and this includes biological control agents agreed terms, possibly with monetary or (United Nations, 2010). Based on the non-monetary benefi t-sharing mechanisms, Nagoya Protocol, each country has the will need to be developed for each responsibility to prepare its own legislation biological control initiative with each and regulations. Article 8 ‘Special Con- country that is a source of potential agents siderations’ of the Nagoya Protocol states: (Cock et al., 2010). Cock et al. (2009, 2010) and Haas et al. (2010) cite examples where In the development and implementation of its access and benefi t-sharing legislation or ABS legislation already in place has regulatory requirements, each Party shall: hindered biological research far more than it has protected a nation’s biota. The (a) Create conditions to promote and success of biological control has benefi ted encourage research which contributes to the global community. In particular, poorer the conservation and sustainable use of biological diversity, particularly in countries have shared the benefi ts when developing countries, including through other nations have invested to discover and simplifi ed measures on access for non- develop biological control agents such as commercial research purposes, taking Anagyrus lopezi (DeSantis) (Hymenoptera: into account the need to address a Encyrtidae) for control of the cassava change of intent for such research; mealybug, Phenacoccus manihoti Matile- (b) Pay due regard to cases of present or Ferrero (Hemiptera: Pseudococcidae) (Cock imminent emergencies that threaten or et al., 2009). ABS legislation that does not damage human, animal or plant health, take such public good consideration into as determined nationally or account will have signifi cant detrimental internationally. Parties may take into consideration the need for expeditious impact on the global community. access to genetic resources and In Canada, more than 400 invertebrate expeditious fair and equitable sharing of species have been released for biological benefi ts arising out of the use of such control against weeds and arthropods (see genetic resources, including access to Mason et al., Chapter 1, this volume). affordable treatments by those in need, Among these are successes, such as especially in developing countries; introduction of the Apanteles (c) Consider the importance of genetic carpatus (Say) (Hymenoptera: ) resources for food and agriculture and for control of satin moth, Leucoma salicis their special role for food security. (L.) (Lepidoptera: Lymantriidae); Cyzenis albicans (Fallen) (Diptera: ) and Agrypon fl aveolatum (Gravenhorst) (Hy- 2.2 Impacts on Biological Control menoptera: ) to control the winter moth, Operophtera brumata (L.) The implications of the ABS on biological (Lepidoptera: Geometridae); Chrysocharis control have the potential for signifi cant laricinellae (Ratzeburg) (Hymenoptera: impacts. Bureaucratic procedures have the ) for control of pistol casebearer, potential to impede surveys for potential Coleophora malivorella Riley (Lepidoptera: biological control agents (BCAs), prevent Coleophoridae); Tetrastichus julis (Walker) sending specimens to experts for identifi - (Hymenoptera: Eulophidae) for control of cation, and create barriers for the export of cereal leaf beetle, Oulema melanopus (L.) 8 Chapter 2

(Coleoptera: Chrysomelidae); Phytoseiulus mission on Access and Benefi t Sharing and persimilis Athias-Henriot (Megostigmata: Biological Control (van Lenteren and Cock, Phytoseiidae) for inundative control of two- 2009). At the request of the Food and spotted spider mite, Tetranychus urticae Agriculture Organization of the United Koch (Trombidiformes: Tetranychidae); the Nations (FAO) the IOBC commission phytophages Chrysolina quadrigemina developed a position paper on biological (Suffrian) and C. hyperici (Förster) (Cole- control and ABS that included recom- optera: Chrysomelidae) for control of St mendations for best practices by prac- John’s wort, Hypericum perforatum L. titioners (Cock et al., 2009). The document (Hypericaceae); and Tyria jacobaeae (L.) was presented to a special meeting prior to (Lepidoptera: Arctiidae) for control of the 12th Regular meeting of the Com- tansy ragwort, Jacobaea vulgaris Gaertn. misson on Genetic Resources for Food and (Asteraceae). Many of our biological control Agriculture in Rome, Italy in October 2009. target species originated from Europe and Using examples from around the world, up to now exploration for and access to the FAO document outlined the im- potential biological control agents has been portance and benefi ts of biological control well facilitated. However, in the future to the global community. The document access to natural enemies for new invasive recommends that ABS regulations should alien species could be restricted or pre- recognize the specifi c features of biological vented where they originate from countries control, which are: that have enacted ABS legislation that does not consider the ‘public good’ aspect that • Countries providing BCAs are also biological control provides. Furthermore, themselves users of this technology; additional bureaucratic procedures will • Many BCAs are exchanged, but have lit- slow down efforts, already dealing with tle recoverable monetary value; tight regulatory procedures and limited • Organisms are not patented, so can be funding, to fi nd biological control solutions used by anyone at any time; to pest problems. • Classical biological control information If biological control is considered as and to a degree augmentative biological non-commercial research, simplifi ed meas- control information are publicly shared; ures for access and benefi t sharing should • There are societal benefi ts for all, such facilitate biological control research and as environmental and public health ben- the use of biological control to address efi ts, and reduction in pesticide use; emergencies and the needs of food and • Biological control is widely used in both agriculture should also be facilitated (Cock, developing and developed countries, 2011). Therefore, depending on the often using the same BCAs; legislation and regulations put in place by • Most use of biological control relates to each country, there is still a risk that if food and agriculture. biological control is not accepted as non- commercial research in this process, some In view of these specifi c positive countries may inadvertently make it un- features, the following recommendations necessarily diffi cult or even impossible to are made: access biological control agents. 1. Governments should build on the exist- ing multilateral practice of exchange of nat- 2.3 What Has Been Done? ural enemies for biological control on a complementary and mutually reinforcing In 2008, the International Organization for basis, which ensures fair and equitable Biological Control (IOBC) recognized the sharing of the benefi ts of biological control need to provide scientifi c advice to parties worldwide. involved in the design and implementation 2. ABS regulations should encourage fur- of an ABS regime and created a Com- ther development of the biological control Chapter 2 9 sector, by facilitating the multilateral 2.4 Canada’s ABS Initiative exchange of BCAs. 3. Countries are encouraged to have a sin- As a signatory to the CBD, Canada and gle point of contact to facilitate survey Canadians are obliged to develop policy missions, provision of information, in - and comply with policies of other stitutional linkages and taxonomic support, countries to ensure that the biodiversity of and provide advice on compliance with each country is fairly and equitably shared regulations for biological control, including amongst all of society. Currently, no ABS. offi cial ABS system is in place although 4. ABS in relation to biological control Canadian genetic resources and associated must be based on non-monetary benefi t traditional knowledge are being accessed sharing, e.g. capacity building, shared for research and commercial use (Environ- research programmes and/or technology ment Canada, 2012). Environment Canada transfer, as already practised by many orga- has been designated as the lead for Canada. nizations and also the augmentative biolog- Since 2004, a Federal/Provincial/Territorial ical control industry. Work ing Group on Access and Benefi t- 5. A document describing best practices sharing (FPTWGABS) has sought input for ABS in relation to biological control, from Aboriginal peoples and other key including guidelines for joint research that stakeholders on the development of ABS are equitable but not restrictive, should be policy in Canada and in 2009 a discussion prepared and disseminated by CBD and paper, Access to Genetic Resources and FAO, and biological control organizations Sharing the Benefi ts from Their Use in would be expected to follow these guide- Canada: Opportunities for a New Policy lines. Direction, presented three possible 6. To improve transparency in the approaches (Biodiv.ca, 2012). A ‘Nationally exchange of BCAs, mechanisms should be consistent approach’ would see Federal, supported globally to establish and allow Provincial and Territorial governments free access to database information on develop ABS policy based on common BCAs including source and target countries. principles and core elements but that 7. In the case of a humanitarian or an would allow each to address unique emergency situation for food security, gov- circumstances in their jurisdiction. An ernments should cooperate within FAO to ‘Independent approach for each fast track action in the exchange of BCAs. jurisdiction’ allows each government to independently develop their own ABS In addition to the FAO report, the policy or maintain the status quo Commission wrote a peer-reviewed forum (including not developing a policy). A paper (Cock et al., 2010) to inform the ‘Single national approach’ tasks the federal biological control community of practice, government to develop a single national many of whom were unaware of the ABS ABS policy. Linked to all approaches is and the implications for biological control. how ABS policy would be implemented While the focus of the FAO report and and this would be done either through Cock et al. (2010) is on arthropods, the building on existing laws by developing arguments presented apply to microbial new voluntary and non-regulatory biological control agents. The paper measures or creating new regulatory recommends that the biological control measures, or through new ABS-specifi c community in each country is encouraged legislation and regulations. An important to contribute to developing the legislation issue raised in the discussion paper is and regulation process to encourage the whether traditional knowledge associated facilitation of biological control along with with genetic resources should be part of other non-commercial research activities, ABS policy in Canada. e.g. relating to taxonomy, ecology and The inclusion of traditional knowledge conservation (Cock, 2011). in ABS policy would require signifi cant 10 Chapter 2

resources to develop a transparent and straightforward and easily implemented. equitable mechanism, whereas exclusion Furthermore, the Entomological Society of would simplify developing and imple- Canada approved a policy statement on 21 menting policy governing only genetic October 2009 that states the ESC’s support resources (Biodiv.ca, 2012). However, it has for the principles of ABS and encourages been argued that the inclusion of native governments to ensure that entomological Canadian interests in ABS policy is research is not compromised by imple- imperative to support indigenous cultures mentation of ABS policy (ESC, 2009). and to reverse the decline of biodiversity Other actions should include develop- (McDermott and Wilson, 2010). ing standards and best practices for bio- It is clear that the issue of ABS policy logical control activities. One such effort for Canada is complex. At present Canada was made by the AAFC Biological Control has not ratifi ed the Nagoya Protocol and a Working Group, which set out the practices clear path is needed. An interdepartmental of Biological Control Scientists in Canada committee is looking at the ABS issue at in two draft documents, ‘Canadian the federal level and the provinces and Biological Control Agent and Pollinator territories are involved in the FPTWGABS Genetic Resources: AAFC Policy for (Environment Canada, 2012). Biological provision of naturally-occurring benefi cial control utilizes biodiversity for the public genetic resources to other jurisdictions’ and good and policy makers in Canada have a standard letter included when shipments been made aware of this. Thus, ABS policy of biological control agents of Canadian development should be informed. origin are made (AAFC Biological Control Working Group, 2009, unpublished results). International initiatives, such as the Swiss 2.5 What Can Be Done? Academy of Sciences (2006) ‘Access and Benefi t Sharing Good practice for academic The Canadian biological control com- research on genetic resources’, can provide munity of practice can take action that will a basis for developing national guidelines ensure research and development of for biological control practice. biological control agents will continue with minimal disruption. As recommended by Cock et al. (2010), biological control practitioners have provided information 2.6 Conclusion and comment about biological control to the FPTWGABS to ensure that Canada Informed ABS policy will be key to ensure plays a lead role in developing procedures that collection and exchange of biological that govern administrative issues such as specimens for scientifi c study can continue. prior informed consent, mutually agreed to It must be accepted that to succeed terms for sharing benefi ts, and permissions biological control of the future will be for access to and export of organisms for required to follow the regulations of each biological control purposes that are country where a project is implemented.

References

Biodiv.ca (2012) Access and Benefi t Sharing (ABS). Available at: http://www.biodivcanada.ca/ default.asp?lang=En&n=A9326342-1 (accessed 30 July 2012). Cock, M.J.W. (2010) Biopiracy rules should not block biological control. Nature 467, 369. Cock, M.J.W. (2011) The Nagoya protocol and biological control. Available at: http://cabiinvasives. wordpress.com/2011/03/28/the-nagoya-protocol-and-biological-control-by-matthew-cock/ (accessed 3 August 2012). Chapter 2 11

Cock, M.J.W., van Lenteren, J.C., Brodeur, J., Barratt, B.I.P., Bigler, F., Bolckmans, K., Cônsoli, F.L., Haas, F., Mason, P.G. and Parra, J.R.P. (2009) The use and exchange of biological control agents for food and agriculture. FAO Background Study Paper No. 47. Available at: ftp://ftp.fao.org/ docrep/fao/meeting/017/ak569e.pdf (accessed 24 September 2012). Cock, M.J.W., van Lenteren, J.C., Brodeur, J., Barratt, B.I.P., Bigler, F., Bolckmans, K., Consoli, F.L., Haas, F., Mason, P.G. and Parra, J.R.P. (2010) Do new access and benefi t sharing procedures under the Convention on Biodiversity threaten the future of biological control? BioControl 55, 199–218. DOI 10.1007/s10526-009-9234-9. Convention on Biological Diversity (CBD) (2012) List of Parties. Available at: http://www.cbd.int/ convention/parties/list (accessed 24 September 2012). Entomological Society of Canada (2009) Policy Statement on Biodiversity Access and Benefi t Sharing. Bulletin of the Entomological Society of Canada 41, 208. Environment Canada (2012) Access and Benefi t Sharing. Available at: http://www.ec.gc.ca/apa-abs/ default.asp?lang=En&n=AEFC44AD-1 (accessed 27 July 2012). Feit, U., von den Driesch, M. and Lobin, W. (eds) (2005) Access and Benefi t-Sharing of Genetic Resources: Ways and means for facilitating biodiversity research and conservation while safeguarding ABS provisions. Report of an international workshop in Bonn, Germany held in 2005, 8–10 November. Convened by the German Federal Agency for Nature Conservation. Available at: http://www.bfn.de/09/090203.htm Skript163 (accessed 24 September 2012). Haas, F., van Lenteren, J.C., Cock, M.J.W., Brodeur, J., Barratt, B., Bigler, F., Bolckmans, K., Mason, P.G. and Parra, J.R.P. (2010) Is the Convention on Biological Diversity promoting environmentally friendly solutions to pest control? Sector Programme for Integrated Pest Management (SP-IPM) Consultative Group on International Agricultural Research (CGIAR). Available at: http://www.spipm.cgiar.org/c/document_library/get_fi le?uuid=53af8458-981c-4ff7- beab-0f1596f081b1&groupId=17812 (accessed 24 September 2012). McDermott, L. and Wilson, P. (2010) ‘Ginawaydaganuk’: Algonquin Law on Access and Benefi t Sharing. Policy Matters 17, 205–214. Prathapan, K.D. and Rajan, P.D. (2011) Biodiversity access and benefi t-sharing: weaving a rope of sand. Current Science 100, 290–293. Swiss Academy of Sciences (2006) Access and Benefi t Sharing: Good practice for academic research on genetic resources. Albreht Druck un Satz, Bern, Switzerland, 58p. Available at: http://abs. scnat.ch (accessed 24 September 2012). United Nations (2010) Nagoya Protocol on Access to Genetic Resources and the Fair and Equitable Sharing of Benefi ts Arising from their Utilization to the Convention on Biological Diversity. Available at: http://treaties.un.org/doc/source/events/2011/Publication/publication-English.pdf (accessed 25 September 2012). van Lenteren, J.C. and Cock, M.J.W. (2009) IOBC reports to FAO on Access and Benefi t Sharing. Biocontrol News and Information 30, 67N–70N. 12 Chapter 3

3 Climate Change and Biological Control in Canada

David R. Gillespie,1 Owen O. Olfert2 and Matthew J.W. Cock3 1Agriculture and Agri-Food Canada, Agassiz, British Columbia; 2Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 3CABI Europe-UK, Egham, Surrey, UK

3.1 Introduction wetter. In Canada, the central plains may see more droughts, interspersed with As a result of the anthropogenic abnormally wet years and the coasts of phenomenon known as Global Climate Canada may see more rainfall (Qian et al., Change (GCC), climatic norms will change 2010). Evidence is accumulating that in many parts of the world (IPCC, 2007a, climate change will be coupled with

b). The carbon dioxide (CO2) concentration unstable, extreme weather events (winds in the atmosphere has risen from a mid- and storms, heatwaves and extreme cold) 19th-century level of 280 ppm, to a 2005 (IPCC, 2007a, b). Because the life cycle and level of greater than 370 ppm; and this biology of biological control organisms and concentration is predicted to continue hosts are strongly affected by weather, GCC rising to around 550 ppm by 2050, less will have an impact on many aspects of the than 40 years hence (IPCC, 2007a, b). As a interactions between natural enemies and

consequence of the effects of CO2 on the pest species and thus affect all aspects of climate engine of the planet, the average biological control (Thomson et al., 2010; global temperature is rising, sea ice is Cock et al., 2011). This chapter addresses melting, and rainfall is increasing across three questions that we consider to be some land areas (IPCC, 2007a, b). In important considerations for biological temperate regions of the globe, Canada control practitioners. First, as the climate included, climate change predictions in- changes across Canada, will the frequency clude increases in the number of frost-free and nature of invasions of new biological days, increases in long-term average tem- control targets change? Second, will it be peratures during growing seasons, and possible to anticipate changes in the increases in long-term average winter geographic range of crops, pests and temperatures (Qian et al., 2010). Growing natural enemies? Finally, will the changed seasons will be longer and warmer, and climate negatively affect the interactions winters will be shorter and warmer. between organisms in biological control Rainfall patterns will change, with some food webs, rendering these programmes areas predicted to become drier and others ineffective?

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 3 13

3.2 GCC Implications for Invasion of The sub-fossil record shows little evidence New Target Pests of evolution of new species or mass extinction of invertebrate species during The results of previous, relatively recent the Quaternary, despite the rapid shifts in climate change events aid in understanding climate (Coope, 2004). The sub-fossil the implications of GCC for invasions of remains can nearly all be matched to new pest species into Canada. We live in existing species, and the fact that species an interglacial period in a 2.6 million year occur in similar associations implies that sequence of alternating glacial and inter- their physiological and ecological require- glacial periods (the Quaternary Period). ments have not changed signifi cantly. During this period, the world has certainly There is evidence that insect species dis- been warmer than it is now, but for much appeared from the sub-fossil record at the of the time it has been colder, and the beginning of the Quaternary, but little transitions between the two extremes have evidence for signifi cant mass extinction been relatively rapid (Coope, 2004; Hof et since then. This implies that the species al., 2011). There have been abrupt periods that exist today have mostly existed of warming in our planet’s recent glacial unchanged since the beginning of the history: temperatures rose from glacial to Quaternary, and that they have survived interglacial values in less than one century, repeated glacial and interglacial periods at a rate of about 1°C per decade, about and the rapid transitions between them 12,800 BP and about 10,000 BP (Coope, (Coope, 2004; Botkin et al., 2007; Hof et al., 2004; Steffensen et al., 2008). The planet 2011). has warmed by about 0.75°C in the 20th Broadly speaking, the species found in century (Easterling et al., 2007) and there is temperate regions during glacial periods compelling evidence for a general pole- are now restricted to cold areas of the ward shift in the breeding distributions of a subarctic and high mountains, whereas the large number of invertebrates (e.g. Hickling species found in temperate regions during et al., 2006; Musolin and Fujisaki, 2006). warmer periods are those which we now Range boundaries are shifting towards the associate with the subtropics (Coope, 1994, poles at an average rate of about 6 km per 2004). The implication is clear: overall, decade (Parmesan and Yobe, 2003), and species do not adapt to changing climate, altitudinally – assuming a lapse rate of but they move to areas where they are well 6.5°C per 1000 m and 3.5°C rise for the adapted to the climate. next century – at a rate of at least 50 m per Insects have moved fairly rapidly when decade (Whittaker and Tribe, 1996; necessary. The changes between glacial Menéndez, 2007; Colwell et al., 2008), and interglacial periods and back have rates that most mobile pest and natural been rapid and the insect groups studied enemy species should be capable of (detritivores and predators) have kept track tracking. However, as noted by Barnovsky with the areas to which they are adapted et al. (2012), barriers caused by habitat (Coope, 2004; Hof et al., 2011). There is disruption and fragmentation may interfere less evidence as yet for fl ightless insects or with such movement. for herbivores, which can only spread to Sub-fossil remains in temperate regions climatically suitable areas where suitable are available in dated layers for many food plants already occur. The extent to insects covering much of the Quaternary which invertebrates will be able to track period. Examination of these remains can climate change will probably vary give us insight into evolution, extinction enormously. Some species will be tied to and movement of insect populations specifi c latitudes because of direct or during periods of climate change, helping indirect photoperiod requirements. In us to understand how insects and other general, habitat specialists, especially those invertebrates are likely to respond during with poor dispersal ability, will be least the anticipated climate change to come. able to keep pace with climate change 14 Chapter 3

(Travis, 2003). Some species, such as some fragmentation, land-use changes and re- predatory mites and many soil in- duction of genetic diversity (Thomas et al., vertebrates, have low dispersal rates and 2004). How a landscape is managed and the time taken for benefi cial species to changes over time is known to affect the integrate into a new area will be infl uenced composition and abundance of the in- particularly by the supplementary re- vertebrate species present. Butterfl y studies sources needed, e.g. nectar and pollen, and have documented the decrease in species winter or summer sites. The diversity that occurred during the rapid potential distribution of species is mostly industrialization of Europe at the end of constrained by their physiological level of the 19th century and when intensive tolerance to extremes, e.g. droughts and large-scale farming was propagated from frosts, and an increase in the frequency of the middle of the 20th century (e.g. such extremes may limit species per- Laussmann et al., 2010). The grain industry sistence (Hance et al., 2007). Therefore in Australia has seen major shifts in current communities, especially those invertebrate pest challenges over a 30-year based on exotic crop species with specialist period as a consequence of climate change, invertebrate assemblages, are unlikely to altered patterns of crop and pesticide use move intact under climate change and there and farm management responses (Hoff- could be some benefi cial (absence of pest) mann et al., 2008). Similarly, 50 years of or negative (absence of benefi cial in- research on the effects of agricultural vertebrates) effects on yield as well as landscape management in western possible destabilization of agro-ecosystems. has shown a progressive increase in heat- The evidence from the geological past also loving (thermophilic) insects related to suggests that species are unlikely to grasslands, probably connected with cli- respond as intact communities (Russell and mate change, as well as with an increasing Grimm, 1990; Lawton, 1998; Colinvaux, share of cereals in crop rotations (Karg and 2005). Balazy, 2009). However, responses may Thus, most invertebrates are expected to be unpredictable, and existing inter- change their geographical distribution in dependencies between species may only response to climate change so as to remain become apparent when they become in areas to which they are well adapted. uncoupled as a result of asynchronous Even so, we recognize that the current responses to climate change (Parmesan, landscape is very different from any that 2007). Groffman and Jones (2000) con- existed during the Quaternary period, cluded that there have been too few being divided by barriers created by human ecosystem-scale experiments on the role of activities. However, these barriers are invertebrates and suggested that if their likely to affect species in natural eco- importance can be demonstrated at the systems rather more than those associated ecosystem scale, then importance at with agro-ecosystems, and the movement landscape, regional and global scales is of the latter is likely to be facilitated rather likely. than hindered by human-induced land- Within North America, aided by acci- scape changes. It has been suggested that dental transfer through human activities, future climates may consist of novel the majority of invertebrate pests and their temperature and precipitation regimes, natural enemies can be expected to move which have no current climatic equivalent, with their host plants as crop and forage resulting in new species associations distributions change. This means that most (Williams et al., 2007), but it is not clear if new alien species will spread into Canada and how that would apply to climate in from the USA, together with whatever Canada. natural enemies co-occur with them. Responses of invertebrates to climate Inevitably there will be temporary mis- change may be inhibited or hampered by matches as crops escape their pests and human activities, through habitat loss and pests escape their natural enemies. In the Chapter 3 15

short term, phytosanitary measures will try the least in 1997 (10 km). Its , to extend the length of time for the former, Macroglenes penetrans (Kirby) (Hymen- while deliberate introductions of biological optera: ), was successfully control agents can minimize the latter. able to expand its range as well, As the climate warms, Canada will establishing in newly infested areas with a become suitable for the colonization of maximum of 1−2 year lag (Olfert et al., alien species from outside North America 2011). However, because abiotic factors, that are adapted to the warmer climates, primarily climate, constrain population i.e. exactly those alien species which growth and survival that ultimately affect represent a risk to parts of the USA today. species distribution and abundance, on- Regions of the world that are presently too going climate change may have a severe cool to contain species that are a threat to impact on our ability to accurately predict Canada will warm, and species invading ranges and expansions. into those regions will also be a threat, as Current climate analogues have been has been suggested for New Zealand used to identify geographic regions that (Kriticos, 2012). In the short term, risk may be susceptible to establishment of assessments and pathway analyses for invasive pest species or to identify regions parts of the USA today can be adapted that are most suitable to establish classical readily for Canada in the future. Dif- biological control agents. They have also ferences may arise that refl ect the extent to been used to compare the results of climate which Canada has different international change scenarios to those regions where trade routes, human destinations and species of interest are already established. sources of visitors, which will provide However, the magnitude of predicted pathways for introduction of pests from temperature change associated with cli- other parts of the world (assuming these mate change is not within the historical patterns persist in the face of global experience of modern ecosystems. As a change). In addition, greater attention will result, it is not likely that we can use have to be paid to those regions of the historical data as analogues to predict the world that have become warm enough to impact of climate change on invasive serve as a source of invasive species of species and their natural enemies. In concern to Canada (Kriticos, 2012). response, bioclimate simulation models (also known as ecological niche models) have been used to predict the impact and related system vulnerability of future 3.3 Climate Modelling and GCC climates. Implications for Range Expansions of Bioclimatic simulation models have Biological Control Species and Targets been used successfully to predict the distribution and extent of pest population Range expansion studies related to bio- establishment in new environments logical control agents have been primarily (Dosdall et al., 2002; Olfert et al., 2003). associated with population surveys of the Bioclimatic modelling software, such as host species and its agent(s). For example, CLIMEX®, enables the development of between 1991 and 2000, Saskatchewan models that describe the potential distrib- experienced a major outbreak of wheat ution and seasonal abundance of a species midge, Sitodiplosis mosellana (Géhin) based on its geographic range, phenology, (Diptera: Cecidomyiidae), during which the seasonal abundance and empirical data. invasive pest population advanced approxi- This, in turn, allows researchers to develop mately 360 km, spreading in southerly and an overview of climatic factors (including westerly directions from the point of climate change) that affect species distrib- introduction (Olfert et al., 2009). The ution and abundance and allows the greatest range expansion of the pest identifi cation of non-climatic factors that population occurred in 1993 (90 km) and limit species distribution range. 16 Chapter 3

Two approaches have been used to assess temperatures whereas its northern range the potential range expansions of pest will be limited by the number of Lygus spp. species and their natural enemies as a result host generations rather than cold stress. of a changing climate, namely, incre- Peristenus digoneutis has the potential to mental temperature/moisture scenarios and occur in the southern parts of the prairie General Circulation Model (GCMs). Studies ecozone of western Canada; however, have shown that both approaches have Ecoclimatic Index (suitability) values in the merit. In relation to the incremental prairies indicate mainly marginal or un- approach, scenarios are typically created favourable conditions, which may explain for all possible combinations (n=72) for why earlier releases of P. digoneutis in temperature (0, +1, +2, +3, +4, +5, +6, and western Canada failed. The model is +7°C of climate normal temperature) and currently being used to conduct sensitivity precipitation (−60%, −40%, −20%, –10%, analyses in relation to the potential impact 0%, +10%, +20%, +40% and +60% of of climate change on range expansion. climate normal precipitation). Due to the Organisms are more vulnerable to different methods used by climate change variations in temperature and precipitation experts in developing GCMs, the literature when located near the outer limits of their indicates that climate change impact preferred climatic range than when located studies benefi t from utilizing multiple in the core area of the range. Sutherst et al. GCMs. Olfert et al. (2012b) employed three (2007) defi ned a core area as a region with GCMs for agricultural studies to compare high Ecoclimatic Index values and little or with current climate. The three models no stress. Populations near the outer limits cover a range of climate sensitivity, defi ned of the core area spend a greater amount of as the amount of global warming for a time in climates that are marginally doubling of the atmospheric CO2 con- suitable (exposed to climatic stress), while centration compared with 1990 levels. populations near the core experience a To date, the majority of bioclimate greater amount of time in favourable modelling activities in Canada have conditions (minimal exposure to climatic focused on the pest species, in part due to stress). As a result, bioclimate model the increased complexities of tri-trophic output for North America typically systems (host–pest species–natural ene- indicates that instances of range expansion mies). At this time there is very little are most prevalent in northern regions of empirical work on the impacts of climate North America. Conversely, model output change on range expansions or con- predicts that the range and relative tractions in biological control com- abundance of these organisms under study munities. In response to agricultural pest could also contract in regions where issues, AAFC and CABI Europe– climate conditions became limiting due to Switzerland have initiated collaborations warmer, drier climates. In other words, to explore the opportunities that bioclimate existing pest pressures and associated modelling offer biological control pro- biological control organisms are likely to grammes, including the potential impacts spread northward, and contract from the of climate change. The canola, Brassica south. napus L., B. rapa L. (Brassicaceae)–lygus Again using Canadian agricultural bugs, Lygus spp. (Hemiptera: Miridae)– examples, compared to predicted range Peristenus digoneutis Loan (Hymenoptera: and distribution under current climate con- Braconidae) system was felt to be ideal for ditions, model results of range expansion bioclimate investigations. The bioclimatic of all crop pest species investigated using model results suggest that P. digoneutis is GCMs to date (Melanoplus sanguinipes likely to continue its spread westwards (Fabricius) (Orthoptera: Acrididae), Olfert throughout the USA along the Great Lakes et al., 2011; Sitona lineatus (L.) in North America. Its southern distribution (Coleoptera: Curculionidae), Olfert et al., is expected to be limited by hot summer 2012a; Kochia scoparia (L.) Schrad. Chapter 3 17

(Amaranthaceae), Fusarium graminearum and the competitive and consumptive Schwabe (Nectriaceae), Oulema melanopus relationships between species. The effects (L.) (Coleoptera: Chrysomelidae), Olfert et of climate change on the organisms in al., 2012b) indicated that they would have terrestrial food webs are predicted to increased range and relative abundance in magnify with increasing trophic position Canada. Though responses were specifi c to (Voigt et al., 2003; Schweiger et al., 2008), species, location and GCM, there were which may create uncertainty and general similarities among the pest species instability in biological control systems that studied to date. Notable changes were have previously been stable. predicted to occur across the Canadian Atmospheric CO2 is not known to have prairies. The three GCMs mentioned earlier many direct effects on the biology of have predicted increased pest status (crop invertebrates. However, for some plant risk) across the northern areas of Alberta, pests and weed BCAs, response cells

Saskatchewan and Manitoba, with saturate under high CO2 (400 ppm or southern areas of the prairies predicted to higher, depending on species) (Guerenstein have conditions similar to concurrent and Hildebrand, 2008). Cactoblastis climate. In a number of cases, GCMs cactorum (Berg) (Lepidoptera: Pyralidae), predicted a signifi cant increase in crop pest an important BCA of prickly cactus, status, particularly regions north of 59°N Opuntia spp. (Cactaceae), in some parts of latitude (i.e. north of Peace River region). the world, is an example of a BCA in This scenario highlights the importance of which host location could be impaired by implementing a tri-trophic approach to elevated CO2 (eCO2) (Stange, 1997). range expansion studies. That is, the issue In most cases, effects of eCO2 on of range expansion of biological control biological control agents are driven by agents is moot if the region is not suitable indirect, bottom-up effects on plant for crop production and pest establishment species. The effects of eCO2 on plants are in this case. However, Mills (1994) relatively well known (Wang et al., 2012). conducted a study of arable soils in north- Under eCO2, plant growth increases western North America (north of 55°N and somewhat (Wang et al., 2012), but this west of 110°W) and predicted that if CO2 effect is only consistent for C3 plants and levels double, i.e. +3.8°C; +17% rain, the is not observed in C4 plants. With respect availability of arable land in the north-west to the natural enemy food webs, the would increase in area to almost equal that bottom-up effects of increases in C:N ratios of the current amount of arable land on the may be of most signifi cance. Under eCO2, Canadian prairies. Still, the expansion of the carbon–nitrogen ratio increases in plant crops and associated arthropod com- tissues, especially in C3 plants (Sardans et munities into these new, more northern al., 2012). Since nitrogen is limiting in regions, may be limited by innate most terrestrial food webs (Elser et al., responses to photoperiod (Saikkonen et al., 2000), herbivores may develop to smaller 2012). sizes, require longer to develop to their adult size and/or suffer increased mortality during development and decreases in 3.4 GCC Implications for Performance fecundity. Development could require that of Biological Controls insects consume more plant tissue as a result (DeLucia et al., 2008). This could In general, modelling and analysis to date decrease the number of generations of predicts that most biological control agents herbivores in a year, and the reproductive will move with their hosts as the host range fi tness of individual pests and natural and crop range increases. However, climate enemies. change factors, i.e. enhanced CO2 (eCO2), Environmental stoichiometric effects of enhanced temperature and increased stress, eCO2 may result in increases in carbon-rich may affect performance of natural enemies compounds such as phenolics and other 18 Chapter 3

defence compounds (Sardans et al., 2012). 2010), heatwaves may ultimately limit the This also has the potential for bottom-up ranges of plants, herbivores and natural impacts on primary and secondary enemies. There is evidence that exposure consumer trophic levels (Ode, 2006; to heatwaves changes interactions within Bidart-Bouzat and Imeh-Nathaniel, 2008; biological control communities (Ban- DeLucia et al., 2008). nerman et al., 2011; Gillespie et al., 2012). The most widely recognized outcome of Many of the microorganisms involved in GCC is the increase in global average biological control, as well as many of the temperatures. These warming effects are microorganism targets, are moisture- already being observed at the regional and limited, i.e. they require free water on continental scale (IPCC, 2007a, b; Qian et surfaces for growth, movement and al., 2010) and, as noted above, are infection. Changes in dew frequency and implicated in range expansions of target abundance and the availability of free pests and natural enemies. In temperate water will have signifi cant impacts on the regions such as Canada, the average fi rst incidence of plant disease and on the frost date of winter is later, and the last effi cacy of biological controls employing frost of winter is earlier (IPCC, 2007a, b). microorganisms (Chakraborty and Newton, This means a longer growing season and, 2011; Garrett et al., 2011; Ye and Peng, coupled with less severe winters and 2011). Extreme drought will likely impair warmer summers, provides opportunities microbial biological control organisms, but for range expansion, and additional will also likely impair some of the generations of pests and natural enemies microbial plant pathogens. Conversely, in (Hance et al., 2007; Thomson et al., 2010). regions where rainfall may become more For most organisms in biological control frequent and extreme, e.g. the Pacifi c coast food webs, the rates of biological processes, of Canada, the reverse may be true. Winds as a function of temperature, follow asym- and storms that disrupt natural and crop metric parabolae, with rates increasing communities may provide opportunities linearly with temperature through a for the establishment, spread and increase moderate range to an optimum tem- of invaders (Dukes and Mooney, 1999). perature, and then sharply declining to Although the available evidence zero at an upper threshold. If important strongly suggests that GCC will have biological processes, e.g. foraging rate, impacts on plants, herbivores and natural development rate, of interacting species enemies in biological control systems, the have different slopes in response to extent and severity of the impacts is not yet temperature increases, different optima known (Cock et al., 2011). None the less, and/or different upper thresholds, then the GCC clearly has widespread implications interaction, e.g. , competition, in agricultural and forest systems that rely will be affected by changes in average on biological control. To date, most studies temperature (Davis et al., 1998). In the reported in the literature have examined absence of adaptation, relative abundance the effects of a single climate change factor, of the two species and effects on top-down e.g. temperature or CO2 concentration, on a trophic cascades should also be affected. single species, and less commonly, on two As a consequence of increased energy in species interactions. Very few studies have the atmosphere, most models predict an examined the combined effects of eCO2, increase in the frequency and severity of and increased temperature and thermal extreme and catastrophic events (IPCC, stress on the performance of complex 2007a, b). Heatwaves will be more frequent natural or experimental food webs. This is and more severe. Since many insects and necessary in order to fully understand and other organisms in temperate regions have adapt to the anticipated changes imposed relatively low upper critical temperature by GCC on agriculture and forest pest limits, above which they die (Hazell et al., management. Chapter 3 19

3.5 Conclusions not possible to accurately predict GCC yet, let alone the changes it will cause in agro- In essence, we can be confi dent that GCC ecosystems. Moreover, GCC is but one will affect pest and natural enemies, and driver of overall anthropogenic global thus biological control programmes, in change (Barnosky et al., 2012) and the Canada. If, as seems likely, GCC unfolds at added effects of other drivers, such as rates that allow organisms in anthro- reductions in natural biodiversity, in- pogenic landscapes to redistribute them- tensifi cation of agriculture and increases selves into suitable habitats, existing in land converted to food production, may crop-pest–natural enemy associations contribute to the dis ruption of biological should persist. Bioclimatic models have control programmes. proven useful to investigate the potential impact of climate on pest populations. However, some cautions have been 3.6 Recommendations expressed regarding the utilization of this approach including: (i) biotic interactions Research and implementation activities are unlikely to remain the same over time should include: in the face of climate change; (ii) genetic and phenotypic composition of popu- 1. Determining if natural enemy com- lations (adaptation) can be expected to plexes are shifting in concert with range change over time and space in response to shifts in hosts and crop systems; changes in climate; and (iii) most species 2. Using bioclimatic models to improve have some limitations to dispersal. prediction capacities, and especially to Overall, experimental studies suggest that identify those biological control systems tem perature averages and extremes, that might be vulnerable to disruption by changed moisture regimes and bottom-up climate change; effects of eCO2 will affect consumption of 3. Investigating the combined effects of cli- prey and competition between natural mate change parameters (eCO2, tem- enemies, mostly to the detriment of perature, variability, moisture regimes) on biological control systems. However, it is biological control food webs.

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4 New Tools in Biological Control: Molecular Markers and Mathematical Models

Tara D. Gariepy1 and Bernie D. Roitberg2 1Agriculture and Agri-Food Canada, London, Ontario; 2Simon Fraser University, Burnaby, British Columbia

4.1 Introduction security purposes. The same is true for biological control. For example, geo- Advances in science usually extend well graphical position satellites (GPS) provide beyond the subject area that was the precise coordinates where natural enemies original focus of an innovation. Many of were discovered and where biological the everyday technologies that are taken for control agents were released, and allow granted were originally developed for tracking of agent dispersal. Furthermore,

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 4 23

advances in chemical ecology have enabled promising approaches for species de- a better understanding of processes in- limitation, particularly for taxonomically volved in natural enemy selection of hosts, diffi cult groups (Gebiola et al., 2012). leading to improved risk assessment of The availability of affordable and high- exotic species that are candidates for throughput DNA analysis, coupled with introductions. Here we examine how increased recognition of the value of recent advances in molecular techniques molecular tools within the biological and systems modelling have and will control community, has led to applications continue to facilitate biological control that extend beyond agent classifi cation, research. In the molecular fi eld, advances identifi cation and detection. In fact, there in technology and reductions in costs of has been a natural progression towards the processing and sequencing have made use of these techniques to address geo- these techniques accessible to all. Simi- graphic origin, host-specifi city and trophic larly, in the mathematical modelling fi eld, interactions among agents and their hosts/ advances in the defi nitions of models, prey to better understand complex inter- combined with fourth-generation pro- actions that cannot easily be revealed using gramming and mathematical languages conventional techniques. Also gaining have meant that sophisticated knowledge popularity is the application of these tools of mathematics is not essential to the to evolutionary and ecological theory development and testing of models. Both surrounding biological control agents and fi elds rely heavily on access to high- their fate in newly introduced environ- throughput computing, which is in- ments (Nicholls et al., 2010; Vorsino et al., creasingly available at the desktop, and on 2012). the community of practice that can be As numerous authors have reviewed the readily accessed from the Internet. utility of these techniques (Symondson, 2002; Atkins and Clark, 2004; MacDonald and Loxdale, 2004; Greenstone, 2006; 4.2 Biological Control in the Stouthamer, 2006; Gariepy et al., 2007; Molecular Era King et al., 2008; Gaskin et al., 2011), our goal is to focus on recent achievements and The initial use of molecular techniques in applications (primarily from 2010 to 2012), biological control was primarily to clarify and suggest future directions for new phylogenetic and taxonomic relationships molecular methodology in biological con- (Dowton and Austin, 1994; Antolin et al., trol. 1996). However, given the levels of nucleotide variation inherent in different genes and gene regions (with some more 4.2.1 Population genetics in biological conserved than others), discrimination at control the species- and population-level became possible, and the development of 4.2.1.1 Detecting founder effects and genetic microsatellite markers, taxon-specifi c PCR bottlenecks in an agent primers and DNA barcode-type method- ology for use in biological control quickly Molecular methods provide a unique followed. The availability of molecular approach to understand and interpret methods for accurate agent identifi cation demographic and evolutionary processes, has been critical in classical biological both in terms of measuring variation control surveys, which have long suffered among populations and in discovering the with taxonomic diffi culties (Palmer et al., diversity and history of genotypes 2010). In fact, the use of integrative (Roderick, 1996). In classical biological taxonomy – the combination of evidence control programmes, promising agents are from molecular, morphological, ecological selected and a subset of their population is and geographic data – is one of the most mass-reared and subsequently released into 24 Chapter 4

the area of introduction. Collection of a allow the assessment of intra-species limited number of individuals from a diversity can help biological control limited number of locations, coupled with researchers to enrich the genetic diversity mortality in shipment and inbreeding in of introduced populations by selecting quarantine often results in loss of genetic additional haplotypes from the area of diversity even before an agent is released origin, and permit long-term monitoring of (Franks et al., 2011; Taylor et al., 2011). the effects of genetic constraints in Deleterious effects associated with reduced founding populations. genetic variation have been linked to decreased fi tness, increased rates of extinc- 4.2.1.2 Tracing the origin and introduction tion and limited evolutionary potential in history of an agent populations (Roderick, 1996; Frankham, 2005; Franks et al., 2011). This lowered The invasive woodwasp Sirex noctilio evolutionary potential can have a critical Fabricius (Hymenoptera: Siricidae) is a impact on the ability of an introduced serious pest in forestry plantations in the species to adapt to a novel environment southern hemisphere and has been targeted (Cox, 2004). When this occurs in a for biological control using the nematode biological control context, it can infl uence Deladenus siricidicola Bedding (Tylen- agent establishment, adaptation to chang- chida: Neotylenchidae) (Mlonyeni et al., ing conditions and the ability of an agent to 2011). Originating in Eurasia and North expand its geographic range from the point Africa, the woodwasp was accidentally of release to follow a target pest to different introduced into New Zealand in the 1900s regions. and has since spread to Australia, South Franks et al. (2011) investigated the Africa and South America. Most recently, consequences of a genetic bottleneck in this invasive pest was found in the Boreioglycaspis melaleucae Moore (Hem- northern hemisphere in the eastern USA iptera: Psyllidae), released for biological and Canada (Hoebeke et al., 2005; de Groot control of the paper bark tea tree, et al., 2006; see Ryan et al., Chapter 38, Melaleuca quinquenervia (Cav.) S.T. Blake this volume). Deladenus siricidicola has (Myrtaceae). This was accomplished by been found with Sirex in the area of pest analysing microsatellite loci and mtDNA origin and areas of introduction, and sequence data from B. melaleucae popu- several strains have been mass produced lations in Australia (area of origin) and and released, including those collected Florida (area of introduction), as well as from Hungary, Tasmania and Brazil (the those reared in quarantine. A loss in latter two appear to be introductions of genetic diversity was observed indicating unknown origin). To understand better the that a bottleneck effect had occurred in the historical relationship and diversity among introduced populations, as refl ected by an strains collected in different regions, absence of several alleles and haplotypes Mlonyeni et al. (2011) characterized D. that were present in populations from the siricidicola from Australia, Argentina, area of origin. Although an immediate Brazil, South Africa and Canada using impact was not apparent, it is diffi cult to micro satellite markers. Their results predict the long-term effects of reduced revealed a high level of homozygosity in genetic diversity in the introduced the nematodes collected from several population (Franks et al., 2011). Increased countries in the southern hemisphere, and susceptibility to pathogens, failure to adapt confi rmed the origin of the population as to changing environmental or climatic those mass produced from the strain conditions and inability to evade the host ‘Kamona’, originally collected in Tasmania. immune response are among the factors This highly inbred population, recovered that could reduce the viability of an agent throughout the southern hemisphere, is as a long-term sustainable pest manage- likely due to repeated population bottle- ment solution. Thus, genetic tools that necks associated with the culturing and Chapter 4 25

introduction processes that were followed the natural enemies (thrips and psyllids) (Mlonyeni et al., 2011). In contrast, those correspond to specifi c haplotypes of D. siricidicola collected in Canada were the host plant (see Cuda et al., 2012). In genetically distinct from the ‘Kamona’ this extremely well-characterized system, strain and the origin and its level of the genetic structure of the Brazilian diversity have yet to be determined. It has peppertree, Schinus terebinthifolius Raddi also been noted that parasitism by D. (Anacardiaceae), two Pseudothrips spp. siricidicola in the southern hemisphere is (Thysanoptera: Phlaeothripidae) and two highly variable, and ranges from 5 to 90% Calophyla spp. (Hemiptera: Calophylidae) in different regions (Hurley et al., 2007). have been elucidated (Williams et al., This is not surprising given the extremely 2007; Mound et al., 2010). Using these different climates in which D. siricidicola data, it has been suggested that it would be has been released (Mediterranean, Contin- advantageous to match the biological ental, Temperate and Subtropical climates). control agent haplotypes being released It is unlikely that a strain of D. siricidicola with specifi c geographic populations of the with extremely low genetic diversity peppertree being targeted for control in the would be able to adapt and establish in area of introduction to achieve the best such different environments and maintain outcome (Cuda et al., 2012). a high level of effi cacy against the When cryptic species’ specifi city issues woodwasp; consideration of additional are not known or not considered in bio- strains should be incorporated in future logical control programmes, varying levels control efforts to boost the level of of control are often observed, and success/ diversity (Mlonyeni et al., 2011). failure can be diffi cult to interpret. In North America, a biological control pro- gramme targeting the invasive toadfl ax species Linaria dalmatica (L.) Miller, L. 4.2.2 Host-specifi city of biological control genistifolia (L.) Miller and L. vulgaris (L.) agents Miller (Plantaginaceae) of European origin led to the release of a stem-mining weevil 4.2.2.1 Cryptic species that vary in host Mecinus janthinus Germar (Coleoptera: specifi city Curculionidae) (see De Clerck-Floate and Safe and effective biological control rests Turner, Chapter 52 and De Clerck-Floate upon the selection of specialized agents and McClay, Chapter 53, this volume). from a pest’s native range that will infl ict Although rapid establishment and signifi cant mortality on pest populations, substantial impact on L. dalmatica was while causing little or no mortality to non- observed, very little impact was reported target organisms. Morphological and on L. vulgaris despite reports that this molecular studies suggest the existence of species serves as a host for M. janthinus in cryptic species that are morphologically Europe (McClay and Hughes, 2007). A indistinguishable, but which vary genetic- recent molecular assessment of mito- ally and/or ecologically. In a biological chondrial cytochrome oxidase II (COII) control context, this is often expressed in gene sequences from European populations terms of differing levels of host-specifi city of M. janthinus suggested the existence of among cryptic species that were initially two cryptic species, one which develops considered to be single, extreme generalist on L. vulgaris and one on L. genistifolia, as species (Goolsby et al., 2006; Smith et al., well as a potential third cryptic species 2006, 2008; Tracy and Robbins, 2009; that also feeds on L. vulgaris (Toševski et Mound et al., 2010). al., 2011). The occurrence of cryptic An example of how molecular genetics species within M. janthinus may explain can ‘fi ne tune’ the selection of natural some of the variability in success of enemies is the biological control of the biological control programmes for Linaria Brazilian peppertree – where haplotypes of spp. in North America, as it is possible that 26 Chapter 4

the specimens of M. janthinus released in (including both the host and natural North America were part of a cryptic enemies) involved in an interaction species complex with a high level of regardless of what developmental stage specifi city for L. dalmatica (Toševski et al., they are in (egg, , , adult). As 2011). However, a complementary study to universal PCR primers are generally used examine and compare the mitochondrial to amplify the DNA, host rearing or haplotypes that occur in North America to dissections are still needed to separate those in Europe would provide additional tissues belonging to different species prior support for this theory to determine the to DNA extraction and subsequent biotype and geographic origin of the amplifi cation and sequencing. When already-established agents and identify a tissues cannot be adequately separated, niche for additional releases. cross-amplifi cation and misidentifi cation Another example of cryptic species that can occur. None the less, this is a valuable exhibit different levels of host-specifi city is tool for defi ning the natural enemy com- the parasitoid Pediobius saulius (Walker) munity associated with different host (Hymenoptera: Eulophidae) being con- species (Hrcek et al., 2011; Santos et al., sidered for release in Europe to control the 2011) and/or the host species utilized by a horse-chestnut leaf miner, Camereria given parasitoid adult (Rougerie et al., ohridella Deschka & Dimic ´ (Lepidoptera: 2011). This approach has generally been Gracillariidae). Although P. saulius has a used to study community ecology, bio- fairly broad host range that spans three diversity and trophic links in Lepidoptera– orders of leaf-mining insects (Noyes, 2011), parasitoid food webs, with the intent to it is the dominant parasitoid of C. ohridella address biodiversity issues or to gain an in the Balkans (the presumed area of pest evolutionary perspective on host– origin). Interestingly, this parasitoid rarely parasitoid interactions. These studies are attacks C. ohridella in Europe (Girardoz et not necessarily conducted in the realm of al., 2007). Hernández-Lopez et al. (2011) biological control, but do provide pertin- used mitochondrial and nuclear DNA ent, advanced methodology that can be sequences to determine whether P. saulius tailored to fi t within surveys for biological is in fact a complex of specialized cryptic control agents, particularly when a priori species. Some evidence of geographic knowledge regarding the natural enemy structuring and host-associated differen- complex of a pest is limited. tiation was observed in the Balkans; Once a promising agent has been however, most haplotypes were collected identifi ed, thorough host range testing is on more than one host species and it required. In host range testing of a appears that there are fi ve ‘generalist’ candidate biological control agent, the aim cryptic species of P. saulius (Hernández- is generally more focused than the scenario Lopez et al., 2011). noted above for DNA barcode analysis of food webs, in that the agent of interest is already known. As such, the question is 4.2.2.2 Assessing the host range of biological whether the agent is restricted to the control agents targeted pest, or whether it is associated One of the challenges in fi eld-based with non-target species as well. It is evaluation of the host range of a candidate basically a ‘yes or no’ question in terms of agent is the morphological similarity the presence or absence of the candidate between the agent and related species agent in different potential host popu- which may attack the same or related lations. In such a case, the development of hosts. DNA barcoding has emerged as a species-specifi c PCR primers for the popular method for identifying host– candidate agent allows the screening of parasitoid relationships in that it allows large numbers of fi eld-collected target and the identifi cation of the entire community non-target specimens to determine whether Chapter 4 27

DNA from the candidate agent(s) is present mortality is experienced in rearing, or absent (Gariepy et al., 2007, 2008). molecular detection of parasitoid DNA is Although not as informative in terms of the most effective way to determine representing the entire parasitoid com- whether the host is attacked and whether munity associated with the host, it there is potential for non-target effects addresses the question of host range of the (Gariepy et al., 2008). Neumann et al. candidate agent, provides a more sensitive (2010) demonstrated that DNA of E. detection technique, does not require time- diaspidicola was detectable in positive consuming dissection to separate host and control samples of P. pentagona; however, parasitoid tissues, and is substantially it was not present in the endemic P. cheaper and more cost-effective than DNA pritchardiae following exposure to E. sequencing a large number of samples diaspidicola, thereby demonstrating that (approximately CAN$1.00 per specimen non-target effects on this species are screened with species-specifi c PCR versus unlikely. CAN$10.00 per specimen for bi-directional A slightly different approach is taken DNA sequencing). when dealing with predators as biological The above approach was recently used control agents. In this case, species-specifi c to assess the host specifi city of Encarsia primers are developed for the target pest, diaspidicola Silvestri (Hymenoptera: and are then used to screen the gut Aphelinidae), a candidate biological con- contents of the predator to detect prey trol agent for white peach scale, DNA (see reviews by Symondson, 2002; Pseudaulacaspis pentagona (Targioni) Sheppard and Harwood, 2005; King et al., (Hemiptera: Diaspididae), in . Prior 2008). A number of complications can to the release of this parasitoid in Hawaii, arise in this scenario; because the prey state and federal regulatory agencies item is undergoing digestion in the require host-specifi city testing to ensure predator gut the detectability of its DNA that non-target effects on endemic can be highly variable. In order to interpret Hawaiian fauna are minimal or non- data from fi eld-collected predators, the rate existent. Neumann et al. (2010) tested the of prey digestion must be determined in laboratory host range of this parasitoid on laboratory-based studies and methods often several invasive, economically important need to be developed and adapted to deal scale insects in Hawaii, as well as an with the fact that the targeted DNA is endemic species of palm scale, Palmario- essentially disappearing. For example, coccus pritchardiae Stickney (= Colobo- Greenstone et al. (2010) used the half-life pyga pritchardiae Beardsley) (Hemiptera: of prey detection from laboratory trials to Halimococcidae). The majority of their no- determine the reliability of prey detection choice tests were evaluated based on and enable the ranking of several fi eld- conventional host rearing to obtain collected predators in terms of their parasitoids; however, those involving the importance in a conservation biological endemic P. pritchardiae were assessed control programme for the Colorado potato using species-specifi c PCR primers for E. beetle, Leptinotarsa decemlineata (Say) diaspidicola (de Leon et al., 2010). As this (Coleoptera: Chrysomelidae). Prischmann- potential host species is in a different Voldseth and Lundgren (2011) investigated family of scale insects than the target pest digestion rates in the predatory mite, and can be diffi cult to rear under Gaeolaelaps aculeifer (Canestrini) (Mego- laboratory conditions, it was likely that stigmata: ), and developed a potentially parasitized palm scales would quantitative PCR (qPCR) approach to detect not survive long enough for the parasitoids and quantify the amount of corn rootworm, to complete development and emerge for Diabrotica virgifera virgifera LeConte detection and identifi cation of parasitism. (Coleoptera: Chrysomelidae), DNA present In scenarios where a high degree of in the gut contents of the mites. The use of 28 Chapter 4

PCR enrichment techniques to enhance 4.2.3 Future directions prey detection and remove contamination from fi eld-collected predators has provided 4.2.3.1 Next-generation sequencing valuable methodological advances in a As next generation sequencing (NGS) biological control context (O’Rorke et al., becomes more readily available and afford- 2012; Greenstone et al., 2012). able, this technology will likely facilitate future studies aimed at defi ning entire 4.2.2.3 Detecting interactions between parasitoid food webs and predator diets. natural enemies Pompanon et al. (2011) review the utility of NGS for the analysis of complex food The interaction between different natural webs, and outline considerations for the enemies that share the same host can also successful application of this technology to be clarifi ed using a molecular approach, food web ecology. NGS has the potential to and is an invaluable tool for detecting characterize several thousand sequences indirect non-target effects that arise from for each PCR product and potentially intraguild competition and hyper- allows the identifi cation of any or all parasitism. For example, parasitoids and species present in a given sample without hyperparasitoids share the same host and a priori knowledge of what may be present compete for resources; however, traditional (Hajibabaei et al., 2011; Pompanon et al., rearing precludes the identifi cation of all 2011; Shokralla et al., 2011). This type of species present within a host, as only one approach is already being used to enhance species survives and completes develop- our knowledge regarding host–parasite ment after having consumed the other ecology and evolution (Paterson and species. Dissection, while allowing the Piertney, 2011), and has emerged as a detection of multiple individuals, often rapid, effective method to facilitate the fails to provide species-specifi c identifi - development of microsatellite markers for cation due to the lack of morphologically population genetic studies on biological distinctive immature stages. Similarly, control agents (Santana et al., 2009; parasitized prey items are often overlooked Mlonyeni et al., 2011). As a further appli- in predator gut content analysis as their cation in biological control, the detection remains are generally unidentifi able by and quantifi cation of all species of prey dissection. The use of multiplex PCR within a single predator’s gut or all species assays with species-specifi c primers for the of parasitoid in or on a single pest could be key players in a host–parasitoid–hyper- accomplished using NGS. Such an approach parasitoid system or host–parasitoid– has been used to characterize the diversity predator system can clarify natural enemy of endosymbionts in insect pests (e.g. interactions in biological control pro- Nachappa et al., 2011) and will likely be grammes (Gariepy et al., 2008; Traugott et useful in future studies to characterize al., 2008; Gariepy and Messing, 2012). This Wolbachia spp. (Rickettsiaceae) endo- approach has shown that multiparasitism symbionts associated with parasitoids, by aphid parasitoids is a rare occurrence in which are known to create reproductive the fi eld although it occurs readily in the barriers that can disrupt biological control laboratory when access to unparasitized efforts (Floate and Kyei-Poku, Chapter 6 this hosts is limited (Gariepy and Messing, volume). 2012). Similarly, molecular diagnostic tools have uncovered previously unknown trophic links between aphid parasitoids 4.2.3.2 Evolutionary tools and their hyper parasitoids, and between predators and parasitoids that may disrupt The application of evolutionary tools in aphid biological control programmes biological control has been suggested as a (Gariepy and Messing, 2012; Traugott et al., means to better understand and enhance 2012). the success of introductions and reduce the Chapter 4 29

risk of non-target impacts. Nicholls et al. a science, not an art (van Lenteren, 1980). (2010) used molecular data to examine the In that realm, ecologists have developed a roles of co-evolution, ecological sorting plethora of population and community and anthropogenic disturbance among models, some of which are highly natural enemies associated with an in- applicable to biological control. Math- vasive host in order to test the Host ematical models can be used to determine Pursuit, Host Shift, and Introduction Hypo- best approaches to suppress pest densities theses. Their data on the origins of and maintain them below economic injury Megastigmus stigmatizans Fabricius levels. (Hymenoptera: Torymidae) associated with an invasive oak gall , Cynips quercusfolii L. (Hymenoptera: Cynipidae), 4.3.1 Types of models suggest that the invading natural enemy populations were derived from numerous Mathematical models take several forms, sources and support all three proposed from heuristic to detailed implementation hypotheses. This highlights the diversity of models. Heuristic models, sometimes mechanisms that must be considered when referred to as strategic models, provide a trying to predict the outcome of means for addressing problems in a general community-level modifi cations, including sense. They are not meant to address the intentional release of biological control specifi c cases such as exactly how many agents (Nicholls et al., 2010). To further agents to release, but they may still provide illustrate this point, Vorsino et al. (2012) great value (Godfray and Rees, 2002). For review the utility of evolutionary tools in example, heuristic, state-dependent models biological control programmes, with a have alerted biological control practitioners focus on host-shifts in biological control to consider egg load when evaluating programmes in Hawaii. By incorporating biological control candidates (Minkenberg molecular genetic tools, evolutionary et al., 1992). Similarly, in a recent paper, theory and modelling, biological control Kidd and Amarasekare (2012) illustrated practitioners can gain a better appreciation the importance of evaluating both attack of the genetic variability that allows an rates (functional response) and conversion agent to establish/adapt to a new environ- rates (numerical response) as predictors of ment, better predict competitive dis- suppression and maintenance of pests placement and host shifts, and defi ne the below economic thresholds. Likewise, a most suitable biotypes with genetic recent paper by Wogin et al. (2012) showed variation that refl ects that of their ancestral that inclusion of fl exible parasitoid sex- population (Vorsino et al., 2012). ratio decisions can greatly impact pest Clearly no individual tool will appear as suppression values. Thus, a critical a panacea for solving all issues encountered question to ask is how much detail to in pest management and biological control. include in heuristic models and for which However, as new tools become available parameter? Caution should be exercised as and are incorporated into existing method- even the inclusion of apparently small ology, the science of biological control can details can impact subsequent model be refi ned and direct and indirect effects dynamics (e.g. Murdoch et al., 1998). (both positive and negative) can be better The classic heuristic biological control and more accurately predicted. model is the Nicholson Bailey model that takes the form:

aPt 4.3 Mathematical Models as Tools for HHtt1 Re aPt Biological Control Practitioners PHcett1 1(4.1)

Biological control is a form of applied where Ht is the number of hosts at ecology and should be treated as such: i.e. generation t, R is the host’s replacement 30 Chapter 4

rate and e−aPt is the proportion of hosts 4.3.2.1 Choice of natural enemy that escape parasitism (essentially the zero term in a Poisson distribution), Pt is the One of the fi rst questions that can be number of parasitoids in generation t and c addressed with mathematical models is is the conversion rate of hosts in which natural enemy is best suited to generation t to parasitoids in generation control the target pest? The models may t+1. take two forms depending upon the life In contrast to heuristic models, imple- history of the organisms in question, mentation or tactical (Godfray and Rees, continuous versus discrete time. Regard- 2002) models include the details for less of the form, however, the models specifi c systems and are meant to solve should take into account dynamics of both specifi c problems. For example, Moerkens the pest and the natural enemy. If the target et al. (2011) developed earwig- organism has discrete generations the specifi c, temperature-dependent develop- model will often take the general form of ment models to determine optimal timing the Nicholson Bailey discussed above. for releasing biological control agents Note, however, that to provide suffi cient against this pest. These kinds of models resolution to evaluate host control poten- may be analytical in form or they may be tial, use of the aforementioned models developed as computer simulation models. often requires one to relax many of the In the latter category, simulations may very restrictive assumptions found in eqn comprise a number of analytical sub- 4.1. For example, Nicholson and Bailey models (e.g. Gutierrez et al., 2011). For described the attack rate of parasitoids as a example, temperature-driven population linear, non-saturating function of host dynamics simulation models often employ density. In more sophisticated models (e.g. the classic analytic Brière et al. (1999) Henry et al., 2010), realistic functional model to describe pest and/or biological responses are included wherein attacks control agent development. increase in some decelerating manner up to To summarize, the choice of heuristic or some maximum; this takes into account the implementation model depends upon the need to include search and handling time, goal of the biological control scientist. In per host, such that at some point, host the case of the former, the goal is to density is so high that the parasitoid develop a general understanding of a spends virtually all of its time handling biological control problem and, from there, hosts (see the I Love Lucy chocolate factory develop appropriate guidelines. In the case skit to visualize such an occasion). The of the latter, the goal is to solve a specifi c lack of egg limitation is another restrictive pest problem. Further, the decision on assumption that can be replaced with an degree of complexity is up to the re- empirically derived egg load and on and searcher but it is recommended that on. The point here is that the basic logic of researchers strive for simplicity, i.e. ele- the Nicholson Bailey model remains but gance. The risk of omitting essential com- modifi cations can easily be incorporated ponents is generally offset by reduction in for specifi c systems. Thus, if differences clarity of complex models. result from inclusion of a new (or modifi ed) term or function, one can be confi dent that this is due to inclusion of 4.3.2 Major questions addressed by models the new term and not due to use of a different model. There are three major areas where mathe- The classic Nicholson and Bailey model matical models can be important tools in has a single age class for each species. If biological control: (i) selection; (ii) pro- the host and control agent populations are duction; and (iii) release of natural age structured then it may be best to enemies. employ population projection matrices that Chapter 4 31

are coupled to describe interactions be- Here, the parasitoid is found in two tween the host and enemy. These matrices stages, immature and mature (1 and 2, typically work with instar classes and take respectively). As noted above, these the form: models will typically include host mortality and parasitoid birth functions §·aF11 00 n ¨¸within the matrix cells that depend upon aa 00 ¨¸21 22 (4.2) densities of their interacting species. ¨¸00aa 32 33  Analysis of matrix-based population ¨¸ ©¹00ann,1  0 growth has matured greatly in the past couple of decades, partly due to Caswell’s where a is the stage (instar)-specifi c n,n−1 (2001) tome on the topic (also see Morris transition probability of moving from the and Doak, 2002, who employ population n−1 to the n’th instar and F is the stage n matrices in their excellent book on (instar)-specifi c fecundity. This transition population viability analysis). In addition, matrix is multiplied by an age class vector matrix analysis software is readily to give a new age class vector in the next available in software packages such as time period. Note that individuals from any Matlab and R and do not require much given stage also have some probability of training to use. remaining in the same stage (a ), moving to nn When pest species grow continuously, it the next stage (an+1,n) or dying; these three probabilities necessarily sum to unity. is more appropriate to employ calculus Particularly useful, these models can be based, differential equation models that are solved to provide elasticity values; these derived from the classic Lotka-Volterra values indicate which specifi c terms, e.g. models, again where many of the highly 2nd instar survival, have the greatest impact restrictive assumptions are relaxed. Here on pest dynamics (Mills, 2008). This can be the basic model takes the form: particularly important when pests comprise several developmental stages. Population dH bdPHHH dt projection matrices typically assume that (4.4) the transition probabilities and age-specifi c dP bHpp d P fecundities are constants but they need not dt be so. For example, per capita mortality of where: H is the host (pest) and P is the hosts could be written as specifi ed predator (parasitoid). Note the asymmetry functions of parasitoid and host density wherein predators impact host death rate (recall the functional response above). and hosts impact predator birth rates but These more realistic models are not not vice versa. analytically tractable but recent methods of Regardless of the models used, there are stochastic analysis are becoming increas- several questions that should be addressed: ingly common in conservation biology and (i) degree of host suppression; (ii) stability could easily be applied to pest management of the pest–agent dynamics; and (iii) (e.g. Stone et al., 2009). collateral impacts (see below). The work of The matrix above is for a single species, Godfray and Waage (1991) provides a for example, the pest. When a natural classic example wherein stage structured enemy is included, the matrix takes the models were used to compare control form: potential for two proposed encyrtid parasitoids of the mango mealy bug §·aF11 00 n 00 ¨¸ aa 0000 Rastrococcous invadens Williams (Hem- ¨¸21 22 iptera: Pseudococcidae). They showed that ¨¸0000aa ¨¸32 33 (4.3) Gyranusoidea tebyg Noyes was superior to 00a  0 0 0 ¨¸nn,1 Anagyrus sp. (Hymenoptera: Encyrtidae) ¨¸00 0 00pF ¨¸11 2 and that release of both agents would not ¨¸ ©¹00 0 00pp21 22 lead to improved control. 32 Chapter 4

4.3.2.2 Production of natural enemies phylogeny theory, i.e. hosts most closely related to target hosts are given most Mathematical models can dramatically stringent tests and more distantly related, increase effi ciencies of rearing methods by non-targets are less stringently tested; explicitly considering the incremental phylogenies are determined as discussed costs and benefi ts from various rearing above in the section on molecular methods. densities. As the number of natural This methodology can be particularly enemies released into a rearing cage effective when working with biological increases so will the increase in prod- control of weeds but less so with biological uctivity of the population in that rearing control of insect pests. The principal cage; however, that increase is rarely linear. reason for this difference is that plants are In fact, the productivity curve generally most readily attacked based upon their decelerates up to some asymptotic value, chemical constituencies whereas insect thus there will be an optimal input where hosts are often attacked based upon their optimal is defi ned as the maximal net locations and ecological relationships, profi t (gross profi t minus costs). This which may or may not link closely with optimal value can be determined relatedness to target hosts. How then might empirically or via marginal or incremental we assess risk to non-target arthropods? analysis (see Roitberg, 2004). Note that an One method is to employ oviposition accurate depiction of the productivity breadth theory. This theory, an offshoot of curve is essential; however, this is not a optimal diet theory, predicts how readily simple task because many insects (in- individuals will increase their willingness cluding parasitoids and predators) are to accept low quality (non-target) hosts. highly labile and generally non-linear in The theory, which derives optimal de- response to rearing conditions. As such, cisions based upon maximizing lifetime simple extrapolation from a few rearing reproductive fi tness, compares the fi tness densities could be very misleading. For from successively broad ‘diets’. In example, it is known that parasitoids Charnov’s original formulation (Charnov, increase their rates of superparasitism as 1973), food item value was based upon the the density of competitors increases but energy content divided by handling time. these rates are highly variable both within Items are ranked according to this and among species. Since superparasitism weighted energy content. Thus, the theory is largely a costly event from a biological assumes that the highest rank item will control factory perspective, it would be always be eaten when encountered but the good to be able to predict and avoid such question is, under what conditions should events. Charnov and Skinner (1985) pro- lower ranked items be accepted? The vided initial theory for predicting clutch answer is, when the rate of energy intake is size in parasitoids and since those initial greater with the lower ranked item papers many modifi cations and improve- included. One fi nal term is required, item- ments have been made that include, specifi c encounter rate h . So, for example, learning, egg load and competition. i when encounter rates with top ranked items are low, it might pay to accept the common lower ranked item when 4.3.2.3 Risks to non-target organisms encountered. The equation (an inequality), An important concern in biological control as derived by Charnov (1973) and Pulliam is the unintended harm to non-target (1974), is shown below: organisms. Thus, importation and release O!OOE/t E/t E/t (4.5) decisions should take this risk into account 11 1 11 1 22 2 under the general umbrella of host range In the optimal diet model, the currency (see Van Driesche and Reardon, 2007). In that is maximized is rate of energy intake. general, non-target risk experiments are A reformulated optimal host breadth model frequently conducted using centrifugal replaces energy with reproductive fi tness Chapter 4 33

units, i.e. offspring produced per unit time. evolved toward the optimal and thus is at Thus, a host with relatively low offspring stasis, genetically speaking. As such, there survival but very short handling time could was little utility to include any genetic have a higher net value than one with high constraints. By contrast, models that survival but inordinately long handling predict evolution of host breadth must time. explicitly consider the genetic architecture Barrette et al. (2009) and Henry et al. of a population along with the relative (2010) provide examples of such an reproductive fi tness of different genetically approach across instars within a single based foraging variants (little is known host species. Here, reproductive fi tness is about the distribution of such variants but denoted by offspring biomass, weighted by the work of Wajnberg (2004) on Tricho- (instar-specifi c) probability of capture. gramma spp. (Hymenoptera: Tricho- To employ the optimal host breadth grammatidae) is a good start). model for non-target risk, one would simply Finally, as discussed above, insect replace instar with host species. What one behaviour is highly labile, thus any then does is to consider worse case predictive models should consider the scenarios and ask whether the potential range of behaviours that a biological control agent will likely expand its oviposition agent might express under a variety of ‘diet’ to include non-target species. Such conditions or environments, the so-called worst-case scenarios would include those genotype-specifi c reaction norm. Roitberg situations where the target hosts are very (2004) provides a means for predicting such rare or absent, perhaps due to impacts from host-fi delity reaction norms where the the biological control agent. environment is host deprivation time, i.e. One potential weakness of the models the length of time over which the target described above is that they make organism is not available. calculations independent of the physio- logical state of the biological control agent. If, for example, eggbound parasitoids are 4.3.3 Future directions more likely to increase their host-diet breadth than individuals with low egg Mathematical models are powerful tools loads, then this must be considered as part that can be used to improve biological of the analysis on risk to non-target control programmes. There are two keys to organisms. Roitberg (2000) provides their successful development and imple- methods for including egg-load state into mentation: (i) theoreticians should listen non-target risk models. carefully to those who employ such models The other concern, and one which is to ensure that they get the details right; and more diffi cult to predict, is the probability (ii) practitioners should carefully examine that the new agent will evolve to attack such models before implemen tation to non-targets. The models required to make ensure that they understand their assump- such predictions take a different form. In tions and implications. This mar riage of the previous models, one assumes that the theory and application will surely benefi t population of insects of interest has us all.

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5 A Novel Approach for Developing Microbial Biopesticides

Susan M. Boyetchko1 and Antonet M. Svircev2 1Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 2Agriculture and Agri-Food Canada, Vineland, Ontario

5.1 Introduction microbial biopesticides as ‘green’ alter- natives to synthetic pesticides. It was During the past several decades, re- almost a century ago when Bacillus searchers worldwide have devoted their thuringiensis Berliner (Bacillaceae) was energy in the pursuit of developing fi rst reported as a possible biological

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 38 Chapter 5

control agent against the European corn economics, sociology, law, international borer, Ostrinia nubilalis (Hübner) (Lepi- trade, business and many other fi elds not doptera: Pyralidae), (Côté, 2007) and since traditionally considered in a scientifi c then, microbial-based biological control endeavour (Lazarovits et al., 2007). has been demonstrated as a promising The early biopesticide models or proto- technology for pest management of not types often had a single pest target, and only insect pests, but plant pathogens and utilized a simple formulation such as water weeds (Mason and Huber, 2002; Glare, and possibly a surfactant for the appli- 2004; Punja and Utkhede, 2004; Vincent et cation on to the target. These early al., 2007; Bailey et al., 2010; Kabaluk and successes that resulted in biopesticide Gazdik, 2011). The literature is replete products led to the perception by re- with reviews and the discovery of searchers, industry and the agri-food and ‘promising’ or ‘potential’ biopesticide forestry sectors that development of bio- candidates. However, those familiar with pesticide products would be easily the premise of developing a microbial resolved once a microbial candidate was biological control agent into a biopesticide identifi ed and selected in the laboratory product will confess that the basic concept (Glare, 2004; Boyetchko, 2005; Hallett, underestimates the complexities involved 2005; Hynes and Boyetchko, 2006; Ash, in taking a living organism from the lab 2010; Glare et al., 2012). The reality facing bench through a process of mass researchers in this scientifi c arena has production and formulation, towards the resulted in the recognition that accom- application into an ecosystem that, in plishing the end goal requires not only itself, is complex. good science, but tenacity, persistence and The discovery of new and promising a great deal of creativity. Further to this microbial candidates for development as end, traditional research in biopesticides active ingredients in biopesticides has far has often been conducted in individual outpaced the knowledge and related laboratories while biological control technology required to bring these to requires networks of scientists across a commercialization. Although there are variety of disciplines, regardless of the numerous biopesticides registered for use commodity (cereals, oilseeds, fruits, globally, including over 100 biopesticide vegetables etc.), ecosystem (forestry, fi eld active ingredients registered in the USA crops, fruit orchards, horticulture) and and more than 24 different microbially target pest (e.g. insect pest, plant pathogen, active substances registered in Canada weed), being studied (Schwartz et al., since 1972 (Mason and Huber, 2002; Glare, 2007; Boyetchko and Svircev, 2009). 2004; Hynes and Boyetchko, 2006; Bailey Moreover, once researchers recognize that et al., 2010; Kabaluk and Gazdik, 2011), the the terminology utilized in their individual public wonders why there are ‘so few’ disciplines is often describing similar biopesticides available in the market place. scientifi c principles, they realize that there The expectation that once a microbial is commonality in the objectives and pro- organism has been discovered in the cesses required to successfully bring to laboratory and that the fi nal biopesticide fruition a microbial organism into a bio- product is imminent has led to dis- pesticide product. As a network, re- appointment and possibly the ‘popular searchers have also accumulated a wide belief’ that biopesticides do not work or range of lessons learned, successes and will not be feasible as pest control failures from the past, developed current products. The fact remains that the fi eld of knowledge, and envisioned future direc- biological control combines various scien- tions that can advance our achievements in tifi c disciplines including biology, micro- biopesticide research (Mason and Huber, biology, entomology, plant pathology, weed 2002; Boyetchko, 2005; Vincent et al., science and agronomy. It is further 2007; Ash, 2010; Boyetchko and Svircev, complicated by subject matters related to 2011). Chapter 5 39

5.2 Strategic Framework for biopesticide candidate must demonstrate Biopesticide Development high effi cacy and/or potency for controlling the target pest during the early discovery Essential to the process of developing a phase. Validation of the biopesticide biopesticide is the discovery and screening candidate in concert with the selected phase, or ‘bioprospecting’. The origin, platform technologies can be conducted in isolation and selection of a potential the fi eld, yet a less than spectacular result biopesticide candidate can be complex and does not mean that the technology should is dependent on the target pest and crop be abandoned. Fermentation and/or for- (Köhl et al., 2011; Pliego et al., 2011). None mulation technologies will not necessarily the less, the selection of a suitable improve a ‘mediocre’ biopesticide can- screening method is critical; and pre- didate (Boyetchko, 2005; Ash, 2010). liminary assessment using a mass-through- However, selection of the best strains is put method will aid in the selection of a essential in the early stages, development few candidates from several hundreds or and improvement of the platform tech- thousands of wild-type isolates. nology will certainly be critical to the The fundamental principles and factors eventual success of a biopesticide product. underlying the selection of a suitable It is important to consider and identify microbial candidate are taxonomy, bio- limitations of the platform technologies logical characterization, mode of action and determine whether improvements or and effi cacy. Integral to developing a modifi cations will optimize biopesticide biopesticide product is the selection of effi cacy. Often, the fermentation and platform technologies that include: (i) formulation technology that is available to fermentation; (ii) formulation; and (iii) industry researchers is limited. Platform application technologies. These factors technologies developed by industry tend to form the basis for the feasibility of creating be proprietary and not readily accessible, if a biopesticide product. Appropriate fer- at all. Research networks and collabor- mentation methods (e.g. liquid/submerged ations involving government, university versus solid-state), formulation approaches and industry are important. Such networks (liquid/spray application versus soil- would allow new biopesticides to be applied versus seed treatment) and developed effi ciently, using the most application methods (e.g. aerial- versus appropriate, state-of the-art platform tech- soil-applied), must be selected and/or nologies. Such networks provide industry developed (Boyetchko and Rosskopf, 2006; with opportunities to build capacity Hynes and Boyetchko, 2006; Ash, 2010; through sharing and licensing platform Leggett et al., 2011; Glare et al., 2012). The technologies. inability to choose the most appropriate fermentation and/or formulation system during the research and development 5.3 The Process of Biopesticide (R&D) process has often led to ‘orphaned’ Development – the Innovation Chain biopesticide technologies. Shelf life and stability of a formulated microbial product With the lessons learned over the past is often affected by the fermentation pro- decades, it has become apparent that there cess prior to formulation since it infl uences is a need to demonstrate that biopesticide microbial physiology (Boyetchko and Peng, research in general has evolved beyond the 2004; Hynes and Boyetchko, 2006; Leggett lab bench and that there is a clear process et al., 2011). for implementation and commercialization. The three platform technologies (fer- For this reason, in 2007, a strategy for mentation, formulation, application tech- developing biopesticides was designed nology) are invariably linked and have a with the creation of a national team of major infl uence on biopesticide perform- Agriculture and Agri-Food Canada scien- ance in the fi eld. First and foremost, the tists working on biopesticides (Boyetchko 40 Chapter 5 and Svircev, 2009; Bailey et al., 2010). The innovation chain contains nine critical concept of the ‘biopesticide innovation stages where ‘Go versus No-Go’ decisions chain’ incorporates knowledge of the target should be made on the feasibility of pest, including pest biology, population proceeding with a biopesticide project to dynamics, economic losses and market the next step. The innovation chain impact, while also taking into consider- encourages the development of a variety of ation the components required to discover platform technologies that can be and develop a biopesticide for the target expanded to other potential applications pest(s) (Fig. 5.1). This model takes the for multiple use patterns, thus broadening researcher from the early discovery and the market to a variety of target pests and bioprospecting phase for new microbial crop production systems (Boyetchko and agents as active ingredients to the early Rosskopf, 2006; Hynes and Boyetchko, proof-of-concept stage where the feasibility 2006; Ash, 2010; Bailey et al., 2010). of the candidate for biological control is Further along the innovation continuum, demonstrated under controlled environ- additional large-scale and multi-site fi eld ment and/or fi eld conditions. Emphasis is trials allow the testing of the mass- placed on the basic biological and environ- produced and formulated biopesticide mental factors affecting the biopesticide as product under the fi eld conditions in well as the platform technologies related to which it will ultimately be used. Any fermentation, formulation, application and further problems encountered with product delivery. The focus is not solely on the formulation can be rectifi ed and other biopesticide, but it superimposes the agronomic situations can be addressed. rationale for selecting the target pest, The importance of economic and which considers pest surveys, pest man- regulatory considerations should not be agement issues, e.g. pesticide resistance, underestimated because they focus on the organic production, invasive species and ‘business’ of biopesticides and thus in- market potential in order to engage fl uence the success or failure for com- industry investment. The biopesticide mercialization (Ash, 2010; Bailey et al.,

licence and uses

Discovery and BCA selection

Build in Go versus No-Go decisions and create smooth transition through stages of innovation chain

Fig. 5.1. A solution for delivery of biopesticides: AAFC Biopesticide Science Innovation Chain (Boyetchko and Svircev, 2009). Chapter 5 41

2010). The proposed fi eld of use and alternatives to chemical pesticides due to market will determine the nature of the the expanding organic food industry, the data required to demonstrate effi cacy under withdrawal and/or phasing out of synthetic large-scale application and thus to register pesticides from the market place and the the product. The later stages of the lack of existing pest control options for innovation chain test the robustness and/or specifi c crop pests and crop commodities weakness of the earlier decisions made in (Floate et al., 2002; Boyetchko, 2005; the process by focusing on selection of Bailey et al., 2010; Leggett et al., 2011). collaborators, regulators and industry part- Because of the immense costs associated ners to develop data packages for regis- with R&D and registration for chemical tration and commercialization. In addition, pesticides, multinational companies are commercial scale-up will still infl uence the inclined to focus on global, high market fi nal stages of product development from potential crops and cropping systems (Ash, the bench to pilot scale to commercial 2010). Therefore opportunities exist for the manufacture and could result in a decision development of new pest control products to terminate or modify the project. The in non-core or niche markets, many of industry partner often takes the lead for which are lucrative markets to small commercial scale-up and registration, but companies. Environmental health and food the scientist’s collaboration with industry safety issues that address environmental in technology adoption can help to identify persistence, lower mammalian toxicity, problems and additional agronomic studies spray drift and chemical residues in soil, that will facilitate implementation and water and the food supply are further integration into pest management pro- accelerating the need for alternatives to grammes. The scientist (or inventor) of the chemicals. In Canada, municipal and original biopesticide technology possesses provincial legislation has resulted in the essential ‘know-how’ and expertise, which banning of synthetic pesticide use in city may be of great value to the industry limits, which thus affects consumers such partner. Thus, a strong collaboration can as the home gardener and lawn care help ease the transition from science and experts. technology to a commercial product, rather There is a general optimism for the than handing off the technology pre- future of biopesticides (Ash, 2010; Bailey maturely to the industry partner. et al., 2010; Glare et al., 2012). Although The strength of the innovation chain pest management has generally focused on concept is that collaborators can enter into synthetic pesticides, particularly during a project anywhere along the innovation the last four to fi ve decades, it has become continuum, as their expertise is required. more expensive for industry to discover This model encourages the assessment of new leading molecules, and the launch of the commercial feasibility of the bio- new chemical pesticides has been on the pesticide product at critical stages of its decline since 2005 (Glare et al., 2012). It development. Technological components could be argued that research and that affect the performance of the bio- discovery of biopesticides has reached a pesticide can be validated and unforeseen coming of age, partly because of greater issues related to effi cacy may result in choice of fermentation and formulation modifi cations, or development of new technologies. However, accessibility to platform technologies. more diverse technologies will be critical to the advancement of biopesticides. Economics and market size certainly play 5.4 Summary an important role for advancing bio- pesticide candidates. Lack of investment There is a greater need, more than ever, to by industry has often been the result of develop biopesticides for the 21st century. poor choices by researchers for target pests, There is an increasing market demand for and the development of a biopesticide for a 42 Chapter 5

single target pest rather than one that has a biopesticide innovation chain represents a broader spectrum of activity. There is a model that could be utilized to evaluate need for a focused strategy that brings and accelerate the progress of a bio- together researchers from diverse back- pesticide project towards commercial- grounds towards a common goal. The ization.

References

Ash, G.J. (2010) The science, art and business of successful bioherbicides. Biological Control 52, 230–240. Bailey, K.L., Boyetchko, S.M. and Längle, T. (2010) Social and economic drivers shaping the future of biological control: a Canadian perspective on the factors affecting the development and use of microbial biopesticides. Biological Control 52, 221–229. doi:10.1016/j.biocontrol.2009.05. Boyetchko, S.M. (2005) Biological herbicides in the future. In: Ivany, J.A. (ed.) Weed Management in Transition. Topics in Canadian Weed Science, Vol. 2. Canadian Weed Science Society – Societe canadienne de malherbologie, Sainte-Anne-de-Bellevue, Quebec, pp. 29–47. Boyetchko, S.M. and Peng, G. (2004) Challenges and strategies for development of mycoherbicides. In: Arora, D.K., Bridge, P. and Bhatnagar, D. (eds) Fungal Biotechnology in Agricultural, Food, and Environmental Applications, Vol. 21. Marcel Dekker, New York, pp. 111–121. Boyetchko, S.M. and Rosskopf, E.N. (2006) Strategies for developing bioherbicides for sustainable weed management. In: Singh, H.P., Batish, D.R. and Kohli, R.K. (eds) Handbook of Sustainable Weed Management. The Haworth Press, New York, pp. 393–430. Boyetchko, S.M. and Svircev, A. (2009) Biopesticides: Strategies for discovery, development, and adoption. Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada, AAFC 10733, Cat. No. A52-120/2009E-PDF, ISBN 978-1-100-11640-2. Boyetchko, S.M. and Svircev, A.M. (2011) Canadian biopesticides and bioherbicides. In: Proceedings of the Soils and Crops Workshop. University of Saskatchewan, Saskatoon, Saskatchewan, Canada, 13 pp. Côté, J.-C. (2007) How early discoveries about Bacillus thuringiensis prejudiced subsequent research and use. In: Vincent, C., Goettel, M.S. and Lazarovits, G. (eds) Biological Control, A Global Perspective, CAB International, Wallingford, UK, pp. 169–178. Floate, K.D., Bérubé, J., Boiteau, G., Dosdall, L.M., van Frankenhuyzen, K., Gillespie, D.R., Moyer, J., Philip, H.G. and Shamoun, S. (2002) Pesticides and biological control. In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981-2000. CAB Intyernational, Wallingford, UK, pp. 4–14. Glare, T.R. (2004) Biotechnological potential of entomopathogenic fungi. In: Arora, D.K., Bridge, P. and Bhatnagar, D. (eds) Fungal Biotechnology in Agricultural, Food, and Environmental Applications, Vol. 21. Marcel Dekker, New York, pp. 79–90. Glare, T., Caradus, J., Gelernter, W., Jackson, T., Keyhani, N., Köhl, J., Marrone, P., Morin, L. and Stewart, A. (2012) Have biopesticides come of age? Trends in Biotechnology 30, 250–258. Hallett, S.G. (2005) Where are the bioherbicides? Weed Science 53, 404–415. Hynes, R.K. and Boyetchko, S.M. (2006) Research initiatives in the art and science of biopesticide formulations. Soil Biology and Biochemistry 38, 845–849. Kabaluk, J.T. and Gazdik, K. (2011) Directory of Biopesticides for Agricultural Crops in OECD Countries. Available at: https://www4.agr.gc.ca/MPDD-CPM/search-recherche.do?lang=eng (accessed 22 November 2012). Köhl, J., Postma, J., Nicot, P., Ruocco, M. and Blum, B. (2011) Stepwise screening of microorganisms for commercial use in biological control of plant-pathogenic fungi and bacteria. Biological Control 57, 1–12. Lazarovits, G., Goettel, M.S. and Vincent, C. (2007) Adventures in biocontrol. In: Vincent, C., Goettel, M.S. and Lazarovits, G. (eds) Biological Control, A Global Perspective, CAB International, Wallingford, UK, pp. 1–6. Leggett, M., Leland, J., Kellar, K. and Epp, B. (2011) Formulation of microbial biocontrol agents – an industrial perspective. Canadian Journal of Plant Pathology 33, 101–107. Chapter 6 43

Mason, P.G. and Huber, J.T. (2002) Biological Control Programmes in Canada, 1981-2000. CAB International, Wallingford, UK. Pliego, C., Ramos, C., de Vicente, A. and Cazorla, F.M. (2011) Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant and Soil 340, 505–520. Punja, Z.K. and Utkhede, R.S. (2004) Biological control of fungal diseases on vegetable crops with fungi and yeasts. In: Arora, D.K., Bridge, P. and Bhatnagar, D. (eds) Fungal Biotechnology in Agricultural, Food, and Environmental Applications, Vol. 21. Marcel Dekker, New York, pp. 157–171. Schwartz, J.-L., Campbell, W. and Llaprade, R. (2007) The biocontrol network: a Canadian example of the importance of networking. In: Vincent, C., Goettel, M.S. and Lazarovits, G. (eds) Biological Control, A Global Perspective. CAB International, Wallingford, UK, pp. 415–427. Vincent, C., Goettel, M.S. and Lazarovits, G. (2007) Biological Control, A Global Perspective. CAB International, Wallingford, UK.

6 Reproductive Parasites: Symbiotic Bacteria for Potential Use in Biological Control

Kevin D. Floate1 and George K. Kyei-Poku2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2Natural Resources Canada, Sault Ste Marie, Ontario

6.1 Introduction Reproductive parasites are symbiotic bacteria that affect host reproduction. Symbiotic bacteria increasingly are being These include species in the genera recognized for their profound and diverse Wolbachia and Rickettsia (_-Proteo- effects on the survival and reproduction of bacteria) (Rickettsiaceae), Arsenophonus their arthropod hosts. This has increased (a-Proteobacteria) (Enterobacteriaceae), interest in the potential application of Car dinium (Bacteroidaceae) and Flavo- these bacteria in biological control pro- bacterium (Flavobacteriaceae), and Spiro- grammes. The current chapter provides an plasma (Spiroplasmataceae) (Duron et al., overview for one group of these symbiotic 2008). Greatest attention has been given to bacteria, i.e. ‘reproductive parasites’, and Wolbachia, which may infect 20–70% of addresses recent developments regarding all insects (Jeyaprakash and Hoy, 2000; their use in pest control. More extensive Floate et al., 2006; Hilgenboecker et al., reviews are provided by Novakova et al. 2008) and which may be ubiquitous in (2009), Harris et al. (2010), Oliver et al. some insect orders, e.g. Phthiraptera (Kyei- (2010), Feldhaar (2011), White (2011) and Poku et al., 2005; Covacin and Barker, Zindel et al. (2011). 2007). Arsenophonus has been reported in

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 44 Chapter 6

11% of 36 insect species (Taylor et al., 2011) and Cardinium in 6% of 99 arthro- pod species (Zchori-Fein and Perlman, 2004). A survey of 139 arthropod taxa detected infection frequencies of 23% for Wolbachia, 4% for Arsenophonus, 4% for Cardinium, 1% for Rickettsia and 7% for Spiroplasma with co-infections of different symbiont genera detected in eight taxa (Duron et al., 2008). Co-infections fre- quently are reported (Enigl and Schaus- berger, 2007; Taylor et al., 2011; Toju and Fukatsu, 2011; White et al., 2011; Sebastien et al., 2012; see Fig. 6.1). Infections of these bacteria are mainly transmitted vertically, from infected females to their offspring via egg cyto- plasm. With the exception of Arseno- phonus (Huger et al., 1985; Duron et al., 2010), horizontal transmission is rare. This places selective pressure on the bacteria to enhance the number and (or) quality of their host’s female offspring to facilitate the spread of infections in the host population. In this regard, they have been remarkably successful. An infection of Wolbachia reportedly spread in Californian popu- lations of Drosophila simulans Sturtevant (Diptera: Drosophilidae) at the rate of 100 km year−1 (Turelli and Hoffmann, 1991). Indirect evidence suggests that a Wol- bachia infection in Drosophila melano- gaster Meigen (Diptera: Drosophilidae) has spread globally within the last century (Riegler et al., 2005). It is this ability to Fig. 6.1. Egg of the wasp Trichomalopsis manipulate host reproduction that makes sarcophagae stained to show two types of this group of symbiotic bacteria particu- intracellular bacteria. Wolbachia (W) are larly attractive to biological control clustered at one end of the cell. Unidentifi ed researchers. (U) bacteria of larger size are scattered throughout the cytoplasm (Photo credit: Fran Leggett). 6.2 Consequences of Infections on Host Reproduction with one or more strains of the symbiont. 6.2.1 Cytoplasmic incompatibility Bidirectional CI arises in crosses between partners infected with different strains of Cytoplasmic incompatibility (CI) is the the symbiont. CI in haplo-diploid species most common form of host manipulation. typically produce male-biased sex ratios It is most often reported for Wolbachia, less and (or) fewer progeny, whereas CI in so for Cardinium (Duron et al., 2008). diplo-diploid species prevents the pro- Unidirectional CI arises in crosses between duction of offspring. In contrast to uninfected females and males infected uninfected females, infected females can Chapter 6 45

mate with either infected or uninfected bidiformes: Tetranychidae) mites do not males without consequence to produce induce parthenogenesis through gamete infected progeny. Thus, the prevalence of duplication, but rather a process of func- infected females increases with each tional apomixis; i.e. progeny are geneti- generation. cally identical to their mother (Weeks and The mechanism for CI is not fully Breeuwer, 2001). understood. The presence of Wolbachia in male hosts is thought to introduce a factor into their sperm that prevents embryo- 6.2.3 Feminization genesis in the fertilized egg, unless the female partner is infected with the same Feminization has been reported for Wolbachia strain to reverse the effect. Wolbachia and Cardinium. Infections of Without this ‘rescue’ effect, the paternal Wolbachia in isopods cause genetic males chromosomes mis-segregate during cell to develop into phenotypic females that division in the fertilized egg (Tram et al., mate and produce offspring (Cordaux et al., 2006). In diplo-diploid species, mis- 2004 and references therein). Sex in segregation kills the embryo. In haplo- isopods is determined by the action of a diploid species, mis-segregation can have male hormone that suppresses female two consequences (Tram et al., 2006). development. Wolbachia is thought to Complete mis-segregation causes the ‘loss’ inhibit development of the androgenic of the paternal chromosomes such that the gland that produces this hormone and also fertilized egg develops as though haploid may block receptor sites required for to produce a male individual, i.e. male- hormone activity. Thus, infected isopods development (MD) type CI. Partial mis- produce female-biased sex-ratios regardless segregation prevents normal cell division, of their sex chromosome complement (WZ which kills the fertilized egg, i.e. female- = females; ZZ = males) (Rigaud et al., mortality (FM) type CI. 1997). Wolbachia also induce feminization in insects, e.g. Lepidoptera (Hiroki et al., 2002) and Hemiptera (Negri et al., 2006), 6.2.2 Parthenogenesis induction although the mechanism is unclear. Infections of Cardinium in the mite Wolbachia, Cardinium and Rickettsia can Brevipalpus phoenicis (Geijskes) (Trom- induce parthenogenesis (PI) in haplo- bidiformes: Tenuipalpidae) have been diploid species by gamete duplication. In associated with haploid females (Weeks et chromosomal sexual reproduction that al., 2001). Infections of Cardinium in the involves strict differentiation and gameto- wasp Encarsia hispida De Santis genesis, males normally develop from (Hymenoptera: Aphelinidae) cause unfertilized (haploid) eggs and females parthenogenesis (Zchori-Fein et al., 2004). from fertilized (diploid) eggs. In un- Because feminized males produce infected fertilized eggs, PI infections interfere with offspring, this reproductive manipulation the separation of chromosomes during the by the symbiont serves to spread the fi rst mitotic division to cause the formation infection in the host population. of a diploid nucleus with two identical sets of chromosomes. By virtue of being diploid, such eggs develop into females 6.2.4 Male-killing (Stouthamer and Kazmer, 1994; Panne- bakker et al., 2004). Conversely, the fi rst Male-killing (MK) has been associated with mitotic division may be unaffected and Arsenophonus, Flavobacterium, Rickettsia, produce haploid nuclei, which then fuse to Spiroplasma and Wolbachia (Stevens et al., restore the diploid condition (Stille and 2001; Duron et al., 2008). In each case, the Dävring, 1980; Gottlieb et al., 2002). In symbiont causes the death of male progeny contrast, Wolbachia in Bryobia spp. (Trom- during embryogenesis via an unknown 46 Chapter 6

mechanism. This increases the fi tness of gaster (Teixeira et al., 2008) and D. infected females by reducing competition simulans (Osborne et al., 2009) against from male siblings, whose corpses also viruses. Spiroplasma protects Drosophila provide a ready source of nutrition for their neotestacea Grimaldi, James & Jaenike newly hatched sisters. These benefi ts help (Diptera: Drosophilidae) against the explain why MK is relatively common in sterilizing effects of a parasitic nematode insects that lay eggs in clutches. For (Jaenike et al., 2010). Spirosplasma in example, MKs have been reported in about Drosophila hydei Sturtevant (Diptera: half of the aphidophagous Coccinellidae Drosophilidae) reduces egg-to-adult sur- (Coleoptera) species in the UK (Hurst and vival of the parasitoid wasp Leptopilina Jiggins, 2000). heterotoma (Thomson) (Hymenoptera: Figitidae) (Xie et al., 2010). Infections may suppress the actions of 6.3 Other Consequences otherwise deleterious genes in the host’s genome. Chi2 is an allele for the chico The persistence of reproductive parasites gene, which affects growth regulation in D. in host populations is intuitive when melanogaster. It is completely lethal in the infections are favoured by altered host homozygous condition, but only when reproduction. Less intuitive is the per- infections of Wolbachia are removed from sistence of these bacteria when they have the host (Clark et al., 2005). Wolbachia also no apparent effect on host reproduction. In has been found to suppress a defect in the such cases, infections can enhance the sex-lethal (Sxl) gene that otherwise pre- fi tness of the host in a number of remark- vents oogenesis in D. melanogaster (Starr able ways. and Cline, 2002). Infections can mediate interactions Infections can affect host behaviour. In between their host insects and the plants some cases, the altered behaviour appears upon which the insects feed. Forty years to be a response by the host to minimize ago, it was shown that leaf-mining insects the adverse effects of cytoplasmic in- can increase levels of the plant hormone compatibility. In populations of the two- cytokinin to generate local areas of spotted spider mite Tetranychus urticae photosynthetic tissue (‘green islands’) in Koch (Trombidiformes: Tetranychidae), otherwise senescent leaves to prolong the infections of Wolbachia alter mating and availability of nutrients for the insect oviposition behaviour such that uninfected (Engelbrecht et al., 1969). Induction of and infected females preferentially mate these green islands by the leaf-mining with males of corresponding infection moth Phyllonorycter blancardella (Fabri- status (Vala et al., 2004). In D. melano- cius) (Lepidoptera: Gracillariidae) now has gaster and D. simulans, infected males been linked to the manipulation of mate with higher frequency than un- cytokinin by the insect’s bacterial infected males. This behaviour increases symbionts (likely Wolbachia), rather than both the spread of Wolbachia in the host by the insect itself (Kaiser et al., 2010). The population and the likelihood of males success of Diabrotica virgifera virgifera mating with females of similar infection LeConte (Coleoptera: Chrysomelidae) as a status (De Crespigny et al., 2006). signifi cant pest of maize, Zea mays L. (Poaceae), appears to be at least partially due to its symbionts (likely Wolbachia), 6.4 Manipulating Infections which down-regulate genes in the plant that confer protection against feeding by Successful application of reproductive the insect (Barr et al., 2010). parasites in biological control research Reproductive parasites also can protect requires the ability to manipulate in- their hosts against pathogens and para- fections. This can be achieved by elimin- sitoids. Wolbachia protects D. melano- ating an existing infection, transferring an Chapter 6 47

infection to a novel host, or by genetically Ideally, the symbiont will establish a stable modifying the symbiont. infection in the new host, which then becomes fi xed across gener ations to express the same effect as that observed in 6.4.1 Elimination the original host. Transfection attempts from infected to uninfected populations of Infections can be eliminated by feeding the same host species are most successful; larval or adult stages of the host with but much less so for attempts between antibiotics, e.g. rifampicin, tetracycline, species (but see Xi et al., 2005 and incorporated into the diet. Elimination also Hoffmann et al., 2011). Transfections of can be achieved by rearing the host at Wolbachia to a novel host typically either elevated temperatures lethal to the fail to establish, persist for only a few symbiont. Infections can be cured within generations, or do not express the desired the lifespan of the adult insect (Wade and effect in the novel host (briefl y summarized Stevens, 1985), may require several gener- in Floate et al., 2006). These outcomes may ations (Kyei-Poku et al., 2003), or may be refl ect variation of symbiont densities in intractable to elimination (Giordano et al., the novel host, ineffective maternal 2010). transmission of the symbiont and (or) the Successful elimination of infections effect of the recipient host genetic most often has been reported for prolifi c background on the establishment of the multivoltine species that are easily symbiont in its new environment. maintained in laboratory culture. This Ease of culture can complicate trans- partially explains why such species fection research. Wolbachia only can be dominate in experimental studies on cultured within the cells of its host, symbionts. In a survey of 510 original whereas at least some strains of Arseno- articles reporting on Wolbachia in insects, phonus are readily cultured on agar (Dale the studied taxa most often were the et al., 2006; Taylor et al., 2011). This lower Drosophilidae (25.5%) and Culicidae physiological constraint makes the latter (19.4%) (Diptera) and the Tricho- group more conducive to experimental grammatidae (8.2%) and Pteromalidae manipulations and facilitates successful (5.1%) (Hymenoptera) (Floate et al., 2006). transfers between host species (Duron et It should be noted that treatments can al., 2010). have undesired consequences. The removal of infections can cause sterility in the host (Dedeine et al., 2005; Chen et al., 2012). 6.4.3 Genetic modifi cation Treatments may eliminate non-target bacteria, e.g. nutritional symbionts, patho- Once discussed only in theoretical terms, gens. Use of antibiotics also may reduce genetic modifi cation of symbiotic bacteria mitochondria function and density in the to control arthropod-vectored diseases is a host for one or more generations after reality. The method, termed para trans- treatment cessation (Ballard and Melvin, genesis, involves the transfer of genes 2007). Weeks et al. (2002) review con- (transgenes) into the genome of the siderations for interpreting the results of symbiont, which then excretes molecules experimental studies in an appropriate that interfere with transmission of the context. disease-causing agent. The spread of the transgene into the wild population of the host arthropod relies upon the success of 6.4.2 Transfers the symbiont. Thus, it is important that the transgene does not adversely affect the Transfer of infections to novel hosts (trans- symbiont or its host. fection) has been experimentally achieved Paratransgenesis is being developed to by microinjection, but with mixed results. control diseases affecting humans and 48 Chapter 6

plants. With regards to the former, Hurwitz arthropod while overlooking its microbial et al. (2011) review developments to associates may prevent interpretation of reduce the competency of Rhodnius the host’s biology in an appropriate prolixus Stål (Hemiptera: Reduviidae) as a context. In turn, this may reduce the vector of Trypanosoma cruzii Chagas likelihood of a successful biological control (Trypanosomatida), which is the causative programme. agent of Chagas disease. They also report As a fi rst step, we recommend genetic on developments to reduce the competency screening of arthropod agents and target of the sand fl y, Phlebotomus argentipes species to characterize their respective Annandale & Brunette (Diptera: Psycho- holobionts. Gaskin et al. (2011) make this didae), as a vector for Leishmania same recommendation in their review of donovani Laveran & Mesnil (Trypano- molecular methods for use in classical somatida), which is the causative agent for biological control programmes for weeds. leishmaniasis. Wang et al. (2012) report on Molecular characterization of arthropods is strains of the symbiont Pantoea agglo- common practice to distinguish among merans (Ewing & Fife) Gavini et al. cryptic species or intraspecifi c popu- (Enterobacteriaceae) that have been lations. With growing awareness of genetically modifi ed in the mosquitoes reproductive parasites and their effects on Anopheles gambiae Giles and A. stephensi host biology, screening for specifi c Liston (Diptera: Culicidae), to reduce symbionts is also now relatively common. proliferation of Plasmodium spp. (Plas- However, these latter screens only detect modiidae), the causative agents for malaria. the microorganisms that carry the genetic With regard to plant diseases, Ramirez et marker being targeted. Thus, screens al. (2008) report on use of paratransgenesis specifi c for Wolbachia will not detect co- to control Pierce’s disease, Xylella occurring infections of other bacteria. fastidiosa Wells et al. (Xantho mona- Although limited screens are still valuable, daceae), in grapes, Vitis vinifera L. use of next generation sequencing methods (Vitaceae), whereas Wangkeeree et al. (e.g. pyrosequencing) is expected to (2012) report on use of the method to become the norm in coming years. These control sugarcane whiteleaf disease, Ca. latter methods can be used to fully Phytoplasma oryzae (Acholeplasmataceae). characterize the holobiont, i.e. detecting and quantifying all bacteria taxa associated with the host. Advances in technology will 6.5 Application of Symbionts in continue to reduce the cost of the method, Biological Control which already is proving its value (e.g. Guerrero et al., 2009; Ishak et al., 2011; Recognition that microorganisms are an Hail et al., 2012; Xie et al., 2012). integral component of their host is One benefi t of characterizing the formalized with the terms ‘holobiont’ and genome of an arthropod’s associated ‘hologenome’. The former refers to a plant symbionts is that it may identify genetic or animal and all of its associated markers to track the spread of invasive microorganisms, whereas the latter refers species. For example, infections of to the collective genome of this assemblage maternally inherited bacteria acquired by a (Zilber-Rosenberg and Rosenberg, 2008). host species at one geographic location The concept is not new, but the theoretically may be present in derivative implications of the concept have not been populations that have established in new fully realized by the biological control regions. Floate et al. (2011) tested this community. For example, in a survey of hypothesis by comparing infections of arthropod species of interest to biological Wolbachia among populations of cabbage control programmes in Canada, Floate et seedpod weevil, Ceutorhynchus obstrictus al. (2006) detected infections of Wolbachia (Marsham) (Coleoptera: Curculionidae), in in 46% of 105 taxa. Focusing on the Eurasia versus populations in North Chapter 6 49

America, where the weevil is a relatively not mate to produce female offspring, the recent introduction. All weevils tested effectiveness of biological control pro- carried infections of the same Wolbachia grammes might be improved by rearing strain, which negated use of the symbiont parthenogenic strains. However, this to detected genetic differences among strategy may fail if parthenogenesis geographically separated populations of adversely affects other aspects of parasitoid the host. The apparent universality of biology and behaviour. infection, however, suggests that the Such trade-offs frequently have been Wolbachia infection confers a strong fi tness studied using Trichogramma spp., which advantage to its host. are widely commercialized as inundative Screening also can identify host– biological control agents against lepi dop- symbiont associations that may affect teran pests. About 9% of these species rearing methods for biological control carry infections of PI Wolbachia (Almeida agents. In Trichogramma spp. (Hymen- et al., 2010), which can be cured with use optera: Trichogrammatidae), uninfected of antibiotics. This provides commercial individuals co-exist with individuals of the insectaries with the option of rearing either same species that are infected with strains infected or uninfected strains depending of PI Wolbachia (Schoenmaker et al., upon how infection status affects the 1998). Field collections, therefore, could performance and production of the agent. result in establishment of either partheno- For T. brassicae Bezdenko (Hymenoptera: genic or non-parthenogenic colonies of the Trichogrammatidae), infection does not agent that may differ in their suitability as affect host attack rates, but does increase biological control agents. If parthenogenic host handling time (Farrokhi et al., 2010). strains are desired and bacterial symbionts For T. atopovirilia Oatman and Platner are the cause, then researchers can avoid (Hymenoptera: Trichogrammatidae), infec- use of antibiotics to preserve the desired tion does not affect locomotion, host trait. Such use may explain the absence of handling behaviour, or oviposition rate Wolbachia in a population of the parasitoid (Almeida et al., 2010). For T. cordubensis wasp cameroni Perkins (Hymen- Vargas & Cabello and T. deion Pinto & optera: Pteromalidae). In a survey of this Oatman (Hymenoptera: Trichogrammati- species, infections of Wolbachia were dae), infection reduces oviposition rates detected in 20 of 21 populations from nine (Silva et al., 2000). countries (Kyei-Poku et al., 2006; Floate et The most successful application of al., 2008). The sole exception was a symbionts in biological control reported population maintained by a commercial thus far may be the use of Wolbachia to insectary for sale as a biological control reduce the spread of the virus causing agent of muscoid fl ies (Diptera: Muscidae) dengue fever (Hoffmann et al., 2011; Walker affecting livestock (see Floate et al., et al., 2011), a disease of major health Chapter 25, this volume). This result concern estimated to infect 50+ million arguably could refl ect the loss of people in 100+ countries every year. A Wolbachia in the population due to use of culture of Aedes aegypti (L.) (Diptera: antibiotics by the insectary targeting Culicidae) mosquito cells was initially pathogenic bacteria. transfected with a wMel strain of Wol- Considerable attention has been given to bachia from D. melanogaster. The strain PI strains of Wolbachia for use in was serially passaged in cell culture for inundative biological control programmes. about 2 years to allow the symbiont to Bisexual populations of parasitic wasps adjust to the intracellular environment of mass-reared in commercial insectaries for the new host. The pre-adapted strain was this purpose typically comprise 40–60% of then transferred by microinjection into male individuals. Because males do not embryos of the mosquito to generate contribute to reductions of the target pest, laboratory colonies of the host in which the and because parthenogenic females need strain became fi xed. Subsequent studies on 50 Chapter 6 this new symbiont–host association months, the wMel strain became suc- showed that the Wolbachia strain had cessfully established and reached near- minimal costs to host fi tness, induced a fi xation in natural A. aegypti populations strong CI effect, and had 100% maternal (Hoffmann et al., 2011). Although the effect transmission effi cacy (Walker et al., 2011). of the programme in reducing the incidence Serendipitously, the presence of the of dengue virus remains to be determined, symbiont also caused the complete this research provides an exciting blockage of transmission of the virus illustration on the use of symbionts in causing dengue fever by Wolbachia- biological control programmes. infected mosquitoes. Releases of wMel- With recognition of symbiotic bacteria infected A. aegypti subsequently were as an integral part of agents’ holobionts, made in two communities near the city of continued new and exciting developments Cairns in north-eastern Australia. Results of in biological control research are expected monitoring indicate that within a few in future years.

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7 Acantholyda erythrocephala L., Pine False Webworm (Hymenoptera: Pamphiliidae)

D. Barry Lyons Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario

7.1 Project Status produced sex pheromone (Staples et al., 2009). Lures incorporating the pheromone Pine false webworm, Acantholyda erythro- elicit strong fi eld response to traps in fl ying cephala (L.) (Hymenoptera: Pamphiliidae), males, and these traps may be useful in is an economic problem in Canada in evaluating the effi cacy of biological control white pine, Pinus strobus L. (Pinaceae) programmes. and its pest status was reviewed by Lyons et al. (2002). Subsequent to the last review, the history of an outbreak in New York was 7.1.1 Parasitoids documented (Asaro and Allen, 2001), and the impact of the sawfl y on white pine Puparia of M. hertingi were exported from stands in New York has been quantifi ed Italy by staff of CABI Europe to the Great (Mayfi eld et al., 2005). After 5 years of Lakes Forestry Centre, Canadian Forest moderate to severe defoliation annual Service, Natural Resources Canada from volume increment was reduced by 97%. 2000 to 2004 for fi eld release in Ontario. In Recent analysis of population data for pine each year, adults were reared from puparia false webworm in New York State sug- to eliminate the chance of releasing gested that population numbers are hyperparasitoids. A hyperparasitoid, Tri- positively correlated with stand size and chopria sp. (Hymenoptera: Diapriidae), has defoliation increases with sandier soils been reported to kill up to 20% of the (Mayfi eld et al., 2007). puparia (Kenis and Kloosterman, 2001). In Biological control activities against A. each year from 2000 to 2002, fl ies were erythrocephala were reviewed for the released into two 3.0 m high by 1.8 m period up to and including 2000 by Lyons square cages enclosing individual A. et al. (2002). Introduction of the parasitoid erythrocephala-infested red pine, Pinus Myxexoristops hertingi Mesnil (Diptera: resinosa Ait. (Pinaceae), trees in a plant- Tachinidae) into Ontario was initiated ation near Apto, Ontario (44.53°, −79.78°). during that period and releases were Twenty-fi ve males and 95 females were continued during the current review released in 2000, 64 males and 12 females period. A baculovirus project was initiated were released in 2001, and 6 males and 36 after the previous review period. females were released into cages in 2002. A signifi cant recent achievement in the In the autumn following the releases, the pest management of the pine false web- soil in the cages under the trees was worm was the identifi cation of a female- excavated and all larvae recovered were

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 7 55

reared for parasitism. However, no dose of NeabNPV, lack of replication of the parasitoids were recovered. Open releases virus in the sawfl y, and the cryptic feeding of M. hertingi were also made in each year behaviour of the larvae in webs. In 2003, from 2002 to 2004 in P. resinosa plantation NeabNPV was aerially applied to near Craighurst, Ontario (44.51°, −79.71°). plantation-grown pines using a fi xed-wing A total of 334 males and 187 females, 719 aircraft. Results were inconclusive because males and 210 females, and 405 males and populations of the sawfl y had been in- 328 females were released into the wild in creasing in some treatment plots and 2002, 2003 and 2004, respectively. declining in other treatment plots in Populations of A. erythrocephala collapsed previous years, making assessment diffi - shortly after the fi eld releases and cult. As part of a larger study on the consequently the possibility of establish- potential for biological control of pine false ment of the parasitoid was diffi cult to webworm using pathogens, bacterial assess. communities associated with the sawfl y have been characterized using polymerase chain reaction amplifi cation of 16S rDNA 7.1.2 Pathogens and denaturing gradient gel electrophoretic techniques (Zahner et al., 2008). Investigations were undertaken by the Canadian Forest Service to examine the potential for the biological control of the 7.2 Future Needs pine false webworm using the baculovirus Neodiprion abietis nucleopolyhedrovirus Future work should include: (Baculoviridae) (NeabNPV) isolated from the balsam fi r sawfl y Neodiprion abietis 1. Evaluation of the establishment and (Harris) (Hymenoptera: Diprionidae) from impact of M. hertingi on the host popu- Newfoundland (Moreau and Lucarotti, lation at release sites in Ontario. This has 2007). Ingestion of droplets containing a never been assessed due to low numbers of dose of 1×106 occlusion bodies (OBs) of host insects in the area of the release. NeabNPV by 3rd instar larvae of the pine false webworm reduced survival to the ultimate instar by 51%. These results Acknowledgements prompted fi eld trials of the effi cacy of NeabNPV against pine false webworm I thank M. Kenis, of CAB International, infesting P. resinosa plantations in Ontario Delémont, Switzerland, and R. Bourchier, in 2002 and 2003. Mistblower applications Agriculture and Agri-Food Canada, of NeabNPV to individual trees at rates as Lethbridge, Alberta for their signifi cant high as 1×109 OBs ha−1 reduced larval contributions to the research on M. survival by an average of 57% but did not hertingi, and to G. Jones for her dedication result in signifi cant foliage protection. This and diligence in undertaking the fi eld poor result was attributed to an insuffi cient release of the parasitoid.

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Asaro, C. and Allen, D.C. (2001) History of a pine false webworm (Hymenoptera: Pamphiliidae) outbreak in northern New York. Canadian Journal of Forest Research 31, 181–185. Kenis, M. and Kloosterman, K. (2001) European parasitoids of the pine false webworm (Acantholyda erythrocephala [L.]) and their potential for biological control in North America. In: Liebhold, A.M., McManus, M.L., Otvos, I.S. and Fosbroke, S.L.C. (eds) Proceedings: integrated management and dynamics of forest defoliating insects, 15–19 August 1999, Victoria, British 56 Chapter 8

Columbia, General Technical Report NE-277. US Department of Agriculture, Forest Service, Northeastern Research Station, Newtown Square, Pennsylvania, pp. 65–73. Lyons, D.B., Kenis, M. and Bourchier, R.S. (2002) Acantholyda erythrocephala (L.), pine false webworm (Hymenoptera: Pamphiliidae). In: Mason, P. and Huber, J. (eds) Biological Control Programmes against Insects and Weeds in Canada 1981-2000. CAB International, New York, pp. 22–28. Mayfi eld III, A.E., Allen, D.C. and Briggs, R.D. (2005) Radial growth impact of pine false webworm defoliation on eastern white pine. Canadian Journal of Forest Research 35, 1071–1086. Mayfi eld III, A.E., Allen, D.C. and Briggs, R.D. (2007) Site and stand conditions associated with pine false webworm populations and damage in mature eastern white pine plantations. Northern Journal of Applied Forestry 24, 168–176. Moreau, G. and Lucarotti, C.J. (2007) A brief review of the past use of baculoviruses for the management of eruptive forest defoliators and recent developments on a sawfl y virus in Canada. The Forestry Chronicle 83, 105–112. Staples, J.K., Bartelt, R.J. and Cossé, A.A. (2009) Sex pheromone of the pine false webworm Acantholyda erythrocephala. Journal of Chemical Ecology 35, 1448–1460. Zahner, V., Lucarotti, C.J. and McIntosh, D. (2008) Application of 16S rDNA-DGGE and plate culture to characterization of bacterial communities associated with the sawfl y, Acantholyda erythrocephala (Hymenoptera, Pamphiliidae). Current Microbiology 57, 564–569.

8 Acrolepiopsis assectella (Zeller), Leek Moth (Lepidoptera: Acrolepiidae)

Peter G. Mason,1 Wade H. Jenner,2,3 Andrea Brauner1, Ulrich Kuhlmann2 and Naomi Cappuccino3 1Agriculture and Agri-Food Canada, Ottawa, Ontario; 2CABI, Delémont, Switzerland; 3Carleton University, Ottawa, Ontario

8.1 Pest Status Prince Edward Island and is predicted to establish widely in eastern North America Leek moth, Acrolepiopsis assectella (Mason et al., 2011). Cultivated (Zeller) (Lepidoptera: Acrolepiidae), native spp., particularly , A. sativum L., to Europe, is an invasive alien pest of leek, A. porrum L. and , A. cepa L., Allium spp. (Amaryllidaceae) in North are the preferred hosts. However, nodding America. First reported in the Ottawa area onion, A. cernuum Roth, and prairie onion, in 1993 (Landry, 2007), A. assectella has A. stellatum Nutt. ex Ker Gawl., native to since spread throughout eastern Ontario North America, can support development and southern Quebec, is found in upper of A. assectella (Allison et al., 2007) and New York State, New Brunswick and are therefore potentially at risk of attack

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 8 57

from this pest. Damage is caused by the approach such as organic growers face larval stages, which feed on the aerial greater challenges. Biologically based growing tissues (Noyes, 1974). In eastern insecticides such as Bacillus thuringiensis Canada, damage is most severe in organic Berliner (Bacillaceae) and Spinosad® are production systems. In garlic, the scapes lethal to leek moth larvae (Mason et al., are destroyed early in the season and the 2006a; Allen et al., 2007; Allen and bulbs can be destroyed after harvest when Appleby, 2008), although to be effective, the crop is hung and larvae move down the they must be applied when 1st instar leek plant as it dries. Damage to can be so moth are present on plant surfaces. Float- severe that plants are unmarketable and ing row covers provide the best protection, entire crops destroyed. particularly in organic production systems, Adult A. assectella overwinter and by preventing leek moth from ovipositing become active in spring when temperatures on the crop (Mason et al., 2006b). rise above 15°C (Abo-Ghalia and Thibout, Pino and Morton (2008) investigated the 1983). Females lay eggs singly on the leaf use of Steinernema feltiae (Filipjev) surfaces, and each female lays an average (Rhabditida: Steinernematidae) against A. of 100 eggs in fi eld conditions. Soon after assectella in leeks. They observed larval hatching, 1st instar larvae mine into the mortalities of 71.1–87.7% in experimental leaf tissue where they feed, completing 5 fi eld plots and concluded that S. feltiae instars. Mature larvae exit from the inner was effective because of the moist micro- plant tissues, spin a loosely woven cocoon habitat provided by the overlapping plant on external surfaces and develop through leaves and the tunnelling habit of A. prepupal and pupal stages. Adults emerge, assectella larvae. and, depending on the time of year, In the area of origin in Europe, a number produce a new generation or enter repro- of parasitoids are reported in the literature ductive diapause to overwinter. Repro- to attack A. assectella (Table 8.1). The ductive diapause (Thibout, 1981) is complex varies from generation to gener- induced when developing larvae are ation (Plaskota and Dabrowski, 1986) and exposed to daylengths shorter than 15 h many of the species have a broad host (Abo-Ghalia and Thibout, 1982). In eastern range (Jenner and Kuhlmann, 2004). Canada, development above a threshold of Although several predators have been 7°C takes 441.7 degree-days (DD) from egg reported, no comprehensive studies have to adult (Mason et al., 2010), similar to been conducted to provide information on requirements (450 DD above 6°C) in central incidence and impact. Europe (Bouchet, 1973) but signifi cantly Jenner (2008) studied A. assectella less than the 630 DD above 6°C required in populations in Switzerland. Four Hymen- (Åsman, 2001). In eastern Ontario, optera species were reared from A. three generations can occur, marked by assectella larval hosts: two Ichneu monidae, fl ight periods in early spring, mid- to late- Diadegma chrysostictos (Gmelin) and D. June and mid-July (Mason et al., 2010). A fenestrale Holmgren; and two Eulophidae, fourth generation is probable in south- Pnigalio soemius (Walker) and P. pectini- western Ontario (Mason et al., 2011) where cornis (L.). Acrolepiopsis assectella pupae A. assectella will likely invade. were parasitized by two Ichneumonidae: Diadromus pulchellus Wesmael and maculator (Fabricius). Among 8.2 Background these, D. pulchellus was the only species that appeared to be host-specifi c. There are Chemical insecticides such as Matador®/ no known records of this parasitoid emerg- Warrior® may provide some protection ing from hosts other than A. assectella in against A. assectella (Allen et al., 2007; the fi eld, whereas the other fi ve species Allen and Appleby, 2008). However, those have been associated with between 29 and using a reduced risk pest management 124 host species (Yu et al., 2009). 58 Chapter 8

Table 8.1. Parasitoids associated with Acrolepiopsis assectella in the European literature.

Host stage European countriesa where Parasitoid species attacked found Reference Hymenoptera: Braconidae Apanteles impurus (Nees) ? AT, BE, BG, CZ, FR, DE, HU, Plaskota and Dabrowski IE, IT, LV, LT, MN, PL, RU, (1986); Yu et al. (2009) SE, CH, GB Aphaereta brevis Tobias ? BG, CZ, HU, RU, ES, RSPL Plaskota and Dabrowski (1986); Jenner and Kuhlmann (2004); Yu et al. (2009) Microchelonus blackburni larva ? Jenner and Kuhlmann (2004); (Cameron) Yu et al. (2009) Microgaster globata (L.) larva AL, AM, AT, AZ, BE, BG, CZ, Jenner and Kuhlmann (2004); FI, FR, GE, DE, GR, HU, IE, Yu et al. (2009) IT, KZ, LV, LT, MD, MN, NL, NO, PL, RO, RU, SK, SI, ES, SE, CH, TR, TM, UA, GB, RS Microgaster hospes Marshallb larva BG, CZ, FI, GE, DE, HU, IE, IT, Plaskota and Dabrowski LT, MD, MN, NL, PL, RU, (1986); Jenner and SK, CH, TR Kuhlmann (2004); Yu et al. (2009) Hymenoptera: Ichneumonidae Campoletis annulata ? AT, BE, BG, CZ, DK, FI, FR, DE, Yu et al. (2009) (Gravenhorst) HU, IE, IL, IT, LV, NL, PL, RO, RU, ES, SE, GB Diadegma fenestrale larva AT, AZ, BE, BG, CZ, DK, FI, FR, Plaskota and Dabrowski (Holmgren) DE, HU, IS, IE, IT, KZ, LV, LT, (1986); Jenner and MD, NL, NO, PL, PT, RO, Kuhlmann (2004) ; Yu et al. RU, ES, SE, CH, TR, TM, UA, (2009) GB, RS Diadromus collaris pupa AT, AZ, BE, BG, CZ, FR, DE, Jenner and Kuhlmann (2004); (Gravenhorst) GR, IT, MD, NL, PL, PT, RO, Yu et al. (2009) ES, SE, TR, TM, UA, GB, RS Diadromus pulchellus pupa BE, FI, DE, FR, PL, SE, GB Jenner and Kuhlmann (2004); Wesmael Yu et al. (2009) Diadromus varicolor ? AT, AZ, BE, BG, FI, FR, DE, HU, Jenner and Kuhlmann (2004); Wesmael NL, RO, RU, ES, SE, CH, GB Yu et al. (2009) Endromopoda nigricoxis ? PL Plaskota and Dabrowski (Ulbricht) (1986) Itoplectis europeator Aubert larva FR, HU, RO, CH, TR Yu et al. (2009) Itoplectis tunetana pupa AM, AT, AZ, BG, FR, GR, HU, Jenner and Kuhlmann (2004); (Schmiedeknecht) IT, KZ, KG, MK, MD, MN, Yu et al. (2009) PL, RO, RU, ES, CH, TR, TM, UA, UZ, RS, ME Tycherus impiger (Wesmael) pupa AT, BE, BG, CZ, FI, FR, DE, Plaskota and Dabrowski HU, IT, LI, NL, NO, PL, RO, (1986); Jenner and RU, SE, GB Kuhlmann (2004) Zaglyptus varipes larva AT, AZ, BY, CZ, DE, FI, FR, DE, Jenner and Kuhlmann (2004); (Gravenhorst)c HU, IT, LV, LT, MD, NL, NO, Yu et al. (2009) PL, RO, RU, ES, SE, TR, GB aISO 3166-1 Encoding list of countries (http://www.iso.org/iso/iso-3166-1_decoding_table); balso in USA; calso in Canada, USA; ?, no data available. Chapter 8 59

Furthermore, D. pulchellus was the most (2008) and Jenner et al. (2012) conducted abundant parasitoid on A. assectella, it was host specifi city testing and showed that in the only species found attacking A. the laboratory D. pulchellus would suc- assectella in all three generations and it cessfully develop in non-target species that was the sole species obtained from A. were taxonomically closely related to A. assectella in the fi nal generation. assectella. Experimental fi eld releases in In Canada, only a few individuals of the the area of origin demonstrated that in the following parasitoid species, Itoplectis wild D. pulchellus only attacked the target, conquisitor (Say), Scambus pterophori A. assectella (Jenner, 2008). This fi nding (Ashmead), Scambus hispae (Harris) confi rmed earlier work by Thibout (1988) (Hymenoptera: Ichneumonidae), Bracon and others that complex chemical cues are furtivus Fyles (Hymenoptera: Braconidae) involved in host location and acceptance. and Conura albifrons (Walsh) (Hymen- Thus, D. pulchellus can be considered to optera: Chalcididae) have been reared from be host specifi c. A. assectella (Mason et al., 2010). Among Jenner et al. (2010b) assessed the effi cacy these C. albifrons is the most common. of D. pulchellus in fi eld trials in its native According to Yu et al. (2009), C. albifrons range in central Europe by simulating is an endoparasitoid/facultative hyper- introductory releases. In a 2-year study, parasitoid with a very broad host range in experimental leek plots were artifi cially several insect orders; B. furtivus is an infested with A. assectella larvae to mimic ectoparasitoid of Gelechiidae and Noctui- the higher pest densities common in dae; I. conquisitor is a prepupal-pupal Canada. Diadromus pulchellus adults were parasitoid of Lepidoptera, Coleoptera and mass-released into the fi eld plots when the Hymenoptera (171 recorded hosts); S. fi rst A. assectella cocoons were observed. pterophori is a larval parasitoid of Lepi- The laboratory-reared agents reproduced doptera and Coleoptera; and S. hispae is a successfully in all trials and signifi cantly larval, prepupal/pupal endo- or ecto- reduced A. assectella survival. Accounting parasitoid of Lepidoptera and Coleoptera for background parasitism by naturally (103 recorded hosts). occurring D. pulchellus, the released individuals parasitized at least 15.8%, 43.9%, 48.1% and 58.8% of the available 8.3 Biological Control Agents hosts in the four release trials, respectively. When this signifi cant mortality is combined 8.3.1 Pathogens with other mortality factors reported by Jenner et al. (2010a), the total pupal Bacillus thuringiensis Berliner serovar. mortality increased from 60.1% to 76.7%. kurstaki (Btk) was lethal to A. assectella in Jenner et al. (2010c) conducted labora- laboratory bioassays, however, fi eld trials tory and fi eld experiments on the over- have shown no signifi cant differences in A. wintering capacity of immature and mature assectella larval numbers between Btk D. pulchellus. They concluded that D. treated plants and untreated plants (Mason pulchellus overwinters primarily, if not et al., 2006a). Since larvae must consume a exclusively, in the adult stage. Results lethal dose, their habit of boring into plant indicated that among adults, females tissues in the 1st larval instar likely protects demon strated greater cold hardiness than them from surface application of Btk. males. Their results suggested that D. pul- chellus should survive winters in the tar- geted release areas of Ontario and Quebec. 8.3.2 Parasitoids A petition for release of D. pulchellus in Canada (Mason et al., 2009) was approved Diadromus pulchellus is the only natural and releases were made in 2010, 2011 and enemy so far investigated as a potential 2012 (Table 8.2). Progeny of D. pulchellus classical biological control agent. Jenner collected from the Seeland region of west- 60 Chapter 8

Table 8.2. Releases and recoveries of Diadromus pulchellus in Ontario during 2010–2012. Location Geographic coordinates Release date Number Recoveries and notes Ottawa 45.3886°, −75.7127° June 2010 648Ƃ, 185ƃ 18 D. pulchellus recovered from sentinel A. assectella in 2010; 1 D. pulchellus recovered from wild A. assectella in 2011 (year after release) June 2012 171Ƃ, 138ƃ July 2012 144Ƃ, 126ƃ August 2012 607Ƃ 641ƃ no recoveries to date Union Hall 45.1441°, −76.2936° September 2010 254Ƃ, 250ƃ no recoveries July 2012 22Ƃ, 131ƃ no recoveries to date August 2012 250Ƃ, 279ƃ Arklan 45.0845°, −76.3407° June 2011 573Ƃ, 478ƃ 5 D. pulchellus recovered from July 2011 287Ƃ, 165ƃ sentinel A. assectella in 2011; 3 D. pulchellus recovered from sentinel A. assectella in 2012 (year after release) June 2012 331Ƃ, 259ƃ 5 D. pulchellus recovered from July 2012 280Ƃ, 212ƃ sentinel A. assectella in year of August 2012 531Ƃ, 586ƃ release Lloyd 45.1438°, −76.3193° July 2011 202Ƃ, 45ƃ no recoveries June 2012 100Ƃ, 53ƃ no recoveries to date July 2012 40Ƃ, 33ƃ August 2012 76Ƃ, 73ƃ central Switzerland (46.9883°, 7.1222°) and 3. Development of a molecular toolkit to Delémont, Switzerland (47.3564°, 7.3267°) identify and quantify parasitism by D. pul- were the source of individuals released. chellus in fi eld samples; 4. Continued monitoring of non-target spe- cies, such as Plutella xylostella (L.) 8.4 Evaluation of Biological Control (Lepidoptera: Plutellidae), to validate host specifi city predictions and impact on local It is too soon to determine if D. pulchellus biodiversity; has established. Recovery of individuals 5. Assess additional parasitoids, e.g. the from sentinel A. assectella pupae during larval parasitoids Aphaereta brevis Tobias the years of release indicates that D. (Hymenoptera: Braconidae) and Diadegma pulchellus females are fi nding and fenestrale (Holmgren) (Hymenoptera: ovipositing in hosts in the fi eld. The Ichneu monidae), and the pupal parasitoids recoveries in the years following release Diadromus collaris (Gravenhorst), Dia- confi rms that adult D. pulchellus can dromus varicolor Wesmael, Dolichogenidea survive winter conditions. impura (Nees) and Phaeogenes impiger Wesmael (Hymenoptera: Ichneumonidae); 8.5 Future Needs 6. Evaluation of nematodes for inundative biological control of A. assectella. Further work should include: 1. Additional releases of D. pulchellus to Acknowledgements ensure that a population establishes; 2. Developing methods for mass produc- Ana Maria Farmakis, Louis Gagnon, tion of D. pulchellus to provide the needed Llewellyn Haines, Melanie Lacroix, Jake numbers for rapid establishment and dis- Miall, Kathryn Makela, Tom Parlee, Warren persal; Pringle, Michael Sarazin and Michael Chapter 8 61

Wogin provided technical assistance. Jack Bennett (Ichneumonidae), Henri Goulet Hinton, Glennis Harwig, Mike Gillespie, (Braconidae) and Gary Gibson (Chalci- Jack Fraser, Ron Farmer, John Moore, didae). The Agriculture and Agri-Food David and Inez McCreery and Dave Cornell Canada, Improving Farming Systems and are gratefully acknowledged for their Practices Initiative grant MU03-Ent2 and collaboration and on-site guidance about the Pesticide Risk Reduction Programme the leek moth in their crops. Expert grants PRR03-360 and PRR10-030 provided identifi cations were provided by Drs Andy funding.

References

Abo-Ghalia, A. and Thibout, E. (1982) Fréquence de la diapause reproductrice en fonction de l’évolution de la photopériode à températures constantes et recherche du stade sensible chez une souche d’Acrolepiopsis assectella (Lepidoptera, Hyponomeutoidea). Annales de la Société Entomologique de 18, 173–179. Abo-Ghalia, A. and Thibout, E. (1983) Levée de la diapause imaginale et reprise de l’activité sexuelle chez la teigne du poireau (Acrolepiopsis assectella) Zell. (Lepidoptera). Agronomie 3, 717–722. Allen, J.K. and Appleby, M. (2008) Evaluation of organic and conventional insecticides for control of leek moth on garlic and onion, 2007. Pest Management Research Report 46, 92–94. Allen, J.K., Appleby, M. and Mason, P. (2007) Evaluation of organic and conventional insecticides for control of leek moth on garlic and onion, 2006. Pest Management Research Report 45, 56–59. Allison, J., Jenner, W., Cappuccino, N. and Mason, P.G. (2007) Oviposition and feeding preference of Acrolepiopsis assectella Zell. (Lepidoptera: Acrolepiidae). Journal of Applied Entomology 131, 690–697. Åsman, K. (2001) Effect of temperature on development and activity periods of the leek moth Acrolepiopsis assectella Zell. (Lep., Acrolepiidae). Journal of Applied Entomology 125, 361–364. Bouchet, J. (1973) La prevision des attaques de la teigne du poireau a la station d’avertissements agricoles des pays de la Loire. Phytoma-Défense des Cultures 25, 24–28. Jenner, W.H. (2008) Evaluation of a candidate classical biological control agent and critical assess- ment of suggested host specifi city testing guidelines. PhD thesis, Carleton University, Ottawa. Jenner, W. and Kuhlmann, U. (2004) Biological control of leek moth, Acrolepiopsis assectella. Annual Report 2004/2005, Unpublished Report, CABI Bioscience Switzerland Centre, Delémont, Switzerland. Jenner, W.H., Kuhlmann, U., Mason, P.G. and Cappuccino, N. (2010a) Comparative life tables of leek moth, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in its native range. Bulletin of Entomological Research 100, 87–97. Jenner, W.H., Mason, P.G., Cappuccino, N. and Kuhlmann, U. (2010b) Native range assessment of classical biological control agents: impact of inundative releases as pre-introduction evaluation. Bulletin of Entomological Research 100, 387–394. Jenner, W.H., Kuhlmann, U., Cappuccino, N. and Mason, P.G. (2010c) Pre-release analysis of the overwintering capacity of a classical biological control agent supporting prediction of establishment. BioControl 55, 351–362. Jenner, W.H., Cappuccino, N., Kuhlmann, U. and Mason, P.G. (2012) Manipulation of parasitoid state infl uences host exploitation by Diadromus pulchellus Wesmael (Hymenoptera: Ichneumonidae). Biological Control 63, 264–269. Landry, J.-F. (2007) Taxonomic review of the leek moth genus Acrolepiopsis (Lepidoptera: Acrolepiidae) in North America. The Canadian Entomologist 139, 319–353. Mason, P.G., Appleby, M., Callow, K. and Allen, J. (2006a) Effects of Bacillus thuringiensis and Spinosad on leek moth in garlic and onion. Pest Management Research Report 44, 32–40. Mason, P.G., Appleby, M., Callow, K., Allen, J., Fraser, H. and Landry, J.-F. (2006b) Leek Moth Acrolepiopsis assectella (Lepidoptera: Acrolepiidae) a Pest of Allium spp.: Biology and Minor Use Insecticide Registration. Final Project Report to ‘Improving Farming Systems Program’, AAFC Pest Management Centre (15 May 2006). 62 Chapter 9

Mason, P.G., Jenner, W.H., Landry, J.-F., Cappuccino, N. and Kuhlmann, U. (2009) Petition to introduce Diadromus pulchellus Wesmael (Hymenoptera: Ichneumonidae) as a classical biological control agent for leek moth, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in Canada. Submission to the Canadian Food Inspection Agency, 21 May 2009. Mason, P.G., Appleby, M., Juneja, S., Allen, J. and Landry, J.-F. (2010) Biology and development of Acrolepiopsis assectella (Lepidoptera: Acrolepiidae) in eastern Ontario. The Canadian Entomologist 142, 393–404. Mason, P.G., Weiss, R.M., Olfert, O. and Landry, J.-F. (2011) Actual and potential distribution of an invasive alien Allium spp. pest, Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), in Canada. The Canadian Entomologist 143, 185–196. Noyes, J.S. (1974) The biology of the leek moth. Acrolepia assectella (Zeller). PhD thesis, University of London, UK. Pino, F.G. del, and Morton, A. (2008) Effi cacy of Steinernema feltiae against leek moth Acrolepiopsis assectella in laboratory and fi eld conditions. BioControl 53, 643–650. Plaskota, E. and Dabrowski, Z.T. (1986) Biological principles of leek moth (Acrolepia assectella Zellar, Lepidoptera: Plutellidae) control. II. Biology. Annals of the Warsaw Agricultural University 13, 35–46. Thibout, E. (1981) Observations préliminaires et caractérisation de la diapause reproductrice chez la teigne du poireau, Acrolepiopsis assectella Zell, (Lepidoptera, Hyponomeutoidea). Acta Œcologica/Œcologia Generalis 2, 171–182. Thibout, E. (1988) La spécifi cité de Diadromus pulchellus [Hyménoptère: Ichneumonidae] vis-à-vis de son hôte Acrolepiopsis assectella, la teigne du poireau. Entomophaga 33, 439–452. Yu, D.S., van Achterberg, C. and Horstmann, K. (2009) Taxapad: Scientifi c names for information management. Available at: http://www.taxapad.com/taxapadmain.php (accessed 22 December 2011).

9 Agrilus planipennis Fairmaire, Emerald Ash Borer (Coleoptera: Buprestidae)

D. Barry Lyons Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario

9.1 Pest Status It probably entered North America in wood-packaging material in a shipping The emerald ash borer, Agrilus planipennis container, probably in the early 1990s Fairmaire (Coleoptera: Buprestidae), is an (Cappaert et al., 2005). As of October 2012, Asian species, fi rst discovered in North A. planipennis has been detected in 18 America in 2002 around Detroit, Michigan states in the USA (Connecticut, Illinois, and Windsor, Ontario (Haack et al., 2002). Indiana, Iowa, Kansas, Kentucky, Maryland, © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 9 63

Massachu setts, Michigan, Minnesota, of potentially infested material, and tree Missouri, New York, Ohio, Pennsylvania, removal with the subsequent destruction of Tennessee, Virginia, West Virginia and infested material by chipping, burning and Wisconsin) and two Canadian provinces deep burial. The management paradigm (Ontario and Quebec). shifted to ‘slow-the-spread’ when the scope Since its arrival in North America, A. of the infestation expanded to a degree that planipennis has killed tens of millions of its eradication was no longer feasible. Current ash tree, Fraxinus spp. (Oleaceae), hosts strategies include detection and delinea- (Duan et al., 2012a). The major impact of A. tion of infested trees, regulatory measures, planipennis has been in urban areas. The e.g. quarantines, and public education, estimated discounted cost of treatment, e.g. ‘Don’t Move Firewood’ campaign. removal and replacement in urban and Additional tools include sanitation (tree semi-urban settings in Canada and the USA removal and destruction) and systemic amounts to many billions of dollars (Kovacs insecticides. Although there are many et al., 2010; Sydnor et al., 2011; McKenney insecticides registered for use against A. et al., 2012). This pertains to street and planipennis in the USA (Herms et al., 2009), back-yard trees and does not include costs only ACECAP® 97 Systemic Insecticide associated with managing trees in parks and Implants, Confi dor® 240 SL Systemic woodlots within municipal boundaries or Insecticide and TreeAzin™ Systemic Insecti- the impact of A. planipennis on ecological cide are registered for use in Canada (Health services such as biogeochemical and water Canada, 2012). To date, TreeAzin only has cycling (Fissore et al., 2012). Loss of ash an emergency registration for use against A. trees would also increase heating and planipennis. Biological controls might cooling costs, reduce property values and provide a sus tainable alternative for long- impact wildlife habitat (Sydnor et al., 2011). term management of A. planipennis in In natural forests and plantations, A. North America. planipennis would also impact the wood Apart from native parasitoids and supply and the hardwood lumber industry. pathogens (see below), other North Ameri- For example, in 2005, ash lumber exports can organisms have made a limited from Canada to the USA amounted to 5937 transition to preying on A. planipennis m3 with a value of US$1.74m not including populations. A few predatory beetles, ash wood chips (Federal Register, 2007). Enoclerus sp. (Coleoptera: Cleridae), Cato- Host plants for A. planipennis probably genus rufus (F.) (Coleoptera: Passandridae) include all 20 species of ash that occur in and Tenebriodes sp. (Coleoptera: Trogos- North America (Wallander 2008). In eastern sitidae), feed on A. planipennis under the Canada, native ash attacked include green bark of host trees (Liu et al., 2003). ash, Fraxinus pennsylvanica Marsh., white Woodpecker predation is probably the ash, F. americana L., black ash, F. nigra most important source of mortality in A. Marsh., blue ash, F. quadrangulata Michx. planipennis populations in Michigan and and pumpkin ash, F. profunda (Bush) Bush has accounted for 9–95% mortality (Oleaceae). Oregon ash, F. latifolia Benth. (Cappaert et al., 2005; Duan et al., 2010). (Oleaceae), occurs in British Columbia Lindell et al. (2008) have observed hairy, (Farrar, 1995). Exotic ash trees planted in Picoides villosus (L.), downy, Picoides Canada, such as European ash, F. excelsior pubescens (L.), and red-bellied, Mela- L. (Oleaceae), have also been attacked. nerpes carolinus (L.) woodpeckers (Pici- formes: Picidae) preying on A. planipennis and recommended the maintenance of 9.2 Background conditions, e.g. nest sites, that attract wood peckers. Ironically, woodpeckers When A. planipennis was fi rst detected in have little impact on A. planipennis popu- Canada, regulators attempted to eradicate lations in Asia (Duan et al., 2012c). The the species using restrictions on movement predatory wasp, Cerceris fumipennis Say 64 Chapter 9

(Hymenoptera: Crabronidae), collects A. density and tracking its dispersal (Cossé et planipennis adults to provision its nest al., 2012). The parasitoid can only be (Careless et al., 2009). Although the impact reared on natural host larvae or host larvae of the wasp on A. planipennis populations implanted under the bark in branch is not signifi cant, C. fumipennis may be a segments (Gould et al., 2011b). There is no useful biosurveillance tool for detecting obligatory diapause in S. agrili, so low density A. planipennis populations parasitoids can be reared year round (Marshall et al., 2005; Careless et al., 2009). (Gould et al., 2011b). In China, S. agrili Two strategies for biological control of appears to be an obligatory parasitoid of A. A. planipennis are being explored. Foreign planipennis (Yang et al., 2005). In host exploration has been conducted by the specifi city tests conducted in China and United States Department of Agriculture the USA, only Agrilus spp. were attacked (USDA) and their collaborators in China, and at a much lower rate than A. Korea, Taiwan, Japan and the Russian Far planipennis (Bauer et al., 2007). East for potential classical biological con- Tetrastichus planipennisi Yang (Hymen- trol agents for A. planipennis since 2003 optera: Eulophidae) was discovered (Liu et al., 2003; Duan et al., 2012c). parasitizing A. planipennis larvae in Jilin Natural enemies of Agrilus spp. related to and Liaoning provinces, China (Liu et al., the pest or parasitoids attacking popu- 2003; Yang et al., 2006). Tetrastichus lations of A. planipennis in North America planipennisi is a gregarious endoparasite are also being sought for augmentative/ that can parasitize 32–65% of A. inundative biological control (Cappaert planipennis in populations in north- and McCullough, 2009; Duan et al., 2009; eastern China. It is a koinobiont and 5–122 Kula et al., 2010; Lyons, 2010; Johny et al., (average 35) individuals may develop per 2012a, b). If suitable, these natural enemies host (Yang et al., 2006; Liu and Bauer, could then be mass reared/cultured and 2007). Both 3rd and 4th instar hosts are released into A. planipennis populations. attacked (Liu and Bauer, 2007). In laboratory tests, T. planipennisi attacked hosts in 2nd larval instar to prepupae, but 9.3 Biological Control Agents did not attack pupae, presumably because they do not make detectable vibrational 9.3.1 Exotic parasitoids cues (Ulyshen et al., 2010b, 2011). In no- choice host range tests, adults of T. Three species of hymenopterous para- planipennisi were exposed to feeding sitoids of A. planipennis, two larval larvae of a variety of forest and factitious parasitoids and one egg parasitoid, were hosts, implanted in small branches and discovered in China. Spathius agrili Yang twigs of their host plants, and rejected all et al. (Hymenoptera: Braconidae) (Yang et larvae except A. planipennis (Liu and al., 2005) is a gregarious ectoparasitoid. Bauer, 2007). Tetrastichus planipennisi This idiobiont has up to four generations a females do not attack A. planipennis larvae year with observed parasitism rates ranging that have been previously attacked by S. from 30 to 90% (Yang et al., 2005). agrili, but S. agrili adults will attack A. Spathius agrili overwinters as prepupae, planipennis larvae parasitized by T. pupates in spring and emerges when host planipennisi (Ulyshen et al., 2010a). Both larvae are feeding in their galleries (Yang et species only attack actively feeding larvae al., 2005). Host volatiles increase fecundity (Ulyshen et al., 2011), thus the idiobiont S. in S. agrili (Gould et al., 2011b) and a agrili paralyses its host and renders it male-produced pheromone blend, that is unacceptable for attack by T. planipennisi. attractive to both sexes, has been identifi ed In contrast, T. planipennisi does not and synthesized, and will be useful for paralyse its host, which remains suitable confi rming establishment of the biological for attack by S. agrili (Ulyshen et al., control agent, assessing its population 2010a). Consequently, separate release sites Chapter 9 65

for the two parasitoids are recommended by the United States Department of (Ulyshen et al., 2010a). Agriculture (Gould et al., 2012). The solitary egg parasitoid, Oobius agrili In Canada, no exotic parasitoids have Zhang and Huang (Hymenoptera: Encyrti- been approved for release. Petitions are in dae) (Zhang et al., 2005), was discovered preparation for the importation and sub- parasitizing A. planipennis in Jilin sequent release of S. agrili, T. planipennisi province, China in 2004 (Bauer et al., and O. agrili in Ontario. 2007). In China, parasitism peaked at Additional exotic parasitoids that might 61.5% in August (Bauer and Liu, 2007; Liu be candidates for introduction into North et al., 2007). Oobius agrili is a thelytokous America include the egg parasitoid, Oobius parthenogenetic idiobiont, has a female- zahaikevitshii Trjpitzin (Hymenoptera: biased sex ratio of 14.5:1, and is at least Encyrtidae) from (Taylor et al., bivoltine in China (Bauer and Liu, 2007; 2012), the potentially cold-hardy Spathius Bauer et al., 2008). The absence of egg galinae Belokobylskij and Strazanac parasitoids attacking A. planipennis in (Hymen optera: Braconidae), from Russia North America suggests that the intro- and Korea and the newly associated duction of O. agrili will not result in Atanycolus nigriventris Vojjnovskaja- competition with other egg parasitoids Krieger (Hymenoptera: Braconidae) (Belo- because this niche is vacant (Liu and ko bylskij et al., 2012). Duan et al. (2012c) Bauer, 2007; Duan et al., 2009). In no- suggested that S. galinae might be a better choice tests, O. agrili were presented with match for more northerly climates in North eggs of six species of Agrilus spp., two of America than S. agrili. Cerambycidae and four of Lepidoptera, and only attacked three Agrilus spp. that had eggs similar in size to A. planipennis 9.3.2 Native parasitoids (Bauer et al., 2008). In choice tests, O. agrili preferred A. planipennis eggs over Parasitism by native parasitoids of A. the other three Agrilus spp. with com- planipennis populations was less than 1% parable size eggs. Methods for evaluating in south-eastern Michigan (Liu et al., 2003). parasitism by O. agrili have been Five species of hymenopteran parasitoids developed (Duan et al., 2011b, 2012a). were reared from A. planipennis larvae in Approval was granted to release S. Pennsylvania with a total parasitism rate of agrili, T. planipennisi and O. agrili into the 3.6% (Duan et al., 2009). No egg parasitoids wild in the USA (USDA-APHIS, 2007) and have been encountered in A. plannipennis fi rst releases were made at sites in populations in Michigan or Pennsylvania Michigan in 2007 (Bauer et al., 2008) and (Liu et al., 2003; Bauer et al., 2007; Duan et in Michigan, Indiana and Ohio in 2008 al., 2009). (Bauer et al., 2010). USDA-APHIS com- Preliminary surveys for native para- pleted construction of its Biological sitoids of A. plannipennis in Michigan Control Production Facility in Brighton, encountered extremely low levels of Atany- Michigan in 2008 for mass rearing the three colus hicorae Shenefelt and A. simplex species of Chinese parasitoids (Bauer et al., (Cresson) (Hymenoptera: Braconidae) (Liu 2008) and it came into production in the et al., 2003). A new species, Atanycolus spring of 2009. The rearing facility had cappaerti Marsh and Staznac, was sub- produced and released over 444,000 sequently described from emerald ash borer parasitoids of A. plannipennis in 12 states (EAB) in Michigan (Marsh et al., 2009). Two by February of 2012 (Gould et al. 2012). additional species, A. tranquebaricae The USDA-APHIS 5-year plan for bio- Shenefelt and A. nigropyga Shenefelt were logical control of A. planipennis is also reported from A. plannipennis-infested available online (USDA-APHIS, 2009). ash bolts in Michigan (Cappaert and Guidelines for the release and recovery of McCullough, 2009). Three species, A. the three parasitoids have been published cappaerti, A. hicoriae and A. longicauda 66 Chapter 9

Shenefelt (Hymenoptera: Braconidae), were estimated arrival of A. planipennis in that reared from EAB-infested logs from south- area (Gibson, 2005). In North America only western Ontario (Lyons, 2010). Cappaert females of B. indica are known, although and McCullough (2009) investigated the males are known to occur in Asia (Gibson, biology and biological control potential of 2005) and the species has successfully A. cappaerti. Observed parasitism rates reproduced parthenogenetically on A. ranged from 9 to 71% in two sites over 2 planipennis in the laboratory (Duan et al., years suggesting that this species might be 2009). The life history of this solitary an effective biological control agent for A. ectoparasitoid was described by Duan et al. planipennis. (2011a). Two specimens of the native parasitoid A single specimen of Metapelma Leluthia astigma (Ashmead) (Hymen- spectabile Westwood (Hymenoptera: Eupel- optera: Braconidae) were collected in midae) was reared from an A. planipennis- Ontario. One specimen was collected from infested ash bolt collected near Windsor, green ash infested with A. planipennis Ontario, a new record for Canada (Lyons, near Windsor and the other specimen was 2010). This species has previously been collected from red oak, L. reported from Agrilus angelicus Horn (Fagaceae), infested by Agrilus bilineatus (Coleoptera: Buprestidae) (Burks, 1979). (Weber) near Midland. Leluthia astigma In south-western Ontario, in the later has been reported from Quebec (Marsh, stages of an A. planipennis outbreak, 1979) but these are the fi rst specimens Phasgonophora sulcata Westwood (Hymen- collected from elsewhere in Canada. The optera: Chalcididae) was reared with a species, which was positively associated parasitism rate of 27.0% and trapped with with host cadavers, was reported as the an apparent parasitism rate of 40.4% most abundant parasitoid attacking A. (Lyons, 2010). The fl ight period of the planipennis in Delaware County, Ohio parasitoid seems to be synchronized with with a parasitism rate of 2.1% (Kula et al., the egg-laying period of A. planipennis and 2010). The species is a solitary idiobiont supports the observation by Haack et al. ectoparasitoid that is broadly distributed in (1981) that the parasitoid may lay eggs near North America (Kula et al., 2010). the host’s eggs. This parasitoid was reared Spathius fl oridanus Ashmead (= S. from A. planipennis in Michigan (Liu et simillimus Ashmead) (Hymenoptera: al., 2003), Agrilus bilineatus (Weber) Braconidae) was reared from A. plani- (Haack et al., 1981), A. anxius Cory (Akers pennis in Michigan (Liu et al., 2003; Duan and Nielsen, 1990) and A. granulatus et al., 2012b) and specimens were reared liragus Barter and Brown (Coleoptera: from Q. rubra infested with A. bilineatus Buprestidae) (Barter, 1965). near Midland, Ontario (Lyons, 2010). It is Other parasitoids reared from A. plani- considered the most promising among the pennis but not encountered in Ontario native Spathius spp. for biological control include: Eupelmus pini Taylor (Hymen- of A. planipennis (Marsh and Strazanac, optera: ), Dolichomitus vitti- 2009). crus Townes, Dolichomitus sp., Orthizema Balcha indica (Mani & Kaul) (Hymen- sp. and Cubocephalus sp. (Hymenoptera: optera: Eupelmidae), native to south- Ichneumonidae) and Eurytoma sp. eastern Asia, was encountered dur ing (Hymenoptera: Eurytomidae) (Duan et al., surveys for parasitoids of A. planipennis in 2009, 2012b). Michigan (Lui et al., 2003; Duan et al., 2012b), Virginia (Gibson, 2005), Pen- nsylvania (Duan et al., 2009) and Ontario 9.3.3 Fungal pathogens (Lyons, 2010). Balcha indica prob ably arrived in North America on some host Liu et al. (2003) reported that native fungal other than A. planipennis because its pathogens only resulted in ca. 3% discovery in Virginia in 1994 pre-dates the mortality in Michigan populations of Chapter 9 67

A. planipennis. The most prevalent fungus deleterious impacts on parasitoids used in collected was Beauveria bassiana (Bal- classical and augmentative biological con- samo) Vuillemin (Cordycipitaceae) (Bauer trol programmes. Fortuitously, T. plani- et al., 2004). Liu and Bauer (2006) have pennisi appears to have very low to no demonstrated the susceptibility of A. susceptibility to B. bassiana, while S. agrili planipennis to commercial strains of B. is only slightly susceptible when exposed bassiana and Metarhizium anisopliae to fungus-inoculated ash twigs (Dean et al., (Metschnikoff) Sorokin sensu lato (Clavi- 2012). The native P. sulcata and cipitaceae), although indigenous strains are Atanycolus spp. appear to be susceptible to as virulent as the commercial GHA strain. the fungus at high exposure levels (B. These may also have potential for Lyons, 2012, unpublished results), but managing A. planipennis populations as autocontamination traps for the dissemin- spray formulations (Liu and Bauer, 2008a, ation of fungi that target A. planipennis b; Castrillo et al., 2010), although viability may mitigate their exposure. of B. bassiana conidia applied as bark or foliar sprays is rather short-lived (Castrillo et al., 2010). Forest managers may be 9.3.4 Other pathogens hesitant to use broad-scale applications of generalist entomopathogens for fear of A small percentage of the A. planipennis impacting non-target insects. samples collected were also infected with a In Ontario, collections of mycosed A. nematode characterized using molecular planipennis prepupal and adult cadavers techniques as a Rhabditis (Oscheius) sp. and frass containing fungi yielded isolates (Rhabditida: Rhabditidae) (see Lyons, of Beauveria spp., the predominant 2010). A microsporidian, Cystosporogenes ‘natural’ pathogen, and Lecanicillium spp. sp. (Microsporidia: Glugeidae), was iso- (Cordycipitaceae), Metarhizium spp. (Clavi- lated from the bronze birch borer, A. cipitaceae) and Paecilomyces spp. (Tri- anxius, and cross-infectivity tests with A. chocomaceae) although at very low levels planipennis are being conducted (Kyei- (see Lyons, 2010). Isaria farinosa Poku et al., 2011). (Holmskjold) Fries (Cordycipitaceae) and Pur pureocillium lilacinum (Thom) Luangsa-ard et al. (Ophiocordycipitaceae) have also been isolated and characterized 9.4 Evaluation of Biological Control from A. planipennis cadavers collected in south-western Ontario (Johny et al., 2012a), In the USA, O. agrili and S. agrili have although bioassays indicated that they were successfully reproduced and overwintered, not as virulent to A. planipennis adults as and were recovered in the spring of 2008 were the commercial isolates of Isaria from Michigan and Ohio (Bauer et al., fumosorosea (LRC176), Metarhizium brun- 2008, 2010). Parasitism by O. agrili in 2009 neum (LRC187) and B. bassiana (GHA). and 2010 ranged from 1 to 6% and it also In 2011, two native isolates of B. overwintered in Maryland (Gould et al., bassiana, INRS-CFL, characterized by 2011a). Tetrastichus planipennisi was fi rst Sabbahi et al. (2009) and L49-1AA, recovered in 2009 (USDA-FS, 2009) and characterized by Johny et al. (2012b), were has successfully overwintered in Michigan, released into A. planipennis populations in Ohio and Maryland, with parasitism of south-western Ontario using auto- 0.1– 50% (Gould et al., 2011a; Duan et al., contamination traps (Lyons et al., 2012). 2012b). Agrilus planipennis larvae Entomopathogens with broad host ranges parasitized by T. planipennisi have been may have limited use in integrated control recovered 800 m from the release sites programmes for A. planipennis, because of (Bauer et al., 2010). 68 Chapter 9

9.5 Future Needs 5. Determining the impact and effi cacy of autocontamination of A. planipennis The importation and release of T. adults by Beauveria bassiana. planipennisi, S. agrili and O. agrili into Ontario populations of A. planipennis is an important step towards biological control Acknowledgements of A. planipennis. Future work should include: I thank G. Jones, A. Kent, N. O’Brien, M. 1. Preparation and submission of petitions Rains, A. Sauve and S. Woodcock for for release of T. planipennisi, S. agrili and assistance in the laboratory and fi eld. O. agrili in Canada; Thanks to A. Keizer and H. Evans for 2. Post-release monitoring to determine the collecting Agrilus-infested logs. Thanks are overwintering success, long-term establish- also extended to G. Gibson and H. Goulet ment and impact of the parasitoids on A. (Agriculture and Agri-Food Canada, planipennis populations; ECORC) for identifying native parasitoids. 3. Redistribution of T. planipennisi, S. Atanycolus spp. were graciously identifi ed agrili and O. agrili once they establish; by P. Marsh (United States National 4. Determining the potential for P. sulcata Museum, retired). George Kyei-Poku and other native parasitoids as inoculative provided the information on his research and augmentative biological control agents on entomopathogens. against A. planipennis;

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10 Agriotes spp. L., Wireworms and Click Beetles (Coleoptera: Elateridae)

Todd Kabaluk,1 Alida Janmaat,2 Claudia Sheedy,3 Mark Goettel3 and Christine Noronha4 1Agriculture and Agri-Food Canada, Agassiz, British Columbia; 2University of the Fraser Valley, Abbotsford, British Columbia; 3Agriculture and Agri-Food Canada, Lethbridge, Alberta; 4Agriculture and Agri-Food Canada, Charlottetown, Prince Edward Island

10.1 Pest Status Schülb. and M. Martens (Apiaceae), and feeding on roots and coleoptiles of seed- Wireworms are the larval stage of click lings that causes plant death, are sources of beetles (Coleoptera: Elateridae) and, as a signifi cant losses from these pests. Click pest group, encompass around 20 species beetle adults are not known to be in Canada (Vernon and van Herk, 2013). agricultural pests. They feed almost exclusively on sub- European Agriotes spp. introduced to terranean plant tissue. Plants can tolerate Canada during the period 1850–1900 (Eidt, wireworm feeding when mature, but cos- 1953; MacNay, 1954) have become major metic damage on root crops, e.g. potatoes, pests. Among these, Agriotes obscurus (L.) Solanum tuberosum L. (Solanaceae), beets, and A. lineatus (L.) (Coleoptera: Elateridae) Beta vulgaris L. (Amaranthaceae), and are the primary pest species in British carrots, Daucus carota subsp. sativus Columbia, Nova Scotia and Newfoundland © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 10 73

(Vernon, 2005; Vernon et al., 2001), and A. with pest control products is their rapid sputator (L.) in Nova Scotia and Prince and somewhat unpredictable vertical Edward Island (Fox, 1961). Agriotes spp. movement in the soil profi le. While a are the only known non-indigenous pest certain degree of vertical movement has species. The full range of Elateridae species been attributed to soil moisture and tem- that are considered pests in Canada are perature over short time periods, the effect shown in Table 10.1. Despite variability, of these variables still needs to be some generalizations can be made about integrated with seasonality and vegetation the behaviour and life cycle of most density to develop a comprehensive model species, particularly Agriotes spp. At the that explains their movement in the soil end of their larval stage, overwintering profi le (Zacharuk, 1962). In general, the pupae or adults will emerge as adults in period of greatest larval activity in herb- the spring (approximately April–June in aceous root zone regions occurs in spring British Columbia), mate, and oviposit at and again in autumn. While wireworms are the base of growing plants. Neonate larvae generally believed to avoid shallow root feed on tender plant tissue, establish in the zones during the warmest and driest soil and for Agriotes spp. in Canada, months (July and August), they have been transition through up to 11 instars over 3–5 observed travelling on a dry soil surface in years (reports on the number of instars and mid-July with air temperatures exceeding length of time in soil vary in the literature). 30°C (T. Kabaluk, 2012, unpublished What makes the larvae diffi cult to target results).

Table 10.1. Elateridae pest species in Canada and regions in which they were found (adapted from W.G. van Herk and R.S. Vernon, 2013, unpublished results).a Species Region of occurrence Agriotes criddlei Van Dyke Prairies Agriotes lineatus (L.) Pacifi c, Atlantic Agriotes mancus (Say) Prairies, Quebec, Atlantic Agriotes obscurus (L.) Pacifi c, Atlantic Agriotes sputator (L.) South Central, Atlantic Aeolus mellillus (Say) Prairies Dalapius vagus Brown South Central, Quebec, Atlantic Selatosomus aeripennis aeripennis (Kirby) British Columbia, Parkland Belt (northern) Selatosomus aeripennis destructor (Brown) Parkland Belt (southern) Sylvanelater cylindriformis (Herbst) Atlantic Hemicrepidius memnonius (Herbst) South Central, Prairies Hypnoidus abbreviatus (Say) South Central, Atlantic Hypnoidus bicolor (Eschscholtz) South Central Limonius agonus Say South Central Limonius californicus (Mannerheim) British Columbia (interior), Prairies Limonius canus LeConte British Columbia (interior) Limonius pectoralis LeConte Prairies communis (Gyllenhal) South Central Melanotus similis (Kirby) South Central aAlthough species found in the regions presented are considered dominant, their absence from a region does not exclude the possibility of their occurrence. 74 Chapter 10

With heightened larval activity in the chlorpyrifos was recently granted regis- spring, newly seeded crops are most tration for use in potato, but because vulnerable at planting time. This is import residue limits do not exist for this particularly the case for maize, Zea mays chemical in the USA, its use is limited to L. (Poaceae) in areas where Agriotes spp. potatoes destined for the Canadian market. are present, but also applies to any crop Phorate is scheduled for deregistration, with a vulnerable germinating seed. Carbon with the last date of permitted use being 1 dioxide produced by tissue respiration of August 2015 (PMRA, 2012). germinating seeds and young respiring The newest class of synthetic agri- roots of seedlings actively attracts wire- chemicals, ‘neonicotinoids’, was created to worms (Doane et al., 1975). Feeding at this replace organophosphates. Of these, stage often causes whole plant loss. Potato clothianadin, thiamethoxam and imidaclo- seed tubers can usually withstand wire- prid are registered for wireworm control. worm feeding during the spring, but the However, their effects on wireworm feed- resurgence of feeding activity in the ing are only suppressive, as they anaesthe- autumn renders new tubers vulnerable to tize and/or repel wireworms for a time, cosmetic damage. rather than kill them. This is also the case The reporting of wireworms as a for the synthetic pyrethroid tefl uthrin, also problem pest in Canada, and worldwide, registered for wireworms (van Herk, 2008). has increased dramatically beginning in Biological control research on wire- the 1990s. This might be due to the decline worms has a long history in North of residual activity of organochlorine America, with signifi cant efforts and insecticides, withdrawal of the majority of advances being made in Canada. The organophosphate and carbamate regis- greatest attention has been on the use of trations, and the increase in agricultural entomopathogens. Observations of out- practices, e.g. cropping buffers, zero tillage, breaks of the entomopathogenic fungus rotations with perennial crops, that favour Metarhizium anisopliae (Metschnikoff) egg-laying habitat for adults and provide Sorokin sensu lato1 (Clavicipitaceae) in food for larvae (Parker and Howard, 2001). natural wireworm populations (e.g. Fox, The increase in wireworm abundance has 1961) and in laboratory collections (e.g. been matched with an increase in research Tinline and Zacharuk, 1960) have been attention, and biological control research most frequent. The fi rst report of M. activities are currently much greater than anisopliae ‘destroying’ a wireworm collec- they have been in the past. tion was made by Comstock and Slingerland (1891). Rockwood (1950) and Fox and Jaques (1958) were pioneers in 10.2 Background laboratory and fi eld experiments using Metarhizium spp. to target wireworms. Historically, control of wireworms was Tinline and Zacharuk (1960) conducted achieved using chemical insecticides. more comprehensive experimentation However, the increase in wireworm abun- using both M. anisopliae and Beauveria dance and damage to agricultural crops has bassiana (Balsamo) Vuillemin (Cordycipi- been associated with loss of highly effi - taceae) to target wireworms and they cacious organochlorine, organo phosphate reported the differential pathogenicity of and carbamate pesticides. The last of the these fungi against two species of organochlorine pesticides, lindane, was Elateridae. Extensive work on the bio- deregistered in Canada in 2004. Two logical control of wireworms using ento- organophosphates are still available for mopathogens resumed in the 2000s after wireworm control in Canada: chlorpyrifos the discovery of a highly pathogenic strain (Pyrinex®) and phorate (trade name of Metarhizium brunneum Petch Thimet®). After re-evaluation by the Pest (Clavicipitaceae) (Kabaluk et al., 2005). Management Regulatory Agency (PMRA), Recent research has encompassed areas Chapter 10 75

including the effect of different application nematodes (Kleespies et al., 2012). Wire- methods of M. brunneum conidia on worms frequently succumb to infection by wireworm mortality and crop protection Metarhizium spp. after collection from the (Kabaluk, T. et al., 2001, 2005, 2007; fi eld, implying that they carry but suppress Kabaluk, J.T. et al., 2007), environmental the disease in nature (M. Goettel, 2012, effects (Kabaluk and Ericsson, 2007), unpublished results). The presence of fungi synergy (Ericsson et al., 2007) and in the haemocoel of wireworms has been wireworm immunology (Ericsson, 2006). documented (C. Sheedy, 2011, un- The study of pathogenesis through published results). immunochemistry and electron microscopy The only microbial product registered (Kabaluk et al., 2012) will help understand for wireworm control is Naturalis® (B. the effi cacy of different fi eld application bassiana strain ATCC 74040; Intrachem methods in response to a variety of Bio Italia) in Italy. The company reported environmental conditions. Most recently, that with one soil application at the very different application methods of M. low rate of 6.9 × 1010 conidia ha−1, a 68% brunneum have been tested against reduction in Elateridae larvae (indicated to Elateridae adults with the ultimate goal of be predominantly Agriotes spp.) (Intra- reducing larvae populations in the fi eld (T. chem, 2005) was achieved, and conferred a Kabaluk and A. Janmaat, 2012, un- signifi cant reduction in feeding damage to published results; Fig. 10.1). The use of potato tubers. This product may be highly entomopathogens against wireworms has biotype-specifi c as other researchers (Koel- also recently gained interest in Europe, liker et al., 2011) reported that ATCC with a notable survey of wireworm 74040 produced no mortality in A. antagonists that includes Metarhizium and obscurus, A. lineatus and A. sputator Beauveria spp. and bacteria (Kleespies et larvae in laboratory trials, nor reduced al., 2012). Kabaluk et al. (2005) reported wireworm feeding damage to potato tubers fi nding one A. obscurus larva infected by in fi eld trials in Switzerland. Tolypocladium cylindrosporum Gams An isolate of M. brunneum, LRC112, (Ophiocordycipitaceae). obtained from an infected wireworm Gulls (Charadriiformes: Laridae) and cadaver near Agassiz, British Columbia has crows, Corvus spp. (Passeriformes: Corvi- been mass produced and used in fi eld and dae), are sometimes reported by farmers to laboratory trials and shows promise in feed on Agriotes spp. larvae exposed during research trials. It is highly virulent toward tillage. Kabaluk et al. (2005) reported several species of wireworms, including fi nding a Diptera pupa in the abdominal those in the genus Agriotes, and cavity of an A. obscurus adult, indicating at particularly A. obscurus (Table 10.2). least one incidence of potential parasitism. Kabaluk et al. (T. et al., 2001; J.T. et al., On one occasion deutonymphs of Acaridae 2007) reported the retrieval of both (Trombidiformes) mites were present on sporulating larval cadavers from the fi eld several specimens of A. obscurus but they (27% of sample) and the development of were confi rmed to be phoretic. Otherwise, mycosis in living wireworms collected information is lacking on the role of from fi eld plots (55% of incubated larvae) predators and parasitoids of A. obscurus testing LRC112 in factorial combinations and their potential role in biological of: wheat, Triticum aestivum L. (Poaceae), control. seeds coated with M. brunneum conidia, conidia granules, and soil mixed with conidia. These promising fi ndings justifi ed 10.3 Biological Control Agents initiation of a comprehensive wireworm biological control programme in Canada. Wireworm cadavers in both undisturbed Nematodes have potential as biological and pertubated land regularly exhibit signs control agents of wireworms. Mermithidae of infection from fungi, bacteria and are observed in a small proportion (<1%) 76 Chapter 10

– – LT50 (95% LT50 C.I.) a Metarhizium % mortality LeConte to LT50 LT50 (95%C.I.) a Limonius canus % mortality (Horn) and LT50 (95% LT50 C.I.) a Ctenicera pruinina (L.), % mortality A. sputator (L.), LT50 (95% LT50 C.I.) a A. lineatus % mortality (L.), LT50 (95% LT50 C.I.) a Agriotes obscurus Agriotes obscurus Agriotes lineatus Ctenicera pruinina Agriotes sputator Limonius canus % mortality Assay # Susceptibility of Susceptibility isolates of varying virulence. LRC 112 1 87 (87) 2 27 (23–33) 3 27 (27) 100 (87) 4 5 17 (13–20) 87 (87) 100 (100) 6 12 (8–19) – 87 (67) 10 (8–12) 100 (100) 7LRC 142 14 (13–16) 100 (87) 23 (18–29) 8LRC 148 100 (100) 67 (67) 3 100 (20) 9 14 (12–16) 21 (16–28)LRC 149 100 (73) 80 (60) 100 (67) 30 (23–38) 10 2 100 (90) 14 (12–17)LRC 177 14 (12–17) 17 (13–21) 23 (16–32) 100 (53) 100 (60) 20 (13) 3 100 (93) 100 (67) 14 (13–15)LRC 178 30 (0) 13 (9–17) 1 13 (10–17) 93 (93) 40 (20) 17 (14–20) 14 (12–18)LRC 180 80 (40) – nd 90 (80) nd 1 40 (13) 19 (15–23) 47 (33) 21 (14–31) 93 (79) 2 – 30 (26–34) 20 (0) nd nd 73 (73) – 23 (19–27) 20 (0) 100 (100) – 80 (40) nd 26 (23–30) 100 (45) – 15 (13–17) 26 (19–36) – 5LRC 181 nd 20 (13) 100 (0) 7 (13–22) 80 (73) – 6 nd 2 0 (0) 100 (87) 12 (8–17) 7 nd 87 (20) 16 (10–27) nd 100 (100) nd nd 8 12 (10–15) 7 (0) 16 (11–24) – 100 (100) 100 (73) 14 (11–18) 20 (20) 100 (100) nd 67 (60) nd nd 13 (11–15) 15 (12–19) 7 (15–18) 100 (100) – 5 nd 7 (7) 14 (12–17) nd 33 (22–49) 100 (80) 6 40 (40) 87 (87) – – 100 (87) 29 (21) 13 (11–16) nd 7 70 (70) 21 (17–27) 93 (33) 100 (93) 73 (67) 8 14 (12–16) 87 (73) 32 (25–41) 23 (18–30) – 100 (100) 100 (67) 14 (11–17) 100 (87) – 26 (22–33) 16 (11–23) nd 100 (80) nd – 93 (93) 17 (13–21) 100 (80) 100 (20) nd 17 (14–20) 17 (14–21) 18 (14–22) 40 (40) 27 (21–34) 0 (0) 15 (11–20) 12 (10–14) nd 10 (0) nd 100 (27) 100 (10) nd 100 (100) 100 (47) 47 (33) nd nd 21 (16–27) nd nd (9–14) 11 22 (18–26) nd 18 (14–22) – nd – 100 (10) nd nd 13 (10–16) nd nd 100 (13) 100 (40) 19 (15–24) nd 19 (15–24) nd nd nd nd nd nd nd nd nd nd nd nd nd nd anisopliae Accession number† Table 10.2. Table Chapter 10 77 – – – – – – Continued % Control mortalities % mortality attained (% mycosis) LRC 182LRC 183 5LRC 186 10 1LRC 187 1 33 (0) 5 87 (87) 13 (0) 20 (7) 20 (15–25)LRC 189 40 (0) –LRC 202 65 (65) 3 – 9LRC 204 10 6 25 (19–34) –LRC 205 4 33 (13) –LRC 206 0 (0) 13 (13) 2 13 (13) 14 (7) 27 (13)LRC 207 nd 6 47 (27)LRC 209 7 (7) – 3 47 (33) 67 (60) –LRC 219 – – – 6 40 (0) – – 9 13 (7) – – – 20 (7) 7 (7) 13 (0) 100 (93) 93 (7) 100 (100) 27 (27) 0 (0) – 13 (11–15) 17 (15–20) 20 (13) 10 22 (17–28) 73 (73) – 100 (73) 47 (40) 20 (13) 71 (57) – – – 27 (22–33) 12 (9–16) 100 (93) – nd – – 0 (0) nd 22 (16–31) – 20 (20) 21 (17–24) 13 (13) – 87 (40) nd 0 (0) 93 (86) nd nd 100 (33) 100 (93) 12 (7–18) nd – 25 (22–30) – – 18 (15–21) 100 (73) 13 (9–19) nd 15 (12–18) – nd nd nd 100 (73) 47 (7) nd nd nd nd 12 (9–17) 67 (0) – 14 (7) 10 27 (27) nd 47 (33) 34 (28–41) nd7 (0) nd – – nd – 71 (71) nd nd nd 26 (21–32) nd nd – 27 (20) 29 (7) 40 (33) 14 (7) 27 (27) nd – nd nd nd 7 (7) – 0 (0) – 9 71 (57) 25 (21–31) 30 (50) 30 (21–43) nd 15 (15) – 1 2 3 27 (7) 7 (0) 4 27 (0) 5 0 (0) 6 13 (0) – 7a – 7 (0) 8 7 (0) – 9 10 (0) 7 (0) – 30 (0) 7 (0) – 7 (0) 7 (0) – 0 (0) – – – 0 (0) – 0 (0) – – 0 (0) 20 (0) – 0 (0) 27 (0) – 33 (13) 20 (0) – – 53 (0) – – – 33 (0) – – 40 (0) – 40 (0) nd 50 (0) – nd nd – nd – nd – nd nd nd nd nd nd 0 (0) nd nd nd – nd nd nd 0 (0) 78 Chapter 10

Key to Table 10.2. Accession number Identifi er Source substrate Source location LRC 112 DAOM231489 Wireworm, Agriotes obscurus Agassiz, BC, Canada LRC 142 – Wireworm, Agriotes obscurus Agassiz, BC, Canada LRC 148 FI-522 Peanut scarab, Heteronyx piceus Australia LRC 149 ARSEF 1377 Wireworm, Agriotes sputator Switzerland LRC 177 Keller 714 Wireworm, Agriotes sp. Switzerland LRC 178 Keller 735 White grub, Phylloptera horticola (Col.) Switzerland LRC 180 180A Wireworm, Agriotes lineatus Pender Island, BC, Canada LRC 181 181A Wireworm, Agriotes lineatus Vancouver, BC, Canada LRC 182 CABI 014746 Wireworm, Agriotes sp. Oregon, USA LRC 183 UAMH 421 Insect West Virginia, USA LRC 186 UAMH 4450 Soil Alberta, Canada LRC 187 F52 Codling moth, Cydia pomonella Austria LRC 189 ARSEF 2518 Wireworm, Conoderus sp. New Zealand LRC 202 ATCC 62176 Nematode, Heterodera gylcines Ichinohe Illinois, USA LRC 204 ARSEF 23 Wireworm, Conoderus sp. North Carolina, USA LRC 205 ARSEF 1903 Wireworm, Conoderus sp. USA LRC 206 ARSEF 2107 Wireworm, Agriotes sp. Oregon, USA LRC 207 ARSEF 1897 Wireworm, Conoderus sp. California, USA LRC 209 ARSEF 5520 Soil Norway LRC 219 – Wireworm, Limonius canus Kelowna, BC, Canada of fi eld collections of A. obscurus and A. (Eschscholtz) (Coleoptera: Elateridae) were lineatus larvae in British Columbia. much more susceptible to infection by M. Heterorhabditis spp. (Rhabditida: Heteror- anisopliae isolated from H. bicolor than habditidae) and Steinernema spp. (Rhab- were larvae of Ctenicera aeripennia (Kirby) ditida: Steinernematidae) have been tested and C. destructor (Brown) (these latter two for activity against wireworms, but the species are now referred to as Ctenicera results have been inconclusive. aeripennis destructor (Brown)) (Coleoptera: Bacteria-infected wireworms are also fre- Elateridae), while the adults of both quently observed, although further studies species were equally susceptible to M. to determine their value as biological anisopliae, as well as to B. bassiana control agents still need to be conducted. isolated from C. a. destructor. Subsequent Lacey et al. (2007) reported the rDNA work on pathogenicity showed a greater sequences of 86 bacterial isolates found in susceptibility of pupae and adults to Limonius canus LeConte (Coleoptera: infection by M. anisopliae than for larvae. Elateridae) larvae, and suggested that Females were more susceptible than males Rahnella aquatilis Izard et al. (Entero- and eggs were the least susceptible bacteraceae) might be useful for wire worm (Zacharuk and Tinline, 1968). This work control through a genetic modifi cation to was followed by studies on pathogenesis enhance wireworm active toxins. describing the fi ne structure of host (wireworm) penetration by M. anisopliae (Zacharuk, 1973). More recently, antibodies 10.4 Evaluation of Biological Control to M. anisopliae are being used to bind mycelia invading larvae of A. obscurus (C. Metarhizium spp. have been the most Sheedy, 2012, unpublished results). To- studied biological control agents, even gether with the use of electron microscopy, though research attention has been the research team aims to evaluate the sporadic over the last century (Wraight et success of different M. brunneum use al., 2009). Tinline and Zacharuk (1960) patterns in infecting wireworms under showed that larvae of Hypolithus bicolor fi eld conditions (Kabaluk et al., 2012). Chapter 10 79

In Canada, almost all of the research on (Ericsson et al., 2007), even at extremely the biological control of wireworms has low rates (3.3 × 102 conidia g−1 soil). The been conducted using M. brunneum strain is equally virulent toward adult LRC112 and strains within its clade beetles, and trials are currently underway (LRC142, LRC180 and LRC181; Inglis et al., to determine its effi cacy under fi eld 2008; Table 10.2). In six independent fi eld conditions. The most recent results show a trials that included a range of use patterns, rapid decline in adult beetle numbers in broadcast pre-plant-incorporated conidia response to the presence of M. anisopliae granules reduced A. obscurus wireworm granule (barley fl akes) bands providing feeding damage to potato tubers by 30% 1014 conidia ha−1 (T. Kabaluk and A. (Kabaluk et al., 2005). Corroborating Janmaat, 2012, unpublished results; Fig. similar fi ndings of Tinline and Zacharuk 10.1). These fi ndings have given rise to (1960), J.T. Kabaluk et al. (2007) reported research on adult beetle behaviour in differences in susceptibility of larvae to response to Metarhizium exposure and the infection by M. anisopliae, even among implications for disease transmission. The Agriotes spp. Table 10.2 lists the results of goal of this research is to determine how our bioassays, and illustrates differences in controlling adults ultimately affects larvae susceptibility among wireworm species populations in the soil. and genera, and differential virulence Entomopathogenic nematodes, Steiner- among Metarhizium isolates. The effi cacy nema spp. and Heterohabditis spp. nema- of LRC112 has been signifi cantly syner- todes as wireworm biological controls are gized when applied together with spinosad currently being investigated (C. Noronha,

100

90

80

70

60

50

40

30

20

10

0 15

Mean beetle mortality control) ± s.e. (percentage of negative 510 Days following application of Metarhizium brunneum conidia

Fig. 10.1. The effect of three different application methods of Metarhizium brunneum conidia (1014 ha−1) on the mortality of Agriotes obscurus adult click beetles. All treatments were applied within a 1.77 m2 circular arena covered with screen to contain beetles (n=6 arenas per treatment). 10 cm wide band of conidia granules bisecting arena ({); conidia dust (z); conidia spray (š); h–cyhalothrin (Matador®) spray positive control ( ).

80 Chapter 10

2012, unpublished results). Development studying the vertical movement of wire- of screening techniques for soil larvae, worms in the soil profi le; (iii) drench appli- including wireworms, to discover promis- cations of Metarhizium together with ing entomopathogen strains is being con- spinosad; and (iv) development of imaging ducted (D. Hendersen, 2012, unpublished techniques to study pathogenesis of results). Metarhizium in wireworms, and applying these techniques to assess performance of inundative applications of Metarhizium in 10.5 Future Needs the fi eld; 3. Development of a systematic screening Future work should include: programme to acquire highly productive Metarhizium strains with virulence equal 1. Research to control Agriotes spp. adults to or greater than that of LRC112; including: (i) determining the effect of 4. Exploration for and evaluation of other adult control on fecundity by evaluating biological control agents, particularly exist- post-treatment soil populations of larvae; ing and newly available nematodes. (ii) characterizing Metarhizium disease transmission of initially-treated adults to adults emerging from the soil later in the season; (iii) assessing the role of phero- Note mones for improving Metarhizium effi cacy; (iv) determining the effect of Metarhizium 1 Early reports of Metarhizium were mostly M. inoculation and pheromones on adult anisopliae according to the taxonomy preceding Bischoff et al. (2009), after which most M. behaviour and disease transmission; and anisopliae were revised to several distinct (v) determining the effect of Metarhizium Metarhizium species. To align recently reported applications on non-target organisms; species with those reported in the past, and to 2. Improving fi eld effi cacy of Metarhizium avoid misrepresenting species identifi ed in early against larvae in soil, including: (i) new reports, we have retained the taxonomy preceding use patterns and more virulent isolates; (ii) Bischoff et al. (2009) in all literature citations.

References

Bischoff, J.F., Rehner, S.A. and Humber, R.A. (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101, 512–530. Comstock, J.H. and Slingerland, M.V. (1891) Wireworms. Bulletin of the Cornell University Agricultural Experiment Station, Bulletin 33. Doane, J.F., Lee, Y.W., Klinger, J. and Westcott, N.D. (1975) The orientation response of Ctenicera destructor and other wireworms (Coleoptera: Elateridae) to germinating grain and carbon dioxide. The Canadian Entomologist 107, 1233–1252. Eidt, D.C. (1953) European wireworms in Canada with particular reference to Nova Scotian infestations. The Canadian Entomologist 85, 408–414. Ericsson, J.D. (2006) Host-pathogen interplay: a study of factors applicable to the infection effi cacy of Metarhizium anisopliae to wireworms (Agriotes spp.) L. MSc thesis, University of British Columbia, Vancouver, British Columbia. Ericsson, J.D., Kabaluk, J.T., Goettel, M.S. and Myers, J.H. (2007) Spinosyns interact synergistically with the insect pathogen Metarhizium anisopliae (Deuteromycete: Hyphomycete) against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera: Elateridae). Journal of Economic Entomology 100, 31–38. Fox, C.J.S. (1961) The distribution and abundance of wireworms in the Annapolis Valley of Nova Scotia. The Canadian Entomologist 93, 276–279. Fox, C.J.S. and Jaques, R.P. (1958) Note on the green-muscardine fungus, Metarrhizium anisopliae (Metch.) Sor., as a control for wireworms. The Canadian Entomologist 15, 314–315. Chapter 10 81

Inglis, D.G., Duke, G.M., Goettel, M.S. and Kabaluk, J.T. (2008) Genetic diversity of Metarhizium anisopliae var. anisopliae in southwestern British Columbia. Journal of Invertebrate Pathology 98, 101–113. Intrachem (2005) Contro gli Elateridi della patata e della carota. Intrachem internal technical report. Kabaluk, J.T. and Ericsson, J.D. (2007) Environmental and behavioral constraints on the infection of wireworms by Metarhizium anisopliae. Environmental Entomology 36, 1415–1420. Kabaluk, J.T., Vernon, R.S. and Goettel, M.S. (2007) Mortality and infection of Agriotes obscurus (Coleoptera: Elateridae) with inundative fi eld applications of Metarhizium anisopliae. Phytoprotection 88, 51–56. Kabaluk, T., Goettel, M., Vernon, B. and Noronha, C. (2001) Evaluation of Metarhizium anisopliae as a biological control for wireworms. Pacifi c Agri-Food Research Centre (Agassiz) contribution no. 165. Kabaluk, T., Goettel, M., Erlandson, M., Duke, G., Ericsson, J. and Vernon, B. (2005) Metarhizium anisopliae as a biological control for wireworms and a report of some other endoparasitic enemies. IOBC/wprs Bulletin Insect Pathogens and Entomoparasitic Nematodes 28, 109–115. Kabaluk, T., Goettel, M., Ericsson, J., Erlandson, M., Casidy, F., Vernon, B., Jaronski, S., Mackenzie, K. and Cosgrove, L. (2007) Promise versus performance: working toward the use of Metarhizium anisopliae as a biological control for wireworms. IOBC/wprs Bulletin Insect Pathogens and Entomoparasitic Nematodes 30, 69–77. Kabaluk, T., Sheedy, C., Duke, G. and Leggett, F. (2012) Detection and imaging of Metarhizium infection of wireworms using antibodies and electron microscopy. Proceedings of the 45th Annual Meeting of the Society for Invertebrate Pathology, Buenos Aires, Argentina, 6–9 August 2012. Kleespies, R.G., Ritter, C., Zimmerman, G., Burghause, F., Feiertag, S. and Leclerque, A. (2012) A survey of microbial antagonists of Agriotes wireworms from Germany and Italy. Journal of Pest Science, DOI 10.1007/s10340-012-0447-9. Koelliker, U., Biasio, L. and Jossi, W. (2011) Potential control of Swiss wireworms with entomopathogenic fungi. IOBC/wprs Bulletin 66, 517–520. Lacey, L.A., Unruh, T.R., Simkins, H. and Thomsen-Archer, K. (2007) Gut bacteria associated with the Pacifi c Coast wireworm, Limonius canus, inferred from 16s rDNA sequences and their implications for control. Phytoparasitica 35, 479–489. MacNay, C.G. (1954) New records of insects in Canada in 1952: a review. The Canadian Entomologist 86, 55–60. Parker, W.E. and Howard, J.J. (2001) The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agricultural and Forest Entomology 3, 85–98. PMRA (Pest Management Regulatory Agency) (2012) Available at: http://www.hc-sc.gc.ca/cps-spc/ pubs/pest/_decisions/rev2008-05/index-eng.php (accessed 30 June 2012). Rockwood, L.P. (1950) Entomogenous fungi of the genus Metarhizium on wireworms in the Pacifi c Northwest. Annals of the Entomological Society of America 43, 495–498. Tinline R.D. and Zacharuk, R.Y. (1960) Pathogenicity of Metarrhizium anisopliae (Metch.) Sor. and Beauveria bassiana (Bals.) Vuill. to two species of Elateridae. Nature 187, 794–795. van Herk, W.G. (2008) Wireworm behaviour in response to insecticides. PhD thesis, Simon Fraser University, Vancouver, Canada. Vernon, B., LaGasa, E. and Philip, H. (2001) Geographic and temporal distribution of Agriotes obscurus and A. lineatus (Coleoptera: Elateridae) in British Columbia and Washington as determined by pheromone trap surveys. Journal of the Entomological Society of British Columbia 98, 257–265. Vernon, R.S. (2005) Aggregation and mortality of Agriotes obscurus (Coleoptera: Elateridae) at insecticide-treated trap crops of wheat. Journal of Economic Entomology 98, 1999–2005. Vernon, R.S. and van Herk, W.G. (2013) Wireworms as pests of potato. In: Giordanengo, P. and Alyokhin, A. (eds) Insect Pests of Potato: Global Perspectives on Biology and Management. Academic Press, Amsterdam, pp. 103–164. Wraight, S.P., Lacey, L.A., Kabaluk, J.T. and Goettel, M.S. (2009) Potential for microbial biological control of Coleopteran and Hemipteran pests of potato. In: Tennant, P. and Benkeblia, N. (eds) Fruit, Vegetable and Cereal Science and Biotechnology – Special Issue 1/Potato II – International Year of the Potato, pp. 25–38. 82 Chapter 11

Zacharuk, R.Y. (1962) Seasonal behavior of larvae of Ctenicera spp. and other wireworms (Coleoptera: Elateridae), in relation to temperature, moisture, food, and gravity. Canadian Journal of Zoology 40, 697–718. Zacharuk, R.Y. (1973) Penetration of the cuticular layers of Elaterid larvae (Coleoptera) by the fungus Metarrhizium anisopliae and notes on a bacterial invasion. Journal of Invertebrate Pathology 21, 101–106. Zacharuk, R.Y. and Tinline, R.D. (1968) Pathogenicity of Metarrhizium anisopliae, and other fungi, for fi ve Elaterids (Coleoptera) in Saskatchewan. Journal of Invertebrate Pathology 12, 294–309.

11 Anoplophora glabripennis (Motschulsky), Asian Longhorned Beetle (Coleoptera: Cerambycidae)

Jean J. Turgeon1 and Michael T. Smith2 1Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario, Canada; 2USDA Agricultural Research Service, Benefi cial Insect Introduction Research Unit, Newark, Delaware, USA

11.1 Pest Status Europe (Braunau-am-Inn, Austria, in 2001 (EPPO, 2001); and Gien, France, in 2003 Asian longhorned beetle, Anoplophora (Cocquempot and Hérard, 2003)). Since glabripennis (Motschulsky) (Coleoptera: then, at least 12 other populations have Cerambycidae), is native to China and the been uncovered in north-eastern North Korean peninsula (Lingafelter and Hoebeke, America and Europe (Haack et al., 2010). 2002) and is considered one the world’s In North America, the most recent top 100 worst invasive alien species detections of A. glabripennis have been in (http://www.issg.org/database/species/ Worcester, Massachusetts, in August 2008 search.asp?st=100ss). A breeding popu- (NAPPO, 2008a) and in Bethel, Ohio, in lation of this insect was detected in July 2011 (NAPPO, 2011a), whereas in Canada, on the outskirts of Toronto and Europe infestations have been found near Vaughan, Ontario, in 2003 (Hopkin et al., Paddock Wood, UK, and Winterswijk, the 2004). The discovery of this alien species Nether lands, as recently as March and July was not the fi rst. Indeed, by 2003, other 2012, respectively (EPPO, 2012a, b). populations had been uncovered in the Haack (2006) established that low USA (New York City, New York, in 1996 quality wood used in the construction of (Haack et al., 1996); Chicago, Illinois, in crates, pallets and dunnage for shipping 1998 (Poland et al., 1998); and Jersey City, goods such as tiles, machinery, steel and New Jersey, in 2002 (Haack, 2003)) and in ironware represented a major pathway for

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 11 83

the transport of live bark- and wood-boring larval development (Shao et al., 1997; insects. There is strong evidence that A. Smith et al., 2009; Tian et al., 2009; M.T. glabripennis has been, and still is being, Smith, 2012, unpublished results). In transported out of its native range on wood Korea, A. glabripennis attacks have been packaging material (Haack et al., 2010). limited to Acer tegmentosum Maxim., A. International phytosanitary measures were pseudosieboldianum (Pax.) Kom., A. mono adopted in 2002, and subsequently revised Maxim. and A. truncatum Bunge (Sapin- (Haack and Brockerhoff, 2011), to reduce daceae) (Williams et al., 2004). the risk of introductions associated with In Canada, most of the trees attacked by this pathway (Haack et al., 2010). A. glabripennis were Acer spp. (J.J. Anoplophora glabripennis is a wood Turgeon, 2012, unpublished results). In borer (xylophagous) that develops in addition, the beetle completed its life several families of broadleaf trees. In cycle, as evidenced by the presence of China, A. glabripennis is an induced pest larvae and exit holes on Betula spp. resulting from the widespread planting of (Betulaceae), Populus spp. and Salix spp. susceptible exotic tree species, e.g. Populus (Turgeon et al., 2007). Smith et al. (2009) deltoides W. Bartram ex Marshall, P. x and Sawyer (2012) reported that in the canadensis Moench and P. nigra L. USA, Acer spp. were also most commonly (Salicaceae), during a programme started attacked by A. glabripennis, but that other in 1978 and aimed at reforesting over 35 genera were suitable for complete develop- million ha of land (Yin and Lu, 2005; Zhao ment, namely: Aesculus (Sapindaceae), et al., 2007). It became a major pest Albizia (Fabaceae), Celtis (Cannabaceae), sometime in the 1980s, killing millions of Cercidiphyllum (Cercidiphyllaceae), Fraxi- trees in the plantations and shelterbelts nus (Oleaceae), Koelreuteria (Sapindaceae), established during the early phase of that Sorbus (), Platanus (Platanaceae) programme (Smith, 1999; Pan, 2005; Yin and Ulmus. In Europe, Hérard et al. (2005) and Lu, 2005). Globally, the total number reported A. glabripennis on additional of trees infested by A. glabripennis outside genera: Carpinus (Betulaceae), Fagus its native range now exceeds 35,000 (Haack (Fagaceae) and Prunus (Rosaceae). et al., 2010; J.J. Turgeon, 2012, un- Whether A. glabripennis had completed its published results), however, tree mortality development on these three genera is caused by the beetle has been relatively unknown. low thus far (Haack et al., 1997; Hérard et Reliable estimates of the economic and al., 2006; Turgeon et al., 2007). This low social impacts and costs of biological tree mortality likely results from a invasions are critical to developing combination of the ecological traits of A. credible management trade and regulatory glabripennis, including: the small size of policies (Aukema et al., 2011); however, the founder populations that is inherent for the potential impacts A. glabripennis could most invasive species; a relatively low have in Canada have yet to be estimated. reproductive capacity; its multi-year Based on knowledge of its current host process of host colonization; and the fact preference and the fact that it can and will that most infestations were discovered kill healthy trees, it was assumed the relatively soon (<10 years) after establish- impact would be devastating. Nowak et al. ment. (2001) estimated that 12–61% of the tree Trees attacked by A. glabripennis in population in nine major US cities would China are predominantly Populus spp. and be at risk of being killed; nationally, this Salix spp. (Salicaceae), followed by Ulmus could translate into a maximum of 30% spp. (Ulmaceae) and Acer spp. (Sapin- tree mortality and a corresponding canopy daceae). In addition, A. glabripennis loss of about 35%. This loss, which Nowak attacked Tilia mongolica Maxim. (Tilia- et al. (2001) estimated at US$669bn, did ceae) and Elaeagnus angustifolia L. not take into account losses that would be (Elaeagnaceae), but could not complete incurred by industries reliant on non-urban 84 Chapter 11

forest resources such as forest products days, respectively (Yan and Qin, 1992). derived from affected hardwood species, Females use their mandibles to chew maple syrup and fall foliage tourism, to oviposition pits into the outer bark. Eggs name a few (Smith et al., 2009). A study by are oblong, 5–7 mm long, and are laid Dodds and Orwig (2011) showed that A. singly between the sapwood and the inner glabripennis can establish in natural bark (Turgeon et al., 2007). Upon hatching, forests, although it has previously been young larvae feed extensively on the inner reported only in urban and suburban bark and cambial tissues, creating feeding environments, including neighbourhood galleries (Yan and Qin, 1992). Maturing parks. The ubiquity of Acer spp. in some larvae create tunnels that begin in the forest regions would make it possible for sapwood and extend into the heartwood, the beetle to spread through eastern North but continue to feed in the inner bark– America and severely impact the cambium–sapwood interface (Yan and Qin, economic, ecological and aesthetic values 1992). Once larval development is almost derived from these forests. completed, larvae expand the feeding area Bolts of infested trees from Toronto to create a pupal chamber in the wood. were sliced into 2.5 cm ‘cookies’ to Under laboratory conditions, adults take facilitate determination of the year when 3–7 days, depending on temperature, to larvae entered the wood and adults sclerotize after eclosion and another emerged. Live specimens of all immature 4–5 days to chew their way out of the stages were found. Examination suggests pupal chamber (Keena and Sanchez, 2007; that most beetles completed their life cycle M.T. Smith, 2012, unpublished results). by spending only one winter in the tree; Mature larvae have been found to tunnel to the remainder spent two winters (J.J. the outer bark and chew the adult exit Turgeon, 2012, unpublished results). Keena hole, and then return to form the pupal (2005) reported that larvae not reaching chamber (M.T. Smith, 2012, unpublished their critical weight for pupation before a results). chill period required a second chill period Detection of A. glabripennis-infested before initiating pupation. Thus, given the trees in Canada currently relies on the limited degree-day (DD) accumulation in visual inspection of trees, from the ground Toronto, it appears likely that in Canada, or by tree climbers, for signs and symptoms eggs laid in summer will hatch about 2 of attack (Haack et al., 2006; Turgeon et al., weeks later and spend only one winter in 2007, 2010). Traps baited with host the heartwood whereas those laid in late volatiles alone (Smith et al., 2009), or in summer or early autumn will take much combination with the male-produced sex longer to hatch and may even overwinter at pheromone (Nehme et al., 2010) are being that stage and spend two winters in the tested as a means to facilitate detection of wood. In northern China (Liaoning A. glabripennis. Province), 11–20% of A. glabripennis overwinter as eggs and 1st instar larvae inside the egg chorion (Yan and Qin, 1992). 11.2 Background Adult emergence of A. glabripennis begins after about 400 DD (threshold = 11.2.1 Within the native range 10°C) have accumulated in a given year (Smith et al., 2004). Mating can take place Infestations of A. glabripennis in China are soon after emergence, but there is an largely found in urban and agricultural obligatory period of maturation feeding areas and in tree plantations. Conversely, that lasts about 9–15 days (Li and Liu, A. glabripennis populations located in 1997; Keena, 2002; Smith et al., 2002). forested areas of north-eastern China are Adults feed on the petiole, foliage and believed to be at endemic levels, primarily twigs and, under fi eld conditions, female because of a greater diversity and the and male beetles live 14–66 days and 3–50 impact of natural enemies (Smith, 1999). Chapter 11 85

Hu et al. (2009) and Haack et al. (2010) stage. Zhao et al. (1991) constructed a life reviewed the various biological, chemical, table for A. glabripennis in China and physical and silvicultural measures that identifi ed categories of mortality factors for are being developed or have been tested to each stage of development, but without control A. glabripennis in urban areas of providing species names. Parasitism of eggs China. Control strategies used against A. was approximately 1% as evidenced by the glabripennis include: planting non-hosts presence of minute holes in the chorion. and resistant tree species; establishing Whether this parasitism was caused by mixed-species plantations or ‘man-made anaplophorae Delvare forests’ typically restricted to two or three (Hymenoptera: Eulophidae), an egg parasit- tree species; and cultivating fast-growing oid of Anoplophora chinensis (Förster) timber species within plantations to reduce (Coleoptera: Cerambycidae) recently stand rotation time and the likelihood of described by Delvare et al. (2004) or by infestations (Pan, 2005). In addition, an another species is unknown. Mortality of attract and kill system has been developed early instar larvae inhabiting the inner for A. glabripennis: the attractant, a potted bark–outer sapwood resulted from a tree of a species that is highly attractive to combination of parasitism (about 20–22%), the beetle, e.g. Acer negundo L. (Sapin- and fungal or bacterial pathogens (5–6%). daceae), is sprayed with a contact Host-tree-induced mortality of A. insecticide to kill landing adult A. glabripennis was approximately 7–10%. glabripennis (Gao and Li, 2002). Further- Mortality of late instar larvae inhabiting the more, T. mongolica (Shao et al., 1997; xylem was estimated at 10–18% and was Zhang et al., 1998; Lu et al., 2001) and E. caused by parasitoids, fungal or bacterial angustifolia (Tian et al., 2003, 2009) are pathogens and by woodpecker predation. reported as highly attractive hosts for Pupal and adult mortality prior to oviposition by A. glabripennis, but when emergence resulted primarily from fungal, these trees are attacked, eggs or early e.g. Beauveria bassiana (Balsamo) instars do not survive. By planting E. Vuillemin (Cordycipitaceae), and bacterial angustifolia as a belt around poplar infection, and was estimated at 8–9%. plantations, Tian et al. (2003) reported a Wang et al. (1995) subsequently analysed signifi cant reduction in oviposition in the the natural mortality factors for one poplars. None the less, control of A. generation of A. glabripennis and found an glabripennis in China continues to rely average natural mortality of 29.7%, with largely on two strategies: (i) spraying the majority attributed to pathogenic micro- contact insecticides on infested trees to kill organisms. Of the 36 bacteria and 30 fungus adults and injecting systemic insecticides strains isolated from A. glabripennis larvae into the trunk of infested trees to kill and pupae extracted from infested trees, larvae; and (ii) completely removing pathogenicity of eight bacteria ranged from infested trees, or removing only infested 16.7 to 66.7% and that of two fungi was branches or sections of the trunk to allow 100%; the remaining bacteria and fungi regrowth of established mature trees (Lu et appeared saprophytic (Wang et al., 1996). al., 2004). The latter approach has been Since the completion of these studies, used increasingly in the past decade greater emphasis has been given to the (Smith et al., 2009). exploration for, and identifi cation of, the The progress of biological control natural enemies of A. glabripennis in its programmes targeting the various life stages native range (Table 11.1). of A. glabripennis in China was reviewed by Hua et al. (1996), Qiu et al. (2004), Pan (2005), Hu et al. (2009) and Haack et al. 11.2.2 Outside the native range (2010). The initial search for natural enemies began with the identifi cation of The response of plant protection organ- mortality factors associated with each life izations around the world to the discovery 86 Chapter 11

Table 11.1. Natural enemies of Anoplophora glabripennis in China. Agent (Guild) Order: Family Species Notes

Parasitoids (Egg) Hymenoptera: Eulophidae Aprostocetus sp.a Endoparasitoid Parasitoids (Larval) Hymenoptera: Bethylidae Scleroderma guani (Xiao et Wu)b Ectoparasitoid Hymenoptera: Braconidae Iphiaulax impostor (Scopoli)c, a Ectoparasitoid Parasitoids (Late larval/pupal) Coleoptera: Bothrideridae Dastarcus helophoroides (Fairmaire)d Ectoparasitoid Predators (Larval) Coleoptera: Hololepta sp.a Hemiptera: Anthocoridae Lyctocoris sp.a Diptera: Milichiidaea : Ascidae Lasioseius ometes (Oudemans)c Lasioseius sp.c Proctolaelaps cossi Dugésc Mesostigmata: Digamasellidae Dendrolaelaps sp. c Predators (Larval/adult) Piciformes: Picidae Dendrocopos major (L.) e Pathogens (Bacteria) Pseudomonadaceae Pseudomonas alcaligenes Moniasf P. putida Trevisanf P. stutzeri (Lehmann & Neumann) Sijderiusf P. syringae Van Hallf Enterobacteriaceae Pantoea agglomerans (Ewing and Fife) Gavini et al. f Serratia marcescens Biziof Alcaligenaceae Alcaligenes faecalis Castellani & Chalmersf Pathogens (Fungi) Cordycipitaceae Isaria farinosa (Holmskjold) Friesf [=Paecilomyces farinosus (Holmskjold) A.H.S. Br. & G. Sm.] Beauveria bassiana (Balsamo) Vuilleminf

Data from: a Wang, W. et al. (1999); b Cheng et al. (2003) (cited in Hu et al., 2009); c Hua et al. (1996); d Wang, S. et al. (1999) (cited in Hu et al., 2009); e Li et al. (2000) (cited in Hu et al., 2009); f Wang et al. (1996)

of A. glabripennis beetles or infested trees all infested trees and following up with on their territory has been to attempt surveys. In the second step, tree species or eradication, with various degrees of genera considered at high risk and located success (Haack et al., 1997, 2010; Hérard et within a certain radius of infested trees al., 2005). In most countries, the were either removed or injected with a eradication strategy was based on surveys pesticide (Haack et al., 2010). This strategy to detect and delimit infestations, regu- has led to successful eradications in the latory tools to contain the spread of USA (Chicago, Illinois in 2008 (NAPPO, established populations, and control 2008b); Jersey City, New Jersey in 2008 actions to remove populations (Haack et (NAPPO, 2008a); Islip, New York in 2011 al., 2010). Control actions comprised two (NAPPO, 2011b)) and Europe (Almere, the steps. The fi rst step consisted of removing Netherlands in 2011 (EPPO 2011a); a Chapter 11 87

private garden, Belgium in 2011 (EPPO, and Isaria farinosa (Holmsk.) Fr. (Cordy- 2011b)). The infestations in Worcester and cipitaceae) (Wang et al., 1999a, 2000); and Bethel, USA, have spread to natural stands, (iv) hanging nesting boxes for wood- making the goal of eradication more peckers, Dendrocopos major (L.) (Pici- challenging given the ubiquity of maples formes: Picidae) in plantations where A. and other suitable host tree species in glabripennis is a problem (Gao et al., 1994; eastern forests. Should these infestations or Cheng et al., 2010). In addition, mortality another yet undetected infestation become of A. glabripennis was synergized when S. impossible to contain, it will be necessary guani was used to disperse B. bassiana or to develop a range of tools and tactics to I. farinosa (Wang et al., 1994, 1999a, b). To manage rather than eradicate this pest. date, the most widely used biological Exploration for native natural enemies control programmes for managing A. of A. glabripennis have been conducted in glabripennis continue to focus on D. infestations in Toronto and Worcester (M.T. helophoroides, S. guani, D. major and B. Smith, 2012, unpublished results). Logs bassiana. showing signs of attack were held in It is important to note that the natural rearing chambers in quarantine facilities, enemies reported thus far from China have and adult parasitoids were collected upon been collected almost exclusively from emergence. A subset of these infested logs urban and agricultural areas, and was also dissected and examined for the plantations, where diversity of broadleaf presence of parasitized immature A. trees is limited to one or two species of glabripennis. No parasitoids have been four genera: Populus, Salix, Ulmus and identifi ed thus far, likely due to the low Acer. Often, these tree genera are densities of A. glabripennis and a limited represented by a single species or clone. availability of damaged logs containing live The natural enemies of A. glabripennis in beetles. such ecosystems also appear limited to a few species with a broad host range. For example, D. helophoroides is a larval/ 11.3 Biological Control Agents pupal ectoparasitoid of 12 cerambycid species (Qin and Gao, 1988). 11.3.1 Within native range

The biological control agents of A. glabri- 11.3.2 Outside of native range pennis and the approaches used in China have included: (i) augmentation by mass Evaluation of A. glabripennis susceptibility rearing and release of parasitoids, specifi - to Bacillus thuringiensis Berliner serovar. cally Dastarcus helophoroides (Fairmaire) tenebrionis (Bacillaceae) (D’amico et al., (Coleoptera: Bothrideridae) (Fan, 2000; Wei 2004), several Beauveria spp. and and Li, 2011) and Scleroderma guani (Xiao Metarhizium anisopliae (Metschnikoff) and Wu) (Hymenoptera: Bethylidae); (ii) Sorokin (Clavicipitaceae) (Dubois et al., injecting of entomopathogenic nematodes 2004a, 2008; Hajek et al., 2008), and into A. glabripennis entrance holes or entomopathogenic nematodes (Fallon et plugging oviposition and/or exit holes with al., 2004) have been assessed largely under nematode-laden moist sponges, including laboratory conditions. Also, fi bre bands Heterorhabditis sp. (Rhabditida: Heteror- impregnated with B. brongniartii cultures habditidae), Steinernema feltiae (Filipjev) have been evaluated under fi eld conditions and S. carpocapsae (Weiser) (Rhabditida: (Dubois et al., 2004b; Hajek et al., 2006, Steinernematidae) (Qin et al., 1988); (iii) 2007). All these studies culminated in the injecting B. bassiana into borer holes or registration of a strain of M. anisopliae for plugging larval or exit holes with cotton pest control (Dubois et al., 2008). balls laden with fungal spores, including B. Exploration for native natural enemies bassiana, B. brongniartii (Saccardo) Petch of native longhorned beetles (Coleoptera: 88 Chapter 11

Cerambycidae: Lamiinae) associated with glabripennis in Canada because this maple in mixed deciduous forests have species is still under eradication and also been undertaken in the USA. Acer results are promising. No parasitoid has rubrum L. and A. saccharum Marshall been released in either the USA or Europe. (Sapindaceae) were girdled or felled at study sites in Delaware and Vermont, respectively, to induce colonization by 11.5 Future Needs native woodborers and associated para- sitoids. Logs showing signs of attack such Future work should include: as frass, oviposition pits or exit holes were 1. Expanding and intensifying explora- placed in rearing chambers and held in an tions for natural enemies of A. glabripennis outdoor insectary. Emerging adult wood- in natural mixed-deciduous forests of its borers and parasitoids were collected daily. native range, focusing on parasitoid species Shortly after, adult parasitoids were with a narrow host range and highly effec- exposed to fresh maple logs containing tive host searching ability (e.g. effective eggs and larvae of A. glabripennis, and under low host population density); parasitism was evaluated. To date, two 2. Completing investigations on life his- gregarious ectoparasitoids, Rhoptrocentrus tory and behaviour of R. piceus and O. piceus Marshall and Ontsira mellipes mellipes, the two gregarious ectoparasi- (Ashmead) (Hymenoptera: Braconidae), toids from the USA shown to parasitize have consistently parasitized, killed and and kill A. glabripennis early-instar larvae; completed development in early-instar 3. Evaluating host preference of R. piceus larvae of A. glabripennis (M.T. Smith and and O. mellipes for A. glabripennis versus R. Kula, 2012, unpublished results). One of their native host; the two parasitoids has been in continuous 4. Developing mass rearing and release culture for more than ten generations on A. methods for R. piceus and O. mellipes; glabripennis immature larvae within 5. Developing more effective tools to infested logs. Preliminary results indicate a detect newly established populations of A. high degree of compatibility and potential glabripennis. synergism of the two species (M.T. Smith, 2012, unpublished results).

Acknowledgements 11.4 Evaluation of Biological Control We thank Jinquan Wu (University of To date, no biological control agent has Delaware) for assistance with the Chinese been released for the management of A. literature.

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12 Aphis glycines Matsumura, Soybean Aphid (Hemiptera: Aphididae)

Jacques Brodeur Université de Montréal, Montréal, Québec

12.1 Pest Status al., 2011 and references therein). The yield of soybean declined with the density of The soybean aphid, Aphis glycines aphids per plant, and plants are Matsumura (Hemiptera: Aphididae), is a particularly susceptible to aphid injury multivoltine species native to Asia. In when infested at an early growth stage. North America it was fi rst detected in Aphid feeding can lead to a decrease in Michigan, USA in 2000 and rapidly spread plant growth, resulting in reduced pod set, through the continent (Venette and Rags- fewer and smaller seeds within pods at dale, 2004). Surveys of soybean, Glycine maturity and a decrease in protein and oil max (L.) Merr. (Fabaceae), fi elds in Ontario content. Aphis glycines also can transmit a and Quebec in 2001 revealed the presence number of plant-pathogenic viruses to of the aphid in Canada (Brodeur et al., soybean, but virus outbreaks have not 2003; Hunt et al., 2003). The establishment occurred so far. However, A. glycines has of A. glycines in Canada represents a caused signifi cant virus epidemics in other spectacular example of biological invasion. crops, e.g. snap bean, Phaseolus vulgaris L. By 2002, all soybean-growing regions in (Fabaceae), potato, Solanum tuberosum L. Quebec were infested, and 51 of 54 (Solanaceae), squash, Cucurbita spp. sampled fields were colonized by A. (Cucurbitaceae), during aphid dispersal. glycines (Brodeur et al., 2003). The aphid Growers now have to routinely budget for has rapidly colonized all US states and aphid scouting and, under some circum- Canadian provinces, e.g. Manitoba, Ontario, stances, application of insecticides to Quebec, where soybean is produced remain profi table. The introduction of A. (Ragsdale et al., 2011) and is causing glycines also has major consequences to profound changes in the agroecosystem the environment as infestations can lead to (Heimpel et al., 2004). For instance, the A. insecticide applications over a vast area of glycines invasion has led to an increase in agricultural land that was previously densities of insect predators, thus putting untreated. For example, following a severe other arthropods at risk through indirect A. glycines outbreak in 2007, 57% of the effects, such as apparent competition. soybean grown in Quebec that was insured The introduction of A. glycines into was treated with insecticides (Financière Canada poses a serious threat to soybean Agricole du Québec, 2007). production and the environment. The aphid Aphis glycines is a holocyclic and can severely reduce the yield of soybean, heteroecious species, alternating from pri- either directly through its feeding activity mary (buckthorn; Rhamnus spp. (Rhamna- or indirectly through the transmission of ceae)) to secondary (soybean; G. max) viral diseases (see review by Ragsdale et hosts. Unfortunately, the establishment in © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 94 Chapter 12

North America of this exotic aphid was fi ed as resistant or mostly resistant, mainly made possible by the prior and intentional through antibiosis and antixenosis mech- introduction of its two host plants: buck- anisms. Resistant varieties have been thorn from northern Europe and soybean commercialized since 2009. from Asia. In spring, on buckthorn, A. As aphid populations increase in glycines nymphs hatch from overwintering abundance and disperse, they trigger eggs and develop into parthenogenetic import ant functional and numerical re- fundatrices. After a few generations on the sponses by native and naturalized primary host, winged morphs emigrate to generalist predators. In Quebec, Mignault cultivated soybean where many over- et al. (2006) and Firlej et al. (2012) lapping generations occur throughout the characterized the species composition of summer. In autumn, winged females, called the foliar and ground fauna, respectively, gynoparae, and males are produced and associated with A. glycines in commercial emigrate on to buckthorn where they feed. soybean fi elds. Coccinellidae (Coleoptera) Gynoparae produce nymphs that develop were the most abundant aphidophagous into oviparae, mate with males and deposit predators in sweep samples in 2002 overwintering eggs on Rhamnus spp. Aphis (58.6%) and 2003 (44.8%), with one native glycines has a great capacity to disperse species, Coleomegilla maculata lengi within and between fi elds as winged Timberlake, and three naturalized species, morphs are produced throughout the grow- Harmonia axyridis (Pallas), Coccinella ing season. Winged morphs can disperse septempunctata L. and Propylea quatuor- between plants or enter low-level jet decimpunctata L., co-occurring with the streams and migrate over great distances soybean aphid throughout the growing (Rhainds et al., 2008; Zhang et al., 2008). season (Mignault et al., 2006). Carabidae (Coleoptera) beetles were the most com- mon ground predators captured in pitfall 12.2 Background traps. A total of 33 species from 15 genera were identifi ed, with the exotic Ptero- Aphis glycines was fi rst managed by foliar stichus melanarius (Illiger) represent ing applications of non-selective pyrethroid 75.8% and 84.5% of all individuals and organophosphate insecticides (dim- trapped in 2004 and 2005, respectively ethoate and Lambda-cyhalotrin) during (Firlej et al., 2012). outbreaks according to decision thresholds, Mortality caused by generalist predators crop maturity and abundance of natural has been repeatedly shown to limit the enemies. More recently, growers have economic impact of A. glycines in Asia and started to use neonicotinoid insecticides North America (reviewed by Ragsdale et (Thiamethoxame) applied as seed treat- al., 2011). In Quebec, Rhainds et al. (2007) ments (Magalhaes et al., 2008). This underlined the collective impact of preda- practice is controversial because aphid tors to regulate A. glycines populations, as population densities do not commonly indicated by the relatively low abundance reach the economic thresholds and because of aphids on plants experimentally infested the effi cacy of such systemic insecticides with aphids in comparison with control decreases with time and is likely not (caged) plants. The impact of carabid suffi cient to control A. glycines infestations beetles on A. glycines populations is less when they occur late in the season obvious than for foliar predators. There (Johnson et al., 2008). was no relationship between carabid trap The introduction of A. glycines into catches and A. glycines density, suggesting North America prompted intense research that carabid beetles do not respond in the development of soybean varieties numerically to soybean aphid populations resistant to aphid infestation (Hill et al., at the spatial scale (Firlej et al., 2012). 2006; Kim et al., 2010). More than two However, using molecular gut-content dozen soybean varieties have been identi- analysis, Firlej et al. (2013) showed that a Chapter 12 95 signifi cant proportion of P. melanarius, the 12.3 Biological Control Agents dominant carabid species in soybean fi elds, typically feed on A. glycines early in the In Canada, in addition to the on-going season when aphid densities are very low. ecological studies on generalist predators As reported in other studies (Holland and attacking A. glycines in soybean fi elds, the Thomas, 1997; Winder et al., 2005), the possibility of introducing exotic parasit- authors hypothesized that carabids are oids to strengthen the complex of natural unlikely to prevent large A. glycines enemies is being evaluated. A classical infestations but they can limit population biological control programme was initiated growth rate under low aphid density. in the USA in 2001, the year following the The benefi cial impact of generalist discovery of A. glycines in North America. predators appears consistent across a wide After exploration in Asia, host specifi city range of soybean management systems studies and experiments to assess potential (Costamagna and Landis, 2006), although effi cacy as biological control agent of A. their effectiveness is infl uenced by the glycines, Binodoxys communis (Gahan) abundance of A. glycines (Costamagna and (Hymenoptera: Bracon idae) was identifi ed Landis, 2007), the landscape structure and as a promising candidate and a permit from spatial distribution of aphid populations United States Department of Agriculture- (Desneux et al., 2006), within-fi eld man- Animal and Plant Health Inspection agement practices (Ragsdale et al., 2011) Service was granted for fi eld release in the and high levels of intraguild predation USA (Wyckhuys et al., 2007). Releases of (Gagnon et al., 2011). This ecological B. communis began in 2007 in the north- context suggests a cautious approach central USA, with approval to conduct toward the introduction of exotic biological laboratory studies in Canada following in control agents and the promotion of 2009. measures to preserve or enhance predator populations, such as limiting the use of pesticides in soybean fi elds. In Asia, parasitoids and entomopatho- 12.4 Evaluation of Biological Control genic fungi complete the typical guild of aphid natural enemies attacking A. Binodoxys communis has so far failed to glycines (Han, 1997). Although a total of establish in North America following seven hymenopteran parasitoids have been multiple releases (Ragsdale et al., 2011) reported attacking A. glycines in North and several nonexclusive explanations may America, parasitism levels have been so far account for this failure: low dispersal very low (see Ragsdale et al., 2011). How- ability, genetic bottlenecks and Allee ever, recent surveys indicated that effects in released parasitoid populations, parasitoids are now gradually responding and intraguild predation (Ragsdale et al., more to the invasion of soybean fi elds by 2011). Furthermore, Gariepy (2011) A. glycines (Noma and Brewer, 2008; recently showed under laboratory and fi eld Heimpel et al., 2010), with the exotic conditions that the Chinese B. communis Aphelinus certus Yasnosh (Hymenoptera: strain tested by our US colleagues has a Aphelinidae) now being the dominant very poor capacity to enter into diapause soybean aphid parasitoid in soybean- (<0.8%) and thus to overwinter in North producing regions of Ontario (>90% of America. It was hypothesized that the B. soybean fields surveyed; Frewin et al., communis strain has gradually lost its 2010) and Quebec (Gariepy, 2011). Seven ability to enter diapause during the species of entomopathogenic fungi have extended periods of quarantine and labora- been observed infecting A. glycines in New tory confi nement during which it was York state (Nielsen and Hajek, 2005), but continuously exposed to non-diapause information about their contribution to rearing conditions. New foreign explor- pest population regulation remains limited. ations have been conducted to recover 96 Chapter 12 natural B. communis strains that can enter 12.5 Future Needs diapause. Since its invasion of North America, A. Future research to manage A. glycines glycines has acquired pest status and has infestations through biological control dramatically changed the arthropod should focus on: community of the soybean agroecosystem. In the USA, but to a much lesser extent in 1. A better understanding of the degree of Canada, efforts have been devoted towards seasonal synchrony between A. glycines classical biological control by introducing and its complex of natural enemies, espe- parasitoids of A. glycines from Asia. cially early in the growing season when However, the knowledge acquired over the soybean plants are more sensitive to feed- last decade on the ecology of A. glycines in ing injury; North America should lead to a 2. A quantitative description of the evolu- reconsideration of the need to continue a tion of parasitism and disease (fungal) classical biological control programme for infection through time and an evaluation of A. glycines. First, several studies showed the contribution of aphid parasitoids and that generalist predators may suppress disease to A. glycines control; soybean aphid populations and mitigate 3. A strategy to integrate biological control their impact on soybean plants. Second, into pest management programmes, with recent surveys indicated that aphid an estimation of how chemical seed treat- parasitoids, mainly A. certus, are becoming ment and plant resistance may impact the more and more common in soybean fi elds effi cacy of natural enemies; and could in the near future play the role 4. The infl uence of landscape structure, we would expect from classical biological agronomic practices and climate on levels control agents. Furthermore, the potential of aphid infestation, predation, parasitism risks to non-target organisms posed by and fungal infection; exotic species introduced for biological 5. The need to introduce exotic natural control are an important concern for enemies to supplement the actions of Canadian regulatory authorities. native and naturalized species.

References

Brodeur, J., Roy, M. and Mignault, M.-P. (2003) Réseau de surveillance du puceron du soya. Programme agroenvironnemental de soutien à la Stratégie phytosanitaire du Plan d’action Saint- Laurent Vision 2000. Québec, Canada. Costamagna, A.C. and Landis, D.A. (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecological Applications 16, 1619–1628. Costamagna, A.C. and Landis, D.A. (2007) Quantifying predation on soybean aphid through direct fi eld observations. Biological Control 42, 16–24. Desneux, N., O’Neil, R.J. and Yoo, H.J. (2006) Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identifi cation of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environmental Entomology 35, 1342–1349. Financière Agricole du Québec (2007) Statistiques et taux/Statistiques/Assurance stabilisation/Coût de production/Soya. Available at: http://www.fadq.qc.ca (accessed 30 August 2012). Firlej, A., Gagnon, A.-É., Laurin-Lemay, S. and Brodeur, J. (2012) Diversity and seasonal density of carabid beetles (Coleoptera: Carabidae) in relation to the soybean aphid in soybean crop in Québec, Canada. The Canadian Entomologist 144, 542–554. Firlej, A., Doyon, J., Harwood, J.D. and Brodeur, J. (2013) A multi-approach study to delineate interactions between carabid beetles and soybean aphids. Environmental Entomology 42, 89–96. Chapter 12 97

Frewin, A.J., Xue, Y., Welsman, J.A., Broadbent, A.B., Schaafsma, A.W. and Hallett, R.H. (2010) Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae). Environmental Entomology 39, 1570–1578. Gagnon, A.-È., Heimpel, G.E. and Brodeur, J. (2011) The ubiquity of intraguild predation among predatory arthropods. PLoS ONE 6, e28061. Gariepy, V. (2011) Évaluation du potentiel des parasitoïdes Binodoxys communis, Aphidius colemani et Aphelinus certus pour la lutte au puceron du soya. Master’s thesis, Université de Montréal, Montréal, Québec, Canada. Han, X.C. (1997) Population dynamics of soybean aphid, Aphis glycines, and its natural enemies in the fi eld. Hubei Agricultural Sciences 2, 22–24. Heimpel, G.E., Ragsdale, D.W., Venette, R., Hopper, K.R., O’Neil, R.J., Rutledge, C.E. and Wu, Z. (2004) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Annals of the Entomological Society of America 97, 249–258. Heimpel, G.E., Frelich, L.E., Landis, D.A., Hopper, K.R., Hoelmer, K.A., Sezen, Z., Asplen, M.K. and Wu, K. (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biological Invasions 12, 2913–2931. Hill, C.B., Li, Y. and Hartman, G.L. (2006) A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Science 46, 1601–1605. Holland, J.M. and Thomas, S.R. (1997) Assessing the role of benefi cial invertebrates in conventional and integrated farming systems during an outbreak of Sitobion avenae. Biological Agriculture and Horticulture 15, 73–82. Hunt, D., Footit, R., Gagnier, D. and Baute, T. (2003) First Canadian records of Aphis glycines (Hemiptera: Aphididae). The Canadian Entomologist 135, 879–881. Johnson, K.D., O’Neal, M.E., Bradshaw, J.D. and Rice, M.E. (2008) Is preventative, concurrent management of the soybean aphid (Hemiptera: Aphididae) and bean leaf beetle (Coleoptera: Chrysomelidae) possible? Journal of Economic Entomology 101, 801–803. Kim, K.-S., Bellendir, S., Hudson, K.A., Hill, C.B., Hartman, G.L., Hyten, D.L., Hudson, M.E. and Diers, B.W. (2010) Fine mapping the soybean aphid resistance gene Rag1 in soybean. Theoretical and Applied Genetics 120, 1063–1071. Magalhaes, L.C., Hunt, T.E. and Siegfried, B.D. (2008) Development of methods to evaluate susceptibility of soybean aphid to imidacloprid and thiamethoxam at lethal and sublethal concentrations. Entomologia Experimentalis et Applicata 128, 330–336. Mignault, M.-P., Roy, M. and Brodeur, J. (2006) Soybean aphid predators in Québec and the suitability of Aphis glycines as prey for three Coccinellidae. BioControl 51, 89–106. Nielsen, C. and Hajek, A.E. (2005) Control of invasive soybean aphid, Aphis glycines (Hemiptera: Aphididae), populations by existing natural enemies in New York State, with emphasis on entomopathogenic fungi. Environmental Entomology 34, 1036–1047. Noma, T. and Brewer, M.J. (2008) Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest. Journal of Economic Entomology 101, 278–287. Ragsdale, D.W., Landis, D.A., Brodeur, J., Heimpel, G.E. and Desneux, N. (2011) Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56, 375– 399. Rhainds, M., Roy, M., Daigle, G. and Brodeur, J. (2007) Toward management guidelines for the soybean aphid in Québec. I. Feeding damage in relationship to seasonality of infestation and incidence of native predators. The Canadian Entomologist 139, 728–741. Rhainds, M., Brodeur, J., Borcard, D. and Legendre, P. (2008) Toward management guidelines for soybean aphid, Aphis glycines, in Québec. II. Spatial distribution of aphid populations in commercial soybean fields. The Canadian Entomologist 140, 219–234. Venette, R.C. and Ragsdale, D.W. (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Annals of the Entomological Society of America 97, 219–226. Winder, L., Alexander, C.J., Holland, J.M., Symondson, W.O.C., Perry, J.N. and Woolley, C. (2005) Predatory activity and spatial pattern: the response of generalist carabids to their aphid prey. Journal of Animal Ecology 74, 443–454. Wyckhuys, K.A.G., Hopper, K.R., Wu, K.M., Straub, C., Gratton, C. and Heimpel, G.E. (2007) Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News and Information 28, 30–34. 98 Chapter 13

Zhang, Y., Wang, L., Wu, K.M., Wyckhuys, K.A.G. and Heimpel, G.E. (2008) Flight performance of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) under different temperature and humidity regimens. Environmental Entomology 37, 301–306.

13 Aphis gossypii Glover, Melon/Cotton Aphid, Aulacorthum solani (Kaltenbach), Foxglove Aphid, and Other Arthropod Pests in Greenhouse Crops

Rosemarije Buitenhuis,1 Graeme Murphy2 and Les Shipp3 1Vineland Research and Innovation Centre, Vineland Station, Ontario; 2Ontario Ministry of Agriculture, Food and Rural Affairs, Vineland Station, Ontario; 3Agriculture and Agri-Food Canada, Harrow, Ontario

13.1 Pest Status 13.1.1 Aphids

Greenhouse crops, both vegetables and Melon/cotton aphid, Aphis gossypii Glover, ornamentals, are attacked by various insect foxglove aphid, Aulacorthum solani and mite pests that can cause signifi cant (Kaltenbach), potato aphid, Macrosiphum losses if not controlled. The year-round euphorbiae (Thomas) and green peach nature and controlled climate of the green- aphid, Myzus persicae (Sulzer) (Hemiptera: house industry result in pest pressures that Aphididae), are all serious pests of a wide can cause signifi cant economic damage at range of greenhouse vegetable and orna- any time of the year. For vegetable crops, mental crops. Chrysanthemum aphids, such damage can translate into yield Macrosiphoniella sanborni (Gillette) losses; for ornamental crops, even low (Hemiptera: Aphididae), are pests of levels of pests and/or damage can detract chrysanthemums, Chrysanthemum spp. from crop quality and cause heavy fi nan- (Asteraceae). Aphid damage is mostly cial losses. The composition of the pest related to the deposits of honeydew, which complex can vary depending on the crop promotes the development of sooty species, but a number of arthropod pests moulds, the presence of the aphids are common across a broad range of both themselves and their cast-off skins. Aphids ornamental and vegetable greenhouse in greenhouses also transmit plant viruses crops. such as Cucumber mosaic virus (Bromo-

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 13 99

viridae). Aulacorthum solani secretes deformation of developing plant tissues, salivary toxins that can cause leaf vein and indirectly through transmission of yellowing, local tissue necroses and severe tospoviruses. Tomato spotted wilt virus twisting and curling of plant tissue. (Bunyaviridae) is of particular concern in Aulacorthum solani is an increasing greenhouse vegetables and some orna- problem in peppers, Capsicum annuum L. mentals such as chrysanthemum, Chrys- (Solanaceae), and various ornamentals, anthemum morifolium Ramat (Asteraceae). potentially due to growers’ adoption of Impatiens necrotic spot virus (Bunya- integrated pest management (IPM) prac- viridae) is also transmitted by thrips and tices and reduction of pesticide sprays. A can devastate many species of greenhouse dark green clone of M. persicae was a ornamentals. widespread problem in British Columbia peppers in 2002–2003 and was found to have reduced vulnerability to parasitoids, a 13.1.3 Whitefl ies higher reproductive rate and less resistance against pyrethroid insecticides compared Bemisia tabaci (Gennadius) (Hemiptera: to other clones (Gillespie et al., 2009). Aleyrodidae) is the most problematic pest Since the early 2000s, a reddish-coloured whitefl y species in ornamental pro- phenotype of M. persicae has caused per- duction, and the greenhouse whitefl y sistent problems for greenhouse growers, Trialeurodes vaporariorum (Westwood) proving more diffi cult to control (G. (Hemiptera: Aleyrodidae) is the main pest Murphy, 2012, unpublished results). in vegetable production and certain ornamentals such as gerbera, Gerbera jamesonii Adlam (Asteraceae). Feeding by 13.1.2 Thrips whitefl ies causes a reduction in plant vigour and their honeydew promotes the Greenhouse crops are mainly attacked by growth of black sooty mould. In western fl ower thrips, Frankliniella ornamental crops, the visible presence of occidentalis (Pergande) (Thysanoptera: whitefl ies and old pupal skins is not Thripidae). Nuclear-mitochondrial barcod- tolerated. In addition, whitefl ies carry ing showed that what is currently plant viruses, especially in greenhouse recognized as F. occidentalis is a complex vegetables, such as Beet pseudo-yellows of two sympatric cryptic species (Rugman- virus (Closteroviridae) in cucumbers, Jones et al., 2010), although no survey has Cucumis sativus L. (Curcu bitaceae). been done in Canada. Occasionally, Bemisia tabaci is primarily a pest of Echinothrips americanus (Morgan) and poinsettia, Euphorbia pulcherrima Willd. Thrips tabaci Lindeman (Thysanoptera: ex Klotzsch (Euphorbiaceae) in Canada, Thripidae) are found. The chilli thrips, and uses the global movement of cuttings Scirtothrips dorsalis Hood (Thysanoptera: as a pathway for introduction. It can be a Thripidae), which established in Florida in major problem that can be diffi cult to 2005 (Hodges et al., 2005), is a potential control in the time frame of the crop, invasive thrips species in Canadian green- particularly if heavy infestations are intro- houses. Thrips are one of the most duced on new plant material. Bemisia important greenhouse pests worldwide tabaci on poinsettia seldom transfers because they are polyphagous and have a directly to other crops, although this tendency to reside and feed in concealed species can also enter Canada on other areas of fl owers and fruits. The relatively tropical ornamental plants that have been short generation time and haplodiploid sex imported from areas such as Florida. determination also contribute to the pest There are two biotypes of B. tabaci status of thrips (Reitz, 2009). All thrips (designated as ‘B’ and ‘Q’), with the species damage crops through direct primary difference (from a practical point feeding, which causes feeding scars and of view) being their resistance profi le to 100 Chapter 13

pesticides. Recent molecular work by de to appear on the leaves and when popu- Barro et al. (2011) suggests the two lations are high, webbing is unsightly and biotypes are separate species within a plant growth and yield are affected. complex of 24 species. Morphologically, all species are identical. Trialeurodes vaporariorum remains as 13.1.6 Tomato russet mites the major whitefl y species in vegetable crops such as tomato, Solanum lyco- Tomato russet mite, Aculops lycopersici persicum L., pepper, C. annuum, auber- (Massee) (Trombidiformes: Eriophyidae), is gine, Solanum melongena L. (Solanaceae), an occasional pest of greenhouse-grown S. and cucumber, C. sativus. It is a routine lycopersicum tomato in Canada, but has target of biological control programmes in become more common in recent years. those crops. Likewise in the ornamental Usually, it is only detected when damage is crop of G. jamesonii (especially those visible and populations have increased to grown as cut fl owers) T. vaporariorum is a high numbers. It can cause severe crop major pest, and populations often develop losses when left untreated. Bronzing of the that are severe enough to damage fl owers stem is visible when infestations move and signifi cantly reduce production. upward in the plant. Leaves turn yellow- brown and the edges curl and infested fruit can show russeting cracks. 13.1.4 Leafminers

In greenhouse ornamentals, leafminers 13.1.7 Broad mite/cyclamen mite have caused serious problems on Chrys- anthemum spp., G. jamesonii and various Broad mites Polyphagotarsonemus latus other crops due to resistance to (Banks) (Trombidiformes: Tarsonemidae) insecticides. The main leafminer species can be a serious pest of greenhouse are the American serpentine leafminer peppers and a wide range of greenhouse Liriomyza trifolii (Burgess) and the pea ornamental plants including G. jamesonii, leafminer Liriomyza huidobrensis (Blan- African violet, Saintpaulia spp. (Gesneria- chard) (Diptera: ). The chrys- ceae), cyclamen, Cyclamen persicum Mill. anthemum leafminer, Chromatomyia (Primulaceae), begonias, Begonia spp. syngenesiae (Hardy) (Diptera: Agromy- (Begoniaceae), impatiens, Impatiens spp. zidae), has little pest status in Canada (Balsaminaceae), verbena, Verbena spp. compared to other leafminer species. (Verbenaceae), and gloxinia, Sinningia Leafminers are normally not a problem in speciosa (G. Lodd.) Hiern (Gesneriaceae). greenhouse vegetables in Canada. Typical Broad mites are easily confused with other mining damage is caused by larvae feeding tarsonemid mites of which cyclamen mite, between the leaf surfaces. Feeding punc- Phytodromus pallidus (Banks) (Trombidi- tures and egg-laying punctures may also formes: Tarsonemidae), is the most com- cause serious damage in some cases. mon. Damage can be mistaken for a nutrient defi ciency or disease. They feed on the underside of young foliage and on 13.1.5 Spider mites developing fl oral structures, i.e. fl ower buds, retarding growth and preventing Twospotted spider mites, Tetranychus fl owers from fully developing. Leaf damage urticae Koch (Trombidiformes: Tetrany- includes bronzing and distorted, down- chidae), affect many greenhouse crops ward curling of leaves resulting from a including S. lycopersicum, C. sativae, C. phytotoxin secreted by feeding mites. In C. annuum, rose, Rosa spp. (Rosaceae) and annuum, young damaged leaves in the crosses, and many other ornamentals. growing point curl up on the edge. Feeding causes small white or yellow spots Severely infested plants become stunted Chapter 13 101

and may eventually die. Polyphagotarsone- routinely controlled using biological con- mus latus can be dispersed within a green- trol and Bacillus thuringiensis Berliner house by attaching themselves to whitefl ies, serovar kurstaki (Btk) applications. It is greenhouse workers or equip ment, or by probably present in greenhouse production movement of infested plant material into in other Canadian provinces as well. and throughout the green house.

13.1.9 New and potential invasive greenhouse pests 13.1.8 Other greenhouse pests Tuta absoluta (Meyrick) (Lepidoptera: Other frequent greenhouse pests are fungus Gelechiidae), native to South America, is a gnats, Bradysia spp. (Diptera: Sciaridae), potentially devastating pest of greenhouse- which can be relatively easily controlled, grown tomatoes S. lycopersicum. It has not and cabbage loopers, Trichoplusia ni yet been reported in Canada, but it is (Hübner) (Lepidoptera: Noctuidae) (see rapidly invading Europe and the Middle Erlandson, Chapter 42, this volume). There East (Desneux et al., 2010). Tomato plants, are several occasional pests that are tomatoes and used containers are known to disruptive to biological control pro- be high-risk pathways for the introduction grammes because they can only be con- of this pest. trolled by pesticides that are not Brown marmorated stink bug, Halyo- compatible with most commonly-used morpha halys (Stål) (Hemiptera: Penta- biological control agents. These pests tomidae), is a new invasive pest recently include: European corn borer, Ostrinia found in Ontario (T. Gariepy and H. Fraser, nubilalis (Hübner) (Lepidoptera: Pyra- 2012, unpublished results). It has a very lidae); pepper weevil, Anthonomus eugenii wide host range and the potential to affect Cano (Coleoptera: Curculionidae) in vegetable and ornamental crops, although peppers; mealybugs, (primarily citrus it is too soon to predict what its impact mealybug, Planococcus citri (Risso) will be on greenhouse production. Hemiptera: Pseudococcidae); Lygus lineo- Spotted wing drosophila, Drosophila laris (Palisot) (Hemiptera: Miridae) in suzukii (Matsumura) (Diptera: Drosophili- greenhouse-grown C. annuum, C. sativae dae), is another recent invasive pest that and various ornamentals; potato psyllid, has been found in fruit and berry crops in Bactericera cockerelli (Sulc) (Hemiptera: British Columbia, Ontario and Quebec (see Triozidae) in C. annuum and S. Thistlewood et al., Chapter 21, this lycopersicum (see McGregor, Chapter 14, volume). It has the potential to infest and this volume); and cucumber beetles cause damage to greenhouse vegetable Diabro tica spp. (Coleoptera: Chryso- crops such as tomato; however, it is un- melidae) in C. sativae. certain if it will affect Canadian green- Duponchelia fovealis (Zeller) (Lepidop- house production. tera: Crambidae) was found in three Ontario greenhouses in 2005 and was probably introduced on imported plant 13.2 Background material. Duponchelia fovealis has a broad host range and can affect many ornamental Factors associated with grower adoption of crops as well as C. annuum. It can feed on biological control include new compatible leaves, crowns and stems and can bore into pesticides, pesticide resistance, loss of fruit. More importantly, presence of D. registered pesticides and new biological fovealis can lead to trade restrictions for control products. Use of biological control export. Duponchelia fovealis is now well in ornamental crops in Canada has established in ornamental greenhouses in increased dramatically during the past the Niagara region of Ontario, where it is decade with much of the change occurring 102 Chapter 13

since 2007 associated with the develop- selection and use of several natural ment of resistance in thrips to the pesticide enemies together, combined with innova- spinosad (Murphy et al., 2011). Growers tive approaches to enhance their effective- were left with few, if any, pesticide options ness. The use of banker plants and and a pest group, which was formerly the supplemental food are preventative major obstacle to greater use of biological approaches that improve the establishment control, became the primary driver of and persistence of biological control agents change. The switch to biological control of in the greenhouse before the pest becomes thrips necessitated the use of biological a problem. At the crop level, growers are control for other pests as well, due to dealing with multiple pests and benefi cial limited availability of pesticides com- species. Greenhouse crops often harbour patible with the natural enemies used for complex artifi cial food webs. Considerable thrips control (Murphy et al., 2011). In research has been done to elucidate intra- greenhouse vegetables, biological control is guild interactions among the principal an established practice and the challenges biological control agents, most notably are more related to fi ne tuning a biological interactions between various species of control programme or dealing with new predatory mites (Buitenhuis et al., 2010), pests. However, recently there has been a and between microbial biological control tendency to return to more chemical-based agents, nematodes and entomopathogenic strategies, presumably because it is less fungi and various predators and parasitoids complex and because there is a lack of (Shipp et al., 2003, 2012; Jandricic et al., registered insecticides that are truly 2006). Biological control programmes are compatible with natural enemies, due to increasingly emphasizing generalist preda- diffi culties in the Canadian registration tors such as Amblyseius swirskii Athias- system. It is inevitable that, with this Henriot (Mesostigmata: Phytoseiidae), and approach, resistance will again emerge as the potential for interference between an obstacle to effective control. natural enemies is a special concern in In the past, especially in greenhouse greenhouses (Messelink et al., 2012). vegetables, biological control was mainly Biological control systems are starting to used in an inoculative approach, relying on involve the whole value chain, from stock establishment of the biological control plants and cuttings at the propagator and agent through limited releases when pest seedling producers to the retailer and even densities were still low. To reduce the risk customers. It has been shown that pests of failure of establishment of the biological enter Canada on vegetative cuttings control agent and subsequent loss of (Romero, 2011). For example, B. tabaci and control, this approach has been replaced by T. vaporarorium are found on poinsettia inundative strategies using repeated cuttings, and F. occidentalis on chrys- regular releases of natural enemies at high anthemum cuttings. Immersion treatment rates. This produces a moderately im- of the cuttings in hot water, entomo- mediate effect of released biological control pathogenic nematodes, fungi and horti- agents on pest numbers, and this is cultural oil have shown great potential for especially effective in high value crops, control of these hitchhiking pests (Romero, such as ornamentals, which have an 2011). Pesticide residues on cuttings or extremely low pest tolerance. In recent IPM young plants may adversely affect natural strategies in greenhouse crops, the em- enemies, in some cases for a month or phasis has been on developing biological more. Little is known about the toxicity control systems that address multiple and persistence of these residues so levels: at the pest species level, a single avoiding their use is an important strategy biological control agent (the pesticide in the development of biological control paradigm) rarely provides satisfactory systems. This situation is aggravated when levels of control. Pests such as F. pests have been exposed to new active occidentalis are managed through strategic ingredients for a number of years before Chapter 13 103

Canadian growers have access to the same As new greenhouse technologies such as products. As a consequence, pests have artifi cial lighting and photo-selective green- developed resistance against these pesti- house covers or screens are developed to cides, which leaves the grower with promote plant growth, these crop pro- virtually no control options. duction practices are expected to have an Innovative techniques to improve the effect on pests and biological control effi cacy and economics of biological agents (Johansen et al., 2011). On-going control have been developed. For example, research is investigating the use and choice bumblebees, Bombus spp. (Hymenoptera: of biological control agents during different Apidae), can do double duty pollinating seasons and environmental conditions crops and carrying biological control (Shipp et al., 2011). Winter is a diffi cult agents such as the entomopathogenic time to maintain biological control pro- fungus Beauveria bassiana (Balsamo) grammes. Agents perform poorly because Vuillemin (Cordycipitaceae) for control of of diapause, e.g. Orius spp. (Hemiptera: whitefl ies in greenhouse tomatoes Anthocoridae), Aphidoletes spp. (Diptera: (Kapongo et al., 2008). Bee vectoring is Cecidomyiidae), and the effects of low now registered in Canada as a new temperatures and light intensities on application system for B. bassiana. This foraging activity (e.g. Zilahi-Balogh et al., new delivery system is being currently 2006, 2007). expanded for other microbial agents and has been shown to be compatible with parasitoids and predatory mites used in 13.3 Biological Control Agents greenhouse crops (Shipp et al., 2012). Another new technique is the use of trap In comparison to the preceding decades, plants (plants that are more attractive to very few new arthropod agents have been the pest than the crop), which are used to developed for release in Canada. Most new concentrate the pest into a limited area biological control agents in Canada are where they can be controlled or used as a generalist predators. Dicyphus hesperus focal point for the release of natural Knight (Hemiptera: Miridae) is a promising enemies (Shelton and Badenes-Perez, whitefl y and spider mite predator 2006). For example, fl owering Chrys- (McGregor et al., 1999; Bennett et al., anthemum sp. plants as trap plants 2009), but its production has been largely lowered the number of adult F. occidentalis discontinued because of its slow in a vegetative Chrysanthemum crop and establishment in the greenhouse and low reduced crop damage (Buitenhuis et al., adoption rate by growers. However, this 2007). may change with the use of supplemental Biological control has to fi t with all lighting and the adoption of banker-plant aspects of crop production. Integration of approaches for conserving this natural biological control with conventional pesti- enemy (Sanchez et al., 2003). The cides remains an important topic. When specialist parasitoid Eretmocerus mundus intervention with chemical pesticides is Mercet (Hymenoptera: Aphelinidae) has necessary, spot sprays and pesticides that been commercialized to control B. tabaci. are compatible with biological controls are In 2005, A. swirskii was brought onto the chosen to minimize their disruptive effect Canadian market after regulatory approval, on the biological control programme. Also, as a predator of thrips and whitefl ies. when resistance to Btk developed in T. n i Under certain conditions it seems to be a in British Columbia commercial vegetable superior thrips predator than Neoseiulus greenhouses in response to grower spray cucumeris (Oudemans) (Mesostigmata: regimes, the use of insecticidal rotation Phytoseiidae) (Messelink et al., 2006), became an important tool in managing Btk although its cost is still too high for many resistance in greenhouse T. n i populations growers to replace all applications of N. (Janmaat and Meyers, 2003). cucumeris with A. swirskii. Its advantage is 104 Chapter 13

that it attacks a large range of different miner (Murphy, 2010) control. Two entomo- prey species, including spider mites and pathogenic fungi have been registered for broad mites, and it does well on mixed pest control in greenhouses: B. bassiana for diets so it will establish easily in a crop thrips, aphids and whitefl ies and Isaria and will control multiple pests (Messelink fumosorosea (Wize) (Cordycipitaceae) for et al., 2010). The predatory mite whitefl ies. A third, Metarhizium anisopliae Amblydromalus limonicus (Garman and (Metschnikoff) Sorokin (Clavicipitaceae), is McGregor) (Mesostigmata: Phytoseiidae) in the process of label expansion to use was introduced in 2011. It is a predator of against thrips. thrips and whitefl y and is reported to be The recent spate of reclassifi cations of even more effective than A. swirskii on arthropods has resulted in a great many some crops and more active at lower changes in the names of biological control temperatures (Koppert Ltd, 2012). Another agents. Scientifi c name changes of ‘old’ new predator for thrips control in the benefi cial species have created consider- substrate is the staphylinid Dalotia able confusion, and many companies, coriaria (Kraatz) (Coleoptera: Staphyl- consultants and growers are still using the inidae) (Carney et al., 2002). old scientifi c names. Name changes have Amblyseius andersoni Chant (Meso- been implemented for Hypoaspis species: stigmata: Phytoseiidae) is a predatory mite Hypoaspis miles (Berelese) is now Stratio- that is mostly used in outdoor fruit crops, laelaps scimitus (Wormersley) and but it will also prey on T. urticae in the Hypoaspis aculeifer (Canestrini) is Gaeolae- greenhouse. A brown lacewing, Micromus laps aculeifer (Canestrini) (Mesostigmata: variegatus Fabricius (Neuroptera: Hemero- Laelapidae) (Walter and Campbell, 2003; biidae), was collected during a survey Beaulieu, 2009). Atheta coriaria Kraatz has searching for parasitoids of A. solani (S. changed to Dalotia coriaria (Kraatz) (Cole- Acheampong and D. Gillespie, 2010, optera: Staphylinidae) (Klimaszewski, unpublished data) and is now available 2007) and many phytoseiid mite species from a few insectaries for aphid control. have been reclassifi ed: e.g. Neoseiulus Gaeolaelaps gillespiei Beaulieu (Meso- cucumeris (Oudemans) (=Amblyseius cucu- stigmata: Laelapidae) is a recently meris (Oudemans)) and N. californicus described predatory mite of fungus gnat (McGregor) (=Amblyseius californicus larvae and thrips in the substrate (McGregor)), Amblyseius swirskii Athias- (Beaulieu, 2009). It has been used pre- Henriot (=Typhlodromips swirskii (Athias- viously as a biological control for these Henriot)), Iphesius degenerans Berlese targets under the names Hypoaspis sp. nr. (=Amblyseius degenerans (Berlese)), aculeifer (Canestrini) and Gaeolaelaps sp. Typhlo dromalus limonicus (Garman and nr aculeifer (Canestrini) (Mesostigmata: McGregor) (= Amblydromalus limonicus Laela pidae) (Gillespie and Quiring, 1990). (Garman and McGregor)) and Amblyseius Finally, there are several new predatory montdorensis (= Typhlodromips mont- mites for which regulatory approval to dorensis (Schicha)) (Megostigmata: Phyto- import into Canada is being pursued. seiidae). These include Amblyseius montdorensis (Schicha) and Euseius ovalis (Evans) (Mesostigmata: Phytoseiidae). 13.4 Evaluation of Biological Control Several microbial biological controls have become available to Canadian Essentially all greenhouse vegetable growers. The entomopathogenic nematode growers are using biological control and Steinernema feltiae (Filipjev) (Rhabditida: these numbers have not changed notice- Steinernematidae), which was originally ably in recent years. In contrast, a survey of produced and marketed for fungus gnat Canadian ornamentals growers in 2001 control, is now widely used for thrips reported that 26% of growers were using (Buitenhuis and Shipp, 2005) and leaf- biological control specifi cally as part of Chapter 13 105

IPM (Murphy et al., 2002). However, a solani and M. persicae using Aphidius spp. survey in 2010 showed that 90% of these (Hymenoptera: Braconidae) and/or Aphid- growers are currently using biological oletes aphidimyza (Rondani) (Diptera: control (Murphy et al., 2011). As described Cecidomyiidae) is not reliable and there above, much of this increase was driven by are few available insecticides for aphid thrips resistance to registered insecticides. control that are compatible with biological Based on the rapid development of control programmes against other pests. resistance against new pesticides, e.g. spinosad (Reitz, 2009), it is unlikely that the development of new pesticides will 13.5 Future Needs reverse this trend. It is expected that IPM programmes in greenhouse ornamentals Future work should include: and vegetables will be based on biological control with the application of pesticides 1. Developing strategies to start a crop only as a backup or for specifi c aspects of with clean cuttings/transplants with crop production, e.g. fi nal fi nishing, regards to pesticide residues and/or secondary or sporadic pests. imported pests; Franklinella occidentalis and aphids are 2. Improving aphid biological control; the principal industry priorities for 3. Finding natural enemies or biological research on biological control in Canada. control compatible strategies for pests with Thrips research mainly involves fi ne no biological control; tun ing and implementation of the bio- 4. Integration of biological control strate- logical control strategies to make it more gies for different pests, especially general- effective and economically viable. Aphid ist with specialist biological control agents; control has become a key factor in the 5. Developing insecticides products and successful implementation of biological use patterns that are truly compatible with control against all pests. Control of A. use of natural enemies.

References

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Urbaneja, A. (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science 83, 197–215. Gillespie, D.R. and Quiring, D.M.J. (1990) Biological control of fungus gnats, Bradysia spp. (Diptera: Sciaridae), and western fl ower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), in greenhouses using a soil-dwelling predatory mite, Geolaelaps sp. nr aculeifer (Canestrini) (Acari: Laelapidae). Canadian Entomologist 122, 975–983. Gillespie, D.R., Quiring, D.M.J., Foottit, R.G., Foster, S.P. and Acheampong, S. (2009) Implications of phenotypic variation of Myzus persicae (Hemiptera: Aphididae) for biological control on greenhouse pepper plants. Journal of Applied Entomology 133, 505–511. Hodges, G., Edwards, G.B. and Dixon, W. (2005) Chilli thrips Scirtothrips dorsalis Hood (Thysanoptera: Thripidae). A new pest thrips for Florida. Pest Alert. Available at: http://www. doacs.state.fl .us/pi/enpp/ento/chillithrips.html (accessed 23 October, 2012). Jandricic, S., Scott-Dupree, C.D., Broadbent, A.B., Harris, C.R. and Murphy, G. (2006) Compatability of Atheta coriaria with other biological control agents and reduced-risk insecticides used in greenhouse fl oriculture integrated pest management programs for fungus gnats. The Canadian Entomologist 138, 712–722. Janmaat, A.F. and Meyers, J. (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proceedings of the Royal Society of London B 270, 2263–2270. Johansen, N.S., Vänninen, I., Pinto, D.M., Nissinen, A.I. and Shipp, L. (2011) In the light of new greenhouse technologies: 2. Direct effects of artifi cial lighting on arthropods and integrated pest management in greenhouse crops. Annals of Applied Biology 159, 1–27. Kapongo, J-P., Shipp, L., Kevan, P. and Broadbent, B. (2008) Optimal concentration of Beauveria bassiana vectored by bumble bees in relation to pest and bee mortality in greenhouse tomato and sweet pepper. BioControl 53, 797–812. Klimaszewski, J., Assing, V., Majka, C.G., Pelletier, G., Webster, R.P. and Langor, D. (2007) Records of adventives aleocharine beetles (Coleoptera: Staphylinidae: Aleocharinae) found in Canada. The Canadian Entomologist 139, 54–79. Koppert Ltd (2012) http://www.koppert.com/news-biological-systems/biological-control/detail/new- predatory-mite-amblydromalus-limonicus-strengthens-system-in-roses-and-cucumbers (accessed 23 October 2012). McGregor, R., Gillespie, D., Quiring, D. and Foisy, M. (1999) Potential use of Dicyphus hesperus Knight (Heteroptera: Miridae) for biological control of pests of greenhouse tomatoes. Biological Control 16, 104–110. Messelink, G.J., Van Steenpaal, S.E.F. and Ramakers, P.M.J. (2006) Evaluation of phytoseiid predators for control of western fl ower thrips on greenhouse cucumber. BioControl 51, 753–768. Messelink, G.J., van Maanen, R., van Holstein-Saj, R., Sabelis, M.W. and Janssen, A. (2010) Pest species diversity enhances control of spider mites and whitefl ies by a generalist phytoseiid predator. BioControl 55, 387–398. Messelink, G.J., Sabelis, M.W. and Janssen, A. (2012) Generalist predators, food web complexities and biological pest control in greenhouse crops. In: Larramendy, M.L. and Soloneski, S. (eds) Integrated Pest Management and Pest Control – current and future tactics. InTech, Open Access, pp. 191–214. Murphy, G.D. (2010) Leafminer control options. Greenhouse Canada 30(12), 14, 16, 25. Murphy, G.D., Ferguson, G., Fry, K., Lambert, L. Mann, M. and Matteoni, J. (2002) The use of biological control in Canadian greenhouse crops. IOBC/wprs Bulletin Integrated Control in Protected Crops 25, 193–196. Murphy, G.D., Gates, C. and Watson, G.R. (2011) An update on the use of biological control in greenhouse ornamental crops in Canada. IOBC/wprs Bulletin Integrated Control in Protected Crops, Temperate Climate 68, 125–128. Reitz, S.R. (2009) Biology and ecology of the western fl ower thrips (Thysanoptera: Thripidae): the making of a pest. Florida Entomologist 92, 7–13. Romero, R. (2011) Development of reduced risk control strategies for western fl ower thrips and silverleaf whitefl y associated with chrysanthemum and poinsettia cuttings. MSc thesis University of Guelph, Guelph, Canada. Rugman-Jones, P.F., Hoddle, M.S. and Stouthamer, R. (2010) Nuclear-mitochondrial barcoding exposes the global pest western fl ower thrips (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. Journal of Economic Entomology 103, 877–886. Chapter 14 107

Sanchez, J.A., Gillespie, D.R. and McGregor, R.R. (2003) The effects of mullein plants (Verbascum thapsus) on the population dynamics of Dicyphus hesperus (Heteroptera: Miridae) in tomato greenhouses. Biological Control 28, 313–319. Shelton, A.M. and Badenes-Perez, F.R. (2006) Concepts and applications of trap cropping in pest management. Annual Review of Entomology 51, 285–308. Shipp, J.L., Zhang, Y., Hunt, D.W.S. and Fergusson, G. (2003) Infl uence of humidity and greenhouse microclimate on the effi cacy of Beauveria bassiana (Balsamo) for control of greenhouse arthropod pests. Environmental Entomology 32, 1154–1163. Shipp, L., Johansen, N., Vänninen, I. and Jacobson, R. (2011) Greenhouse climate: an important consideration when developing pest management programs for greenhouse crops. Acta Horticulturae 893, 133–143. Shipp, L., Kapongo, J-P., Park, H.-H. and Kevan, P. (2012) Effect of bee-vectored Beauveria bassiana on greenhouse benefi cials under greenhouse cage conditions. Biological Control 63, 135–142. Walter, D.E. and Campbell, N.J.H. (2003) Exotic vs endemic biocontrol agents: would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), please stand up? Biological Control 26, 253–269. Zilahi-Balogh, G.M.G., Shipp, J.L., Cloutier, C. and Brodeur, J. (2006) Infl uence of light intensity, photoperiod, and temperature on the effi cacy of two aphelinid parasiotids of the greenhouse whitefl y. Environmental Entomology 35, 581–589. Zilahi-Balogh, G.M.G., Shipp, J.L., Cloutier, C. and Brodeur, J. (2007) Predation by Neoseiulus cucumeris on western fl ower thrips, and its oviposition on greenhouse cucumber under winter vs. summer conditions in a temperate climate. Biological Control 40, 160–167.

14 Bactericera cockerelli (Sulc), Tomato/ Potato Psyllid (Hemiptera: Triozidae)

Robert R. McGregor Douglas College, New Westminster, British Columbia

14.1 Pest Status 2008) and exceed 80% in tomato (Liu et al., 2006). Since the 1930s, B. cockerelli Bactericera cockerelli (Sulc) (Hemiptera: has been documented to cause ‘psyllid Triozidae), the tomato/potato psyllid, is a yellows’, a disease that may occur due to major pest of fi eld-grown potatoes, So- transmission of a phytotoxin during psyllid lanum tuberosum L., and tomatoes, feeding, but whose causal agent remains Solanum lycopersicum L. (Solanaceae), in unconfi rmed (Pletsch, 1947; Munyaneza et the southern USA and Mexico (Liu et al., al., 2007; Sengoda et al., 2010). Psyllid 2006; Butler et al., 2012). Direct feeding by yellows constitutes a suite of symptoms B. cockerelli can cause yield reductions of including yellow or purple shoots, stunting up to 93% in potato (Munyaneza et al., of shoots, aerial tubers and thickening of © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 108 Chapter 14

internodes (Sengoda et al., 2010). More The morphology of B. cockerelli was recently, B. cockerelli has been shown to described by Pletsch (1947) and Al-Jabr vector a disease called ‘Zebra chip’ (1999). Eggs are oviposited on stalks, often (Munyaneza et al., 2007; Sengoda et al., along the margins of leaves, and are 2010; Buchman et al., 2011), which is oblong-ovate and shiny yellow. There are caused by the newly described Gram- fi ve nymphal instars, which have been negative _-proteobacterium ‘Candidatus reported to range from 12–21 days. Wing Liberibacter psyllaurous’ (Rhizobiaceae) pads are visible in the 3rd instar and (Hansen et al., 2008). Zebra chip disease obvious in the 4th and 5th instars. Adults renders potatoes destined for potato chip are minute (~2 mm in length) with clear or french fry processing unmarketable due wings held roof-like over the body, which to the presence of a striped necrotic pattern has a striped thorax and abdomen. The on tubers that intensifi es after frying host range of B. cockerelli includes plants (Munyaneza et al., 2007; Sengoda et al., in 20 families, but B. cockerelli shows a 2010). preference for feeding on species of Although seasonal northern migration of Solanaceae (Liu and Trumble, 2004, 2006). B. cockerelli into southern Canada has Nymphal development is reported to be been reported historically (presumably due considerably longer on non-solanaceous to dispersal on summer air currents) hosts than on solanaceous hosts (Pletsch, (Pletsch, 1947), this insect has never been a 1947). Overwintering populations origin- serious pest of fi eld crops in Canada. The ating on non-cultivated solanaceous hosts, presence of B. cockerelli in the western e.g. nightshade species, in Texas and USA has also been rare, but serious northern Mexico are thought to migrate infestations of fi eld tomatoes and peppers northward each summer to infest potato were recorded in California and Baja and tomato (Pletsch, 1947; Al-Jabr, 1999). California starting in 2001, caused by a There is no information available regarding genetically distinct, invasive, western migration patterns of the invasive strain of the insect (Liu et al., 2006; Liu California strain of B. cockerelli. and Trumble, 2007). The invasive nature of the California strain of B. cockerelli appears to be mediated by resistance to two insecticides commonly used in tomato 14.2 Background production (imidacloprid and spinosad) (Liu and Trumble, 2007). Damaging Management of B. cockerelli and zebra chip infestations of B. cockerelli on greenhouse- disease on potatoes in the USA has relied grown tomatoes were fi rst recorded in British Columbia in 1996 (Opit, 1998; exclusively on application of insecticides, Sawyer, 2008). An infestation of B. particularly imidacloprid (Butler et al., cockerelli in a single tomato greenhouse in 2012). In California, appli cations of Ontario was also recorded in 2001 (G. imidacloprid are recommended for potatoes Ferguson, Harrow, Ontario, 2012, pers. at planting, and abamectin, spiromesifen comm.). By 2000, the presence of damaging and spinosad are recommended for psyllid infestations of B. cockerelli in British control during the growing season for both Columbia tomato greenhouses was wide- potatoes and tomatoes (University of spread (Sawyer, 2008). Since 2000, occur- California, 2008a, b). In Texas, an integrated rence of this insect in British Columbia pest management (IPM) programme for B. greenhouses has been sporadic with low cockerelli on potatoes has been developed (or no) pest pressure in 2004–2006 and in based on applications of imidacloprid at 2010–2011 (A. Davenport, Langley, British planting and foliar applications of Columbia, 2012, pers. comm.). It is spiromesifen and dinotefuran during the unknown whether the psyllids in British growing season (Goolsby et al., 2007). Columbia greenhouses are from the Resistance to both imidacloprid and invasive western strain of B. cockerelli. spinosad have been detected in California Chapter 14 109

populations of B. cockerelli collected from including Coccinellidae, Chrysopidae, fi eld-grown tomato and pepper (Liu and Nabidae, Syrphidae, Anthocoridae, Trumble, 2007). Miridae and (Pletsch, 1947; Al- A number of insecticides were screened Jabr, 1999). The most prevalent predators for B. cockerelli on greenhouse tomatoes in of B. cockerelli in Montana, USA, were Colorado and the most effective products ladybird beetles, predominantly Hippo- were acetamiprid and spinosad (Al-Jabr, damia convergens (Say) (Coleoptera: 1999). The same study documented Coccinellidae), green lacewings Chrys- signifi cant reductions in B. cockerelli operla spp. (Neuroptera: Chrysopidae) and oviposition after application of the big-eyed bugs, spp. (Hemiptera: repellants Sunspray (paraffi nic oils) and Geocoridae) (Pletsch, 1947). There is no Trilogy (neem oil) (Al-Jabr, 1999). In British information available regarding feeding by Columbia, a number of chemical products generalist predators on B. cockerelli in were screened for B. cockerelli control. The British Columbia. most effective materials identifi ed were diazanon, malathion, naled, parathion, dichlorvos, sulfotepp, Trounce (potassium 14.3 Biological Control Agents salts of fatty acids and pyrethrins), dormant oil and canola oil (Opit, 1998). 14.3.1 Parasitoids Currently in British Columbia, abamectin (Avid) is available for B. cockerelli control Tamarixia triozae was fi rst sold com- through a minor-use label expansion and mercially for psyllid management in June naled (Dibrom) is available for clean-up in 2001 (A. Davenport, 2012, Langley, British pepper greenhouses (T. Hueppelsheuser, Columbia, pers. comm.). In 2001 and 2002, Abbotsford, British Columbia, 2012, pers. augmentative releases of T. triozae were comm.). Since the advent of infestations in made in several British Columbia green- British Columbia greenhouses, growers houses for management of B. cockerelli. have relied on a combination of de-leafi ng These releases resulted in successful and chemical applications for psyllid parasitism and, in some greenhouses, management (A. Davenport, 2012, Langley, suppression of populations of B. cockerelli. British Columbia, pers. comm.). Removal Pest pressure by B. cockerelli in British of culls, prunings and old plants from Columbia greenhouses decreased during greenhouses during clean-up is also 2002 and 2003, and T. triozae was thought to be effective in reducing popu- discontinued in 2003 as a product due to lations in subsequent seasons (A. Daven- lack of market demand (A. Davenport, port, Langley, British Columbia, 2012, pers. Langley, British Columbia, 2012, pers. comm.). comm.). North American fi eld populations of B. After 3 years with no apparent occur- cockerelli are often parasitized by rence of B. cockerelli in British Columbia Tamarixia (Tetrastichus) triozae (Burks) greenhouses (2004–2006), B. cockerelli (Hymenoptera: Eulophidae) (Pletsch, 1947; infestations again became a problem be- Al-Jabr, 1999; Butler and Trumble, 2011). tween 2007 and 2009. Commercial pro- This wasp is widely distributed in North duction of T. triozae was resumed in America and Mexico (Pletsch, 1947; Butler Mexico in 2008, but, although some test and Trumble, 2011). In south-western releases have been made in British British Columbia, collections have been Columbia, this product is not currently made of Tamarixia spp. parasitizing both being distributed in Canada due to a lack of B. cockerelli on sentinel tomato seedlings market demand (A. Davenport, Langley, and unidentifi ed psyllids feeding on sting- British Columbia, 2012, pers. comm.). ing nettle, Urtica dioica L. (Urticaceae). Virtually no B. cockerelli were observed in A range of generalist predators has been British Columbia greenhouses in 2010 and reported to feed upon B. cockerelli, 2011. 110 Chapter 14

14.3.2 Predators caused substantially higher mortality of B. cockerelli nymphs (95–99%) than B. Although several taxa of generalist preda- bassiana (53–78%) (Lacey et al., 2009). tors have been recorded to feed on B. Lacey et al. (2009) suggested that B. cockerelli (Pletsch, 1947; Al-Jabr, 1999), bassiana still has considerable potential as few augmentative releases of predators for a B. cockerelli control product, and that the psyllid control have been attempted. Two lower performance of B. bassiana in this species of green lacewing, Chrysoperla study could be explained by characteristics carnea (Stephens) and Chrysoperla of the strain used (a low germination rate rufi labris (Burmeister) (Neuroptera: Chrys- and adaptation to its original host, Cydia opidae), could complete their life cycles on pomonella (L.) (Lepidoptera: Tortricidae)). a diet of B. cockerelli, but releases of one (C. carnea eggs) on infested potatoes failed to reduce psyllid populations in the fi eld 14.4 Evaluation of Biological Control (Al-Jabr, 1999). Releases of high numbers of Dicyphus hesperus Knight (Hemiptera: Augmentative releases of T. triozae were Miridae) were successful in managing a considered to be an effective tool for population of B. cockerelli in a small management of B. cockerelli populations in research greenhouse (D. Gillespie, Agassiz, British Columbia greenhouses during the British Columbia, 2012, pers. comm.). period of time when this parasitoid was Despite this initial success, predation rates available to growers. Although generalist by both D. hesperus and another mirid predators have not, to date, been predator, Deraeocoris brevis (Uhler) adequately tested to make any reasonable (Hemiptera: Miridae), (measured in Petri- evaluation of their effi cacy, a number of dish feeding trials and releases on infested taxa may have potential for biological seedlings in cages) were extremely low, control of B. cockerelli. Similarly, fungal and further development of these predators pathogens have been shown to have for B. cockerelli management has not been potential for management of B. cockerelli pursued. populations, but no testing has been done under operational conditions in BC greenhouses. 14.3.3 Pathogens 14.5 Future Needs There has been little evaluation of micro- bial biological control products versus B. Bactericera cockerelli is not currently a cockerelli, although there may be strong pest in British Columbia vegetable green- potential for their use. Three fungal houses. Bactericera cockerelli were virtu- pathogens were tested against B. cockerelli ally undetectable in greenhouses in the on psyllid-infested leaves of greenhouse- 2010 and 2011 growing seasons (A. Daven- grown tomatoes (Al-Jabr, 1999). Of these, port, Langley, British Columbia, 2012, pers. Beauveria bassiana (Balsamo) Vuillemin comm.). Despite this, further work should (Cordycipitaceae) and Metarhizium ani- include: sopliae (Metschnikoff) Sorokin (Clavi- cipitaceae) were both effective at reducing 1. Monitoring populations of B. cockerelli psyllid populations on tomato leaves, but in British Columbia in both greenhouses Verticillium lecanii (Zimmerman) Viégas and fi eld crops, perhaps through coordin- (Plectosphaerellaceae) caused little mortal- ation of information available from pest ity (possible due to inappropriate environ- management consultants, because British mental conditions during the trial) (Al-Jabr, Columbia populations of B. cockerelli have 1999). In laboratory bioassays on excised fl uctuated widely since this insect was fi rst potato leaves, both M. anisopliae and Isaria detected in a greenhouse in 1996 and will fumosorosea (Wize) (Cordycipitaceae) likely continue to do so; Chapter 14 111

2. Further evaluation of parasitoids, preda- and further efforts to evaluate potential tors and pathogens of B. cockerelli as this biological control agents are strongly pest will likely re-emerge as a problem in warranted. the future; 3. Determining the potential incidence and importance of this pest in Canada under Acknowledgements global climate change, because there is sub- stantial potential for B. cockerelli to Many thanks to Andrea Davenport become not only a greenhouse pest in (Koppert Canada Ltd), Gillian Ferguson Canada but a pest of fi eld crops such as (Ontario Ministry of Agriculture, Food and potato, tomato and pepper, Capsicum ann- Rural Affairs), Dave Gillespie (Agriculture uum L. (Solanaceae), and a vector of zebra & Agri-Food Canada) and Tracy Hueppels- chip disease. heuser (British Columbia Ministry of Clearly, B. cockerelli has considerable Agriculture) for providing unpublished potential as an agricultural pest in Canada information on tomato psyllid.

References

Al-Jabr, A. (1999) Integrated pest management of tomato/potato psyllid Paratrioza cockerelli (Sulc) (Homoptera: Psyllidae) with emphasis on its importance in greenhouse grown tomatoes. PhD Dissertation, Colorado State University, Fort Collins, CO, USA. Buchman, J.L., Heilman, B.E. and Munyaneza, J.E. (2011) Effects of Liberibacter-infective Bactericera cockerelli (Hemiptera: Triozidae) density on zebra chip potato disease incidence, potato yield, and tuber processing quality. Journal of Economic Entomology 104, 1783–1792. Butler, C.D. and Trumble, J.T. (2011) New records of hyperparasitism of Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) by Encarsia spp. (Hymenoptera: Aphelinidae) in California. Pan- Pacifi c Entomologist 87, 130–133. Butler, C.D., Walker, G.P. and Trumble, J.T. (2012) Feeding disruption of potato psyllid, Bactericera cockerelli, by imidicloprid as measured by electrical penetration graphs. Entomologia Experimentalis et Applicata 142, 247–257. Goolsby, J.A., Adamczyk, J., Bextine, B., Lin, D., Munyaneza, J.E. and Bester, G. (2007) Development of an IPM program for management of the potato psyllid to reduce incidence of zebra chip disorder in potatoes. Subtropical Plant Science 59, 85–94. Hansen, A.K., Trumble, J.T., Stouthamer, R. and Paine, T.D. (2008) A new Huanglongbing species, ‘Candidatus Liberibacter psyllaurous,’ found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Applied and Environmental Microbiology 74, 5862–5865. Lacey, L.A., de la Rosa, F. and Horton, D.R. (2009) Insecticidal activity of entomopathogenic fungi (Hypocreales) for potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae): development of bioassay techniques, effect of fungal species and stage of the psyllid. Biocontrol Science and Technology 19, 957–970. Liu, D. and Trumble, J.T. (2004) Tomato psyllid behavioral responses to tomato plant lines and interactions of plant lines with insecticides. Journal of Economic Entomology 97, 1078–1085. Liu, D. and Trumble, J.T. (2006) Ovipositional preferences, damage thresholds, and detection of the tomato/potato psyllid (Bactericera cockerelli (Sulc)) on selected tomato accessions. Bulletin of Entomological Research 96, 197–204. Liu, D. and Trumble, J.T. (2007) Comparative fi tness of invasive and native populations of the potato psyllid (Bactericera cockerelli). Entomologia Experimentalis et Applicata 123, 35–42. Liu, D., Trumble, J.T. and Stouthamer, R. (2006) Genetic differentiation between eastern populations and recent introductions of potato psyllid (Bactericera cockerelli) into Western North America. Entomologia Experimentalis et Applicata 118, 177–183. Munyaneza, J.E., Crosslin, J.M. and Upton, J.E. (2007) Association of Bactericera cockerelli (Homoptera: Psyllidae) with ‘Zebra Chip,’ a new potato disease in southwestern United States and Mexico. Journal of Economic Entomology 100, 656–663. 112 Chapter 15

Munyaneza, J.E., Buchman, J.L., Upton, J.E., Goolsby, J.A., Crosslin, J.M., Bester, G., Miles, G.P. and Sengoda, V.G. (2008) Impact of different potato psyllid populations on zebra chip disease incidence, severity, and potato yield. Subtropical Plant Science 60, 27–37. Opit, G. (1998) Development of pest management strategies for potato psyllid, Paratrioza cockerelli, in greenhouse crops. Pro-tect Department of Coast Agri, unpublished report. Pletsch, D.J. (1947) The potato psyllid Paratrioza cockerelli (Sulc), its biology and control. Montana Agricultural Experiment Station Bulletin 446. Sawyer, N. (2008) Biology and impact of potato psyllid (Bactericera cockerelli) on greenhouse tomatoes and peppers. E.S. Cropconsult Ltd., unpublished report to British Columbia Ministry of Agriculture and Lands and British Columbia Greenhouse Growers Association. Sengoda, V.G., Munyaneza, J.E., Crosslin, J.M., Buchman, J.L. and Pappu, H.R. (2010) Phenotypic and etiological differences between psyllid yellows and zebra chip diseases of potato. American Journal of Potato Research 87, 41–49. University of California (2008a) Potato psyllid, Bactericera cockerelli, UC IPM Online. Available at: http://www.ipm.ucdavis.edu/PMG/r607300811.html (accessed 25 September 2012). University of California (2008b) Tomato psyllid, Bactericera cockerelli, UC IPM Online. Available at: http://www.ipm.ucdavis.edu/PMG/r783303011.html (accessed 25 September 2012).

15 Cephus cinctus Norton, Wheat Stem Sawfl y (Hymenoptera: Cephidae)

Héctor Cárcamo and Brian Beres Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, Alberta

15.1 Pest Status reviewed by Beres et al. (2011a). The species was described from a specimen The wheat stem sawfl y, Cephus cinctus collected from native grass in Colorado Norton (Hymenoptera: Cephidae), has been (Norton, 1872). Comstock (1889) fi rst a major pest of wheat, Triticum aestivum L. reported a related species of stem sawfl y (Poaceae), in the northern Great Plains of Cephus pygmaeus (L.) (Hymenoptera: North America for more than 100 years. Tenthridinidae) as a pest of T. aestivum in Within this geographical region the areas northern New York. Cephus cinctus was prone to attack are southern Alberta and fi rst observed infesting wheat in Canada in Saskatchewan, south-western Manitoba, 1895 near Souris, Manitoba and Indian eastern and northern Montana, North Head, Saskatchewan (Fletcher, 1896). Dakota, northern South Dakota, western Reports of C. cinctus infestations followed Minnesota, Colorado and Nebraska. Wheat the westward movement of wheat stem sawfl y biology and management was production across the Canadian prairies © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 15 113

and the northern states of North Dakota producers can decide on the need to plant and Montana (Fletcher, 1904; Ainslie, solid-stemmed cultivars, which remain a 1920). By 1910, infestations of wheat stem key component of sawfl y management. sawfl y were reported as far west as Furthermore, a neural network predictive Claresholm, Alberta (Holmes, 1979). model allows growers to estimate potential Yield losses from C. cinctus result from sawfl y damage to solid pith cultivars larvae mining the wheat stems and lodging based on climatic variables that reduce upon girdling the stem when it builds its pith expression (ftp://ftp.agr.gc.ca/pub/out overwintering chamber at the base. These going/bb-stb) and the need to swath or use losses are signifi cant and can reach specialized harvesting equipment. Other millions of dollars per year in the region agronomic strategies include continuous during outbreak years (Beres et al., 2007). cropping with appropriate pre-seed Wheat cultivars with solid pith are widely residue management (Beres et al., 2011c), planted (DePauw et al., 2005) and reduce seeding rates no greater than 300 seeds damage and negatively affect sawfl y fi tness m−2, fertilizer management with 30 to 60 (Cárcamo et al., 2005). Cephus cinctus kg N ha−1 (Beres et al., 2011d) and harvest outbreaks are likely ended by a combin- cut ting heights of at least 15 cm to ation of factors including the weather and enhance overwintering survivorship of interaction with natural enemies and use of parasitoids (Beres, 2011; Beres et al., solid pith cultivars. 2011b). Few parasitoids attack C. cinctus in Canada or the junior synonym C. hyalin- 15.2 Background atus Konow (Hymenoptera: Cephidae) in Eurasia. Eight species of Hymenoptera are There are multiple factors that contributed known to parasitize C. cinctus in Canada to a resurgence of C. cinctus (Beres et al., (Meers, 2005; Morrill et al., 1998) (Table 2011a). Monoculture wheat production 15.1). Ainslie (1920) and Criddle (1923) provides C. cinctus with an abundance of reported parasitoids of C. cinctus larvae in nearby hosts each spring when the pest grass stems but not in wheat stems and emerges from the previous year’s infested only two of the nine parasitoids have been stubble. Many producers are reluctant to recorded in C. cinctus populations in rotate into immune broad-leaf crops as wheat (Morrill et al., 1998). However, a continuous wheat production provides thorough survey of parasitoids of Asian relatively low economic risk and higher Cephidae remains to be done (Shanower returns compared to other cropping and Hoelmer, 2004). Braconidae are the systems in semi-arid regions (Zentner et most important C. cinctus parasitoids and al., 2006). Continuous or wheat–fallow only B. cephi causes signifi cant mortality systems in association with dry weather in cultivated fi elds (Runyon et al., 2002). cycles further enhance C. cinctus popu- This species is widespread throughout the lations while wet weather patterns tend to range of C. cinctus in the Canadian prairies inhibit reproduction (Wallace and McNeal, and adjacent areas in the USA. A closely 1966) and enhance parasitism by Bracon related species, Bracon lissogaster Muese- cephi Gahan (Hymenoptera: Braconidae) beck (Hymenoptera: Braconidae), is also (Holmes et al., 1963). common in the USA (Somsen and A comprehensive decision support sys- Luginbill, 1956) and is present in southern tem has been developed to reduce wheat Alberta (Cárcamo et al., 2012). Both species stem sawfl y damage (Beres et al., 2011b). It are idiobiont, larval ectoparasitoids with consists of diligent pest surveillance that two generations of adults per year. They allows risk assessment of pest damage overwinter as mature larvae inside grass through online maps (Meers and Barkley, stems above ground and have similar 2012). These maps are updated annually biology except that B. lissogaster is before the planting season so that gregarious. 114 Chapter 15 . (2006); et al (2012); Muesebeck (1953) et al. Noyes (2011) Noyes (2011) (1953); Meers (2005) Nelson (1953); Noyes (2011) Nelson (1953) ; Gibson Nelson (1953); Noyes (2011) Nelson (1953); Noyes (2011) Salt (1931); Holmes (1953) Criddle (1924); Nelson and Farstad Neilson (1949); Noyes (2011) Morocco, Russia, South Africa, USA Africa, USA Morocco, Russia, South (widespread) Eurasia (widespread), New Zealand, North (widespread) Africa, UK, USA (DE, MD, NJ, NY, ND, OH, OR, PA, TN, WA) ND, OH, OR, PA, (DE, MD, NJ, NY, (CA, ID, MA, MI, Eurasia (widespread), UK, USA WA) OR, PA, MN, NH, NY, MN, MO, MT, NE, ND, SD, UT, WY) NE, ND, SD, UT, MN, MO, MT, (widespread), UK, USA (IN, ME, MT, ND, UT) (IN, ME, MT, (widespread), UK, USA (widespread), Russia , UK, USA (widespread, (widespread), Russia , UK, USA north and central) Holarctic: Canada (PEI, QC, SK), Europe Holarctic: Holarctic: Canada (MB, ON, PEI), Hawaii, Mexico, Holarctic: SK), Canada (AB, BC, NB, NS, ON, QP, Holarctic: Holarctic: Canada (AB, SK), Morocco, Russia, USA Canada (AB, SK), Morocco, Russia, USA Holarctic: Canada (AB, BC, NB, NS, ON QC), Holarctic: Nearctic: Canada (AB, BC, MB, SK), USA (IA, KS, Canada (AB, BC, MB, SK), USA Nearctic: Canada (AB), USA (MT)Canada (AB), USA Canada (AB, MB, SK), Eurasia Holarctic: Cárcamo polyphagous , , , , , , , polyphagous , polyphagous , polyphagous , polyphagous cinctus cephi . . in Canada, their host range and distribution. C B B. cephi B. cephi C. cinctus C. cinctus C. cinctus B. cephi C. pygmaeus, C. cinctus C. cinctus C. cinctus polyphagous C. cinctus =Eupelmus Crawford] Cephus cinctus [

Girault] (Girault) (Holmgren) (Retzius) Muesebeck

Holmgren] utahensis (French) (Walker) (Walker)

Gahan

a (Gahan) . (2006) provided the new nomenclatural combination for this species Parasitoids of Parasitoids (French)] et al Pleurotropis Merisus febriculosus detrita allynii [ [= [= Gibson Parasitoid Host rangeDistributionParasitoid Host Reference Eupelmus vesicularis Eurytomidae Eurytoma atripes Ichneumonidae Endromopoda detrita Pteromalidae Homoporus febriculosus Table 15.1. Table Braconidae Bracon cephi a Eupelmidae Brasema allynii Bracon lissogaster Eulophidae Pediobius eubius Chapter 15 115

Although Ichneumonidae (Hymen- C. cinctus (Meers, 2005). Adults and larvae optera) are the dominant parasitoids of forage within the stem and larvae can Cephidae in Eurasia, only one species overwinter inside cocoons and cadavers of attacks C. cinctus in Canada. Endromopoda C. cinctus in plant stubs, leaving char- detrita (Holmgren) (Hymenoptera: Ichneu- acteristic large, irregular exit holes on the mondiae) has been reared from C. cinctus top of the stubs in the spring (Morrill et al., from southern Alberta (Holmes et al., 2001). Cárcamo et al. (2011) noted isolated 1963). Rates of attack for this species are occurrences of up to 5% mortality of C. very low but are likely underestimated. cinctus by this beetle. The role of other This species also attacks agromyzid fl ies predators has not been explored. (Diptera: Agromyzidae) and C. pygmaeus Pathogens can kill moderate proportions and Trachelus tabidus (Fabricius) (Hymen- of C. cinctus populations. So far, a complex optera: Cephidae) in the USA and Europe of well-known phytopathogens, Fusarium (Shanower and Hoelmer, 2004). pseudograminearum O’Donnell & T. Aoki, The other parasitoids reared from C. F. culmorum (Wm. G. Sm.) Sacc., F. avena- cinctus in Canada belong to the superfamily ceum (Fries) Saccardo and F. acuminatum Chalcidoidea but only one, Pediobius Ell. and Ev. sensu Gordon (Nectriaceae), eubius (Walker) (= Pleutropis utahensis has been demonstrated to kill larvae inside (Crawford)) (Hymenoptera: Eulophidae), the stems in controlled and fi eld studies in seems to exploit C. cinctus as a primary Montana, USA (Wenda-Piesik et al., 2009). host. Neilson (1949) described its life cycle In southern Alberta, a study of over- in southern Alberta and noted over 50% wintering mortality of C. cinctus in relation parasitism in roadside grass habitats, in to host plant resistance noted that up to Bromus and Agropyron species (Poaceae) 16% of larvae appeared to be killed by but only 1–2% in adjacent wheat fi elds. fungi (Cárcamo et al., 2011). Criddle (1924) recognized early on the occurrence of hyperparasitoids and reported Brasema allynii (French) (Hymenoptera: 15.3 Biological Control Agents Eupelmidae) as a secondary parasite attacking B. cephi. A related species, Only one species has been released against Eupelmus vesicularis (Retzius) (Hymen- C. cinctus in Canada. Collyria coxator optera: Eupelmidae), is a wingless (Villers) (=Collyria calcitrator (Graven- facultative hyperparasitoid of C. cinctus and horst)) (Hymenoptera: Ichneumonidae), B. cephi that has 3–4 generations that reared from C. pygmaeus, was imported develop on whichever host is available from England and released near Swift (Nelson and Farstad, 1953). Eurytoma Current, Saskatchewan (50.2833°, atripes Gahan (Hymenoptera: Eurytomidae) −107.75°) in 1930, but did not become is another opportunistic winged hyper- established (Smith, 1931). A second parasitoid with a very similar life cycle also attempt 30 years later used material from reported by Nelson and Farstad (1953) from continental Europe. On 28 June 1960, 119 southern Alberta. Nelson and Farstad (1953) adult C. coxator from Chernovsky, Russia, reared a single male of Homoporus were released near Lethbridge (49.35°, febriculosus (Girault) (=Merisus febriculosus −112.39°) and several hundreds of adults Girault) (Hymenoptera: Ichneumonidae) of this species from Sweden and Ukraine from a B. cephi cocoon and concluded that were also released that same year near this species was also a hyperparasitoid. Swift Current (Smith, 1961). An earlier Natural enemies of C. cinctus include release of this species in Montana and the predatory beetle Phyllobaenus dubius North Dakota from 1952 to 1954 also failed (Wolcott) (Coleoptera: Cleridae), which can (Turnbull and Chant, 1961). However, this occasionally infl ict moderate mortality to parasitoid was established from releases in C. cinctus (Morrill et al., 2001; Beres et al., 1940 in south central Ontario (44.15°, 2009) and occurs throughout the range of −77.8°) (Smith, 1959) and it is considered 116 Chapter 15 effective against the European wheat stem 15.4 Evaluation of Biological sawfl y, C. pygmaeus (Turnbull and Chant, Control 1961). Collyria species are koinobiont endoparasitoids that track the sawfl y life The only attempt to control C. cinctus cycle starting at the egg stage and through the release of Collyria coxator eventually emerge the following spring failed both in Canada and the USA. This from the mature sawfl y larva (Salt, 1931). parasitoid seems to be specifi c to C. Collyria catoptron Wahl (Hymenoptera: pygmaeus, which was the host used to rear Ichneumonidae) was recently described the specimens released against C. cinctus from the arid grasslands of northern China in the Canadian release (McLeod, 1962). In and it is considered a candidate for eastern North America C. coxator has biological control of C. cinctus in the successfully controlled C. pygmaeus Northern Great Plains of North America (Turnbull and Chant, 1961). Smith (1959) (Wahl et al., 2007). suggested that C. coxator failed in western Several studies have been conducted to Canada because of poor host suitability – improve conservation biological control of as pointed out by McLeod (1962), C. C. cinctus by B. cephi in Canada and the pygmaeus and not C. cinctus is its native USA. Annual variability in its effi cacy host. Another possible factor for the failure against C. cinctus populations has been in Lethbridge was the small size of the attributed to the late emergence of the release. Furthermore, the health of the second generation when mature C. cinctus adults may have been compromised while larvae are at the base of the plant and less being transported from eastern laboratories vulnerable to attack (Nelson and Farstad, to the western sites (Shanower and 1953). Holmes et al. (1963) suggested that Hoelmer, 2004). two successive years of cool and wet growing conditions that caused late plant maturity resulted in high levels of parasitism by the second generation in the 15.5 Future Needs third year. Hence, early maturing cultivars may be detrimental to B. cephi. Tillage, Future work should include: particularly aggressive soil disturbance, also reduces parasitoid populations without 1. A comprehensive revision of Holarctic controlling C. cinctus (Runyon et al., 2002). Cephus spp., using molecular taxonomic Less aggressive light tillage appeared to techniques to resolve the phylogeny of reduce the negative impact on B. cephi Eurasian and North American Cephidae (Beres et al., 2011c). Meers (2005) and Beres and test the hypothesis (Ivie, 2001) that C. (2011) demonstrated that harvesting wheat cinctus invaded western North America via by leaving stubble as high as possible, for Russian immigrants, and its synonymy example using a head-stripper, results in with C. hyalinatus; higher B. cephi populations. Another 2. Explore for more effective natural ene- strategy to conserve B. cephi populations is mies from Eurasian Cephus spp. from to use mixtures of solid- and hollow- appropriate climatic zones, considering stemmed cultivars rather than monocultures that species of Ichneumonidae such as of the former (Beres, 2011). In the Canadian Collyria catoptron currently under evalua- Prairies, solid-stemmed cultivars do not tion by the USDA may complement have a direct negative impact on B. cephi as endemic parasitoids and improve biologi- observed in north-eastern Montana (Rand et cal control of C. cinctus in Canada; al., 2012), but do reduce B. cephi 3. Conduct basic research to understand populations indirectly by limiting the the unsuccessful adaptation by native para- number of available hosts (Wu et al., 2012). sitoid species to cereal crop habitats. Chapter 15 117

References

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16 Ceutorhynchus obstrictus (Marsham), Cabbage Seedpod Weevil (Coleoptera: Curculionidae)

Tim Haye,1 Peter G. Mason,2 Lloyd M. Dosdall,3 Dave R. Gillespie,4 Gary A.P. Gibson2 and Ulrich Kuhlmann1 1CABI, Delémont, Switzerland; 2Agriculture and Agri-Food Canada, Ottawa, Ontario; 3University of Alberta, Edmonton, Alberta; 4Agriculture and Agri-Food Canada, Agassiz, British Columbia

16.1 Pest Status 1948; Crowell, 1952; McCaffrey, 1992; Dosdall and Dolinski, 2001). It was The cabbage seedpod weevil, Ceutorhyn- reported from southern Quebec and chus obstrictus (Marsham) (= C. assimilis Ontario in 2001 (Brodeur et al., 2001; (Paykull)) (Coleoptera: Curculionidae), an Mason et al., 2004, 2011). The Quebec invasive alien species of European origin, population is likely due to a second is an important pest of canola, Brassica introduction (Laffi n et al., 2005). Bio- napus L. and B. rapa L. (Brassicaceae) in climatic models predict that C. obstrictus western and eastern Canada (Dosdall and will eventually be present throughout the Mason, 2010). First detected in Vancouver, entire region of canola production in British Columbia in 1931 (McLeod, 1962), western Canada (Dosdall et al., 2002; Olfert the source was likely western or northern and Weiss, 2006; Cárcamo et al., 2009). Europe (Laffi n et al., 2005). By 1995, C. Each C. obstrictus larvae consumes 5–6 obstrictus had dispersed into the USA canola seeds (Bonnemaison, 1957) and Pacifi c Northwest, California, the south- reduces yield of a pod by about 18% eastern USA and Alberta (Hanson et al., (Williams and Free, 1978). In Europe, © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 120 Chapter 16

losses in winter canola fi elds are about 4% perimeter trap crop, B. rapa fl owered if plants are infested with one adult weevil approximately 1 week before canola and per plant (Williams, 2010). In North concentrated C. obstrictus adults effec- America, C. obstrictus larvae can cause 15– tively, and the trap crop was sprayed with 35% yield losses in winter canola fi elds insecticides to prevent migration into the not treated with insecticides (McCaffrey et main crop (Cárcamo et al., 2007). During al., 1986; Buntin, 1999). Outbreaks of C. the early pod stage, trap crops become less obstrictus in southern Alberta and effective and C. obstrictus adults were no Saskatchewan in 1999 resulted in crop longer retained in the trap crop area (Cook losses of approximately CAN$1m (Kuhl- et al., 2004). Later seeding in spring and mann et al., 2002). Estimated annual costs high plant densities can help reduce C. to the Canadian canola industry are obstrictus infestations and damage (Dosdall approximately CAN$5m (Colautti et al., et al., 2006a). 2006). Genetic lines of canola resistant to C. In Canada, reproductively immature C. obstrictus have been developed through obstrictus adults emerge from over- introgression of white mustard, Sinapsis wintering sites from the end of May to mid- alba L. (Brassicaceae), to B. napus (Dosdall June (Ulmer and Dosdall, 2006). Adults and Kott, 2006; Tansey et al., 2010a). feed fi rst on brassicaceous weeds and Resistance is expressed as reduced C. volunteer crop plants (Fox and Dosdall, obstrictus feeding and oviposition (anti- 2003), then migrate into canola crops at the xenosis) and longer larval development bud to early fl ower stage (Dosdall and time and reduced larval frass (antibiosis) Moisey, 2004). Female C. obstrictus must (McCaffrey et al., 1999; Dosdall and Kott, feed on buds, racemes, fl owers or siliques 2006; Tansey et al., 2010a). In addition, C. of host plants for 2–3 weeks to develop obstrictus are less responsive to visual and their ovaries (Ni et al., 1990) and can infl ict olfactory cues associated with resistant damage by causing racemes to bear few genotypes (Tansey et al., 2009, 2010b). siliques (Dosdall et al., 2001). Repro- Mixed cropping strategies, and planting C. ductively mature females usually oviposit obstrictus-susceptible and -resistant geno- single eggs into young, developing siliques types in alternating strips, resulted in some (Free and Williams, 1978). Larvae pass degree of associational resistance, and through three instars in 2–3 weeks, and deterred attack by C. obstrictus on sus- mature larvae exit the silique and pupate ceptible canola genotypes. However, newly below the soil surface. The new adults developed canola genotypes can still emerge 2–4 weeks later, in mid-August, support larval development and colon- and feed on late maturing siliques or ization (Tansey et al., 2010a). fl owers of secondary shoots (Dosdall et al., Little evidence of parasitism of C. 2001). obstrictus adults or larvae was uncovered during its invasion of western Canadian canola crops (Kuhlmann et al., 2002). 16.2 Background Microctonus melanopus (Ruthe) (Hymen- optera: Braconidae) was reared and Apart from biological control, C. obstrictus dissected from C. obstrictus adults in is controlled by chemical insecticide appli- southern Alberta in 2000 and 2001, and cations, cultural strategies and host plant adults were also collected in sweep net resistance (Dosdall and Mason, 2010). samples from canola near Creston, British Foliar insecticides are applied at a Columbia (Fox et al., 2004). However, threshold of 3–4 adult weevils per sweep at parasitism of adult C. obstrictus was 10–20% fl ower (Dosdall et al., 2001; less than 10% (Fox et al., 2004), compared Cárcamo et al., 2005). with 71% in Idaho, USA (Harmon Trap crops can be an alternative to and McCaffrey, 1997) and 60% in insecticide applications. Planted as a Europe (Bonnemaison, 1957). Microctonus Chapter 16 121

melan opus also parasitizes Ceutorhynchus America (Table 16.1). In British Columbia, quadridens (Panzer) and Ceutorhynchus greatest parasitism was by Trichomalus assimilis (Paykull) (=Ceutorhynchus pleuro- lucidus (Walker) and Stenomalina gracilis stigma (Marsham)) in Europe (Jourdheuil, (Walker) (Hymenoptera: Pteromalidae) 1960). The parasitoid has limited potential (Gillespie et al., 2006). A diverse as a biological control agent in western assemblage of larval idiobiont parasitoids Canada. Microctonus melanopus can com- has been reared from C. obstrictus larvae in plete two generations per year and its southern Alberta, Saskatchewan, Ontario weevil host is univoltine (Harmon and and Quebec, some 20 Chalcidoidea species McCaffrey, 1997), but parasitoid popu- representing fi ve families (Gibson et al., lations did not increase in southern Alberta 2005; Dosdall et al., 2006b, 2007, 2009; from 2002 to 2005 (L.M. Dosdall, 2012, Mason et al., 2011). Mason et al. (2011) unpublished results). reported Trichomalus perfectus (Walker) The Chalcidoidea parasitoid commun- (Hymenoptera: Pteromalidae) for the fi rst ities associated with C. obstrictus differ time from eastern Canada, a noteworthy between eastern and western North discovery because Kuhlmann et al. (2002)

Table 16.1. Species composition of Chalcidoidea parasitoids reared from collections of siliques of Brassica napus and B. rapa and putatively associated with Ceutorhynchus obstrictus in British Columbia (2005), southern Alberta and Saskatchewan (2003–2005), and Ontario and Quebec (2007).

British Columbiaa Alberta/Saskatchewanb Ontario/Quebecc Chalcididae Conura albifrons (Walsh) + + + Conura torvina (Cresson) – + – Eulophidae Euderus albitarsus (Zetterstedt)d –++ Euderus glaucus Yoshimoto – – + Necremnus tidius (Walker) d ++ + Unidentifi ed taxa – – + Eupelmidae Eupelmus vesicularis (Retzius) d +– + Eurytomidae Eurytoma tylodermatis Ashmead + + + Pteromalidae Catolaccus aenoviridis (Girault) – + – Chlorocytus sp. – + + Lyrcus incertus (Ashmead) – + + Lyrcus maculatus (Gahan) – + + Lyrcus perdubius (Girault) – + + Mesopolobus gemellus Baur and Muller – – + Mesopolobus bruchophagi Gahan – + – Mesopolobus moryoides Gibson + + + Mesopolobus sp. + – – Pteromalus spp.d –++ Stenomalina gracilis (Walker) e +– – Trichomalus lucidus (Walker) e ++ + Trichomalus perfectus (Walker) – – + aGillespie et al. (2006); bDosdall et al. (2009); cMason et al. (2011); dat least two undescribed species; ePalaearctic. 122 Chapter 16

considered T. perfectus a potential of Europe (Murchie, 1996; Haye et al., candidate for biological control of C. 2010). obstrictus in Canada. The importance of ground-dwelling The North American Chalcidoidea fauna predators is still not well understood of C. obstrictus comprises species with (Büchs and Nuss, 2000), although general- both Nearctic and Holarctic distributions ist predators, such as Amara aenea Degeer, (Dosdall et al., 2009; Mason et al., 2011). A. ovata Fabricius, A. similata Gyllenhal, Some species are restricted in their host dorsalis Pontoppidan, Poeci- ranges; for instance, T. lucidus is known to lus cupreus L., madidus parasitize larvae in the (Fabricius), P. melanarius (Illiger) almost exclusively. The discovery that T. (Coleoptera: Carabidae), may be important lucidus and N. tidius parasitized the (Warner et al., 2008; Zaller et al., 2009; indigenous Nearctic Ceutorhynchus neglec- Haye et al., 2010). Conservation biological tus Blatchley (Coleoptera: Curculionidae) control strategies to enhance naturally suggests that the parasitoids have ex- occurring populations of carabids in canola panded their host ranges to exploit the fi elds may help reduce C. obstrictus abundant resource of C. obstrictus larvae in populations in Europe and Canada. canola siliques in western Canada (Dosdall Little is known about the impact of soil- et al., 2007). Other parasitoids appear to be borne pathogens, such as nematodes, more niche- than taxon-specifi c because bacterial diseases, or entomopathogenic they can attack a wide range of hosts from fungi on C. obstrictus populations. In different insect orders and families general, entomopathogenic nematodes and (Dosdall et al., 2009). fungi abundances in the soil of European In Europe C. obstrictus is attacked by at canola fi elds were too low to cause least 31 species of parasitoids, mostly signifi cant infections of canola pests larval ectoparasitoids, of which three, T. (Vänninen et al., 1989; Zec-Vojinovic et al., perfectus, Mesopolobus morys (Walker) 2006), and thus their impact on C. and S. gracilis (Hymenoptera: Ptero- obstrictus pupae is considered low. malidae), were identifi ed as key biological control agents (Ulber et al., 2010). Haye et al. (2010) reported that larval parasitism 16.3 Biological Control Agents accounted for 45.5–51.9% of the seasonal mortality of C. obstrictus in Switzerland, Three larval ectoparasitoid species were dominated by M. morys (44–48%) and T. released in south-western British Columbia perfectus (37–48%). Jourdheuil (1960) in 1949 (McLeod, 1962). These were reported that in France larval endo- reported as Habrocytus sp. (= Pteromalus parasitism by Diospilus oleraceus Haliday sp.), Trichomalus fasciatus (Thomson) (= (Hymenoptera: Braconidae) ranged from Trichomalus lucidus (Walker)) and 1% to 10%, but unlike ectoparasitoids, Xenocrepis pura Mayr (= Mesopolobus larval endoparasitoids appear to be of morys (Walker)) (Hymenoptera: Ptero- negligible importance for controlling C. malidae). Re-examination of voucher speci- obstrictus in Europe (Williams, 2003; Haye mens from the releases determined that the et al., 2010). Parasitoids attacking the eggs species were misidentifi ed, and were of C. obstrictus, mostly Mymaridae actually T. perfectus, M. morys and S. (Hymen optera), have been reported from gracilis (Gibson et al., 2005, 2006). Surveys various parts of Europe, but levels of near the original release sites in Fraser parasitism were generally low (Williams, Valley and in central British Columbia 2003). Adult C. obstrictus are attacked by found no evidence for establishment of T. the solitary endoparasitoid M. melanopus, perfectus or M. morys (Gibson et al., 2006; which caused substantial parasitism in Gillespie et al., 2006). Specimens of S. France (Bonnemaison, 1957; Jourdheuil, gracilis were found near the release sites 1960), but was rare or absent in other parts and hundreds of kilometres away in the Chapter 16 123

Creston Valley, confi rming that S. gracilis females do not start producing eggs until established (Gibson et al., 2006; Gillespie the following spring. The overwintering et al., 2006). Since earlier records of T. biology of T. perfectus is poorly under- perfectus and M. morys in North America stood, but it is assumed that adults are likely misidentifi cations of T. lucidus overwinter in pine forests, evergreen foli- and M. moryoides (Gibson et al., 2005), age and other sheltered places (Szcze- both European parasitoids have been panski, 1972). reconsidered for introduction into Canada. Several Trichomalus spp. are important Although never intentionally released in in the parasitoid complexes of Ceutorhyn- eastern Canada, T. perfectus was fi rst chinae (Muller et al., 2007), but their recorded from Ontario (Ottawa area) and ecological host ranges are relatively Quebec (St Célestin) in 2009 (Mason et al., unknown. Kuhlmann et al. (2006) noted 2011). The simultaneous occurrence of the that several Ceutorhynchinae species have parasitoid in a wide area indicates that it is been introduced to North America to quickly spreading throughout eastern control invasive weeds, and thus host Canada. The absence of T. perfectus from specifi city of potential biological control other areas of North America suggests that agents for C. obstrictus, e.g. T. perfectus, it was accidentally introduced at the same must be carefully evaluated to avoid time as the Quebec C. obstrictus popu- confl icts between insect and weed lation (Mason et al., 2011). Trichomalus biological control. Apart from C. obstrictus, perfectus is a univoltine solitary ecto- T. perfectus has been reared from ten hosts parasitoid of C. obstrictus larvae. In spring, in Europe (Table 16.2). Although T. overwintered females migrate into canola perfectus was sporadically recorded from fi elds 3–4 weeks after weevil adults, when various non-target hosts in the fi eld, it was the majority of C. obstrictus larvae have never found to be the dominant parasitoid reached the 3rd instar (Dmoch, 1975). of any of these Ceutorhynchus spp. (T. Females locate their hosts by drumming Haye, 2012, unpublished results). with their antennae on the walls of infested Mesopolobus morys is a solitary larval canola siliques and detecting the odour ectoparasitoid, and its biology is similar to from the frass of C. obstrictus larvae that of T. perfectus. Similar to T. perfectus, (Dmoch and Rutkowska-Ostrowska, 1978; females locate their hosts using olfactory Dmoch, 1998). Females then inject cues from the frass of the weevil larvae. paralysing venom into the C. obstrictus Single eggs are laid on the surface of the larva, and deposit a single egg directly on host larva or its frass. The larvae feed the surface of the host or in its frass nearby. externally on hosts and development from The C. obstrictus larva is also an important egg to adult lasts 18–19 days at 20°C source of nutrients for the synovigenic T. (Wogin, 2011). Apart from C. obstrictus, the perfectus females. Feeding on the host ecological host range of M. morys includes haemolymph provides crucial nutrients for at least three other species: Ceutorhynchus egg production. Each T. perfectus female turbatus Schultze (Baur et al., 2007; Muller produces 42–104 adult offspring over 4 et al., 2011b), C. typhae (Herbst) (Klander, weeks (T. Haye, 2012, unpublished 2001) and C. constrictus Marsham (T. Haye, results). Eggs hatch after 1–2 days and 2012, unpublished results). It was the most larvae immediately start feeding on the common species parasitizing C. turbatus in outside of the immobilized C. obstrictus Switzerland and Hungary, where it larvae. At 20°C, larval development is com- accounted for nearly 40% of parasitism pleted after 8 days and pupation occurs (Muller et al., 2011b). Mesopolobus morys alongside the larval remains, lasting 8–9 was reported to be more abundant than T. days (Wogin, 2011). In July, newly emerged perfectus only in Switzerland (Buechi, parasitoid adults chew through the silique 1993) and Sweden (Herrström, 1964). walls before crops are harvested. Mating In Europe, fi eld experiments on com- occurs immediately after emergence, but petition between M. morys and T. perfectus 124 Chapter 16

Table 16.2. List of Ceutorhynchinae species serving as host for Trichomalus perfetus in Europe. Ceutorhynchinae species Host plant Feeding niche Source Brassicaceae Ceutorhynchus obstrictus Brassica napus L. silique Ulber et al. (2010) (Marsham) Ceutorhynchus Brassica rapa L. (?) root Secretariat du service pleurostigma (Marsham) d’identifi cation des entomophages (1963) Ceutorhynchus alliariae Alliaria petiolata (Bieb.) stem Klander (2001) Brisout Cavara & Grande Ceutorhynchus roberti Alliaria petiolata stem Klander (2001) Gyllenhal Ceutorhynchus constrictus Alliaria petiolata silique Klander (2001) Marsham Ceutorhynchus erysimi Capsella bursa-pastoris (L.) stem T. Haye (2012, unpublished (Fabricius) Medik. results) Ceutorhynchus typhae Capsella bursa-pastoris silique Haye (2012, unpublished (Herbst) results) Ceutorhynchus cadariae Cardaria draba (L.) Desv. stem Diaconu and Haye (2012, Korotyaev unpublished results) Ceutorhynchus turbatus Cardaria draba silique Muller et al. (2011a) Schultzea Ceutorhynchus assimilis Cardaria draba root, stem Haye, Hinz and Bon (2012, (Paykull) unpublished results) Asteraceae Microplontus edentulus Tripleurospermum perforatum stem Muller et al. (2011b) (Schultze)a (L.) Sch. Bip. aParasitoids were identifi ed as Trichomalus cf. perfectus.

showed no synergistic effects on C. tended to be more abundant from C. obstrictus host suppression when both obstrictus associated with R. raphanistrum, parasitoid species were released simul- with T. lucidus constituting a larger taneously. Accordingly, a multiple species proportion of the parasitoid complex from introduction might be ill-advised for C. obstrictus on Brassica spp. (Gillespie et classical biological control of this pest in al., 2006). Canada (Wogin, 2011). In Alberta and Saskatchewan, para- sitism of C. obstrictus by native parasitoids was initially low, but levels subsequently 16.4 Evaluation of Biological Control increased over time. Only 0.1% of the weevil population was parasitized in 2002, Suppression of C. obstrictus by parasitoids but this increased to 5.0% by 2004 (Dosdall was relatively low in south-western British et al., 2006b). Parasitism increased further Columbia, where only 2–4% of weevils from 2004 to 2005, but varied among were parasitized (Gillespie et al., 2006). species. Greatest parasitism levels by T. Why only S. gracilis among the three lucidus, Pteromalus sp. and Chlorocytus European parasitoids released in British sp. were approximately 2, 9 and 10%, Columbia did establish is still not respectively (Dosdall et al., 2009). understood. Host plant species affected the However, parasitism by N. tidius reached parasitoid species composition: S. gracilis 45% in some canola fi elds in the southern Chapter 16 125 prairies (Dosdall et al., 2007). Parasitism 16.5 Future Needs levels for all four species varied depending on year and site, suggesting that environ- Further work should include: mental factors have important effects on their population densities. The situation in 1. Tracking the spread of T. perfectus Alberta and Saskatchewan appears to throughout eastern Canada and estimating refl ect a parasitoid community composed its economic impact on C. obstrictus popu- primarily of indigenous species that have lations; expanded their host ranges to exploit C. 2. Estimating potential non-target effects obstrictus larvae (Dosdall et al., 2006b). on indigenous weevils in areas where T. The low impact of S. gracilis in British perfectus is already established (Quebec Columbia, its possible interference with and Ontario); native C. obstrictus parasitoids present in 3. Mapping the distribution of T. perfectus Alberta, and its relatively broad host range and M. morys in Europe to determine effec- are the reasons why S. gracilis was not tive range limits and conducting degree- redistributed into Alberta and Saskat- day development and temperature tolerance studies for developing biocli- chewan. ® In eastern Canada, indigenous parasitoid matic models, e.g. CLIMEX ; populations were more variable in stands of 4. Clarifying the taxonomy of parasitoids autumn-seeded canola than in spring- associated with C. obstrictus in North seeded crops (Mason et al., 2011). In America and Europe using molecular tools; autumn-seeded canola, parasitism ranged 5. Comparing T. perfectus specimens from from 0 to 100% in 2006, but in most of European and Canadian locations using these fi elds, less than 10% of the C. molecular tools to assess population struc- obstrictus larvae were parasitized. In spring- ture and determine points of origin for seeded fi elds parasitism ranged from 0 to North American introductions; 29%, with an average parasitism of 6. Developing conservation biological con- approximately 18%. Numbers of parasitoid trol methods using indigenous and adven- species reared from siliques were generally tive generalist predators; higher in autumn-seeded than spring- 7. Continuing to monitor C. obstrictus par- seeded canola (Mason et al., 2011). asitoid densities in western Canada. Populations of the adventive T. perfectus are still low (P.G. Mason, 2012, un published results) and thus the parasitoid does not yet Acknowledgements suppress pest populations. Depending on the impact of T. perfectus in Quebec and The project was funded by Alberta Ontario on C. obstrictus populations and Agricultural Research Institute, Agriculture potential negative effects on indigenous and Agri-Food Canada, the Canola Council non-target weevils, T. perfectus might be of Canada, Alberta Agriculture and Rural considered for redistribution into other Development, and the AAFC Pest canola growing areas of Canada. Management Centre.

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Laffi n, R.D., Dosdall, L.M. and Sperling, F.A.H. (2005) Population structure of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae): origins of North American introductions. Environmental Entomology 34, 504–510. Mason, P.G., Baute, T., Olfert, O. and Roy, M. (2004) Cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae) in Ontario and Quebec. Journal of the Entomological Society of Ontario 134, 107–113. Mason, P.G., Miall, J.H., Bouchard, P., Gillespie, D.R., Broadbent, A.B. and Gibson, G.A.P. (2011) The parasitoid communities associated with an invasive canola pest, Ceutorhynchus obstrictus (Coleoptera: Curculionidae), in Ontario and Quebec, Canada. The Canadian Entomologist 143, 524–537. McCaffrey, J.P. (1992) Review of U.S. canola pest complex: cabbage seedpod weevil. Proceedings of the 1992 US Canola Conference 5–6 March 1992, Washington, DC, pp. 140–143. McCaffrey, J.P., O’Keefe, L.E. and Homan, H.W. (1986) Cabbage Seedpod Weevil Control in Winter Rapeseed. Agricultural Experiment Station Information Series 782, University of Idaho, Moscow, Idaho. McCaffrey, J.P., Harmon, B.L., Brown, J., Brown, A.P. and Davis, J.B. (1999) Assessments of Sinapis alba, Brassica napus and S. alba x B. napus hybrids for resistance to cabbage seedpod weevil, Ceutorhynchus assimilis (Coleoptera: Curculionidae). Journal of Agricultural Science 132, 289– 295. McLeod, J.H. (1962) Cabbage seedpod weevil – Ceutorhynchus assimilis (Payk.) Curculionidae. In: McLeod, J.H., McGugan, B.M. and Coppel, H.C. (eds) A Review of the Biological Control Attempts against Insects and Weeds in Canada. Commonwealth Agricultural Bureaux (CAB), Farnham Royal, UK, pp. 5–6. Muller, F.J., Baur, H., Gibson, G.A.P., Mason, P.G. and Kuhlmann, U. (2007) Review of the species of Trichomalus (Chalcidoidea: Pteromalidae) associated with Ceutorhynchus (Coleoptera: Curculionidae) host species of European origin. The Canadian Entomologist 139, 643–657. Muller, F.J., Dosdall, L.M., Mason, P.G. and Kuhlmann, U. (2011a) Larval phenologies and parasitoids of two seed-feeding weevils associated with hoary cress and shepherd’s purse in Europe. The Canadian Entomologist 143, 399–410. Muller, F.J., Mason, P.G., Dosdall, L.M. and Kuhlmann, U. (2011b) European ectoparasitoids of two classical weed biological control agents released in North America. The Canadian Entomologist 143, 197–210. Murchie, A.K. (1996) Parasitoids of cabbage seed weevil and brassica pod midge in oilseed rape. PhD thesis, University of Keele, Keele, UK. Ni, X., McCaffery, J.P., Stoltz, R.L. and Harmon, B.L. (1990) Effects of postdiapause adult diet and temperature on oogenesis of the cabbage seedpod weevil (Coleoptera: Curculionidae). Environmental Entomology 15, 884–888. Olfert, O. and Weiss, R.M. (2006) Impact of climate change on potential distributions and relative abundances of Oulema melanopus, Meligethes viridescens and Ceutorhynchus obstrictus in Canada. Agriculture, Ecosystems and Environment 113, 295–301. Secretariat du service d’identifi cation des entomophages (1963) Liste d’Identifi cation No. 5. Entomophaga 8, 335–373. Szczepanski, H. (1972) The rape Pteromalid - Trichomalus perfectus (Walk.) (Hymenoptera, Pteromalidae) in forest biocoenosis and the problem of the biological protection of rape. Polskie Pismo Entomologiczne 42, 865–871. Tansey, J.A., Dosdall, L.M., Keddie, B.A. and Noble, S.D. (2009) Contributions of visual cues to cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), resistance in novel host genotypes. Crop Protection 29, 476–481. Tansey, J.A., Dosdall, L.M., Keddie, B.A., Fletcher, R.S. and Kottt, L.S. (2010a) Antixenosis and antibiosis modes of resistance to Ceutorhynchus obstrictus of novel germplasm developed by Sinapis alba L. x Brassica napus. Canadian Entomologist 142, 212–221. Tansey, J.A., Dosdall, L.M., Keddie, B.A., Fletcher, R.S. and Kott, L.S. (2010b) Responses of Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae) to olfactory cues associated with novel genotypes developed by Sinapis alba L. × Brassica napus L. Arthropod-Plant Interactions 4, 95–106. Ulber, B., Williams, I.H., Klukowski, Z., Luik, A. and Nilsson, C. (2010) Parasitoids of oilseed rape pests in Europe: key species for conservation biocontrol. In: Williams, I.H. (ed.) Biocontrol- Chapter 16 129

Based Integrated Management of Oilseed Rape Pests. Springer Science, Dordrecht, the Netherlands, pp. 45–76. Ulmer, B.J. and Dosdall, L.M. (2006) Spring emergence biology of the cabbage seedpod weevil (Coleoptera: Curculionidae). Annals of the Entomological Society of America 99, 64–69. Vänninen, I., Husber, G.B. and Hokkanen, H.M.T. (1989) Occurence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland. Acta Entomologica Fennica 53, 65–71. Warner, D.J., Allen-Williams, L.J., Warrington, S., Ferguson, A.W. and Williams, I.H. (2008) Implications for conservation biocontrol of spatio-temporal relationships between carabid beetles and coleopterous pests in winter oilseed rape (Brassica napus). Agricultural and Forest Entomology 10, 375–387. Williams, I.H. (2003) Parasitoids of cabbage seed weevil. In: Alford, D.V. (ed.) Biocontrol of Oilseed Rape Pests. Blackwell Science, Oxford, UK, pp. 97–112. Williams, I.H. (2010) The major insect pests of oilseed rape in Europe and their management: an overview. In: Williams, I.H. (ed.) Biocontrol-Based Integrated Management of Oilseed Rape Pests. Springer Science, Dordrecht, the Netherlands, pp. 1–43. Williams, I.H. and Free, J.B. (1978) The feeding and mating behaviour of pollen beetles (Meligethes aeneus Fabricius) and seed weevils (Ceutorhynchus assimils Payk.) on oil-seed rape (Brassica napus L.). Journal of Agricultural Science 91, 453–459. Wogin, M.J. (2011) Competition between parasitoids of the cabbage seedpod weevil: effects on sex ratios and consequences for biological control. MSc thesis, Simon Fraser University, Burnaby, Canada. Zaller, J.G., Moser, D., Drapela, T. and Frank, T, (2009) Ground-dwelling predators can affect within- fi eld pest insect emergence in winter oilseed rape fi elds. BioControl 54, 247–253. Zec-Vojinovic, M., Hokkanen H.M.T., Büchs, W., Klukowski, Z., Luik, A., Nilsson, C., Ulber, B. and Williams, I.H. (2006) Natural occurrence of pathogens of oilseed rape pests in agricultural fi elds in Europe. Proceedings of the International Symposium of Integrated Pest Management in Oilseed Rape, 3–5 April 2006, Goettingen, Germany. 130 Chapter 17

17 Choristoneura rosaceana (Harris), Obliquebanded Leafroller (Lepidoptera: Tortricidae)

Joan Cossentine,1 Charles Vincent,2 Mike Smirle1 and Jean-Charles Côté 2 1Agriculture and Agri-Food Canada, Summerland, British Columbia; 2Agriculture et Agroalimentaire Canada, St-Jean-sur-Richelieu, Québec

17.1 Project status rosaceana mating disruption product in Canada in 2004 (Judd and Gardiner, 2004), The obliquebanded leafroller, Choristo- Bacillus thuringiensis Berliner serovar. neura rosaceana (Harris) (Lepidoptera: kurstaki (Btk) (Bacillaceae) was the only Tortricidae), is a common secondary pest registered non-chemical C. rosaceana on many deciduous trees and shrubs in control option for organic growers. Canada including , Malus domestica Resistance to Btk has been documented in Borkh., , Pyrus communis L., cherries, other Lepidoptera (Tabashnik, 1994). Prunus avium (L.) L., P. cerasus L., and Populations of C. rosaceana and of the raspberries, Rubus ideaus L. (Rosaceae) (Li sympatric three-lined leafroller, Pandemis et al., 2001). It overwinters as an early- limitata (Robinson) (Lepidoptera: Tortri- instar larva and emerges to feed on cidae), obtained from organic orchards in developing blossoms and young fruit in the Okanagan and Similkameen valleys of spring. A second generation produces the British Columbia, exhibited varying toler- early instars that seek overwintering sites ance to Btk that refl ected Btk usage in late summer and early autumn (Madsen patterns (Smirle et al., 2003). The two and Procter, 1982). From 2001 to 2012, leafroller populations exhibiting the progress was made in Canada in the highest tolerance to B. thuringiensis were development and integration of C. both collected from apple orchards rosaceana parasitoid, predator and managed under organic production guide- pathogen biological controls. lines. As Btk is recommended for appli- In British Columbia, the Okanagan- cation to protect blossoms and developing Kootenay Sterile Insect Release programme fruit in the spring and summer, research (SIR) is used for area-wide management of was conducted to improve its protection the key apple and pear pest, the codling from spring rains and sun. Côté et al. moth, Cydia pomonella (L.) (Lepidoptera: (2001) developed an experimental en- Tortricidae). Within the SIR programme, C. capsulated formulation of Btk that signifi - rosaceana can become a problem in cantly extended the residual impact of the orchards where chemical suppression of C. bacterial product on C. rosaceana larvae. pomonella is no longer used. Prior to the This work was instrumental in developing registration of a dual C. pomonella and C. two new formulations of Btk, BioprotecTM

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 17 131

CAF, an aqueous formulation, and Bio- found to host-feed from wounds they protecTM 3P, a dustless dry fl owable infl icted on early instar larvae and A. granule with extended residual effi cacy simplicipes females were observed to following spraying. The two improved macerate 1st instar larvae (Cossentine et formulations were registered for the control al., 2004a, 2007b). Both A. polychrosidis of Lepidoptera in apple orchards in 2001 and A. simplicipes parasitized signifi cantly and 2004, respectively. more C. rosaceana larvae under autumn A nucleopolyhedrovirus (Baculoviridae) versus summer conditions whereas G. isolated from C. rosaceana larvae collected variegata parasitized signifi cantly more in an apple orchard in Quebec in 1997 2nd instar C. rosaceana under summer (Pronier et al., 2000) was found to cause versus autumn conditions (Cossentine et 75% mortality in 3rd instar larvae exposed al., 2005, 2007b). Host larvae parasitized to the virus for 23 days in laboratory assays by the polyembryonic endoparasitoid M. (Pronier et al., 2002). The cuboidal linearis consumed more meridic diet than occlusion bodies of the virus were found to non-parasitized hosts, indicating that more multiply primarily in the fat body of fruit damage may be done by C. rosaceana infected larvae (Pronier et al., 2000, 2002). parasitized by this species before the Todorova et al. (2002) demonstrated the parasitized hosts eventually die (Cossen- susceptibility of C. rosaceana larvae under tine et al., 2005). In contrast, A. poly- laboratory conditions to 23 isolates of the chrosidis that emerged from 3rd or 4th entomopathogenic fungus Beauveria instar larvae and A. simplicipes and G. bassiana (Balsamo) Vuillemin (Cordycipi- variegata that emerged from 5th and 6th taceae). Two B. bassiana isolates caused instar larvae caused their parasitized C. higher larval mortality and sub-lethal rosaceana hosts to consume signifi cantly effects on pupae and adults. less diet than unparasitized hosts indi- Over 30 species of parasitoids were cating that the parasitism by these species recorded from C. rosaceana in organically may decrease fruit damage. Although A. managed orchards in the Okanagan and polychrosidis and G. variegata parasitized Similkameen valleys of British Columbia another tortricid host, M. linearis and A. (Cossentine et al., 2004b, 2007a). Not all simplicipes only parasitized 1st through parasitoid species occurred in all of the 4th instar C. rosaceana in laboratory trials orchards surveyed, but rather different (Cossentine et al., 2004a, 2005, 2007b). communities of species were found in The release of native parasitoid species orchards separated by relatively short to suppress wild C. rosaceana may be distances. A signifi cant inverse correlation effective in orchards that are converting to was documented between numbers of C. minimal-chemical pest management. Host rosaceana in orchards and percent parasit- location and parasitism of sentinel hosts ism within a generation, demonstrating was assessed under orchard conditions that parasitism probably has a signifi cant through caged and uncaged releases of impact on host population densities each of the parasitoids on potted apple (Cossentine et al., 2004b). The biology of trees. Seasonal timing of the trials varied each of the most common C. rosaceana for each parasitoid species based on their parasitoid species that emerge from relative performance under simulated overwintered larvae in the spring, namely summer/autumn conditions. After the Apophua simplicipes (Cresson), Glypta release of 5 or 50 parasitoid females, the variegata Dasch (Hymenoptera: Ichneu- mean percentage parasitism of C. rosa- monidae), Apanteles polychrosidis Viereck ceana larvae collected from infested trees and Macrocentrus linearis (Nees) (Hymen- ranged from 0 to 75% depending on the optera: Braconidae), was determined in parasitoid species involved. Release of A. more detail. All four species parasitized simplicipes had a signifi cant impact on C. early instar C. rosaceana larvae. Females of rosaceana host population density in these both A. simplicipes and G. variegata were trials (Cossentine, 2008). 132 Chapter 17

A study in the southern interior of actinomycete Saccharopolyspora spinosa British Columbia determined how spring Mertz & Yao (Pseudonocardiaceae). The Btk treatments on apple could be more insecticide was registered for use on apples strategically timed to maximize survival of in Canada in 2001. Spinosad-based prod- C. rosaceana parasitoids (Cossentine et al., ucts have become increasingly used in 2003). Second through 4th instar C. organic and conventionally managed rosaceana larvae were found in varying orchards in Canada since the registration of proportions in orchards from pink through a formulation that is acceptable for organic petal-fall stage of apple development. use in 2006. Choristoneura rosaceana is Laboratory-reared 2nd through 4th instar highly susceptible to spinosads (Smirle et C. rosaceana larvae, either unparasitized, al., 2003) and, consequently, it is important or parasitized by A. simplicipes, A. to recognize and evaluate the potential polychrosidis or M. linearis, were fed damage that the insecticide may have on untreated apple leaves or leaves treated the C. rosaceana parasitoid complex. There with Btk. Choristoneura rosaceana larvae is clear evidence that spinosad has a are most susceptible to Btk in their 4th negative impact on parasitoid survival and instar (Li et al., 1995; Cossentine et al., fecundity (Williams et al., 2003). In 2003), whereas Btk-induced mortality in laboratory trials exposing A. simplicipes- the unparasitized 2nd and 3rd instars was parasitized C. rosaceana larvae to both oral less than 50%. This relatively low sus- and topical spinosad treatments, A. ceptibility of C. rosaceana larvae to Btk simplicipes survival was signifi cantly allowed from 38 to 43% survival of the reduced within parasitized spinosad- parasitoids in 2nd and 3rd instar hosts. treated 2nd and 4th instar larval hosts Fourth instar C. rosaceana larvae were (Cossentine et al., 2010). This research found at full bloom and petal-fall stage of supports the prediction that applications of apple development in the orchard when spinosad will reduce biological control of Btk treatments were recommended for C. rosaceana populations by killing optimal C. rosaceana control. The highest ichneumonid endoparasitoids within parasitoid mortality due to Btk-induced treated hosts. host mortality was recorded in hosts Research also continued on the pre- parasitized by A. simplicipes and M. dation of C. rosaceana larvae by two linearis and treated as 4th instar larvae. aphidophagous coccinellids, Harmonia Both of these species emerge from 5th and axyridis (Pallas) and Coccinella septem- 6th instar C. rosaceana larvae. Btk did not punctata L. (Coleoptera: Coccinellidae) have as negative an impact on A. (Lucas et al., 2004). More 1st instar C. polychrosidis that emerged from an earlier rosaceana were consumed by H. axyridis instar larva. When C. rosaceana mortality when 3rd instar green apple aphids, Aphis and parasitism were combined, the Btk pomi DeGeer (Hemiptera: Aphididae), were treatment did not signifi cantly increase present than when only the C. rosaceana host elimination above that of parasitism larvae were offered to the coccinellid. The alone, except for larvae parasitized by A. consumption of C. rosaceana larvae by C. simplicipes in the 4th instar. Consumption septempunctata was not affected by the of Btk by unparasitized larvae also slowed presence of A. pomi. Both predators were larval development. This study resulted in found to prefer to feed on aphids over C. a recommendation to time spring Btk rosaceana larvae. treatments earlier than full bloom and petal-fall in an effort to reduce spring parasitoid mortality within 4th instar larval 17.2 Future needs hosts (Cossentine et al., 2003). Spinosad® (Dow AgroSciences) is an The obliquebanded leafroller is a good insecticide that contains spinosyns A and example of a pest species that has many D, two fermentation products of the non-chemical control options, including Chapter 17 133

numerous biological control agents and 1. Research on strategies to introduce or strategies that can be integrated to result in augment specifi c indigenous C. rosaceana economic pest suppression. Chemical sup- parasitoid species in orchards; pression, including the use of spinosad 2. Continued assessment of the impact of formulations, should be minimized to novel insecticides, including biopesticides, allow parasitoid establishment within on C. rosaceana and its parasitoids to help agricultural crops. guide growers in their management of this Future work should include: pest.

References

Cossentine, J.E. (2008) Testing the impact of laboratory reared indigenous leafroller parasitoids on sentinel hosts in controlled orchard releases. European Journal of Entomology 105, 241–248. Cossentine, J.E., Jensen, L.B. and Deglow, E.K. (2003) Strategy for orchard use of Bacillus thuringiensis while minimizing impact on Choristoneura rosaceana parasitoids. Entomologia Experimentalis et Applicata 109, 205–210. Cossentine, J.E., Deglow, E.K., Jensen, L.B.M. and Bennett, A.M.R. (2004a) A biological assessment of Apophua simplicipes (Hymenoptera: Ichneumonidae) as a parasitoid of the oblique banded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Biocontrol Science and Technology 14, 691–699. Cossentine, J., Jensen, L., Deglow, E., Bennett, A., Goulet, H., Huber, J. and O’Hara, J. (2004b) The parasitoid complex affecting Choristoneura rosaceana and Pandemis limitata in organically managed apple orchards. Biocontrol 49, 359–372. Cossentine, J.E., Deglow, E.K., Jensen, L.B.M. and Goulet, H. (2005) Biological assessment of Macrocentrus linearis and Apanteles polychrosidis (Hymenoptera: Braconidae) as parasitoids of the obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Biocontrol Science and Technology 15, 711–720. Cossentine, J., Bennett, A., Goulet, H. and O’Hara, J. (2007a) Parasitism of the spring leafroller (Lepidoptera: Tortricidae) complex in organically managed apple orchards in the north Okanagan valley of British Columbia. Pan-Pacifi c Entomologist 83, 276–284. Cossentine, J.E., Deglow, E.K., Jensen, L.B.M. and Bennett, A.M.R. (2007b) A biological assessment of Glypta variegata (Hymenoptera: Ichneumonidae) as a parasitoid of Choristoneura rosaceana (Lepidoptera: Tortricidae). Biocontrol Science and Technology 17, 325–329. Cossentine, J.E., Zurowski, C.L. and Smirle, M.J. (2010) Impact of spinosad on ichneumonid- parasitized Choristoneura rosaceana larvae and subsequent parasitoid emergence. Entomologia Experimentalis et Applicata 136, 116–122. Côté, J.-C., Vincent, C., Son, K.-H. and Bok, S.H. (2001) Persistence of insecticidal activity of novel bioencapsulated formulations of Bacillus thuringiensis var. kurstaki against Choristoneura rosaceana (Lepidoptera: Tortricidae). Phytoprotection 82, 73–82. Judd, G.J.R. and Gardiner, M.G.T. (2004) Simultaneous disruption of pheromone communication and mating in Cydia pomonella, Choristoneura rosaceana and Pandemis limitata (Lepidoptera: Tortricidae) using isomate-CM/LR in apple orchards. Journal of the Entomological Society of British Columbia 101, 3–13. Li, S.Y., Fitzpatrick, S.M. and Isman, M.B. (1995) Susceptibility of different instars of the obliquebanded leafroller (Lepidoptera: Tortricidae) to Bacillus thuringiensis var. kurstaki. Journal of Economic Entomology 88, 610–614. Li, S.Y., Fitzpatrick, S.M., Hueppelsheuser, T., Cossentine, J.E. and Vincent, C. (2001) Choristoneura rosaceana (Harris), obliquebanded leafroller (Lepidoptera: Tortricidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada 1981–2000. CAB International, Wallingford, UK, pp. 78–83. Lucas, E., Demougeot, S., Vincent, C. and Coderre, D. (2004) Predation upon the oblique-banded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae), by two aphidophagous coccinellids (Coleoptera: Coccinellidae) in the presence and absence of aphids. European Journal of Entomology 101, 37–41. 134 Chapter 18

Madsen, H. and Procter, J. (1982) Insects and Mites of Tree Fruits in British Columbia. Ministry of Agriculture and Food, Victoria, British Columbia. Pronier, I., Paré, J., Wissocq, J.-C., Vincent, C. and Stewart, R.K. (2000) Étude préliminaire d’un virus agent de la polyédrose nucléaire dans les tissus de son hôte, la tordeuse à bandes obliques. Bulletin de la Société Zoologique de France 125, 174–176. Pronier, I., Paré, J., Wissocq, J.-C. and Vincent, C. (2002) Nucleopolyhedrovirus infection in the obliquebanded leafroller (Lepidoptera: Tortricidae). Canadian Entomologist 134, 303–309. Smirle, M.J., Lowery, D.T. and Zurowski, C.L. (2003) Susceptibility of leafrollers (Lepidoptera: Tortricidae) from organic and conventional orchards to azinphosmethyl, spinosad, and Bacillus thuringiensis. Journal of Economic Entomology 96, 879–884. Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39, 47–79. Todorova, S.I., Coderre, D., Vincent, C. and Côté, J.-C. (2002) Screening of Beauveria bassiana (Hyphomycetes) isolates against Choristoneura rosaceana (Lepidoptera: Tortricidae). Canadian Entomologist 134, 77–84. Williams, T., Valle, J. and Viñuela, E. (2003) Is the naturally derived insecticide Spinosad® compatible with insect natural enemies? Biocontrol Science and Technology 13, 459–475.

18 Contarinia nasturtii Kieffer, Swede Midge (Diptera: Cecidomyiidae)

Paul K. Abram,1 Guy Boivin,2 Tim Haye3 and Peter G. Mason4 1Université de Montréal, Montréal, Québec; 2Agriculture et Agroalimentaire Canada, St Jean-sur-Richelieu, Québec; 3CABI, Delémont, Switzerland; 4Agriculture and Agri-Food Canada, Ottawa, Ontario

18.1 Pest Status rapa L., as well as many cruciferous weeds (Barnes, 1946; Stokes, 1953; Darvas et al., The swede midge, Contarinia nasturtii 2000; Hallett, 2007; Chen et al., 2009b). Kieffer (Diptera: Cecidomyiidae), is a plant- Contarinia nasturtii is a sporadic pest in its feeding cecidomyiid whose Brassicaceae native range, which includes a large area in hosts include economically important Europe, extending north to , crucifer crops such as broccoli, Brassica south to the Mediterranean, west to Britain, oleracea L. var. italica Plenk, caulifl ower, and east to Turkey and western Russia B. oleracea var. botrytis L., cabbage, B. (Skuhravá, 1997; Darvas et al., 2000; Fauna oleracea var. capitata L., Brussels sprouts, Europaea, 2011). In 2000, the fi rst positive B. oleracea var. gemmifera (DC.) Zenker, identifi cation of C. nasturtii in Canada was and canola, Brassica napus L. and Brassica made in southern Ontario, although there © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 18 135

were reports of damage symptoms in ceptible to bacterial rot, and which may crucifer crops as early as 1996 (Hallett and limit seed production in canola (Barnes, Heal, 2001). Not long after, crop losses of 1946; Hallett and Heal, 2001; Hallett et al., up to 85% were reported in southern 2007). Full-grown larvae, 3–4 mm long and Ontario (Hallett and Heal, 2001), and its whitish yellow, fall or ‘jump’ from their presence subsequently caused the abandon- host plant into the soil where they con- ment of Integrated Pest Management (IPM) struct a cocoon (Barnes, 1946; Readshaw, programmes previously developed for other 1966). Some C. nasturtii larvae pupate crucifer pests (Chen et al., 2011). Con- immediately and emerge as adults 1–3 tarinia nasturtii has now been found in weeks later, while others will enter Quebec, Nova Scotia, Manitoba and Saska- diapause and emerge the following spring; tchewan, as well as fi ve US states: New the proportion of pupae entering diapause York, Massachusetts, New Jersey, Connecti- in each generation increases through the cut and Ohio (Canadian Food Inspection growing season (Readshaw, 1966). Agency, 2008a; Chen et al., 2009b). Modelling of C. nasturtii distribution and abundance, based on climate, has shown 18.2 Background that populations could become established The application of synthetic insecticides, throughout much of Canada and the USA in particular neonicitinoids, is the primary (Olfert et al., 2006; Mika et al., 2008). method of C. nasturtii control where the Infestation of spring-planted canola in pest causes economic damage to crucifer Ontario was fi rst reported in 2005 crops (Wu et al., 2006; Chen et al., 2007; (Canadian Food Inspection Agency, 2008b), Hallett et al., 2009). In the fi eld, however, thus there is concern that spring-planted the effi cacy of chemical control is variable, canola crops in western Canada could also and is complicated by the high degree of be attacked, especially in years when crops overlap between C. nasturtii generations are seeded later than usual and plants are and diffi culty in achieving adequate spray still in a susceptible stage when the fi rst coverage (Hallett et al., 2009). generation emerges (Hallett and Baute, Cultural control methods could play an 2007). important role in C. nasturtii management. In both the native and invaded ranges, Crop rotation may be the single most C. nasturtii has from three to fi ve over- effective method. Simulated crop rotation lapping generations between May and systems have shown that as little as one October (Mesnil, 1938; Rygg and Braekke, season without suitable hosts can provide 1963; Hallett et al., 2007; Corlay and complete control of C. nasturtii, although Boivin, 2008). Adult females mate soon these experiments did not take into after emerging from the soil, and lay eggs account the possibility of the extended in batches of 2–50 on the actively growing diapause of a portion of each generation tissue of their host plant, most often on (Chen et al., 2009a; Abram et al., 2012b). heart leaves near the central growing tip Management of brassicaceous weeds (Readshaw, 1966). Larvae hatch 1–3 days border ing fi elds may also be important in later and feed gregariously by extra-oral crop rotation systems, as they can serve as digestion, where salivary secretions liquefy alternate hosts for C. nasturtii when their the host tissue (Readshaw, 1966). Larval preferred, crucifer crop hosts are not feeding induces gall-like structures in the present (Chen et al., 2009b). growing tips of host plants, causes leaf Physical barriers, such as insect fences distortion and twisting, the development of surrounding a fi eld, or insect nets covering compensatory side-shoots, and prevents the young seedlings, can provide some proper development of infl orescences protection against C. nasturtii in fi elds that (Barnes, 1946; Darvas et al., 2000; Hallett have not been planted with infested and Heal, 2001). Larval feeding also leaves Brassica crops in the 2 previous years corky scars, which make plants more sus- (Sauer and Fähndrich, 2010). 136 Chapter 18

Bacillus thuringiensis Berliner serovar. 18.3 Biological Control Agents israelensis (Bacillaceae), the entomopatho- genic soil nematode Heterorhabditis A comprehensive survey was conducted bacteriophora Poinar (Rhabditida: Heteror- between 2008 and 2011 to identify habditidae) and two predatory beetles, potential classical biological control agents Coccinella septempunctata L. and Har- in Europe (Abram et al., 2012b). Four monia axyridis (Pallas) (Coleoptera: Coc- species of larval endoparasitoids attacking cinellidae) have been tested against C. C. nasturtii were identifi ed: Inostemma nasturtii in the lab but are either untested opacum Thomson, M. chalybeus, S. myles or unlikely to be effective in fi eld systems and S. osaces Walker (Hymenoptera: Platy- (Wu et al., 2006; Corlay et al., 2007). gastridae) (Abram et al., 2012a,b). Among Following the detection of the C. these, M. chalybeus and S. myles were nasturtii in North America, Corlay et al. found throughout the surveyed range and (2007) conducted a survey for associated attacked every C. nasturtii generation. parasitoids in Québec, Canada. They col- Levels of attack, although sometimes 30– lected a total of 5142 C. nasturtii larvae 40%, were typically <10% and many from two fi eld sites over 2 years (2005– generations of C. nasturtii were subject to 2006) but recorded no parasitoid emer- very low levels of parasitism. In addition, gence (Corlay et al., 2007). These fi ndings both M. chalybeus and S. myles are suggest that associated parasitoids from reported to attack several other gall midge the native range in Europe were probably species in Europe on several different host not introduced along with their host, and plants, casting doubt on their host no native North American parasitoids specifi city (e.g. Strong and Larsson, 1992; attack C. nasturtii. However, widespread Romankow and Dankowska, 1993; Keller surveys are needed to confi rm this and Schweizer, 1994; Buhl and Notton, hypothesis. 2009). At present, neither species appears Until recently, surprisingly little was to be a promising candidate for intro- known about the parasitoid complex of the duction to North America. swede midge in its native range. Bovien and Knudsen (1950) observed that swede midge in Denmark was attacked by 18.4 Future Needs Macroglenes eximius (Haliday) (=Pirene eximia Haliday) (Hymenoptera: Ptero- Further research should include: malidae); however, it is likely that the species reported by these authors was 1. More rigorous evaluation of the impact actually Macroglenes chalybeus Haliday. In and host ranges of M. chalybeus and S. England, two Synopeas spp. and one myles is needed, along with surveys of Platygaster sp. (Hymenoptera: Platy- Southern and Eastern Europe, where C. gastridae) have been reared from C. nasturtii has never been reported as a pest nasturtii larvae (Rogerson, 1963; Readshaw, and may occur at low densities because of 1966). Buhl and Notton (2009) reported regulation by more effi cient natural ene- several instances of Synopeas myles mies; Walker and a single record of Synopeas 2. Life table studies in Europe and North ventrale Westwood (Hymenoptera: Platy- America to identify other important biotic gastridae) being reared from C. nasturtii in mortality factors for C. nasturtii, to inform Great Britain. future management techniques. Chapter 18 137

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Abram, P.K., Haye, T., Mason, P.G., Cappuccino, N., Boivin, G. and Kuhlmann, U. (2012a) Biology of Synopeas myles, a parasitoid of the swede midge, Contarinia nasturtii, in Europe. BioControl 57, 789–800. Abram, P.K., Haye, T., Mason, P.G., Cappuccino, N., Boivin, G. and Kuhlmann, U. (2012b) Identity, distribution, and seasonal phenology of parasitoids of the swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae) in Europe. Biological Control 62, 197–205. Barnes, H.F. (1946) Gall Midges of Root and Vegetable Crops. Crosby Lockwood & Son, London. Bovien, P. and Knudsen, P. (1950) Krusesygegalmyggen (Contarinia nasturtii Kieff.), dens biologi og bekaempelse. Tidsskrift for Planteavl 53, 235–257. Buhl, P. and Notton, D. (2009) A revised catalogue of the of the British Isles (Hymenoptera: Platygastroidea). Journal of Natural History 43, 1651–1703. Canadian Food Inspection Agency (2008a) Plant protection survey report. CFIA Plant Health Division. Available at: http://www.inspection.gc.ca/english/plaveg/pestrava/surv/sit2008e. shtml#connas (accessed 25 October 2011). Canadian Food Inspection Agency (2008b) RMD-08-03: Review of the pest status of the swede midge (Contarinia nasturtii) in Canada - Risk Management Document. Available at: http://www. inspection.gc.ca/plants/plant-protection/directives/risk-management/rmd-08-03/ eng/1304794114305/1304822057238 (accessed 5 June 2012). Chen, M., Zhao, J.-Z. and Shelton, A.M. (2007) Control of Contarinia nasturtii Kieffer (Diptera: Cecidomyiidea) by foliar sprays of acetamiprid on caulifl ower transplants. Crop Protection 26, 1574–1578. Chen, M., Li, W. and Shelton, A.M. (2009a) Simulated crop rotation systems control swede midge, Contarinia nasturtii. Entomologia Experimentalis et Applicata 133, 84–91. Chen, M., Shelton, A.M., Wang, P., Hoepting, C.A., Kain, W.C. and Brainard, D.C. (2009b) Occurrence of the new invasive insect Contarinia nasturtii (Diptera: Cecidomyiidae) on cruciferous weeds. Journal of Economic Entomology 102, 115–120. Chen, M., Shelton, A.M., Hallett, R.H., Hoepting, C.A., Kikkert, J.R. and Wang, P. (2011) Swede midge (Diptera: Cecidomyiidae), ten years of invasion of crucifer crops in North America. Journal of Economic Entomology 104, 709–716. Corlay, F. and Boivin, G. (2008) Seasonal development of an invasive exotic species, Contarinia nasturtii (Diptera: Cecidomyiidae), in Quebec. Environmental Entomology 37, 907–913. Corlay, F., Boivin, G. and Bélair, G. (2007) Effi ciency of natural enemies against the swede midge Contarinia nasturtii (Diptera: Cecidomyiidae), a new invasive species in North America. Biological Control 43, 195–201. Darvas, B., Skuhrava, M. and Andersen, A. (2000) Agricultural Dipteran pests of the Palearctic region. In: Papp, L. and Darvas, B. (eds) Contributions to a Manual of Palearctic Diptera, with Special Reference to of Economic Importance. Science Herald, Budapest, Hungary. Fauna Europaea (2011) Version 2.4. Available at: http://www.faunaeur.org (accessed 2 September 2011). Hallett, R.H. (2007) Host plant susceptibility to the swede midge (Diptera: Cecidomyiidae). Journal of Economic Entomology 100, 1335–1343. Hallett, R.H. and Baute, T. (2007) Swede midge impact and management in spring canola. In: Crop Advances: Field Crop Reports. Available at: http://www.ontariosoilcrop.org/docs/V3Can3.pdf (accessed 30 October, 2011). Hallett, R.H. and Heal, J.D. (2001) First Nearctic record of the swede midge (Diptera: Cecidomyiidae), a pest of cruciferous crops from Europe. The Canadian Entomologist 133, 713–715. Hallett, R.H., Goodfellow, S.A. and Heal, J.D. (2007) Monitoring and detection of the swede midge (Diptera: Cecidomyiidae). The Canadian Entomologist 139, 700–712. Hallett, R.H., Chen, M., Sears, M.K. and Shelton, A.M. (2009) Insecticide management strategies for control of swede midge (Diptera: Cecidomyiidae) on cole crops. Journal of Economic Entomology 102, 2241–2254. Keller, S. and Schweizer, C. (1994) Populationsdynamische Untersuchungen an der Erbsengallmücke Contarinia pisi Winn. (Dipt., Cecidomyiidae) und ihrer Parasitoide. Journal of Applied Entomology 118, 281–299. 138 Chapter 18

Mesnil, L. (1938) La cécidomyie du chou-fl eur dans la région de Saint-Omer. Annales des Épiphyties et de Phytogénétique, Paris 4, 281–311. Mika, A.M., Weiss, R.M., Olfert, O., Hallett, R.H. and Newman, J.A. (2008) Will climate change be benefi cial or detrimental to the invasive swede midge in North America? Contrasting predictions using climate projections from different general circulation models. Global Change Biology 14, 1721–1733. Olfert, O., Hallett, R., Weiss, R.M., Soroka, J. and Goodfellow, S. (2006) Potential distribution and relative abundance of swede midge, Contarinia nasturtii, an invasive pest in Canada. Entomologia Experimentalis et Applicata 120, 221–228. Readshaw, J.L. (1966) The ecology of the swede midge, Contarinia nasturtii (Kieff.) (Diptera, Cecidomyiidae). I. Life-history and infl uence of temperature and moisture on development. Bulletin of Entomological Research 56, 685–700. Rogerson, J.P. (1963) Swede midge on two Northumberland farms, 1959-1961. Plant Pathology 12, 161–171. Romankow, W. and Dankowska, E. (1993) Parasites of the lucerne fl ower gall midge Contarinia medicaginis Kieff. (Diptera, Cecidomyidae) in the region of Poznan. In: Pruszynski, S. and Lipa, J.J. (eds) Materials of the 34th Research Session of Institute of Plant Protection. Pt. 1. Reports, Poznan (Poland): Panstwowe Wydawnictwo Rolnicze i Lesne, 1994, pp. 222–228. Rygg, T.D. and Braekke, H.P. (1963) Swede midge (Contarinia nasturtii Kieffer) (Diptera Cecidomyiidae); investigations on biology, symptoms of attack and effects on yield. Meldinger fra Norges Landbrukshoegskule 59, 1–9. Sauer, C. and Fähndrich, S. (2010) Die Kohldrehherzgallmücke (Contarinia nasturtii) (Kieffer). Merkblatt Extension Gemüsebau Forschungsanstalt Agroscope Changins-Wädenswil ACW, Wädenswil, Switzerland. Skuhravá, M. (1997) Family Cecidomyiidae. In: Papp, L. and Darvas, B. (eds) Contribution to a Manual of Palaearctic Diptera. Science Herald, Budapest, Hungary, pp. 71–204. Stokes, B.M. (1953) Biological investigations into the validity of Contarinia species living on the Cruciferae, with special reference to the swede midge, Contarinia nasturtii (Kieffer). Annals of Applied Biology 40, 726–741. Strong, D.R. and Larsson, S. (1992) The importance of herbivore population density in natural and agricultural ecosystems. Series Entomologica 49, 5–13. Wu, Q.-J., Zhao, J.-Z., Taylor, A.G. and Shelton, A.M. (2006) Evaluation of insecticides and application methods against Contarinia nasturtii (Diptera: Cecidomyiidae), a new invasive insect pest in the United States. Journal of Economic Entomology 99, 117–122. Chapter 19 139

19 Cydia pomonella (L.), Codling Moth (Lepidoptera: Tortricidae)

Joan Cossentine1 and Charles Vincent2 1Agriculture and Agri-Food Canada, Summerland, British Columbia; 2Agriculture et Agroalimentaire, St Jean-sur-Richelieu, Québec

19.1 Project Status moth control programmes have been found to be highly effi cacious and by 2009, the The codling moth, Cydia pomonella (L.) Okanagan-Kootenay SIR programme had (Lepidoptera: Tortricidae), is a major pest resulted in undetectable codling moth of apple, Malus domestica Borkh. and pear, populations in 37% of its orchard area. In Pyrus communis L. (Rosaceae), orchards the remaining orchard area within the SIR worldwide and in Canada it is found where programme where codling moth were M. domestica are commercially produced found, the majority of the orchards (85%) in British Columbia, Ontario, Quebec, New supported extremely low populations Brunswick and Nova Scotia. In 2000, the (fewer than ten wild caught per codling moth Cydia pomonella granulo- season in one trap per hectare) (Judd and virus (CpGV) (Baculoviridae) was regis- Thompson, 2012). Both SIR and mating tered for use in Canadian orchards. The disruption are effective non-chemical con- strain of virus used for the original trol strategies that integrate extremely well commercial formulation was collected with biological control, although neither from wild Quebec C. pomonella larvae pest management strategy is a classical (Vincent et al., 2007) and the resulting biological control and therefore their in- product, Virosoft CP4® (BioTepp Inc., dependent roles in C. pomonella sup- Quebec) (BioTepp, 2012), was the fi rst pression in Canada during this decade will horticultural viral insecticide registered in not be discussed in this chapter. SIR and Canada. The virus was not extensively mating disruption strategies are only used in eastern Canada from 2001 to 2010 effective when codling moth population where the single generation C. pomonella densities are low and therefore orchards populations are relatively low and are with excessive in-season codling moth suppressed by chemical treatments applied populations were required to be treated by to control other orchard pests (Cossentine an insecticide of which CpGV was an and Vincent, 2001). option. Cydia pomonella is a key apple and Neonate C. pomonella have been shown pear pest in the interior of British Colum- to acquire CpGV on leaf surfaces before bia, where it is managed by the area-wide reaching an apple and therefore can Okanagan-Kootenay Sterile Insect Release contract infections prior to and while programme (SIR) using multiple technolo- entering the fruit (Ballard et al., 2000). The gies including the release of sterile moths virus is highly virulent to neonate C. and mating disruption. Area-wide codling pomonella, however feeding damage prior © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 140 Chapter 19

to mortality is common, with some result- Columbia orchards (A. Bennett, 2007, ing shallow fruit injury post CpGV unpublished results). Mastrus pilifrons had application (Lacey et al., 2008). The been previously reared from C. pomonella virulence of the Virosoft CP4® applied in collected in Victoria and Vernon, British June and early July, under conditions that Columbia although this was the fi rst are typical for the southern interior of recognition that it was an overwintering British Columbia, was found to signifi - codling moth biological control agent in cantly decrease on the leaves by 1 day after the area-wide control programme. application and by day 6 on the apples Cydia pomonella overwinter as dia- (Cossentine and Jensen, 2004). These pausing late instar larvae that frequently results were corroborated by trials con- form cocoons within the wooden bins that ducted in an organic orchard in southern are used by growers to transport their Quebec (Provost et al., 2008). As a result of harvested fruit (Higbee et al., 1999). The these studies, weekly reapplication of the larvae are subsequently moved with the virus was recommended. bins when they are delivered to the pack- Indigenous CpGV played a large role in ing houses and into different orchards the SIR mass codling moth rearing facility when the bins are redistributed in the where it had been found since the colony spring. The redistribution of wild moths was fi rst established in 1993 (Eastwell et results in a re-infestation of C. pomonella al., 1999). In the early 2000s the trans- into orchards where the pest may have mission of the virus within the rearing been reduced or eliminated and therefore facility was documented using molecular bin redistribution is considered an integral tests (Cossentine et al., 2005). The virus part of area-wide C. pomonella manage- was found associated with wing scales and ment. The entomopathogenic nematode eggs, and consequently contaminated egg Steinernema carpocapsae (Weiser) (Rhab- sheet wash water, air fi lters and communal ditida: Steinernematidae) was tested as a rearing trays. Protocols were modifi ed to possible biological control solution to this suppress CpGV transmission within the problem. In Washington State, USA, Lacey facility in order to maintain the health of and Chauvin (1999) demonstrated S. carpo- the SIR colony and the sterile release capsae suppression of sentinel diapausing programme. C. pomonella larvae in miniature bins With the low C. pomonella population immersed in water containing the nema- densities in the commercial fruit-pro- tode and recommended including nema- ducing region of British Columbia, less todes in the fruit packing line. In trials research emphasis was focused on C. conducted in British Columbia, over 80% pomonella parasitism from 2001 through of sentinel C. pomonella larvae placed in 2010. Mastrus ridibundus (Gravenhorst) wooden harvest bins died after the bins (Hymenoptera: Ichneumonidae), an exotic were washed for 1 min with water gregarious ectoparasitoid of larval C. containing 50 S. carpocapsae infective pomonella, was introduced into Washing- juveniles ml−1 in an industrial bin washer ton State orchards as a biological control and held at almost 100% RH (Cossentine et agent in 1997 (Unruh, 1998) and was a al., 2002). The nematodes survived being possible classical biological control intro- continuously pumped through the washer duction for British Columbia. Semio- for over 6 h. chemical studies by Jumean et al. (2005, 2009) determined that M. ridibundus uses C. pomonella aggregation pheromone as a 19.2 Future Needs host-location kairomone. In 2007, a related, solitary ectoparasitoid species, Mastrus Area-wide suppression of the codling moth pilifrons (Provancher) (Hymenoptera: Ich- as a key pest in western Canada has worked neumonidae) was identifi ed parasitizing effectively. diapausing C. pomonella larvae in British Future work should focus on: Chapter 19 141

1. The integration of more biological con- ticide in Quebec orchards where in 2008 trol alternatives, including the effi cacious and 2009 there was evidence of codling use of CpGV, into area-wide control pro- moth resistance to azinphosmethyl and grammes. CpGV may be a valuable biopes- thiachloprid (Bellerose et al., 2011).

References

Ballard, J., Ellis, D.J. and Payne, C.C. (2000) Uptake of granulovirus from the surface of apples and leaves by fi rst instar larvae of the codling moth, Cydia pomonella L. (Lepidoptera: Olethreutidae). Biocontrol Science and Technology 10, 617–625. Bellerose, S., Chouinard, G. and Cormier, D. (2011) Résistance du carpocapse aux insecticides utilisés dans les vergers du Québec: mythe ou réalité? Fiche technique IRDA, Saint-Hyacinthe, QC. Available at: http://www.irda.qc.ca/fr/Publications/27/388 (accessed 22 February 2012). Biotepp (2012) Virosoft CP4 Technical Data sheet. Available at: http://www.biotepp.com/en/ products/docs/Virosoft%20CP4_TechnicalSheet.pdf (accessed 22 February 2012). Cossentine, J.E. and Jensen, L.B.M. (2004) Active persistence of a commercial codling moth granulovirus product on apple fruit and foliage. Journal of the Entomological Society of British Columbia 101, 87–92. Cossentine, J.E. and Vincent, C. (2001) Cydia pomonella (Linnaeus), codling moth (Lepidoptera: Tortricidae) In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada 1981–2000. CAB International, Wallingford, UK, pp. 90–93. Cossentine, J.E., Jensen, L.B. and Moyls, L. (2002) Fruit bins washed with Steinernema carpocapsa (Rhabditida: Steinernematidae) to control Cydia pomonella (Lepidoptera: Tortricidae). Biocontrol Science and Technology 12, 251–258. Cossentine, J.E., Jensen, L.B.M. and Eastwell, K. (2005) Incidence and transmission of a granulovirus in a large codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae) rearing facility. Journal of Invertebrate Pathology 90, 187–192. Eastwell, K.C., Cossentine, J.E. and Bernardy, M.G. (1999) Characterization of Cydia pomonella granulovirus from codling moths in a laboratory colony and in orchards in British Columbia. Annals of Applied Biology 134, 285–291. Higbee, B.S., Calkins, C.O. and Temple, C. (1999) Larval infestation of harvest bins by codling moth. Good Fruit Grower March 15, 26–31. Judd, G. and Thompson, D. (2012) Taking a FLEXible approach to mating disruption in British Columbia. Abstracts, Orchard Pest Management Conference, Portland, Washington, January 2012. Jumean, Z., Unruh, T., Gries, R. and Gries, G. (2005) Mastrus ridibundus parasitoids eavesdrop on cocoon-spinning codling moth, Cydia pomonella, larvae. Naturwissenschaften 92, 20–25. Jumean, Z., Jones, E. and Gries, G. (2009) Does aggregation behaviour of codling moth larvae, Cydia pomonella, increase the risk of parasitism by Mastrus ridibundus? Biological Control 49, 254– 258. Lacey, L.A. and Chauvin, R.L. (1999) Entomopathogenic nematodes for control of codling moth in fruit bins. Journal of Economic Entomology 92,104–109. Lacey, L.A., Thomson, D., Vincent, C. and Arthurs, S.P. (2008) Codling moth granulovirus: a comprehensive review. Biocontrol Science and Technology 18, 639–663. Provost, C., Rasamimanana, H., Vincent, C. and Valéro, J. (2008) VirosoftCP4 fi eld trials in an organic apple orchard. Abstracts, Proceedings of the XXIII International Congress of Entomology, Durban, South Africa, July 2008, p. 2388. Unruh, T.R. (1998) From Russia with love: new predators and parasites for control of tree fruit insect pests. Abstracts, Proceedings of the Washington Horticultural Association 1997, 93, 42–49. Vincent, C.M., Andermatt, M. and Valero, J. (2007) Madex and Virosoft, viral bioopesticides for codling moth control. In: Vincent, C., Goettel, M.S. and Lazarovits, G. (eds) Biological Control: a Global Perspective. CAB International, Wallingford, UK, pp. 336–343. 142 Chapter 20

20 Delia radicum (L.), Cabbage Maggot (Diptera: Anthomyiidae)

Neil J. Holliday,1 Lars D. Andreassen,1 Peggy L. Dixon2 and Ulrich Kuhlmann3 1University of Manitoba, Winnipeg, Manitoba; 2Agriculture and Agri- Food Canada, St John’s, Newfoundland; 3CABI, Delémont, Switzerland

20.1 Pest Status L., and in varieties of B. oleracea L. (Brassicaceae), including cabbage, cauli- The cabbage maggot, Delia radicum L. fl ower, broccoli and Brussels sprouts. (Diptera: Anthomyiidae), known in Europe Among fi eld crops, D. radicum attacks as the cabbage root fl y, has 22 synonyms, of canola, B. napus L. and B. rapa subsp. which Hylemya brassicae (Bouché), Erio- oleifera (DC) Metzger, and mustards, B. ischia brassicae (Bouché) and D. brassicae juncea L. and Sinapis alba L. (Brassi- (Bouché) appear most frequently (Griffi ths, caceae); of these, B. rapa is most and S. 1991). Delia radicum is distributed in alba is least susceptible to maggot attack. temperate regions of the Palaearctic and The severity and extent of economic losses Nearctic, including cultivated regions of all in canola in the Prairie provinces have Canadian provinces (CAB International, increased markedly in recent decades 1989). Canadian populations of D. radicum (Soroka et al., 2004 and references therein). originated from north-western Europe, Root maggots in canola are noted in 14 of probably through a single introduction 30 annual pest reports from the Prairie early in the 19th century (Biron et al., provinces for 2001–2010, with damage 2000). The natural history and manage- most consistently severe in Alberta (Wes- ment of D. radicum is well known (Finch, tern Committee on Crop Pests, 2001–2010). 1989; Griffi ths, 1991; Soroka et al., 2002; Up to fi ve Delia species may be part of the Soroka and Dosdall, 2011), and the reader root maggot complex attacking brassi- is referred to these reviews for details. caceous crops. In prairie canola, D. radi- Delia radicum larvae attack roots of cum is predominant in southern and many Brassicaceae, causing direct injury eastern areas, but in northern growing and allowing entry of root pathogens. regions D. fl oralis (Fallén) (Diptera: Antho- Attacks on young plants often result in myiidae) is more prevalent. plant death. For leafy and seed-bearing Delia radicum overwinters as a dia- crops, yield losses result from inhibition of pausing pupa in the soil. The time of translocation or from lodging, but in root spring emergence is determined by thermal vegetables loss is largely due to reduced accumulations and by whether the insect is quality. Economic losses attributable to D. of the early- or late-emerging phenotype. radicum occur in turnip, Brassica rapa Thermal responses and the proportion of (L.), rutabaga, B. napus var. napobrassica each phenotype vary regionally, probably (L.) Rchb., and radish, Raphanus sativus in response to local climate and prevalent

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 20 143

host crop (Andreassen et al., 2010 and Soil conditions interacting with climatic references therein). Newly emerged adults factors affect survival of immature D. aggregate and mate at nectar sources; radicum, as well as infl uencing stem size carbohydrates are essential for maturation and maggot tolerance of host plants. These of eggs, and protein is required for full interactions no doubt contribute to regional fecundity (Finch and Coaker, 1969). Males differences in response to weather con- stay at aggregation sites, but mated gravid ditions and soil type, and to the com- females leave these sites in low-level plexity of responses to tillage and nutrient fl ights (Bomford and Vernon, 2000) to additions (Soroka and Dosdall, 2011). Con- oviposit in fi elds of host crops, where they sequently, there are no specifi c recom- are the prevalent sex. Females use chemi- mended fertility or tillage practices for cal and visual cues to locate oviposition cultural control of D. radicum in canola. habitat. Canola plants become suitable for Economic factors are favouring reduced oviposition at the time of bolting (Griffi ths, intervals between canola crops on the 1986). At potential oviposition sites, Canadian prairies, and continuous crop- females make repeated short fl ights and ping of canola is sometimes practised. landings: an uninterrupted series of land- After 3 years of continuous cropping, ings on chemically appropriate leaf canola exhibits higher levels of D. radicum surfaces leads to oviposition. Most eggs are damage and lower seed yields than does laid singly, concealed in soil close to a host canola grown in rotational systems plant. Plants with thick stems or that have (Dosdall et al., 2012). Barriers that impede gravid D. radicum been damaged by conspecifi c larvae (Baur females can be used to prevent oviposition. et al., 1996) receive most eggs. Larvae Fly-proof fences 90–135 cm high hatch within 3–10 days and feed initially surrounding vegetable brassicas (Bomford on the root surface of the host plant. and Vernon, 2000; Vernon et al., 2011) and Development through three instars takes polyethylene mesh row covers (P. Dixon et 3–4 weeks, and older larvae tunnel into the al., 2012, unpublished results) can greatly root. Pupation occurs within a puparium reduce crop damage. Row covers provided either in the root or nearby soil. In the similar levels of control to chlorpyrifos in Prairie provinces, D. radicum completes transplanted and direct-seeded rutabaga one generation per year in canola; in (Prasad, 2007, 2009). brassicaceous vegetables there may be 2–4 Increasing vegetational diversity inter- generations per year, depending on locality. rupts the sequence of appropriate landings required before oviposition (Dosdall et al., 2003; Dixon et al., 2004; Parsons et al., 20.2 Background 2007; Broatch et al., 2008a; Hummel et al., 2009). Reducing stem size of canola In conventional production, applications consistently reduces oviposition and infest- of insecticides at planting or as post-emer- ation levels, and can be achieved by gence high-volume drenches can protect delayed seeding or higher seeding rates brassicaceous vegetables from D. radicum (Dosdall et al., 1996, 1998). Reduced stem damage. The only currently registered size appears to be the main mechanism of active ingredient in Canada is chlorpyrifos host plant resistance in a programme to (Health Canada, 2012), and resistance and introgress germplasm from S. alba into B. regulatory issues cast doubt on its future. napus (Dosdall et al., 2000; Ekuere et al., Pesticide labels recommend that drenches 2005). A breeding programme for maggot- be made at set intervals, as gravid D. resistant rutabaga utilizes the S. alba germ- radicum are present in vegetable crops plasm that was previously intro gressed throughout the growing season. There are into B. napus; resistance in ruta baga is no longer any insecticides registered in associated with leaf glucosino lates, which Canada for control of D. radicum in may affect oviposition choice (Malchev et canola. al., 2010). 144 Chapter 20

Natural enemies affect all life stages of chandra et al., 2007). Parasitism by A. D. radicum. Adults are affected by the bilineata of the fi rst available D. radicum bacterium Bacillus thuringiensis Berliner puparia is particularly detrimental to larval (Bacilliaceae), two fungal pathogens, Ento- T. rapae already parasitizing the pupae mophthora muscae (Cohn) Fresenius and (Reader and Jones, 1990). Parasitism by A. Strongwellsea castrans Batko and Weiser bilineata declines with increasing pro- (Entomopthoraceae), and by a nematode portions of non-brassicas mixed with Heterotylen chus sp. (Tylenchida: Sphaeru- rutabaga (Dixon et al., 2004) and canola lariidae). Females infected with either (Hummel et al., 2010) when vegetation fungus fail to produce eggs, and epizootics diversity is increased to reduce D. radicum of S. castrans infl ict signifi cant mortality. oviposition. In addition to the two Eggs and larval stages of D. radicum are ubiquitous parasitoids, Aleochara verna consumed by epigeic predators, particu- Say parasitizes D. radicum puparia in larly adult Carabidae and Staphylinidae. Canada but not in Europe, and Aleochara Hughes and Mitchell (1960) concluded that bipustulata (L.) is restricted to the 90–95% of eggs are eaten, but it is now Palaearctic (Hemachandra et al., 2005, considered that this mortality seldom 2007) where parasitism by this species can exceeds 30% (Finch, 1996). Limitations to exceed 40% (Brunel and Fournet, 1996). predation include diffi culties of predators Low levels of parasitism by other Aleo- fi nding buried D. radicum eggs (Finch and chara and Trybliographa spp. and by Elliott, 1999; L. Andreassen, 2012, un- Phygadeuon spp. (Hymenoptera: Ichneu- published results), alternative prey (Prasad monidae), Trichopria spp. (Hymenoptera: and Snyder, 2010) and intraguild predation Proctotrupidae) and Aphaereta spp. (Prasad and Snyder, 2004, 2006). Increas- (Hymenoptera: Braconidae) have been re- ing vegetation diversity for D. radicum ported in North America and Europe management reduces activity of some (Hemachandra et al., 2007 and references predators and so may reduce mortality of therein). eggs and larvae (Dixon et al., 2004; Broatch et al., 2010). No egg parasitoids of D. radicum are known (Wishart, 1957; Hemachandra et al., 20.3 Biological Control Agents 2007). The larval pupal parasitoid Tryblio- grapha rapae (Westwood) (Hymenoptera: 20.3.1 Pathogens Figitidae) and the pupal parasitoid Aleo- chara bilineata (Gyllenhall) (Coleoptera: Currently there are no biopesticides Staphylinidae) are important sources of registered in Canada for use on Delia spp., mortality in the Palaearctic and the and no trial applications of the natural Nearctic (Hemachandra et al., 2007 and pathogens E. muscae and S. castrans have references therein; Hummel et al., 2010). In been reported. In Finnish fi eld trials, 20 canola in the Prairie provinces, parasitism isolates of fi ve potential fungal biopesticides by A. bilineata is generally higher than that were applied to seedling brassicas, but only by T. rapae (Hemachandra et al., 2007; isolates of Metarhizium anisopliae (Mets- Hummel et al., 2010). In prairie canola, chnikoff) Sorokin (Claviciti paceae) were spring emergence of A. bilineata is well considered promising enough to be worthy synchronized with availability of D. of further study (Vänninen et al., 1999). radicum eggs (Broatch et al., 2008b; Canadian researchers have screened several Andreassen et al., 2010). In the same fungal entomopathogens, including Beau- system, the earliest available D. radicum veria bassiana (Balsamo) Vuillemin (Cordy- puparia have the highest levels of A. cipitaceae), M. anisopliae and Lecanicillium bilineata parasitism, suggesting that para- lecanii (Zimmerman) Zare and W. Gams sitoid larvae are host-seeking before the (=Verticillium lecanii (Zimmerman) Viégas) majority of hosts are available (Hema- (Cordycipitaceae) (P. Dixon et al., 2012, Chapter 20 145

unpublished results). Of these, a com- Diptera species were exposed to A. mercial formulation of M. anisopliae (Met52 bipustu lata larvae in no-choice tests. EC, prototype 2008, Novozymes®) was most Puparia of a non-target anthomyiid, and promising: in the laboratory, an application four Diptera with smaller puparia than D. rate of 1×107 cfu g−1 sand killed 70% of 2nd radicum were consistently suitable for instar larvae (Dixon, 2011). parasitoid development (Andreassen et al., Laboratory screening suggested that the 2009). In follow-up studies, adult A. entomogenous nematode Steinernema bipustulata from small puparia had reduced feltiae (Filipjev) (Rhabdita: Steinerne- lifespans and fecundity (L. Andreassen, matidae) could have useful activity against 2012, unpublished results). Puparia of D. radicum (Morris, 1985), but fi eld trials Lonchaea corticis (Taylor) (Diptera: Lon- with S. feltiae and other entomopathogenic chaeidae), an important predator of the nematodes have failed to provide practical Canadian forest pest Pissodes strobi Peck levels of control of D. radicum (e.g. (Coleoptera: Curculionidae), support Bracken, 1990; Vänninen et al., 1999). develop ment of A. bipustulata. However, There is evidence that applications of S. there appears to be little risk to L. corticis, feltiae reduce parasitoid populations, as A. bipustulata prefers open habitats and particularly those of Aleochara spp. (Niel- has not been found in forests (Andreassen sen and Philipsen, 2004). et al., 2009 and references therein). There is little published about the diet of the predatory adult A. bipustulata, except that it includes immature D. radicum. In no- 20.3.2 Parasitoids and predators choice Petri dish prey range studies of 30 invertebrate groups found in brassica Releases of parasitoids for classical crops, items in most groups were seldom biological control of D. radicum in Canada eaten, but Diptera larvae and immature began in 1949, following surveys in Europe Amara similata Gyllenhal (Coleoptera: and Japan (Table 20.1) (Wishart et al., Carabidae) were frequently eaten (L. 1957). Taxonomic studies and surveys in Andreassen, 2012, unpublished results). As Canada concurrent with the releases Petri dish trials tend to overestimate the (Wishart, 1957), suggested that the species risk of predation on non-target organisms, being released were already in Canada, so the real risk to Canadian Diptera and the biological control programme was dis- Carabidae was investigated by testing the continued (McLeod, 1962). However, A. gut contents of fi eld-collected A. bipustu- bipustulata is not present in Canada lata for the presence of DNA of these non- (Hemachandra et al., 2005), and is a target groups. The DNA of D. radicum was widespread European parasitoid that is detected in 18% of adult A. bipustulata abundant in spring-seeded canola (Hema- from Swiss canola fi elds, but there was no chandra et al., 2007). Therefore, since detection of DNA of A. similata or Bembi- 2004, the potential of A. bipustulata as an dion quadrimaculatum (L.) (Coleoptera: agent for classical biological control of D. Carabidae), which were common Carabidae radicum in canola has been investigated. in the fi elds (L. Andreassen, 2012, Aleochara bipustulata larvae are parasitic unpublished results). on pupae of D. radicum and A. bipustulata It is desirable to have evidence that risks adults eat eggs and larvae of D. radicum. of introducing A. bipustulata will be offset Research has focused on risks to non-target by increased D. radicum mortality. Labora- species, and whether A. bipustulata is tory and fi eld cage studies with A. likely to complement existing natural bipustulata, A. bilineata and the small enemies in Canada and so increase D. carabid B. quadrimaculatum have sug- radicum mortality. gested that the addition of A. bipustulata is Following a review to identify determin- unlikely to increase predation of D. of the host range of A. bipustulata radicum eggs (L. Andreassen, 2012, un- (Andreassen et al., 2007), puparia of 18 published results). Parasitism was studied 146 Chapter 20

Table 20.1. Parasitoids released for Delia radicum management in Canada 1949–1954. Origin in all cases was ‘Europe’, except Aphaereta sp. from Japan. Compiled from Biological Control Investigations Unit (1949, 1952) and MacNay (1953, 1954).

Species Year Location Number released Coleoptera: Staphylinidae Aleochara bilineata (Gyllenhall) 1951 Brandon, MB 1496 Saskatoon, SK 541 1954 Mt Stewart, PEI 730 Aleochara bipustulata (L.) 1949a Chatterton, ON 446 Huff Island, ON 75 Mill Grove, ON 219 1951 Guelph, ON 106 Hymenoptera: Braconidae Aphaereta sp. 1953 Prince Edward County, ON 137 Dacnusa pubescens (Curtis)b 1949 Mill Grove, ON 43

Hymenoptera: Cynipidae Trybliographa rapae (Westwood) 1951 Brandon, MB 496 Trybliographa sp. 1949 Chatterton, ON 226 Huff Island, ON 150 Mill Grove, ON 497 Hymenoptera: Ichneumonidae Phygadeuon trichops Thompson 1949 Mill Grove, ON 10 1954 Uigg, PEI 270 Phygadeuon sp. 1951 Guelph, ON 5 1953 Prince Edward County, ON 175 Holland Marsh, ON 360 aAs Baryodma bipustulata (L.); bAs Rhizarcha pubescens (Curtis); likely leafminer parasitoid mistakenly included in a soil-fi lled laboratory arena, where 30 natural enemies already present in Canada D. radicum puparia were exposed to either when interaction is forced upon the actors, 10 or 20 larvae of A. bilineata, or 10 or 20 so D. radicum mortality across the prairies larvae of A. bipustulata, or a combination could be expected to increase in proportion of 10 larvae of each species (L. Andreassen, to the extent to which A. bipustulata 2012, unpublished results). At these densi- thrives in geographical regions or micro- ties, although A. bipustulata larvae may climates that the other species do not. have experienced intraspecifi c com- Risks to non-target organisms are petition, parasitism was not reduced by infl uenced by the chemical cues that A. competition between the larvae of the two bipustulata uses for host and prey fi nding, species. Aleochara larvae do not survive and the chemicals could be tools for superparasitism of a D. radicum puparium, enhanc ing biological control. Mulches of but generally avoid entry into a previously mustard seed meal increase activity attacked puparium (Fournet et al., 1999). density of adult A. bipustulata, reduce Thus, as a parasitoid, A. bipustulata may maggot damage to brassica vegetables and complement A. bilineata and its introduc- elevate levels of parasitism by A. bipustu- tion may increase mortality of D. radicum lata (Ahlström-Olsson and Jonasson, 1992; pupae. Overall, there is nothing to suggest Riley et al., 2007). Maggot-infested roots of that A. bipustulata disrupts the activities of B. napus give off the volatile dimethyl Chapter 20 147

disulfi de (DMDS) (Ferry et al., 2007), but canola offers an opportunity for reassess- this is not the active volatile in mustard ment of classical biological control as part seed meal (Holliday et al., 2012). Release of of an integrated pest management system DMDS increases pitfall trap catches of for D. radicum (Turnock et al., 1995; adult A. bipustulata, A. bilineata and B. Soroka et al., 2002). Soroka et al. (2002) quadrimaculatum (Ferry et al., 2007), but recommended the surveys (Hemachandra does not enhance mortality of root maggots et al., 2007) that led to the conclusions that (Ferry et al., 2009). In the laboratory, both the recommended ‘Assessment of the Aleochara spp. showed similar responses biotype of A. verna not present in Canada’ to DMDS: restricted area searching was (Soroka et al., 2002, p. 103) actually induced in larvae and resulted in higher referred to A. bipustulata, and that ‘Assess- levels of parasitism of D. radicum puparia; ment of P. trichops’ is unpromising because DMDS repelled newly emerged unmated levels of parasitism by Phygadeuon spp. adults, but induced positive anemotaxis in are low in spring-seeded canola in Europe mated gravid females (J. Du et al., 2012, and Canada (Hemachandra et al., 2007). unpublished results). These responses Since Soroka et al. (2002), considerable re- would facilitate oviposition and the search has been conducted on A. bipustu- parasitism of D. radicum puparia in the lata, and initiation of a petition for its vicinity of D. radicum-infested brassicas. release in Canada is imminent. It is not expected that establishment of A. bipustulata would, by itself, reverse the 20.4 Evaluation of Biological Control trend of increasing severity of root maggot infestations in canola in the Prairie Evaluation of the biological control pro- provinces, but the additional mortality, in gramme of the 1940–1950s is complicated the context of an integrated pest manage- by taxonomic confusion. The programme ment programme (IPM) for D. radicum was designed to protect brassicaceous vege- man agement, may cause the desired pest tables from root maggots, but was con- population reductions. Host-plant resist- current with the introduction of persistent ance and compatible cultural controls synthetic insecticides for this purpose. should also be part of the IPM of root These insecticides create crop environ- maggots in canola. Elucidation of inter- ments that are extremely hostile to natural actions of cultural control measures with enemies (Finlayson et al., 1980). In North mortality from indigenous and introduced America, D. radicum is confi ned to natural enemies is needed. Unfortunately, cultivated land (Griffi ths, 1991), so host- the existing cultural controls of increased specifi c introduced natural enemies, even seeding rates and maintenance of rotation if established before abandonment of the intervals run contrary to the canola programme, may have been subsequently industry’s objectives of reducing input destroyed by insecticides. The emergency costs and increasing production. Continu- registration of cypermethrin in 2011 in ation of the management status quo is response to resistance-related failure of likely to promote further increases in chlorpyrifos (British Columbia, 2011) is a severity of losses due to maggot damage to signal that substitute insecticides will be canola. found for D. radicum control in conven- In brassicaceous vegetables, introduc- tional vegetable production. Thus, new tion of A. bipustulata is likely to be biological control initiatives should not benefi cial in organic and other production focus on conventional vegetable pro- systems with minimal insecticide use. duction. Again, the biological control should be The expansion of canola since the 1970s integrated with other pest management provides a new context for D. radicum, and tools such as exclusion fences and vege- the current and likely future absence of tation diversifi cation, if they are com- insecticides for root maggot control in patible. In these systems, entomopathogens 148 Chapter 20

may have a role to play, if reliably effi - 3. In parallel with efforts to introduce and cacious strains can be identifi ed. However, establish A. bipustulata, coordination of re- the potential for those entomopathogens to search and development by scientists and disrupt predators and parasitoids must be other stakeholders concerned with D. radi- assessed. cum management to produce IPM plans that are favourable to indigenous and intro- duced natural enemies. IPM plans should 20.5 Future Needs be developed for canola and for brassica- ceous vegetable production systems that Future work should include: are organic or have minimal pesticide use. 1. Submission of a petition for the intro- duction of A. bipustulata and, if necessary, additional research conducted to fi ll gaps Acknowledgements in knowledge that are identifi ed during review; We are grateful for the provision of 2. Introductions of A. bipustulata followed unpublished data by J. Du, L. Kott and R. by planned post-release studies to assess Vernon. effi cacy and improve establishment;

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Griffi ths, G.C.D. (1986) Phenology and dispersion of Delia radicum (L.) (Diptera: Anthomyiidae) in canola fi elds at Morinville, Alberta. Quaestiones Entomologicae 22, 29–50. Griffi ths, G.C.D. (1991) Anthomyiidae. Flies of the Nearctic Region 8(2), No. 7. E. Schweizerbart’sche Verlagsbuchhandlung, Science Publishers, Stuttgart, Germany, pp. 953–1040. Health Canada (2012) Product label search. Available at: http://pr-rp.hc-sc.gc.ca/ls-re/index-eng.php (accessed 17 February 2012). Hemachandra, K.S., Holliday, N.J., Klimaszewski, J., Mason, P.G. and Kuhlmann, U. (2005) Erroneous records of Aleochara bipustulata from North America: an assessment of the evidence. The Canadian Entomologist 137, 182–187. Hemachandra, K.S., Holliday, N.J., Mason, P.G., Soroka, J.J. and Kuhlmann, U. (2007) Comparative assessment of the parasitoid community of Delia radicum in the Canadian prairies and Europe: a search for classical biological control agents. Biological Control 43, 85–94. Holliday, A.E., Pak, D.M. and Holliday N.J. (2012) The Aleochara (Coleoptera: Staphylinidae) attractant in mustard seed meal is not dimethyl disulphide. Proceedings of the Entomological Society of Manitoba 67(2011), 5–10. Hughes, R.D. and Mitchell, B. (1960) The natural mortality of Erioschia brassicae (Bouché) (Dipt., Anthomyiidae): life tables and their interpretation. Journal of Animal Ecology 29, 359–374. Hummel, J.D., Dosdall, L.M., Clayton, G.W., Harker, K.N. and O’Donovan, J.T. (2009) Effects of canola-wheat intercrops on Delia spp. (Diptera: Anthomyiidae) oviposition, larval feeding damage, and adult abundance. Journal of Economic Entomology 102, 219–228. Hummel, J.D., Dosdall, L.M., Clayton, G.W., Harker, K.N. and O’Donovan, J.T. (2010) Responses of the parasitoids of Delia radicum (Diptera: Anthomyiidae) to the vegetational diversity of intercrops. Biological Control 55, 151–158. MacNay, C.G. (1953) Summary of parasite and predator liberations in Canada in 1953. The Canadian Insect Pest Review 31, 307–317. MacNay, C.G. (1954) Summary of parasite and predator liberations in Canada in 1954. The Canadian Insect Pest Review 32, 332–341. Malchev, I., Fletcher, R. and Kott, L. (2010) Breeding of rutabaga (Brassica napus var. napobrassica L. Reichenb.) based on biomarker selection for root maggot resistance (Delia radicum L.). Euphytica 175, 191–205. McLeod, J.H. (1962) Part I. Biological control of pests of crops, fruit trees, ornamentals, and weeds in Canada up to 1959. In: McLeod, J.H., McGugan, B.M. and Coppel, H.C. (eds) A Review of the Biological Control Attempts Against Insects and Weeds in Canada. Technical Communication No. 2, Commonwealth Institute of Biological Control, Trinidad. Commonwealth Agricultural Bureaux, Farnham Royal, UK, pp. 1–33. Morris, O.N. (1985) Susceptibility of 31 species of agricultural insect pests to the entomogenous nematodes Steinernema feltiae and Heterorhabditis bacteriophora. Canadian Entomologist 117, 401–407. Nielsen, O. and Philipsen, H. (2004) Occurrence of Steinernema species in cabbage fi elds and the effect of inoculated S. feltiae on Delia radicum and its parasitoids. Agricultural and Forest Entomology 6, 25–30. Parsons, C.K.P., Dixon, P.L. and Colbo, M. (2007) Relay cropping caulifl ower with lettuce as a means to manage fi rst-generation cabbage maggot (Diptera: Anthomyiidae) and minimize caulifl ower yield loss. Journal of Economic Entomology 100, 838–846. Prasad, R. (2007) Root maggot control tactics. Final report to Lower Mainland Horticultural Improvement Association. ES Cropconsult Ltd, Surrey, British Columbia. Prasad, R. (2009) Field-scale evaluation of row covers for cabbage maggot management in rutabagas. Final report to Lower Mainland Horticultural Improvement Association. ES Cropconsult Ltd, Surrey, British Columbia. Prasad, R.P. and Snyder, W.E. (2004) Predator interference limits fl y egg biological control by a guild of ground-active beetles. Biological Control 31, 428–437. Prasad, R.P. and Snyder, W.E. (2006) Polyphagy complicates conservation biological control that targets generalist predators. Journal of Applied Ecology 43, 343–352. Prasad, R.P. and Snyder, W.E. (2010) A non-trophic interaction chain links predators in different spatial niches. Oecologia 162, 747–753. Reader, P.M. and Jones, T.H. (1990) Interactions between an eucoilid (Hymenoptera) and a staphylinid (Coleoptera) parasitoid of the cabbage root fl y. Entomophaga 35, 241–246. Chapter 20 151

Riley, K.J., Kuhlmann, U., Mason, P.G., Whistlecraft, J., Donald, L.J. and Holliday, N.J. (2007) Can mustard seed meal increase attacks by Aleochara spp. on Delia radicum in oilseed rape? Biocontrol Science and Technology 17, 273–284. Soroka, J.J. and Dosdall, L.M. (2011) Coping with root maggots in prairie canola crops. Prairie Soils and Crops Journal 4, 24–31. Soroka, J.J., Kulhmann, U., Floate, K.D., Whistlecraft, J., Holliday, N.J. and Boivin, G. (2002) Delia radicum (L.), cabbage maggot (Diptera: Anthomyiidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 99–104. Soroka, J.J., Dosdall, L.M., Olfert, O.O. and Seidle, E. (2004) Root maggots (Delia spp., Diptera: Anthomyiidae) in prairie canola (Brassica napus L. and B. rapa L.): spatial and temporal surveys of root damage and prediction of damage levels. Canadian Journal of Plant Science 84, 1171–1182. Turnock, W.J., Boivin, G. and Whistlecraft, J.W. (1995) Parasitism of overwintering puparia of the cabbage maggot, Delia radicum (L.) (Diptera: Antomyiidae), in relation to host density and weather factors. Canadian Entomologist 127, 535–542. Vänninen, I., Hokkanen, H. and Tyni-Juslin, J. (1999) Screening of fi eld performance of entomopathogenic fungi and nematodes against cabbage root fl ies (Delia radicum L. and D. fl oralis (Fall.); Diptera, Anthomyiidae). Acta Agriculturae Scandinavica, B - Soil and Plant Science 49, 167–183. Vernon, R.S., Blackshaw, R. and Prasad, R. (2011) Large scale demonstration of exclusion fences for management of cabbage root maggot Delia radicum: opportunities for IPM? IOBC/WPRS Bulletin Integrated Protection of Field Vegetables 65, 23–31. Western Committee on Crop Pests (2001–2010) Annual meeting minutes. Available at: http://www. westernforum.org/WCCP%20Minutes.html (accessed 16 February 2012). Wishart, G. (1957) Surveys of parasites of Hylemya spp. (Diptera: Anthomyiidae) that attack cruciferous crops in Canada. Canadian Entomologist 89, 450–454. Wishart, G., Colhoun, E.H. and Monteith, E.A. (1957) Parasites of Hylemya spp. (Diptera: Anthomyiidae) that attack cruciferous crops in Europe. Canadian Entomologist 89, 510–517. 152 Chapter 21

21 Drosophila suzukii (Matsumura), Spotted Wing Drosophila (Diptera: Drosophilidae)

Howard M.A. Thistlewood,1 Gary A.P. Gibson,2 David R. Gillespie3 and Sheila M. Fitzpatrick3 1Agriculture and Agri-Food Canada, Summerland, British Columbia; 2Agriculture and Agri-Food Canada, Ottawa, Ontario; 3Agriculture and Agri-Food Canada, Agassiz, British Columbia

21.1 Pest Status America were in 2008 from California, although D. suzukii may have been present Spotted wing drosophila, Drosophila earlier (Hauser, 2011). In Canada, it was suzukii (Matsumura) (Diptera: Droso- found in British Columbia in 2009, fi rst philidae), is a newly established invasive throughout the Lower Mainland associated insect in North America. It feeds on the with signifi cant damage to berry crops, then fruit of a wide range of cultivated and non- later in the year in the Okanagan Valley cultivated plants, and has caused signifi - (Thistlewood et al., 2012). By July 2011 it cant damage in some locations or years, had been reported from Ontario, Quebec, with grave consequences for integrated Manitoba and Alberta (Anonymous, 2011), pest management (IPM) programmes and and it continues to spread within Canada. pesticide use (Walsh et al., 2011). In Japan Research into its biology and agronomic and elsewhere, D. suzukii has regularly effects began in each effected province caused considerable crop losses, often 20– almost immediately after detection. 80% of fruit (Kanzawa, 1939; Lee et al., Unlike most vinegar fl ies, which 2011). Therefore, it poses a serious risk to normally infest overripe, fallen, decaying some fruit and berry industries in western fruit, females lay their eggs inside sound North America. The recent collection of fruit before harvest. This contaminates fruit endemic natural enemies of drosophilid with larvae and causes it to become soft fl ies from D. suzukii in British Columbia and unmarketable, often followed by and Oregon in the USA suggests great invasion of other drosophilid species value for biological control efforts in the attracted to the decaying fruit. It is classi- future. fi ed amongst Japanese drosophilid fl ies as a fruit specialist (Mitsui et al., 2010), and known to infest thin-skinned fruit includ- 21.2 Background ing: blueberry, Vaccinium spp. (Ericaceae); sweet cherry Prunus avium (L.) L., sour Drosophila suzukii is an oriental species of cherry P. cerasus L., strawberry Fragaria × vinegar fl y that was fi rst reported outside ananassa Duschesne ex Rozier, raspberry Asia from Hawaii in 1980. The fi rst Rubus idaeus L., blackberry R. fructicosus confi rmed records in continental North L., peach P. persica var. persica Dippel,

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 21 153

nectarine P. persica var. nucipersica defi nitely parasitoids of D. suzukii, because Dippel, plum P. domestica L. (Rosaceae); they were reared directly from the host on and grape, Vitis vinifera L. (Vitaceae) (cf. several occasions. Kanzawa, 1939; Guo, 2007; Mitsui et al., Pachycrepoideus vindemmiae was de- 2010). In Europe, it was reared recently scribed in 1875 from Italy and is a from: fi g, Ficus sp. (Moraceae); honey- cosmopolitan parasitoid known from every suckle, Lonicera sp. (Caprifoliaceae); biogeographic realm. It is a primary or European black elderberry, Sambucus facultative pupal, idiobiont hyperpara- nigra L. (Adoxaceae); and alder buckthorn, sitoid, primarily of 12 different families of Frangula alnus Mill. (Rhamnaceae) (Lee et higher Diptera (48 species recorded) al., 2011). Since 2010, it has been reared in (Wharton, 2012). It is commonly reported the British Columbia interior from fi eld- in the biological literature, mostly as a collected fruits of: tall Oregon-grape parasitoid of fi lth-breeding fl ies, but also as Mahonia aquifolium (Pursh) Nutt. (Berberi- a parasitoid of Drosophila melanogaster daceae); elderberry Sambucus sp., blue Meigen (Diptera: Drosophilidae) (Wang and elderberry S. cerulea Raf. var. cerulean Messing, 2004), of D. suzukii (Chabert et al., (Adoxaceae); Tatarian honeysuckle Lonicera 2012), or fruit fl ies (Diptera: Tephri tidae), tatarica L. (Caprifoliaceae); northern black- and has been recorded frequently from currant Ribes hudsonianum var. petiolare various habitats across Canada including (Douglas) Jancz, golden currant, Ribes fruit crops. Wharton (2012) mentions its aureum Pursh (Grossulariaceae); and tendency to attack hosts such as Mahaleb cherry, Prunus mahaleb L. (Rosa- drosophilids, even when mass-reared for ceae) (H.M.A. Thistlewood and B. Rozema, release against tephritid pests, and its ready 2012, unpublished results). ability to expand its host range to other species was noted by Wang and Messing (2004). Pachycrepoideus vindemmiae has 21.3 Biological Control Agents been reared from Sarcophagidae and Tachinidae that are primary parasitiods of Natural enemies of D. suzukii have been Coreidae (Hemiptera) and Lepidoptera, as known since the fi rst comprehensive publi- well as from a wide variety of parasitic cation on this pest, when a Phaenopria sp. Hymenoptera (Wharton, 2012). The (Hymenoptera: Diapriidae) was found potential of P. vindemmiae for biological attacking it in Japan (Kanzawa, 1939). control of D. suzukii was made obvious in However, the literature to date has very few Summerland, British Columbia, when in reports of its natural enemies in Asia (Guo, 2010 it moved between insect rearing cages 2007; Mitsui et al., 2007). (BugDorm, BioQuip Products, California, The fi rst natural enemies recorded for D. USA) through tiny cracks at joints. It built suzukii in Canada were Pachycrepoideus up rapidly and eliminated several vindemmiae (Rondani) (Hymenoptera: populations of D. suzukii that were being Pteromalidae) collected in the British reared on unsprayed berries and cherries. Columbia interior in 2010. Similar col- Vrestovia brevior was described in 1993 lections in Hood River, Oregon, at the same from ‘Drosophila sp.’ on apple in Massa- time also yielded P. vindemmiae (P. chusetts, USA (Bouc ˇek, 1993). It is Shearer, 2010, Hood River, Oregon, pers. restricted to North America and is trans- comm.). In 2011, a second parasitoid, continental in distribution. Previously pub- Vrestovia brevior Boucek (Hymenoptera: lished records include locations in Canada Pteromalidae), was identifi ed from col- (Alberta, British Columbia, Ontario, Quebec) lections in the Lower Mainland, British and the USA (Maryland, Massachusetts, Columbia and was successfully reared on Michigan, Pennsylvania, Virginia), but there puparia of D. suzukii. The P. vindemmiae are specimens in the Canadian National and V. brevior records are new and both are Collection of Insects from Saskatchewan 154 Chapter 21

and New Brunswick, as well as from National Collection of Insects. Future rear- Florida, Louisiana, Montana, North Caro- ings and generic or specifi c identifi cations lina, Ohio, South Carolina and West should provide further insight into the Virginia in the USA. It was successfully recent collections. Unfortunately, early reared on puparia of D. suzukii in 2011. indications are that European larval para- Little else is known about the species, but sitoids do not attack D. suzukii to a great based on the reported numbers to date V. extent (Chabert et al., 2012) and suggest brevior is less common as a parasitoid of D. that host switching of more specialized suzukii than is P. vindemmiae. local parasitoids in North America may be In 2011, in the lower mainland of equally unsuccessful. British Columbia, parasitoids were reared There are presently ongoing surveys for from D. suzukii that were placed as eggs, natural enemies of D. suzukii in Asia by within fermenting banana baits, in and other agencies. A parasitoid survey in around small-fruit fi elds. These included Japan revealed a complex of parasitoids on Asobara sp., likely A. tabida Nees von D. suzukii that is similar in composition to Esenbeck (Hymenoptera: Braconidae), that found in coastal British Columbia Ganaspis sp., Trybliographa sp., Kleido- (Mitsui et al., 2007), so whether or not toma sp. (Hymenoptera: Figitidae) and V. natural enemies can generally restrain brevior. Other Drosophila spp. were reared populations from outbreak levels is unclear from the baits seeded with D. suzukii, so because D. suzukii is reportedly managed the parasitoids reared from these traps may only by heavy pesticide use within Japan. have been associated with species other Somewhat paradoxically, D. suzukii is very than D. suzukii. Asobara tabida was the common in traps in Hawaii (Leblanc et al., most abundant parasitoid, followed by V. 2009), but is not of concern in their context brevior, and no specimens of P. vindem- of area-wide integrated pest management miae were found. Ganaspis xanthopoda (IPM) programmes for other pests. This is (Ashmead) (Hymenoptera: Figitidae) has one reason for research to determine if any been reared from D. suzukii in Japan limiting factors are present elsewhere, (Mitsui and Kimura, 2010). Species of which could be employed in its new range. Trybliographa and Kleidotoma are para- sitoids of small Diptera, so it is conceivable 21.4 Future Needs that both of these were actually reared from a Drosophila host. Also in 2011, other As a new and economically signifi cant in- potential parasitoids were reared in the vasive species, future work should include: laboratory in Summerland out of col lec- tions of cherries made well after harvest 1. Study of the basic biology and ecology that were infested with D. suzukii. These of D. suzukii in Canada, including its host yielded mostly P. vindemmiae, a few V. range, crop damage and associated thresh- brevior, Aprostocetus sp. (Hymenoptera: olds, response to environmental conditions Eulophidae), a male of the family and ability to overwinter, and pest manage- Encyrtidae, and three non-chalcidoids ment (cf. Lee et al., 2011); including Ceraphron sp. (Hymenoptera: 2. Searching for native species, e.g. Ceraphronidae) and Asobara sp. (Hymen- Braconidae, Eucoilidae or Figitidae (Cyni- optera: Braconidae). In view of the very poidea) and Diapriidae (Diaprioidea), that few individuals reared, it is possible that may expand their host range from other these latter parasitoids were reared from drosophilids or similar-sized hosts to D. some other host(s) on or in the fruit. Only suzukii; more rearings will clarify this, but the 3. Collaboration with colleagues elsewhere alysiine braconid might well be a valid who are already examining the putative record because this genus is a small group centres of origin of D. suzukii in Asia for known to parasitize drosophilid fl ies, with possible species for classical biological at least three species in the Canadian control. Chapter 21 155

Acknowledgements Oregon, USA), as well as Grant McQuate (USDA-ARS, Hilo, Hawaii, USA) for We thank Tracy Hueppelsheuser and valuable discussions. H.M.A.T. was aided Susanna Acheampong (BC Ministry of Agri- via a fellowship under the OECD Co- culture, Abbotsford and Kelowna, BC) for operative Research Programme: Biological collaborations; Brigitte Rozema, Naomi Resource Management for Sustainable Agri- DeLury (AAFC, Summerland) and Peggy cultural Systems, in the laboratory of Laura Clarke (AAFC, Agassiz) for technical assist- Monteiro Torres, CITAB, School of Agri- ance; Peter Shearer and Preston Brown culture & Veterinary Sciences, University of (Oregon State University, Hood River, Trás-os-Montes and Alto Douro, Portugal.

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Anonymous (2011) RMD-11-01: Pest Risk Management Document – Drosophila suzukii (spotted wing drosophila). Canadian Food Inspection Agency, Ottawa, Ontario. Available at: http://www.inspection.gc.ca/plants/plant-protection/directives/risk-management/rmd-11-01/ eng/1330738873775/1330738972893 (accessed 31 October 2012). Bouc ˇek, Z. (1993) New taxa of North American Pteromalidae and Tetracampidae (Hymenoptera), with notes. Journal of Natural History 27, 1271–1272. Chabert, S., Allemand, R., Poyet, M., Eslin, P. and Gibert, P. (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biological Control 63, 40–47. Guo, J.-M. (2007) Bionomics of fruitfl ies, Drosophila melanogaster, damage cherry in Tianshui. Chinese Bulletin of Entomology 44, 743–745. Hauser, M. (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identifi cation. Pest Management Science 67, 1352–1357. Kanzawa, T. (1939) Studies on Drosophila suzukii Mats. Yamanashi Agric. Exp. Station, Kofu, Japan. Leblanc, L., Rubinoff, D. and Vargas, R.I. (2009) Attraction of nontarget species to fruit fl y (Diptera: Tephritidae) male lures and decaying fruit fl ies in traps in Hawaii. Environmental Entomology 38, 1446–1461. Lee, J.C., Bruck, D.J., Dreves, A.J., Ioriatti, C., Vogt, H. and Baufeld, P. (2011) Focus: Spotted Wing Drosophila, Drosophila suzukii, across perspectives. Pest Management Science 67, 1349–1351. Mitsui, H. and Kimura, M.T. (2010) Distribution, abundance and host association of two parasitoid species attacking frugivorous drosophilid larvae in central Japan. European Journal of Entomology 107, 535–540. Mitsui, H., Van Achterberg, K., Nordlander, G. and Kimura, M.T. (2007) Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. Journal of Natural History 41, 1731–1738. Mitsui, H., Beppu, K. and Kimura, M.T. (2010) Seasonal life cycles and resource uses of fl ower- and fruit-feeding Drosophilid fl ies (Diptera: Drosophilidae) in central Japan. Entomological Science 13, 60–67. Thistlewood, H., Shearer, P.W., Van Steenwyk, R., Walton, V. and Acheampong, S. (2012) Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), a new pest of stone fruits in western North America. Integrated Protection of Fruit Crops IOBC/wprs Bulletin 74, 133–137. Walsh, D.B., Bolda, M.P., Goodhue, R.E., Dreves, A.J., Lee, J., Bruck, D.J., Walton, V.M., O’Neal, S.D. and Zalom, F.G. (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management 2, 1–7. Wang, X.G. and Messing, R.H. (2004) The ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), attacks other primary tephritid fruit fl y parasitoids: host expansion and potential non-target impact. Biological Control 31, 227–236. Wharton, R.A. (2012) Parasitoids of fruit-infesting Tephritidae. Available at: http://www.paroffi t.org/ public/site/paroffi t/home (accessed 31 October 2012). 156 Chapter 22

22 Enarmonia formosana Scopoli, Cherry Bark Tortrix (Lepidoptera: Tortricidae)

Wade H. Jenner,1 Emma J. Jenner,1 Ulrich Kuhlmann,1 Andrew M. Bennett2 and Joan E. Cossentine3 1CABI Europe-Switzerland, Delémont, Switzerland; 2Agriculture and Agri-Food Canada, Ottawa, Ontario; 3Agriculture and Agri-Food Canada, Summerland, British Columbia

22.1 Pest Status (Roediger, 1956), the known host range of E. formosana in Europe and North America The cherry bark tortrix, Enarmonia formo- also includes apple, Malus spp., quince, sana Scopoli (Lepidoptera: Tortricidae), is Cydonia oblonga Mill., pear, Pyrus spp., native to the Palaearctic where it has a fi rethorn, Pyracantha spp., hawthorn, history of minor to moderate importance as spp., and mountain ash, Sorbus a pest. However, since it was fi rst identifi ed spp. (Rosaceae) (Dang and Parker, 1990). A in Richmond, British Columbia in 1989 survey of infested plant species in 2001– (Dang and Parker, 1990), E. formosana has 2002 confi rmed occasional E. formosana established itself as a key pest of orna- infestations in Vancouver and Victoria, mental cherries, Prunus serrulata Lindl. British Columbia residential areas in (Rosaceae), along the Pacifi c coast down to mountain ash, apricot and English laurel, Oregon, USA (Klaus, 1992). In 2000, an E. Prunus laurocerasus L. (Rosaceae). In formosana adult was trapped on the east general, older trees appear to be more side of the Cascades in Salmon Arm, susceptible to attack. British Columbia and subsequent phero- Damage is caused by E. formosana mone trap surveys found occasional E. larvae, which feed between the cork and formosana further south in the dry interior cambium of the trunk and major limbs. fruit-producing Okanagan and Similka- The damaged areas of bark expand with meen valleys. Enarmonia formosana moths each successive generation, sometimes (identity verifi ed by Dr J.-F. Landry, AAFC, resulting in the death of large branches or Ottawa) were trapped in Vernon, West even entire trees (Winfi eld, 1964). Kelowna, Oliver and Cawston by 2006. Densities of E. formosana larvae on trees in Discovery of E. formosana in traps in the North America are signifi cantly higher than interior region was extremely rare and no in Europe (Jenner et al., 2004). It has tree infestations were found at these caused serious damage to ornamental locations. While the preferred host plants cherry trees in city boulevards and there is are cherry, Prunus avium (L.) L., plum, concern that, if left unchecked, E. Prunus nigra Aiton, almond, Prunus dulcis formosana could pose a risk to the fruit (Mill.) D.A. Webb, apricot, Prunus industry in British Columbia and in armeniaca L., and peach and nectarine, Washington and Oregon in the USA. Prunus persica (L.) Batsch (Rosaceae) Enarmonia formosana overwinters in © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 22 157

the larval stage. Sermann and Zahn (1986) application of entomopathogenic nema- found that larval feeding activity ceases todes (Murray et al., 2004; C. McNair, completely once the temperature drops Burnaby, British Columbia, 2001, pers. below a threshold of approximately 7°C. comm.), and biological control with the The species is univoltine, although native egg parasitoid Trichogramma cacoe- pheromone-based trapping of males in both ciae Marchal (Hymenoptera: Trichogram- Europe and the USA has revealed a matidae) (Breedveld and Tanigoshi, 2007). bimodal fl ight pattern. The fi rst peak of Many of these management approaches activity occurs in May or June and the have caused a reduction in local pest second in late-July or August, depending densities; however, most are not con sist- on seasonal temperatures (Roediger, 1956; ently reliable or viable. The extended fl ight Winfi eld, 1964; Tanigoshi et al., 1998). season of E. formosana, for instance, can Enarmonia formosana eggs are deposited make chemical control very diffi cult or singly or in small clusters on the trunk of impractical (Klaus, 1991). host trees. Ovipositing females apparently In the late 1990s, the Washington State prefer sites where the bark has been Department of Agriculture, Oregon Depart- damaged by previous feeding or pruning ment of Agriculture and Washington State (Roediger, 1956). University launched a survey for native A 1st instar larva immediately seeks parasitoids that attack the immature stages shelter and feeds exclusively in the outer of E. formosana in north-western Washing- part of the phloem. The solitary larva lives ton. This investigation found several completely concealed beneath the bark, species of Hymenopteran parasitoids expanding its feeding tunnel as it grows. believed to be associated with E. for- The entrance to the feeding tunnel is mosana. These belonged to the families sealed off with silk and faecal matter. This Tricho grammatidae, Scelionidae and Ich- protective structure, or ‘frass tube’, is neu monidae, including Itoplectis quadri- enlarged over time and ultimately serves as cingulata (Provancher) and Pimpla the pupation site. The frass tube is the only hesperus (Townes), Braconidae, Eupel- visual cue revealing the location of E. midae and Eurytomidae. However, the formosana and it also plays a role in the combined parasitism rate of all species was detection of larvae by specialist natural very low: 1.7% in 1997 and 2.1% in 1998 enemies (see below). (Tanigoshi et al., 1998). A similar survey of E. formosana larvae and pupae was conducted in infested ornamental cherry 22.2 Background trees in Vancouver and Victoria, British Columbia from 2001 to 2003. Indigenous Active control measures applied against E. parasitism in 2002 was 1.7% in Vancouver formosana in Europe include the appli- (n=237: four Pimpla hesperus were reared). cation of insecticides, creosote and tar oil, No parasitoids were found in Vancouver mechanical removal of dead and peeling (n=29) or Victoria (n=223) in 2001 and bark, thinning of the tree canopy, reduction none in the Vancouver or Victoria survey of orchard tree density (Roediger, 1956) areas in 2002 (n=231) or 2003 (n=216). In a and removal of vegetation from the bases of separate survey, three Diadegma sp. trees (Dickler and Zimmerman, 1972). In (Ichneumonidae) were reared from E. general, however, it is rare that European formosana in New Westminster, British farmers make any efforts to manage E. Columbia in 2001. All voucher specimens formosana in their orchards. In North of the parasitoids are deposited at the America, attempts have been made to Canadian National Collection of Insects in regulate E. formosana densities through Ottawa. pyrethroid or organophosphate application A literature review found only three (Murray et al., 1998), pheromone-based publications that describe the natural mating disruption (McNair et al., 1999), enemies of E. formosana in Europe and 158 Chapter 22

Asia. The natural enemies reported prior to reared from E. formosana larvae and 2000 are listed in Table 22.1. Since no pupae, then sent to taxonomic experts for mortality levels were provided in identifi cation (Table 22.2). association with these natural enemies, their importance in the suppression of E. formosana populations is not known. 22.3 Biological Control Agents An extensive fi eld survey for E. formosana and its parasitoids was carried 22.3.1 Parasitoids out in central Europe from 2000 to 2003. Each year, fi eld sampling was conducted at 22.3.1.1 Campoplex dubitator several sites between late April and mid- September, when E. formosana larvae were The only parasitoid rigorously investigated actively feeding and it was possible to as a potential classical biological control locate their feeding tunnels (Jenner et al., agent for E. formosana in Canada is 2004). This survey specifi cally targeted Campoplex dubitator Horstmann (Hymen- sweet cherry trees, including both culti- optera: Ichneumonidae). It was the para- vated and wild varieties. Once each feed- sitoid most commonly recovered from ing tunnel was located, the E. formosana fi eld-collected E. formosana hosts in larva or pupa was mechanically removed Europe and from all survey regions (Table from beneath the bark and then reared in 22.2; Jenner et al., 2004). This koinobiont the laboratory. Twelve primary parasitoid parasitoid oviposits in the larvae of E. and one hyperparasitoid species were formosana. The immature parasitoid only

Table 22.1. Arthropod natural enemies associated with Enarmonia formosana in European literature (pre- 2000). Host stage Predator/parasitoid species attacked Reference Comments Raphidioptera: Raphidiidae Agulla xanthostigma (Schummel) larva Boldyrev and An important predator of young Dobroserdov larvae (1981) Hymenoptera: Ichneumonidae Lissonota versicolor Holmgren ? Schuetze and Host was likely incorrectly Roman (1931) identifi ed as E. formosana (K. Horstmann, Germany, 2003, pers. comm.) Campoplex difformis (Gmelin) larva Roediger (1956) Possibly a misidentifi cation of (reported as C. mutabilis Campoplex dubitator since Holmgren) this species, a close relative of C. mutabilis, was only described in 1985 (K. Horstmann, Germany, 2003, pers. comm.) Isadelphus inimicus (Gravenhorst) larva Roediger (1956) (reported as Hemiteles inimicus Gravenhorst) Hymenoptera: Braconidae Apanteles laevigatus (Ratzeburg) larva Roediger (1956) (reported as Dolichogenidea laeviagata Ratzeburg) Diptera: Tachinidae aurea (Fallén) larva Roediger (1956) Chapter 22 159

Table 22.2. Parasitoids reared from immature Enarmonia formosana specimens collected in central European fi eld studies (2000–2003). Frequency of Host stage collection Parasitoid species attacked (% of total) Comments Hymenoptera: Ichneumonidae Campoplex dubitator Horstmann Larva 86.1 The only parasitoid to be collected in all 3 survey regions Tycherus vagus (Berthoumieu) Pupa 4.4 Pimpla spuria Gravenhorst Pupa 4.1 Theroscopus hemipteron (Riche) 1° parasitoid 1.4 Hyperparasitoid Pimpla contemplator (Müller) Pupa 0.3 Pimpla turionellae (Linnaeus) Pupa 0.3 Gelis longicauda (Thomson) Pupa 0.3 Isadelphus inimicus (Gravenhorst) Larva 0.3 Lissonota sp. Larva 0.3 Mastrus sp. Pupa 0.3 Pupa 0.3 Hymenoptera: Pteromalidae Dibrachys affi nis Masi Pupa 1.4 Cyclogastrella simplex (Walker) Pupa 0.3

kills and fully consumes its host when the rendering them completely unsuitable for latter has spun its pupation cocoon. In parasitoid development, while 50% of preparation for detailed studies of C. parasitized 2nd instar larvae also died dubitator behaviour and host range, prematurely. In contrast, early mortality alternative methods for the production of was only 15–30% for larvae parasitized in E. formosana and C. dubitator were the 3rd to 5th instars. Regardless of the investigated. While rearing E. formosana instar at oviposition, approximately 90% on an artifi cial (bean-based) diet was of the host larvae that survived until relatively successful and signifi cantly less cocoon formation yielded parasitoids. labour-intensive, larval survival was higher Jenner and Kuhlmann (2006) further and development time was faster when showed that the younger the host larva at larvae were allowed to feed on fresh cherry the time of parasitism, the larger and more bark (Jenner et al., 2005a). Furthermore, fecund the parasitoid offspring will be. parasitized E. formosana larvae feeding on However, there is a direct trade-off between cherry bark yielded more fecund para- fecundity and development time for C. sitoids (roughly 50% more ovarioles) than dubitator because the parasitoids always parasitized larvae given artifi cial diet kill the host at the end of the host’s larval (Jenner et al., 2005b). A critical argument development. for using cherry bark in the parasitoid Campoplex dubitator females searching production system is that frass tubes for concealed E. formosana larvae rely constructed by E. formosana larvae feeding heavily on chemical cues emitted by the on artifi cial diet are not recognized by C. faecal pellets that make up the host’s frass dubitator and therefore do not stimulate tube. Volatile cues from the frass enable the oviposition behaviour in the parasitoid. parasitoids to locate the host feeding sites Jenner et al. (2005b) demonstrated that and, once found, contact cues in the frass C. dubitator will attack all E. formosana material elicit a strong oviposition larval instars. However, all parasitized 1st response (Jenner et al., 2005b). Enarmonia instar larvae died shortly after the attack, formosana larvae, particularly later instars 160 Chapter 22

with deeper tunnels, are often out of reach member of the C. difformis group). Campo- of the parasitoid’s ovipositor. Furthermore, plex capitator is a known natural enemy of E. formosana feeding sites are often the European grapevine moth Lobesia abandoned and C. dubitator does not botrana (Denis & Schiffermüller) and the appear to be able to effectively distinguish European grape berry moth Eupoecilia between occupied and recently abandoned ambiguella Hübner (Lepidoptera: Tortri- host mines. Using laboratory assays, Jenner cidae). According to Horstmann (1985), C. and Roitberg (2009) observed that C. capitator and C. dubitator can be separated dubitator forages more effi ciently at lower based on differences in the dimensions of host densities, which fi ts with patterns of the female antennae, but we were not able parasitism observed in the fi eld in Europe. to fi nd consistent differences in the Host-range assessment for C. dubitator antennae of our specimens of these two has been complicated not only by rearing species. The molecular analysis found such challenges but also by taxonomic uncer- minor variation that the two species tainty regarding it and other species within appeared to be one. Campoplex capitator the Campoplex difformis (Gmelin) group specimens from France showed no (Hymenoptera: Ichneumonidae). When C. consistent differences in COI and D2 and dubitator was fi rst described (Horstmann, only four base-pair differences in ITS2 1985), it was thought to have at least eight compared to C. dubitator, while C. capi- tortricid hosts. This reported host range tator specimens from Hungary showed no has since been questioned due to sus- differences in ITS2 from C. dubitator picions that C. dubitator may be a species whatsoever (Hunt and Kuhlman, 2007, complex with cryptic species or subspecies 2008). Therefore, the only supporting evi- (Hunt and Kuhlmann, 2006). Since morpho- dence that these two ‘species’ are separate logical characteristics seemed insuffi cient is based on the very different host range to defi nitively separate species in the C. and their associated habitats (external difformis group, a number of molecular feeders on grapes compared to cambium and behavioural studies were conducted feeders under the bark of cherry trees). between 2005 and 2008 to test the To resolve this taxonomic puzzle, hypothesis that C. dubitator parasitoids studies were undertaken to fi nd corroborat- reared from E. formosana larvae were a ing independent evidence of the presence single species and uniquely associated or absence of isolating mechanisms with that host. between these two species. Campoplex To test this, two sequences from the dubitator females were placed in arenas nucleus were obtained: the D2 region of with the frass from L. botrana larvae fed on 28S ribosomal DNA, and the internal grapes to assess whether the faecal material transcribed spacer 2 (ITS2) region, as well would stimulate oviposition behaviour as as one mitochondrial sequence: the ‘DNA does E. formosana frass. Indeed, approxi- barcode’ region of cytochrome oxidase I mately one-third of the tested parasitoids (COI). These sequences were compared probed the L. botrana frass with their between C. dubitator specimens reared ovipositors (Hunt and Kuhlmann, 2008). In from E. formosana larvae collected in the next experiment, the suitability of L. eastern France, north-western Switzerland, botrana for C. dubitator development was south-western and north-eastern Germany, evaluated by inducing C. dubitator females and south-eastern UK. All three sequences to oviposit in L. botrana and E. formosana showed no consistent variation between larvae. This was done by offering a larva of these populations (Hunt and Kuhlmann, each species sequentially and by covering 2007). Subsequent molecular comparisons both types of larvae with frass from E. using the CO1, D2 and ITS2 gene regions formosana. It had been planned to were made between C. dubitator and the simultaneously assess whether C. capitator closely related C. capitator Aubert reared from L. botrana could develop on E. (Hymenoptera: Ichneumonidae) (also a formosana hosts, but this was not possible Chapter 22 161

due to a lack of available C. capitator able nematodes Steinernema carpocapsae parasitoids. From 125 paired replicates, not (Weiser) and S. feltiae (Filipjev) (Rhabdi- one C. dubitator offspring emerged from tida: Steinernematidae). This study also the parasitized L. botrana larvae, whereas examined methods for evaluating resultant several emerged from the E. formosana mortality of the concealed pest larvae as hosts (Hunt and Kuhlmann, 2008). This well as the effi cacy of different pre- indicates that the L. botrana hosts were treatment preparation methods. The either rejected at oviposition or were protocol described by Murray et al. (2004) physio logically unsuitable for the develop- was later used to conduct similar treat- ment of C. dubitator. It is possible that the ments of commercially acquired S. carpo- development time of L. botrana larvae is scapsa and Heterorhabditis sp. (Rhabditida: too short to allow C. dubitator to complete Heterorhabditidae) on portions of infested its development before this host pupates. ornamental cherry tree trunks in Victoria, These collective results suggest that C. British Columbia in 2004 (J. Cossentine, dubitator reared from E. formosana may 2012, unpublished results). have a relatively restricted host range; however, further assays would be needed with additional tortricid species to 22.4 Evaluation of Biological Control delineate the limits of C. dubitator’s host range. 22.4.1 Parasitoids

22.4.1.1 Campoplex dubitator 22.3.1.2 Trichogramma cacoeciae The study results described above suggest The egg parasitoid Trichogramma cacoeciae that C. dubitator shows some promise as a Marchal (Hymenoptera: Trichogram- classical biological control agent against E. matidae), widely used as a biological formosana; however, a number of logistical control agent against orchard pests (Herz and taxonomic issues need to be resolved and Hassan, 2006), was observed to before comprehensive host range tests can occasionally parasitize E. formosana eggs be achieved. in Washington State. Inundative biological control trials using this native egg 22.4.1.2 Trichogramma cacoeciae parasitoid were conducted at urban sites around Seattle, Washington in 2001 and At the end of each fi eld season in 2001 and 2002 (Breedveld and Tanigoshi, 2007). 2002, the average parasitism of E. formo- These T. cacoeciae trials assessed rates of sana eggs by mass-released T. cacoeciae egg parasitism, dispersion of parasitoids across all fi eld sites around Seattle, from release points and year-to-year Washing ton was 74% and 72%, colonization of the E. formosana host respectively (Breedveld and Tanigoshi, population. 2007). Both the E. formosana and T. cacoeciae adults appear to have high fi delity to the tree on which they 22.3.2 Nematodes developed, and thus exhibit low dispersal rates. The authors observed a reduction in Entomopathogenic nematodes have been E. formosana populations at trial sites in shown to cause signifi cant mortality in 2002 and suggested a possible link to the mature codling moth, Cydia pomonella (L.) egg parasitism in 2001; however, it is (Lepidoptera: Tortricidae), larvae which diffi cult to estimate how the higher egg overwinter under bark crevices on host mortality caused by T. cacoeciae might fruit trees (Lacey and Unruh, 1998). In translate to increased tree vigour in the 2003, Murray et al. (2004) conducted fi eld long term. trials in Bellingham, Washington to assess Sentinel eggs placed on trees at the trial the effi cacy of using commercially avail- sites at the start of the 2002 fi eld season 162 Chapter 22

were not parasitized by T. cacoeciae, 2. Further clarifi cation of the taxonomy of suggesting that populations had failed to the C. difformis group, through a combin- establish from the 2001 releases (Breedveld ation of morphological, molecular and and Tanigoshi, 2007). This is not surprising behavioural studies, specifi cally, oviposi- because E. formosana overwinters in the tion and rearing experiments of Campoplex larval stage and therefore does not provide capitator on E. formosana larvae; an appropriate egg host for T. cacoeciae. 3. Further investigation of an egg parasi- While many other tortricid species in the toid for inundative releases. Seattle area do overwinter as eggs and could support T. cacoeciae overwintering (Breedveld and Tanigoshi, 2007), the use of this parasitoid for managing E. formosana Acknowledgements may require annual inundative releases. Early work on the biological control of E. 22.4.2 Nematodes formosana was done in collaboration with Lynell Tanigoshi and Terry Miller (Washing- Small-scale fi eld applications of S. feltiae ton State University), Todd Murray (What- and S. carpocapsae in Bellingham, com County Cooperative Extension) and

Washington using a CO2 backpack sprayer Barry Bai ( Oregon Department of Agri- at a rate of 1000 nematodes ml−1, yielded culture). Expert identifi cations were pro- mixed results in controlling E. formosana vided by Dr Klaus Horstmann (University larvae on Prunus emarginata (Douglas) of Würzberg, Germany), Dr Erich Diller Eaton (Rosaceae), P. serrulata and P. avium. (Zoologische Staatssammlung, Munich, Through destructive sampling as well as Germany), Dr Hannes Baur (Natural counting active pest feeding galleries (frass History Museum of Bern, Switzerland), Dr tubes), Murray et al. (2004) found that Claire Villemant (Muséum national E. formosana numbers were generally d’histoire naturelle, Paris) and Dr Jean- reduced on nematode-treated trees, François Landry (AAFC, Ottawa). Manfred although the difference was not always Grossrieder, Hans-Martin Bürki, Erik statistically signifi cant. In contrast, there Osborn, Jake Miall, Basri Pulaj, C.-Jae was no evidence of signifi cant suppression Morden, Jane Allison, Serge Hämmerli, of active E. formosana feeding sites in the Jenny Lazebnik, Marco D’Allesandro, Victoria trial (J. Cossentine, 2012, Linda Jensen and Jay Whistlecraft provided unpublished results). technical assistance. Funding was pro- vided by AAFC, The National Biological Control Institute (USDA, APHIS), the 22.5 Future Needs Science Council of British Columbia and Cannor Nurseries Ltd. Some of the research Further work should include: was also conducted at Simon Fraser 1. Reassessment of the distribution and University’s Global Forest Quarantine economic impact of E. formosana in west- Facility, construction of which was ern Canada and the USA, including further supported by Global Forest (GF-18-2000- assessment of native natural enemies; SFU-2).

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Boldyrev, M.I. and Dobroserdov, S.G. (1981) The raphidiid – an active predator of insects. Zashchita Rastenii 9, 29. Breedveld, K.G.H. and Tanigoshi, L.K. (2007) Seasonal phenology of Enarmonia formosana (Lepidoptera: Tortricidae) and egg parasitism by Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) in Washington State, USA. Journal of Pest Science 80, 15–19. Chapter 22 163

Dang, P.T. and Parker, D.J. (1990) First records of Enarmonia formosana (Scopoli) in North America (Lepidoptera: Tortricidae). Journal of the Entomological Society of British Columbia 87, 3–6. Dickler, E. and Zimmerman, H. (1972) [Investigations on the control of the bark Tortricid Enarmonia formosana Scop. (Lepid., Tortr.)] Mitteilungen aus der Biologischen fur Land- und Forstwirtschaft, Berlin-Dahlem 144, 143–150. Herz, A. and Hassan, S.A. (2006) Are indigenous strains of Trichogramma sp. (Hym., Trichogrammatidae) better candidates for biological control of lepidopterous pests of the olive tree? Biocontrol Science and Technology 16, 841–857. Horstmann, K. (1985) Revision der mit difformis (Gmelin, 1790) verwandten westpaläarktischen Arten der Gattung Campoplex Gravenhorst, 1829 (Hymenoptera, Ichneumonidae). Entomofauna 6, 129–163. Hunt, E. and Kuhlmann, U. (2006) Biological control of cherry bark tortrix, Enarmonia formosana, Annual Report 2005/2006. Unpublished Report, CABI Bioscience Switzerland Centre, Delémont, Switzerland. Hunt, E. and Kuhlmann, U. (2007) Biological control of cherry bark tortrix, Enarmonia formosana, Annual Report 2006/2007. Unpublished Report, CABI Europe, Delémont, Switzerland. Hunt, E. and Kuhlmann, U. (2008) Biological control of cherry bark tortrix, Enarmonia formosana, Annual Report 2007/2008. Unpublished Report, CABI Europe, Delémont, Switzerland. Jenner, W.H. and Kuhlmann, U. (2006) Signifi cance of host size for a solitary endoparasitoid: a trade- off between fi tness parameters. Basic and Applied Ecology 7, 461–471. Jenner, W.H. and Roitberg, B.D. (2009) Foraging behaviour and patch exploitation by Campoplex dubitator (Hymenoptera: Ichneumonidae), a parasitoid of bark-mining larvae. Journal of Insect Behavior 22, 257–272. Jenner, W.H., Kuhlmann, U., Cossentine, J.E. and Roitberg, B.D. (2004) Phenology, distribution, and the natural parasitoid community of the cherry bark tortrix. Biological Control 31, 72–82. Jenner, W.H., Cossentine, J.E., Whistlecraft, J. and Kuhlmann, U. (2005a) Host rearing is a bottleneck for classical biological control of the cherry bark tortrix: a comparative analysis of artifi cial diets. Biocontrol Science and Technology 15, 519–525. Jenner, W.H., Kuhlmann, U., Cossentine, J.E. and Roitberg, B.D. (2005b) Reproductive biology and small-scale rearing of cherry bark tortrix and its candidate biological control agent. Journal of Applied Entomology 129, 437–442. Klaus, M.W. (1991) Cherry Bark Tortrix in Washington State. Proceedings of the Washington State Horticultural Association 87. Klaus, M.W. (1992) Cherry Bark Tortrix Survey Report. Washington State Department of Agriculture, Yakima, Washington, USA. Lacey, L.A. and Unruh, T.R. (1998) Entomopathogenic nematodes for control of codling moth: effect of nematode species, dosage, temperature and humidity under laboratory and simulated fi eld conditions. Biological Control 13, 190–197. McNair, C., Gries, G. and Sidney, M. (1999) Toward pheromone-based mating disruption of Enarmonia formosana (Lepidoptera: Tortricidae) on ornamental cherry trees. The Canadian Entomologist 131, 97–105. Murray, T., Lacey, L., Sumerfi eld, H. and MacConnell, C. (2004) Entomopathic nematodes for managing the cherry bark tortrix, Enarmonia formosana Scopoli (Lepidoptera: Tortricidae). Proceedings from the 78th Western Orchard Pest and Disease Management Conference, 14–16 January 2004, Portland, Oregon. Murray, T.A., Tanigoshi, L.K., Bai, B. and LaGasa, E. (1998) Cherry bark tortrix, Enarmonia formosana (Scopoli), bionomics, natural enemy survey and control research project, 1997-98. Washington State University Report. Roediger, H. (1956) Untersuchungen über den Rindenwickler Enarmonia woeberiana Schiff. (Lepid. Tortr.) Zeitschrift fur Angewandte Entomologie 38, 195–321. Schuetze, K.T. and Roman, A. (1931) Schlupfwespen. Isis Budissina 12. Sermann, H. and Zahn, H. (1986) [Studies on the autecology of the cherry bark tortrix moth (E. form. Scopoli)] Nachrichtenblatt fur den Pfl anzenschutz in der DDR 40, 128–132. Tanigoshi, L.K., Bai, B.B. and Murray, T.A. (1998) Biology and Control of the Exotic Cherry Bark Tortrix, Enarmonia formosana. Oregon Department of Agriculture Interim Project Report, 1997 and 1998. Winfi eld, A.L. (1964) The biology and control of the cherry-bark tortrix moth. Plant Pathology 13, 115–120. 164 Chapter 23

23 Euxoa ochrogaster (Guenée), Redbacked Cutworm, Euxoa messoria (Harris), Darksided Cutworm, and Euxoa auxiliaris (Grote), Army Cutworm (Lepidoptera: Noctuidae)

John Gavloski1 and Vincent Hervet2 1Manitoba Agriculture, Food and Rural Initiatives, Carman, Manitoba; 2University of Lethbridge, Lethbridge, Alberta

23.1 Pest Status to control cutworms. The insecticides that are used to control cutworms in fi eld crops The redbacked cutworm, Euxoa ochro- are generally broad spectrum, and will kill gaster (Guenée), darksided cutworm, Euxoa many non-target insects. messoria (Harris), and army cutworm, Populations of Euxoa spp. can at times Euxoa auxiliaris (Grote) (Lepidoptera: be heavily parasitized, and predators and Noctuidae), are all native species that as diseases also help to regulate populations. larvae feed on a variety of host plants, Natural enemies are known to be an including crops such as wheat, Triticum important regulating factor of some species aestivum L. and Triticum turgidum convar. of cutworms (Schaaf, 1972). Biological durum (Desf.) Bowden (Poaceae), canola, control factors have been considered to be Brassica napus L. and B. rapa L. (Bras- of greater importance than meteorological sicaceae), sunfl ower, Helianthus annuus L. factors in reducing outbreaks of the (Asteraceae), fl ax, Linum usitatissimum L. redbacked cutworm (King and Atkinson, (Linaceae), and weeds such as plantains, 1928). Plantago spp. (Plantaginaceae ). Euxoa Euxoa auxiliaris, E. messoria and E. ochrogaster and E. messoria overwinter in ochrogaster are all native species; therefore the egg stage, and it is the feeding by larvae opportunities for releases of exotic species on young plants in the spring that damages as classical biological control agents may be crops. Eggs of E. auxiliaris are laid and limited. An understanding of some of the hatch in late-August to October and this natural enemies of Euxoa and con ditions species overwinters as partly grown larvae that favour their abundance could assist in (Beirne, 1971). Larvae resume feeding in managing populations of these cutworms. the spring on young plants.

23.3 Biological Control Agents 23.2 Background 23.3.1 Parasitoids High cutworm populations in crops often result in insecticides being used to control Parasitoids are not currently incorporated them. There are few other options available into control strategies for cutworms, even

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 23 165

though their benefi cial effects are known of the redbacked cutworm were parasitized (Schaaf, 1972; Turnock et al., 1993). A by four species of , at least diverse assemblage of Hymenoptera and four species of Tachinidae and several Diptera parasitize Euxoa spp. (Table 23.1). species of Hymenoptera (King and Atkin- A study in Saskatchewan found that larvae son, 1928).

Table 23.1. Parasitoids of army cutworm, Euxoa auxiliaris, darksided cutworm, Euxoa messoria, and redbacked cutworm, Euxoa ochrogaster. Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Diptera: Bombyliidae Poecilanthrax Canada: SK King and Atkinson halcyon (Say) (1928) Poecilanthrax Canada: SK King and Atkinson willistoni (1928) (Coquillet) Villa alternata (Say) Canada: AB, SK, ON Brooks (1952) Villa fulviana (Say) Canada: SK King and Atkinson (1928) Villa lateralis (Say) Canada: SK King and Atkinson (1928) Diptera: Muscidae Muscina stabulans Worldwide Cheng (1977) (Fallén) Diptera: Sarcophagidae cimbicis Canada: AB, SK, MB, Crumb (1929); Townsend ON, QC, NS; Dahlem and USA: throughout Downes (1996) Diptera: Tachinidae Aphria ocypterata Canada: YK, BC, AB, Arnaud (1978); Townsend SK, MB, ON, QC, Cheng (1977, NB; 1981); USA: WA to ME, O’Hara and south to CA, NM Wood (2004) and VA Bonnetia comta Canada: YK, NT, BC, Arnaud (1978); Arnaud (1978); Arnaud (1978) ; (Fallén) AB, SK, MB, ON, Capinera Cheng (1977, King and Atkinson QC, NB, NS, PE; (2001); 1981) (1928); Mexico: throughout; O’Hara (2004) O’Hara and Wood USA: AK, (2004) throughout continental US Chetogena Canada: AK to ON; Arnaud (1978); claripennis but probably a Capinera (2001); (Macquart) mixture with O’Hara and edwardsii; QC Wood (2004) Throughout USA and Mexico

Continued 166 Chapter 23

Table 23.1. Continued Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Chetogena edwardsii Distribution confused Arnaud (1978); Arnaud (1978); (Williston) with that of C. O’Hara and O’Hara and Wood (probably) claripennis Wood (2004) (2004) Gonia aldrichi Tothill Canada: BC to NB; O’Hara and Arnaud (1978); USA: South to CA and Wood (2004) King and Atkinson VA (1928) Gonia breviforceps Canada: BC to QC; Arnaud (1978); Tothill USA: MT, south to CA O’Hara and Wood and AZ, also MI (2004) and KS Gonia fuscicollis Canada: SK and MB; Arnaud (1978); Tothill USA: south to NE and King and Atkinson TN, also MD and (1928); IN O’Hara and Wood (2004) Gonia spp. Arnaud (1978) Panzeria spp. Arnaud (1978); Capinera (2001); rubescens Arnaud (1978) Robineau- Desvoidy Peleteria texensis USA only Arnaud (1978); Curran O’Hara and Wood (2004) Periscepsia cinerosa Canada: BC to MB, Arnaud (1978); (Coquillett) also YT and AB; Capinera (2001) USA: MT south to CA, AZ, CO Periscepsia helymus Canada: BC to NS, Arnaud (1978); Arnaud (1978); (Walker) also YT and NU; Capinera (2001); O’Hara and Wood USA: south to CA, O’Hara and (2004) NM, KS, CT and Wood (2004) AK Periscepsia laevigata Canada: AK to NU; Arnaud (1978); (Wulp) also BC, QC, NB, Krombein et al. NS and NL; (1979); Mexico; O’Hara and USA: south to CA, TX Wood (2004) and VA Tachina algens Canada: BC; NT to Arnaud (1978); Wiedemann NL, NS and QC; O’Hara and USA: south to CA, Wood (2004) AZ, NM, MA and AK Winthemia Canada: ON Cheng (1977) deilephilae (Osten Sacken) Winthemia rufopicta Canada: ON Cheng (1977) (Bigot)

Continued Chapter 23 167

Table 23.1. Continued Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Winthemia Canada: YT, NT; BC Arnaud (1978); quadripustulata to NS; USA: south O’Hara and Wood Fabricius to CA, AZ, KS and (2004) NJ, also WV and VA

Hymenoptera: Braconidae Chelonus insularis Mexico; Capinera (2001); Cresson USA: AR, CA, CO, FL, Krombein et al. GA, HI, IL, KS, LA, (1979) MS, MO, NM, OK, SC, TX, UT Cotesia acronyctae Canada: AB, ON, SK; Yu (2012) (Riley) USA: CA, CO, CT, IL, IN, IA, ME, MD, MA, MO, NH, NJ, OH Cotesia griffi ni Canada: AB, QC, NB; Krombein et al. Schaaf (1972); (Viereck) USA: AR, FL, KS, MA, (1979); Yu (2012) NY, OK, SC, SD, Soteres et al. TX, WA (1984); Yu (2012) Cotesia laeviceps Canada: AB, BC, MB, Krombein et al. Cheng (1977, Krombein et al. (1979); Ashmead NB, ON, QC, SK; (1979); 1981); Yu Strickland (1923); USA: CA, CO, CT, Strickland (2012) Yu (2012) GA, IL, IA, MO, (1923); NM, NY, UT Yu (2012)

Cotesia vanessae Canada: AB, ON Hervet (2012)a Hervet (2012)a (Reinhard) Habrobracon USA: AZ, CA, CO, erucarum ID, MT, OK, OR, Yu (2012) Cushman UT, WY

Macrocentrus Canada: AB, SK; Capinera (2001); incompletus north of Mexico; Krombein et al. Muesebeck USA: AZ, CA, CO, (1979); KS, MT, NE, NM, Yu (2012) OK, OR, SD, UT, WY Meteorus dimidiatus Canada: AB, BC, MB, Strickland Strickland (1923) (Cresson) NS, ON; (1923); USA: AK, AZ, CA, Yu (2012) CO, DC, IL, KS, MA, ME, MI, MN, MO, NH, NJ, NY, OH, OR, PA, UT, VT, VA, WA

Continued 168 Chapter 23

Table 23.1. Continued Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Meteorus pendulus Canada: BC, NB, NS, Cheng (1977, (Müller) ON, QC; 1981); USA: AK, CA, CO, Krombein et al. CT, DC, IL, KS, ME, (1979); MA, MI, MO, NH, Yu (2012) NJ, NC, NY, OR, PA, RI TX, VA, VT, WV Meteorus rubens Canada: AB, BC, MB, Cheng (1977); Cheng (1977); Schaaf (1972); (Nees) NB, NT, NS, ON, Krombein et al. Krombein et al. Yu (2012) QC, SK (1979); (1979); USA: throughout Soteres et al. Yu (2012) (1984); Yu (2012) Microplitis feltiae USA: AL, AZ, CA, Capinera (2001); Muesebeck CO, ID, IL, IN, KS, Krombein et al. LA, MO, ND, OK, (1979); SC, TN, TX, WA Yu (2012) Microplitis kewleyi Canada: AB, MB, NB, Schaaf (1972); Muesebeck ON, QC; Yu (2012) USA: CA, DC, IA, ME, MD, MI, NY, WI Microplitis melianae Canada: AB, ON; Capinera (2001); Viereck USA: IA, IL, KS, MI, Krombein et al. MN, NY, OH, OK, (1979) TN, TX Protapanteles alticola Canada: BC, NB; Yu (2012) Ashmead USA: AK, CA, CO, ID, ME, NH, OR, UT Protapanteles Canada: MB, NB, Krombein et al. Cheng (1977); militaris (Walsh) ON, QC; Mexico; (1979); Yu (2012) USA: AR, AZ, CA, CT, Yu (2012) DC, FL, HI, IL, IA, IN, KS, LA, MD, MA, MI, MN, MO, NJ, NM, NY, OK, TN, TX, VA Rogas sp. Capinera (2001) Zele mellea (Cresson) North America Capinera (2001); Krombein et al. (1979) Hymenoptera: Encyrtidae Copidosoma bakeri Canada: AB, NB, ON, Byers (1993); Cheng (1977); Cheng (1977); (Howard) SK; USA: AZ, CO, Noyes (2011); Noyes (2011); Noyes (2011); KS, MA, MT, NM, Yu (2012) Peck (1963); Peck (1963); UT Yu (2012) Schaaf (1972); Yu (2012)

Continued Chapter 23 169

Table 23.1. Continued Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Hymenoptera: Ichneumonidae Arenetra canadensis Canada: AB, NB, ON, Yu (2012) Cresson SK; USA: CA, CO, ID, IA, IL, KS, MI, MT, NM, OR, SD, UT, WA, WI, WY Arenetra fumipennis Canada: AB; USA: Yu (2012) Townes MT, ND, CO Arenetra rufi pes Canada: AB, BC, MB, Cheng (1977); Yu (2012) Cresson NL, NS, ON, QC, Yu (2012) SK; USA: AK, AZ, CA, CO, ID, KS, MA, ME, MI, MN, MT, ND, NH, NM, NY, OR, PA, SD, WA, WY Campoletis atkinsoni Canada: AB, SK, MB Schaaf (1972); (Viereck) USA: WA, OR, ID Yu (2012) Campoletis australis Canada: AB Schaaf (1972); (Viereck) USA: NM Yu (2012) Campoletis Canada: AB, BC, NB, Capinera (2001) Cheng (1977); fl avicincta ON; Mexico; Yu (2012) (Ashmead) USA: AR, CA, CO, DE, FL, GA, IL, IN, KS, NC, OH, OK, SC, TN, VA Campoletis Canada: AB, BC, ON; Capinera (2001); Hervet (2012)a Hervet (2012)a sonorensis Mexico; Murillo (2008); (Cameron) USA: AL, AZ, CA, FL, Yu (2012) GA, KY, MS, NC, OK, SC, TN, TX, WA Campoletis sp. Canada: ON Cheng (1977, 1981) Diphyus apiculatus Canada: AB; Schaaf (1972); (Walkley) USA: CO, ID, MT, Yu (2012) OR, WY Diphyus euxoae Canada: AB, BC; Yu (2012) Cheng (1977, Schaaf (1972); Heinrich USA: CA, CO, ME, 1981); Yu (2012) NJ, NM Yu (2012) Diphyus nuncius Canada: AB, BC; Capinera (2001); (Cresson) USA: CA, NJ, NY, UT Yu (2012) Diphyus subfuscus Canada: AB, BC; Strickland Strickland (1923); (Cresson) USA: CA, CO, NV, (1923); Yu (2012) NJ, NY Yu (2012) Enicospilus sp. Canada: ON Cheng (1977)

Continued 170 Chapter 23

Table 23.1. Continued Parasitoid Order: Family and species Known distribution Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Erigorgus ambiguus Canada: AB, MB, NB, Schaaf (1972); (Norton) ON, QC, SK; Yu (2012) USA: AR, AZ, CA, CO, KS, KY, MA, ME, MI, MO, MN, MS, MT, NC, ND, NH, NM, NY, OH, PA, SD, TX Eutanyacra suturalis Canada: AB, BC, MB, Cheng (1977); Schaaf (1972); (Say) NB, NL, NU, ON, Yu (2012) Yu (2012) QC, SK; Mexico; USA: CO, DE, GA, IL, KS, MA, NH, NJ, NM, NY, PA, UT, VA Exetastes USA: CA, KS, NE, WY Capinera (2001); Cushman Yu (2012) Exetastes obscurus Canada: AB, MB; Schaaf (1972); Cresson Mexico; Yu (2012) USA: AL, CO, CT, DC, GA, ID, IL, KS, MD, MA, MI, MO, NH, NJ, NY, NC, OH, OR, PA, SC, TX, VA, WV Ichneumon longulus Canada: AB, BC; Yu (2012) Cresson USA: AZ, CA, CO, GA, IL, KS, NJ, NM, UT Netelia sp. Canada: AB Schaaf (1972) Spilichneumon Canada: AB, BC, NL, Yu (2012) inconstans NT, QC, YT; (Cresson) USA: CA, CO, CT, IL, MA, ME, MI, NJ, NY, VA Spilichneumon Canada: AB, BC, MB, Capinera (2001); Cheng (1977, Krombein et al. (1979); superbus NL, NT, NS, ON, Yu (2012) 1981); Schaaf (1972); (Provancher) QC, SK; Krombein et al. Yu (2012) USA: CO, HI, TX (1979); Yu (2012) Nemathoda: Mermithidae Agamermis sp. Canada: AB Schaaf (1972) (probably) aV. Hervet, Lethbridge, Alberta 2012, unpublished results.

Twenty-four species of parasitoids have attack the larvae and kill the pupae or been reared from E. ochrogaster (Schaaf, prepupae. The Braconidae and one of the 1972). These include six Tachinidae, six Ichneumonidae kill the later larval stages, Bombyliidae, six Ichneumonidae, four and Copidosoma bakeri (Howard) (Hymen- Braconidae, one Encyrtidae and one optera: Encyrtidae) attack the eggs and kill Mermithidae (Mermithida). Most of these the later instar larvae. Chapter 23 171

During an outbreak of army cutworm in formes: Sturnidae), and grackles, Quiscalus southern Alberta in 1990, 61% of larvae quiscula (L.) (Pas seriformes: Icteridae), can were parasitized by C. bakeri in samples consume large numbers of E. messoria from seven fi elds (Byers et al., 1993). (Cheng, 1973). Cutworms parasitized by C. bakeri feed more and longer and grow considerably larger than unparasitized cutworms, which 23.3.3 Pathogens can result in an overestimation of para- sitization rate (Van Driesche et al., 1991) as There has been very little research on the well as complicate management recom- pathogens of the North American popu- mendations. Copidosoma bakeri can also lations of Euxoa spp. Viral diseases have be one of the most important parasitoids of been noted for E. auxiliaris (Sutter, 1972, E. messoria (Cheng, 1977), and is also a 1973; McCarthy et al., 1975; Jackson and parasitoid of E. ochrogaster (Schaaf, 1972). Sutter, 1985) (Table 23.3). Bacterial diseases can be common under certain conditions, and several fungal diseases thrive in cool 23.3.2 Predators damp weather (King and Atkinson, 1928). It has been suggested that diseases can be the Predators of E. auxiliaris, E. messoria and most effective factor in reducing outbreaks E. ochrogaster are listed in Table 23.2. of E. ochrogaster (King and Atkinson, 1928). Carabid beetles are among the most A study on mortality factors of E. important and best studied of the insect messoria reported that bacterial, micro- predators (King and Atkinson, 1928; Frank, sporidian and other diseases collectively 1971; Cheng, 1984; Larochelle, 1990). accounted for about 30% mortality, whereas Twenty-one Carabidae (Coleoptera) species nuclear polyhedrosis virus and fungal fed on eggs of E. ochrogaster in laboratory pathogens occurred only at low levels, trials, and seven species fed on E. 0.6% and 0.3%, respectively (Bucher and ochrogaster larvae or pupae in the fi eld Cheng, 1971). The authors concluded that (Frank, 1971). Two species, cali- fungal diseases are not likely to become dum (Fabricius) and Harpalus caliginosus established in the dry sandy areas of Fabricius, were the most important insect Ontario where the study was conducted, but predators of E. messoria in a study done in establishment of viral diseases might have Ontario (Cheng, 1984). Both adult and favourable economic results. larval stages destroyed numerous cutworm individuals. 23.4 Future Needs , rodents and grizzly bears, Ursus arctos horribilis Ord (Carnivora: Ursidae), Resources to assist with identifi cation of have been documented as potentially parasitoids of cutworms are needed. important predators of some Euxoa species. Future work should include: Rodents have been noted to destroy larvae, prepupae and pupae of E. messoria (Cheng, 1. Developing tools to routinely identify 1973), and in some alpine habitats U. arctos key parasitoids of the main Euxoa species; horribilis have been seen feeding almost 2. Research on the basic biology of some of exclusively on E. auxiliaris adults for up to the main cutworm parasitoids; 3 months during summer (French and 3. Investigating diseases of Euxoa ochro- French, 1994). The Franklin’s gull, gaster. Diseases have been suggested to be Leucophaeus pipixcan (Wagler) (Charadrii- effective in reducing outbreaks of Euxoa formes: Laridae), often follows a plough or ochrogaster, but the specifi c organisms cultivator in great numbers and has been involved are not known; noted to devour many insects, including E. 4. Investigating ways to enhance natural ochrogaster (King and Atkinson, 1928). enemy populations through habitat man- Starlings, Sturnus vulgaris (L.) (Passeri- agement strategies. 172 Chapter 23

Table 23.2. Predators of army cutworm, Euxoa auxiliaris, darksided cutworm, Euxoa messoria, and redbacked cutworm, Euxoa ochrogaster. Euxoa Known auxilia- Predator species distribution ris Euxoa messoria Euxoa ochrogaster Coleoptera: Carabidae cupreum Dejean Canada, USA Frank (1971); Larochelle (1990) Agonum placidum (Say) Canada, USA Frank (1971); Larochelle (1990) Amara apricaria (Paykull) Canada, USA Frank (1971); Larochelle (1990) Amara avida (Say) Canada Frank (1971); Larochelle (1990) Amara ellipsis (Casey) Canada Frank (1971); Larochelle (1990) Amara latior (Kirby) Canada, USA Frank (1971); Larochelle (1990) Amara patruelis Dejean Canada Frank (1971); Larochelle (1990) Amara quenseli Canada Frank (1971); Larochelle (1990) (Schönherr) Amara torrida (Panzer) Canada Frank (1971); Larochelle (1990) Bembidion bimaculatum Canada Frank (1971); Larochelle (1990) (Kirby) Bembidion canadianum Canada Frank (1971); Larochelle (1990) Casey Bembidion mutatum Canada Frank (1971); Larochelle (1990) Gemminger & Harold Bembidion nitidum (Kirby) Canada Frank (1971); Larochelle (1990) Bembidion obscurellum Canada, USA Frank (1971); Larochelle (1990) (Motschulsky) Bembidion Canada, USA Frank (1971); Larochelle (1990) quadrimaculatum oppositum Say Bembidion rupicola Canada Frank (1971); Larochelle (1990) (Kirby) Bembidion versicolor Canada Frank (1971); Larochelle (1990) (LeConte) Calosoma calidum Canada, USA King and Atkinson King (1928); Larochelle (1990) (Fabricius) (1928); Larochelle (1990) Carabus serratus Say Canada, USA Frank (1971); Larochelle (1990) Carabus taedatus Fabricius Canada, USA Frank (1971); Larochelle (1990) Harpalus amputatus Say Canada, USA Frank (1971); Larochelle (1990) Harpalus caliginosus Canada, USA Cheng (1984); (Fabricius) Larochelle (1990) Harpalus funerarius Csiki Canada Frank (1971); Larochelle (1990) Pterostichus adstrictus Canada Frank (1971); Larochelle (1990) Eschscholtz Pterostichus lucublandus Canada, USA Frank (1971); Larochelle (1990) (Say) Trichocellus cognatus Canada Frank (1971); Larochelle (1990) (Gyllenhal) Coleoptera: Staphylinidae Leptacinus batychrus Canada Frank (1971); Larochelle (1990) (Gyllenhal) Philonthus occidentalis Canada Frank (1971); Larochelle (1990) Horn Tachyporus sp. Canada Frank (1971); Larochelle (1990) Hymenoptera: Formicidae Lasius niger neoniger Temperate King and Atkinson (1928); Emery (ant that feeds on region of Wang et al. (1995) eggs) North America Chapter 23 173

Table 23.2. Continued Euxoa Known auxilia- Predator species distribution ris Euxoa messoria Euxoa ochrogaster Opiliones: Phalangiidae Leiobunum vittatum (Say) Canada Cheng (1984) Phalangium opilio (L.) Canada Cheng (1984) Odiellus pictus (Wood) Canada Cheng (1984) Opiliones: Sclerosomatidae Hadrobunus maculosus Canada Cheng (1984) (Wood) Passeriformes: Sturnidae Sturnis vulgaris (L.) Canada: ON Cheng (1984) Passeriformes: Icteridae Quiscalus quiscalus (L.) Canada: ON Cheng (1984) Charadriiformes: Laridae Leucophaeus pipixcan Throughout King and Atkinson (1928) (Wagler) (Franklin’s gull North that feeds on larvae) America Carnivoraa: Ursidae Ursus arctos horribilis Ord USA: WY, ID, French (Grizzly bears that feed MT (Yellow- and on moths) stone French National (1994) Park area)

Table 23.3. Pathogens of army cutworm, Euxoa auxiliaris, darksided cutworm, Euxoa messoria, and redbacked cutworm, Euxoa ochrogaster. Pathogen species Euxoa auxiliaris Euxoa messoria Euxoa ochrogaster Alcaligenaceae Achromobacter spp. Cheng (1984) Bacillaceae Bacillus cereus Frankland & Frankland Cheng (1984) Bacillus sphaericus Meyer & Neide Cheng (1984) Enterobacteraceae Enterobacter cloacae (Jordan) Cheng (1984) Hormaeche & Edwards Enterobacter aerogenes Hormaeche & Cheng (1984) Edwards Klebsiella pneumoniae (Schroeter) Cheng (1984) Trevisan Pseudomonadaceae Pseudomonas spp. Cheng (1984) Streptococceae Streptococcus faecalis Andrewes & Cheng (1984) Horder Nosematidae Nosema sp. Cheng (1984) Hypocreales (Incerta sedis) Sorosporella uvella (Krass.) Giard Cheng (1984) Baculoviridae Nuclear polyhedrosis virus Jackson and Sutter (1985); Cheng (1984) McCarthy et al. (1975) Granuloviruses Jackson and Sutter (1985) Cheng (1984) Poxviridae Entomopox, and non-occluded viruses Sutter (1972, 1973) 174 Chapter 23

References

Arnaud, P.H. Jr (1978) A Host-Parasite Catalog of North American Tachinidae (Diptera). Miscellaneous Publication No. 1319. United States Department of Agriculture, Washington. Beirne, B.P. (1971) Pest insects of annual crop plants in Canada. I, Lepidoptera; II, Diptera; III, Coleoptera. Memoirs of the Entomological Society of Canada 103, Suppl. 78. Brooks, A.R. (1952) Identifi cation of Bombyliid parasites and hyperparasites of Phalaenidae of the prairie provinces of Canada, with description of six other Bombyliid pupae (Diptera). The Canadian Entomologist 84, 357–372. Bucher, G.E. and Cheng, H.H. (1971) Mortality in larvae of Euxoa messoria (Lepidoptera: Noctuidae) collected from the tobacco area of Ontario. The Canadian Entomologist 103, 888–892. Byers, J.R., Yu, D.S. and Jones, J.W. (1993) Parasitism of the army cutworm, Euxoa auxiliaris (Grt.) (Lepidoptera: Noctuidae), by Copidosoma bakeri (Howard) (Hymenoptera: Encyrtidae) and effect on crop damage. The Canadian Entomologist 125, 329–335. Capinera, J.L. (2001) Army cutworm. In: Capinera J.L. (ed.) The Handbook of Vegetable Pests. Academic Press, New York, pp. 371–373. Cheng, H.H. (1973) Observations on the bionomics of the darksided cutworm, Euxoa messoria (Lepidoptera: Noctuidae), in Ontario. The Canadian Entomologist 105, 311–322. Cheng, H.H. (1977) Insect parasites of the darksided cutworm, Euxoa messoria (Lepidoptera: Noctuidae), in Ontario. The Canadian Entomologist 109, 137–142. Cheng, H.H. (1981) Additional hymenopterous parasites newly recorded from the darksided cutworm, Euxoa messoria (Lepidoptera: Noctuidae), in Ontario. The Canadian Entomologist 113, 773–774. Cheng, H.H. (1984) Euxoa messoria (Harris), darksided cutworm (Lepidoptera: Noctuidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes against Insects and Weeds in Canada 1969–1980. CAB International, London, pp. 33–37. Crumb, S.E. (1929) Tobacco Cutworms. United States Department of Agriculture, Washington, USA. Dahlem, G.A. and Downes, W.L. (1996) Revision of the genus Boettcheria in America North of Mexico (Diptera: Sarcophagidae). Insecta Mundi 10, 76–103. Frank, J.H. (1971) Carabidae (Coleoptera) as predators of the red-backed cutworm (Lepidoptera: Noctuidae) in Central Alberta. The Canadian Entomologist 103, 1039–1044. French, S.P. and French, M.G. (1994) Grizzly bear use of army cutworm in the Yellowstone ecosystem. International Conference on Bear Research and Management 9, 389–399. Jackson, J.J. and Sutter, G.R. (1985) Pathology of a granulosis virus in the army cutworm, Euxoa auxiliaris (Lepidoptera: Noctuidae). Journal of the Kansas Entomological Society 58, 353–355. King, K.M. and Atkinson, N.J. (1928) The biological control factors of the immature stages of Euxoa ochrogaster Gn. (Lepidoptera, Phalaenidae) in Saskatchewan. Annals of the Entomological Society of America 21, 167–188. Krombein, K.V., Hurd, P.D. Jr, Smith, D.R. and Burks, B.D. (1979) Catalog of Hymenoptera in America North of Mexico. Vols I and III. Smithsonian Institution Press, Washington, USA. Larochelle, A. (1990) The Food of Carabid Beetles (Coleoptera: Carabidae, including Cicindelinae), Fabreries Supplement 5. Ateliers Graphiques Marc Veilleux Inc., Cap-Saint-Ignace, Canada. McCarthy, W.J., Granados, R.R., Sutter, G.R. and Roberts, D.W. (1975) Characterization of entomopox virions of the army cutworm, Euxoa auxiliaris (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 25, 215–220. Murillo, H. (2008) Evaluation of the larval endoparasitoid Campoletis sonorensis Cameron (Hymenoptera: Ichneumonidae) of a biocontrol agent of the cabbage looper, Trichoplusia ni Hübner (Lepidoptera: Noctuidae). MSc thesis. University of Windsor, Windsor, Ontario, Canada. Noyes, J.S. (2011) Universal Chalcidoidea Database. Available at: http://www.nhm.ac.uk/chalcidoids (accessed 24 August 2011). O’Hara, J.E. and Wood, D.M. (2004) Catalogue of the Tachinidae (Diptera) of America North of Mexico. Memoirs on Entomology, International 18, 410 pp. Peck, O. (1963) A Catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). The Canadian Entomologist, Suppl. 30, 1092 pp. Schaaf, A.C. (1972) The parasitoid complex of Euxoa ochrogaster (Guenée) (Lepidoptera: Noctuidae). Quaestiones Entomologicae 8, 81–120. Chapter 24 175

Soteres, K.M., Berberet, R.C. and McNew, R.W. (1984) Parasites of larval Euxoa auxiliaris (Grote) and Peridroma saucia (Hübner) (Lepidoptera: Noctuidae) in alfalfa fi elds of Oklahoma. Journal of the Kansas Entomological Society 57, 63–68. Strickland, E.H. (1923) Biological notes on parasites of prairie cutworms. Dominion of Canada, Department of Agriculture. Technical Bulletin 26; New Series. Sutter, G.R. (1972) A pox virus of the army cutworm. Journal of Invertebrate Pathology 19, 375–382. Sutter, G.R. (1973) A nonoccluded virus of the army cutworm. Journal of Invertebrate Pathology 21, 62–70. Turnock, W.J., Timlick, B. and Palaniswamy, P. (1993) Species and abundance of cutworms (Noctuidae) and their parasitoids in conservation and conventional tillage fi elds. Agriculture, Ecosystems and Environment 45, 213–227. Van Driesche, R.G., Bellows, T.S., Elkinton, J.S., Gould, J.R. and Ferro, D.N. (1991) The meaning of percentage parasitism revised: solutions to the problem of accurately estimating total losses from parasitism. Environmental Entomology 20, 1–7. Wang, D., McSweeney, K., Lowery, B. and Norman, J.M. (1995) Nest structure of ant Lasius neoniger Emery and its implications to soil modifi cation. Geoderma 66, 259–272. Yu, D.S.K. (2012) Home of . In: TAXAPAD. Available at: http://www.taxapad.com (accessed 27 November 2012).

24 Fenusa pumila Leach, Birch Leaf Miner, Profenusa thomsoni (Konow), Ambermarked Birch Leaf Miner (Hymenoptera: Tenthredinidae)

Chris J.K. MacQuarrie,1 David W. Langor,2 Scott C. Digweed3 and John R. Spence4 1Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario; 2Natural Resources Canada, Canadian Forest Service, Edmonton, Alberta; 3Midwinter Consulting Inc., Edmonton, Alberta; 4University of Alberta, Edmonton, Alberta

24.1 Project Status dinidae), are common, widespread pests of native and exotic birch, Betula spp. The birch leafminer, Fenusa pumila Leach (Betulaceae), in North America. Both (Hymenoptera: Tenthredinidae), and the leafminer species were introduced early in ambermarked birch leafminer, Profenusa the last century and are now found thomsoni (Konow) (Hymenoptera: Tenthre- throughout Canada and in parts of the USA © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 176 Chapter 24

(Snyder et al., 2007; Digweed et al., 2009). female) and 1753 G. albipes (1022 male: Defoliation by birch leafmining sawfl ies 731 female) were introduced at one site in causes foliage to turn brown and drop Newfoundland and Labrador and 14 sites earlier than normal. This damage decreases in Quebec (Quednau, 1984). In western the aesthetic value of individual trees, Canada, the programme ran from 1993 to particularly in urban areas where birch is a 1996 and targeted the population in common and valued ornamental. Repeated, Edmonton, Alberta. A total of 1167 L. severe defoliation may eventually weaken nigricollis (591 male: 576 female) and 348 trees causing them to be more susceptible G. albipes (166 male: 182 female) were to colonization by secondary pests or released at three sites within the city diseases. (Langor et al., 2002). The programmes in The biological control programmes Newfoundland and Labrador, Quebec, and against F. pumila and P. thomsoni were the Alberta were successful and control of F. subject of two earlier reviews in this series. pumila was achieved in all three Quednau (1984) reviewed the programmes provinces. There have been no signifi cant targeted against F. pumila in Newfound- outbreaks of F. pumila in Canada since the land and Labrador and Quebec. Langor et late 1990s and a recent survey found it to al. (2002) reviewed the programme against be rare to absent at most sites that were F. pumila in and around Edmonton, visited (Digweed et al., 2009). Alberta. The same authors also reported on Parasitism of P. thomsoni by L. thomsoni the suppression of P. thomsoni by a native was fi rst observed in Edmonton in the early parasitoid (Langor et al., 2002), with a 1990s (Digweed et al., 2003). Between 1992 more extensive summary later given by and 1995, L. thomsoni increased in Digweed et al. (2003). abundance in Edmonton and apparently Two notable revisions to the taxonomy suppressed an outbreak of P. thomsoni that of Fenusa and Lathrolestes have occurred had started in the 1970s (Drouin and Wong, since the 2002 update. Taeger and Blank 1984; Digweed et al., 1997). It appears that (1996, 2011) revised Fenusa and deter- the parasitoid continues to hold most mined that the species known as Fenusa populations of P. thomsoni at low levels, pusilla (Lepeletier) (Hymenoptera: Ten- although occasional pockets of moderate or thredinidae) for most of the last century severe defoliation caused by this species should be named F. pumila. More recently, are found in Edmonton every year. Reschikov et al. (2010) partially revised However, these pockets seem to be located Lathrolestes and determined that the and suppressed by L. thomsoni within 1–3 species attacking P. thomsoni, and years (C. MacQuarrie, 2012, unpublished formerly reported as Lathrolestes luteolator results). Surveys done in Canada between (Gravenhorst) (Hymenoptera: Ichneu- 2003 and 2009 showed that P. thomsoni monidae), was in fact a new species, was prevalent across the country, with a Lathrolestes thomsoni Reshchikov (Hymen- few small to moderately sized outbreaks optera: Ichneumonidae). Lathrolestes thom- occurring in northern Alberta, the soni is believed to be native to North Northwest Territories and British Columbia America but its native host remains (Digweed et al., 2009). A large outbreak was unknown (Reschikov et al., 2010). also reported in Alaska (Snyder et al., The biological control programmes in 2007). Three outbreaking populations of P. eastern and western Canada that targeted F. thomsoni in Edson, Alberta and in Fort pumila resulted in the introduction of two Smith and Hay River, Northwest Territories parasitoid species from Europe, Lathro- were parasitized by L. thomsoni lestes nigricollis (Thomson) (Hymenoptera: (MacQuarrie, 2008). Ichneumonidae) and Grypocentrus albipes Since 2000, all biological control pro- Ruthe (Hymenoptera: Ichneumonidae). In grammes in Canada against birch leaf- eastern Canada, between 1972 and 1978, a mining sawfl ies have targeted P. thomsoni total of 4994 L. nigricollis (2347 male: 2647 using L. thomsoni (Table 24.1). Two Chapter 24 177

Table 24.1. Releases of Lathrolestes thomsoni in North America, 2004–2007. Site Year ƂƃTotal Yellowknife, Northwest Territories 2004 11 50 61 2005 11 12 23 2006 47 114 161 2007 57 403 460 Total 126 579 705

Prince George, British Columbia 2007 38 216 254 Total 38 216 254

Alaska, USA (all sites) 2004 44 15 59 2005 76 82 158 2006 125 298 423 2007 932 1137 2069 2008 471 456 927 Total 1648 1988 3636 Grand total 1812 2783 4595

separate initiatives in 2001 and 2004–2007 based on the evidence that a single L. targeted an infestation in Yellowknife, thomsoni was collected there in 2003 (S. Northwest Territories and a third initiative Digweed, 2012, unpublished results). in 2007 targeted an infestation in Prince Regardless, populations of P. thomsoni George, British Columbia. In 2001, 2000– were still large in Yellowknife in 2003 3000 birch leaves containing P. thomsoni prompting the second initiative in 2004– larvae were collected in Edmonton and 2007. One male L. thomsoni was collected then placed at the base of birch trees in in Yellowknife in 2007 at the location Yellowknife (Environment Canada – where releases were made in 2006 (S. Ecoaction, 2003). The species and numbers Digweed, 2012, unpublished results). of parasitoids introduced were not Anecdotal observations indicate that birch recorded and only one introduction of this leafminer defoliation was at trace levels in type was attempted. The second initiative 2010 (R. Brett, Edmonton, Alberta, 2012, in Yellowknife made a series of introduc- pers. comm.) but it was not known if L. tions between 2004 and 2007 using adult L. thomsoni was responsible. A subsequent thomsoni collected in Hay River and Fort investigation in the summer of 2012 found Smith and released in Yellowknife on birch that L. thomsoni was established at two that were infested with P. thomsoni (S. sites in the city (D. Williams, 2012, Digweed, 2012, unpublished results). A unpublished results). Evidence from the total of 705 L. thomsoni (579 male: 126 2012 survey also suggests that parasitoid female) were introduced over the 4 years. populations were relatively large (17% of In 2007, 254 adult L. thomsoni (216 male, the total catch), suggesting that L. thomsoni 38 female) from Edson were released in is having an impact on populations of P. Prince George. thomsoni in Yellowknife. However, more The attempts to introduce L. thomsoni work would be required to confi rm this to Yellowknife and Prince George appear to hypothesis. have been successful. The fi rst initiative in The 2007 release in Prince George was Yellowknife (in 2001) may have succeeded, assessed in 2009 but there was no evidence 178 Chapter 24

of parasitism by L. thomsoni in a sample of update we revisited these recommenda- approximately 150 P. thomsoni collected tions to determine which had been from the release site (C. MacQuarrie, 2012, addressed by work done since 2000. unpublished results). None the less, Quednau (1984) in reviewing the declines in birch leafminer populations programmes in Newfoundland and were noted in 2011 and 2012 (S. Lindgren, Labrador and Quebec, recommended that: Prince George, British Columbia, 2012, (i) basic life history work be done on L. pers. comm.) but, as in Yellowknife, the nigricollis and G. albipes; (ii) life tables be cause of this decline was not investigated. constructed for F. pumila; and (iii) mass A survey in 2012 did fi nd 11 L. thomsoni rearing techniques be developed for L. over an 8 week period (D. Williams, 2012, nigricollis and G. albipes. Langor et al. unpublished results). However, these small (2002) in their review of programmes in numbers suggest only that the parasitoid is Alberta recommended that: (iv) western present. At this point we cannot conclude Canada be surveyed to determine the range that parasitism is responsible for the of Lathrolestes; (v) the rate of parasitism of decline of P. thomsoni in Prince George. F. pumila by L. nigricollis and of P. In addition to the biological control thomsoni by L. thomsoni be measured at a initiatives in Canada, L. thomsoni was also variety of sites; (vi) the trophic interactions introduced from Canada to the state of among the biological control agents, their Alaska as part of a collaborative pro- hosts and other mortality factors be gramme between American and Canadian investigated to quantify the impact of the researchers. Profenusa thomsoni was fi rst biological control programme in Alberta; detected in Alaska in 1991 (United States (vii) the fate of G. albipes in Alberta be Department of Agriculture Forest Service, determined; and (viii) the use of 1992) but remained at low levels until the dimethoate in urban areas should be fi rst outbreak occurred in the early 2000s quantifi ed to determine if its use in urban near Anchorage, Alaska (Snyder et al., settings against birch leafminers decreased 2007). No evidence of L. thomsoni was after the introduction of biological control found in samples taken in Anchorage in agents. 2002 and 2003 (D. Williams, 2012, To our knowledge no work in eastern unpublished results), therefore a pro- Canada since 1984 has addressed gramme was launched in 2003 to introduce recommendations i, ii or iii. A life table the parasitoid to the state from populations was constructed for F. pumila (recom- in Edmonton, Edson, Fort Smith and Hay mendation ii), but for populations in River. Initially, parasitized P. thomsoni Alberta (Digweed, 1998). Recent work pupae were shipped to Alaska and reared developed techniques to rear L. thomsoni to obtain adult L. thomsoni. Later, adult L. (MacQuarrie, 2008) (recommendation iii), thomsoni were collected in Canada and but these methods were adapted from those carried to Alaska by couriers. In total, developed to rear L. nigricollis and G. between 2004 and 2007, 2685 L. thomsoni albipes (Guèvremont and Quednau, 1977; (1530 males: 1155 females) were released Fuester et al., 1984). There has been no in Alaska at Anchorage, Soldotna, Fair- systematic survey of western Canada for banks and Eielson Air Force Base Lathrolestes since 1995 (Digweed et al., (MacQuarrie, 2008) (Table 24.1). Establish- 2003) (recommendation iv) but a survey in ment of L. thomsoni in Anchorage was 2003 of northern Alberta and the southern confi rmed in 2010 and 2011 (Soper, 2012), Northwest Territories found large popu- but suppression of the Alaskan populations lations of L. thomsoni at a few sites has not yet occurred. (MacQuarrie, 2008). Also in 2003, L. The two previous reviews of biological nigricollis was found in Hinton, Alberta (S. control of F. pumila and P. thomsoni made Digweed, 2012, unpublished results). a total of eight recommendations for future Hinton is ~275 km from the sites in work on these species in Canada. For this Edmonton where L. nigricollis was released Chapter 24 179

in 1994, giving the parasitoid an estimated detected during a small survey in 2003 (S. dispersal rate of 30 km year−1, if the Digweed, 2012, unpublished results), populations did not arise de novo from suggests that G. albipes does not play a role native hosts. Work in the USA found two in suppressing F. pumila in Alberta. new parasitoids attacking P. thomsoni Dimethoate use appears to have populations in Anchorage and Massa- declined in areas infested with birch chusetts (Soper, 2012). One, Lathrolestes leafmining sawfl ies (recommendation viii). soperi Reshchikov (Hymenoptera: Ichneu- The City of Edmonton stopped using the monidae), is a koinobiont endoparasitoid insecticide in 1995 around the same time of P. thomsoni with a life history similar to as F. pumila and G. albipes were fi rst that of L. thomsoni (Barron, 1994; introduced (C. Saunders, Edmonton, Reschikov et al., 2010). The other, Aptesis Alberta, 2012, pers. comm.). Dimethoate segnis (Provancher) (Hymenoptera: Ichneu- was voluntarily removed from the monidae), is either a hyperparasitoid of domestic market, i.e. for private use by Lathrolestes spp. pupae or a pupal home-owners, in 2004; registration for parasitoid of P. thomsoni that attacks the domestic uses was offi cially removed in pupal case as it overwinters underground 2011, although registration for use by (Soper, 2012). Of the two, only A. segnis professional pesticide applicators is still has been observed to parasitize P. permitted (Health Canada, 2011). However, thomsoni outside of Alaska (Soper, 2012) current regulations governing Dimethoate and neither species has been investigated use by professional pesticide applicators for its potential as a biological control now preclude its use in most urban settings agent of P. thomsoni. (Health Canada, 2011). The rate of parasitism of F. pumila by L. The programmes against F. pumila and nigricollis was not investigated anywhere P. thomsoni have been one of the success in Canada. However, the rate of parasitism stories of biological control in Canada. of P. thomsoni by L. thomsoni was Based on the track record of the previous measured at a few locations (recommenda- work there is some confi dence that control tion v). Between 2003 and 2006, parasitism will eventually be achieved in Yellowknife, rates of 12–95% were observed for P. Prince George and the state of Alaska. thomsoni populations in Edmonton, Edson, Fort Smith and Hay River (MacQuarrie, 2008). Trophic interactions have not been 24.2 Future needs examined in Alberta for either leafminer species (recommendation vi) and there has We extend the comments of Digweed et al. been no ecological work on birch leaf- (2009), recommending that future work on miners anywhere in Canada since the mid- the biological control of birch leafminers in 1990s (Digweed, 2006). None the less, the Canada should include: programme against F. pumila in Edmonton appears to be successful despite the lack of 1. Estimating percentage parasitism of P. effort towards measuring the impact of the thomsoni by L. thomsoni in Prince George parasitoids. The leafminer has been scarce and Yellowknife and quantifying the infl u- since the late 1990s, which suggests that L. ence of the parasitoid on the intensity of nigricollis integrated with other mortality the outbreaks; agents to suppress populations of F. 2. Initiating Canada-wide surveys to assess pumila. parasitism by L. nigricollis of F. pumila The role of G. albipes in suppressing F. and L. thomsoni of P. thomsoni to deter- pumila was not assessed (recommendation mine the geographic distributions and host vii). The previous review reported that G. associations of both parasitoids; albipes failed to thrive in Edmonton 3. Initiating ecological studies on the inter- (Langor et al., 2002), that observation, and actions among species of birch leafminers, the fact that the parasitoid was not their parasitoids and other mortality factors 180 Chapter 24

to quantify the factors responsible for the Canada (Digweed et al., 2009), and develop initiation and suppression of outbreaks; rearing methods for parasitoids of these 4. Surveying populations of F. pumila and species. related native and non-native species in Alberta, Newfoundland and Labrador, and Quebec to determine the status of G. albi- Acknowledgements pes; 5. Evaluating rates of parasitism by L. We thank the following for their assistance: soperi and A. segnis to determine their fea- R. Brett and D. Williams (Natural sibility as biological control agents against Resources Canada Canadian Forest Service, P. thomsoni elsewhere in North America Edmonton); E. Holsten, C. Snyder and K. and investigating the interactions among L. Zogas (United States Department of soperi, A. segnis and L. thomsoni to quan- Agriculture Forest Service, Anchorage, tify competition and its impact on suppres- Alaska); A. Soper and R. Van Driesche sion of P. thomsoni; (University of Massachusetts, Amherst); S. 6. Exploration within Europe and North Carriere (Government of Northwest Terri- America for parasitoids of Fenusella nana tories, Yellowknife); S. Lindgren (Uni- (Klug), Heterathrus nemoratus (Fallen) and versity of Northern British Columbia, Scolioneura vicina Konow (Hymenoptera: Prince George); M. Jenkins and C. Saunders Tenthridinidae), three introduced species (Community Services, City of Edmonton); of birch leafmining sawfl ies that are and N. McKenzie (Health Canada, Pesticide increasing in both range and abundance in Management Regulatory Agency, Ottawa).

References

Barron, J.R. (1994) The nearctic species of Lathrolestes (Hymenoptera, Ichneumonidae, Ctenopelmatinae). Contributions of the American Entomological Institute 28, 1–135. Digweed, S.C. (1998) Mortality of birch leafmining sawfl ies (Hymenoptera: Tenthredinidae): impacts of natural enemies on introduced pests. Environmental Entomology 27, 1357–1367. Digweed, S.C. (2006) Oviposition preference and larval performance in the exotic birch-leafmining sawfl y Profenusa thomsoni. Entomologia Experimentalis et Applicata 120, 41–49. Digweed, S.C., Spence, J.R. and Langor, D.W. (1997) Exotic birch-leafmining sawfl ies (Hymenoptera: Tenthredinidae) in Alberta: distributions, activities and the potential for competition. The Canadian Entomologist 129, 319–333. Digweed, S.C., McQueen, R.L., Spence, J.R. and Langor, D.W. (2003) Biological control of the ambermarked birch leafminer, Profenusa thomsoni (Hymenoptera: Tenthredinidae). Report #NOR-X-389, Natural Resources Canada Canadian Forest Service, Northern Forestry Centre. Digweed, S.C., MacQuarrie, C.J.K., Langor, D.W., Williams, D.J.M., Spence, J.R., Nystrom, K.L. and Morneau, L. (2009) Current status of exotic birch-leafmining sawfl ies (Hymenoptera: Tenthredinidae) in Canada, with keys to species. The Canadian Entomologist 141, 201–235. Drouin, J.A. and Wong, H.R. (1984) Birch leaf-mining sawfl ies in Alberta (Hymenoptera: Tenthredinidae). Report # NOR-X-260, Environment Canada, Canadian Forestry Service, Northern Forest Research Centre. Environment Canada – Ecoaction (2003) Birch leafminer control using parasitic wasps. Available at: http://www.ec.gc.ca/ecoaction/success_display_stories_e.cfm?story_ID=12030119 (accessed 3 January 2007). Fuester, R.W., Taylor, P.B., Day, W.H., Hendrickson Jr, R.M. and Bluementhal, E.M. (1984) Introduction of exotic parasites for biological control of the birch leafminer (Hymenoptera: Tenthredinidae) in the middle Atlantic states. Journal of Economic Entomology 77, 1565–1570. Guèvremont, H.C. and Quednau, F.W. (1977) Introduction de parasites ichneumonides pour la lutte biologique contre Fenusa pusilla (Hymenoptera: Tenthredinidae) au Quebec. The Canadian Entomologist 109, 1545–1548. Chapter 24 181

Health Canada (2011) Proposed Re-evaluation Decision Dimethoate. Report #PRVD2011-12, Health Canada Pest Management Regulatory Agency. Langor, D.W., Digweed, S.C. and Spence, J.R. (2002) Fenusa pusilla (Lepeletier), birch leafminer, and Profenusa thomsoni (Konow) ambermarked birch leafminer (Hymenoptera: Tenthredinidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 123–127. MacQuarrie, C.J.K. (2008) Distribution, biological control and population dynamics of Profenusa thomsoni in Alaska. PhD thesis, University of Alberta, Edmonton, Alberta, Canada. Quednau, F.W. (1984) Fenusa pusilla (Lepeletier), birch leaf-miner (Hymenoptera: Tenthredinidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, UK, pp. 291–294. Reschikov, A.V., Soper, A. and Van Driesche, R.G. (2010) Review and key to Nearctic Lathrolestes Förster (Hymenoptera: Ichneumonidae), with special reference to species attacking leaf mining tenthredinid in Betula Linnaeus (Betulaceae). Zootaxa 2614, 1–17. Snyder, C., MacQuarrie, C.J.K., Zogas, K., Kruse, J. and Hard, J. (2007) Invasive species in the Last Frontier: Distribution and phenology of birch leafmining sawfl ies in Alaska. Journal of Forestry 105, 113–119. Soper, A. (2012) Biological control of the ambermarked birch leafminer (Profenusa thomsoni) in Alaska. PhD thesis, University of Massachusetts, Amherst, Massachusetts. Taeger, A. and Blank, S.M. (1996) Kommentäre zur taxonomie der Symphyta (Hymenoptera). Beitrage zur Entomologie 46, 251–275. Taeger, A. and Blank, S.M. (2011) ECatSym - Electronic World Catalog of Symphyta (Insecta, Hymenoptera) program version 3.9 data version 38. Digital Entomological Information, Müncheberg, Germany. Available at: http://www.sdei.de/ecatsym (accessed 15 February 2012). USDA Forest Service (1992) Forest Health Management Report – Forest insect and disease conditions – 1991. Report # R10-TP-22, United States Department of Agriculture, Forest Service Forest Pest Management, State and Private Forestry. 182 Chapter 25

25 Haematobia irritans L., Horn Fly, Musca domestica L., House Fly, and Stomoxys calcitrans (L.), Stable Fly (Diptera: Muscidae)

Kevin D. Floate,1 Tim J. Lysyk1 and Gary A.P. Gibson2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2Agriculture and Agri-Food Canada, Ottawa, Ontario

25.1 Pest Status up to 16% (Steelman et al., 1991). Stomoxys calcitrans reduces both weight Horn fl y, Haematobia irritans L., house fl y, gains and feed conversion effi ciency in Musca domestica L., and stable fl y, feedlot cattle by up to 20% (Campbell et Stomoxys calcitrans (L.) (Diptera: al., 1987) and reduces milk fl ow in dairy Muscidae), are common pests of livestock cattle by up to 20% (Bruce and Decker, in Canada. Separate chapters were devoted 1958). Musca domestica do not bite, but to each species in Biological Control cause indirect losses. They spread disease, Programmes in Canada, 1981–2000 (Floate reduce the aesthetics of livestock facilities, et al., 2002; Lysyk, 2002; Lysyk and Floate, irritate employees, and generate lawsuits as 2002), but since then little research on suburban housing development expands these pests has been done in Canada. This into rural areas. chapter summarizes work since 2001 for all The three species have similar life three species. cycles. Females lay eggs that hatch in about Haematobia irritans and S. calcitrans 1 day. Larvae pass through three instars in are blood-feeders. Stomoxys calcitrans 1–2 weeks, feeding on bacteria at the attacks cattle, Bos taurus L. (Artiodactyla: breeding site. Pupae develop for a further Bovidae), horses, Equus ferus L. (Perriso- 1–2 weeks before adult emergence. Three dactylus: Equidae), people, Homo sapiens or four generations are completed in L. (Primates: Hominidae), dogs, Canis southern Canada from May until diapause lupus familiaris L. (Carnivora: Canidae), is induced in overwintering pupae by the and swine, Sus scrofa domestica Erxleben onset of colder temperatures in September (Artiodactylida: Suidae), whereas H. and October. Stomoxys calcitrans and M. irritans generally only attacks cattle. The domestica are primarily associated with painful bites of the two species interrupt livestock confi nements, e.g. feedlots, feeding of the hosts and trigger avoidance dairies, swine barns, poultry houses, and behaviour that results in lost productivity. secondarily with compost piles in urban Haematobia irritans can reduce weight areas and accumulations of rotting vege- gains of yearling cattle by up to 18% tation along bodies of water. Haematobia (Haufe, 1982) and calf weaning weights by irritans are pests of cattle on pasture;

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 25 183

adults spend most of their lives on the dative biocontrol agents. Commercialized backs of cattle, leaving the host to oviposit species reported by White and Johnson in fresh cattle manure. (2010) include the pteromalids Muscidi- furax raptor Girault & Saunders, M. raptorellus Kogan & Legner, M. zaraptor 25.2 Background Kogan & Legner, Nasonia vitripennis (Walker), Spalangia cameroni Perkins, S. Control of M. domestica and S. calcitrans endius Walker and Trichomalopsis sp. (= T. is best achieved through sanitation to sarcophagae (Gahan)) (see ‘Parasitoids’ remove potential breeding sites before under ‘Evaluation of Biological Control’). populations reach pest status. Sanitation is Floate and Spooner (2002) compared impractical for H. irritans, which breeds in the ability of fi ve parasitoid species, M. pats scattered about pastures (but see raptor, M. raptorellus, M. zaraptor, T. ‘Dung beetles’ under ‘Biological Control sarcophagae and Urolepis rufi pes (Ash- Agents’). mead) (Hymenoptera: Pteromalidae), to Insecticides can provide effective locate freeze-killed M. domestica pupae control, though effi cacy is limited to adult buried 0–6 cm in rearing media under fl ies because immature stages are protected laboratory conditions. In large arenas (988 within the breeding media. Hence, cm2) with low host densities, almost no applications weekly or every second week hosts were parasitized at depths below 1 may be required when immature stages cm. In small arenas (3 cm2) with high host complete development to emerge as adults. densities, three species parasitized hosts However, repeated applications facilitate buried up to 4 cm. Combined across the development of insecticide resistance experiments, M. raptor achieved the (Harris et al., 1982; Mwangala and highest level of parasitism, followed by M. Galloway, 1993). Haematobia irritans, M. zaraptor, M. raptorellus, U. rufi pes and T. domestica and S. calcitrans are attacked by sarcophagae. The greatest number of F1 a suite of pathogens, predators and females were produced by the gregarious parasitoids. These natural enemies were species T. sarcophagae and M. raptorellus, reviewed by Floate et al. (2002), Lysyk followed by the solitary species M. raptor, (2002) and Lysyk and Floate (2002). There M. zaraptor and U. rufi pes. High parasitism have been no subsequent studies in Canada by M. raptor and high production of on predators, and only a few studies on offspring by T. sarcophagae identify these pathogens. species as being particularly attractive as biological control agents. Lysyk (2004a) examined the effect of 25.3 Biological Control Agents host density on the mortality of M. domestica and S. calcitrans pupae exposed 25.3.1 Parasitoids to M. raptor, M. raptorellus, M. zaraptor and T. sarcophagae, and on the production Legner (1995) listed over 30 principal of parasitoid progeny. For all species, host parasitoids of synanthropic Diptera from mortality decreased as host density worldwide studies. Most of these species increased. Host mortality was greatest for occur in North America and most are M. zaraptor and similar between hosts. species of Chalcidoidea (Floate and However, fewer M. zaraptor progeny Gibson, 2004). Gibson (2000b) provided an emerged from S. calcitrans pupae. This illustrated key to the 32 chalcidoid species type of residual mortality can result from known to be parasitoids of M. domestica, either host stinging with no oviposition, or S. calcitrans and H. irritans pupae in North from failure of the parasitoid progeny to America. All but four are species of develop on the host. Muscidifurax raptor Pteromalidae (Hymenoptera), and several also induced similar levels of mortality taxa have been commercialized as inun- between M. domestica and S. calcitrans 184 Chapter 25

hosts. Residual mortality was relatively Surveys in western and eastern Canada constant across host density for S. recovered at least 21 species of parasitoids calcitrans, but increased at lower densities from pupae of M. domestica and S. calci- for M. domestica. Slightly more M. raptor trans, with strong regional differences in emerged from S. calcitrans pupae. Muscidi- species composition (Table 25.1). Muscidi- furax raptorellus tended to kill fewer furax raptor, U. rufi pes and Phygadeuon pupae than either M. zaraptor or M. raptor, fumator Gravenhörst (Hymenoptera: Ich- with greater residual mortality on stable fl y neu monidae) are relatively common across pupae. Number and sex ratio of progeny all regions. Trichomalopsis sarcophagae were unaffected by host density. The and M. zaraptor are common in Alberta, gregarious T. sarcophagae killed relatively but rare or absent in Manitoba and further few M. domestica pupae, even fewer S. east. Spalangia spp. are common in eastern calcitrans pupae, and tended to produce Canada, but rare in Manitoba and Alberta. more males at low host densities. Its kill Regional variation is attributed to potential was generally less than for the differences in overwintering survival. Muscidifurax species. Phygadeuon fumator and U. rufi pes are Floate (2002) assessed production of six cool-climate species that typically are parasitoid species on M. domestica pupae absent from surveys in the USA. Spalangia varying in age, status (fresh versus freeze- killed) and storage regime. Production of are most common in warmer regions. all species was greatest on pupae aged >24 Results for seven parasitoid species from h post-pupation. Muscidifurax raptor, M. southern Alberta identifi ed three categories raptorellus, M. zaraptor, T. sarcophagae of cold-hardiness when ambient air and U. rufi pes could be reared on either temperatures are near 0°C (Floate and fresh or freeze-killed pupae stored at −20°C Skovgard, 2004). Category 1 species, e.g. S. for up to 6 months prior to parasitism, but cameroni, have extremely low survival production of S. cameroni was essentially with most individuals likely to perish early limited to the use of fresh pupae. Fresh in the winter. Category 2 species, e.g. M. pupae could not be refrigerated at 10°C or raptor, M. raptorellus, M. zaraptor, are less, or at 15°C without a signifi cant likely to survive several months under decline in their suitability as hosts. A such conditions, but may not survive until decline in the suitability of freeze-killed spring. Category 3 species, e.g. N. vitri- pupae was observed with duration in pennis, T. sarcophagae and U. rufi pes, are storage for M. raptorellus and M. zaraptor. most cold-tolerant with at least a portion of No other effects of storage on parasitoid the population likely to survive the winter. production were detected. Results there- Microhabitat differences, e.g. snow cover, fore indicate that during times of over- depth in rearing media, greatly affect production insectaries can stockpile fl y pupae in freezers for future use to mass- overwintering success (Floate and Skov- rear all the species except S. cameroni. gard, 2004). The effects of cold storage on survival of Trichomalopsis sarcophagae is wide- three parasitoid species was also examined spread in North America with numerous (Lysyk, 2004b). Survival of M. raptor and Diptera host species (Gibson and Floate, M. zaraptor was lowest at 0.5°C and 2001). It is often recovered from M. greatest at 10°C. Some development of M. domestica and S. calcitrans pupae in raptor occurred at 10°C. Survival of T. Alberta (Lysyk, 1995; Floate et al., 1999, sarcophagae was greater at temperatures 2000), but elsewhere only has been below 5°C compared with M. raptor and M. recovered from these hosts in low zaraptor. A simple model suggested that numbers, e.g. in Nebraska (Petersen and stockpiling M. raptor and M. zaraptor at Watson, 1992). These two populations may 10°C and T. sarcophagae at 5°C over three represent different biotypes. The Nebraska generations could result in 3.5, 2.6 and 3.2- population is essentially unable to develop fold increases in availability, respectively. at temperatures ≤20°C (Dobesh et al., Chapter 25 185

Table 25.1. Species of parasitoids (Hymenoptera) recovered in Canada from house fl y and stable fl y pupae (AB = Alberta, MB = Manitoba, ON and QC = Ontario and Quebec, NB = New Brunswick, PEI = Prince Edward Island). Values are percentage of parasitized pupae. Species in bold font are known to harbour infections of the symbiotic bacteria Wolbachia (W) (Kyei-Poku et al., 2006) and/or Arsenophonus (A) (Taylor et al., 2011). ON and ON and Species ABa, c MBa, d, e QCa, f QCb, f NBb, g PEIb, g Braconidae unidentifi ed sp. <1 – – – – – Aphaereta pallipes (Say) W –– – 11<1 Diapriidae Synacra sp. <1 – – – – – Eupelmidae Eupelmus vesicularis (Retzius) A, W <1j <1j –––– Ichneumonidae Phygadeuon fumator Gravenhörst – 67 – – – – Phygadeuon sp. (P. fumator?) 6 – – 14 73 54 Pteromalidae Dibrachys microgastri (Bouché) [=D. cavus (Walker)] <1 – – – – – Muscidifurax raptor Girault & Saunders 36 6 81 17 1 22 Muscidifurax zaraptor Kogan & Legner 15 2 – – – – Nasonia vitripennis (Walker) A,W 28h <1 1 – – Pachycrepoideus vindemiae (Rondani) – – <1 <1 – – Spalangia cameroni Perkins A,W 1 <1 2 25 – 11 Spalangia drosophilae Ashmead – – – <1 – – Spalangia endius Walker A,W –– – 2–– Spalangia haematobiae Ashmead – – – <1 – – Spalangia nigra Latreille W – <1 1 20 20 – Spalangia nigroaenea Curtis W –– 15–– Spalangia subpunctata Förster – <1 – <1 – – Trichomalopsis americana (Gahan) 1i ––<1–1 Trichomalopsis dubia (Ashmead) <1i 2i –<1–– Trichomalopsis sarcophagae (Gahan) W 24 – – – – – Trichomalopsis viridescens (Walsh) 1i –<1––– Urolepis rufi pes (Ashmead) W 13 14 5 5 <1 11 Unidentifi ed – 1 – – – – Number of parasitized pupae examined 2119 2999 908 2268 228 914 a Results obtained using sentinel house fl y pupae; b results obtained using naturally occurring house fl y and stable fl y pupae; c results for Alberta averaged across columns from Table 1 in Floate et al. (2002), original data from Lysyk (1995), Floate et al. (1999, 2000); d McKay (1997); e single specimens of Figitidae (Hymen- optera), Aphaereta sp. and Staphylinidae (Coleoptera) were recovered from naturally occurring fl y pupae; f Gibson and Floate (2004); g Noronha et al. (2007); h infl ated by mass-releases; i modifi ed after Gibson and Floate (2001); j K.D. Floate (2012, unpublished results).

1994), whereas the Alberta population species of Trichomalopsis associated with develops at temperatures as low as 15°C H. irritans, M. domestica, face fl y, Musca (Lysyk, 1998). autumnalis DeGeer (Diptera: Muscidae), New host records and information and S. calcitrans in North America. Gibson arising from surveys of fl y parasitoids have (2000a) reviewed the three world species of given rise to related taxonomic works. Urolepis. Gibson (2009) revised the 31 New Gibson and Floate (2001) reviewed the fi ve World species of Spalangia. 186 Chapter 25

25.3.2 Pathogens 70% mortality within 2 days. This dose is equivalent to fl ies ingesting about 0.08 μl Lysyk et al. (2010) screened 85 isolates (= of bacterial protein. Topical applications 57 subspecies) of Bacillus thuringiensis resulted in greater than 75% mortality in 2 Berliner (Bacillaceae) against H. irritans days when fl ies were treated with doses as and S. calcitrans larvae. The majority had low as 0.14 μl protein per fl y. This little effect on larval survival. Bacillus mortality was only expressed when fl ies thuringiensis Berliner serovar. tolworthi were fed protein in the form of blood. It (serotype 9), B. thuringiensis Berliner was hypothesized that protein feeding serovar. darmstadiensis (serotype 10a, resulted in secretion of proteolytic 10b), B. thuringiensis Berliner serovar. enzymes in the gut of the fl y, and that these thompsoni (serotype 12), B. thuringiensis enzymes activated the bacterial toxins kurstaki (serotype 3a3b3c) and B. resulting in mortality. Field use of these thuringiensis thuringiensis (serotype 1) bacterial toxins may require their were consistently effective against larvae of incorporation into protein baits, or both species. DNA hybridization indicated incorporation of activated toxins into sugar the presence of toxin genes similar to one baits. Mist or spray applications may also with demonstrated effect against higher be useful. Diptera. Dose-response studies indicated that H. irritans larvae were more sus- ceptible to all of the isolates than were S. 25.3.3 Symbionts calcitrans larvae. Direct application to control H. irritans is not feasible, because Early studies of N. vitripennis showed it to larvae occur in widely dispersed cattle harbour the symbiotic bacteria Arseno- dung pats. However, this could be phonus (Enterobacteraceae) (Gherna et al., overcome by development of a bolus that 1991) and Wolbachia (Rickettsiaceae) could be placed in the rumen of cattle to (Breeuwer and Werren, 1990), both of release bacteria into the faeces. Replace- which can dramatically affect host survival ment of about 2% of the pat bacterial and reproduction. Subsequent surveys populations with Bacillus thuringiensis have shown single and multiple infections would likely be effective. Because S. of Wolbachia to be common in parasitoids calcitrans occurs in confi ned systems, of M. domestica and S. calcitrans (Kyei- applications could be made to breeding Poku et al., 2006; Floate et al., 2008), with sites, and effective doses would constitute infections of Arsenophonus much less so about 3% of the native bacterial popu- (Taylor et al., 2011) (Table 25.1). Research lations. Further work indicates that effi cacy on symbionts is of interest as a possible against S. calcitrans larvae increases as method to manipulate host reproduction – temperature decreases, which would make either to increase the effi cacy of biological the bacteria more advantageous in colder control agents or to reduce reproduction of climates (Lysyk and Selinger, 2012). The arthropod species (see Floate and Kyei- isolates are most effective against small Poku, Chapter 6, this volume). larvae and have little effect in 3rd instars. Infections of Wolbachia in U. rufi pes Thus, fi eld applications would have to be induce complete cytoplasmic incompati- repeated for at least one generation to bility (CI) (Kyei-Poku et al., 2003). Crosses signifi cantly reduce adult numbers (Lysyk between uninfected females and infected and Selinger, 2012). males are incompatible, producing no F1 The same fi ve isolates were sub- females (complete CI) and more than sequently examined as oral toxins against expected F1 males. Crosses between adult S. calcitrans (Lysyk et al., 2012). infected parents, between uninfected Ingestion of blood inoculated with B. t. parents, and between infected females and thompsoni at doses greater than 4 μg uninfected males produce an F1 sex ratio of protein ml−1 blood caused greater than two females for each male. The absence of Chapter 25 187

F1 females from the incompatible cross degrade dung pats over a period of weeks. refl ects the death of female embryos Adults tunnel and lay eggs in fresh pats. developing from fertilized eggs (female Feeding by the developing larvae slowly mortality CI). The unexpectedly high changes much of the pat into a dry, number of F1 males suggests that some granular material that is scattered by wind fertilized eggs may be altered to essentially and worked into the soil by biotic and function as haploid embryos, developing abiotic factors. into males (male development CI). In 2007, a programme was initiated to Infections of Wolbachia in S. cameroni assess the likelihood of establishing two cause an incomplete form of female species of ‘tunnellers’, Digitonthophagus mortality CI (Kyei-Poku et al., 2006). (Onthophagus) gazella (Fabricius) and Laboratory studies showed incompatible Onthophagus taurus (Schreber) (Cole- crosses (uninfected female × infected male) optera: ) in Canada. Such to produce fewer progeny, which had a species can bury and scatter fresh dung strong male-biased sex ratio. All other pats in a period of days. Adults remove crosses produced more progeny, which had manure from the pats, which they bury 15 a female-biased sex ratio. Also, develop- to 20 cm deep. They then oviposit into this mental times of progeny were increased ‘brood ball’, which provides food for the when the paternal parent was infected with developing larvae. The burial activity Wolbachia, regardless of whether the improves soil aeration, water fi ltration and maternal parent was infected or whether nitrogen levels. Both species are of offspring developed from fertilized eggs. European origin, and were introduced in This result may refl ect the action of the south-eastern USA, from whence their Wolbachia on components of the seminal distributions since have been expanding fl uid that then affect the development of (Hoebeke and Beucke, 1997). Onthophagus offspring from inseminated females. taurus already may be established in south- Experimental crosses show that infec- eastern Canada and may eventually spread tions of Wolbachia in T. sarcophagae cause further west. It was collected in New York complete CI (Floate and Coghlin, 2010). state in 2006 (Pimsler, 2007) and in large Affecting host reproduction in this manner numbers in northern Michigan in 2011 favours the spread of infection in the host (Rounds and Floate, 2012). Establishment population. From starting levels of 50%, of D. gazella in Canada is not expected. infections of Wolbachia reached near Releases in New Jersey were unsuccessful fi xation in fi ve generations in laboratory and the distribution of this species is colonies of T. sarcophagae (K.D. Floate, restricted to the southern USA (Hoebeke 2012, unpublished results). and Beucke, 1997). The above conclusions are supported by experimental results and fi eld studies in 25.3.4 Dung beetles (habitat manipulation) southern Alberta (Floate et al., 2011). In laboratory studies, minimum constant Dung beetles (Coleoptera: Scarabaeidae) temperatures for egg-to-adult development can be seasonally important in accelerating were 16 and 22°C for O. taurus and D. the degradation of cattle dung on pastures. gazella, respectively. In fi eld studies, Accelerated degradation is desired because adults of both species were added to fi eld undegraded dung supports the develop- enclosures starting in June, with fresh ment of H. irritans and other pests of cattle, cattle dung added weekly until October. reduces the amount of pasture available for The following spring, enclosures and the grazing and removes nitrogen and minerals soil therein were examined carefully for from pasture soils (Fincher, 1981). Most live beetles. No live adult D. gazella were species of dung beetles common in cattle recovered, whereas a small number of live dung in Canada are ‘dwellers’ (Floate and adults were recovered for O. taurus. The Gill, 1998; Floate, 2011), and slowly pristine condition of these latter beetles 188 Chapter 25

and the recovery of some individuals from results). In 2009, 1513 O. taurus and 480 D. brood balls identifi ed these adults as the F1 gazella were released on native pastures progeny of beetles placed in the tubs the near Lethbridge (the unsuitability of D. previous year. These results document that gazella was unknown at that time). In the O. taurus can overwinter and complete summer of 2010, a further 1480 O. taurus egg-to-adult development in southern were released. Pitfall trapping at these sites Alberta. However, it is not known whether 3 weeks later recovered a small number of reproductive success in Alberta is O. taurus, which documented their suffi cient to allow populations to become survival for at least this period post- established. release. Release sites will be monitored in the future to assess the longer term outcome of the releases. 25.4 Evaluation of Biological Control

25.4.1 Parasitoids 25.5 Future Needs

The Alberta biotype of T. sarcophagae was Future work should include: studied in southern Alberta for com- mercialization as a biological control agent. 1. Development of more streamlined and Floate (2003) showed that the species can consistent regulations for the import and be reared easily in large numbers, releasing export of biological control agents that tar- an estimated 4.63 million wasps into three get fi lth fl ies. Commercialization of T. sar- commercial feedlots during a 2-year study. cophagae, for example, has been hindered Each of several releases predictably and by legislative barriers preventing sales into repeatedly enhanced parasitism of sentinel regions where the parasitoid is likely M. domestica pupae, whereas parasitism endemic but not recorded in the literature remained low in three paired control as present (S. Penn, California, 2012, pers. feedlots where wasps were not released. comm.); Releases every second week had a 2. Surveys in northern regions of Europe disproportionately greater effect than and Asia for additional parasitoid species releases every second month, supporting with potential for commercialization as insectary recommendations for regular, these might be better suited for use in repeated releases of wasps every second or north temperate climates than the species fourth week throughout the summer. currently developed for southern US mar- Colonies of the Alberta biotype were kets; provided to commercial insectaries in the 3. Assessments of fi lth fl y parasitoids for USA, where it was mass-reared and sold on use against new targets. Muscidifurax rap- a limited basis (K.D. Floate, 2012, tor (Kapongo et al., 2007) and Spalangia unpublished results). Sales of T. sarco- cameroni (Tormos et al., 2010) have been phagae appear to have been discontinued, studied for application against Mediter- partially because of its perceived poor ranean fruit fl y, Ceratitis capitata performance at sites in the southern USA (Wiedemann) (Diptera: Tephritidae), in and partially because of regulations orchards and vinyards; imposed in some states that restricted 4. Expanded use of molecular methods to sales. characterize pathogenic and symbiotic bac- teria. Taylor et al. (2006) used genetic markers to clarify taxonomic relationships 25.4.2 Dung beetles (habitat manipulation) among species of Spalangia and this same approach could be used to determine Field releases of O. taurus and D. gazella whether populations of T. sarcophagae were made in the summers of 2009 and reported from Alberta and Nebraska are 2010 (K.D. Floate, 2012, unpublished indeed two biotypes or possibly cryptic Chapter 25 189

species. Furthermore, genetic markers velop appropriate methods of application; could be used to clarify the taxonomy of 6. Investigation of the potential of sym- Muscidifurax species as these are presently biotic bacteria for use in biocontrol (see identifi ed primarily by biological features Floate and Kyei-Poku, Chapter 6, this vol- and are diffi cult to separate reliably based ume); solely on morphology; 7. Potential release of more effi cient spe- 5. Studies to characterize the insecticidal cies of scarabaeid beetles into Canada to activity of pathogenic bacteria under fi eld accelerate the degradation of cattle dung on conditions, to determine their feasibility pastures. for mass-production and storage, and to de-

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Lysyk, T.J. and Selinger, L.B. (2012) Effects of temperature on mortality of larval stable fl y (Diptera: Muscidae) caused by fi ve isolates of Bacillus thuringiensis. Journal of Economic Entomology 105, 732–737. Lysyk, T.J., Kalischuk-Tymensen, L.D., Rochon, K. and Selinger, L.B. (2010) Activity of Bacillus thuringiensis isolates against immature horn fl y and stable fl y (Diptera: Muscidae). Journal of Economic Entomology 103, 1019–1029. Lysyk, T.J., Kalischuk-Tymensen, L.D. and Selinger, L.B. (2012) Mortality of adult Stomoxys calcitrans (L.) fed isolates of Bacillus thuringiensis. Journal of Economic Entomology 105(5), 1863–1870. McKay, T. (1997) Parasitoid wasps (Hymenoptera: Pteromalidae, Ichneumonidae) for control of house fl ies and stable fl ies (Diptera: Muscidae) in dairy operations in Manitoba. MSc thesis, The University of Manitoba, Winnipeg, Manitoba, Canada. Mwangala, F.S. and Galloway, T.D. (1993) Susceptibility of horn fl ies, Haematobia irritans (L.) (Diptera: Muscidae), to pyrethroids in Manitoba. The Canadian Entomologist 125, 47–53. Noronha, C., Gibson, G.A.P. and Floate, K.D. (2007) Hymenopterous parasitoids of house fl y and stable fl y puparia in Prince Edward Island and New Brunswick, Canada. The Canadian Entomologist 139, 748–750. Petersen, J.J. and Watson, D.W. (1992) Comparison of sentinel and naturally occurring fl y pupae to measure fi eld parasitism by pteromalid parasitoids (Hymenoptera). Biological Control 2, 244– 248. Pimsler, M.L. (2007) A survey of the dung beetles in cattle manure on pastures of an organic and a conventional dairy farm in New York state. Undergraduate thesis, Cornell University, Ithaca, New York. Rounds, R.J. and Floate, K.D. (2012) Diversity and seasonal phenology of coprophagous beetles at Lake City, Michigan with a new state record for Onthophagus taurus (Coleoptera: Scarabaeidae). The Coleopterists Bulletin 66, 169–172. Steelman, C.D., Brown, A.H., Gbur, E.E. and Tolley, G. (1991) Interactive response of the horn fl y (Diptera: Muscidae) and selected breeds of beef cattle. Journal of Economic Entomology 84, 1275–1282. Taylor, D.B., Moon, R., Gibson, G. and Szalanski, A. (2006) Genetic and morphological comparisons of New and Old World populations of Spalangia species (Hymenoptera: Pteromalidae). Annals of the Entomological Society of America 99, 799–808. Taylor, G.P., Coghlin, P.C., Floate, K.D. and Perlman, S.J. (2011) The host range of the male-killing symbiont Arsenophonus nasoniae in fi lth fl y parasitioids. Journal of Invertebrate Pathology 106, 371–379. Tormos, J., Beitia, F., Alonso, M., Asís, J.D. and Gayubo, S.F. (2010) Assessment of Ceratitis capitata (Diptera, Tephritidae) pupae killed by heat or cold as hosts for rearing Spalangia cameroni (Hymenoptera: Pteromalidae). Annals of Applied Biology 156, 179–185. White, J. and Johnson, D. (2010) Vendors of benefi cial organisms in North America. ENTFACT-125. Available at: http://www.ca.uky.edu/entomology/entfacts/ef125.asp (accessed 12 January 2012). 192 Chapter 26

26 Harmonia axyridis (Pallas), Multicolored Asian Ladybeetle (Coleoptera: Coccinellidae)

Charles Vincent1 and Gary Pickering2 1Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, Québec; 2Brock University, St Catharines, Ontario

26.1 Pest Status Because H. axyridis was considered as one of the most voracious and aggressive The multicolored Asian ladybeetle, Har- coccinellid predators, it has been intro- monia axyridis (Pallas) (Coleoptera: Coc- duced in Europe and the USA for cinellidae), originates from north-eastern biological control purposes. It was intro- Asia. It is found in numerous habitats duced into France in 1982, where large- including forests, marshes, agricultural and scale rearing at the Research Station of urban areas. Harmonia axyridis overwinter INRA-Antibes allowed planned experi- as adults and, depending on the location, mental activities (e.g. Vincent et al., 2000). can have several generations per year, It has been introduced on several occasions given its relatively fast developmental time into the southern USA (Koch, 2003) where (Labrie et al., 2006). Both larvae and adults it fi nally established in Louisiana in 1988 feed on a wide variety of food, including and, from there, invaded large areas of the coleopteran and lepidopteran eggs and continent. In Canada, it was fi rst reported larvae (Lucas et al., 2004), aphids (and from southern Quebec (Coderre et al., probably most soft-bodied insects; Lucas et 1995). al., 1997), mites and pollen. When food The establishment of H. axyridis in resources are scarce, adults cannibalize North America created several unexpected their own eggs and larvae. In laboratory problems, related in Kovach (2004) and feeding experiments conducted to deter- Lucas et al. (2007a): (i) H. axyridis dis- mine if H. axyridis can infl ict primary placed existing coccinellid species (Lucas damage to pumpkins, Curcubita spp. et al., 2007b) in several crops/habitats; (ii) (Cucurbitaceae), apples, Malus spp. (Rosa- in the mid-1990s it became a nuisance as ceae), grapes, Vitis vinifera L. (Vitaceae), large populations invaded households in and raspberries, Rubus idaeus L. (Rosa- autumn, irritating homeowners by making ceae), only raspberries were attacked (Koch their way into food and drinks, and by et al., 2004). In choice tests, H. axyridis disrupting activities such as sleeping preferred damaged to non-damaged fruit. (Huelsman and Kovach, 2004), creating Like several other coccinellids, H. axyridis negative attitudes in laypeople, as well as adults exhibit defensive tactics, notably unwelcome media coverage; (iii) H. refl ex bleeding of isopropyl methoxy- axyridis is the fi rst natural enemy reported pyrazine. to induce allergic reactions in humans

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 26 193

(Yarbrough et al., 1999); and (iv) H. 26.2.1 H. axyridis as a viticultural pest axyridis caused unexpected problems in a number of crops, notably in vineyards For agriculture one consequence of the (Ejbich, 2003; Ker and Pickering, 2006; proliferation of H. axyridis has been its Galvan et al., 2009). negative impact on the quality of grapes Since 1980, numerous papers have been and wine. When H. axyridis adults are published to document issues raised by the inadvertently incorporated into grape juice establishment of H. axyridis in North during normal harvesting operations, a America and Europe. Major reviews have pronounced tainting of the resultant juice been published by Koch (2003), Pervez and wine may follow. (2006) and Hahn and Kovach (2004). The The off-fl avour is known within oeno- scientifi c journal BioControl published two logical circles as ‘ladybug taint’, and is special issues on H. axyridis, in 2008 (vol. characterized by undesirable groundnut 53) and 2011 (vol. 56), the former being and bell pepper aroma and increased republished as a book (Roy and Wajnberg, bitterness (Pickering et al., 2004). The taint 2008). Hereafter, contributions made by is caused by alkyl-methoxypyrazines, con- Canadian scientists between 2001 and 2010 stituents of H. axyridis haemolymph on H. axyridis are reported. (Pickering et al., 2005), and surprisingly little is required to affect the fi nished wines; as few as one beetle per vine may be 26.2 Background suffi cient (Pickering et al., 2007). This ‘pest potential’ for viticulture was fi rst widely The soybean aphid, Aphis glycines recognized in Ontario during the 2001 Matsumura (Hemiptera: Aphididae), is a vintage, but it is likely that H. axyridis was major invasive species that was fi rst adversely affecting the quality of juice and detected in Wisconsin in 2000 in soybean, wine in parts of the USA prior to this date. Glycine max (L.) Merr. (Fabaceae), fi elds Now, ladybug taint is a recognized wine (Landis et al., 2004; Ragsdale et al., 2011). defect in many winemaking regions around It rapidly invaded 21 US states and parts of the world, including traditional viticultural Canada, and the ca. 18 million ha of areas in France and Germany. The factors soybean fi elds, which were devoid of aphid that drive H. axyridis to vineyards are prey, became a huge reservoir of A. unknown, but in many instances their glycines. Harmonia axyridis became a arrival en masse appears linked to the variable but important component of the harvest of soybeans, or grain crops in close natural enemy complex of the soybean proximity to the vineyards. Likely, this aphid (Landis et al., 2004; Ragsdale et al., harvest removes principal prey species, 2011). such as aphids (Hemiptera: Aphididae) and The nuisance associated with invasions scale insects (Hemiptera: Coccoidea), and of houses by H. axyridis adults has resulted the beetles move to neighbouring grape- in a lot of media attention. To address the vines either in search of further food- issue, Labrie et al. (2008) conducted sources, and/or to make use of vines as planned experiments to determine potential overwintering sites. This ‘migra- overwintering survival of adults in nature tion’ often corresponds with or precedes versus inside human houses. They found grape harvest. that survival ranged from 25 to 53% in Remediation of grape juice and wine different houses and that H. axyridis did affected by ladybug taint using con- not survive outside in southern Quebec. ventional wine and juice-processing They concluded that in harsh winter options is largely ineffective (Pickering et conditions, human houses or structures al., 2006). One innovation that has had offer frost-free spaces facilitating survival some success is the use of custom-designed of invading H. axyridis. ‘shaker tables’. As the harvested grapes 194 Chapter 26

pass along a conveyor on the table, (OMAFRA, 2008). Effi cacy of these sprays vibrations cause beetles that are hiding varies, but reasonably good initial knock- within grape bunches to become detached down success of target beetles can be and fall between gaps in the stainless steel achieved, and an extended repellancy mesh, where they are detained. However, effect has been reported for RipcordTM 400 there are signifi cant limitations with this EC (KCMS Applied Research and Con sult- system: it is not suitable for machine- ing, 2009). However, the biggest limitation harvested grapes, and the throughput is with these insecticides is that re-infestation slow, making it unsuitable for large winery may occur rapidly, within the pre-harvest operations or when there are high pro- interval for these compounds, as beetles cessing demands from a condensed grow- are very mobile and their densities in ing season. These, and the general vineyards can fl uctuate greatly from day to limitations in remediating tainted juice and day (Seko et al., 2008). Also, in an attempt wine, have led researchers and wine- to remove beetles from grapes immediately growers to focus on preventative strategies prior to harvest, injudicious use of at the vineyard level. insecticides may occur, increasing the risk of unsafe levels of pesticide residues in grapes, juice and wine (Pickering et al., 26.2.2 Management options in vineyards 2012). Thus, alternative and more sus- tainable strategies for controlling H. Galvan et al. (2006) found a strong axyridis in vineyards are needed, con- correlation between H. axyridis densities sistent with the wider movement toward and freshly damaged grapes in the fi eld, reduced-risk pest management practices in suggesting that beetles are attracted to agriculture. damaged grapes, possibly because of their high sugar content. This suggests that a 26.2.2.2 Repellent sprays prudent preventative strategy for grape growers is to employ cultural practices that One approach that has been investigated prevent or reduce damage to fruit, includ- recently is using sulfur dioxide as a ing maintaining an open vine canopy, potential repellent spray. To our know- judicious use of antifungal agents, and ledge, it has not previously been assessed protection measures. Fortunately, these in this capacity, although sulfur dioxide is interventions are conducive to quality a commonly used antimicrobial and anti- grape and wine production anyway, oxidant used in the food and wine regardless of their purported ability to industries. It is typically added to food and reduce the attractiveness of grapevines to beverages as potassium metabisulfi te

H. axyridis. (KMS), which produces sulfur dioxide upon hydrolysis. In wine, it prevents browning and inhibits the activity of many 26.2.2.1 Insecticides spoilage bacteria and yeast. While KMS is Currently, application of insecticides in the not yet registered for use in vineyards, it is vineyard is the most widely utilized permitted in winemaking in all wine intervention in North America to control regions and is relatively inexpensive; thus, H. axyridis. In the USA, permitted its use in vineyards for repelling beetles insecticides include Clutch® 50WDG may be more appropriate than many other (clothianidin), Venom® 70SG (dinotefuran) chemicals. Glemser et al. (2012) found that and Mustang® Max EC (permethrin) with KMS reduced the number of beetles on pre-harvest intervals ranging from 0 to 1 vines at 5 and 10 g l−1. days. In Canada, grape growers can use Reducing densities to below ca. 1400 Malathion 85 E (malathion) and/or Rip- beetles t−1 grapes may be suffi cient to cordTM 400 EC (cypermethrin) up to 3 and prevent development of taint in the wines 7 days prior to harvest, respectively (Pickering et al., 2007). If the number of Chapter 26 195

beetles in a vineyard exceeds this estab- determine parasitism (Firlej et al., 2005). lished sensory detection threshold, KMS While total larval parasitism by the solitary could be used to reduce the density to koinobiont Dinocampus coccinellae below the threshold level. Schrank (Hymenoptera: Braconidae) was 4.6 and 32.1% in H. axyridis and C. maculata lengi, respectively, zero para- 26.2.2.3 Semiochemical-based push–pull sitism occurred in H. axyridis. Studying strategy increase in size and number of teratocytes A push–pull strategy uses both highly as a function of time following parasitism attractive and highly repellent stimuli to by D. coccinellae, Firlej et al. (2007) manipulate the abundance and distribution concluded that H. axyridis is a marginal of beetles in the vineyard. Grape-derived host and C. maculata is a suitable host. compounds were recently assessed by Only H. axyridis larvae were parasitized, Glemser et al. (2012, unpublished results) while both C. maculata larvae and adults using olfactometry and fi eld testing for were parasitized. In laboratory choice tests, their potential use in a push–pull strategy H. axyridis adults exhibited a greater for managing H. axyridis in the vineyard. number of defensive behaviours when Unexpectedly, H. axyridis preferred attacked by D. coccinellae compared to C. undamaged grapes to damaged grapes, but maculata adults or H. axyridis larvae did not discern between undamaged grapes (Firlej et al., 2010). and blank air nor damaged grapes and Roy et al. (2011) published a major blank air. In olfactometry trials on juice review of the parasites and pathogens of H. volatiles, H. axyridis were attracted to axyridis in its native and invaded range. acetic acid, acetaldehyde, acetic acid plus Amongst hymenopterans, Braconidae ethanol, acetic acid plus isobutanol, and (Hymenoptera) (including D. coccinellae, 2-isopropyl-3-methoxypyrazine (IPMP). which is reported to parasitize 18 species Harmonia axyridis were repelled by ethyl of Coccinellidae in Europe), Homalotylus acetate alone, and by acetic acid plus spp. (Hymenoptera: Encyrtidae) and Tetra- acetaldehyde. Thus, single volatile com- stichus spp. (Hymenoptera: Eulophidae) pounds and some mixtures associated with are reported. The phorids Phalacrotophora spoiled grapes or fermentative metabolites berolinensis Schmitz. and P. fasciata were attractive. IPMP was the only alkyl- (Fallén) (Diptera: Phoridae) are reported. methoxypyrazine that elicited a behav- Roy et al. (2011) noted 14 species of ioural response. IPMP has previously been ectoparasitic mites, all Coccipolipus spp. shown to be attractive to both sexes of (Trombidiformes: Podapolipidae), that live Coccinella septempunctata L. (Coleoptera: underneath the elytra of their hosts. Some Coccinellidae) in olfactory bioassays (Al of these species can reduce winter survival Abassi et al., 1998), and it is possible that of H. axyridis adults. Roy et al. (2011) also IPMP functions at low concentrations as an reviewed nematodes, fungi and bacteria aggregation pheromone for H. axyridis, found associated with H. axyridis. Their whereas higher concentrations may signal overall conclusion is that, in nature, these high levels of competition. pathogenic organisms play a minor role in regulating H. axyridis populations.

26.3 Biological Control Agents 26.4 Evaluation of Biological Control Adult H. axyridis and Coleomegilla maculata lengi Timberlake (Coleoptera: Biological control of H. axyridis has not Coccinellidae) collected in lucerne, been attempted, and no agents have been Medicago sativa L. (Fabaceae), and maize, released. The introduction of exotic species Zea mays L. (Poaceae), fi elds of southern to control this exotic ‘pest’ must be care- Quebec were dissected or reared to fully considered. Alternative approaches, 196 Chapter 26

such as repelling or excluding beetles from organizations who have assisted in various the fruit or vineyard, or remediation of ways with the research/data presented affected juice and wine, may be the here: Erik Glemser, Dr Rebecca Hallett, Dr appropriate management strategies. Debbie Inglis, Dr Wendy McFadden-Smith, Dr Kevin Ker, Cara McCreary, Indrajith Wickramananda, Ryan Brewster, Kristen 26.5 Future Research Eddington, Neil Carter, Lisa Dowling, Christine Bahlai, Dr Ai-Lin Beh, Dr Mark Further work should include: Sears, Dr Helen Fisher, Jamie-Lee Robb, 1. Continuing to search for and evaluate Kerrie Pickering, Jacques Lasnier, Pierre native natural enemies associated with the Lemoyne, Vincor Canada, the landowners North American coccinellid communities and vintners of Niagara, Ontario, Le that might contribute to regulation of H. vignoble l’Orpailleur (Dunham, Quebec), axyridis populations; Le vignoble Dietrich-Jooss (Iberville, 2. Developing an integrated push–pull Quebec). Some of the research reviewed strategy using semiochemicals to manipu- here was funded by the following agencies, late H. axyridis populations away from who are sincerely thanked: Ontario Grape crops and into alternative habitats, includ- and Wine Research Inc, Ontario Ministry of ing those where natural enemies may have Agriculture, Food and Rural Affairs – an impact. University of Guelph Sustainable Pro- duction Program, Natural Sciences and Engineering Research Council of Canada Acknowledgements Strategic Project Grant, the Wine Council of Ontario and Grape Growers of Ontario, The authors would like to acknowledge The MII program of Agriculture and Agri- and thank the following individuals and Food Canada.

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Hahn, J. and Kovach, J. (eds) (2004) Multicolored Asian Lady Beetles in Agriculture and Urban Environment – Instant Symposium. American Entomologist 50, 152–168. Huelsman, M.F. and Kovach, J. (2004) Behavior and treatment of the multicolored Asian lady beetle (Harmonia axyridis) in the urban environment. American Entomologist 50, 163–164. KCMS Applied Research and Consulting (2009) Multicolored Asian Lady Beetle (Harmonia axyridis Pallas) Regional Monitoring in Niagara Peninsula Vineyards 2008. Unpublished report to The Wine Council of Ontario and the Ontario Grape Growers of Ontario. Ker, K. and Pickering, G.J. (2006) Biology and control of the novel grapevine pest – the multicolored Asian lady beetle Harmonia axyridis. In: Dris, R. (ed.) Crops: Growth, Quality and Biotechnology. IV. Control of Pests, Diseases and Disorders of Crops. WFL Publisher, Helsinki, Finland, pp. 991–997. Koch, R.L. (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3, 1–16. Koch, R.L., Burkness, E.C., Wold Burkness, S.J. and Hutchison, W.D. (2004) Phytophagous preferences of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) for autumn- ripening fruit. Journal of Economic Entomology 97, 539–544. Kovach, J. (2004) Impact of the multicolored Asian lady beetle as a pest of fruit and people. American Entomologist 50, 165–167. Labrie, G., Lucas, E. and Coderre, D. (2006) Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biological Invasions 8, 743–754. Labrie, G., Coderre, D. and Lucas, E. (2008) Overwintering strategy of the multicolored Asian lady beetle (Coleoptera: Coccinellidae): cold-free space as a factor of invasive success. Annals of the Entomological Society of America 101, 860–866. Landis, D.A., Fox, T.B. and Costamagna, A.C. (2004) Impact of multicolored Asian lady beetle as a biological control agent. American Entomologist 50, 153–154. Lucas, E., Coderre, D. and Vincent, C. (1997) Voracity and feeding preferences of Coccinella septempunctata and Harmonia axyridis on Tetranychus urticae and Aphis citricola. Entomologia Experimentalis et Applicata 85, 151–159. Lucas, E., Demougeot, S., Vincent, C. and Coderre, D. (2004) Predation of the obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae) by two aphidophagous coccinellids (Coleoptera: Coccinellidae) in presence or absence of aphids. European Journal of Entomology 101, 37–41. Lucas, E., Labrie, G., Vincent, C. and Kovach, J. (2007a) The multicoloured Asian ladybeetle Harmonia axyridis – benefi cial or nuisance organism? In: Vincent, C., Goettel, M. and Lazarovits, G. (eds) Biological Control: a global perspective. Case Histories from around the world. CAB International, Wallingford, UK, pp. 38–52. Lucas, E., Vincent, C., Labrie, G., Chouinard, G., Fournier, F., Pelletier, F., Bostanian, N.J., Coderre, D., Mignault, M.-P. and Lafontaine, P. (2007b) The multicolored Asian ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in Quebec agroecosystems ten years after its arrival. European Journal of Entomology 104, 737–743. Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA) (2008) Fruit Production Recommendations 2008-2009 (Publication 360). Queen’s Printer for Ontario, Toronto, Ontario. Pervez, A.O. (2006) Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: a review. Biocontrol Science and Technology 16, 111–128. Pickering, G.J., Lin, J., Riesen, R., Reynolds, A., Brindle, I. and Soleas, G. (2004) Infl uence of Harmonia axyridis on the sensory properties of white and red wine. American Journal of Enology and Viticulture 55, 153–159. Pickering, G.J., Lin, J., Reynolds, A., Soleas, G., Riesen, R. and Brindle, I. (2005) The infl uence of Harmonia axyridis on wine composition and aging. Journal of Food Science 70, 128–135. Pickering, G.J., Lin, Y., Reynolds, A., Soleas, G., Riesen, R. and Brindle, I. (2006) The evaluation of remedial treatments for wine affected by Harmonia axyridis. International Journal of Food Science and Technolology 41, 77–86. Pickering, G.J., Ker, K. and Soleas, G.J. (2007) Determination of the critical stages of processing and tolerance limits for Harmonia axyridis for ‘ladybug taint’ in wine. Vitis 46, 85–90. 198 Chapter 27

Pickering, G., Glemser, E.J., Hallett, R., Inglis, D., McFadden-Smith, W. and Ker, K. (2012) Good bugs gone bad: Coccinellidae, sustainability and wine. In: Brebbia, C.A. (ed.) Sustainability Today. WIT Press, Southampton, UK, pp. 239–251. Ragsdale, D.W., Landis, D.A., Brodeur, J., Heimpel, G.E. and Desneux, N. (2011) Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56, 375– 399. Roy, H.E. and Wajnberg, E. (eds) (2008) From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species. Springer, Dordrecht, the Netherlands. Roy, H.E., Rhule, E., Harding, S., Lawson Handley, L.-J., Poland, R.L., Riddick, E.W. and Steenberg, T. (2011) Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. BioControl 56, 663–679. Seko, T., Yamashita, K. and Miura, K. (2008) Residence period of a fl ightless strain of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in open fi elds. Biological Control 47, 194–198. Vincent, C., Ferran, A., Guige, L., Gambier, J. and Brun, J. (2000) Effects of imidacloprid on Harmonia axyridis Pallas (Coccinellidae) larval biology and locomotory behavior. European Journal of Entomology 97, 501–506. Yarbrough, J.A., Armstrong, J.L., Blumberg, M.Z., Phillips, A.E., McGahee, E. and Dolen, W.K. (1999) Allergic rhinoconjunctivitis caused by Harmonia axyridis (Asian lady beetle, Japanese lady beetle, or lady bug). The Journal of Allergy and Clinical Immunology 104, 704–705.

27 Hoplocampa testudinea (Klug), European Apple Sawfl y (Hymenoptera: Tenthredinidae)

Charles Vincent,1 Dirk Babendreier,2 Ulrich Kuhlmann2 and Jacques Lasnier3 1Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, Québec; 2CABI, Delémont, Switzerland; 3Co-Lab R&D, Division de Ag Cord Inc., Granby, Québec

27.1 Pest status First instar larvae of H. testudinea may feed underneath the epidermis of young The European Apple Sawfl y, Hoplocampa fruit, leaving a ribbon-scar on fruit. Fruit testudinea (Klug) (Hymenoptera: Ten- bearing that type of damage, called primary thredinidae), is a primary pest of apple, damage by Miles (1932), often stay on the Malus spp. (Rosaceae), orchards and its tree until harvest and are easily only known host is the apple tree. Eggs are distinguishable from those affected by laid singly in the receptacle of the fl ower. other insects (Vincent and Hanley, 1997).

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 27 199

Second and 3rd instar larvae frequently Frelighsburg, Quebec, cellulose sheeting enter another fruit and in doing so produce has been researched to manage weeds, C. a deep hole plugged by frass. Such nenuphar and H. testudinea (Benoit et al., damaged fruit has a typical and strong 2006). Cellulose sheeting has been odour. Fruit bearing this type of damage, deployed on the soil underneath apple called secondary damage by Miles (1932), trees to prevent seed germination, and to usually fall on the ground in June. Larvae prevent C. nenuphar and H. testudinea complete their development in the soil larvae that live in fallen apples from underneath apple trees at a depth of 10–25 completing their development in the soil. cm and overwinter as eonymphs inside Over 4 years, the overall reduction (control their cocoons. Some individuals may versus treatment) in adult emergence of the diapause for 2 years in the soil. H. testudinea ranged from 60 to 95%. Primary damage caused by H. testudinea As there were no known natural at harvest ranged from 0 to 14% in enemies of the H. testudinea in North commercial orchards and from 0 to 4.1% in America, a classical biological control an unsprayed orchard at Frelighsburg, programme was initiated to study and Quebec, Canada (Vincent and Mailloux, potentially introduce European parasitoids 1988). By 1988, H. testudinea became a of H. testudinea into Canada. serious concern for apple growers in Quebec (Vincent, 1988; Vincent and Roy, 1992). Since 1995, H. testudinea has been 27.3 Biological Control Agents found in the Ottawa Valley in Ontario (H. Goulet, Ottawa, 2012, pers. comm.). Lathrolestes ensator Brauns (Hymenoptera: Hoplocampa testudinea has further Ichneumonidae) is found in Europe, extended its distribution westward in including Poland (Jaworska, 1987), the Ontario and eastward to New Brunswick Netherlands (Zijp and Blommers, 1993), where it was fi rst observed in 1997 (C. Germany and Switzerland (Babendreier, Maund, Fredericton, New Brunswick, 2012, 1998). It is a solitary larval endoparasitoid pers. comm.). Primary damage has been known only to attack H. testudinea (Cross observed in organic orchards of Nova and Jay, 2001). Lathrolestes ensator is Scotia in 2006 (J. Reekie, Nova Scotia, univoltine and is well synchronized with 2012, pers. comm.). its host. Only 1st and 2nd instar host larvae are parasitized successfully, but not 3rd instar larvae even if they are abundant 27.2 Background (Babendreier, 1996, 1998). Consequently, the search period of the parasitoid is Although biorational tactics are available limited to about 2 weeks in orchards for a number of tree-fruit pests (Aluja et al., (Babendreier, 1998). This can limit the 2009), the only effective tactic to control success of L. ensator in the fi eld, especially H. testudinea is the use of synthetic if environmental conditions are un- insecticides sprayed as larvacide (Vincent favourable (weather conditions etc.). and Rancourt, 1988). However, the timing From 1995 to 1999, a total of 2571 H. and harmonization of sprays with those testudinea cocoons containing the larval targeted against adults of plum curculio, parasitoid L. ensator were shipped from Conotrachelus nenuphar Herbst (Cole- Switzerland to Canada. From these, a total optera: Curculionidae), at petal fall are of 604 live L. ensator adults were released diffi cult. The overall situation often results in an unsprayed orchard at Frelighsburg in higher usage of insecticides per season. (45.0410°, −72.8539°), Quebec, where it Physical control methods encompass successfully established (Vincent et al., several families of technologies that may be 2001b, 2002). sound alternatives to insecticides (Vincent Advances on the biology and impact of et al., 2001a, 2003). In an apple orchard at Lathrolestes ensator have been published 200 Chapter 27

in Europe since 2000. In England, Cross dissemination of the parasite was and Jay (2001) reported low (<11.6% fruit undertaken from 2002 to 2012. As the damaged at harvest) infestations caused by parasites released in one orchard naturally H. testudinea, and variable but low invaded a nearby (150 m) untreated incidence of L. ensator parasitism. In the orchard, two orchards of the Agriculture Netherlands, larvae of H. testudinea and Agri-Food Canada experimental farm parasitized by L. ensator varied from 0 to at Frelighsburg were used as sources of L. 42% in a number of apple cultivars in an ensator. Both orchards were minimally insecticide-treated orchard, and from 0 to sprayed with fungicides only, so as to 64% in an organic orchard (Zijp and prevent the development of apple scab, Blommers, 2002a). The authors remarked Venturia inaequalis (Cooke) G. Winter that when H. testudinea had been reduced (Venturiaceae). by pesticide applications, L. ensator was Fruitlets showing secondary damage often found in nearby untreated apple were collected from apple trees in source trees. Zijp and Blommers (2002b) orchards. Such fruitlets were available for determined that female L. ensator carry about 7–8 days on trees. The number of 120–175 eggs but seldom lay more than fruitlets collected varied from one year to 50% of this egg load. These authors another, depending on fruit load and estimated that 60% larval parasitism is importance of H. testudinea populations required to curtail H. testudinea and damage. The presence of frass at the populations. They also hypothesized that entry hole provided an unreliable hint of the fungicide nitrothal-isopropyl and the presence of H. testudinea, as the larva herbicide diuron may negatively impact L. could have exited the fruitlet to enter a ensator. During 27 fi eld collections nearby fruitlet, as reported by Zijp and conducted in IPM orchards in Switzerland Blommers (1993). and Germany between 1992 and 1997, A random sample of fruitlets showing parasitism rates of L. ensator ranged secondary damage were dissected to assess between 0.6 and 43.8% (Babendreier, the number of fruitlets with H. testudinea 1998). The oligophagous ectoparasitoid of larvae and, among these, the number of H. cocoons, Aptesis nigrocincta Gravenhorst testudinea larvae parasitized by L. ensator. (Hymenoptera: Ichneumonidae), showed Immature stages of L. ensator were visible parasitism rates ranging from 12.1 to 39.7% through the skin of the developing H. in one organically managed apple orchard testudinea larvae. The remainder of the in Switzerland between 1995 and 1997 collected fruit was used for releases. (Babendreier, 2000). In Germany, Fruitlets showing secondary damage were Babendreier and Hoffmeister (2003) in- released under the canopy of apple trees in vestigated if H. testudinea cocoons the centre of orchards, usually within 24 h parasitized by L. ensator are successfully of collection of fruitlets. This method attacked by A. nigrocincta. In no-choice allowed estimation of the numbers of laboratory experiments, they found that parasitized larvae released with a there was no signifi cant difference between minimum of dissection. It also allowed the acceptance of cocoons parasitized by H. parasitized larvae to enter the soil to testudinea and unparasitized cocoons by pupate with a minimum of disturbance. A. nigrocincta. Based on a population Apple fruitlets showing secondary dynamics model, Babendreier (1998) damage were released underneath apple concluded that A. nigrocincta, despite trees in orchards located at Henryville, showing high parasitism rates, is unlikely Quebec (45.1266°, −73.2183°), Saint- to add to biological control of H. testudinea Hilaire, Quebec (45.526°, −73.2183°), St- beyond what L. ensator can achieve Paul d’Abbotsford, Quebec (45.4523°, (Babendreier, 1998). −72.8869°), Magog, Quebec (45.2138°, After proving the establishment of L. −72.1376°), Mountain, Ontario (45.0250°, ensator in Canada (Vincent et al., 2001b), −75.5259°), Hilton, Ontario (44.1036°, Chapter 27 201

−77.8084°) and Madbury, New Hampshire, 1. Monitoring and further dissemination of USA (43.2846°, −71.5606°). Collection of the European parasitoid L. ensator in fruitlets to determine if L. ensator had infested areas as needed; successfully established was done yearly 2. Studies to determine the impact of from 2007 to 2011. As of 2012, the parasite insecticide applications used in Canadian was recovered at Henryville, Saint-Hilaire, IPM orchards on L. ensator to predict the Magog and Hilton. potential or limitation for area-wide estab- lishment of the biological control agent; and 27.4 Evaluation of Biological Control 3. Studies to assess interactions of L. ensa- Attempts tor with native natural enemies such as hyperparasitoids and their impact on bio- A study involving a physical method in the logical control of the larval parasitoid. Netherlands aimed at determining if kaolin particle fi lms suppress a number of pests in apple orchards of Europe (Markó et al., 2008). One conclusion of that study is that Acknowledgements kaolin treatments reduced percentage parasitism of H. testudinea by the We thank the following persons for their parasitoid L. ensator from 48% (control) to collaboration: Benoit Rancourt, Pierre 17% (kaolin). Lemoyne, Alain Désilets, Christian deCavel, Margaret Appleby, Alan Eaton and Pierre Jodoin. The Agriculture and 27.5 Recommendations Agri-Food Canada Pesticide Risk Reduction Programme grant PRR10-060 Future projects should include: partially funded the research activities.

References

Aluja, M., Leskey, T.C. and Vincent, C. (eds) (2009) Biorational Tree-Fruit Pest Management. CAB International, Wallingford, UK. Babendreier, D. (1996) Studies on two ichneumonid parasitoids as potential biological control agents of the European apple sawfl y, Hoplocampa testudinea Klug (Hymenoptera: Tenthredinidae). IOBC/wprs Bulletin Integrated Plant Protection in Orchards 19(4), 236–240. Babendreier, D. (1998) Oekologie der Parasitoiden Lathrolestes ensator und Aptesis nigrocincta (Hymenoptera: Ichneumonidae) sowie deren Einfl uss auf Populationen ihres gemeinsamen Wirtes, der Apfelsägewespe, Hoplocampa testudinea (Hymenoptera: Tenthredinidae). PhD thesis, University of Kiel, Germany. Babendreier, D. (2000) Life history of Aptesis nigrocincta (Hymenoptera: Ichneumonidae) a cocoon parasitoid of the apple sawfl y, Hoplocampa testudinea (Hymenoptera: Tenthredinidae). Bulletin of Entomological Research 90, 291–297. Babendreier, D. and Hoffmeister, T.S. (2003) Facultative hyperparasitism by the potential biological control agent Aptesis nigrocincta (Hymenoptera: Ichneumonidae). European Journal of Entomology 100, 205–207. Benoit, D.L., Vincent, C. and Chouinard, G. (2006) Management of weeds, apple sawfl y (Hoplocampa testudinea Klug) and plum curculio (Conotrachelus nenuphar Herbst) with cellullose sheets. Crop Protection 25, 331–337. Cross, J. and Jay, C. (2001) Exploiting the parasitoids Lathrolestes ensator and Platygaster demades for control of apple sawfl y and apple leaf midge in IPM in apple orchards. IOBC/wprs, Bulletin International Conference on Integrated Fruit Protection 24(5), 161–165. Jaworska, M. (1987) Obserwacje nad Lathrolestes marginatus (Thompson), pasozytem owocnicy jablkowej-Hoplocampa testudinea (Klug) (Hymenoptera, Tenthredinidae). [Observations on 202 Chapter 27

Lathrolestes marginatus (Thompson), a parasite of apple sawfl y, Hoplocampa testudinea (Klug) (Hymenoptera, Tenthredinidae)] Polskie Piusmo Entomologiczne 57, 553–567 [in Polish]. Markó, V., Blommers, L.H.M., Bogya, S. and Helsen, H. (2008) Kaolin particle fi lms suppress many apple pests, disrupt natural enemies and promote woolly apple aphid. Journal of Applied Entomology 132, 26–35. Miles, H.W. (1932) On the biology of the apple sawfl y, Hoplocampa testudinea Klug. Annals of Applied Biology 39, 420–431. Vincent, C. (1988) The European Apple Sawfl y: insect pest of apple orchards in Quebec. Canadian Fruitgrower 44(8), 8. Vincent, C. and Hanley, J. (1997) Measure of agreement between experts on apple damage assessment. Phytoprotection 78, 11–16. Vincent, C. and Mailloux, M. (1988) Abondance, importance des dommages et distribution de l’hoplocampe des pommes au Québec de 1979 à 1986. Annales de la Société Entomologique de France 24, 39–46. Vincent, C. and Rancourt, B. (1988) Chemical control of the European apple sawfl y with pre-bloom treatments. Pesticide Research Report. Agriculture Canada, Ottawa, 9. Vincent, C. and Roy, M. (1992) Entomological limits to the implementation of biological programs in Quebec apple orchards. Acta Entomologica et Phytopathologica Hungarica 27, 649–657. Vincent, C., Panneton, B. and Fleurat-Lessard, F. (2001a) (eds) Physical Control Methods in Plant Protection. Springer-Verlag/INRA, Heidelberg, Germany, 329 pp. Vincent, C., Rancourt, B., Sarazin, M. and Kuhlmann, U. (2001b) Releases and fi rst recovery of Lathrolestes ensator Brauns (Hymenoptera: Ichneumonidae) in North America, a parasitoid of Hoplocampa testudinea Klug (Hymenoptera: Tenthredinidae). The Canadian Entomologist 133, 147–149. Vincent, C., Babendreier, D. and Kuhlmann, U. (2002) European Apple sawfl y, Hoplocampa testudinea Klug (Hymenoptera: Tenthredinidae. In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada 1981–2000. CAB International, Wallingford, UK, pp. 135–139. Vincent, C., Hallman, G., Panneton, B. and Fleurat-Lessard, F. (2003) Management of agricultural insects with physical control methods. Annual Review of Entomology 48, 261–281. Zijp, J.P. and Blommers, L. (1993) Lathrolestes ensator, a parasitoid of the apple sawfl y. Proceedings of Experimental and Applied Entomology 4, 237–242. Zijp, J.P. and Blommers, L.H.M. (2002a) Apple sawfl y Hoplocampa testudinea (Hym., Tenthredinidae) and its parasitoid Lathrolestes ensator in Dutch apple orchards (Hym., Ichneumonidae, Ctenopelmatinae). Journal of Applied Entomology 126, 265–274. Zijp, J.P. and Blommers, L.H.M. (2002b) Impact of the parasitoid Lathrolestes ensator (Hym., Ichneumonidae, Ctenopelmatinae) as antagonist of apple sawfl y Hoplocampa testudinea (Hym., Tenthredinidae). Journal of Applied Entomology 126, 366–377. Chapter 28 203

28 Lambdina fi scellaria (Guenée), Hemlock Looper (Lepidoptera: Geometridae)

Christian Hébert1 and Jacques Brodeur2 1Natural Resources Canada, Canadian Forest Service, Québec; 2Université de Montréal, Montréal, Québec

28.1 Pest Status balsam fi r, Abies balsamea (L.) Mill. (Pinaceae), in the east and on western The hemlock looper, Lambdina fi scellaria hemlock, Tsuga heterophylla (Raf.) Sarg. (Guenée) (Lepidoptera: Geometridae), is a (Pinaceae), in the west. Lambdina fi scel- native species widely distributed across laria is univoltine and overwinters in the Canada. Three subspecies of L. fi scellaria egg stage. Eggs hatch in late spring, well were formerly recognized until the late after bud-break of balsam fi r. Larvae of the 1980s: L. fi scellaria fi scellaria (Guenée) fi rst two instars feed on current-year (eastern hemlock looper), L. fi scellaria needles, but at the 3rd instar they switch to lugubrosa (Hulst) (western hemlock looper) previous years’ foliage and they may thus and L. fi scellaria somniaria (Hulst) (western affect all the photosynthetic potential of a oak looper). However, McGuffi n (1987) tree. Moreover, larvae feed wastefully reported that there were no morphological because they chew on almost all needles differences in genitalia and thus considered without eating them completely (Carroll, L. fi scellaria as a transcontinental species. 1956). Damaged needles dry out and fall Recently, genetic studies have indicated during autumn, which often results in the that the formerly recognized subspecies death of trees during the year in which were in fact expressing polymorphism defoliation is detected. This makes out- within a single species (Sperling et al., break detection particularly challenging 1999). In eastern Canada, two ecotypes but extremely important to improve man- have been recognized: one in the southern age ment of L. fi scellaria populations. part of L. fi scellaria’s range, in which larvae Pupae are frequently located on host trees, go through fi ve instars, and one in the either in bark crevices, under strips of bark northern part of its range, in which larvae or in , but their distribution changes only have four instars (Berthiaume, 2007). with population density (Hébert et al., The most damaging outbreaks have been 2001a). In outbreak conditions, they can be reported in the four-instar ecotype region found abundantly in old stumps or on the (Berthiaume, 2007). The presence of ground, hidden under dead wood, even on ecotypes in the west is unknown. small branches. Adults emerge in late Lambdina fi scellaria is highly poly- summer with males preceding females by a phagous, feeding on a wide variety of both few days (Carroll, 1956). Females live for deciduous and coniferous trees. However, 20–25 days and lay between 100 and 300 most outbreaks have been reported on eggs (Berthiaume et al., 2009).

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 204 Chapter 28

In the east, the most severe outbreaks When infestations are restricted to small have occurred mainly in Newfoundland areas that are easily accessible, severely and Quebec. The most damaging outbreak defoliated stands can be salvaged. Finally, ever recorded peaked in 2000 on the Mimic™ (tebufenozide) has been tested Lower North Shore region in Quebec with successfully in small areas of Newfound- nearly 925,000 ha defoliated (Chabot et al., land from 2001 to 2003 (Crummey, 2001, 2001). In 2009, outbreaks covering 7685 ha 2002, 2003). were also recorded in that region, but even Several native parasitoids attack L. further north, just south of Labrador fi scellaria. The most important parasitoid (Blanc-Sablon region), and it increased to attacking early instars is Apanteles sp. nr. 12,936 ha in 2010 (Ministère des fl avovariatus (Muesebeck) (Hymenoptera: Ressources naturelles et de la Faune, Braconidae) and it can kill up to 50% of L. 2010). During the last decade, several fi scellaria larvae (Carroll, 1956; Hébert et small infestations of short duration were al., 2004). The most important parasitoid also reported in the Lower St Lawrence attacking late-instar larvae is Winthemia region in Quebec, as well as in Nova occidentis Reinhard (Diptera: Tachinidae). Scotia, New Brunswick and Ontario. It lays its eggs on larvae but emerges from Lambdina fi scellaria was also active yearly the host pupa. Parasitism can reach up to in Newfoundland and Labrador between 40% of pupae (Hébert et al., 2004). Pupae 2001 and 2010, peaking in 2003 with are also parasitized by a number of 64,287 ha of defoliation (National Forestry Ichneumonidae (Hymenoptera) species, the Database, 2012). More over, for the fi rst most common ones being Itoplectis con- time in L. fi scellaria outbreak history, quisitor (Say) and Aoplus velox (Cresson). defoliation was reported from southern Overall, ichneumonids can kill up to 35% Labrador in 2006 (Crummey, 2006), the of L. fi scellaria pupae (Hébert et al., 2004). northernmost record for L. fi scellaria. This A number of entomopathogenic micro- incipient outbreak continued until 2010 organisms are known to infect L. fi scellaria. (Evans, 2010) and spray operations were Smirnoff and Jobin (1973) found a Nosema even carried out in 2009 (Carter, 2009). In (Nosematidae) microsporidium and a British Columbia, L. fi scel laria was also nuclear polyhedrosis virus on Anticosti active each year of the decade except in Island, Quebec. However, most declines in 2006, peaking in 2002 with 43,830 ha L. fi scellaria populations involving entomo- defoliated (National Forestry Database, pathogens were caused by two fungus 2012). species, Entomophthora sphaerosperma Fres. and Entomophaga aulicae (E. Reichardt) Humber (Entomophthoraceae) 28.2 Background (Otvos et al., 1973; Jobin and Desaulniers, 1981). These fungi infect young and mature During major outbreaks, the biological larvae, but their impact is mostly observed insecticide Bacillus thuringiensis Berliner at the end of larval development (Carroll, serovar. kurstaki (Btk) (Bacillaceae) is the 1956; Otvos, 1973). A mass rearing tech- product that is most often used against L. nique for E. aulicae was developed by fi scellaria. Foray® 76B is the most widely Nolan (1993). Furthermore, a new species used formulation, but the province of of Protozoa, Leidyana canadensis Clopton Newfoundland and Labrador also tested and Lucarotti (Eugregarinida: Leidyanidae), Bioprotec HP and VBC-60074. Spraying was found and described by Clopton and with Btk is usually done when egg hatching Lucarotti (1997) and Lucarotti et al. (1998) is completed, while larvae feed on the new during an outbreak collapse in New foliage. When heavy defoliation is Brunswick. However, it has not been expected, a second Btk application may be possible to estimate its real contribution to made. L. fi scellaria pest population decline. Chapter 28 205

28.3 Biological Control Agents 28.4 Evaluation of Biological Control

Since 2000, research has shown that egg The possibility of introducing exotic parasitism by Telenomus spp. (Hymen- parasitoids to strengthen the complex of optera: Scelionidae) plays a key role in L. natural enemies in Newfoundland has been fi scellaria population dynamics (Hébert et evaluated without success (West and al., 2001b; Carleton et al., 2010; Legault et Kenis, 1997). The four parasitoids tested al., 2012). A major outbreak predicted for attacked larvae under laboratory conditions 1997 in the Gaspé Peninsula (Quebec) but were all encapsulated. No other trials collapsed due to very high egg parasitism were done in the 2000s. by Telenomus spp. This was the fi rst In the past, egg parasitism was not report of a natural biological control considered in L. fi scellaria outbreak fore- involving Telenomus spp. on L. fi scellaria. casting, probably because egg surveys were Investi gations on the taxonomy of this done in autumn when parasitism is low poorly known genus revealed the presence (Hébert et al., 2001b, 2006; Carleton et al., of three species attacking L. fi scellaria: 2009; Legault et al., 2012). This lack of Teleno mus coloradensis Crawford, T. knowledge with respect to the intensive droozi Muesebeck and T. fl avotibiae spring activity of Telenomus spp. may have Pelletier, the last being new to science led to unnecessary spraying of insecticides. (Pelletier and Piché, 2003). More recently, Since the role of Telenomus spp. has been a fourth, as yet unidentifi ed Telenomus sp. discovered, spring surveys are now con- was found in Quebec (Carleton et al., ducted to confi rm population densities. In 2009; G. Pelletier, Quebec, 2012, pers. Quebec, this approach led to the cancel- comm.). Telenomus coloradensis is the lation of a 50,000-ha spray programme on most common species, followed by T. the North Shore region in 2001 when most droozi. Field studies showed that L. fi scellaria populations collapsed (Chabot Telenomus spp. are active very early in et al., 2001). The Newfoundland and spring, even when snow is still present Labrador region also cancelled a control (Hébert et al., 2006), suggesting that programme in 2006 (Crummey, 2006). females are active at low temperatures. In the past, huge efforts have been Laboratory experiments showed that devoted to classical biological control females of both T. coloradensis and T. attempts (introducing exotic species) to droozi can attack hemlock looper eggs at improve natural control of indigenous 4–8°C, and that the former have a lower pests such as L. fi scellaria. The Telenomus threshold (3.08°C) than the latter (4.67°C). spp. example shows that we should be The thermal threshold of T. coloradensis more aware of indigenous natural enemies activity is nearly the same as for hatching affecting indigenous pests. This conclusion of L. fi scellaria eggs (3°C) (Hartling et al., was part of the fi rst recommendation in a 1991), which would provide an ecological report by van Frankenhuyzen et al. (2002), advantage to this species (Legault et al., and the knowledge acquired over the last 2012). This could explain T. coloradensis’s decade confi rms that research on Teleno- higher capacity to respond to host density mus spp. should continue. Any natural and thus its higher potential to regulate L. enemy that can attack and kill >70% of its fi scellaria populations (Carleton et al., host within 1 week certainly deserves the 2010). Weekly parasitism by Telenomus highest consideration. spp. using sentinel traps reached >70% in Implementing the second part of van spring, thus confi rming the strong Frankenhuyzen et al.’s (2002) recom- potential of Telenomus spp. for biological mendation, which deals with the inte- control (Legault et al., 2012). gration of biological control into a pest 206 Chapter 28

management programme, implies con tinu- 3. Estimating how global warming will ing research on Telenomus spp. parasitoids. change synchrony between Telenomus spp. and L. fi scellaria, and how it will impact their effi cacy across its geographic distribu- 28.5 Future Needs tion. A fi rst appraisal of this issue is pre- sented in Legault (2012). Future work should include: 1. Incorporating estimates of Telenomus spp. egg parasitism levels into L. fi scellaria Acknowledgements defoliation forecasting; 2. Improving knowledge of the life cycle of We thank Isabelle Lamarre from the Telenomus spp. to develop effi cient rearing Laurentian Forestry Centre of the Canadian techniques to test inundative biological Forest Service for editing the manuscript. control;

References

Berthiaume, R. (2007) Écologie évolutive des populations d’arpenteuse de la pruche. PhD thesis, Université Laval, Québec, Canada. Berthiaume, R., Hébert, C., Lamontagne, L., Picard, I. and Bauce, É. (2009) Daily oviposition pattern of Lambdina fi scellaria (Lepidoptera: Geometridae) under laboratory conditions. The Canadian Entomologist 141, 309–315. Carleton, D., Royer, L., Hébert, C., Delisle, J., Berthiaume, R., Bauce, E. and Quiring, D. (2009) Seasonal parasitism of hemlock looper (Lepidoptera: Geometridae) eggs in eastern Canada. The Canadian Entomologist 141, 614–618. Carleton, D., Quiring, D., Heards, S., Hébert, C., Delisle, J., Berthiaume, R., Bauce, E. and Royer, L. (2010) Density-dependent and density-independent responses of three species of Telenomus parasitoids of hemlock looper eggs. Entomologia, Experimentalis et Applicata 137, 296–303. Carroll, W.J. (1956) History of the hemlock looper, Lambdina fi scellaria fi scellaria (Guen.), (Lepidoptera: Geometridae) in Newfoundland, and notes on its biology. The Canadian Entomologist 88, 587–599. Carter, N. (2009) Newfoundland and Labrador 2009 forest insect control program. In: Proceedings of the Forest Pest Management Forum 2009. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 127–130. Chabot, M., Bordeleau, C. and Aubin, É. (2001) Arpenteuse de la pruche, Lambdina fi scellaria fi scellaria (Guen.). In: Insectes, maladies et feux dans les forêts québécoises en 2001. Ministère des Ressources naturelles, Québec, Québec, Canada, pp. 12–16. Clopton, R.E. and Lucarotti, C.J. (1997) Leidyana canadensis n. sp. (Apicomplexa: Eugregarinida) from larval eastern hemlock looper, Lambdina fi scellaria fi scellaria (Lepidoptera: Geometridae). Journal of Eukaryotic Microbiology 44, 383–387. Crummey, H. (2001) Newfoundland: status of forest insect activity in 2001 and preliminary outlook for 2002. In: Proceedings of the Forest Pest Management Forum 2001. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 271–280. Crummey, H. (2002) Newfoundland: status of forest insect activity in 2002 and preliminary outlook for 2003. In: Proceedings of the Forest Pest Management Forum 2002. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 160–169. Crummey, H. (2003) Newfoundland and Labrador: status of forest insect activity in 2003 and preliminary outlook for 2004. In: Proceedings of the Forest Pest Management Forum 2003. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 175–184. Crummey, H. (2006) Status of important forest insect activity in 2006 and outlook for 2007 – Newfoundland & Labrador. In: Proceedings of the Forest Pest Management Forum 2006. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 167–178. Evans, J. (2010) Newfoundland & Labrador 2010 forest insect and disease control program. In: Proceedings of the Forest Pest Management Forum 2010. Natural Resources Canada, Ottawa, Ontario, Canada, pp. 7–11. Chapter 28 207

Hartling, L., MacNutt, P.M. and Carter, N. (1991) Hemlock looper in New Brunswick: notes on biology and survey methods. Department of Natural Resources & Energy, Fredericton, New Brunswick, Canada. Hébert, C., Jobin, L., Berthiaume, R., Coulombe, C. and Dupont, A. (2001a) Changes in hemlock looper [Lepidoptera: Geometridae] pupal distribution through a 3-year outbreak cycle. Phytoprotection 82, 57–63. Hébert, C., Berthiaume, R., Dupont, A. and Auger, M. (2001b) Population collapses in a forecasted outbreak of Lambdina fi scellaria (Lepidoptera: Geometridae), caused by spring egg parasitism by Telenomus spp. (Hymenoptera: Scelionidae). Environmental Entomology 30, 37–43. Hébert, C., Jobin, L., Berthiaume, R., Mouton, J.-F., Dupont, A. and Bordeleau, C. (2004) A new standard pupation shelter for sampling pupae and estimating mortality of the hemlock looper (Lepidoptera: Geometridae). The Canadian Entomologist 136, 879–887. Hébert, C., Berthiaume, R. and Bordeleau, C. (2006) Polyurethane foam strips to estimate parasitism of hemlock looper (Lepidoptera: Geometridae) eggs by Telenomus spp. (Hymenoptera: Scelionidae). The Canadian Entomologist 138, 114–117. Jobin, L.J. and Desaulniers, R. (1981) Results of aerial spraying in 1972 and 1973 to control the eastern hemlock looper (Lambdina fi scellaria fi scellaria [Guen.]) on Anticosti Island. Information Report LAU-X-49E, Canadian Forestry Service, Sainte-Foy, Québec, Canada. Legault, S. (2012) Écologie saisonnière des parasitoïdes des œufs de l’arpenteuse de la pruche. MSc thesis, Université de Montréal, Montréal, Québec, Canada. Legault, S., Hébert, C., Blais, J., Berthiaume, R., Bauce, E. and Brodeur, J. (2012) Seasonal ecology and thermal constraints of Telenomus spp. (Hymenoptera: Scelionidae), egg parasitoids of the hemlock looper (Lepidoptera: Geometridae). Environmental Entomology 41(6), 1290–1301. Lucarotti, C.J., Leclerc, T.L. and Clopton, R.E. (1998) Incidence of Leidyana canadensis (Apicomplexa: Eugregarinida) in Lambdina fi scellaria fi scellaria larvae (Lepidoptera: Geometridae). The Canadian Entomologist 130, 583–594. McGuffi n, W.C. (1987) Guide to the Geometridae of Canada (Lepidoptera). II. Subfamily Ennominae. 4. Memoirs of the Entomological Society of Canada 138, 1–182. Ministère des Ressources naturelles et de la Faune (MRNF) (2010) Arpenteuse de la pruche, Lambdina fi scellaria fi scellaria (Guen.). In: Insectes, maladies et feux dans les forêts québécoises, 2010. Ministère des Ressources naturelles du Québec, p. 5. National Forestry Database (2012) Forest Insects – National tables, Table 4.1 Area within which moderate to severe defoliation occurs including area of beetle-killed trees by insects and province/territory, 1975-2010 – Hemlock looper. Available at: http://nfdp.ccfm.org/data/ compendium/html/comp_41e.html#bookMark_Da (accessed 14 May 2012). Nolan, R.A. (1993) An inexpensive medium for mass fermentation production of Entomophaga aulicae hyphal bodies competent to form conidia. Canadian Journal of Microbiology 39, 588– 593. Otvos, I.S. (1973) Biological control agents and their role in the population fl uctuation of the eastern hemlock looper in Newfoundland. Information Report N-X-102, Canadian Forest Service, St John’s, Newfoundland, Canada. Otvos, I.S., MacLeod, D.M. and Tyrrell, D. (1973) Two species of Entomophthora pathogenic to the eastern hemlock looper (Lepidoptera: Geometridae) in Newfoundland. The Canadian Entomologist 105, 1435–1441. Pelletier, G. and Piché, C. (2003) Species of Telenomus (Hymenoptera: Scelionidae) associated with the hemlock looper (Lepidoptera: Geometridae) in Canada. The Canadian Entomologist 135, 23–29. Smirnoff, W.A. and Jobin, L.J. (1973) Étude de certains facteurs affectant les populations de Lambdina fi scellaria fi scellaria dans le bassin de la rivière Vauréal, île d’Anticosti. The Canadian Entomologist 105, 1039–1040. Sperling, F.A.H., Raske, A.G. and Otvos, I.S. (1999) Mitochondrial DNA sequence variation among populations and host races of Lambdina fi scellaria (Gn.) (Lepidoptera: Geometridae). Insect Molecular Biology 8, 97–106. van Frankenhuyzen, K., West, R.J. and Kenis, M. (2002) Lambdina fi scellaria fi scellaria (Guenée), Hemlock Looper (Lepidoptera: Geometridae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 141–144. West, R.J. and Kenis, M. (1997) Screening four exotic parasitoids as potential controls for the eastern hemlock looper, Lambdina fi scellaria fi scellaria (Guenée) (Lepidoptera: Geometridae). The Canadian Entomologist 129, 831–841. 208 Chapter 29

29 Lilioceris lilii (Scopoli), Lily Leaf Beetle (Coleoptera: Chrysomelidae)

Naomi Cappuccino,1 Tim Haye,2 Lisa Tewksbury3 and Richard Casagrande3 1Carleton University, Ottawa, Ontario; 2CABI Europe-Switzerland, Delémont, Switzerland; 3University of Rhode Island, Kingston, Rhode Island

29.1 Pest Status 2001). This feature makes infestations especially repulsive to gardeners. Because Lily leaf beetle, Lilioceris lilii (Scopoli) Asiatic lilies are themselves non-native, L. (Coleoptera: Chrysomelidae), a pest of lilii has been considered to be primarily a cultivated Asiatic lilies Lilium spp. and horticultural pest. However, L. lilii has fritillaries Fritillaria spp. (Liliaceae), was recently expanded its diet to include the fi rst recorded in Montreal in 1943 (LeSage, native Lilium canadense L. (Liliaceae) in 1992). Limited to the island of Montreal Quebec (Bouchard et al., 2008) and New until around 1978 (Bouchard et al., 2008), Brunswick (Majka and LeSage, 2008). its range has since been expanding and it Natural infestations of L. lilii have been has now been reported from Quebec, found on L. canadense L. and Lilium Ontario, Manitoba, the Maritime provinces, superbum L. (Liliaceae) in Rhode Island (L. New England, New York and New Jersey Tewksbury, 2012, unpublished results). In (Gold, 2003; Majka and Kirby, 2011; R. the laboratory, the larvae perform well on Casagrande, 2012, unpublished results). Lilium philadelphicum L. (Liliaceae) (Ernst Pockets of infestation have been reported et al., 2007), although natural infestations in Alberta (Ken Fry, Olds, Alberta, 2011, on this potential host plant have not yet pers. comm.). Given its large Palaearctic been recorded. As it expands its range native range – from northern Africa to across North America, the beetle will Scandinavia and east to and China undoubtedly come into contact with (Gold, 2003) – it is likely that L. lilii will be several species of native lilies, approxi- able to colonize much of North America mately half of which are threatened or (Kenis et al., 2003). endangered (USDA, NRCS, 2012). Both adults and larvae feed on the leaves of their host plants and, in dense infestations, they may damage the buds 29.2 Background and fl owers as well. As they feed, the larvae cover their dorsal surfaces with their 29.2.1 Life history wet excrement, forming a shield that pro- tects them from most predators and general- The scarlet-and-black adults of L. lilii ist parasitoids (Schaffner and Müller, overwinter and emerge from early April

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 29 209

through June to lay orange eggs on the et al., 2001; Majka and LeSage, 2008). undersides of the leaves in linear groups of Lilioceris lilii only rarely attains pest status 3 to 12 (Gold, 2003). Newly-hatched larvae throughout most of continental Europe feed communally, chewing pits in the where it is regulated by a suite of native ventral surface of the leaves. Later instars parasitoids that can impose generally high feed singly, consuming entire leaves and levels of parasitism, with averages of 25– moving up the plant to undamaged foliage. 78% (Table 29.1.) (Gold et al., 2001; Haye After 2–3 weeks, the 4th instars leave the and Kenis, 2004). Populations of L. lilii on plant to pupate in the soil in cocoons the native European lily, Lilium martagon formed by gluing soil particles together. L. (Liliaceae), are particularly heavily para- The new generation adults eclose in mid- sitized (Haye and Kenis, 2004). In England summer, and feed until autumn. A pro- (Salisbury, 2008) and Sweden (Rämert et tracted oviposition period leads to the al., 2009), where both lilies and L. lilii are presence of adults throughout the growing non-native, beetle infestations are generally season and the appearance that L. lilii may much higher than in central Europe. In be bi- or multivoltine; however, Haye and Sweden, the parasitoid assemblage and Kenis (2004) have shown that the beetle is parasitism rates are similar to that in strictly univoltine. central Europe, so it is somewhat surpris- ing that infestations of the beetle can be severe (Rämert et al., 2009). 29.2.2 Non-biological control approaches

For small gardens, the recommended 29.3 Biological Control Agents control is to hand-pick adults off the plants and squash the eggs (University of Rhode Following host-specifi city screening (Haye, Island Plant Sciences Department, 2002). 2000; Scarborough, 2002; Casagrande and With the long adult emergence and Kenis, 2004), three parasitoids from Europe oviposition period, hand picking must be were chosen for release in New England, carried out throughout the summer. Many USA, for classical biological control of L. gardeners loathe hand-picking late instars lilii: Tetrastichus setifer Thomson (Hymen- because of their messy faecal shields. For optera: Eulophidae), Diaparsis jucunda larger infestations, effective insecticides Holmgren and Lemophagus errabundus include carbaryl (Sevin) as well as the (Gravenhorst) (Hymenoptera: Ichneu- systemic insecticide imidacloprid (Uni- monidae) (Table 29.1). versity of Rhode Island Plant Sciences Tetrastichus setifer is the most widely Department, 2002); however, these are non- distributed parasitoid of L. lilii in Europe; selective and especially harmful to however, it is dominant only in northern pollinators (Lu et al., 2012). The botanical Germany and central Sweden (Haye and pesticide neem, a powerful antifeedant and Kenis, 2004; Rämert et al., 2009). T. setifer growth disruptor that is non-toxic to is a gregarious parasitoid; up to 26 mammals and pollinators (Isman, 2006), individuals have been reported emerging provides effective control of 1st instar from a single host (Haye and Kenis, 2004). larvae. However, neem must be re-applied Females attack all four larval instars of L. throughout the summer as new eggs hatch lilii, although they have more diffi culty (University of Rhode Island Plant Sciences penetrating the thick faecal shield of older Department, 2002). larvae (Haye and Kenis, 2004). Tetrastichus setifer is univoltine and kills the host in the prepupal stage. The mature larvae over- 29.2.3 Natural enemies winter in the host’s cocoon in the soil. Adult emergence, like that of its host, is In North America, no arthropod natural spread over several weeks in the spring enemies of L. lilii have been reported (Gold (Haye and Kenis, 2004). 210 Chapter 29

Table 29.1. Parasitoids associated with Lilioceris lilii in Europe, their host range and status as biological control agents in North America (After Haye and Kenis, 2004; Gold, 2003; Tschorsnig and Herting, 1998; Tewksbury et al., 2005; Cerretti and Tschorsnig, 2010). Release year(s) Parasitoid species Host range (USA) Established (year) Larval parasitoids Hymenoptera: Ichneumonidae Coleoptera: Chrysomelidae Diaparsis jucunda (Holmgren) Lilioceris lilii (Scopoli) 2003 Massachusetts (2007) Lilioceris merdigera L. Rhode Island (2004) Lilioceris tibialis Villa New Hampshire (2006)

Lemophagus errabundus Lilioceris lilii 2003–2004 Massachusetts (2005) (Gravenhorst) Lilioceris merdigera Rhode Island (2006) Lilioceris tibialis

Lemophagus pulcher (Szepligeti) Lilioceris lilii Lilioceris merdigera Lilioceris tibialis Crioceris asparagi (L.)1 Lema trilineata (Olivier)1

Hymenoptera: Eulophidae Tetrastichus setifer Thomson Lilioceris lilii 1999–2004 Massachusetts (2001) Lilioceris merdigera Rhode Island (2003) Lilioceris tibialis Maine (2004) New Hampshire (2005) Ontario (2010, 2012)

Diptera: Tachinidae Meigenia simplex Tschorsnig and Lilioceris lilii Herting Crioceris asparagi Crioceris quatuordecimpunctata (L.) Chrysomela populi L. Chrysomela tremula Fabricius Phratora laticollis Suffrian

Meigenia uncinata Mesnil Lilioceris lilii Agelastica alni (L.) Altica brevicollis Foudras Chrysomela populi

Egg parasitoids Hymenoptera: Mymaridae Anaphes spp. Lilioceris lilii Lilioceris merdigera unknown host(s) for overwintering

1Attacked in laboratory host range tests Chapter 29 211

Diaparsis jucunda is the dominant sidered for biological control of L. lilii due parasitoid of L. lilii in central Europe to their lower host specifi city (Table 29.1) (Switzerland, Austria, Italy), causing high (Casagrande and Kenis, 2004). levels of parasitism, particularly in natural Anaphes sp. (Hymenoptera: Mymari- lily stands in Switzerland. Although dae), a common egg parasitoid of L. lilii in reported from Sweden, Finland and forest areas of Switzerland (Haye and Denmark, it is nearly absent from western Kenis, 2004), has been considered for aug- and northern Europe (Horstmann, 1971; mentative or inundative releases against L. Haye and Kenis, 2004; Rämert et al., 2009). lilii in Sweden (Rämert et al., 2009), but This solitary parasitoid attacks all larval since it likely needs to overwinter in an stages of L. lilii and is active from May to unknown alternate host to complete its July when the highest densities of beetle cycle, it is not considered for releases in larvae are found in the fi eld. Females can Canada. produce more than 360 eggs and live for In the USA, between 1999 and 2004, T. about 1 month. The host is killed in the setifer was released in Massachusetts, prepupal stage, and the univoltine para- Rhode Island, Maine and New Hampshire. sitoid overwinters as a mature larva in the It has successfully established in all four host cocoon in the soil (Haye and Kenis, and is providing excellent control of L. lilii, 2004). imposing parasitism rates of up to 100% Lemophagus errabundus, also solitary, (Tewksbury et al., 2005). It has spread over is the dominant larval parasitoid in 11 km from the original release sites western and northern Europe (England, the (Casagrande and Tewksbury, 2007). Netherlands, Belgium, western France and Lemophagus errabundus was released in northern Germany) where it displaces D. Massachusetts and Rhode Island; it, too, jucunda (Salisbury, 2003; Haye and Kenis, has established and has spread a 2004). In central Europe it is rare. The considerable distance. Diaparsis jucunda univoltine parasitoid attacks 2nd to 4th has successfully established in Massa- instar larvae and kills its host in the chusetts, Rhode Island and New Hamp- prepupal stage. The adults are found from shire (L. Tewksbury and R. Casagrande, mid-May to the end of June. The parasitoid 2012, unpublished results). overwinters as a teneral adult in its cocoon In Canada, a petition for release of T. made inside the beetle’s pupal cell (Haye setifer (Cappuccino et al., 2009) was and Kenis, 2004). approved and a fi rst release was made in Larval parasitism by T. setifer is highest mid-June, 2010, at the Central Experi- from mid-June to mid-August, but low in mental Farm, Ottawa, Ontario (45.3886°, May when its competitors D. jucunda and −75.7127°). Tetrastichus setifer adults for L. errabundus are most active (Haye, 2000). release were obtained from populations Competition trials indicate that when T. established in Rhode Island, USA. setifer oviposits fi rst it is more likely to Approximately 50 individuals were survive and develop in L. lilii larvae than released in a small plot of Asiatic lilies D. jucunda and L. errabundus (Gold, 2003). ‘Pixie’ (100 plants in a grid of approxi- However, when D. jucunda oviposits fi rst, mately 30 m2) with densities of 1–2 larvae it is more likely to outcompete T. setifer. per plant. The release was timed so that Oviposition of L. errabundus followed by most host larvae were in the 3rd instar. oviposition by T. setifer seems to decrease survival of both species (Gold, 2003). Other larval parasitoids found in Europe 29.4 Evaluation of Biological include Lemophagus pulcher (Szepligeti) Control (Hymenoptera: Ichneumonidae), Meigenia simplex Tschorsnig and Herting and In July, 2011 larvae of L. lilii were collected Meigenia uncinata Mesnil (Diptera: Tach- in the release plot and reared until inidae). These species have not been con- pupation. Upon dissection of the cocoons, 212 Chapter 29

5 of 30 were found to be parasitized by T. nearby sites to determine its effectiveness setifer, indicating that the agent over- in reducing populations of L. lilii and its wintered successfully. It is too soon to capacity for dispersal; determine whether there has been an 2. Further releases of T. setifer in other impact on pest population levels. regions of Canada in close cooperation with Canadian Lily Grower Societies; 3. Possible releases of L. errabundus or D. jucunda in Canada to achieve higher para- 29.5 Future Needs sitism of L. lilii larvae in spring before T. setifer has emerged. Since L. errabundus Future work should include: causes high parasitism in northern Europe, 1. Continued monitoring of T. setifer para- it might be well suited to climatic condi- sitism levels at the release site as well as tions in Canada.

References

Bouchard, A.M., McNeil, J.N. and Brodeur, J. (2008) Invasion of American native lily populations by an alien beetle. Biological Invasions 10, 1365–1372. Cappuccino, N., Mason, P.G., Casagrande, R.A., Kenis, M., Haye, T. and Tewksbury, L. (2009) Petition for cage- and open fi eld release of Tetrastichus setifer (Hymenoptera: Eulophidae) for biological control of the lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae) in Canada. Carleton University, Ottawa, Ontario, Canada. Casagrande, R.A. and Kenis, M. (2004) Evaluation of lily leaf beetle parasitoids for north American introduction. In: Van Driesche, R. and Reardon, R. (eds) Assessing Host Ranges for Parasitoids and Predators Used for Classical Biological Control: A guide to best practice. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, FHTET 2004-03, pp. 110–124. Casagrande, R.A. and Tewksbury, L.A. (2007) Lily Leaf Beetle Biological Control. Research Report to the North American Lily Society, 12 January 2007. Department of Plant Sciences, University of Rhode Island. Cerretti, P. and Tschorsnig, H.P. (2010) Annotated host catalogue for the Tachinidae (Diptera) of Italy. Stuttgarter Beiträge zur Naturkunde A, Neue Serie 3, 305–340. Ernst, C., Cappuccino, N. and Arnason, J.T. (2007) Potential novel hosts for the lily leaf beetle Lilioceris lilii Scopoli (Coleoptera: Chrysomelidae) in eastern North America. Ecological Entomology 32, 45–52. Gold, M.S. (2003) Biological control of the lily leaf beetle, Lilioceris lilii, in North America. PhD thesis, University of Rhode Island, Kingston, USA. Gold, M.S., Casagrande, R.A., Tewksbury, L.A., Livingston S.B. and Kenis, M. (2001) European parasitoids of Lilioceris lilii (Coleoptera: Chrysomelidae). The Canadian Entomologist 133, 671– 674. Haye, T. (2000) Ökologische Studien zum Parasitoidenkomplex von Lilioceris lilii (Scop.) (Coleoptera: Chrysomelidae) an ausgewählten Mitteleuropäischen Standorten. Diploma Thesis, Christian-Albrechts-University, Kiel, Germany. Haye, T. and Kenis, M. (2004) Biology of Lilioceris spp. (Coleoptera: Chrysomelidae) and their parasitoids in Europe. Biological Control 29, 399–408. Horstmann, K. (1971) Revision der europäischen Tersilochinen (Hymenoptera: Ichneumonidae) Teil 1. Veröffentlichungen der Zoologischen Staatssammlung München 15, 45–138. Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 45–66. Kenis, M., Haye, T., Casagrande, R.A., Gold, M.S. and Tewksbury, L.A. (2003) Selection and importation of European parasitoids for the biological control of the lily leaf beetle in North America and prospects for control in Europe. In: Van Driesche, R. (ed.) Proceedings of the 1st International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, USA. United Chapter 29 213

States Department of Agriculture, Forest Service, Morgantown, West Virginia, FHTET-2003-05, pp. 416–419. LeSage, L. (1992) The lily beetle, Lilioceris lilii (Scopoli) (Coleoptera: Chrysomelidae) in Canada. La Revue Canadienne des Insectes Nuisibles aux Cultures 70, 88–96. Lu, C., Warchol, K.M. and Callahan, R.A. (2012) In situ replication of honeybee colony collapse disorder. Insectology 65, 99–106. Majka, C.G. and Kirby, C. (2011) Lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae), in Maine and the Maritime Provinces: the continuing dispersal of an invasive species. Journal of the Acadian Entomological Society 7, 70–74. Majka, C.G. and LeSage, L. (2008) Introduced leaf beetles of the Maritime Provinces, 5: the lily leaf beetle, Lilioceris lilii (Scopoli) (Coleoptera: Chrysomelidae). Proceedings of the Entomological Society of Washington 110, 186–195. Rämert, B., Kenis, M., Kroon, H. and Nilsson, U. (2009) Larval parasitoids of Lilioceris lilii (Coleoptera: Chrysomelidae) in Sweden and potential for biological control. Biocontrol Science and Technology 19, 335–339. Salisbury, A. (2003) Two parasitoids of the lily beetle Lilioceris lilii (Scopoli) (Coleoptera: Chrysomelidae), in Britain, including the fi rst record of Lemophagus errabundus Gravenhorst (Hymenoptera: Ichneumonidae). British Journal of Entomology and Natural History 16, 103–104. Salisbury, A. (2008) Lily beetle and prospects for control. Plantsman 7, 230–234. Scarborough, C. (2002) An investigation of the parasitoids of the lily leaf beetle, Lilioceris lilii (Scopoli) (Coleoptera: Chrysomelidae): a case study for biological control in North America. MSc Thesis, University of London, Imperial College, London. Schaffner, U. and Müller, C. (2001) Exploitation of the fecal shield of the lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae), by the specialist parasitoid Lemophagus pulcher (Hymenoptera: Ichneumonidae). Journal of Insect Behaviour 14, 739–757. Tewksbury, L., Gold, M.S., Casagrande, R.A. and Kenis, M. (2005) Establishment in North America of Tetrastichus setifer Thomson (Hymenoptera: Eulophidae), a parasitoid of Lilioceris lilii (Coleopetera: Chrysomelidae). In: Hoddle, M. (compiler) Proceedings of the 2nd International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12–16 September 2005. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, FHTET- 2005-08, pp. 142–143. Tschorsnig, H.P. and Herting, B.H. (1998) A new species of the genus Meigenia Robineau-Desvoidy (Diptera: Tachinidae). Stuttgarter Beiträge zur Naturkunde Serie A 569, 1–5. University of Rhode Island Plant Sciences Department (2002) Fact sheet: Lily leaf beetle. Available at: http://www.uri.edu/ce/factsheets/sheets/lilyleafbeetle.html (accessed 31 July 2012). USDA, NRCS (2012) The PLANTS Database. National Plant Data Team, Greensboro, NC 27401-4901 USA. Available at: http://plants.usda.gov (accessed 31 July 2012). 214 Chapter 30

30 Listronotus oregonensis (LeConte), Carrot Weevil (Coleoptera: Curculionidae)

Guy Boivin Agriculture et Agroalimentaire Canada, St Jean-sur-Richelieu, Québec

30.1 Pest Status Listronotus oregonensis has from one to three generations per year depending on The carrot weevil, Listronotus oregonensis the location. While it has one to two (LeConte) (Coleoptera: Curculionidae), is generations in Quebec (Boivin, 1985), native to north-east North America Ontario (Stevenson, 1976) and Massa- (Simonet, 1981) and its distribution ranges chusetts (Whitcomb, 1965), it has two in from Nova Scotia to Manitoba and Iowa in Illinois (Wright and Decker, 1958), New the west and south to Louisiana (Boyce, Jersey (Ryser, 1975), Ohio (Simonet, 1981) 1927; Perron, 1971; Stevenson, 1976; and Michigan (Grafi us et al., 1983) and Grafi us and Collins, 1986; Le Blanc and three in New York (Boyce, 1927) and Iowa Boivin, 1993; Boivin, 1999). It is a major (Harris, 1926). However, it is expected that pest of carrots, Daucus carota subsp. climate change will affect the number of sativus Schülb. and M. Martens, and generations of this species. Listronotus celery, Apium graveolens L., and a minor oregonensis had only one generation in pest of parsnip, Pastinaca sativa L., Quebec until the mid-1990s but since then parsley, Petroselinum crispum (Mill.) Fuss, a second generation has appeared and the dill, Anethum graveolens L. (Apiaceae), importance of this pest has been increasing and turnip, Brassica rapa L. (Brassicaeae) steadily. (Pepper and Hagmann, 1938; Whitcomb, Listronotus oregonensis overwinters as 1965; Hill, 1987). Several wild plants are adults that emerge early the following hosts of the carrot weevil: wild carrot, spring. Most females are mated prior to Daucus carota L., dill, A. graveolens, wild overwintering (Ryser, 1975; Simonet and parsnip, Apium petroselinum L., water Davenport, 1981) as mating occurs shortly parsnip, Sium suave Walter (Apiaceae), after the emergence of the females in late common plantain, Plantago major L., summer (Baudoin and Boivin, 1985). The lance-leafed plantain, Plantago lanceolata females start ovipositing as soon as the L. (Plantaginaceae), wild turnip, B. rapa, degree-day accumulation permits (Boivin, and several Rumex species, Rumex patiena 1988). On carrots, the eggs are laid mostly L., R. acetosa L., R. obtusifolius L. and R. in leaf petioles (80%) and in the crown of crispus L. (Polygonaceae) (Ryser, 1975; the plant (18%) (Boivin, 1988). Less than Collins and Grafi us, 1984; Boivin, 1994, 1% of all eggs are laid below the root 1999). crown. Upon emergence the larva either

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 30 215

crawls on the surface of the carrot foliage The relatively low reproductive to the crown of the plant or burrows down potential of L. oregonensis, about 200 eggs a leaf petiole toward the root. It then starts per female, and its limited range of a tunnel that is normally found super- migration are positive characteristics when fi cially in the upper third of the root biological control is considered (Boivin, (Boivin, 1994). As the larvae mature, they 1992). However, the fact that the fi rst three stop feeding and leave the carrot as larval instars spend most of their prepupae to build an earthen pupation cell development inside carrot roots may limit near the carrot (Martel et al., 1976). the action of natural enemies on these A reproductive diapause has been stages. shown in female L. oregonensis (Stevenson In laboratory studies, conidiospores of and Boivin, 1990). The occurrence of Beauveria bassiana (Balsamo) Vuillemin repro ductive diapause is regulated by (Corycipitaceae) and Metarhizium anisopliae inter action of photoperiod and tem- (Metschnikoff) Sorokin (Clavicipitaceae) perature. When sexually immature females caused some mortality of larvae (Searle and are exposed to low photoperiod (12 or 14 h Yule, 1988), but no data are available on the light at <20°C) they do not lay eggs and, prevalence of microorganisms in natural when dissected, contain no eggs. Sexually populations of L. oregonensis. Three species mature females cease oviposition at of entomo phagous nematodes were tested gradually higher temperatures as daylength against the late larvae, pupae and adults of L. increases. Overwintered females do not oregonensis (Bélair and Boivin, 1985). All respond to photoperiod, which enables stages were killed by Steinernema carpo- them to start ovipositing as soon as the capsae (Weiser) (DD136 strain), S. feltiae degree-day accumulation permits (Boivin, (Filipjev) (T335 strain) (Rhabdita: Steiner- 1988). nematidae) and Heterorhabditis bacterio- phora Poinar (Rhabdita: Heterorhabditidae). Late instar larvae were more susceptible to 30.2 Background the nematodes than the pupae and adults. A local strain of S. carpocapsae was isolated At present, adults of L. oregonensis are from L. oregonensis adults and compared to controlled in Canada by applying one or the commercially available strain DD136 two foliar insecticides, ideally following (Boivin and Bélair, 1989). Both strains monitoring to indicate proper timing. decreased longevity and oviposition by L. Treatments must be made after most adults oregonensis adults. have left their overwintering sites but prior More recently a nematode, Bradynema to egg laying (Boivin, 1994). Crop rotation listronoti Zeng et al. (Tylenchida: Allen- is effective if a carrot fi eld is planted tonematidae), that acts more as a castrator remotely from fi elds previously planted in parasite than a parasitoid, was described carrots (Stevenson and Chaput, 1993); from L. oregonensis adults (Zeng et al., however, it is almost impossible to isolate 2007). This nematode parasitized 30–60% carrot fi elds from a source of L. of adults sampled in spring. While B. oregonensis in areas of intensive carrot listronoti causes only low mortality, it cultivation (Boivin, 1994). Sowing date castrates female L. oregonensis after a few also infl uences damage intensity as late- days and as such eliminates damage to host sown carrots escape most L. oregonensis plants. Both sexes, when infected, continu- oviposition. Carrots seeded after 400 ously release nematodes into the environ- degree-days (base of 7°C) should escape ment throughout their life. However, none most of the damage (Boivin, 1988), but the of these microorganisms or nematodes is increased preva lence of a second used commercially. generation decreases the usefulness of late The only L. oregonensis predators for sowing of carrot. which we have data are carabid beetles 216 Chapter 30

(Coleoptera: Carabidae). As expected, in percentage of egg mortality caused by these the laboratory the smallest species, parasitoids has been estimated to be 49% Bembidion quadrimaculatum oppositum in Michigan (Collins and Grafi us, 1986b), Say and Clivina fossor L., consumed the 68% in Ontario (Cormier et al., 1996) and most eggs while the larger Pterostichus 60% in Quebec (Boivin, 1986). In all, four melanarius (Illiger) consumed more teneral species of Mymaridae have been found to and overwintered L. oregonensis adults in parasitize L. oregonensis eggs. These are A. no-choice tests (Baines et al., 1990). victus from Quebec, Ontario and Michigan, However, when B. quadrimaculatum A. listronoti from Quebec, Ontario and oppositum adults were placed in contact Michigan, Anaphes cotei Huber (Hymen- with carrot plants on which L. oregonensis optera: Mymaridae) from Nova Scotia and females had oviposited, they did not fi nd an Anagrus sp. (Hymenoptera: Mymaridae) and consume a single egg (Zhao et al., from Quebec (Hooper et al., 1996; Huber et 1990), while the larger P. melanarius al., 1997). consumed almost four L. oregonensis adults in a 24 h period. Direct observation showed that the large carabids were 30.3 Biological Control Agents effi cient at detecting and eating L. oregonensis adults when on the soil but as A new host/parasitoid association has been soon as these adults climbed on the plant, created in the laboratory between the carrot the carabids were unable to fi nd them. weevil and Microctonus hyperodae Loan These results suggest that the Carabidae are (Hymenoptera: Braconidae, Euphorinae) natural enemies of the carrot weevil but (Cournoyer and Boivin, 2004). Microctonus that their effect is at best limited. It is hyperodae is a parasitoid of the adults of unlikely that these insects could be used the Argentine stem weevil, Listronotus directly in a biological control programme. bonariensis Kuschel (Coleoptera: Curcu- Chittenden (1924) documented a Micro- lionidae). This South American weevil was bracon sp. (Hymenoptera: Braconidae) as a introduced into New Zealand in the 1920s possible parasitoid and Whitcomb (1965) and has since become a major pasture pest reared Aliolus curculionis (Fitch) (Hymen- in that country (Phillips et al., 1997). optera: Braconidae) from 2% of L. Microctonus hyperodae was released in oregonensis larvae in Massachusetts. These New Zealand in 1991 following collection authors, however, mentioned that these from eight diverse South American species were not important as natural locations (Phillips et al., 1997). In areas of mortality factors for L. oregonensis. Neither New Zealand where M. hyperodae has of these two species has been ever recorded established, parasitism levels as high as again from this host. Extensive sampling 80% have been reported (Goldson et al., and dissection of L. oregonensis larvae, 1994; Barker and Addison, 2006). pupae and adults in Quebec over more Microctonus hyperodae reproduces by than 10 years never found a larval, pupal thelytokous parthenogenesis, and is a or adult parasitoid (G. Boivin, 2002, solitary koinobiont endoparasitoid that unpublished results). attacks Curculionidae adults of the The eggs of L. oregonensis are the stage Brachycerinae subfamily (Loan and Lloyd, most susceptible to attack by parasitoids. 1974; Goldson et al., 1992; Barratt et al., First identifi ed as Anaphes sordidatus 1997). Although the only known host was (Girault) (Hymenoptera: Mymaridae) (Col- L. bonariensis (Loan and Lloyd, 1974), lins and Grafi us, 1986a), these egg para- once released, it was found to also sitoids were later identifi ed as two new parasitize Irenimus aequalis Broun and separate species, Anaphes victus Huber Sitona lepidus Gyllenhal (Coleoptera: and A. listronoti Huber (Hymenoptera: Curculionidae) under fi eld conditions, Mymaridae) (Huber et al., 1997). The albeit at very low levels (Barratt et al., Chapter 30 217

1997). In laboratory experiments, prior to related, but in fact M. hyperodae and subsequent to fi eld release, M. responded only to L. oregonensis and its hyperodae showed a wider host range than faeces. When faeces and host insects were under fi eld conditions. Seven other tested separately, M. hyperodae responded Brachycerinae species were parasitized, to the odours emitted by L. oregonensis but again, parasitism was signifi cantly less adults but not to their faeces, suggesting than for L. bonariensis (Goldson et al., that most of the kairomones came from the 1992; Barratt et al., 1997). Post-release host itself. Host plants were also tested, but studies have validated the predictions that M. hyperodae responded neither to Lolium the impact of M. hyperodae on non-target multifl orum Lamarck (Poaceae) nor to D. weevils would be minimal (Barratt et al., carota leaves (Cournoyer and Boivin, 2010). 2004). Microctonus hyperodae was imported Following these results, in June 2002, from New Zealand into Canada under three releases were made in two untreated quarantine in 1996 and the strain UR21, plots of carrots at Ste-Clotilde, Quebec which originated from Uruguay, has (45.165239°, −73.677471°). A total of 92 adapted to L. oregonensis (Boivin, 1999). adult M. hyperodae and 1449 adult L. The level of parasitism decreased drasti- oregonensis that had been exposed to M. cally in the fi rst few generations to less hyperodae were released. The parasitism than 5% as would be expected in a new level of the released L. oregonensis was host–parasitoid association. After 15 gener- estimated to be around 20%. ations on its new host the parasitism level stabilized at 20–25% and the percentage of emergence from parasitized weevils was 30.4 Evaluation of Biological Control 90% (G. Boivin, 2012, unpublished results). From September 2002 to September 2011, The host specifi city of M. hyperodae samples of adult L. oregonensis were was tested against 24 North American obtained either by hand collection on Curculionidae. It parasitized fi ve species, carrot plants or using a plate trap (Boivin, Listronotus sparsus Say, Listronotus macu- 1985) in experimental plots. A total of licollis Kirby, Nedyus fl avicaudis Bohe- 3690 carrot weevil adults were dissected man, Ceutorhynchus erysimi Fabricius and for the presence of M. hyperodae larvae but Gymnetron tetrum Fabricius (Coleoptera: no parasitized individual was found. There Curculionidae) in addition to L. orego- is therefore no indication that the nensis (G. Boivin, 2012, unpublished parasitoid established following these results). It appears that M. hyperodae releases. females attack mobile hosts and that the Microctonus hyperodae established in behaviour of the host species is important several areas of New Zealand that have a (Cournoyer and Boivin, 2005). temperate climate, but its capacity to The infochemicals used by M. hyper- survive winter in eastern Canada was not odae when searching for its adult weevil evaluated. The lack of success of the hosts were investigated using a Y-shaped introduction could therefore be due to olfactometer. Three Curculioninae species, climatic effects. L. oregonensis, L. sparsus and N. fl avi- The most effective biological control caudis and one Bruchinae, Callosobruchus agents remain the egg parasitoids and the maculatus (Fabricius) (Coleoptera: Curcu- nematode B. listronoti. However, neither of lionidae), and their faeces, were tested. It these natural enemies is able to maintain L. was expected that hosts phylogenetically oregonensis population densities below and ecologically close to L. bonariensis economic thresholds under natural con- would be more attractive than species less ditions. 218 Chapter 30

30.5 Future Needs Acknowledgements

Further research recommended includes: I thank Danielle Thibodeau, Julie Frenette and Josiane Vaillancourt for technical 1. A comprehensive study of the effects of assistance and Michel Cournoyer for some climate on M. hyperodae if further releases of the laboratory data on Microctonus are planned; hyperodae. 2. Testing augmentative releases or habitat manipulation to increase the mortality of L. oregonensis early in the season.

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Ryser, B.W. (1975) Investigations regarding the biology and control of the carrot weevil, Listronotus oregonensis (LeConte), in New Jersey. MSc Thesis, Rutgers University, New Brunswick, New Jersey. Searle, T. and Yule, W.N. (1988) Fungal control of the carrot weevil, Listronotus oregonensis. Abstracts, Proceedings 18th International Congress of Entomology, Vancouver, British Columbia, p. 262. Simonet, D.E. (1981) Carrot weevil management in Ohio vegetables. Ohio Report 66, 83–85. Simonet, D.E. and Davenport, B.L. (1981) Temperature requirements for development and oviposition of the carrot weevil. Annals of the Entomological Society of America 74, 312–315. Stevenson, A.B. (1976) Seasonal history of the carrot weevil, Listronotus oregonensis (Coleoptera: Curculionidae) in the Holland Marsh, Ontario. Proceedings of the Entomological Society of Ontario 107, 71–78. Stevenson, A.B. and Boivin, G. (1990) Interaction of temperature and photoperiod in control of reproductive diapause in the carrot weevil (Coleoptera: Curculionidae). Environmental Entomology 19, 836–841. Stevenson, A.B. and Chaput, J. (1993) Carrot insects. Ontario Ministry of Agriculture and Food. Factsheet Agdex 258/605. Available at: http://www.omafra.gov.on.ca/english/crops/facts/93-077. htm (accessed 13 September 2012). Whitcomb, W.D. (1965) The carrot weevil in Massachusetts. Biology and control. University of Massachusetts Agricultural Experimental Station Bulletin 550, 1–30. Wright, J.M. and Decker, G.C. (1958) Laboratory studies on the life cycle of the carrot weevil. Journal of Economic Entomology 51, 37–39. Zeng, Y., Giblin-Davis, R.M., Ye, W., Bélair., G., Boivin, G. and Thomas, W.K. (2007) Bradynema listronoti n. sp. (Nematoda: Allantonematidae), a parasite of the carrot weevil Listronotus oregonensis (Coleoptera: Curculionidae) in Quebec, Canada. Nematology 9, 609–623. Zhao, D.X., Boivin, G. and Stewart, R.K. (1990) Consumption of carrot weevil, Listronotus oregonensis, (Coleoptera: Curculionidae) by four species of carabids on host plants in the laboratory. Entomophaga 35, 57–60. Chapter 31 221

31 Lygus lineolaris (Palisot), Tarnished Plant Bug (Hemiptera: Miridae)

A. Bruce Broadbent,1 Tim Haye,2 Tara Gariepy,1 Owen Olfert3 and Ulrich Kuhlmann2 1Agriculture and Agri-Food Canada, London, Ontario; 2CABI Europe- Switzerland, Delémont, Switzerland; 3Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

31.1 Pest Status and seeds to collapse (Butts and Lamb, 1990). All Lygus spp. overwinter as adults The tarnished plant bug, Lygus lineolaris in refuges such as shelterbelts, which (Palisot de Beauvois) (Hemiptera: Miridae), provide maximum winter protection is the most widespread of the 29 Nearctic (Cleveland, 1982; Craig and Loan, 1987; species of native Lygus spp. (Schwartz and Gerber and Wise, 1995; Schwartz and Foottit, 1998). It is polyphagous (Young, Foottit, 1998). When they become active in 1986) and damages vegetables, fruits, green- spring they move to the fi rst plants in house crops, canola, Brassica napus L. and fl ower, generally weeds and volunteer crop B. rapa L. (Brassicaceae) and legume plants, e.g. canola, where the females lay crops, primarily those grown for seed, e.g. eggs. The fi rst generation develops on these lucerne, Medicago sativa L. (Fabaceae) plant hosts and new adults disperse to the (Broadbent et al., 2002a). Other pest Lygus next group of fl owering plants, which species, abundant in agricultural crops in includes many agricultural crops. Depend- western Canada, include L. borealis ing on climatic zone, from one to fi ve (Kelton), L. elisus (Van Duzee), L. hesperus generations of Lygus spp. occur in Canada Knight, L. keltoni Schwartz and L. shulli (Craig and Loan, 1987; Gerber and Wise, Knight (Hemiptera: Miridae) (Schwartz and 1995; Schwartz and Foottit, 1998). Foottit, 1998; Braun et al., 2001; Cárcamo et al., 2002, 2003). Economic loss data for Lygus spp. in Canadian cropping systems 31.2 Background are limited (Broadbent et al., 2002a). Adults and immatures feed by piercing Cultural practices, e.g. crop rotation and the plant tissues, secreting digestive weed management, do not successfully enzymes and pumping out the liquefi ed control Lygus spp. The harvest of lucerne plant material (Tingey and Pillemer, 1977). reduces available host stages of Lygus for Feeding damage on various crops is parasitism and subsequent levels of para- described in Broadbent et al. (2002a), but sitism but does not cause elimination of typically feeding injury consists of lesions parasitoid populations (Mason et al., on the surfaces of stems, buds, fl owers and 2011b). Control has been primarily by pods that cause buds and fl owers to abscise chemical insecticides but there are few

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 222 Chapter 31

registered for use against Lygus spp. in since then it has spread west into Ontario Canada. Toxicity of these insecticides to and east toward the Maritime Provinces pollinating insects is a concern, particu- (Haye et al., 2012). larly since spraying is often done during maximum pollination periods. Concerns about non-target safety of insecticides to 31.3 Biological Control Agents humans and benefi cial insects also make biological control an important alternative A review of the Nearctic species of management strategy. In greenhouses, bio- Leiophron and Peristenus that parasitize logical control programmes are well Lygus spp. described 16 species, including developed for other pests and use of eight new species (Goulet and Mason, insecticides for control of Lygus would kill 2006). This has greatly improved the natural enemies, disrupting these pro- baseline data for native species of Lygus grammes (Gillespie et al., 2000). Lygus spp. parasitoids in Canada. Three agricultural are susceptible to certain pathogens, regions, primarily lucerne, in southern including Beauveria bassiana (Balsamo) Ontario (London, Niagara and Guelph) Vuillemin (Cordycipitaceae) (Bidochka et were sampled weekly from May to al., 1993). Formulations of this fungus have September for L. lineolaris and their para- been tried against L. lineolaris in cotton, sitoids in 1998, 1999 and 2000 (Broadbent Gossypium herbaceum L. (Malvaceae), et al., 2006). Overall rates of parasitism fi elds in the southern USA with some (determined from dissections) by native success, especially if combined with the parasitoids were consistent from year to insecticide imidacloprid (Steinkraus and year and the averages of the three regions Tugwell, 1997). Beauveria bassiana has in each growing season were below 11%. also been tested against Lygus in green- Both nymphs and adults of L. lineolaris houses with moderate success (Al- were parasitized, with the highly mobile mazra’awi et al., 2005; Ugine, 2011). adults being a potential means of dis- Several native parasitoids attack eggs, persing the parasitoids. In general, L. nymphs and adults of Lygus spp. (Broad- lineolaris in weedy fi elds were more highly bent et al., 2002a; Goulet and Mason, parasitized than those in fi elds of weed- 2006). At least four egg parasitoids are free lucerne. Six species of native braconid known (Al-Ghamdi et al., 1995) and one, parasitoids were collected from L. lineo- Anaphes iole Girault (Hymenoptera: laris in southern Ontario (in decreasing Mymaridae), is commercially available for order of abundance): Peristenus pallipes Lygus control in the USA. In Canada, (Curtis), P. pseudopallipes (Loan), Leio- univoltine Peristenus spp. and multi- phron lygivorus (Loan), L. solidaginis Loan, voltine Leiophron spp. (Hymenoptera: L. uniformis (Gahan), and Leiophron sp. Braconidae) are considered to be relatively near brevipetiolatus Loan (Hymenoptera: ineffective, with low fi eld parasitism of Braconidae). The large populations of L. Lygus spp. (Broadbent et al., 2006). In lineolaris and the low baseline parasitism Europe, several Peristenus spp. have in southern Ontario, particularly of second signifi cant impact on Lygus spp. (Bilewicz- generation L. lineolaris, have supported the Pawinska, 1982). One of these, Peristenus need for introduction of a multivoltine digoneutis Loan, was released in the early European parasitoid species in this region 1980s in New Jersey and has successfully (Broadbent et al., 2006). Data from 1991– established in the north-eastern USA on L. 1992 have been compiled as baseline lineolaris (Day et al., 1990, 1992, 1998), parasitism data for the native Peristenus resulting in decreased Lygus densities on species in south-western Quebec agri- lucerne (Day, 1996) and strawberries (Day culture prior to the establishment of P. and Hoelmer, 2012). Broadbent et al. (1999) digoneutis (Carignan et al., 2007). confi rmed the fi rst presence of P. Comparison of the suitability of two digoneutis in southern Quebec in 1998 and European species, P. digoneutis and Chapter 31 223

P. relictus (Ruthe) (= P. stygicus Loan) assumed that no introduced parasitoid (Hymenoptera: Braconidae), for the control species established there. In 2005 at of Lygus spp. suggested that P. relictus was Saskatoon, P. digoneutis and Lygus the more effective biological control agent nymphs were placed together in fi eld cages for L. lineolaris, when only fecundity was that were left out through the winter. In considered (Haye, 2004; Haye et al., May 2006, sticky traps were placed in 2005a). A study of P. digoneutis and P. these fi eld cages and monitored weekly for relictus was conducted to determine their emergence of any P. digoneutis adults but potential host ranges in North America no wasps were recovered (L. Braun, (Mason et al., 2011a). No-choice laboratory Saskatoon, 2012, unpublished results). tests suggested that native Lygus spp. were Successful establishment of P. digo- equally likely to be hosts of both neutis occurred in the north-eastern USA parasitoids (Mason et al., 2011a). Other in the 1980s (Day et al., 1990) and this non-target Miridae were not suitable hosts species subsequently spread into Canada for P. digoneutis but Amblytylus nasutus via southern Quebec in the 1990s (Broad- (Kirschbaum), Leptopterna dolabrata (L.) bent et al., 1999). In 2005 P. digoneutis was and Melanotrichus coagulatus (Uhler) recovered in the Niagara region (Gariepy et (Hemiptera: Miridae) may be suitable for al., 2008a) and between 2000 and 2005 this development of P. relictus. Comparison species was released and established in the with fi eld data in North America and London area (Broadbent et al., 2002b; B. studies in Europe (Haye et al., 2005b) Broadbent, 2012, unpublished results). suggests that non-target Lygus spp. may be Large releases (approx. 14,300 individuals impacted by P. digoneutis whereas other over 3 years, 2006–2008) in Ontario straw- non-target species would not. In contrast, berry, Fragaria × ananassa Duschesne ex the non-target Lygus spp. and at least Rozier (Rosaceae), fi elds were possible due several other non-target mirid species are to the mass rearing procedure for P. likely to be impacted by P. relictus (Haye et digoneutis developed in London (Whistle- al., 2006). Potential impact on non-target craft et al., 2010). In 2007, P. digoneutis Lygus spp. would be greatest in the was recovered in strawberry production Western North American bioregion where areas around Simcoe and subsequently 17 species occur west of the Mississippi released on specifi c strawberry farms in River and some of these endemic species Simcoe and Centreville (Table 31.1; are restricted to one or a few breeding host Broadbent et al., 2009). In 2010 P. plants in a limited geographic and digoneutus was recovered at New Liskeard, ecological range; whereas in the Eastern Ontario (47.5°, −79.7°) from lucerne grown North American bioregion where the Lygus close to the southern limit of the boreal fauna consists of fewer, mainly widespread forest. There have been no recoveries of P. species, impacts on non-target Lygus spp. digoneutis as yet from limited L. lineolaris are expected to be minimal (Mason et al., nymph collections from south-western 2011a). After reviewing data from these Ontario, west of Talbotville (B. Broadbent, non-target studies in Europe and laboratory 2012, unpublished results), but its range is tests in Canada, it was decided to release expected to extend that far and beyond Peristenus digoneutis and not P. relictus in (Haye et al., 2012). eastern Canada and speed up the dispersal of the former species, which is presently invading into Canada from releases in the 31.4 Evaluation of Biological Control USA. Releases of Peristenus spp. against Lygus A bioclimatic model (CLIMEX®) for P. spp. between 1981 and 1999 are listed in digoneutis in North America was Broadbent et al. (2002a). From the fi eld developed, based on climate and ecological releases in the Saskatoon region, no parameters, and validated with actual recoveries were ever reported and so it is distribution records (Haye et al., 2013). 224 Chapter 31

Table 31.1. Field releases of Peristenus digoneutis (estimated numbers) into Canada against Lygus lineolaris 2000–2008. Year Site GPS coordinates Number and stage 2001 London, ON 43.0295°, −81.2055° 6800 adults 2002 London, ON 43.0295°, −81.2055° 2575 adults 2003 London, ON 43.0295°, −81.2055° 3000 adults 2004 London, ON 43.0295°, −81.2055° 9400 parasitized nymphs 2005 London, ON 43.0295°, −81.2055° 2890 parasitized nymphs 2006 Simcoe, ON (2 sites) 42.9828°, −80.3808° 6115 parasitized nymphs Talbotville, ON 42.8357°, −81.2715° 1925 parasitized nymphs 2007 Simcoe, ON (2 sites) 42.9834°, −80.3728° 1000 adult females Centreville, ON 44.4186°, −76.9139° 200 adult females 2008 Simcoe, ON (2 sites) 42.9834°, −80.3728° 2730 adult females Centreville, ON 44.4186°, −76.9139° 2300 adult females

The current distribution of P. digoneutis in Broadbent, 2012, unpublished results) and eastern North America (Fig. 31.1) matched Quebec (Goulet and Mason, 2006), many the predicted distribution well. The model years of post-release monitoring are suggests that P. digoneutis will probably required before a correlation with P. digo- continue its spread westwards throughout neutis establishment can be proven. the USA along the Great Lakes. Its southern distribution will likely be limited by hot summer temperatures whereas its northern 31.5 Future Needs range is limited by the number of generations of the Lygus spp. hosts rather Future work should include: than cold stress. Peristenus digoneutis has 1. Continued post-release monitoring of P. the potential to occur in the southern parts digoneutis dispersal and assessment of of the prairie ecozone of western Canada; impact on L. lineolaris populations in however, ecoclimatic index values in the southern Ontario crop systems, particularly prairies indicate mainly marginal or in non-sprayed lucerne fi elds; unfavourable conditions, which may 2. Monitoring of parasitism of non-target explain why earlier releases of P. Lygus spp. and other mirid species in crop digoneutis in western Canada have failed and non-crop habitats to validate host- (Haye et al., 2013). range predictions; Better tools have become available for 3. Development of habitat management confi rming the identifi cation of Peristenus practices that enhance parasitism levels in spp., especially in the larval stage, using non-crop and crop habitats. PCR analysis (Tilmon et al., 2000; Erlandson et al., 2003; Ashfaq et al., 2004; Gariepy et al., 2005). However, beyond agent identifi cation, molecular diagnostics Acknowledgements can facilitate and expedite pre- and post- release studies on the ecological host range L. Braun, J. Soroka, P. Mason, H. Goulet of parasitoids, potential non-target effects, and D. Gillespie provided useful insight host–parasitoid associations and trophic and information for this chapter. We also interactions (Gariepy et al., 2008b). express sincere appreciation to Lola Although lower populations of L. Gualtieri, who retired in 2011, for her lineolaris are being noted in Ontario (B. assistance in this project. Chapter 31 225

Kilometres

Fig. 31.1. Distribution of Peristenus digoneutis in eastern North America. Triangles indicate confi rmed occurrences and dark shading indicates the optimal region for parasitoid establishment according to the CLIMEX analysis (Haye et al., 2013).

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Gariepy, T., Kuhlmann, U., Gillott, C. and Erlandson, M. (2008b) A large-scale comparison of conventional and molecular methods for the evaluation of host-parasitoid associations in non- target risk-assessment studies. Journal of Applied Ecology 45, 708–715. Gerber, G.H. and Wise, I.L. (1995) Seasonal occurrence and number of generations of Lygus lineolaris and L. borealis (Heteroptera: Miridae) in southern Manitoba. The Canadian Entomologist 127, 543–559. Gillespie, D., Foottit, R. and Shipp, J.L. (2000) Management of Lygus bugs on protected crops. In: Foottit, R. and Mason, P. (eds) Proceedings of the Lygus Working Group Meeting, 26 September 1999, Saskatoon, Saskatchewan. Agriculture and Agri-Food Canada, Research Branch, Ottawa, Ontario, pp. 1–8. Goulet, H. and Mason, P.G. (2006) Review of the Nearctic species of Leiophron and Peristenus (Hymenoptera: Braconidae: Euphorinae) parasitizing Lygus (Hemiptera: Miridae: Mirini). Zootaxa 1323, 3–118. Haye, T. (2004) Studies on the ecology of European Peristenus spp. (Hymenoptera: Braconidae) and their potential for the biological control of Lygus spp. (Hemiptera: Miridae) in Canada. PhD thesis, Christian-Albrechts-University, Kiel, Germany, 171pp. Haye, T., Broadbent, A.B., Whistlecraft, J. and Kulhmann, U. (2005a) Comparative analysis of the reproductive biology of two Peristenus species (Hymenoptera: Braconidae), biological control agents of Lygus plant bugs (Hemiptera: Miridae). Biological Control 32, 442–449. Haye, T., Goulet, H., Mason, P.G. and Kuhlmann, U. (2005b) Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biological Control 35, 55–67. Haye, T., Kuhlmann, U., Goulet, H. and Mason, P.G. (2006) Controlling Lygus plant bugs (Heteroptera: Miridae) with European Peristenus relictus (Hymenoptera: Braconidae) in Canada – Risky or not? Bulletin of Entomological Research 96, 187–196. Haye, T., Olfert, O., Weiss, R., Gariepy, T., Broadbent, B. and Kuhlmann, U. (2013) Bioclimatic analyses of distributions of a parasitoid, Peristenus digoneutis (Hymenoptera: Braconidae), and its host species, Lygus spp. (Hemiptera: Miridae). Agricultural and Forest Entomology 15, 43–55. Mason, P., Broadbent, A.B., Whistlecraft, J.W. and Gillespie, D.R. (2011a) Interpreting host range: a case study of Peristenus digoneutis and P. relictus (Hymenoptera: Braconidae) for biological control of Lygus spp. (Hemiptera: Miridae) in North America. Biological Control 57, 94–102. Mason, P.G., Goulet, H. and Bostanian, N. (2011b) Effect of harvest on Euphorine (Hymenoptera: Braconidae) parasitism of Lygus lineolaris and Adelphocoris lineolatus (Hemiptera: Miridae) in alfalfa. Journal of the Entomological Society of Ontario, 142, 3–10. Schwartz, M.D. and Foottit, R.G. (1998) Revision of the Nearctic Species of the Genus Lygus Hahn, with a Review of the Palaearctic Species (Heteroptera: Miridae). Associated Publishers, Gainesville, Florida. Steinkraus, D.C. and Tugwell, N.P. (1997) Beauveria bassiana (Deuteromycotina: Moniliales) effects on Lygus lineolaris (Hemiptera: Miridae). Journal of Entomological Science 32, 79–90. Tilmon, K.J., Danforth, B.N., Day, W.H. and Hoffmann, M.P. (2000) Determining parasitoid species composition in a host population: a molecular approach. Annals of the Entomological Society of America 93, 640–647. Tingey, W.M. and Pillemer, E.A. (1977) Lygus bugs: crop resistance and physiological nature of feeding injury. Entomological Society of America Bulletin 23, 277–287. Ugine, T.A. (2011) The effect of temperature and exposure to Beauveria bassiana on tarnished plant bug Lygus lineolaris (Heteroptera: Miridae) population dynamics, and the broader implications of treating insects with entomopathogenic fungi over a range of temperatures. Biological Control 59, 373–383. Whistlecraft, J.W., Haye, T., Kuhlmann, U., Muth, R., Murillo, H. and Mason, P. (2010) A large-scale rearing method for Peristenus digoneutis (Hymenoptera: Braconidae), a biological control agent of Lygus lineolaris (Hemiptera: Miridae). Biocontrol Science and Technology 20, 923–937. Young, O.P. (1986) Host plants of the tarnished plant bug, Lygus lineolaris (Heteroptera: Miridae). Annals of the Entomological Society of America 79, 747–762. 228 Chapter 32

32 Mamestra confi gurata Walker, Bertha Armyworm (Lepidoptera: Noctuidae)

Martin A. Erlandson Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

32.1 Project Status baculovirus and entomopathogenic fungi are often associated with massive collapses The bertha armyworm, Mamestra con- of late instar M. confi gurata larval popu- fi gurata Walker (Lepidoptera: Noctudidae), lations and it is speculated that these is one of the major insect pests of canola, diseases are major mortality factors that Brassica napus L. and B. rapa L. (Bras- dampen M. confi gurata outbreak cycles sicaceae) in western Canada (Mason et al., (Mason et al., 1998). In addition, native 1998). Mamestra confi gurata is a poly- parasitoids appear to contribute to the phagous insect, feeding on a wide range of regulation of M. confi gurata populations plant species. Its major economic impact is (Mason et al., 2002b). on canola, in which larvae feed on foliage Attempts at biological control of M. and developing seedpods causing sub- confi gurata and basic and applied research stantial decreases in seed yield and on potential biological control agents in negatively affecting seed quality. Across Canada were reviewed previously (Mason western Canada, M. confi gurata popu- et al., 2002b). The previous review covered lations appear to be cyclic, with major the following aspects of biological control: regional outbreaks occurring every 6–8 (i) the native parasitoids that attack M. years and lasting up to 3 years (Mason et confi gurata larvae, including Banchus al., 1998). The scale of insecticide spray fl avescens Cresson (Hymenoptera: Ichneu- application can be signifi cant when M. monidae) and Athrycia cinerera (Coquil- confi gurata outbreaks occur. In the most lette) (Diptera: Tachnidae), or that attack recent outbreaks (1994–1996 and 2005– M. confi gurata eggs, such as Trichogramma 2007), between 600,000 and 800,000 ha of inyoense Pinto and Oatman (Hymenoptera: canola were sprayed annually at a cost of Trichogrammatidae); (ii) studies on the approximately CAN$16.5m. Estimated biology and classical biological control yield losses ranged from CAN$10m to releases of the European parasitoids CAN$40m annually despite these control Microplitis mediator Haliday (Hymen- efforts. Currently, M. confi gurata popu- optera: Braconidae) and Ernestia conso- lations are increasing across the Prairie brina (Meigen) (Diptera: Tachnidae); (iii) Provinces and another outbreak is likely in the effi cacy of strains of Bacillus the next several years. thuringiensis Berliner (Bt) (Bacillaceae) for The factors that drive the outbreak M. confi gurata larval control; and (iv) cycles of M. confi gurata populations are biological characterization of the Alpha- not completely understood, but a few baculovirus species, Mamestra confi gurata factors have been implicated. Epizootics of nucleopolyhedrovirus (Baculo viridae), and

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 32 229

its potential effi cacy for control of M. fi gurata larvae in feeding bioassays confi gurata larval outbreaks. In the current (Erlandson et al., 2002). While this in vitro review, progress on these projects will be assay system can potentially streamline the updated. screening of newly identifi ed or previously Limited new research has been under- untested Bt toxins, the current focus on taken on the M. confi gurata parasitoid implementing Bt toxin deployment in complex (e.g. Mason et al., 2001). However, genetically modifi ed crop plants has had two M. confi gurata parasitoids, T. inyoense an impact on industry interest in develop- and M. mediator, were used as model ing Bt products for spray applications in species to examine the potential impact on large fi eld crop agriculture. Thus screening benefi cial non-target species from appli- for Bt toxins active against M. confi gurata cation of Spinosad (Mason et al., 2002a). larvae has not been extended beyond the Spinosad belongs to a class of insecticides panel of 16 toxins screened in the initial developed from secondary metabolites of study (Erlandson et al., 2002). an actinomycete bacterium and it is con- Substantial progress has been made in sidered to have a lower impact on bene- the characterization of the baculoviruses fi cial insect species than other synthetic associated with M. confi gurata popu- pesticides. Laboratory experiments showed lations. The Baculoviridae are rod-shaped measureable impacts on these parasitoids viruses with large circular, covalently- in both their adult and larval stages. closed, double-stranded DNA genomes of Although there is no evidence that M. between 80–180 kb pairs. The rod-shaped mediator has become established in virions of baculoviruses are characteristic- western Canada and the prevalence and ally occluded into a crystalline protein impact of T. inyoense is unclear (Mason et matrix or occlusion body. Baculoviruses al., 2002b), the results of this study indicate are infectious only to insects and have that incorporating even putatively selective demonstrated potential as biopesticides or insecticides into an integrated pest biological control agents for insect pest management programme for M. confi gurata management in agriculture and forestry control should consider potential negative (Erlandson, 2008). Previously, a number of impacts on egg and larval parasitoids. baculoviruses from the genus Alphabaculo- As outlined in a previous review, virus (Baculoviridae) (formerly referred to commercial formulations of B. thuringi- as Nucleopolyhedrovirus (NPV) exclusively ensis Berliner serovar. kurstaki (Btk) are infecting lepidopteran hosts) were identi- not highly effective against M. confi gurata fi ed from M. confi gurata larval popu- larvae (Mason et al., 2002b). In an attempt lations. These virus isolates could be to develop a more effi cient screening distinguished based on restriction endo- method to identify potentially useful B. nuclease analysis of purifi ed genomic DNA thuringiensis toxins, an in vitro midgut and their infectivity for M. confi gurata epithelial cell model, originally developed larvae (Erlandson, 1990). The physical map in Trichoplusia ni (Hübner) (Lepidoptera: of the genome and the DNA sequence of Noctuidae) (Braun and Keddie, 1997), was several key genes were determined for one adapted for use with M. confi gurata of these isolates (Li et al., 1997). Advances (Erlandson et al., 2002). In these assays, in high throughput DNA sequencing whole-mounts of isolated M. confi gurata techniques have allowed for cost effective midgut epithelium tissue were incubated sequencing of virus genomes, which in with purifi ed Bt b-endotoxins and a turn has led to a more complete under- fl uorochrome dye, which only enters standing of baculovirus biology and their midgut cells if the Bt b-endotoxins interact potential pathogenicity for host insects. with and alter the permeability of cell The complete genome sequence of three membranes. This assay was successful in geographic strains of alphabaculoviruses identifying Bt b-endotoxins that also that were isolated from infected M. demonstrated activity against M. con- confi gurata larvae have been published (Li, 230 Chapter 32

Q. et al., 2002; Li, L. et al., 2002, 2005). A unique restriction endonuclease profi le major fi nding from the genetic character- and its lower infectivity and virulence for ization of these viruses was that two M. confi gurata larvae compared to the fi rst distinct species of alphabaculoviruses are strain characterized and sequenced, found in M. confi gurata, and these have MacoNPV-A v90/2. Analysis of the been designated as Mamestra confi gurata genomic sequence of the MacoNPV-A nucleopolyhedrovirus-A (MacoNPV-A) (Li, v90/4 isolate revealed that, although it was Q. et al., 2002) and Mamestra confi gurata highly similar to the sequence of the nucleopolyhedrovirus-B (MacoNPV-B) MacoNPV-A v90/2 isolate, it did contain (Baculo viridae) (Li, L. et al., 2002). The numerous (>500) single nucleotide changes MacoNPV-A and MacoNPV-B viruses are as well as insertions and deletions that closely related to each other based on their change the amino acid sequence of more virtually identical gene order within their than 25 virus proteins (Li, L. et al., 2005). genomes and an average 87% identity at The precise genetic difference(s) that the nucleotide level for the common genes account for the differences in infectivity shared by both viruses. However, each and virulence of MacoNPV-A v90/2 versus virus has a subset of nine to ten unique v90/4 has not yet been identifi ed. A series genes not found in the other virus (Li, L. et of 15 additional single-infected-larva al., 2002). The two viruses can also be MacoNPV-A samples isolated from M. con- distinguished on the basis of major fi gurata populations from across western differences in the restriction endonuclease Canada are being characterized and fragment profi le for each. Restriction sequenced to gain a better understanding of endonuclease fragment pattern analysis of the genetic diversity within populations of a large number of single-infected-larva this virus (M. Erlandson, 2012, unpub- samples from M. confi gurata populations lished results). Signifi cantly, these isolates from across western Canada indicates that show moderate differences in virulence for MacoNPV-A is much more prevalent than M. confi gurata larvae and extensive MacoNPV-B. Interestingly, MacoNPV-B genome sequence variation. These results appears to be somewhat less virulent than indicate that natural baculovirus popu- MacoNPV-A for M. confi gurata larvae but it lations, such as those of MacoNPV-A, has a substantially wider host range and represent a spectrum of genotypes that may infects a number of noctuid species that are allow for the survival and adaptation of important pests of agricultural crops (Li, L. these viruses in response to potentially et al., 2002). The wider host range of dynamic changes in host subpopulations MacoNPV-B suggests that it has potential across their geographic range and changing for development as a bioinsecticide for climatic conditions. control of a number of important noctuid The availability of the complete genome pests in a variety of crops. Interestingly, sequence of MacoNPV-A and MacoNPV-B MacoNPV-B is closely related to an NPV viruses has allowed the identifi cation of that was previously isolated from Mamestra virus gene products that are likely to play a brassicae L. (Lepidoptera: Noctuidae) in role in the virulence and host range Europe and was developed as a biological determination of these viruses. We have control agent under the trade name focused primarily on viral proteins that Mamestrin (Erlandson, 2008). play a role in the initial infection of the Geographic variants are common among host midgut epithelium as a fi rst step in baculovirus species and these variants are oral infection. One of the genes present in often genotypically distinct and display both MacoNPV-A and MacoNPV-B encodes differential infectivity and virulence for a metalloprotease referred to as ‘virulence their host. This is the case for MacoNPV-A enhancing factor’ or ‘enhancin’ and which where an additional geographic isolate, plays a role in increasing the effi ciency of MacoNPV-A v90/4, was characterized as oral infection (Li, Q. et al., 2003). It has being a distinct genotype based on its been proposed that enhancin increases Chapter 32 231 baculovirus infectivity by degrading the (Peng et al., 2012). Thus it is possible that peritrophic matrix (PM) within the host MacoNPV pif proteins are unable to midgut thus allowing the more effi cient interact with other AcMNPV pif proteins to passage of virions through the PM to the form a viable pif complex. It is likely that midgut epithelial cells. Indeed, we were the pif complex on the envelope of able to demonstrate that MacoNPV-A baculovirus virions interact with and bind enhancin specifi cally degrades insect to specifi c proteins on host insect midgut intestinal mucin proteins, which are epithelial cell membranes allowing the integral components of the M. confi gurata virus to enter and infect host midgut cells. PM thus allowing increased access of Studies aimed at identifying baculovirus MacoNPV virions to midgut cells (Toprak genes that play a role in infectivity and et al., 2012). Further, by utilizing DNA virulence have expanded our under- recombinant techniques the MacoNPV-A standing of the pathogenesis process in enhancin gene was transferred to and host insect guts. A thorough understanding expressed in the Autographa californica of baculovirus pathogenesis and infection multiple nucelopolyhedrovirus (AcMNPV) dynamics will aid in the development of genome and the recombinant virus was these viruses as microbial pesticides and referred to as AcMNPV-en. The AcMNPV allow for their rational deployment in virus does not contain an enhancin gene integrated pest management systems. and oral bio assays demonstrated that AcMNPV-en was approximately fi ve times more infectious for T. n i larvae than was the wild-type AcMNPV virus (Li, Q. et al., 32.2 Future Needs 2003). In addition, through the development of an AcMNPV bacmid Future work should include: system in which individual genes can be deleted or replaced we have begun to 1. Exploration of the potential of investigate the function of a number of core MacoNPV-B for use as a biopesticide for genes found in all baculoviruses. Using management of other noctuid pest species this approach we have been able to identify in high value crop systems as its potential several genes that are essential for oral application in additional insect pest com- infectivity of NPVs and that are referred to plex/crop systems would make it a more as per os infectivity ( pif) genes (Fang et al., economically attractive option for develop- 2009; Nei et al., 2012; Peng et al., 2012). In ment as a biopesticide; all cases the MacoNPV pif gene 2. Identifi cation and characterization of homologues could not functionally replace the Entomophothorales fungal pathogens any of the AcMNPV pif genes at least with that continue to produce signifi cant epizo- respect to restoring the oral infectivity of a otics in late instar populations of M. confi g- recombinant virus, which suggests these urata larval infestations in canola crops, genes may also play a role in host particularly in warm, moist summers. In specifi city determination. However, these light of changing climactic conditions results need to be interpreted in light of the identifi cation and characterization of this fi nding that at least six pif gene products pathogen would produce a more robust interact with each other to form a complex estimate of its impact as a natural regula- on the envelope of baculovirus virions tory agent of M. confi gurata populations. 232 Chapter 32

References

Braun, L. and Keddie, B.A. (1997) A new tissue technique for evaluating effects of Bacillus thuringiensis toxins on insect midgut epithelium. Journal of Invertebrate Pathology 69, 92–104. Erlandson, M.A. (1990) Biological and biochemical comparison of Mamestra confi gurata and Mamestra brassicae nuclear polyhedrosis virus isolates pathogenic for the bertha armyworm, Mamestra confi gurata (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 56, 47–56. Erlandson, M.A. (2008) Insect pest control by viruses. In: Mahy, B.W.J. and Van Regenmortel, M.H.V. (eds) Encyclopedia of Virology, Vol 3. Elsevier, Oxford, UK, pp. 125–133. Erlandson, M.A., Braun, L. and Bradfi sch, G. (2002) Screening Bacillus thuringiensis b-endotoxins for activity against the bertha armyworm, Mamestra confi gurata (Lepidoptera: Noctuidae). Journal of Invertebrate Pathology 80, 191–193. Fang, M., Yie, Y., Harris, S., Erlandson, M.A. and Theilmann, D.A. (2009) Autographa californica multiple nucleopolyhedrovirus core gene ac96 encodes a per os infectivity factor (pif-4). Journal of Virology 83, 12569–12578. Li, L., Donly, C., Li, Q., Willis, L., Erlandson, M.A. and Theilmann, D.A. (2002) Identifi cation and genomic analysis of a second species of nucleopolyhedrovirus isolated from Mamestra confi gurata. Virology 297, 226–244. Li, L., Li, Q., Willis, L.G., Erlandson, M.A., Theilmann, D.A. and Donly, C. (2005) Complete comparative genomic analysis of two fi eld isolates of Mamestra confi gurata nucleo- polyhedrovirus-A. Journal of General Virology 86, 91–105. Li, Q., Donly, C., Li, L., Willis, L., Theilmann, D.A. and Erlandson, M.A. (2002) Sequence and organization of the Mamestra confi gurata nucleopolyhedrovirus genome. Virology 294, 106–121. Li, Q., Li, L., Moore, K., Donly, C., Theilmann, D.A. and Erlandson, M.A. (2003) Characterization of Mamestra confi gurata nucleopolyhedrovirus enhancin and its functional analysis in an AcMNPV recombinant. Journal of General Virology 84, 123–132. Li, S., Erlandson, M.A., Moody, D. and Gillott, C. (1997) Physical map of Mamestra confi gurata nucleopolyhedrovirus (MacoNPV) genome and sequence analysis of the polyhedrin gene. Journal of General Virology 78, 265–271. Mason, P.G., Arthur, A.P., Olfert, O.O. and Erlandson, M.A. (1998) The bertha armyworm (Mamestra confi gurata) (Lepidoptera: Noctuidae) in Western Canada. The Canadian Entomologist 130, 321– 336. Mason, P.G., Erlandson, M.A. and Youngs, B.J. (2001) Effects of parasitism by Banchus fl avescens (Hymenoptera: Ichneumonidae) and Microplitis mediator (Hymenoptera: Braconidae) on the bertha armyworm, Mamestra confi gurata (Lepidoptera: Noctuidae). Journal of Hymenoptera Research 10, 81–90. Mason, P.G., Erlandson, M.A., Elliott, R.H. and Harris, B.J. (2002a) Potential impact of spinosad on parasitoids of Mamestra confi gurata (Lepidoptera: Noctuidae). The Canadian Entomologist 134, 59–68. Mason, P.M., Turnock, W.J., Erlandson, M.A., Kuhlmann, U. and Braun, L. (2002b) Mamestra confi gurata Walker, Bertha Armyworm (Lepidoptera: Noctuidae). In: Mason, P.G. and Huber, J. (eds) Biological Control Programmes Against Insects and Weeds in Canada, 1980–2000. CAB International, Wallingford, UK, pp. 169–176. Nie, Y., Fang, M., Erlandson, M.A. and Theilmann, D.A. (2012) Analysis of the AcMNPV overlapping gene pair lef3 and ac68 reveals that AC68 is a per os infectivity factor (PIF6) and LEF3 is critical, but not essential for virus replication. Journal of Virology 86, 3985–3994. Peng, K., van Lent, J., Boeren, S., Fang, M., Theilmann, D.A., Erlandson, M.A., Vlak, J. and van Oers, M. (2012) Characterization of novel components of the baculovirus per os infectivity factor (PIF) complex. Journal of Virology 86, 4981–4988. Toprak, U., Harris, S., Baldwin, D., Hegedus, D.D., Theilmann, D.A. and Erlandson, M.A. (2012) The role of enhancin in Mamestra confi gurata nucleopolyhedrovirus virulence: selective degradation of host peritrophic matrix proteins. Journal of General Virology 93, 744–753. Chapter 33 233

33 Oulema melanopus (L.), Cereal Leaf Beetle (Coleoptera: Chrysomelidae)

Swaroop V. Kher,1 Lloyd M. Dosdall1 and Héctor Cárcamo2 1University of Alberta, Edmonton, Alberta; 2Agriculture and Agri-Food Canada, Lethbridge, Alberta

33.1 Pest Status No serious crop losses have yet been attributed to O. melanopus in Alberta, The cereal leaf beetle, Oulema melanopus Saskatchewan, or Manitoba. However, (L.) (Coleoptera: Chrysomelidae), has been given the potential of the pest to invade established in eastern Canada since 1970. and establish and considering the current A detailed account of its control using its rate of spread by O. melanopus, appro- principal natural enemy Tetrastichus julis priate crop protection measures may be (Walker) (Hymenoptera: Eulophidae) was necessary. Oulema melanopus was presented by Harcourt et al. (1984). The recorded in Edmonton in a triticale, × beetle was fi rst discovered in western Triticosecale Wittmack ex A. Camas Canada in the Creston Valley, British (Poaceae), fi eld in May 2011 (S. Kher, Columbia in 1998 (CFIA, 1999), and 2012, unpublished results), and this was recently it expanded its range to likely an accidental, human-assisted intro- encompass southern Alberta (2005), south- duction. The potential economic impact of western Saskatchewan (2008), Manitoba the pest has been assessed as ‘medium’ (2009) (Dosdall et al., 2011) and near (25–50% losses in the absence of control Edmonton in north central Alberta (2011) measures) and the restrictions on the (Western Committee on Crop Pests, 2011). domestic movement of cereal hay and Surveys to monitor O. melanopus popu- straw have been removed due to the low lations in recently invaded provinces survivorship of O. melanopus in storage indicate an increase in its range and (CFIA, 2011). In eastern Canada, O. abundance since 2006 (Dosdall et al., melanopus is well established but its 2011). In Alberta, the beetle is currently populations are kept below pest levels by widespread throughout the southern part natural enemies (Ontario Ministry of of the province from Pincher Creek to Agriculture, Food and Rural Affairs, 2009). Medicine Hat and north to High River and Strathmore. Over the last 5 years, steady increases in the numbers of fi elds infested 33.2 Background and its population densities have been observed, particularly in winter wheat, Oulema melanopus is native to Eurasia Triticum aestivum L. (Poaceae), fi elds in and widespread in Europe. The beetle was the Municipal District of Taber. discovered in Michigan, USA in 1962

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 234 Chapter 33

(Dysart et al., 1973), and has since 6 days and occurs inside O. melanopus dispersed across the USA and southern cocoons. Adults of the fi rst generation Canada. Tactics for controlling O. emerge in early to mid-June, mate, and melanopus in North America include females disperse in search of O. melanopus biological control, quarantine, chemical larvae. Parasitoid adult activity thus control, cultural control and plant synchronizes with the peak period of fi rst- resistance (Webster et al., 1978). generation O. melanopus larval activity in Biological control using introduced the fi eld. Parasitized O. melanopus larvae natural enemies has been the most drop down to the soil and form earthen successful management strategy (Harcourt cocoons but die before reaching the pupal et al., 1984). Tetrastichus julis is a host- stage. Tetrastichus julis larvae developing specifi c, bivoltine, gregarious larval inside these dead O. melanopus larvae endoparasitoid of O. melanopus (Dysart et then burst out and pupate within their al., 1973; Haynes and Gage, 1981; Evans et host’s earthen cocoon as naked pupae. The al., 2006), and remains well established as total developmental time from parasit- a successful biological control agent in ization to adult emergence ranges from 20 North America due to its close life cycle to 25 days for T. julis, resulting in the synchronization with the host, gregarious emergence of second-generation parasitoid development, and capacity to track its host adults. The mated second-generation throughout its range (Haynes and Gage, females then parasitize available O. 1981). Other parasitoids introduced in melanopus larvae in the fi eld. Parasitized North America, but with limited establish- O. melanopus larvae of the second ment success, include the larval para- generation drop down to soil and form sitoids Diaparsis carinifer (Thomson) and earthen cocoons and the parasitoid larvae Lemophagus curtus Townes (Hymenoptera: developing inside these host larvae over- Ichneumonidae) and an egg parasitoid, winter inside O. melanopus earthen Anaphes fl avipes (Förster) (Hymenoptera: cocoons. Hence, pupation in second- Mymaridae) (Haynes and Gage, 1981; generation T. julis larvae occurs only upon LeSage et al., 2007). In eastern Canada, T. completing overwintering in the following julis dispersed naturally, established, and spring (Kher et al., 2011). As many as 16 T. reached parasitism levels in the range of julis larvae have been observed developing 14–95% (Harcourt et al., 1977). inside one cocoon; however, it is more common to have four to six parasitoids per host larva (S. Kher, 2012, unpublished 33.3 Biological Control Agents results). Levels of parasitism have increased In Alberta, T. julis was discovered in local steadily since 2007 in south-eastern larval populations of the pest (Dosdall et Alberta (Table 33.1). Greatest parasitism al., 2011) and no intentional releases were has occurred near Taber, Alberta. The required. The surveys conducted to moni- beetle is widely spread, with localized tor O. melanopus activity across southern high-density fi elds in southern regions of Alberta since 2006 indicated that T. julis Alberta. The current estimates of para- has been tracking and parasitizing O. sitism, although from small sample sizes, melanopus populations and its range suggest that T. julis is being consistently expansion is in synchrony with that of the recorded in the infested areas and its beetle (Kher et al., 2011). populations continue to increase over time. Tetrastichus julis is bivoltine in most Oulema melanopus was discovered in regions, including Alberta. The parasitoid west-central Manitoba in 2009 (Dosdall et overwinters as 5th instar larvae inside the al., 2011), but populations appeared not to cocoons of its host. Overwintering ends at be parasitized. Consequently, T. julis was the beginning of spring when T. julis larvae relocated to this region. Parasitized O. enter the pupal stage. Pupation lasts about melanopus larvae were collected from sites Chapter 33 235

Table 33.1. Parasitism of cereal leaf beetle, Oulema melanopus, larvae by Tetrastichus julis in western Canada (L.M. Dosdall and H.A. Cárcamo, 2012, unpublished results). % Parasitism Coordinates (decimal (number of O. melanopus Year Location degrees) examined) 2007 Creston Valley, BC 49.06°, −116.32° 62.2 (159) 2007 Lethbridge, AB 49.41°, −112.45° 9.4 (96) 2008 Lethbridge, AB 49.41°, −112.45° 17.8 (107) 2008 Pincher Creek, AB 49.49°, −113.95° 14.6 (41) 2008 Coaldale, AB 49.73°, −112.62° 26.3 (57) 2008 Bow Island, AB 49.87°, −111.38° 00.0 (37) 2009 Lethbridge, AB 49.41°, −112.45° 32.8 (232) 2009 Coaldale, AB 49.73°, −112.62° 35.6 (45) 2009 Burdett, AB 49.83°, −111.52° 07.9 (38) 2009 Taber, AB 49.79°, −112.14° 48.1 (77) 2009 Swan River, MB 52.06°, −101.12° 00.0 (28) 2010 Lethbridge, AB 49.41°, −112.45° 17.0 (100) 2010 Taber, AB 49.79°, −112.14° 48.3 (150) 2010 Bow Island, AB 49.87°, −111.38° 18.0 (75) 2010 Grassy Lake, AB 49.83°, −111.70° 12.0 (50) 2011 Swan River, MB 52.05°, −101.05° 22.0 (103)

in southern Alberta in 2009 and 2010 and Species considered at risk of attack by T. released in the Swan River region of julis were determined using the guidelines Manitoba. In 2009, relocation was per- proposed by Kuhlmann et al. (2006) and formed at 11 sites, and in 2010 parasitized Cappuccino et al. (2009). Species selected larvae were released at approximately 24 for testing in no-choice tests were those sites. No parasitoids were recovered in that occur in southern Alberta and are 2009. However, in 2011, adult T. julis were closely related taxonomically and in life recovered from approximately 22% of O. history to O. melanopus. The species melanopus larvae collected (n=103) from tested were scarlet lily leaf beetle, release sites (H. Cárcamo, 2012, unpub- Lilioceris lilii (Scopoli), twelve-spotted lished results, Table 33.1). This confi rms asparagus beetle, Crioceris duodecimpunc- that T. julis has established in the Swan tata (L.), Colorado potato beetle, River Valley, Manitoba. Leptinotarsa decemlineata (Say), Gastro- It appears that when T. julis was physa polygoni (L.), Galerucella calmari- initially released in the USA for biological ensis Duftschmidt and Cassida azurea control of O. melanopus, host specifi city Fabricius (Coleoptera: Chrysomelidae). The testing was not conducted, or at least this authors concluded that in all cases some O. testing was not reported in the scientifi c melanopus control larvae were parasitized literature. To address this gap in know- but none of the potential non-target hosts ledge, Hervet (2010) and Cárcamo (2012, were parasitized. In one assay, even unpublished results) conducted host range smearing the larvae of C. azurea with the tests with potential non-target beetles. faeces of O. melanopus did not result in 236 Chapter 33

parasitism. Therefore it appears that T. julis levels suggests it may keep this pest from is quite host-specifi c to O. melanopus in reaching injurious levels. western Canada and poses little threat to local biodiversity. 33.5 Future Needs The entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Cordy- In view of the potential of O. melanopus to cipita ceae) has been reported to infect O. establish in western Canada, further work melanopus larvae under natural con- should: ditions, causing lowered larval feeding and mortality (Paschke, 1965). It is reported 1. Continue to monitor the distribution, that single spore isolates of this fungus can abundance and ability of T. julis to track control beetle populations (Paschke, 1965). range expansions of O. melanopus; No specifi c studies have been conducted, 2. Focus on the dispersal characteristics of especially in western Canada, to test the O. melanopus and T. julis over space and effi cacy of B. bassiana against O. melan- time and with respect to host-plant nutri- opus. Current studies by Kher (2011–2012, tion and landscape diversity parameters to unpublished results) near Lethbridge quantify the ecological parameters that suggest that this fungus may have a role in make this system so successful and apply it the management of O. melanopus and may to others; have limited non-target effects on T. julis. 3. Assess the importance of other potential natural enemies such as predators and entomopathogenic fungi that have not been 33.4 Evaluation of Biological Control widely explored for managing O. melano- pus to diversify the biological control pro- The cereal leaf beetle is currently in its gramme; early establishment phase in western 4. Determine the effi cacy of B. bassiana as Canada. It can potentially affect the a biological control agent and the interac- viability of cereal production in this region tions between B. bassiana and T. julis and has economic implications for grain when parasitized larvae are sprayed with a trade and export. Classical biological fungal formulation to determine the com- control using T. julis from Europe has been patibility of two biological control agents; widely successful in the management of O. 5. Determine the developmental biology of melanopus throughout North America and T. julis at constant and fl uctuating tempera- has become the primary management tures in order to develop a bioclimatic strategy. In western Canada, as elsewhere, model to predict regions of the country T. julis has dispersed along with the beetle capable of sustaining populations of this and a steady increase in the parasitization parasitoid.

References

Canadian Food Inspection Agency (CFIA) (1999) Summary of plant quarantine, pest and disease situations in Canada, 1999: Cereal leaf beetle: Oulema melanopus. Available at: http://www. inspection.gc.ca/english/sci/surv/sit99e.shtml#Oulema (accessed 20 February 2010). Canadian Food Inspection Agency (CFIA) (2011) Cereal leaf beetle (Oulema melanopus L.). RMD # 07-02. Available at: http://www.inspection.gc.ca/english/plaveg/protect/rmd/rmd-07-02e.shtml (accessed 15 March 2010). Cappuccino, N., Mason, P., Casagrande, R., Kenis, M., Haye, T. and Tewksbury, L. (2009) Petition for cage and open fi eld release of Tetrastichus setifer (Hymenoptera: Eulophidae) for biological control of the lily leaf beetle, Lilioceris lilii (Coleoptera: Chrysomelidae) in Canada. Technical Report, Carlton University, Ottawa, Ontario. Chapter 33 237

Dosdall, L., Cárcamo, H., Olfert, O., Meers, S., Hartley, S. and Gavloski, J. (2011) Insect invasions of agro-ecosystems in the western Canadian prairies: case histories, patterns, and implications for ecosystem functioning. Biological Invasions 13, 1135–1149. Dysart, R.J., Maltby, H.L. and Brunson, M.H. (1973) Larval parasites of Oulema melanopus in Europe and their colonization in the United States. Entomophaga 18, 133–167. Evans, E.W., Karren, J.B. and Israelsen, C.E. (2006) Interactions over time between cereal leaf beetle (Coleoptera: Chrysomelidae) and larval parasitoid Tetrastichus julis (Hymenoptera: Eulophidae) in Utah. Journal of Economic Entomology 99, 1967–1973. Harcourt, D.G., Guppy, J.C. and Ellis, C.R. (1977) Establishment and spread of Tetrastichus julis, a parasitoid of the cereal leaf beetle in Ontario, Canada. Canadian Entomologist 109, 473–476. Harcourt, D.G., Guppy, J.C. and Ellis, C.R. (1984) Cereal leaf beetle (Coleoptera: Chrysomelidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes Against Insects and Weeds in Canada 1969–1980. CAB international, Slough, UK, pp. 65–67. Haynes, D.L. and Gage, S.H. (1981) The cereal leaf beetle in North America. Annual Review of Entomology 26, 259–287. Hervet, V. (2010) Assessment of non-target effects in southwestern Canada of the parasitoid Tetrastichus julis Walker (Hymenoptera: Eulophidae) introduced for biological control of the cereal leaf beetle (Oulema melanopus L., Coleoptera: Chrysomelidae). Thesis, Institut Polytechnique LaSalle Beauvais, Beauvais Cedex, France. Kher, S.V., Dosdall, L.M. and Cárcamo, H.A. (2011) The cereal leaf beetle: biology, distribution and prospects for control. Prairie Soils and Crops 4, 32–41. Kuhlmann, U., Mason, P.G., Hinz, H.L., Blossey, B., De Clerck-Floate, R.A., Dosdall, L.M., McCaffrey, J.P., Schwarzlaender, M., Olfert, O., Brodeur, J., McClay, A.S., Gassmann, A. and Wiedenmann, R.N. (2006) Avoiding confl icts between insect and weed biological control: selection of nontarget species to assess host specifi city of cabbage seedpod weevil parasitoids. Journal of Applied Entomology 130, 129–141. LeSage, L., Dobesberger, E.J. and Majka, C.G. (2007) Introduced leaf beetles of the Maritime Provinces, 2: The cereal leaf beetle Oulema melanopus (Linnaeus) (Coleoptera: Chrysomelidae). Proceedings of the Entomological Society of Washington 109, 286–294. Ontario Ministry of Agriculture, Food and Rural Affairs (OMAFRA) (2009) Insects and Pests of Field Crops: Cereal Insects and Pests. Available at: http://www.omafra.gov.on.ca/english/crops/ pub811/13cereal.htm#clbeetle (accessed 20 January 2012). Paschke, J.D. (1965) Infection of the cereal leaf beetle, Oulema melanopa (Linnaeus) by Beauveria bassiana (Bals.) Vuill. Journal of Invertebrate Pathology 7, 101–102. Western Committee on Crop Pests (WCCP) (2011) Determination of the distribution, abundance, and phenology of cereal leaf beetle in Alberta. Alberta Research Report, Western Committee of Crop Pests, Kelowna, British Columbia, 18 October 2011. Webster, J.A., Smith, D.H. and Gage, S.H. (1978) Cereal leaf beetle (Coleoptera: Chrysomelidae): Infl uence of seeding rate of oats in populations. Great Lakes Entomologist 11, 117–120. 238 Chapter 34

34 Panonychus ulmi (Koch) European Red Mite (Trombidiformes: Tetranychidae)

Howard M.A. Thistlewood,1 Noubar J. Bostanian2 and J. Michael Hardman3 1Agriculture and Agri-Food Canada, Summerland, British Columbia; 2Agriculture et Agroalimentaire Canada, Saint Jean-sur-Richelieu, Québec; 3Agriculture and Agri-Food Canada, Kentville, Nova Scotia

34.1 Pest Status native strains. Phytoseiidae (Megostigmata) mites were the main focus of previous The European red mite, Panonychus ulmi work (cf. Hardman and Thistlewood, 2002) (Koch) (Trombidiformes: Tetranychidae), because they are the most useful predators continues to be the most serious mite pest of P. ulmi, have heritable resistance to of apple, Malus spp., and peach, Prunus agricultural chemicals, high searching cap- persica (L.) Batsch (Rosaceae), in Canada acity, multivoltinism, and a reproductive and can be very damaging to many other rate that often exceeds that of their prey. fruit and berry crops, including grapes, Other important acarine enemies are Vitis vinifera L. (Vitaceae). By feeding on within the Stigmaeidae, Anystidae and leaves, P. ulmi reduces photosynthesis and Erythraeidae (Trombidiformes). Important adversely affects vegetative growth of insect predators are Coccinellidae (Cole- plants, fruit yield and fruit quality attri- optera) beetles such as Stethorus spp., and butes such as size, fi rmness, fl avour and some species of Anthocoridae, Derae- storage life (Marini et al., 1994). High ocoridae and Miridae (Hemiptera) bugs. population densities can result from their Conservation biological control, i.e. a high reproductive rate, short generation strategy for the preservation of natural time, multivoltinism and ability for rapid enemies, is the most important technique evolution of resistance to insecticides and for suppression of P. ulmi to sub-economic acaricides that are used in the crops. population levels. This is because unrestrained outbreaks of P. ulmi can occur after the application of a wide range of 34.2 Background agricultural chemicals. These have various effects upon predators including indirect Natural enemies of P. ulmi and other and direct toxicity, repellency from treated tetranychid (spider) mites have been surfaces, or sterility of females as described studied intensively by Canadian acar- below. Augmentative or inundative ologists since at least the 1950s. Most effort releases of natural enemies of P. ulmi have has concentrated on the con servation, and been made in Canada since at least the augmentative or inundative release of 1980s (Bostanian and Coulombe, 1986; indigenous species of predators, with some Hardman and Thistlewood, 2002) to research on genetically improved or non- restore conservation biological control in © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 34 239

pesticide-treated sites. Where biological studied the functional and numerical control fails completely, P. ulmi and other responses of N. fallacis and T. pyri for tetranychid mites are managed using biological control of P. ulmi and the specifi c acaricides. twospotted spider mite, Tetranychus urticae Koch (Trombidiformes: Tetrany- chidae), on apple leaf discs and on small 34.3 Biological Control Agents potted apple trees. Lester et al. (2005) extended earlier fi eld studies of the role of From the 1960s to 1990s, attention was patch number and connectivity in multi- concentrated on the phytoseiid mites, patch landscapes. They examined inter- particularly on Galendromus occidentalis actions by N. fallacis when feeding on P. (Nesbitt) (=Metaseiulus occidentalis (Nes- ulmi in experiments that varied patch bitt), = Typhlodromus occidentalis Nesbitt) number, and individual-based simulation in western Canada, on Neoseiulus fallacis models that varied in both patch number (Garman) (=Amblyseius fallacis Garman) in and connectivity. They found that altering Ontario and Quebec and on Typhlodromus patch number or connectivity did not pyri Scheuten (Megostigmata: Phyto- change the predator’s functional response, seiidae) in the Maritime provinces. In the even with an 80-fold decrease in patch last decade, basic knowledge of the natural connectivity. enemies of P. ulmi in Canada has continued to grow. Extensive exploration of acarine predators of P. ulmi on apple in 34.4 Evaluation of Biological Control Quebec revealed that a diverse fauna of predatory mites was important in regu- 34.4.1 Conservation of natural enemies lation of the pest (Bostanian et al., 2006, 2009a). Neoseiulus fallacis, Typhlodromus Conservation biological control of P. ulmi caudiglans Schuster (Mesostigmata: Phyto- requires that pesticides used to manage seiidae) and Agistemus fl eschneri Summers other arthropod pests or diseases are (Trombidiformes: Stigmaeidae) were the harmless to the predatory mites that feed most abundant species. Other phytoseiids on it. The value of conserving predator were found in low numbers, as were populations was shown in a 4-year study Anystis baccarum L. (Trombidiformes: in a Quebec apple orchard (Bostanian et Anystidae) and Balaustium sp. (Trombidi- al., 2007). When few or no predators were formes: Erythraeidae). Typhlodromus present, increased densities of P. ulmi caudiglans and A. fl eschneri can represent winter eggs were always found in the 80% or more of the naturally occurring following spring. By contrast, the presence predators (Bostanian et al., 2005). Marshall of signifi cant numbers of predators in July– et al. (2001) concluded that T. pyri appears September was followed by a ten-fold to be particularly useful for biological decrease in the mean density of winter eggs control of phytophagous mites in Ontario of P. ulmi in the following year. and recommend continued testing for Management of functional biodiversity conservation and augmentative release. within crops is an important new approach They also observed T. caudiglans, N. in the conservation of predators. Manipu- fallacis and Zetzellia mali (Ewing) (Trom- lation of the ground fl ora of orchards can bidiformes: Stigmaeidae) at population lead to the absence of phytophagous mites levels suffi cient for biological control in (Bostanian et al., 2004a). Similarly, orchards. manipulation of the within-orchard and Fundamental studies of the complex of under-tree ‘herbicide strip’ can result in predators of P. ulmi and applied studies of increased action of natural enemies on P. conservation or augmentative release of ulmi and other pests (Hardman et al., predators were aided by insights from the 2011). In the latter study, the abundance of laboratory. Lester and Harmsen (2002) pest and predator mites was monitored in 240 Chapter 34

apple trees and on tree trunks, within plots released for the fi rst time into Ontario created with wide (2 m) or narrow (0.5 m) apple orchards (Marshall and Lester, 2001) herbicide strips, for 2 years. These manipu- and vineyards (Marshall et al., 2001) for lations ultimately resulted in reduced biological control of P. ulmi. Marshall et al. densities of P. ulmi in plots with wide (2001) released a strain of T. pyri from herbicide strips compared to plots with Nova Scotia, with organophosphate- and narrow strips, and predator–prey ratios pyrethroid-resistant traits, into apple were usually several-fold higher owing to orchards. They followed its progress over an enhanced presence of phytoseiid four seasons, when it established in the predators, mostly T. pyri. orchards, became the dominant predator Conservation biological control for P. and was associated with low densities of P. ulmi, and phytophagous mites in general, ulmi and T. urticae, as well as Aculus requires that newly registered pesticides be schlechtendali (Nalepa) (Trombidiformes: compatible with key species of predators. Eriophyidae). Typhlodromus pyri moved The recent introduction of ‘reduced risk’ slowly through orchards and took 4 years pesticides has led to a perception of to move 84 m from the release point in two general safety when, in reality, some new orchards. However, movement did not materials can be very toxic to natural appear to be infl uenced by the predomin- enemies. Evaluations of new ‘reduced risk’ ant wind direction. Typhlodromus pyri products have recently been conducted, as occurred in high numbers on release trees, well as comparisons with older products. or trees near the release trees, each summer Moderate to severe effects of toxicity, or after release. Other predatory species in the reduced fecundity, were observed for one orchards, including T. caudiglans, N. or more life stages of mite predators in 14 fallacis and Z. mali were more generally of 25 insecticides or acaricides that were distributed. They noted that T. pyri appears evaluated, and in 2 of 11 fungicides particularly useful for biological control of (Bostanian and Larocque, 2001; Hardman phytophagous mites in Ontario and is et al., 2003, 2006, 2010; Provost et al., worthy of further testing for conservation 2003; Bostanian et al., 2004b, 2009b, c; and augmentative release. Laurin and Bostanian, 2007a, b; Lefebvre et Major outbreaks of P. ulmi occurred in al., 2011). The sum of these studies Ontario vineyards, arising principally from provided much knowledge that has been a breakdown in biological control fol- used in different ways, such as in lowing pesticide use (Marshall and Lester production guides, compatibility charts, 2001). Grape leaves were transferred from a brochures, and in IPM or IFP-compliant donor vineyard with T. pyri in early pesticide classifi cation tools, which are summer to introduce and establish popu- now available in many formats, usually lations of T. pyri and restore biological from provincial agencies, e.g. Fédération control of P. ulmi. In the fi rst season, T. pyri des producteurs de pommes du Québec, established in similar densities in both 2012. release treatments and was more abundant than in no-release control plots. In the year after release, signifi cantly fewer P. ulmi 34.4.2 Augmentative and inundative release mite-days were observed in release plots of predators compared to the control. Marshall and Lester (2001) concluded that T. pyri can be During the last decade, augmentative and effective for P. ulmi biological control in inundative releases of predators of P. ulmi Ontario vineyards and may be introduced were continued in orchards and vineyards easily by transferring leaves rather than of eastern Canada. Although the phytoseiid winter prunings (transfer of prunings is the mite T. pyri is now relatively well standard method of inoculating T. pyri in understood in Nova Scotia (reviewed by European vineyards). They also observed Hardman and Thistlewood, 2002), it was that N. fallacis appeared on the vines too Chapter 34 241 late in the season to maintain low P. ulmi different sites (Bostanian et al., 2009a). densities, and was out-competed by T. pyri This approach requires an understanding in at least one of the seasons under study. of the relative toxicity to key predatory Insect predators of P. ulmi were reared mites of the pesticides employed in fruit and released over some years in southern crops, as described above. Such infor- Quebec. Releases of Hyaliodes vitripennis mation is transferred regularly to growers (Say) (Hemiptera: Miridae) reduced who prepare their own pest management numbers of P. ulmi in semi-natural programmes, with the help of extension conditions on caged apple trees and in agents. A simple technique was developed orchards (Brodeur et al., 1999). Firlej et al. to transfer pruned winter- and summer- (2003) assessed the establishment and wood from a donor orchard where bio- dispersal ability of H. vitripennis in a logical control of mites had established to a commercial apple orchard where the recipient orchard where it was in the predator was previously absent. Predators process of being established. Bostanian et were introduced, once each year on to four al. (2005) summarized the knowledge apple trees within a 0.2 ha zone in the gained in methods of establishment of centre of the orchard, at a rate of 200 predacious mites by such transfers of predators per tree. Mite populations were pruned wood. Detailed instructions are monitored in the central 0.2 ha, as were given such as what type of wood to cut at predator populations within a further 0.8 what time of year, release rates within ha. Populations of P. ulmi decreased in orchards of ‘dwarfi ng’ rootstock trees or trees where H. vitripennis was introduced standard size trees, how many leaves in 2000, and increased populations of the should remain if branches are transferred predator were found in both years. in summer, ideal predator numbers per Predators occurred early in the season on leaf, and infestation levels (two or three trees that did not receive any predators in mites per leaf) of pest tetranychids within 2000, and throughout the monitored areas target release orchards. in the 2002 season. The potential of H. The fundamental importance of con- vitripennis for biological control of mites serving natural enemies for biological and aphids in Quebec apple orchards was control of mites is recognized by all fruit, examined further in a 3-year study berry, or grape growers and related exten- (Chouinard et al., 2006). Populations of P. sion personnel. However, this requires ulmi and T. urticae were reduced continuous research to assess and under- signifi cantly in trees with H. vitripennis stand all new agricultural chemicals, during 3 years of releases, and there were particularly pesticides, as to their com- signifi cant effects on two aphid species. patibility with different mite predators in Although they concluded that release of H. at least two major regions of Canada. In vitripennis may also interfere with Europe, but not yet North America, such predatory mites present in the orchards, research is part of the registration either by resource competition or by direct requirements for pesticides and the costs predation, the combined effect of the are borne by the companies as part of the various predators was always a signifi cant registration and decision process. The reduction in P. ulmi numbers. arrival of invasive species, such as The approach of large scale mass-rearing Drosophila suzukii (Matsumura) (Diptera: and inundative release of N. fallacis or T. Drosophilidae), creates additional pres- pyri has been found to be unreliable and sures on biological control programmes impractical for P. ulmi in Quebec. A robust against P. ulmi through emergency use of and ‘grower-friendly’ philosophy for bio- agrochemicals of unknown or high toxicity logical control of phytophagous mites has to mite predators. Presently, there is a emerged, using a combination of conser- relatively high level of adoption of vation, re-colonization and augmentation biological control approaches for P. ulmi in of naturally occurring predacious mites at Canada. 242 Chapter 34

34.5 Future Needs 4. Working with legislators to alter regis- tration requirements to require compatibil- Future work should include: ity test data in registration packages.

1. Research on the biology of important, but lesser known, species such as Anystis Acknowledgements spp. and Balaustium spp.; 2. Development of practical approaches by We thank Fred Beaulieu, Gérald Chouinard, determining quantity and timing of Gaétan Racette and Brigitte Rozema for releases, predator dispersal and movement, valuable assistance in sourcing documents so as to encourage use of augmentative and or for comments on an earlier draft of the inundative releases of biological control report. HMAT was aided via a fellowship agents against P. ulmi on different crops under the OECD Co-operative Research and in different regions of Canada; Programme: Biological Resource Manage- 3. Determining the compatibility of exist- ment for Sustainable Agricultural Systems, ing and new agricultural chemicals, partic- in the laboratory of Laura Monteiro Torres, ularly pesticides, with different mite CITAB, School of Agriculture & Veterinary predators in at least two major regions of Sciences, University of Trás-os-Montes and Canada; Alto Douro, Portugal.

References

Bostanian, N.J. and Coulombe, L.J. (1986) An integrated pest management program for apple orchards in southwestern Quebec. The Canadian Entomologist 118, 1131–1142. Bostanian, N.J. and Larocque, N. (2001) Laboratory tests to determine the intrinsic toxicity of four fungicides and two insecticides to the predacious mite Agistemus fl eschneri. Phytoparasitica 29, 215–222. Bostanian, N.J., Goulet, H., O’Hara, J., Masner, L. and Racette, G. (2004a) Towards insecticide free apple orchards: fl owering plants to attract benefi cial arthropods. Biocontrol Science and Technology 14, 25–37. Bostanian, N.J., Vincent, C., Hardman, J.M. and Larocque, N. (2004b) Toxicity of indoxacarb to two species of predacious mites and a predacious mirid. Pest Management Science 60, 483–486. Bostanian, N.J., Lasnier, J. and Racette, G. (2005) A grower-friendly method to transfer predacious mites to commercial orchards. Phytoparasitica 33, 515–525. Bostanian, N.J., Hardman, J.M., Racette, G., Franklin, J.L. and Lasnier, J. (2006) Inventory of predacious mites in Quebec apple orchards where integrated pest management programs are implemented. Annals of the Entomological Society of America 99, 536–544. Bostanian, N.J., Hardman, J.M., Racette, G. and Franklin, J.L. (2007) The relationship between winter egg counts of the European red mite Panonychus ulmi (Acari: Tetranychidae) and its summer abundance in a reduced spray orchard. Experimental and Applied Acarology 42, 185–195. Bostanian, N.J., Racette, G. and Lasnier, J. (2009a) Biocontrol of phytophagous mites in Quebec apple orchards. In: Sabelis, M.W. and Bruin, J. (eds) Trends in Acarology. Proceedings of the 12th International Congress. Springer Verlag, Hamburg, Germany, pp. 451–455. Bostanian, N.J., Thistlewood, H.M.A., Hardman, J.M., Laurin, M.-C. and Racette, G. (2009b) Effect of seven new orchard pesticides on Galendromus occidentalis in laboratory studies. Pest Management Science 65, 635–639. Bostanian, N.J., Thistlewood, H.M.A., Hardman, J.M. and Racette, G. (2009c) Toxicity of six novel fungicides and sulphur to Galendromus occidentalis (Acari: Phytoseiidae). Experimental and Applied Acarology 47, 63–69. Brodeur, C., Chouinard, G., Laplante, G. and Morin, Y. (1999) Études préliminaires sur l’activité et l’effi cacité du prédateur indigène Hyaliodes vitripennis (Heteroptera: Miridae) pour la lutte biologique contre les acariens en vergers de pommiers au Québec. Annales de la Société Entomologique de France 35(Suppl.), 458–462. Chapter 34 243

Chouinard, G., Bellerose, S., Brodeur, C. and Morin, Y. (2006) Effectiveness of Hyaliodes vitripennis (Say) (Heteroptera: Miridae) predation in apple orchards. Crop Protection 25, 705–711. Fédération des Producteurs de Pommes du Québec (2012) Production fruitière intégrée 2009-2010 – Un regard sur les bonnes pratiques. Available at: http://www.agrireseau.qc.ca/reseaupommier/ documents/Affi che%20PFI_2009_fi nale.pdf (accessed 31 October 2012). Firlej, A., Chouinard, G., Morin, Y., Cormier, D. and Coderre, D. (2003) Établissement et dispersion du prédateur Hyaliodes vitripennis (Hemiptera: Miridae) suite à des introductions dans une pommeraie commerciale au Québec. Phytoprotection 84, 93–103. Hardman, J.M. and Thistlewood, H.M.A. (2002) Panonychus ulmi (Koch), European red mite (Acari: Tetranychidae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 213–216. Hardman, J.M., Franklin, J.L., Moreau, D.L. and Bostanian, N.J. (2003) An index for selective toxicity of miticides to phytophagous mites and their predators based on orchard trials. Pest Management Science 59, 1321–1332. Hardman, J.M., Franklin, J.L., Jensen, K.I.N. and Moreau, D.L. (2006) Effects of pesticides on mite predators (Acari: Phytoseiidae) and colonization of apple trees by Tetranychus urticae. Phytoparasitica 34, 449–462. Hardman, J.M., Franklin, J.L. and Bostanian, N.J. (2010) Application of a non-selective acaricide aggravates outbreaks of Tetranychus urticae on apple by suppressing its predator, Typhlodromus pyri, and its competitor, Panonychus ulmi. Bulletin of the International Organisation of Biological Control/Western Palaearctic Regional Section 55, 1–10. Hardman, J.M., Franklin, J.L., Bostanian, N.J. and Thistlewood, H.M.A. (2011) Effect of the width of the herbicide strip on mite dynamics in apple orchards. Experimental and Applied Acarology 53, 215–234. Laurin, M.-C. and Bostanian, N.J. (2007a) Laboratory studies to elucidate the residual toxicity of eight insecticides to Anystis baccarum (Acari: Anystidae). Journal of Economic Entomology 100, 1210–1214. Laurin, M.-C. and Bostanian, N.J. (2007b) Short-term contact toxicity of seven fungicides on Anystis baccarum. Phytoparasitica 35, 380–385. Lefebvre, M., Bostanian, N.J., Thistlewood, H.M.A., Mauffette, Y. and Racette, G. (2011) A laboratory assessment of the toxic attributes of six ‘reduced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). Chemosphere 84, 25–30. Lester, P.J. and Harmsen, R. (2002) Functional and numerical responses do not always indicate the most effective predator for biological control: an analysis of two predators in a two-prey system. Journal of Applied Ecology 39, 455–468. Lester, P.J., Yee, J.M., Yee, S., Haywood, J., Thistlewood, H.M.A. and Harmsen, R. (2005) Does altering patch number and connectivity change the predatory functional response type? Experiments and simulations in an acarine predator-prey system. Canadian Journal of Zoology 83, 797–806. Marini, R.P.D., Pfeiffer, D.G. and Sowers, D.S. (1994) Infl uence of European red mite (Acari: Tetranychidae) and crop density on fruit size and quality and on crop value of ‘Delicious’ apple trees. Journal of Economic Entomology 87, 1302–1311. Marshall, D.B. and Lester, P.J. (2001) The transfer of Typhlodromus pyri on grape leaves for biological control of Panonychus ulmi (Acari: Phytoseiidae, Tetranychidae) in vineyards in Ontario, Canada. Biological Control, 20, 228–235. Marshall, D.B., Thistlewood, H.M.A. and Lester, P.J. (2001) Release, establishment, and movement of the predator Typhlodromus pyri (Acari: Phytoseiidae) on apple. Canadian Entomologist 133, 279–292. Provost, C., Coderre, D., Lucas, E., Chouinard, G. and Bostanian, N.J. (2003) Impacts of a sublethal dose of lambda-cyhalothrin on phytophagous mite intraguild predators in apple orchards. Phytoprotection 84, 105–113. 244 Chapter 35

35 Phyllonorycter blancardella (Fabricius), Spotted Tentiform Leafminer (Lepidoptera: Gracillariidae)

Charles Vincent,1 John T. Huber,2 Gary A.P. Gibson3 and Henri Goulet3 1Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, Québec; 2Natural Resources Canada, Canadian Forest Service, Ottawa, Ontario; 3Agriculture and Agri-Food Canada, Ottawa, Ontario

35.1 Pest Status Quebec, P. blancardella has three gener- ations per season and overwinters as pupae The spotted tentiform leafminer, Phyllon- in fallen apple leaves. Eggs are laid on orycter blancardella (Fabricius) (Lepi- apple leaves and larvae develop in the doptera: Gracillariidae), is a western parenchyma, leaving a mine visible in Palaearctic species reported as far east as leaves. Apples may fall when trees are Iran and Russia (De Prins and De Prins, heavily attacked, causing immediate losses. 2005). It was fi rst reported in the Nearctic In addition, heavily attacked apple trees from Nova Scotia in the 1940s (Johnson et are likely to bloom every second year, al., 1976), but may have been accidentally causing major management problems to introduced into North America early in the apple growers. In the late 1970s and early 1900s (Laing, 1984). The Nova Scotia 1980s some populations of P. blancardella report corresponds to the time that leaf- in Ontario developed resistance to organo- mining moths became serious pests in phosphates (Pree et al., 1980) and pyre- apple, Malus spp., and pear, Pyrus com- throids (Pree et al., 1986). This impaired munis L., (Rosaceae) orchards in most insect management programmes, notably European countries from the end of the by restricting the number of insecticides 1940s. It was surmised that one of the available for control. The possibility of factors in this change in their pest status escalating resistance levels to insecticides was the destruction of their natural increased the diffi culty of implementing enemies by pesticides (Cross et al., 1999). sustainable protection programmes in In eastern North America, P. blancardella orchards. is a pest of apple, Malus domestica Borkh. (Rosaceae), trees (Pottinger and LeRoux, 1971; Maier, 1994). In some areas it occurs 35.2 Background with the apple blotch leafminer, Phyllon- orycter crataegella (Clemens) (Lepidoptera: Numerous parasitoid species have been Gracillariidae) (Maier, 1983), but is the recorded from P. blancardella from various dominant species in Ontario, Quebec and parts of its current range in the Palaearctic Nova Scotia (Pottinger and LeRoux, 1971; and Nearctic regions. Most of them are Vincent et al., 1986). In central Ontario and Chalcidoidea (Noyes, 2012) but some are

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 35 245

Ichneumonoidea (Yu et al., 2011). Cross et families, i.e. Braconidae, Ichneumonidae, al. (1999) mentioned some of the most Eulophidae, Encyrtidae and Pteromalidae – important parasitoids in various European 19 species) and constitutes a baseline for countries. Tomov (2002) listed 40 species biodiversity of natural enemies attacking P. in Bulgaria, all reared from the leaves blancardella in orchards in Quebec. containing overwintering generation mines gathered in autumn in unsprayed apple 35.3 Biological Control Agents orchards. Several surveys conducted in Quebec In 1978, the exotic braconid species and Ontario before 1982 (e.g. Pottinger and Pholetesor pedias (Nixon) (Hymenoptera: LeRoux, 1971; Johnson et al., 1976; Hagley, Braconidae) was released and established 1985) determined that 36 species of near Guelph, Ontario (Laing and Heraty, hymenopterous parasitoids were naturally 1981). In 1983, P. pedias was also released associated with Phyllonorycter spp. in an unsprayed apple orchard at the Pholetesor ornigis (Weed) (Hymenoptera: experimental farm of Agriculture and Agri- Braconidae) and Sympiesis gordius Food Canada in Frelighsburg, Quebec. (Walker) (= S. marylandensis (Girault)) However, it was not recovered in the (Hymenoptera: Eulophidae) (Maier and survey by Bishop et al. (2001). Hansson, 2006) were the dominant para- sitoid species. Surveys were conducted also in 1983–1985 in Quebec and in 1994– 35.4 Evaluation of Biological Control 1995 in Nova Scotia (Bishop et al., 2001). In Quebec, 1506 specimens were Biological control of P. blancardella is recovered, the most prevalent species being affected by physical control methods used P. ornigis (67%) together with S. gordius to manage apple scab, a fungal disease (11%), Sympiesis sericeicornis (Nees) (7%), caused by Venturia inaequalis (Cooke) G. Pnigalio maculipes (Crawford) (1.5%) and Winter (Venturiaceae), which is a major Tetrastichus spp. (1.2%) (Hymenoptera: challenge in apple protection (Aluja et al., Eulophidae). In Nova Scotia, 2640 speci- 2009). Depending on the weather and mens were recovered, the most prevalent disease pressure prevailing in spring, man- species being P. ornigis (52%). Others were agement of apple scab in eastern Canada P. maculipes (14%), S. sericeicornis (12%), typically requires 6–14 fungicide treat- S. gordius (9.5%), Sympiesis spp. (5%) and ments per season. Physical control Horismenus fraternus (Fitch) (1.8%) methods are sound alternatives to insecti- (Hymenoptera: Eulophidae), Praleurocerus cides and other pesticides (Vincent et al., sp. (1.3%) (Hymenoptera: Encyrtidae) and 2001, 2003). Thus, apple leaf shredding Stictopisthus fl aviceps (Provancher) (1.1%) was evaluated in the fi eld (Vincent et al., (Hymenoptera: Ichneumonidae). 2004). The main principle was that Since 2000, new North American para- shredding leaves that fall naturally on to sitoid records for P. blancardella include the ground in autumn would increase leaf Sticopisthus bilineatus (Thomson) and S. surface, thereby allowing faster leaf fl aviceps (Hymenoptera: Ichneumonidae), decomposition by soil bacteria and fungi Euderus sp., Pnigalio epilobii Bouc ˇek and competing with V. inaequalis. Destruction P. pallipes (Provancher) (Hymenoptera: of apple scab inoculum by leaf shredding Eulophidae) and Ageniaspis bicoloripes was expected to provide ca. 90% reduction (Girault) (Hymenoptera: Encyrtidae) of apple scab risk the following spring. (Bishop et al., 2001). The survey suggested However, because P. blancardella and its that the parasitoid fauna of Quebec is more parasitoids overwinter in fallen apple diverse (seven families, i.e. Braconidae, leaves, they could be impacted as well. Ichneumonidae, Eulophidae, Encyrtidae, A 3-year fi eld study demonstrated that Pteromalidae, Aphelinidae and Scelionidae leaf shredding in autumn not only – 29 species) than that of Nova Scotia (fi ve signifi cantly reduced apple scab inoculum 246 Chapter 35

the next spring, but also negatively growers and virtually no specifi c treat- impacted overwintering P. blancardella ments were required. Should this situation populations and all species of associated prevail, no action is required in the short parasitoids (Vincent et al., 2004). For and medium term. Otherwise, leaf example, in 1995, out of six groups of 350 shredding is thought to be a tactic that can leaves left on the ground to overwinter, an greatly reduce V. inaequalis and P. average of 16.5 parasites emerged in the blancardella pressure. However, its impact control (non-shredded) in the following on parasitoid populations and subsequent year, versus no emergence from the population dynamics should be con- shredded leaves. sidered.

35.5 Future Needs Acknowledgements

In the decade 2001–2010, P. blancardella We thank Benoit Rancourt for technical did not pose a major concern to apple input.

References

Aluja, M., Leskey, T.C. and Vincent, C. (eds) (2009) Biorational Tree-Fruit Pest Management. CAB International, Wallingford, Oxon, UK. Bishop, S.D., Smith, R.F., Vincent, C., Goulet, H., Huber, J., Gibson, G., Sharkey, M.J. and Borden, J.H. (2001) Hymenopterous parasites associated with Phyllonorycter blancardella (Lepidoptera: Gracillariidae) in Nova Scotia and Quebec. Phytoprotection 82, 65–71. Cross, J.V., Solomon, M.G., Babeandreier, D., Blommers, L., Easterbrook, M.A., Jay, C.N., Jenser, G., Jolly, R.L., Kuhlmann, U., Lilley, R., Olivella, E., Toepfer, S. and Vidal, S. (1999) Biocontrol of Pests of Apples and Pears in Northern and Central Europe: 2. Parasitoids. Biocontrol Science and Technology 9, 277–314. De Prins, W. and De Prins, J. (2005) World Catalogue of Insects. Vol. 6. Gracillariidae (Lepidoptera). Apollo Books, Stenstrup, Denmark. Hagley, E.C.A. (1985) Parasites recovered from the overwintering generation of the spotted tentiform leafminer, Phyllonorycter blancardella (Lepidoptera: Gracillariidae) in pest management orchards in southern Ontario. The Canadian Entomologist 117, 371–374. Johnson, E.F., Laing, J.E. and Trottier, R. (1976) The seasonal occurrence of Lithocolletis blancardella (Gracillariidae), and its major natural enemies in Ontario apple orchards. Proceedings of the Entomological Society of Ontario 107, 31–45. Laing, J.E. (1984) Phyllonorycter blancardella (F.), Spotted tentiform leafminer (Lepidoptera: Gracillariidae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, UK, pp. 69–76. Laing, J.E. and Heraty, J.M. (1981) Establishment in Canada of the parasite Apanteles pedias Nixon on the spotted tentiform leafminer, Phyllonorycter blancardella (Fabr.). Environmental Entomology 10, 933–935. Maier, C.T. (1983) Relative abundance of the spotted tentiform leafminer, Phyllonorycter blancardella (F.), and the apple blotch leafminer, P. crataegella (Clements) (Lepidoptera: Gracillariidae), on sprayed and unsprayed apple trees in Connecticut. Annals of the Entomological Society of America 76, 992–995. Maier, C.T. (1994) Biology and impact of parasitoids of Phyllonorycter blancardella and P. crataegella (Lepidoptera: Gracillariidae), in North American apple orchards, In: Maier, C.T. (ed.) Integrated Management of Tentiform Leafminers, Phyllonorycter spp. (Lepidoptera: Gracillariidae), in North American Apple Orchards. Thomas Say Publications in Entomology. Entomological Society of America, Lanham, Maryland, pp. 6–24. Chapter 35 247

Maier, C.T. and Hansson, C. (2006) Palearctic Sympiesis acalle and Sympiesis gordius (Hymenoptera: Eulophidae) in North America: taxonomic changes and a review of Nearctic host records. Proceedings of the Entomological Society of Washington 108, 14–23. Noyes, J.S. (2012) Universal Chalcidoidea Database. Available at: http://www.nhm.ac.uk/research- curation/research/projects/chalcidoids (accessed 18 September 2012). Pottinger, R.P. and LeRoux, E.J. (1971) The biology and dynamics of Lithocolletis blancardella (Lepidoptera: Gracillariidae). Memoirs of the Entomological Society of Canada 103 (Suppl. S77), 1–437. Pree, D.J., Hagley, E.A.C., Simpson, C.M. and Hikichi, A. (1980) Resistance of the spotted tentiform leafminer, Phyllonorycter blancardella to organophosphorous insecticides in southern Ontario. The Canadian Entomologist 112, 469–474. Pree, D., Marshall, J.D.B. and Archibald, D.E. (1986) Resistance to pyrethroid insecticides in the spotted tentiform leafminer, Phyllonorycter blancardella in southern Ontario. Journal of Economic Entomology 79, 318–322. Tomov, R. (2002) Species composition of parasitoids (Hymenoptera) on apple feeding Phyllonorycter (Lepidoptera: Gracillariidae) in Bulgaria. In: Melika, G. and Thuróczy, C. (eds) Parasitic Wasps: evolution, systematics, biodiversity and biological control. International symposium: ‘Parasitic Hymenoptera: Taxonomy and Biological Control’ (14–17 May 2001, Köszeg, Hungary). Agroinform Kiadó & Nyomda, Budapest, Hungary, pp. 440–441. Vincent, C., Mailloux, M. and Hagley, E.A.C. (1986) Nonsticky pheromone-baited traps for monitoring the spotted tentiform leafminer (Lepidoptera: Gracillariidae). Journal of Economic Entomology 79, 1666–1670. Vincent, C., Panneton, B. and Fleurat-Lessard, F. (eds) (2001) Physical Control Methods in Plant Protection. Springer-Verlag/INRA, Heidelberg, Germany. Vincent, C., Hallman, G., Panneton, B. and Fleurat-Lessard, F. (2003) Management of agricultural insects with physical control methods. Annual Review of Entomology 48, 261–281. Vincent, C., Rancourt, B. and Carisse, O. (2004) Apple leaf shredding as a non-chemical management tactic for apple scab and spotted tentiform leafminer. Agriculture, Ecosystems and Environment 104, 595–604. Yu, D.S.K., van Achterberg, C. and Horstmann, K. (2011) Taxapad 2012, Ichneumonoidea 2011. Database on fl ash-drive. http://www.taxapad.com, Ottawa, Ontario. 248 Chapter 36

36 Phyllotreta cruciferae (Goeze), Crucifer Flea Beetle and P. striolata (Fabricius), Striped Flea Beetle (Coleoptera: Chrysomelidae)

Juliana J. Soroka Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

36.1 Pest Status (Milliron, 1953; Beirne, 1971). The 2–3 mm long beetles are black with a bluish sheen The crucifer fl ea beetle, Phyllotreta and are the most common fl ea beetle cruciferae (Goeze), and striped fl ea beetle, species in central and southern regions of P. striolata (Fabricius) (Coleoptera: Chrys- Prairie canola production (Burgess, 1977a, omelidae), are primary pests of bras- 1981, 1984). Phyllotreta striolata was sicaceous oilseed crops and vegetables introduced to North America from Eurasia across Canada. They are the most at a very early date. Specimens of P. economically detrimental insect pest of striolata dating to the last quarter of the canola, Brassica napus L. and B. rapa L. 17th century have been found in archaeo- (Brassicaceae) in western Canada, where logical excavations of latrines in Boston, annual canola yield losses from fl ea beetle Massachusetts (Bain and LeSage, 1998). damage average 8–10% and damage costs These beetles are black in colour with a can exceed CAN$300m (Lamb and distinctive sinuous yellow stripe on each Turnock, 1982; Knodel and Olson, 2002). elytron. Phyllotreta striolata traditionally They are challenging to manage because was most commonly found in the northern they attack the crop at the seedling stage Parkland and Peace River regions of the when it is most vulnerable, can invade a Prairie provinces (Burgess, 1984). Recently, fi eld very quickly in huge numbers, can increased numbers of P. striolata have been cause irreversible plant damage in a short found in areas where P. cruciferae once time (Lamb, 1984), and their occurrence dominated (Soroka et al., 2008; Soroka, and movements are diffi cult to forecast 2011). This may be due to decreased (Burgess, 1977a). mortality of the striped species to the Phyllotreta cruciferae and P. striolata are neonicotinoid insecticides (Tansey et al., the principal species in a complex of eight 2008, 2009) present in all canola seed fl ea beetle species attacking canola in dressings currently registered in Canada to western Canada (Burgess, 1977a, 1981). control the beetles. Both species are present in all provinces Phyllotreta spp. are univoltine in except Newfoundland (Burgess, 1977a; western Canada, overwintering as adults Bousquet, 1991; C. Noronha, Charlotte- near the soil surface along shelterbelts, town, 2012, pers. comm.). Originating in headlands and in fi elds (Burgess, 1977a, Eurasia, P. cruciferae was fi rst found in 1984; Wylie, 1979). Emergence begins with North America in British Columbia in 1921 the fi rst extended period of warm weather

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 36 249

in April and May, with P. striolata adults al., 2008), primarily for control of emerging 1–4 weeks earlier than those of P. Phyllotreta spp. and often in a prophylactic cruciferae (Westdal and Romanow, 1972). manner. More insecticide is applied Peak emergence of P. cruciferae occurs annually for control of these pests than for when ground temperatures reach 15°C any other insects in the crop (Lamb and (Ulmer and Dosdall, 2006). Emerging Turnock, 1982; Madder and Stemeroff, beetles initially feed on winter annual 1988). If damage to seedlings exceeds 25% weeds or volunteer canola, and fl y to leaf area eaten, seed treatments may need newly seeded canola crops when daytime to be supplemented with foliar appli- temperatures exceed 14°C (Burgess, 1977a; cations of insecticides. Because of the Lamb, 1983). Females lay eggs in the soil speed of invasion, under high beetle near host plants from late May until early pressure and warm temperatures a treat- July (Westdal and Romanow, 1972; ment delay of 1–2 days can result in loss of Burgess, 1977a). The white, grub-like entire canola fi elds. larvae feed on root hairs and the surface of Some cultural control methods have a the taproot before pupating in earthen cells measure of success in management of near their host plant. The next generation Phyllotreta spp. Practices that encourage of adults emerges from late July to October rapid seedling emergence and good stand (Wylie, 1979), feeds, and moves to over- establishment such as sowing large seed wintering sites when temperatures decline. with a high germination capacity (Elliott et The host range of P. cruciferae is con- al., 2007, 2008) can alleviate damage from fi ned to the order Capparales, principally the insects in direct-seeded crops such as to the family Brassicaceae (Feeny et al., canola. Manipulation of seeding date 1970), which contains anionic glucosino- (Milbrath et al., 1995; Cárcamo et al., 2008; late compounds that can act as attractants Knodel et al., 2008), minimum or no tillage or deterrents (Chew, 1988; Louda and prior to seeding (Milbrath et al., 1995; Mole, 1991). In western Canada, canola Dosdall et al., 1999) and higher seeding and mustard, Brassica juncea (L.) Czern. rates (Philip and Mengersen, 1989; Dosdall (Brassicaceae), are the main cultivated et al., 1999; Dosdall and Stevenson, 2005; hosts of Phyllotreta fl ea beetles (Lamb and Cárcamo et al., 2008) can decrease damage Palaniswamy, 1990; Palaniswamy et al., to canola from Phyllotreta spp. In 1992; Pachagounder et al., 1998). Yellow cruciferous vegetable production, a well- mustard, Sinapis alba L. (Brasssicaceae), prepared seedbed and the use of large, exhibits resistance to fl ea beetle feeding, in vigorous transplants, fl oating row covers or part because of the presence of the other screening methods, destruction of deterrent glucosinalbin in the seedlings Phyllotreta spp. in more-preferred, nearby (Bodnaryk, 1991) and in part because of trap crops, or intercropping with non-hosts the tolerance of mustard seedlings to fl ea (Tahvanainen and Root, 1972) can reduce beetle injury (Bodnaryk and Lamb, 1991). the impact of Phyllotreta spp. feeding on Trichomes or plant hairs deter Phyllotreta their cruciferous hosts. spp. feeding (Lamb, 1980; Paliniswamy Host-plant resistance is a promising and Bodnaryk, 1994; Soroka et al., 2011). means of Phyllotreta spp. management. Canola lines with elevated trichomes can be as effective as insecticidal seed treat- 36.2 Background ments in protecting seedlings against Phyl- lotreta spp. damage (Soroka et al., 2011), Insecticidal seed treatment is the principal while introgression of genetic sources of means of Phyllotreta spp. control in Phyllotreta spp. resistance from S. alba into Canadian canola production. Currently susceptible crucifer germplasm has met more than 90% of the 6 million ha seeded with some success (Gavloski et al., 2000). to canola in North America is treated with Several native generalist predators neonicotinoid seed treatments (Soroka et occasionally feed on Phyllotreta spp., 250 Chapter 36

including adults of the fl ower beetle North latitude) (Hines and Hutchison, Collops vittatus (Say) (Coleoptera: Mely- 2011). ridae) (Gerber and Osgood, 1975), the big- Several species of Phyllotreta feed on eyed bug Geocorus bullatus (Say) crucifers in Europe (Carl and Sommer, (Hemiptera: Geocoridae) (Burgess, 1977b), 1975). The most common of these, P. the spined soldier bug Podisus maculi- undulata Kutsch. and P. chrysocephala (L.) ventris (Say) (Hemiptera: Pentatomidae) (Coleoptera: Chrysomelidae), do not occur (Culliney, 1986), damsel bugs Nabis in Canada. Phyllotreta striolata (=P. vittata alternatus Parshley and Nabicula Chen) and P. cruciferae are present but of americolimbata (Carayon) (Hemiptera: minor importance in Europe. Nabidae) (Burgess, 1982; Culliney, 1986), A survey for biological control agents of the fi eld cricket Gryllus pennsylvanicus Phyllotreta spp. in the 1970s in Austria, Bermeister (Orthoptera: Gryllidae) (Burgess Germany and Switzerland found four and Hinks, 1987) and larvae of the green species of nematodes and three species of lacewing Chrysoperla carnea (Stephens) braconid wasps attacking Phyllotreta spp. (Neuroptera: Chrysopidae) (Burgess, 1980). (Sommer, 1981). Although the over- However, predators appear to play a wintering generation of P. cruciferae adults negligible role in population regulation of in Europe is sometimes heavily parasitized these pests in western Canada. (up to 90%) by the nematodes Howardula Morris (1985), examining the suscepti- phyllotreta Oldham (Tylenchida: Allanto- bility of P. cruciferae to the widely nematidae) and Hexamermis albicans distributed nematode Steinernema feltiae Steiner and Amphimermis elegans Kab. (Filipjev) (Rhabditida: Steinernematidae), and Imam. (Mermithida: Mermithidae), the concluded that, although the nematode overall impact of the nematodes on fl ea could kill adult P. cruciferae and reproduce beetle population survival is minor (Wylie in their bodies, it had little potential as a and Loan, 1984; Morris, 1987). Recently, biological control agent. In Manitoba, two isolates of entomopathogenic nematodes parasitic nematodes in the families have been found that are promising Mermithidae (Mermithida) and Allantone- candidates for the biological control of P. matidae (Tylenchida) were found on the striolata under fi eld conditions in China fl ea beetle complex in oilseed rape (Wylie, (Xu et al., 2010; Yan et al., 2013). 1984; Wylie and Loan, 1984), but neither of One of the three wasp species found in the nematodes is suffi ciently abundant to the European survey was rare and restrict populations of P. cruciferae or P. unidentifi ed, and one was indistinguish- striolata (Wylie et al., 1984). able from P. brevipetiolatus (Wylie and Five Nearctic euphorine wasp species in Loan, 1984). The third wasp, Townselitis the family Braconidae parasitize adults of bicolor (Wesmael) (Hymenoptera: crucifer-infesting Phyllotreta spp. (Wylie Braconidae), has 2–3 generations a year and Loan, 1984). One of these, Perilitus and was found to parasitize up to 50% of brevipetiolatus Thomson (=Microctonus Phyllotreta spp. adults (Wylie et al., 1984). vittatae Mueseback) (Hymenoptera: Townselitis bicolor attacks Phyllotreta spp. Braconidae), is the only common native more aggressively and oviposits more parasitoid, and possibly the only native rapidly than does P. brevipetiolatus, and parasitoid of P. cruciferae and P. striolata in therefore was considered to be a suitable Canada (Wylie and Loan, 1984). Pevilitis candidate for biological control. brevipetiolatus exerts a low level of biological control of these beetles, usually at an incidence of less than 5% in the 36.3 Biological Control Agents Canadian provinces (Wylie et al., 1984). However, the parasitoid is reported to be a In total, 1936 adults of T. bicolor from major biological control agent of P. striolata Europe and approximately 2639 Phyllo- in cole crops in the eastern USA north of treta spp. collected in Manitoba and the Mason–Dixon line (approximately 40° parasitized in the laboratory were released Chapter 36 251

in the summers of 1978–1983, with 24 producer’s canola fi eld near Grandview, releases at Glenlea, Manitoba (49.642°, Manitoba. Phyllotreta spp. were collected −97.119°) during 1978–1982 and two from the traps once or twice a week, releases at Grandview, Manitoba (51.052°, brought or shipped back to the laboratory, −100.586°) in 1982 and 1983 (Wylie, 1988). and reared on cabbage in a growth chamber set at 16:8 dark:light, 23–15°C until all the beetles had died. None of the 23 36.4 Evaluation of Biological Control parasitoids recovered from the 1836 Phyllotreta spp. beetles was T. bicolor Phyllotreta spp. were collected from the (Table 36.1). release site at Glenlea during 1979–1983 In an investigation of distribution of and again in 1985, and at Grandview in native parasitoids, Microctonus spp. 1983 and 1985, and maintained for numbers were monitored in a prairie-wide emergence of parasitoids (Wylie, 1988). survey of Phyllotreta spp. during 2008– Townesilitis bicolor was never recovered 2011. Five or ten yellow sticky card traps, (Wylie, 1988). In the laboratory T. bicolor 7.5×12 cm in dimension, were placed at the was found to oviposit readily in P. edge of newly seeded canola fi elds in spring striolata, but only occasionally in P. and replaced weekly, typically for 2–4 cruciferae (Wylie, 1983). The semi-annual weeks. A few locations were sampled dispersal of the host and parasitoid to and throughout the growing season. Number from canola fi elds scattered the population and species of fl ea beetles were counted, of parasitized beetles and made establish- and the presence of Microctonus spp. noted. ment, or at least detection of establishment, Microctonus spp. specimens were uncertain in the short term. The release identifi ed from 36 of 134 location-years programme was discontinued. sampled across the three prairie provinces In an effort to determine if T. bicolor had and North Dakota. In 12 of 14 sites from or had not established near the release Alberta, four of eight sites from Saska- sites, in June 2007 a survey was conducted tchewan, and four of ten sites from in which modifi ed mustard oil traps Manitoba from which Microctonus spp. (Soroka et al., 2005) were placed at the were collected, P. striolata was the most Glenlea Research Farm and adjacent to a numerous fl ea beetle surveyed at the site. In

Table 36.1. Microctonus sp. parasitism of crucifer-feeding fl ea beetles, Phyllotreta spp., collected from two locations in Manitoba, 2007. Gleanlea Grandview Flea beetles Parasitoids Flea beetles Parasitoids Date collected No. Date emerged No. Date collected No. Date emerged No. 4 June 87 25 June 3 6 June 55 6 July 1 6 July 1 4 August 1 11 June 232 27 June 1 8 June 12 0 6 July 3 15 June 62 6 July 2 22 June 328 13 July 2 20 July 5 23 July 1 4 August 1 20 August 1 18 June 159 15 July 1 29 June 114 0 22 June 168 0 6 July 372 0 26 June 16 0 29 June 231 0 Total 955 11 881 12 252 Chapter 36

one site from Alberta, four sites from Possible reasons for lack of establish- Saskatchewan, six sites from Manitoba and ment of T. bicolor in the 1970s and early three sites from North Dakota where 1980s may include the small number of Microctonus spp. were found, P. cruciferae parasitoids released at any one time predominated. In one Alberta site adults of (Wylie, 1988), poor synchrony of T. bicolor Psylliodes punctulata Melsheimer (Cole- with the life cycle of P. cruciferae (Wylie, optera: Chrysomelidae) were the most 1982), scattering of the parasitized numerous fl ea beetle caught on the traps, Phyllotreta spp. population in the autumn and in one site in North Dakota other fl ea and the preference for P. striolata, which beetles, Chaetocnema spp. (Coleoptera: was not present in large numbers at Chrysomelidae), were most numerous. Glenlea at the time of release (Wylie et al., Although sticky trap collection made 1984). identifi cation of Microctonus spp. diffi cult, all specimens appeared to be P. brevipetiolatus except for one M. pusillae 36.5 Future Needs Muesebeck collected from Avonlea, Saskatchewan, in 2009, and two M. Because populations of P. striolata have punctulatae Loan and Wylie (Hymenoptera: been increasing across western Canada in Braconidae) collected singly from Regan the last 10 years and because T. bicolor and Minot, North Dakota in 2010. wasps prefer to parasitize P. striolata The presence of native Microctonus spp. beetles over P. cruciferae congeners, future may have been underestimated because of work should include: the time of sampling. Although P. brevipetiolatus can have three to four 1. Re-investigation of T. bicolor as a poten- generations per year in southern Manitoba tial biological control agent of P. striolata (Wylie and Loan, 1984), in the current and, incidentally, P. cruciferae, including survey specimens were detected development of improved release methods principally in May–June, and/or September and releases of greater numbers of parasi- in the few locations that were surveyed all toids, which may make establishment of season. In surveys that extended parasitoids from Europe into North throughout the growing season, many more America more successful than in the past; Microctonus spp. were collected on traps 2. Investigation of higher temperatures in September than in spring (Fig. 36.1). and longer photoperiods as means of

150 134 25

20 2009 2011 15

10 Microctonus vittatae Microctonus 5 No. No.

0 4 Jun 18 Jun 13 Aug 27Aug 10 Sep 24 Sep

Sampling period

Fig. 36.1. Number of Microctonus spp. specimens collected from yellow sticky traps near a canola fi eld at Melfort, Saskatchewan, 2009 and 2011. Chapter 36 253 preventing diapause of immature wasps in Acknowledgements rearing, which could increase numbers available for release; Ian Wise, Cereals Research Centre, 3. Investigation of the potential for inter- Winnipeg, Manitoba, collected fl ea beetles specifi c competition between T. bicolor and from Glenlea in 2007. Funding for the fl ea P. brevipetiolatus to determine if introduc- beetle surveys was provided by the Alberta tion of T. bicolor will be detrimental to P. Canola Producers’ Commission, the brevipetiolatus populations; Saskatchewan Canola Growers’ Associ- 4. Examination of other potential classical ation, the Manitoba Canola Growers’ biological control agents from eastern Association, the Canola Council of Canada Europe and Asia; and Agriculture and Agri-Food Canada 5. Better understanding of the host/para- through the Canola Agriculture Research sitoid relationships to increase the effec- Program. The technical assistance of L. tiveness of parasitism of Phyllotreta spp. Grenkow is greatly appreciated. by nematodes.

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37 Plutella xylostella (L.), Diamondback Moth (Lepidoptera: Plutellidae)

Sadia Munir,1 Lloyd M. Dosdall,1 Juliana J. Soroka,2 Owen Olfert2 and Ruwandi Andrahennadi2 1University of Alberta, Edmonton, Alberta; 2Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

37.1 Pest Status its host plants are cultivated (Anonymous, 1996; Dosdall et al., 2004, 2011). In both The diamondback moth, Plutella xylostella eastern and western Canada, P. xylostella (L.) (Lepidoptera: Plutellidae), is globally re-establishes each year from annual distributed and a destructive oligophagous immigrations of adults borne on northward pest of Brassicaceae crops (Talekar and trajectory winds from the southern USA Shelton, 1993). Although P. xylostella is and Mexico; they can travel up to 1500 km, believed to have evolved in Africa (Kfi r, and consequently diamondback moth 1998) or China (Liu et al., 2000), North densities can vary considerably from year American populations are most probably of to year (Smith and Sears, 1982; Dosdall et European origin and were likely introduced al., 2004, 2008; Hopkinson and Soroka, about 150 years ago (Hardy, 1938). 2010). Plutella xylostella has been reported Plutella xylostella was fi rst reported to survive under mild winter conditions in from western Canada in 1885 (Harcourt, western Canada (Dosdall, 1994), but 1962), and it now occurs almost annually successful overwintering is considered a throughout the Canadian prairies wherever rare phenomenon (Dosdall et al., 2008).

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 37 257

In western Canada (Manitoba, Saska- canola, B. napus and B. rapa, in Canada tchewan, Alberta and British Columbia), tripled from 2.6–7.5 million ha during the canola, Brassica napus L. and Brassica period 1987–2011 (Canola Council of rapa L. and mustard, Brassica juncea (L.) Canada, 2011). Czern. and Sinapis alba L. (Brassicaceae) The pest status of P. xylostella in any are the primary host crops of P. xylostella given year is dependent primarily on its (Philip and Mengersen, 1989). In eastern arrival time from southern regions of North Canada (Ontario, Quebec, New Brunswick, America, the size of invading populations, Nova Scotia, Prince Edward Island, the number of population infl uxes and Newfoundland and Labrador), P. xylostella environmental and biological conditions in can be a serious pest of Brassicaceae crops the region of its invasion (Dosdall et al., (Madore, 2010), and in Newfoundland and 2008, 2011; Miluch, 2010). Harcourt (1954) Labrador P. xylostella can pose a threat to determined that 283 degree-days (DD) were survival of some endemic Brassicaceae required for completion of one generation (Squires et al., 2009). Plutella xylostella of P. xylostella using a developmental can also feed and develop on many threshold of 7.3°C. An early arrival time of Brassicaceae weeds that are common in invading adults could enable completion of agricultural cropland across the country more generations of this multivoltine (Sarfraz et al., 2011). species than a later invasion. Usually three In most years P. xylostella causes minor generations per year occur in Alberta economic damage, but in some years (Philip and Mengersen, 1989) and four to populations reach outbreak densities and fi ve in Ontario (Harcourt, 1990). Under extensive crop losses occur (Dosdall et al., Canadian fi eld conditions, the average 2011). For instance, in 1995, this insect times for development from 1st to 4th caused substantial crop damage in western instar are 4.0, 3.6, 3.4 and 4.2 days Canada and in Quebec, with estimated (Harcourt, 1957). economic losses of at least CAN$40m to Other factors that affect the survival and CAN$50m (Braun et al., 2004). Outbreaks development of P. xylostella include host responsible for economic damage to canola plant genotype and quality. Among com- and mustard in western Canada have mercial crop species that included B. occurred approximately every 2–3 years napus, B. rapa, B. juncea, S. alba, Brassica since 1995, but the frequency of economic- oleracea L. and Brassica carinata Braun ally damaging densities is not correlated (Brassicaceae), Sarfraz et al. (2007) deter- with increases in the area devoted to mined that P. xylostella most preferred to canola production (Dosdall et al., 2008). oviposit on plants of S. alba, probably There are several factors responsible for because of its preference for the rather the signifi cant pest status of P. xylostella glossy leaf surface of this host plant and its and the severe economic losses it can cause higher concentrations of aromatic gluco- to Brassicaceae crops in Canada. Its host sinolates. Larval and pupal development plants are abundant and widely distrib- was usually fastest on B. juncea and S. alba uted. Brassicaceae is a very diverse plant and slowest on B. oleracea and B. carinata family, grown in all Canadian agricultural (Sarfraz et al., 2007). Among Brassicaceae regions and includes many indigenous weed species, survival of P. xylostella was species as well as invasive weeds (Warwick highest on wild mustard, Sinapis arvensis et al., 2003). Plutella xylostella populations L., and wormseed mustard, Erysimum can increase rapidly due to their high cheiranthoides L., and lower on shepherd’s reproductive potential (Talekar and purse, Capsella bursa-pastoris (L.) Medik. Shelton, 1993). The area devoted to Bras- (Sarfraz et al., 2011). Flixweed, Descurainia sicaceae crops has increased dramatically sophia (L.) Webb ex Prantl (Brassicaceae), in Canada during recent decades, and this was a poor host for P. xylostella in terms provides a resource readily exploited by P. of pre-imaginal developmental biology xylostella. For instance, production area of (Sarfraz et al., 2010). 258 Chapter 37

The preference and performance of P. Gujar, 2005), but Btk is not registered for xylostella is also affected by host plant application to canola in Canada (Dosdall et quality (Furlong et al., 2013). Females al., 2011). Canola genetically modifi ed to select plants for oviposition on which pre- express the cry1Ac gene of Bacillus imaginal survival of their offspring is thuringiensis is effective for minimizing greatest and larval development is fastest plant damage from P. xylostella attack (Sarfraz et al., 2009). Intermediate levels of (Ramachandran et al., 2000; Mason et al., fertility, rather than low or high levels, are 2003); however, Bt-canola crops are not optimum for survival and development of currently registered in Canada or else- immatures, pupal weight, and longevity of where. adults (Sarfraz et al., 2009). Populations of Some cultural practices have been P. xylostella within commercial canola proposed to enhance integrated manage- fi elds are often aggregated, especially dur- ment of P. xylostella. If spring invasions of ing early fl owering (Ulmer et al., 2005; P. xylostella occur before crop emergence, Sarfraz et al., 2010). Plutella xylostella tillage can reduce populations of bras- fi eld distributions are signifi cantly associ- sicaceous weeds and volunteer canola, and ated with some nutrients (nitrogen, sulfur so reduce establishment success of the fi rst and potassium) in canola leaf tissues generation of P. xylostella (Agriculture and (Sarfraz et al., 2010). Agri-Food Canada, 2005). Sarfraz et al. (2007, 2009) found that plants responded to P. xylostella herbivory by increasing root 37.2 Background mass development. Root mass changes associated with infestation by P. xylostella Plant damage by P. xylostella is caused by larvae varied with plant genotype (Sarfraz larval feeding. Leaf tissues between the et al., 2007) and with soil fertility level upper and lower epidermal layers are (Sarfraz et al., 2009), and consequently the mined by 1st instar larvae (Harcourt, 1957), authors proposed that optimal levels of and the remaining three instars feed on fertility be maintained to improve plant upper surfaces of leaves, buds, fl owers, compensation following attack by this pest. stems, siliques and developing seeds The greater attractiveness of S. alba to (Anonymous, 1996). Control of P. xylostella ovipositing females of P. xylostella (Sarfraz infestations is achieved through chemical, et al., 2007) suggests an opportunity for cultural and biological means. using S. alba as a trap crop, but this has Application of insecticide is the not been tested under fi eld conditions. principal strategy for control of P. xylostella. Organophosphate and pyr- ethroid compounds are registered in 37.3 Biological Control Agents Canada for P. xylostella control (Western Committee on Crop Pests, 2010); foliar More than 135 parasitoid species have application is recommended for canola at a been recognized worldwide to attack nominal threshold of 25 to 33% defoliation different life stages of P. xylostella (Delvare, in the seedling and rosette stages, and at 2004). In Canada, three parasitoid species, larval densities of 100 to 150 m−2 when the Diadromus subtilicornis (Gravenhorst), crop is in early fl ower. The recommended Diadegma insulare (Cresson) (Hymen- economic threshold is 200 to 300 larvae optera: Ichneumonidae) and Microplitis m−2 when the crop is in pod development plutellae (Muesebeck) (Hymenoptera: (WCCP, 2010). Foliar application of the Braconidae), attack larval, pupal and pre- bioinsecticide Bacillus thuringiensis pupal stages of P. xylostella (Harcourt, Berliner serovar kurstaki (Btk) (Bacillaceae) 1990; Anonymous, 1996; Braun et al., can be effective and less damaging to non- 2004; Dosdall et al., 2004). The larval target organisms than chemical insecticides parasitoids D. insulare and M. plutellae are (Talekar and Shelton, 1993; Kumar and the most effective species in North Chapter 37 259

America and are known to regulate P. Diadromus subtilicornis is a prepupal xylostella effectively in some cropping and pupal solitary parasitoid of P. xylo- systems and locations (Sarfraz et al., 2005). stella (Harcourt, 1960; Anonymous, 1996; Diadegma insulare is native to the Braun et al., 2004). It has often been reared Neotropics (Azidah et al., 2000). Its origins from P. xylostella (Braun et al., 2004; in western Canada are unknown, but it Dosdall et al., 2004), but little is known of likely migrates northward in spring along its biology in western Canada (Dosdall et with its hosts rather than overwintering, al., 2011). because diapause has not been shown in Surveys conducted in western Canada this species and at temperatures at or determined the greater importance of D. below 15°C it does not parasitize P. insulare and M. plutellae than D. xylostella (Monnerat et al., 2002). This subtilicornis for biological control of P. species can parasitize all four larval instars xylostella. Parasitism by D. insulare of P. xylostella, and the specifi c instar accounted for 30–45% mortality of its hosts parasitized can affect the sex ratio of in the early 1990s, but D. subtilicornis only offspring. More males than females are accounted for 15% parasitism (Braun et al., produced when 2nd instars are parasitized, 2004). In the early 2000s, the estimated but when 3rd and 4th instars are rates of parasitism pooled from four areas parasitized the progeny comprise a greater were 23% for M. plutellae, 17% for D. proportion of females than males (Fox et insulare and 5% for D. subtilicornis (Braun al., 1990; Monnerat et al., 2002). The et al., 2004). Such parasitism rates for D. mature larva of D. insulare emerges from insulare are relatively low compared to the prepupal stage of its host, and the some other regions of North America, parasitoid subsequently pupates within the where parasitism has been reported to silken cocoon of P. xylostella (Harcourt, sometimes surpass 50 and 80% for 3rd and 1960). The parasitoid appears to prefer 4th instar larvae, respectively (Lee et al., habitats with abundant food sources (Idris 2003; Hutchison et al., 2004). and Grafi us, 2001), especially sites with Some species of Chalcidoidea have been fl owering plants such as alyssum, associated with P. xylostella in western Lobularia maritima (L.) Desv. (Bras- Canada, but it is unclear whether these are sicaceae) (Johanowicz and Mitchell, 2000). primary parasitoids or hyperparasitoids. Field populations of D. insulare are often Conura albifrons (Walsh) and Conura aggregated, with distributions that correlate torvina (Cresson) (Hymenoptera: Chalci- with host populations and with content of didae) were recorded from P. xylostella in sulfur in canola leaf tissues (Ulmer et al., Saskatchewan and Alberta, respectively, 2005; Sarfraz et al., 2010). and Pteromalus semotus Walker (Hymen- Microplitis plutellae is a primary larval optera: Pteromalidae) from Alberta in 2001 endoparasitoid with a transcontinental (Braun et al., 2004). Two hyperparasitoids distribution in North America (Harcourt, of D. insulare, Catolaccus cyanoideus 1960; Braun et al., 2004; Sarfraz et al., Burks and Catolaccus aeneoviridis 2005). Females can parasitize all four larval (Girault) (Hymenoptera: Pteromalidae), instars of P. xylostella, and they emerge were also identifi ed in 2003 from canola in from 4th instars (Sarfraz et al., 2005). Alberta (Ulmer et al., 2005). Microplitis plutellae can undergo diapause, enabling it to overwinter in western Canada and to be present early in the 37.4 Evaluation of Biological Control season to parasitize diamondback moth (Putnam, 1978). Although populations of Biological control of P. xylostella was M. plutellae in canola can be aggregated, investigated to determine the species this behaviour appears inconsistent and composition, distribution and percentage not related to canola leaf tissue nutrient parasitism of important parasitoid species levels (Sarfraz et al., 2010). of P. xylostella in southern and central 260 Chapter 37

Alberta during 2010 and 2011 and in 37.5 Future Needs Saskatchewan in 2010. Plutella xylostella larvae and pupae were collected from Future work should include: commercial fi elds of canola or mustard 1. Conducting annual surveys of different with sweep nets and by hand-picking host crops and geographical areas to deter- specimens from host plants. In 2010, mine changes in parasitoid species compo- specimens were collected from six sites in sitions and population densities over time central and southern Saskatchewan. Para- and space; sitism levels were high and ranged from 82 2. Obtaining a more detailed under- to 96%, and D. insulare, D. subtilicornis, standing of the biology of the parasitoid Mesochorus sp., Itoplectis conquisitor (Say) fauna of P. xylostella in western Canada; and Itoplectis quadricingulata (Provancher) 3. Determining the importance of provid- (Hymenoptera: Ichneumonidae) were pre- ing natural sources of nectar in the form of sent. Data were obtained from 11 locations fl owering plants to enhance the effective- in southern Alberta, and a Cotesia sp. ness and conservation of P. xylostella natu- (Hymenoptera: Braconidae) was the ral enemies; dominant parasitoid, responsible for 92% 4. Determining the predator assemblage of parasitism, followed by D. insulare, which P. xylostella, and their roles in reducing was responsible for 7.1% parasitism. In populations of the pest; central Alberta in 2010 parasitism of P. 5. Developing an effective monitoring xylostella by these two larval parasitoid system for P. xylostella natural enemies to species was comparatively low (41% refi ne forecasting of risks associated with collectively). pest infestations; In 2011 a survey of P. xylostella 6. Determining the importance of various parasitism was conducted at 12 locations cultural practices such as trap cropping, in central and southern Alberta. Collective weed management and intercropping for parasitism by the three larval parasitoid enhancing natural enemies of P. xylostella; species D. insulare, Cotesia sp. and M. 7. Determining the developmental biology plutellae ranged from 80 to 36%. The of D. insulare at constant and fl uctuating dominant parasitoid species was D. temperatures so that data can be used to insulare. A facultative hyperparasitoid of develop a bioclimatic model to predict ichneumonids and tachinids, Mesochorus regions of the country capable of sustaining bilineatus Thomson (Hymenoptera: population development of this principal Ichneumonidae), was identifi ed as a parasitoid of P. xylostella. primary parasitoid of P. xylostella. Diadromus subtilicornus accounted for 65, 40 and 13.2% parasitism in fi elds near Medicine Hat, Orion and Etzikom, Acknowledgements respectively. A Conura sp. was also responsible for a low level of parasitism Sincere appreciation is extended to Dr A. (9.3%) from central Alberta in 2011. Bennett of Agriculture and Agri-Food The role and mortality of P. xylostella Canada for identifying the Ichneumonidae caused by invertebrate predators is specimens. Funding for the diamondback unknown in western Canada, with the moth parasitoid surveys was provided by exception of Carabidae (Coleoptera). The the Canola Council of Canada and effective use of predators needs to be Agriculture and Agri-Food Canada through considered and evaluated for controlling P. the Canola Cluster Program. We thank K. xylostella (Polis et al., 1989). Van Camp for technical assistance. Chapter 37 261

References

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38 Sirex noctilio Fabricius (Hymenoptera: Siricidae)

Kathleen Ryan,1 Sandy M. Smith2 and Jean J. Turgeon3 1 Silv-Econ Ltd, Newmarket, Ontario; 2University of Toronto, Toronto, Ontario; 3Natural Resources Canada, Canadian Forest Service, Sault Ste Marie, Ontario

38.1 Pest Status S. noctilio is typically a secondary pest of Pinus spp. (Pinaceae) and is of little eco- Sirex noctilio Fabricius (Hymenoptera: nomic concern (Wermelinger and Thomsen, Siricidae) was fi rst detected in Canada in 2012), whereas in other introduced regions 2005 (de Groot et al., 2006), and it has had signifi cant economic impact in subsequent surveys indicate that it is introduced Pinus spp. plantations (Morgan established in much of southern Ontario and Stewart, 1966; Hurley et al., 2007). and a few locations in Quebec (Canadian Although Yemshanov et al. (2009) predict Food Inspection Agency, 2008; see Fig 1. in signifi cant losses as a result of this insect, Dodds et al., 2010; L. Shields, Ontario, CAN$86 to $254 million per year after 20 2012, pers. comm.). Since its detection, years, Dodds et al. (2010) note that S. there has been considerable debate about noctilio is currently functioning some- its potential impact in Canada. This debate where between a primary and secondary stems from its pest status elsewhere; in its pest in Pinus spp. stands in eastern North native range in Eurasia and northern Africa America. © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 264 Chapter 38

Sirex noctilio’s complex life history noctilio offspring. The mucus facilitates A. allows it to kill trees. Unlike native areolatum growth in the host tree (Boros, woodwasps, S. noctilio attacks living trees; 1968; Titze and Turnbull, 1970), and the it favours stressed, suppressed and fungus is essential for egg hatching and for declining ones but also attacks and kills larval development and nutrition healthy hosts (Rawlings, 1948; Morgan and (reviewed in Ryan and Hurley, 2012). Stewart, 1966; Neumann et al., 1987). It There fore when tree and climate con- has an obligate association with Amylo- ditions are favourable for fungal growth stereum areolatum (Chaillet ex Fries) offspring are larger, and when environ- Boidin (Amylostereaceae), a white rot mental conditions are poor egg eclosion fungus, which the female carries and can be delayed or larvae may be small nurtures within internal storage organs (Madden, 1981). (Gaut, 1969). The wasp also manufactures a Sirex noctilio usually completes its life phytotoxic mucus (Coutts and Dolezal, cycle in 1 year, although it can range from 1969). After a female S. noctilio oviposits 3 months in very warm climates to 2–3 into tunnels drilled into the sapwood of its years in cooler ones (Morgan, 1968; host tree, she drills an adjacent tunnel and Neumann and Minko, 1981). Development inoculates it with fragments of the fungal time is related to both ambient temperature symbiont, along with the phytotoxin and wood moisture; models estimate that (Coutts, 1969a; Coutts and Dolezal, 1969). the wasp’s development requires 2500 The fungus and mucus are thought to act in degree days above a threshold of 6.8°C combination to cause physiological stress (Madden, 1981). This suggests that the to the tree (Coutts, 1969a, b). These wasp will have a development time of 1 substances cause altered water balance year or more in Canada. Adults emerge within the needles, and impaired photo- between late June and late September in synthate translocation and respiration Ontario, with emergence peaking between within the tree; tree death may follow mid-July and late August (Ryan et al., (Coutts, 1969a; Fong and Crowden, 1973; 2012b). The adult lifespan is brief: males Madden, 1977; Madden and Coutts, 1979). live up to 12 days and females up to 5 days Symptoms of toxicity include foliar (Neumann et al., 1987). Adults are sexually chlorosis, reddening and senescence, mature at emergence and do not feed, occurring as early as 2 weeks after S. surviving on fat reserves (Taylor, 1981; noctilio attack (Coutts, 1969a; Ryan, 2011; Neumann et al., 1987). Immediately after Ryan et al., 2013). Sirex noctilio tends to mating, females begin searching for suit- show a higher oviposition density, pro- able host trees. Unmated females show a duces more mucus and manufactures a similar host location response (Madden, more potent phytotoxin than other wood- 1988); S. noctilio is facultatively partheno- wasp species, which allows it to kill trees genetic with unfertilized eggs producing (Spradbery, 1973, 1977). Sirex noctilio only males (Rawlings, 1953). favours Pinus spp. and most species are The potential fecundity of S. noctilio believed to be susceptible to the wasp (e.g. varies according to body size, ranging Morgan and Stewart, 1966; Spradbery and between 21 and 500 eggs per female Kirk, 1978). In its current North American (Madden, 1974; Zondag and Nuttall, 1977; range, S. noctilio has successfully attacked Neumann et al., 1987). Mean potential and completed development in Scots pine, fecundity estimates of 264 and 212 eggs per Pinus sylvestris L., red pine, P. resinosa female have been reported for populations Aiton, jack pine, P. banksiana Lambert, and in Europe and Australia, respectively white pine, P. strobus L. (Pinaceae) (Dodds (Spradbery, 1977; Neumann et al., 1987). In and de Groot, 2012; Ryan et al., 2012a). Ontario, females appear to be smaller and In addition to assisting with overcoming therefore less fecund (estimated average tree defences, the mucus and fungus are 111 eggs per female; K. Ryan, 2012, necessary for the development of S. unpublished results). Even in ideal Chapter 38 265

conditions females only lay, on average, Ibaliidae), which attack eggs and early 82% of their egg complement, with smaller instar larvae, and Rhyssa and Megarhyssa females laying an even smaller percentage spp. (Hymenoptera: Ichneumonidae), (Neumann and Minko, 1981). Egg and early which parasitize later larval instars (Taylor, larval mortality can occur as a result of 1976). Parasitoid species, representing all effective compartmentalization by the host three of these genera, are present tree or when growth of A. areolatum is throughout Canada, including S. noctilio’s lacking or insuffi cient (summarized in current range, where they parasitize native Neumann et al., 1987). Because females are woodwasps (Table 38.1). In the wood- parthenogenetic, high male:female sex wasp’s native range, Rhyssa persuasoria ratios can occur (Rawlings, 1953). When persuasoria (L.) (Hymenoptera: Ichneu- this happens, mate fi nding is diffi cult and monidae) and Ibalia leucospoides the reproductive potential would be leucospoides (Hochenwarth) (Hymen- lowered (e.g. Zondag and Nuttall, 1977; optera: Ibaliidae) account for the highest Iede et al., 1998; Hurley et al., 2008). parasitism in the siricid community at 34% Natural dispersal is estimated to be up and 22%, respectively (Spradbery and to 30–50 km year−1 (Haugen et al., 1990). Kirk, 1978). Ibalia leucospoides is abun- Healthy S. noctilio females can fl y an dant in S. noctilio-infested trees in Ontario, average of 30 km in 23 h in a fl ight mill accounting for a mean hypothetical (Villicide and Corley, 2008) and this fi ts parasitism rate of 19.8% in 60 trees; with the dispersal estimate of Haugen et al. Rhyssa lineolata (Kirby) (Hymenoptera: (1990). Movement of infested material Ichneumonidae) and R. persuasoria augments natural dispersal; life stages are persuasoria account for a further 2.2 and reported to be resistant to wood drying and 1.4%, respectively (Ryan et al., 2012b). In sometimes to chemical treatment (Haugen the conterminous USA Long et al. (2009) et al., 1990). Woodwasps oviposit directly report similar parasitism by I. leucospoides into the sapwood of the tree, thus, it can be (20.5% per tree), and R. lineolata and diffi cult to determine if material is infested Megarhyssa nortoni (Cresson) (Hymen- with immature stages of S. noctilio. optera: Ichneumonidae) collectively account for a further 1.3% parasitism per tree. In Ontario, parasitism by I. 38.2 Background leucospoides is generally uniform between tree species, stands and years, and there- The natural enemies of S. noctilio in its fore is expected to provide consistent native Eurasian range include several population control (Ryan et al., 2012b). hymenopteran parasitoid species, a para- The infective stage of the nematode sitic nematode and birds (Bedding and Deladenus (Beddingia) siricidicola Bedding Akhurst, 1978; Spradbery and Kirk, 1978; (Tylenchida: Neotylenchidae) parasitizes S. Spradbery, 1990). A cytoplasmic poly- noctilio eggs, sterilizing the adult females hedral virus has been identifi ed in S. (Bedding, 1968, 1972; Bedding and noctilio in Germany, however, it remains Akhurst, 1978). Deladenus siricidicola has unstudied (Talbot, 1977). Tree and stand two separate life cycles, a free-living conditions also have a strong infl uence on fungus feeding cycle and a parasitic cycle. S. noctilio populations (e.g. Neumann et The mycetophagous form of D. siricidicola al., 1987). In its present range in Canada, lives in the tracheids and resin canals of natural enemies currently function to limit the tree, feeding on S. noctilio’s fungal S. noctilio populations and stand con- symbiont A. areolatum; the parasitic form ditions can be expected to affect the wasp emerges when S. noctilio larvae are present populations locally. (Bedding, 1972). A female D. siricidicola of The most common hymenopteran the parasitic form breaches the woodwasp’s species known to parasitize S. noctilio larval integument and when the nematode include Ibalia spp. (Hymenoptera: strain is compatible with the woodwasp 266 Chapter 38

Table 38.1. Hymenoptera parasitoids of Sirex noctilio known from North America and Eurasia (Data from: Cameron, 1965; Taylor, 1976). Eurasia and Trans- Western Eastern northern Canada Canada Canada USA Africa Aulacidae Pristaulacus niger (Schukard) X Ichneumonidae Ibalia jakowlewi Jacobson X Ibalia leucospoides ensiger Norton XXX Ibalia leucospoides leucospoides (Hochewarth) X Ibalia montana Cresson XXX Ibalia rufi collis Cameron X Ibalia rufi pes drewseni Borries X Ibalia rufi pes rufi pes Cresson XX Megarhyssa emarginatoria (Thunberg) X Megarhyssa nortoni nortoni (Cresson) XX Megarhyssa nortoni quebecensis (Provancher) XX Odontocolon geniculatum (Kriechbaumer) X Pseudorhyssa rufi coxis (Kriechbaumer) X Rhyssa alaskensis Ashmead XX Rhyssa amoena (Gravenhorst) X Rhyssa crevieri (Provancher) XX Rhyssa hoferi Rohwer X Rhyssa howdenorum Townes X Rhyssa lineolata (Kirby) XX Rhyssa persuasoria persuasoria (L.) XXX Stephanidae Megischus sp. X Schlettererius cinctipes (Cresson) X

species and strain, the offspring of the in the haemocoel or the egg sheaths of the infective female nematode enter the wasp rather than the eggs so it is unlikely reproductive organs of the wasp just before to cause sterilization (Yu et al., 2009; Ryan the end of its pupation (Bedding, 1972). et al., 2012b). Williams et al. (2012) When S. noctilio females are parasitized, hypothesized that the reason why S. ovary and egg development are suppressed noctilio eggs were not sterilized by the and the remaining eggs contain juvenile nematode strain present in North America nematodes that are introduced into the tree is because of the presence of a develop- when the woodwasp attempts to oviposit. mental asynchrony between the two Deladenus siricidicola has been the focus organisms; the sterilizing D. siricidicola of most of the classical biological control juveniles may emerge too late, the wood- efforts throughout the introduced range of wasp’s egg sheath having hardened and the wasp in the southern hemisphere, some become impenetrable. The ‘North Ameri- of which have been highly successful can’ nematode strain could function as a (reviewed in Hurley et al., 2007). However, sub-lethal natural enemy if the presence of the infection rate and function of this the nematode in the wasp’s haemocoel natural enemy in S. noctilio populations in affects the performance of female S. the wasp’s native range are undescribed. noctilio. Nematode-sterilized S. noctilio Deladenus siricidicola is prevalent in S. females are often smaller and have reduced noctilio in Canada, being found in 38% of fat bodies (Bedding, 1972; Villicide and 1445 females wasps, however, it is found Corley, 2008). Because body size is Chapter 38 267

correlated with fecundity (Madden, 1974), include: appropriate site selection for and smaller females have less dispersal planting; timely thinning to maintain capacity (Villicide and Corley, 2008), non- optimal stocking density, with removal of sterilizing nematode infection could still suppressed, deformed, diseased or dying have a negative effect on S. noctilio trees; thinning outside of the insects’ fl ight populations if they caused a similar season, i.e. in late autumn and winter; difference in body size. minimizing tree injury; and early salvage of Bird predation augments S. noctilio trees damaged by thinning or natural mortality caused by invertebrate natural causes (Neumann et al., 1987; Madden, enemies; woodpeckers (Piciformes: Picidae) 1988; Dodds et al., 2010). attack larval woodwasps within the sapwood and aerial predators attack the fl ying adults. Predation by woodpeckers in 38.3 Biological Control Agents the wasp’s native range is estimated to account for 6% of larval mortality (Sprad- To date, research about S. noctilio in bery, 1990). Aerial predators are reported Canada has focused on examining the to attack mating swarms where they feed community of natural enemies and on the adult S. noctilio as well as disrupt competitors of S. noctilio already present mating, resulting in higher male:female in its Canadian range, and on determining ratios in subsequent years (Madden, 1982). to what degree these organisms function to Although there has been no investigation limit the woodwasp’s population (e.g. Yu et of bird predation in Canada, these al., 2009; Ryan et al., 2012a, b). As predators are expected to be part of the described in the previous section, there is natural enemy complex here. Woodpecker strong evidence that both ibaliid (egg) and activity, often extensive, is seen in S. rhyssine (larval) parasitoids are currently noctilio-infested trees (K. Ryan, 2012, parasitizing S. noctilio in its present range unpublished results). in Ontario and New York State, and I. Sirex noctilio favours trees that are leucospoides appears to be the woodwasp’s suppressed, or physiologically stressed by primary natural enemy (Ryan et al., 2012b). drought, nutritional deprivation, patho- There is also evidence that subcortical gens, or other insect pests (e.g. Neumann et beetles interact with the wasp and have a al., 1987). Poor silviculture, resulting in negative effect on S. noctilio populations overstocking and thus an abundance of (Ryan et al., 2012a). These interactions suppressed and stressed trees in a stand, is may be mediated, at least in part, by the cited as a main factor in outbreaks fungal associates of the insects; some (Neumann et al., 1987; Madden, 1988; beetle-vectored species of blue stain Dodds et al., 2010). Sirex noctilio can also fungus, e.g. Leptographium wingfi eldii M. exploit short-term stressors including Morelet and Ophiostoma minor mechanical damage during management (Hedgecock) H. and P. Sydow (Ophiosto- operations, weather-event related tree mataceae), outcompete S. noctilio’s fungal injury, herbicide use, cone harvesting or symbiont, and there is evidence that the stand thinning, especially when these presence of these blue stain species deter events occur during the insect’s fl ight S. noctilio oviposition activity (Ryan et al., season (summarized in Madden, 1988). An 2011, 2012c). The effect of non-sterilizing abundance of S. noctilio-favourable trees in nematodes on S. noctilio is less clear, and a stand can lead to a local build-up in research has been initiated to begin to woodwasp populations; the wasps sub- address this question. The development of sequently attack healthier trees, severely PCR-RFLP methods for distinguishing D. stressing them and predisposing them to siricidicola isolates in North America has future attack (Madden, 1968, 1975). recently been completed (Leal et al., 2012). Silvicultural management recommendations Deladenus siricidicola has been, and to maintain S. noctilio at endemic levels continues to be, the central focus of 268 Chapter 38 classical biological control efforts con- 38.4 Evaluation of Biological Control ducted in most of the introduced range of S. noctilio in the southern hemisphere To date, no biological control agents have (Bedding, 1993; Hurley et al., 2007; been released for S. noctilio in Canada. Slippers et al., 2012). Soon after the discovery of S. noctilio in North America, D. siricidicola was considered as a 38.5 Future Needs biological control option in the USA as well (Williams et al., 2012). The Future work should include: mycetophagous life cycle of D. siricidicola facilitates its mass production as a bio- 1. Developing more effective sampling and logical control agent since it can persist in survey tools and methods to continue mon- this cycle in culture for several generations itoring of populations and for range exten- (Bedding, 1993). Results are highly suc- sions; cessful in some regions, e.g. 75% to close 2. Confi rming the ubiquity and impact of to 100% infection in Australasia, but S. noctilio parasitoids and parasites in control with the nematode is poor in other Canada to better assess their potential for areas, e.g. KwaZulu-Natal, South Africa biological control; <10% (reviewed in Hurley et al., 2007). 3. Investigating why the strain(s) of D. siri- Wood moisture is thought to be a key cidicola present in North America do(es) factor inhibiting infection, and this is not sterilize S. noctilio eggs to inform infl uenced by climate; KwaZulu-Natal future research about nematode biological receives most of its precipitation in the control should it become necessary; summer unlike Australasia, where the 4. Investigating D. siricidicola sterilization methodology was developed, which rates in Eurasia to clarify the need for the receives more precipi tation in the winter nematode to function as a sterilizing agent (Hurley et al., 2008; Slippers et al., 2012). in North America; Soon after the discovery of S. noctilio in 5. Determining how subcortical insect New York State in 2004, and prior to the competition affects S. noctilio populations discovery of the presence of the ‘North may elucidate further management options American’ nematode strain, controlled and could result in novel pest management release experiments with D. siricidicola strategies; began in the USA (Williams and Mastro, 6. Investigating overwintering mortality of 2008). Early investigators assumed that it S. noctilio and its invertebrate natural ene- would be relatively simple to adapt the mies, as well as the effect of natural, fl uctu- techniques developed in Australasia to ating, temperature conditions on the North America (Williams et al., 2012). wasp’s development, to forecast population However, climatic differences affecting the density and thus the need for biological timing of D. siricidicola application, the control in new ranges or changing climate potential for non-target effects on native conditions; woodwasps and other wood-boring 7. Vigilance against further introductions insects, as well as com petition or because they may result in introductions of hybridization with the ‘North American’ more vigorous strains of A. areolatum and nematode strain are areas for further consequently bigger wasps with greater investigation before releases can be made reproductive abilities, thus affecting its (Williams et al., 2012). future pest status. Chapter 38 269

References

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Spradbery, J.P. (1973) A comparative study of the phytotoxic effects of siricid woodwasps on conifers. Annals of Applied Biology 75, 309–320. Spradbery, J.P. (1977) The oviposition biology of siricid woodwasps in Europe. Ecological Entomology 2, 225–230. Spradbery, J.P. (1990) Predation of larval siricid woodwasps (Hymenoptera: Siricidae) by woodpeckers in Europe. The Entomologist 109, 67–71. Spradbery, J.P. and Kirk, A.A. (1978) Aspects of the ecology of siricid woodwasps (Hymenoptera: Siricidae) in Europe, North Africa and Turkey with special reference to the biological control of Sirex noctilio F. in Australia. Bulletin of Entomological Research 68, 341–359. Talbot, P.H.B. (1977) The Sirex-Amylostereum-Pinus association. Annual Review of Phytopathology 15, 41–54. Taylor, K.L. (1976) The introduction and establishment of insect parasitoids to control Sirex noctilio in Australia. Entomophaga 21, 429–440. Taylor, K.L. (1981) The sirex woodwasp: ecology and control of an introduced forest insect. In: Kitching, R.L. and Jones, R.E. (eds) The Ecology of Pests: some Australian Case Studies. CSIRO, Australia, pp. 231–248. Titze, J.F. and Turnbull, C.R.A. (1970) The effect of club gland secretions of Sirex noctilio on the growth of the symbiotic fungus Amylostereum areolatum. Australian Forest Research 4, 27–29. Villicide, J.M. and Corley, J.C. (2008) Parasitism and dispersal potential of Sirex noctilio: implications for biological control. Agricultural and Forest Entomology 10, 341–345. Wermelinger, B. and Thomsen, I.M. (2012) The woodwasp Sirex noctilio and its associated fungus Amylostereum areolatum in Europe. In: Slippers, B., de Groot, P. and Wingfi eld, M.J. (eds) The Sirex Woodwasp and its Fungal Symbiont: Research and Management of a Worldwide Invasive Pest. Springer, Dordrecht, the Netherlands, pp. 65–80. Williams, D.W. and Mastro, V. (2008) Evaluation of Beddingia siricidicola as a biological control agent of Sirex noctilio in North America. In: McManus, D. and Gottschalk, K.W. (eds) Proceedings. 19th US Department of Agriculture Interagency Research Forum on Invasive Species 2008; 8–11 January 2008; Annapolis, Maryland. Gen. Tech. Rep. NRS-P-36. Department of Agriculture, Forest Service, Northern Research Station, Newtown Square, Pennsylvania, pp. 85–86. Williams, D.W., Zylstra, K.E. and Mastro, V.C. (2012) Ecological considerations in using Deladenus (=Beddingia) siricidicola for the biological control of Sirex noctilio in North America. In: Slippers, B., de Groot, P. and Wingfi eld, M.J. (eds) The Sirex Woodwasp and its Fungal Symbiont: Research and Management of a Worldwide Invasive Pest. Springer, Dordrecht, the Netherlands, pp. 135–148. Yemshanov, D., McKenney, D.W., de Groot, P., Haugen, D., Sidders, D. and Joss, B. (2009) A bioeconomic approach to assess the impact of an alien invasive insect on timber supply and harvesting: a case study with Sirex noctilio in eastern Canada. Canadian Journal of Forest Research 39, 154–168. Yu, Q., de Groot, P., Leal, I., Davis, C., Ye, W. and Foord, B. (2009) Characterization of Deladenus siricidicola (Tylenchida: Neotylenchidae) associated with Sirex noctilio (Hymenoptera: Siricidae) in Canada. International Journal of Nematology 19, 23–32. Zondag, R. and Nuttall, M.J. (1977) Sirex noctilio Fabricius (Hymenoptera: Siricidae). Forest and Timber Insects in New Zealand No. 20. New Zealand Forest Service. 272 Chapter 39

39 Sitodiplosis mosellana (Géhin), Orange Wheat Blossom Midge (Diptera: Cecidomyiidae)

John F. Doane,1 Owen O. Olfert,1 Robert H. Elliott,1 Scott Hartley2 and Scott Meers3 1Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 2Saskatchewan Ministry of Agriculture, Regina, Saskatchewan; 3Alberta Agriculture and Rural Development, Brooks, Alberta

39.1 Pest Status of the wheat-growing area of the northern Great Plains (Olfert et al., 2011). Sitodi- The orange wheat blossom midge, plosis mosellana also occurs in wheat- Sitodiplosis mosellana (Géhin) (Diptera: growing areas of Nova Scotia, Ontario, Cecidomyiidae), Palaearctic in origin, is Quebec, British Columbia and a number of believed to have been accidentally intro- the neighbouring US states. duced into North America in the early On the northern Great Plains, adults 1800s (Felt, 1912). It is a major pest of emerge over a 6-week period beginning in spring wheat, Triticum aestivum L., durum late June or early July. The highest wheat, Triticum durum Desf., triticale, × populations usually occur during the Triticale hexaploide Lart., and to a lesser second or third week of July. Adults are extent spring rye, Secale cereale L. relatively poor fl iers and may be distrib- (Poaceae), in the northern Great Plains, uted over long distances by thermal including the Canadian prairies (Olfert et updrafts and wind. They are diffi cult to al., 2009). Sitodiplosis mosellana is widely detect during the day because they remain distributed in many parts of the world within the crop canopy, close to ground where wheat production occurs, especially level where it is more humid. Females between the 42nd and 62nd parallels become more active in the evening. Most (Affolter, 1990). In western Canada, S. egg laying occurs at dusk when conditions mosellana was fi rst reported in Manitoba are calm and temperatures are above 10– (Fletcher, 1902) but was not considered to 11°C. Females live 3–7 days and lay an be a pest until the 1950s (Allen, 1955). In average of 80 eggs underneath the glumes 1983, S. mosellana emerged as a major pest or on grooves on the fl oret surface. Eggs in north-east Saskatchewan (Olfert et al., are laid singly or in clusters of up to four 1985) and north-west Manitoba (Barker, eggs on the fl orets of emerging wheat 1984). The outbreak then spread through- heads. Larvae crawl into the fl oret and out most of Manitoba and Saskatchewan by feed on the kernel surface for 2–3 weeks. the early 1990s (Barker et al., 1995). The Mature larvae remain within their cast area of infestation in 2011 included much skin in the wheat head when conditions

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 39 273

are dry. Once moist conditions occur, properties. Small, lighter kernels are lost larvae drop to the ground, burrow into the during harvesting operations, resulting in soil, spin a cocoon and overwinter. The lower grain yield. following spring, further larval develop- ment depends on temperature and soil moisture; if con ditions are dry during May 39.2 Background and June, larvae remain dormant until the following year, if moist, larvae leave their Insecticide applications are recommended cocoons and move to the soil surface to when there is at least one adult midge for pupate. every four to fi ve wheat heads at several Traditional varieties of Canadian hard locations in the fi eld (Elliott, 1988a, b). red spring wheat, durum wheat and soft These are applied at dusk. spring wheat differ in their susceptibility Cultural practices are also an important to damage. The severity of damage management strategy (Elliott and Mann, depends on the synchrony between egg 1996). Continuous wheat cropping should laying and heading. Wheat heads are most be avoided to discourage build-up of S. susceptible to damage when egg laying mosellana populations. In areas where occurs during heading, at Zadoks growth populations exceed 1200 larvae m−2, stages 51–59 (Zadoks, 1974). Damage resistant crops, e.g. canola, Brassica napus declines dramatic ally when egg laying L. and B. rapa L. (Brassicaceae), fl ax, occurs after the anthers are visible. Wheat Linum usitatissimum L. (Linaceae), and varieties that head in late June and early legumes (Fabaceae) should be grown July usually have low damage because instead. Other cereal crops such as barley, heading and anthesis occur before high Hordeum vulgare L., oats, Avena sativa L., populations of S. mosellana are present. and annual canary grass, Phalaris Sitodiplosis mosellana populations may canariensis L. (Poaceae), can be grown exist at low levels for several years causing with little or no risk of S. mosellana minor crop losses. However, under damage. For low to moderate infestations, favourable con ditions, populations can damage can be reduced by selecting less exceed economic ally damaging levels susceptible varieties of spring wheat, plant- within 1 or 2 years. Moist conditions in ing early and at higher densities. These May and June favour larval development; practices promote uniform, advanced head- warm, calm conditions increase egg-laying ing to avoid high adult S. mosellana activity (Wright and Doane, 1987; Elliott populations. and Mann, 1996). Sitodiplosis mosellana Sitodiplosis mosellana-tolerant varieties, caused an estimated yield loss in spring with the Sm1 gene, have been introduced wheat of CAN$30m in Saskatchewan in to mitigate the lower yields and market 1983 (Olfert et al., 1985). grades caused by S. mosellana and they Injury is caused by S. mosellana larvae offer producers more fl exibility in crop feeding on the surface of developing rotations (Barker and McKenzie, 1996). kernels. Usually only some of the fl orets on The Sm1 gene prevents larvae from a wheat head are infested and the infest- establishing on developing seeds (Ding et ation level can vary from one to eight or al., 2000). Gene expression activates a more larvae per fl oret. If one larva develops natural response within seeds when larvae on a kernel, the surface is scarred and begin to feed by releasing ferulic and slightly depressed, resembling drought or p-coumaric acids at the feeding site. These frost injury. If three or more larvae develop acids return to normal levels at maturity within a fl oret, the kernel may abort or not and do not affect seed quality. Host-plant fi ll properly. Mature kernels from infested tolerance based on a single gene is often fl orets are cracked, shrivelled or deformed. short-lived due to genetic mutations that Damaged kernels that are harvested will occur in insect pest populations. To lower grain quality, i.e. milling and baking conserve the effectiveness of the Sm1 gene, 274 Chapter 39 new tolerant cultivars have been released 39.3 Biological Control Agents as a blend, containing a ratio of 90% resistant seed and 10% seed of a registered 39.3.1 Pathogens susceptible cultivar. The blend helps to prevent the development of resistant Although the impact of disease organisms mutations in midge populations by on S. mosellana mortality remains largely allowing suffi cient numbers of susceptible not quantifi ed, diseases, e.g. the fungus midge to survive and mate with midges Entomophthora brevinucleata Keller & that become resistant to the Sm1 gene. The Wilding (Entomophthoraceae) and entomo- susceptible cultivar also serves as a refuge pathogenic viruses, do not appear to be a and helps to conserve the parasitic wasp signifi cant mortality factor in most years Macroglenes penetrans (Kirby) (Hymen- (Affolter, 1990). optera: Pteromalidae). In Europe, S. mosellana is a pest of secondary importance (Meier, 1985), 39.3.2 Predators probably because of its numerous natural enemies. Affolter (1990) documented 27 In Europe, several predators attack adults, parasitoids. On the northern Great Plains, eggs and larvae of S. mosellana (Affolter, the European M. penetrans, introduced 1990). Spiders (Araneae) are known to with S. mosellana (Affolter, 1990), is capture adults; eggs are preyed upon by signifi cant in reducing infestations. A thrips (Thysanoptera); larvae in the wheat parasitized S. mosellana larva completes head are eaten by Coccinellidae (Cole- development and overwinters in the soil. optera) and Syrphidae (Diptera); and The next spring, the larval parasitoid larvae in or on the soil are eaten by consumes its host and emerges as an adult Carabidae and Staphylinidae (Coleoptera). in July. In western Canada, Floate et al. (1990) Emergence of adult M. penetrans was documented Carabidae as predators of S. evaluated in Saskatchewan (1991–2000) in mosellana. relation to accumulated degree-days (DD) (Elliott et al., 2011). Male wasps were found to emerge 1–2 days before the female 39.3.3 Parasitoids wasps. Accumulated DD above 9°C provided the most accurate estimates of In 1985, a study was begun to evaluate adult wasp emergence (10% at 450 DD; parasitoids that could be introduced to 50% at 503 DD; 90% at 579 DD). augment the biological control provided Deviations between observed and expected by M. penetrans. Affolter (1990) provided emergence were greatest at sites with either information on the host specifi city of low or high precipitation. In most individual parasites and showed that the instances, M. penetrans adults emerged parasitoid complex attacking S. mosellana 1–8 days earlier than expected at sites that is distinct from that associated with the received 20–40 mm rain in May and 1–11 related European pest, Contarinia tritici days later than expected at sites that (Kirby) (Diptera: Cecidomyiidae). As a received more than 145 mm rain in May result, Platygaster tuberosula Kieffer and and June. Forecast maps, based on DD Euxestonotus error (Fitch) (Hymenoptera: accumulations above 9°C, would assist Platygasteridae) were recommended for producers in monitoring their fi elds for the introduction. Females of both species presence of M. penetrans. Producers could lay their eggs in S. mosellana eggs or also adjust the timing, rate and placement early instar nymphs, and the parasitoid of sprays for control of S. mosellana to adults emerge from the host pre-pupae or protect and conserve the parasitoid. pupae. Chapter 39 275

39.3.4 Releases and recoveries Table 39.1. Mean parasitism of Sitodiplosis mosellana cocoons sampled in Saskatchewan and In Saskatchewan, P. tuberosula and E. error Alberta, 2001–2010, based on annual autumn were released within the canopy of spring surveys of larval cocoons. wheat fi elds heavily infested with S. Saskatchewan Alberta mosellana. Releases were timed to co- incide with occurrence of oviposition Cocoon Cocoon Year (no.) % (no.) % (July). The selected fi eld sites were at Wakaw (52.65°, −105.73°), Saltcoats 2001 206 45 34 16 (51.03°, −102.17°), Langenburg (50.83°, 2002 172 32 3 33 −101.70°) and Blaine Lake (52.83°, 2003 164 39 11 38 −106.88°). In total, 2022 Platygaster sp. and 2004 237 25 6 17 1397 E. error adults were released, the 2005 312 31 50 33 majority (1371 P. tuberosula; 1094 E. error) 2006 315 26 47 38 at Langenburg. From 1996 to 1998, approximately 2007 321 28 128 12 20,000 wheat heads were collected 2008 299 42 127 25 annually from commercial fi elds in the 2009 247 38 62 22 Langenburg release area, spread out in an 2010 338 46 133 12 even layer, and left at room temperature to dry after which they were threshed with a single-head thresher. Sitodiplosis mosel- lana larvae were separated from the seeds 49 wheat midge larval cocoons recovered, and chaff with a seed cleaner. The 16 (33%) were parasitized with M. harvested larvae were placed in a penetrans and 11 (22%) with P. tuberosula. vermiculite and sphagnum mixture, and So it appears that the two species are co- stored at 2°C for 5–6 months before existing, and could enhance the control of incubating the mixture at 22°C until no S. mosellana. more adults of S. mosellana or parasitoids emerged. Only three E. error were recovered in the year following the fi rst 39.5 Recommendations release. Adult P. tuberosula recovered in 1996, 1997, and 1998, were numbered 7, Further work should include: 21 and 23, respectively (Olfert et al., 2003). 1. Monitoring to determine establishment of E. error and spread of P. tuberosula; 2. Efforts to preserve the natural enemies 39.4 Evaluation of Biological Control to ensure that they continue to play a major role in regulating S. mosellana in western Macroglenes penetrans continues to play a Canada. lead role in regulating S. mosellana infestations in western Canada. The mean rates of parasitism in Saskatchewan ranged from 25 to 46% and from 12 to 38% in Acknowledgements Alberta for the years 2001–2010 (Table 39.1). Although its overall impact on S. The authors would like to acknowledge the mosellana populations still needs to be efforts of M. Braun for identifi cation of the quantifi ed, the introduction of P. tubero- parasitoid larvae, and the numerous col- sula to Saskatchewan was successful. In laborators over the past 10 years involved 2011, soil core samples from the in sampling wheat midge and its natural Langenburg release site revealed that of the enemies. 276 Chapter 39

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40 Sitona spp. Germar, Broad Nosed Weevils (Coleoptera: Curculionidae)

Héctor Cárcamo1 and Meghan Vankosky2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2University of Windsor, Windsor, Ontario

40.1 Pest Status Saskatchewan (Vankosky et al., 2009). All Sitona spp. consume plant foliage of The genus of broad nosed weevils, Sitona Fabaceae as adults, potentially reducing or (Germar) (Coleoptera: Curculionidae), has preventing crop establishment. As larvae, over 100 species worldwide (Bright, 1994; they feed on Rhizobium spp. (Rhizo- Bright and Bouchard, 2008). In Canada, biaceae) associated with root nodules there are six native and fi ve introduced (Johnson and O’Keeffe, 1981), which species that include a number of well- reduces nitrogen fi xation (Corre-Hellou and recognized crop pests. The adventive Crozat, 2005) and can reduce yield as Sitona lineellus (Bonsdorff) (= S. demonstrated by Vankosky et al. (2011a, b) scissifrons Say) (Bright, 1994; Bright and for S. lineatus. Bouchard, 2008) prefers lucerne, Medicago In general, the life cycle of Sitona spp. sativa L., but also attacks vetches, Vicia weevils is similar, although they differ in spp., including Vicia cracca L. and fi eld host preferences; S. lineatus will be used to peas, Pisum sativum L. (Fabaceae) (Loan, illustrate the life history of this genus. A 1963). Sitona fl avescens (Marshall) and S. detailed account of the morphology of S. hispidulus (Fabricius), both known lineatus can be found in Jackson (1920) commonly as the clover root curculio, can and in Bright (1994). Sitona lineatus is damage clover, Trifolium arvense L., T. univoltine and adults overwinter in a state pratense L. and T. repens L. (Fabaceae), of quiescence in fi eld margins or lucerne and lucerne crops (Soroka and Otani, 2009, fi elds (Jackson, 1920; Schotzko and 2011). Sitona cylindricollis (Fahraeus), the O’Keeffe, 1988). Feeding may occur during clover root weevil, is a key pest of sweet the overwintering period if temperatures clover, Melilotus offi cinalis (L.) Lamarck are mild (Murray and Clements, 1992). (Fabaceae) (Craig, 1978) and has severely During spring migration, S. lineatus adults limited its production in Canada (Bird, are oligophagous and will feed on various 1947). Sitona lineatus (L.), the pea leaf Fabaceae (Landon et al., 1995). No weevil, is an introduced pest of fi eld peas incidence of successful larval development (Vankosky et al., 2009; Cárcamo and has been quantifi ed on legumes other than Vankosky, 2011) and faba beans, Vicia faba fi eld peas or faba beans (Fisher and L. (Fabaceae) (Nielsen, 1990), which has O’Keeffe, 1979; Hoebeke and Wheeler, recently expanded its range from British 1985), although Hans (1959) stated that Columbia and the north-western USA into vetches are ‘equally suitable as brood the southern prairies of Alberta and plants.’ Female S. lineatus fed pea foliage

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 278 Chapter 40 can produce more than 3000 eggs over an populations in the soil (Anonymous, 2010). extended period (Schotzko and O’Keeffe, Suggestions for the integrated management 1988). Eggs are scattered on the ground or of S. lineatus in fi eld pea and faba beans laid in crevices near the base of seedlings are more extensive. These include using (Jackson, 1920). Larvae undergo fi ve instars winter peas as trap crops (Cárcamo and and feed on Rhizobium spp. in the root Vankosky, 2011), reduced tillage (Hanavan nodules (Jackson, 1920; Hamon et al., et al., 2008, 2010), irrigation (McEwen et 1984). Intraspecifi c competition for al., 1981) and intercropping with oats, nodules is considered a primary mortality Avena sativa L. (Poaceae) (Baliddawa, factor in S. lineatus (Nielsen, 1990; 1984). A number of insecticides are Vankosky et al., 2011a). Failure by 1st registered in Canada against Sitona spp. instar larvae to penetrate some soils under pests in forage crops, seed lucerne and dry conditions can be a second major pulse crops and are available in current mortality factor, as shown for S. hispidulus provincial guidelines. (Pacchioli and Hower, 2004). Upon An exhaustive survey of native natural maturity, larvae pupate in the soil and the enemies attacking Sitona spp. in Canada adults emerge to search for Fabaceae hosts remains to be done but the genus seems to to continue feeding. At this time they are support few parasitoid species and no oligophagous, and will feed on a variety of larval or egg parasitoids have been reported Fabaceae until late in the summer when in Canada (Table 40.1). Loan (1963) they migrate to permanent leguminous documented the biology of Microctonus crops such as lucerne or to fi eld margins to sitonae Mason (Hymenoptera: Braconidae), overwinter (Schotzko and O’Keeffe, 1988). a specialist parasitoid of S. lineellus near The entire development period from egg to Belleville, Ontario and during the same adult takes approximately 10 weeks study recorded Centistes lituratus (Hali- (Vankosky et al., 2009) and in southern day) (Hymenoptera: Braconidae) from S. Alberta in an average year, emergence of lineellus and Hyalomyiodes trianguliffera new adults begins in late July and peaks in Loew (Diptera: Tachinidae) from S. the fi rst half of August (H. Cárcamo, V. lineellus, S. fl avescens and S. hispidula. Herle and M. Vankosky, 2012, unpublished According to Loan (1969), M. sitonae is the results). only species of Nearctic Microctonus with a Sitona host. Vankosky (2010) found no evidence of adult or egg parasitism in S. 40.2 Background lineatus in southern Alberta. Several ground beetles including Pterostichus Sitona cylindricollis and S. lineatus are melanarius (Illiger) (Hamon et al., 1990) serious pests in sweet clover and in fi eld and Bembidion quadrimaculatum (L.) pea crops, respectively. Sitona lineellus, a (Coleoptera: Carabidae) (Vankosky et al., secondary pest of lucerne, is generally 2011c) prey on eggs of S. lineatus. maintained below damaging levels by Few other parasitoids of Sitona spp. timely cutting of forage lucerne (Harper et have been reported from other regions and al., 1990). In seed lucerne, S. lineellus is some of them have been released in Canada generally suppressed with insecticides and may be established as discussed below applied for other insects (Calvin, 2002). For (Table 40.1). In a survey of Mediterranean S. cylindricollis, agronomic recommenda- Sitona weevils found on Medicago spp. tions in sweet clover include sowing high (Fabaceae), Aeschlimann (1980) identifi ed quality, scarifi ed, seed into a fi rm seedbed fi ve parasitoids of adult Sitona including at less than 2.5 cm to promote even Pygostolus falcatus (Nees), Perilitus rutilus seedling emergence, planting fi elds as far (Nees), Perilitus aethiops Nees (=Microc- as possible from second year stands, and tonus aethiopoides (Loan) = Microctonus shallow cultivation of second year stands aethiops (Nees)), Allurus muricatus promptly after harvest to reduce weevil (Haliday) (Hymenoptera: Braconidae) and Chapter 40 279

Table 40.1. Parasitoids of Sitona weevils, native or introduced to Canada; their origin, distribution and host range. Taxa Origin [Distribution] Sitona spp. hostsa References Hymenoptera: Braconidae Perilitus aethiops Nees Palaearctic [Europe; S. cylindricollis, Loan (1971, 1975) [=Microctonus aethiopoides Canada (ON); USA (CA, S. discoideus, Aeschlimann (1980, Loan; Microctonus aethiops CT, DE, ME, MD, MI, S. fl avescens, 1986) (Nees)] NJ, OH, PA, RI, VA, S. hispidulus, VT, WV); Australia; S. lineellus, New Zealand] S. lineatus, H. posticab Microctonus sitonae Mason Nearctic [Canada (ON)] S. cylindricollis, Loan (1963, 1969) S. hispidulus, S. lineellus Microctonus secalis (Haliday) Palaearctic [Europe] S. fl avescens Jackson (1928) [= Perilitus cerealium Haliday] Allurus muricatus (Haliday) Palaearctic [Europe] S. lineatus Aeschlimann (1980) Pygostolus falcatus (Nees) [Europe; Canada (ON); S. lineatus Loan (1965), USA] Aeschlimann (1980) Perilitus rutilus (Nees) Palaearctic [Canada S. lineatus Aeschlimann (1980) (ON?c); Europe] Loan (1971) Centistes lituratus (Haliday) Holarctic [Canada (ON)] S. lineellus Loan (1963, 1971) Hymenoptera: Mymaridaed Anaphes diana Girault Palaearctic S. discoideus Aeschlimann (1980), [=Patasson lameerei Debauche] [Mediterranean, S. lineatus Aeschlimann (1986) Romania, Turkey, Syria, Bulgaria] Diptera: Tachinidae Hyalomyodes triangulifera Loew Nearctic [Canada: ON] S. lineellus Loan (1963) Microsoma exigua (Meigen) Palaearctic [Europe] S. lineatus, Aeschlimann (1980) [= Campogaster exigua Meigen] S. hispidulus aSitona species nomenclature as per Bright (1994) bH. postica = Hypera postica cEstablishment not evaluated dEgg parasitoids, all others attack adults

Microsoma exigua (Meigen) (= Campo- concentration of spores and the stage of S. gaster exigua Meigen) (Diptera: Tachnidae) lineatus that is exposed to the pathogen (Table 40.1). He also reported three mym- (Poprawski et al., 1985; Verkleij et al., arid egg parasitoids, including Anaphes 1992). Newly hatched larvae are more diana Girault (= Patasson lameerei susceptible to most fungal species than S. Debauche) (Hymenoptera: Mymaridae) that lineatus eggs (Poprawski et al., 1985), and occurred on both S. discoideus (= S. virulent Beauveria bassiana (Balsamo) humeralis Stephens) (not reported from Vuillemin (Cordycipitaceae) is effective North America; Bright, 1994) and S. against new generation adults with lineatus. A number of Allothrombium spp. mortality levels reaching 50% in 10 days (Trombidiformes: Trombidiidae) and (Müller-Kögler and Stein, 1970). The Anystis spp. (Trombidiformes: Anystidae) entomopathogenic nematodes Heterorhab- are also known to prey on Sitona eggs in ditis bacteriophora Poinar (Rhabditida: Europe (Aeschlimann, 1980). Heterorhabditidae), Steinernema carpo- Fungal pathogens and nematodes have capsae (Weiser) and Steinernema feltiae been investigated in Europe. The effi cacy (Filipjev) (Rhabditida: Steinernematidae) of fungal pathogens is dependent on the are all extremely effective against larval 280 Chapter 40

S. lineatus (Jaworska, 1998), with mortality (Loan, 1975) was established in southern reaching 100% in less than a week. Ontario from releases made in the 1960s Heterorhabditis bacteriophora is also able (Agriculture Canada, 1971) and has likely to penetrate the cuticle of adult insects spread throughout the agricultural regions (Bedding and Molyneux, 1982), making it of Canada via dispersal from the USA, effective against adults (Wiech and where it occurs widely, including the Jaworska, 1990). Unfortunately, their lack northern Great Plains. of host specifi city, high production and A large classical biological control effort application costs and climatic conditions has been on-going in New Zealand and in Canada have prevented the widespread Australia, primarily against S. lineellus (= use of nematodes (Vankosky et al., 2009). S. lepidus Gyllenhal) and S. discoideus. A Moroccan strain of M. aethiopoides with rather poor biological control attributes 40.3 Biological Control Agents was established in New Zealand but more effi cacious strains from Europe are Loan (1971) summarized the biological presently being considered for release control efforts directed mainly towards S. (Goldson et al., 2005; Phillips et al., 2008). cylindricollis in Canada; given the recent This parasitoid is effective in controlling S. invasion of the prairies by S. lineatus, it is discoideus in lucerne (Barlow and Gold- worth reviewing here. In 1952 and 1953, son, 1993). As part of these efforts, a partial M. exigua, Perilitus aethiops Nees and list of parasitoids attacking adult S. Perilitus rutilus (Nees) (Hymenoptera: lineellus from Europe and North America Braconidae) obtained from France and has been compiled (Phillips et al., 2000); largely reared on S. lineatus were released all of these species were known parasitoids near Portage La Prairie in Manitoba of Sitona spp. of economic importance in (49.9667°, −98.2667°) against S. cylindri- Canada (Table 40.1). collis, but were not recovered (Loan, 1961; Loan and Holdaway, 1961). In 1958, P. rutilus and Pygostolus falcatus (Nees) 40.4 Evaluation of Biological Control (Hymenoptera: Braconidae) from Sweden were released in larger quantities (up to Thus far, biological control of S. cylindri- 7000 females). These were reared largely collis in sweet clover has not been from S. lineatus, were released near successful. Based on post-release surveys, Brandon, Manitoba (49.8167°, −99.9167°) it appears that the parasitoids did not and were recovered in 1959 and 1960 but establish. The current status is diffi cult to not in subsequent annual surveys up to evaluate because no recent studies have 1964 (Loan, 1971). Pygostolus falcatus was been conducted on S. cylindricollis due to also released in smaller quantities (150:200 the reduction of sweet clover cultivation in males:females) near Belleville, Ontario the prairies in areas where the weevil is (44.1667°, −77.4167°) against S. lineellus problematic. Nevertheless, S. cylindricollis and recovered in 1961 and 1963–1964 from is still considered a key pest of sweet both the target and from S. cylindricollis, clover (Soroka and Otani, 2011), and a although at very low rates (Loan, 1971). recent attempt to include clover in a Another release of P. rutilus was done in dryland rotation near Lethbridge was 1958 in the Milk River Valley south of abandoned because of this pest (M. Davis, Lethbridge, Alberta (49.1°, −111.75°) for Lethbridge, Alberta, 2012, pers. comm.). management of Hypera postica (Gyllenhal) Biological control programmes for S. (Coleoptera: Curculionidae), but none was lineatus in Canada have yet to be initiated recovered in 1959 (Loan, 1958, 1971). and no parasitoid releases have been made Hypera postica is controlled in the USA by to date. In 2009, S. lineatus adults were the introduced M. aethiopoides (Coles and collected and sampled for parasitoids in Puttler, 1963). A strain of M. aethiopoides the Lethbridge and Vauxhall regions of Chapter 40 281 southern Alberta in May and July and Future work should include: sentinel eggs were exposed during the same time periods, but no evidence of 1. Effi cacy and host-specifi city testing in parasitism was observed (Vankosky, 2010). Canada for natural enemies such as P. fal- To our knowledge, no further attempts to catus that appears to preferentially para- identify parasitoids of S. lineatus have sitize S. lineatus in Sweden; been made in Canada. In laboratory con- 2. Searching for strains of species, e.g. M. ditions, the small and ubiquitous carabid aethoipoides, specifi c to S. lineatus, given beetle B. quadrimaculatum has been recent molecular tool developments show- shown to be an effective predator of S. ing the importance of strains from various lineatus eggs (Vankosky et al., 2011c) and hosts; is worth future study in the context of 3. Exploration for parasitoids of S. lineatus conservation biological control and inte- in more northern ranges, such as Russia grated pest management (IPM). and Kazakhstan; It is unlikely that any parasitoid with 4. Field trials to integrate conservation bio- high rates of success against S. logical control agents such as B. quadri- cylindricollis will be monophagous. maculatum egg predators with other IPM Therefore, the public and policy regulators strategies, e.g. the use of insecticide seed will need to come to terms with the fact treatments rather than blanket sprays of that some negative impacts on native foliage may enhance natural biological con- Sitona spp. are inevitable. However, any trol; measurable effects are likely to be minor 5. Studies on parasitoids of other Sitona relative to the benefi ts of an effi cient spp. such as S. cylindricollis as recom- biological control programme, which mended by Phillips et al. (2008), based on reduces insecticide inputs and reduces their fi ndings that geographic provenance losses due to the pest, thereby decreasing was less important than host species in costs to growers while preserving critical terms of determining genetic differences biodiversity and biodiversity-based among strains of M. aethoipoides – select- ecosystem services. ing species and strains of parasitoids from the same hosts as the target species will likely yield better results for biological 40.5 Future Needs control of this pest in North America; 6. Studies to increase the diversity of sus- As populations of S. lineatus continue to tainable crop and forage production sys- grow, in terms of size and range, so will the tems that require clover as part of the demand for effective biological control rotation, since advances in organic farm- options. Biological control programmes ing systems show that clovers are impor- should be considered a vital part of any tant as green manure to promote soil integrated pest management system, and to fertility and weed control (see Blackshaw date, our options are extremely limited. et al., 2001).

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41 Synanthedon myopaeformis (Borkhausen), Apple Clearwing Moth (Lepidoptera: Sesiidae)

Joan Cossentine,1 V. Marius Aurelian2 and Gary J.R. Judd1 1Agriculture and Agri-Food Canada, Summerland, British Columbia; 2Department of Biological Sciences, University of Alberta, Edmonton, Alberta

41.1 Pest Status Osoyoos and north Kelowna, at several locations in the Fraser Valley near Synanthedon myopaeformis (Borkausen) Vancouver, and in one orchard at Fingal, (Lepidoptera: Sesiidae), commonly called near London, Ontario (Beaton and Carter, apple clearwing moth (Alford, 2007), is an 2006). The fi rst and currently most important pest of commercial apples, extensive infestation of S. myopaeformis in Malus domestica Borkh. (Rosaceae), Canada is in the Similkameen Valley in throughout Europe (Dickler, 1976; Blaser British Columbia, where 50% of apple and Charmillot, 1984; Castellari, 1987; hectarage is under organic production (G. Sahinoglou et al., 1999; Kutinkova et al., Judd, 2012, unpublished results). A ground 2006) and eastern Mediterranean countries survey in 2008 found the species had as far south as Egypt and Jordan (Abd invaded 97% of the apple orchards within Elkader and Zaklama, 1971; Ateyyat and the Similkameen and in 39% of infested Al-Antary, 2006). In parts of Europe S. orchards more than 80% of the trees were myopaeformis is also known as the small infested. Pheromone trapping surveys in red-belted clearwing moth and sometimes 2009–2012 have shown that pest numbers infests apricot, Prunus armeniaca L., have continued to increase from 356 to 766 cherry, Prunus avium (L.) L., crabapple, moths per trap per season (G. Judd, 2012, Malus sylvestris Mill., hawthorne, Cratae- unpublished results). Synanthedon myo- gus spp., mountain ash, Sorbus americana paeformis has now spread south into Mars., pear, Pyrus communis L., plum, Washington State, USA (LaGasa et al., Prunus domestica L., and quince, Cydonia 2009) and randomly throughout the oblonga Mill. (Rosaceae) (Ateyyat, 2005; Okanagan valley in British Columbia. Ateyyat and Al-Antary, 2006). Populations of S. myopaeformis in The fi rst North American detection of S. Summerland and Penticton in 2012 were myopaeformis was in an organic apple almost 40-fold lower than those in the orchard in Cawston, British Columbia in Similkameen (British Columbia Ministry of the summer of 2005 (Philip, 2006). Sub- Agriculture and Lands, 2011). Interestingly, sequent pheromone trapping surveys by moths have been detected in orchards as the Canadian Food Inspection Agency far north as Armstrong but were absent (2012) detected moths in Keremeos, Oliver, from many orchards in Peachland, West

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 286 Chapter 41

Kelowna and Vernon that are located some level of control (Ciglar and Masten, between Summerland and Armstrong 1979; Van Frankenhuyzen and Wijnen, within the Okanagan valley (G. Judd, 2012, 1979; Kilic et al., 1988; Ateyyat and Al- unpublished results). Antary, 2006). Nematodes and Bacillus Phenology studies have suggested that S. thuringiensis Berliner (Bacillaceae) appear myopaeformis may have a 2-year life cycle to be the only entomopathogens evaluated in British Columbia with an 8–10 week as potential controls for European adult fl ight period each year arising from populations of S. myopaeformis (Deseo and trees infested with mixed, overlapping Miller, 1985; Kahounova and Mracek, cohorts of larvae (Judd, 2008; Judd et al., 1991; Shehata et al., 1999). Under fi eld 2009). In British Columbia, the moths fl y conditions entomo pathogenic nematodes from June through August whereas in can reportedly infect and suppress other Ontario the annual fl ight appears truncated Synanthedon spp. (Miller and Bedding, and ends by late July (Bedford and Judd, 1982; Cossentine et al., 1990; Cottrell and 2010). Female S. myopaeformis oviposit on Shapiro-Ilan, 2006; Shapiro-Ilan and damaged bark near graft unions and Cottrell, 2006; Bruck et al., 2008). Several pruning cuts. Emergent larvae bore into the studies have also reported that fi eld- tree and feed on cambial tissue within collected larvae of the currant clearwing tunnels usually located from below the moth, Synanthedon tipuliformis (Clerck) crown area up to the scaffold branches. (Lepidoptera: Sesiidae), were often infected Infestations are mainly found below the by the entomopathogenic fungus Beauveria graft union but a small percentage of larvae bassiana (Balsamo) Vuillemin (Cordy- are commonly found beneath the soil cipitaceae) (Scott and Harrison, 1979; surface (Bedford and Judd, 2010). In Baker, 1981; Hardy, 1982). Europe, infestations of S. myopaeformis In fi eld screening trials, Voerman et al. can reportedly cause a loss of tree vigour (1978) found that male apple clearwing and fruit yield (Dickler, 1976; Castellari, moths were attracted by 3Z,13Z- 1987). Although similar insect infestation octadecadienyl acetate, a common sesiid and tree health or yield data have not yet sex attractant (El-Sayed, 2009) that was been collected in Canada, it has been recently confi rmed as a female-produced observed that foliage of heavily infested sex pheromone for S. myopaeformis (Judd trees is sparse, trees appear stunted and et al., 2011). Research on the utility of this some die prematurely. Surveys in the sex pheromone for use in monitoring, mass Similkameen Valley have indicated trees trapping and disrupting mating of adult older than 3 years are infested, but damage populations is on-going (Aurelian, 2011). is heaviest on 5–8-year-old, high-density Although males were found to be attracted plantings of apple varieties Ambrosia and by the pheromone of the peach tree borer, Gala on M9, M26 and Ottawa 3 dwarfi ng Synanthedon exitiosa (Say) (Lepidoptera: rootstocks (Judd, 2008; British Columbia Sesiidae), orchard treatments with Iso- Ministry of Agriculture and Lands, 2011). mate®-P, a registered pheromone-based mating disruption product for peach tree borer were ineffective, possibly due to the extremely high densities of S. myo- 41.2 Background paeformis (Judd, 2008; Bedford and Judd, 2010). Swarms of S. myopaeformis fl y In Eurasia, non-chemical control strategies during the day and feed on damaged fruits for S. myopaeformis have included mass and various fl owering weeds (Eby, 2012). trapping (Trematerra, 1993; Bosch et al., Mass trapping studies demonstrated that 2001) and mating disruption of the adults 2-l plastic bottle traps baited with Concord (Steuber and Dickler, 1987; Kyparissoudas grape juice were highly attractive to both and Tsourgianni, 1993). Coating or wrap- male and female moths (Aurelian et al., ping the damaged bark also appears to offer 2012). Painting the traps yellow increased Chapter 41 287 their attractiveness to moths, resulting in several parasitoids and predators associ- the baited trap captures exceeding those of ated with or feeding on apple clearwing the pheromone traps (Judd, 2008; Aurelian, larvae. In 2007 and 2008 a dozen pupae 2011). were extracted from larval galleries near In 2008 three screening trials with the root–scion junction while assessing reduced-risk insecticides for conventional seasonal phenology of pupation and adult and organic apple production were estab- emergence. A number of solitary ecto- lished in a commercial high-density parasitoids were found attached to the mixed-variety apple planting in Cawston, exterior ventral side of recently formed British Columbia. Single pre-season trunk pupae between the wing buds and sprays were applied in May as curative abdomen. As the larval parasitoid grew the treatments targeting 2-year-old S. myo- clearwing pupae shrivelled and died. paeformis larvae. Effi cacy of treatments There was never more than one parasitoid was assessed by counting pupal exuviae on each pupa. The parasitoid was identi- protruding from tree trunks within a 25 cm fi ed as Pimpla varians (Townes) (Hymen- zone from the soil surface to just above the optera: Ichneumonidae) (A. Bennett, rootstock–scion graft union. Exuviae Ottawa, Ontario, 2012, pers. comm.). counts are equivalent to measuring adult emergence. Assessments were made on the same trees in August 2008 and 2009. In 41.3.2 Predators 2008, Rimon®, Belt® and entomo- pathogenic nematodes, Steinernema feltiae Aurelian (2011) also observed many (Filipjev) (Rhabditida: Steinernematidae), clearwing larvae being attacked and eaten in wet burlap and cardboard wraps at the external entry of larval galleries in appeared most promising as spring the spring by European earwigs, Forfi cula treatments, but Rimon® was the only auricularia (L.) (Dermaptera: Forfi culidae), material causing a signifi cant reduction in in organic apple orchards. Many adult adult emergence compared with untreated clerids, mostly the redbellied clerid, checks. In 2009, adult emergence con- Enoclerus sphegeus (Fabricius) (Cole- tinued to decline on trees treated once with optera: Cleridae), were captured in juice Rimon®. Entrust® was a weak control traps placed in organic apple orchards, and material appearing effective only as a at least one clerid larvae was found feeding summer treatment, and only in one out of on an apple clearwing larva in its gallery in two summer trials. Entrust® and Purespray 2007 (Aurelian, 2011). Green® summer oil are the only products currently registered for control of S. 41.3.3 Pathogens myopaeformis larvae in organic apples, although neither provides reliable control 41.3.3.1 Fungi (Bedford and Judd, 2010). Synanthedon myopaeformis larvae col- lected from apple orchards in Cawston, 41.3 Biological Control Agents British Columbia in 2009, were found to host a fungus subsequently identifi ed as 41.3.1 Parasitoids Metarhizium brunneum Petch (Clavi- cipitaceae) (Cossentine et al., 2010). Wild Larval stages of S. myopaeformis feed S. myopaeformis larvae collected from within the wood of the infested tree and infested apple trees and exposed to both M. pupae are found on the exterior end of the brunneum (apple clearwing moth isolate) feeding tunnel. While studying the biology and B. bassiana (isolate GHA) in the and conducting mass-trapping studies in laboratory, were found to be susceptible to organic apples in Cawston, British infection and dose-related mortality caused Columbia, Aurelian (2011) discovered by both fungi. Metarhizium brunneum and 288 Chapter 41

B. bassiana applied at 1×106 spores ml−1 41.4 Evaluation of Biological resulted in mean larval mortalities of 73– Control 76% at 7 days after treatment, respectively, and 91% mortality 14 days after treatment Both fungal isolates may have potential for (Cossentine et al., 2010). fi eld suppression of S. myopaeformis, although it has yet to be demonstrated that exterior trunk treatment with the fungi will 41.3.3.2 Nematodes result in host infections. It is unclear how Commercially obtained Heterorhabditis entomopathogenic nematodes may result bacteriophaga Poinar (Rhabditida: Hetero- in reliable orchard biological control due rhabditidae) (Biobest Biological Systems, to the apparent inability of the infective Leamington, Ontario) and Steinernema juveniles to reach larvae in deeper tunnels carpocapsae (Weiser) (Rhabditida: Steiner- within infested trees. Heterorhabditis nematidae) (The Bugfactory Ltd., Nanoose bacteriophaga and S. carpocapsae were Bay, British Columbia) were applied to the both found to suppress S. myopaeformis rootstock–scion graft unions of Gala apples emergence when used in combination with on M26 rootstocks either in the spring laborious and possibly impractical trunk before adult emergence, or in the autumn wraps. after a summer oviposition was complete. Two types of wet trunk wraps were included in the trials to reduce nematode 41.5 Future Needs desiccation. Pupal exuviae on the exterior of lower tree trunks at the end of each Biological control strategies have a greater growing season were used to assess chance in contributing to the control of this suppression of S. myopaeformis. In the invasive pest when integrated with non- springtime treatment, placement of a wet chemical methods to reduce the extreme sawdust-based trunk wrap around the base population densities. Future work should of the trees was found to signifi cantly include: suppress the total number of emerging S. myopaeformis adults by the autumn with 1. Development of semiochemical-based and without inclusion of nematodes. When monitoring and mass-trapping and or mat- H. bacteriophaga and S. carpocapsae were ing disruption for S. myopaeformis to ena- applied to the bottom 45 cm of infested ble biological control strategies; trees in autumn, both species were shown 2. Developing laboratory rearing methods to signifi cantly suppress S. myopaeformis to address the apparent reluctance of S. adult emergence the following season; myopaeformis to mate in captivity – this however, these nematode treatments were step requires attention in order that only effi cacious when the trees were also entomopathogens can be more realistically coated with the wet sawdust wrap. It is not screened and that we gain a better under- clear how the wraps increase mortality of standing of the species’ biology and its S. myopaeformis and/or the effi cacy of impact on tree health; nematodes. Any oviposition-deterring or 3. Research targeted at understanding all ovicidal effect of the wrap would not likely parasitoids and predators associated with have infl uenced the pupal counts in these S. myopaeformis, as there is a possibility trials, providing the hypothesis that S. that an exotic parasitoid introduction may myopaeformis has a 2-year larval be appropriate to help to suppress numbers developmental period is correct. in organic orchards. Chapter 41 289

References

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42 Trichoplusia ni Hübner, Cabbage Looper (Lepidoptera: Noctuidae)

Martin A. Erlandson Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

42.1 Pest Status iptera: Aleyrodidae), due to the application of chemical insecticides applied against T. The cabbage looper, Trichoplusia ni ni, and increased damage from these other Hübner (Lepidoptera: Noctuidae), feeds on pests due to release from biological control a broad range of host plants and is an agent impacts (Gillespie et al., 2002). important pest of vegetable crops, particularly in Ontario and Quebec. It is also a chronic pest of greenhouse vegetable 42.2 Background production in British Columbia and Ontario. In greenhouses, T. n i causes Trichoplusia ni has a worldwide distrib- signifi cant economic damage to cucumbers, ution and is a key insect pest in most Cucumis sativus L. (Curcubitaceae), crucifer-growing areas. Since T. n i has no tomatoes, Solanum lycopersicum L., sweet diapause, although it can spend extended peppers, Capsicum annuum L. (Solana- periods as a pupa it cannot tolerate ceae), and lettuce, Lactuca sativa L. prolonged periods of cold, it overwinters (Asteraceae), as a result of defoliation and only in climates with warm winters, direct damage to fruit. Indirect economic typically subtropical regions (Anonymous, impacts result from the decline of 2004). However, T. n i is highly dispersive introduced biological control agents target- and adults reinvade northern temperate ing other insect pests, such as aphids areas each summer. In British Columbia, (Hemiptera: Aphididae), thrips (Thysan- T. n i populations apparently are estab- optera: Thripidae) and whitefl ies (Hem- lished by an annual migration of adults on

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 292 Chapter 42 high-altitude winds from California and which larvae feed (Janmaat and Myers, Mexico (Franklin et al., 2011). As well, 2005). The development of resistance to B. there is evidence that T. n i populations thuringiensis (Bt) in ‘fi eld’ or ‘wild’ overwinter in greenhouses as pupae (Caron populations of insect pests after its and Myers, 2008; Cervantes et al., 2011) extensive use as a microbial pesticide is and these populations subsequently can not unique to T. ni and widespread spread between greenhouses (Franklin and resistance to Bt products has been demon- Myers, 2008). In eastern Canada, T. n i strated in populations of the diamondback populations are established by long- moth, Plutella xylostella (L.) (Lepidoptera: distance migration of moths from the Plutellidae) (Tabashnik, 1994). Genetic southern USA, primarily Florida engineering approaches have been sug- (Lafontaine and Poole, 1991). gested as a potential solution to the resistance problem and these approaches have been useful in controlling Bt-resistant 42.3 Biological Control Agents populations of insect pests. Indeed, development of genetically modifi ed and 42.3.1 Bacteria hybrid Bt b-endotoxins were demonstrated to counter the resistance in greenhouse- A microbial-based insecticide formulation selected resistant populations of T. ni that includes the spores and crystal toxins (Franklin et al., 2009). (b-endotoxins) of Bacillus thuringiensis Berliner serovar. kurstaki (Btk) (Bacil- laceae) has been a highly successful 42.3.2 Viruses insecticide for the control of lepidopteran pests and it has been used extensively in Alphabaculoviruses (nucleoployhedro- greenhouse and fi eld vegetable production viruses) and betabaculoviurses (granulo- for the control of T. ni. In greenhouses, Btk viruses) have been isolated from T. n i products have the advantage of being populations. In particular the Alphabaculo- highly specifi c to Lepidoptera and thus virus species Trichoplusia ni single preserve populations of introduced bio- nucleopolyhedrovirus (TnSNPV) and logical control agents such as insect preda- Trichoplusia ni multiple nucleopolyhedro- tors and parasites. Commercial formulations virus (TnMNPV) (Baculoviridae) are often for use on greenhouse vegetables include isolated from T. n i populations and have Dipel®, Foray® and Bioprotec® and these been shown to have high potential for are important tools for T. ni management. development of microbial insecticides for However, in the last decade some popu- cabbage looper control (Jaques, 1972, 1977; lations of T. ni infesting vegetable Vail et al., 1999). The latter NPV species is greenhouses in British Columbia were now recognized as one of numerous shown to have developed high levels of strains/variants of Autographa californica resistance (25–100-fold) to Btk products multiple nucleopolyhedrovirus (AcMNPV) (Janmaat and Myers, 2003). The basis of the (Baculoviridae) (Theilmann et al., 2005; resistance in these T. ni populations likely Harrison et al., 2012). Numerous geo- involves changes in the effi ciency of graphic isolates or strains of both TnSNPV binding of the Cry1Ac and Cry1Ab toxin and AcMNPV-like viruses have been (major b-endotoxins in Btk products) to isolated from T. n i populations worldwide target receptors in the midgut epithelium and many have been genetically char- of resistant lines of T. ni as the result of acterized to some degree (Bilimoria, 1983; mutations of specifi c midgut membrane Del Rincón-Castro and Ibarra, 1997; proteins (Wang et al., 2007). The genetics Erlandson et al., 2007). The AcMNPV virus of this resistance inheritance indicate that has a relatively large host range amongst it comes with a fi tness cost and that this Lepidoptera, having been demonstrated to cost varies depending on the crop plant on be infectious to at least 95 species from 15 Chapter 42 293 families (Cory, 2003). The host range of son et al., 2009). Standard aqueous spray TnSNPV is likely much more restrictive application technology delivered at 400 l (Del Rincón-Castro and Ibarra, 1997) and ha−1 with 1.0×1011 virus occlusion bodies probably infects only a few closely related ha−1 equivalent or higher, with either species within the subfamily Plusiinae (M. AcMNPV or TnSNPV, produced high Erlandson, 2012, unpublished results). mortality in populations of both 2nd and Although the published results from 4th instar T. ni by 7 days post-spray. In infectivity assays with these two alpha- addition to population control, the virus baculoviruses in T. n i larvae are somewhat treatments produced signifi cant reductions variable, the general trend is that the two in T. n i -related defoliation and fruit viruses are equally infectious for early damage even under very high pest density instar larvae. (25 larvae per plant). The results of these Recently, an extensive survey of T. n i initial spray trials on cucumbers were very larval populations from commercial promising and the indigenous British greenhouses in British Columbia for Columbia AcMNPV isolate is now under baculoviruses showed that by far the most consideration for registration and develop- prevalent natural infections were due to ment as a microbial control agent for TnSNPV and only a few AcMNPV-infected control of T. ni in vegetable greenhouses in larvae were detected (Erlandson et al., Canada. 2007). The TnSNPV isolates were shown to be very homogeneous but were distinct from the TnSNPV isolate from Ontario 42.3.3 Insects (Jaques, 1972) based on genetic analysis, including restriction endonuclease digests Gillespie et al. (2002) reviewed the use of and high throughput DNA sequencing of the insect predators Podisus maculiventris selected virus genes. In contrast, several (Say) (Hemiptera: Pentatomidae), Dicyphus different strains of AcMNPV with different hesperus Knight (Hemiptera: Miridae) and genotypes were isolated (Willis et al., 2005; Orius spp. (Hemiptera: Anthocoridae), as Erlandson et al., 2007). Biological char- well as the potential for inundative release acterization of the British Columbian of parasitoids such as Trichogramma spp. TnSNPV and AcMNPV isolates showed (Hymenoptera: Trichogrammatidae), which that they were equally infectious for 2nd to attack the egg stage and the larval 4th instar T. n i larvae but that AcMNPV parasitoid Cotesia marginiventris (Cresson) strains were signifi cantly more infectious (Hymenoptera: Braconidae). Among their than TnSNPV in 5th instars (Erlandson et general conclusions were that use of C. al., 2007). In addition, the AcMNPV strains marginiventris for inundative releases is killed T. n i larvae 12–18 h sooner after too expensive to be practical but could infection than did TnSNPV isolates; play a role in suppressing T. n i populations however, TnSNPV produced substantially before outbreaks occur. A recent study more virus occlusion bodies in infected concluded that the introduction of Tricho- larvae than did AcMNPV. This study gramma sibericum Sorkina alone or in demonstrated that both the AcMNPV and combination with T. brassicae Bezdenko TnSNPV strains showed tremendous (Hymenoptera: Trichogrammatidae), the potential for development as biological only commercially available egg parasitoid control agents for T. n i . On the basis of this for control of T. n i , was not superior to established potential, the indigenous the use of T. brassicae alone. This study British Columbia isolates with the highest also concluded that the dispersal of these virulence for both TnSNPV and AcMNPV egg parasitoids was limited and for the were chosen to be assessed in a series of most part vertical suggesting improve- small- (6 m2 cages) and medium-sized (12 ments in parasitoid egg cards are needed m2 plots) greenhouse spray trials on a for maximum control effects (Prasad, commercial variety of cucumber (Erland- 2006). 294 Chapter 42

42.4 Evaluation of Biological Control consideration for registration and develop- ment as a microbial control agent for control Genetic engineering approaches have been of T. ni in vegetable greenhouses in Canada. suggested as a potential solution to the Bt The state of biological control of T. n i in resistance problem and these approaches vegetable greenhouses largely consists of have been useful in controlling Bt-resistant the use of Btk products and inundative populations of insect pests. Although releases of egg parasitoids. However, issues development of genetically modifi ed and around the dispersion of T. sibericum and hybrid Bt b-endotoxins were demonstrated T. brassicae need to be addressed. to counter the resistance in greenhouse- Although C. marginiventris has limited use selected resistant populations of T. n i , past for inundative biological control it could experience would suggest that sole reliance play a role in suppressing T. n i populations on Bt-based microbial insecticides as an before outbreaks occur. insect control strategy invites further development of resistant pest populations. Therefore, the development of additional 42.5 Future Needs microbial insecticides with entirely differ- ent modes of action than that of Bt products Future work should include: is desirable and particularly so for the greenhouse markets in which insect 1. Development of additional microbial biological control agents are used exten- insecticides with novel modes of action; sively. The indigenous British Columbia 2. Developing improved delivery methods AcMNPV isolate has good potential as a for inundative applications of Tricho- biopesticide against T. ni. It is now under gramma spp. egg parasitoids.

References

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43 Ambrosia artemisiifolia L., Common Ragweed (Asteraceae)

Alan K. Watson and Miron Teshler McGill University, Ste Anne de Bellevue, Québec

43.1 Pest Status bronchitis and asthma. The complex of 22 proteins released from ragweed pollen Common ragweed (herbe-à-poux), Ambrosia grains are some of the most powerful artemisiifolia L. (Asteraceae), a native antigens/allergens known (Bagarozzi and annual weed species, occurs throughout Travis, 1998). Although ragweed pollen North America and is most abundant in can travel great distances, allergenic southern Ontario and Quebec and in the reactions are caused by A. artemisiifolia north-east and north-central US states growing very close to the susceptible (Bassett and Crompton, 1975). It is a individual. Within urban and suburban pioneer species that fl ourishes in disturbed regions, effective control of ragweed habitats such as along rights-of-way, in infestations would substantially lower the vacant lots and cultivated fi elds. Ambrosia incidence of allergenic reactions. Ambrosia artemisiifolia is often the most frequent artemisiifolia has rapidly become a serious species in these habitats, and forms dense agricultural weed, especially in vegetable linear populations along the fi rst metre of crops grown in the muck soils of south- roads and highways in eastern Canada western Quebec and Ontario. Ambrosia (DiTommaso, 2004; Joly et al., 2011). There artemisiifolia seeds germinate in spring, is strong historical evidence that the the vegetative phase occurs from May to expansion of road networks has contrib- August, fl owering commences on the fi rst uted to the spread of A. artemisiifolia week of August and produces copious (Lavoie et al., 2007; Simard and Benoit, quantities of airborne pollen, and seeds are 2010). Moreover, this weed species is set in late summer or autumn. Individual highly plastic and very variable in size, leaf plants produce 3000 to 62,000 seeds that shape, infl orescence form, degree of can remain viable for 39 years or more hairiness and life-form strategy. Germin- when buried in the soil (Bassett and ation response for roadside populations of Crompton, 1975). A. artemisiifolia may be locally adaptive to salinity and allows A. artemisiifolia to emerge relatively early in spring thus 43.2 Background providing a competitive advantage over later emerging roadside plants (DiTommaso, Ambrosia artemisiifolia can easily be 2004). uprooted in most soil types; however, it Ambrosia artemisiifolia pollen is the can readily adapt to frequent mowing by primary cause of allergenic hay fever, quickly producing new stems and fl owers

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 43 297

below the cutting height (Vincent and grammes in Australia, eastern Europe and Ahmin, 1985; Patracchini et al., 2011). eastern Asia, with variable results (Julien Repeated mowing can reduce pollen pro- and Griffi ths, 1998; Zhou et al., 2009). duction but will not reduce the seed bank Tarachidia candefacta Hübner (Lepi- (Simard and Benoit, 2011). Various herbi- doptera: Noctuidae) and Zygogramma cides and tank mixtures have provided suturalis Fabricius (Coleoptera: Chrys- control of A. artemisiifolia in maize, Zea omelidae) are two natural enemies from mays L. (Poaceae), and soybean, Glycine Canada and the USA that were introduced max (L.) Merr. (Fabaceae), crops, but popu- into the former Soviet Union in 1966. They lations of A. artemisiifolia have developed became established and provided control resistance to herbicides having the follow- of the invasive A. artemisiifolia (Reznik, ing sites of action: Photosystem II inhibi- 1991; Goeden and Teerink, 1993). Of great tors, ALS inhibitors, PPO inhibitors, ureas recent interest, populations of T. cande- and amides and glycines (Heap, 1997; facta have recently begun to expand, many Patzoldt et al., 2001; Saint-Louis et al., years after introduction in southern Russia 2005), thus restricting control options. (Poltavsky et al., 2008). Zygogramma Several herbicides, including 2,4-D suturalis leaf beetles were also introduced ((2,4-dichlorophenoxy) acetic acid), MCPA into Croatia, but failed to become ((2 methyl-4-chlorophenoxy) acetic acid) established (Igrc et al., 1995). Releases of Z. and dicamba (3,6-dichloro-2-methoxy- suturalis in China in 1985, both from benzoic acid), have been the mainstay of A. Canada and from the former Soviet Union, artemisiifolia control strategies along road- established in some locations, but failed in ways and marginal areas in most com- others (Wan et al., 1995). In 1990, Z. munities. However, herbicide use for the suturalis was introduced into Australia control of A. artemisiifolia in urban areas from the USA but failed to establish (Julien has declined in recent years due to the and Griffi ths, 1998). implementation of municipal and pro- Ambrosia artemisiifolia is presently vincial legislation throughout Canada that considered under good control in south- bans or severely restricts herbicide use. eastern Queensland and in northern New Currently, foliar application of sodium South Wales and is regarded as an chloride solutions is being used in cities outstanding success in Australia (Palmer et and municipalities of Quebec (Grégoire et al., 2010); but the success is not due to the al., 2002; Watson, 2008). Ambrosia introduction of specifi c biological control artemisiifolia is very sensitive to desic- agents against A. artemisiifolia. From 1980 cation and dries up whereas surrounding to 1984, three biological control agents, plants are not impacted. including the leaf-feeding chrysomelid beetle Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae), the sap- 43.3 Biological Control Agents sucking bug Stobaera concinna (Stål) (Hemiptera: Delphacidae) and the tip- 43.3.1 Insects galling moth Epiblema strenuana (Walker) (Lepidoptera: Tortricidae) from Mexico Over 400 insect species have been known were introduced into Australia for the to attack A. artemisiifolia (Harris and biological control of parthenium weed, Piper, 1970) and more than 30 of these Parthenium hysterophorus L. (Asteraceae) have been examined as potential biological (McFadyen, 1992). Parthenium hystero- control agents for A. artemisiifolia phorus is very closely related to the genus (Kovalev, 1970). Ambrosia artemisiifolia is Ambrosia and coincidentally it was an exotic invasive weed in Australia, observed that these three insects also Europe and central Asia. There have been attacked A. artemisiifolia. Epiblema strenu- several classical biological control pro- ana was the most effective biological 298 Chapter 43

control agent, and has reduced the size, pupation, the 3rd instar larvae spin loosely abundance and pollen production of woven cocoons on the upper or lower leaf ragweed to a greater extent than the two surfaces. Development time for the pupa other insects. stage is about 7 days and the total development time from oviposition to adult emergence is about 22 days (Welch, 1978). 43.3.1.1 Inundative biological control From 1995 to 1999, host-specifi city, life In Canada, Z. suturalis and Ophraella table, biotic potential, mortality, feeding communa LeSage (Coleoptera: Chrys- potential and mass rearing studies of O. omelidae) are native natural enemies of A. communa were conducted on transplanted artemisiifolia. They have been the main ragweed plants (Teshler et al., 1996, 1999). focus of biological control studies at the Conclusions derived from these studies Macdonald Campus of McGill University suggested that O. communa was a very as inundative biological control agents in promising candidate for inundative bio- Quebec (Teshler et al., 2002). In North logical control of A. artemisiifolia. Char- America, under natural conditions, popu- acteristics of O. communa include: (i) being lation densities and impact of O. communa native to Quebec; (ii) having a restricted on A. artemisiifolia tend to be low, host range; (iii) causing signifi cant A. presumably because of strong attack by artemisiifolia damage, especially at the predators and parasitoids by the end of vulnerable seedling stage; and (iv) having a summer (Teshler et al., 2002). Thus, high intrinsic reproductive rate, which has inundative releases of Z. suturalis and O. facilitated its mass rearing under controlled communa early in the growing season conditions (Teshler et al., 2002; Dernovici (Teshler et al., 1996) would be a reasonable et al., 2006). In 1999 and 2000, inundative approach. However, the reduction or cage releases were conducted using various cessation of Z. suturalis oviposition on O. communa beetle-to-A. artemisiifolia and extensively damaged plants (as observed in O. communa egg-to-A. artemisiifolia ratios the former Soviet Union) and pupation in in carrot, Daucus carota L. subsp. sativa soil are the most important limitations for Schübl. & M. Martens (Apiaceae), cabbage, the mass-rearing of this species (Teshler et Brassica oleracea L. (Brassicaceae ), and al., 2002). Thus, O. communa became the soybean fi elds in Sherrington and St agent of choice. Isidore, Quebec. Four to fi ve O. communa Ophraella communa is oligophagous beetles per A. artemisiifolia plant caused and feeds on various members of the complete defoliation and death of 4- to subtribe Ambrosiinae (Asteraceae). All 6-leaf-stage plants within 14 days. In 2001, developmental phases of this multivoltine small-scale open fi eld release trials were insect occur on A. artemisiifolia. Fertile conducted with O. communa in soybean adult females overwinter in soil debris and fi elds in St Isidore, Quebec. Larval feeding are observed, along with their eggs, on of O. communa signifi cantly reduced A. ragweed seedlings in early spring. Eggs are artemisiifolia growth when the insect generally deposited in clusters on the host infestation occurred early in the season plant and the development time of each of (Teshler et al., 2002). the three larvae instars is 3–4 days (LeSage, Ophraella communa was mass reared 1986). Larval instars are distinguished by on transplanted A. artemisiifolia plants in the size and colour of the head capsule the greenhouse. All development stages of (Welch, 1978). Neonate larvae generally O. communa can be produced on 6- to skeletonize leaves while adults and older 8-leaf-stage ragweed plants in the instar larvae can devour the entire leaves. greenhouse with a temperature of 24±4°C, Under favourable conditions, O. communa a relative humidity of 60±20% and a adults and larvae can completely defoliate photoperiod of 16:8 L:D conditions ragweed plants (LeSage, 1986). Prior to (Teshler et al., 1999). Approximately 40–60 Chapter 43 299

beetles (1:1 male:female ratio) and 100–200 mass rearing of O. communa was at 28°C larvae can be kept per rearing cage (Zhou et al., 2010). Initial release density (17.5×31×8 cm). Ophraella communa of O. communa adults for effective control pupae were collected and plants replaced of A. artemisiifolia in the fi eld in China bi-weekly. Pupae were placed into should be ≥1 beetles per plant at early 17.5×31×8 cm plastic containers and stored growth stages or ≥12 beetles per plant at under laboratory conditions until adults the later growth stages (Guo et al., 2011). emerged (Teshler et al., 2004). A multi- purpose device was then developed for the collection, short-term storage, transport 43.3.2 Pathogens and delivery of O. communa pupae or adults (Teshler et al., 2004). To achieve a In Canada, the incidence and biological successful A. artemisiifolia control through control potential of a forma specialis of large-scale releases of O. communa, mass Pustula tragopogonis (Pers.) Thines (= production techniques for O. communa Albugo tragopogonis (DC) Gray) (Albu- need to be improved. ginaceae) on A. artemisiifolia has been Mass production of O. communa on described (Hartmann and Watson, 1980). transplanted A. artemisiifolia plants in the When A. artemisiifolia is attacked by P. greenhouse is being compromised by high tragopogonis, considerable damage can labour costs, large space requirements and occur and signifi cant reduction in pollen high growth-facility costs. The collection and seed production occurs if systemic and handling methods of the specimens infection is achieved (Hartmann and need to be mechanized. A semi-artifi cial Watson, 1980); however, diffi culties in medium for rearing Coccinellidae spp. mass producing this white blister rust have (Daniel Coderre, Montreal, Quebec, 2012, so far prevented it from being produced pers. comm.) was tested and found not commercially (Teshler et al., 2002). In suitable for rearing larvae and adults of O. Quebec, a Phoma sp. (incertae sedis) was communa. The evaluation of several media discovered on A. artemisiifolia and evalu- used for rearing various herbivorous insect ated as a potential mycoherbicide candi- species and the incorporation of A. date (Brière et al., 1995). A combination of artemisiifolia leaf powder as a feeding this Phoma sp. and O. communa provided stimulant were conducted but limited pro- a synergistic effect and resulted in high gress has been achieved in fi nding an plant mortality (Teshler et al., 1996). artifi cial diet for the production of O. Unfortunately, this Phoma sp. isolate lost communa. its virulence and attempts to revive or re- Ophraella communa was accidentally isolate it from natural sites were unsuc- introduced in Japan in 1996 (Yamazaki et cessful (Teshler et al., 2002). al., 2000; Yamanaka et al., 2007) and in In Europe, A. artemisiifolia has once China in 2001 (Zhang et al., 2005). A mass- again become a major target for biological rearing programme was established in control with the recent approval of a China with the aim to implement inun- coordinated European research programme dative release of mass-reared O. communa on ‘Sustainable Management of Ambrosia in heavily A. artemisiifolia-infested habi- artemisiifolia in Europe’ (COST FA1203- tats (Zhou et al., 2009). Critical life table SMARTER). Currently, there are 18 insects data on the establishment potential of O. and fi ve fungal pathogens considered as communa in new environments with promising candidates for classical bio- diverse temperature regimes were gener- logical control (Gerber et al., 2011). How- ated (Zhou et al., 2010, 2011). Ophraella ever, it was noted that an inundative communa preferred moist microclimates approach will be necessary for A. with 75–90% relative humidity (Zhou et artemisiifolia-infested crop fi elds. al., 2009). The optimum temperature for Ophraella slobodkini Futuyma (Coleoptera: 300 Chapter 43

Chrysomelidae) and the fungus, Septoria and fungal pathogens for host specifi city epambrosiae D.F. Farr, Sydowia (Myco- and effectiveness against A. artemisiifolia. sphaerellaceae) are candidate biological control agents for mass-rearing and repeated releases against ragweed (Gerber Acknowledgements et al., 2011). The future success of the biological control of A. artemisiifolia We thank Robert Anderson (Canadian worldwide may rely on successful opti- Museum of Nature, Ottawa) and Laurent mization of mass rearing techniques. LeSage (Canadian National Collection of Insects and Arachnids, Ottawa) for confi rming the taxonomic status of 43.4 Future Needs Ophraella communa; Daniel Coderre (Université du Québec à Montréal) for his Future work should include: collaboration in diet development, and Luc 1. Developing and optimizing mass rearing Brodeur (Phytodata Inc.) for the assistance for O. communa, O. slobodkini and S. in securing AAFC/NSERC Research epambrosiae; Partnership Program funding. 2. Evaluating additional candidate insects

References

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44 Centaurea diffusa Lamarck, Diffuse Knapweed, and Centaurea stoebe subsp. micranthos (S.G. Gmel. ex Gugler) Hayek, Spotted Knapweed (Asteraceae)

Rob S. Bourchier1 and Brian H. Van Hezewijk2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2Natural Resources Canada, Canadian Forest Service, Victoria, British Columbia

44.1 Project Status control in Canada with the fi rst agent, Urophora affi nis (L.) (Diptera: Tephritidae), Knapweeds, Centaurea diffusa Lamarck released in 1970 (Harris and Myers, 1984). and Centaurea stoebe subsp. micranthos The biology of all of the biological control (S.G. Gmel. ex Gugler) Hayek (=Centaurea agents for knapweeds in Canada was maculosa Lamarck) (Asteraceae), were reviewed in previous volumes of this series among the earliest targets for biological (Harris and Myers, 1984; Bourchier et al.,

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 44 303

2002). There have been 12 biological fi rmed that the two Larinus spp. were still control agents released in Canada for C. present at these sites. Larinus minutus was stoebe subsp. micranthos and C. diffusa found at both C. stoebe subsp. micranthos with seven insect species now relatively and C. diffusa sites whereas L. obtusus was common (Bourchier et al., 2002). Of only found at C. stoebe subsp. micranthos particular interest are the seed head weevil locations (Myers et al., 2012, unpublished Larinus minutus Gyllenhal and the root results). These on-going studies will com- weevil Cyphocleonus achates Fahraeus pare fi eld material from British Columbia (Coleoptera: Curculionidae), which have with both European collected beetles and been implicated in successful biological voucher specimens of released Larinus control of C. diffusa and C. stoebe subsp. spp. populations. micranthos (Story et al., 2006, 2008; Confi rming the identity and genetic Seastedt et al., 2007; Myers et al., 2009; structure of Larinus spp. populations on Knochel and Seastedt, 2010). No new Centaurea spp. is of importance because L. biological control agents have been minutus has been suggested to be the released in Canada for knapweeds since ‘silver bullet’ or single agent required for 1993 when Larinus obtusus Gyllenhal control of C. diffusa (Myers, 2007; Myers et (Coleoptera: Curculionidae) was estab- al., 2009). However, with up to seven lished in British Columbia (Bourchier et biological control agents being present at al., 2002). individual Centaurea spp. sites in British Since 2000, the primary focus of the Columbia, it is diffi cult to look at the knapweed biological control project has impact of a single agent like L. minutus, a been on: (i) understanding the impact and seed-head feeder, in isolation, particularly spread of Larinus spp. and C. achates; and when root-feeding species are also present. (ii) redistribution of these biological con- To address this issue, we studied the trol agents, as part of operational release impact of L. minutus at C. diffusa sites in programmes, in all regions with new Alberta where no root-feeding biological populations of invasive knapweeds. control agents were present. In 2005, 300 L. Larinus minutus and L. obtusus were minutus were released at a riparian C. introduced to Canada in the early 1990s diffusa site on the Oldman River, where (Bourchier et al., 2002). At the time of their only the seed-head fl ies Urophora spp. release both Larinus spp. were known to were present. Three additional C. diffusa attack both C. stoebe subsp. micranthos stands 2, 7 and 9 km downstream were and C. diffusa, with L. minutus expected to identifi ed at that time. Annually until be effective in drier sites and L. obtusus 2011, all stands were monitored to assess preferring moist sites (Groppe, 1990, 1992). the density of C. diffusa stems and rosettes Morphological keys (Ter-Minasyn, 1978) to as well as the density of L. minutus. By separate the two Larinus spp. are available, 2011, L. minutus had spread to the down- however, since their release consistent stream patches at a rate of approximately 2 separation of the two species in the fi eld in km year−1. At the initial release site, L. British Columbia has been diffi cult. In minutus numbers grew quickly, reaching general, Larinus spp. populations are sustained densities of 356 beetles m−2 after identifi ed by site characteristics (moist 3 years. At the stand 2 km downstream, versus dry) and by the known source populations grew more slowly but reached population that has been released in the a density of 382 beetles m−2 5 years after area (V. Miller, Nelson, British Columbia, the initial upstream release. The patches 2012, pers. comm.). Myers et al. (2011) located 7 and 9 km downstream were initiated a re-examination of Larinus spp. colonized 3 and 4 years after release, populations at ten historic release locations respectively, and in 2011 L. minutus to assess the status of Larinus spp. on C. populations were still growing quickly. At stoebe subsp. micranthos and C. diffusa. all of the sites, both C. diffusa stem and Comparison of CO1 gene sequences con- rosette densities are signifi cantly higher 5 304 Chapter 44

years post-release than they were at the conducted with this population and it was time of fi rst release in 2006. Thus to 2011, found that C. achates adults were very while L. minutus populations have grown sedentary, moving 0.27 m day−1 in a and spread quickly, any reductions in C. natural stand (Rondeau, 2007). Releasing diffusa densities, at least at some sites, will C. achates later in the season and releasing take more than 5 years. Monitoring con- them at densities greater than 24 beetles tinued at these sites in 2012 and is planned per plant resulted in increased movement for subsequent years. At sites in British distances (Rondeau, 2007). Compatibility Columbia with a longer period since L. of C. achates and L. minutus was also minutus establishment, there was a decline assessed in Alberta with a manipulative in C. diffusa cover that was followed by an fi eld plot experiment (Van Hezewijk and increase in the presence of native plant Bourchier, 2012). In year one, C. achates species but also non-native grasses were released into Centaurea spp. fi eld (Stephens et al., 2009). plots and their impact assessed, followed As L. minutus populations have by release of L. minutus in the following increased at fi eld sites there have been year. Cyphocleonus achates was found to opportunities for multiple studies on the have direct negative effects on C. diffusa interaction between L. minutus and other density, size, and seed-head diameter. Both seed-head insects with variable results indirect positive and negative impacts on (Smith and Mayer, 2005; Crowe and L. minutus were also observed. In aggregate Bourchier, 2006; Seastedt et al., 2007; however, C. achates and L. minutus are Myers et al., 2009; Knochel and Seastedt, expected to have additive impacts when 2010; Bourchier and Crowe, 2011; released together on C. diffusa (Van Stephens and Myers, 2012). What is Hezewijk and Bourchier, 2012). consistent is that L. minutus is effective at British Columbia has historically had removing all seed in seed heads, has a the most serious problem with C. stoebe signifi cant impact on individual plants, subsp. micranthos and C. diffusa and thus and that multiple seed-head species can has had the most active programme of persist in the C. diffusa system. The redistribution of biological control agents variation observed in the intensity of the (Bourchier et al., 2002). All Centaurea spp. seed-feeding species interactions may be a biological control agents were released in function of differing relative densities, cage British Columbia prior to 2000 (Bourchier (Smith and Mayer, 2005; Crowe and et al., 2002); the seed-head fl y Chaetorellia Bourchier, 2006) versus fi eld studies acrolophi White (Diptera: Tephritidae) was (Seastedt et al., 2007; Myers et al., 2009) or the agent that was most recently confi rmed variations in plant phenology (Bourchier as established in 2008 (British Columbia and Crowe, 2011). For C. stoebe subsp. Ministry of Forests, Lands and Natural micranthos, the persistence of multiple Resource Operations, 2012). Redistribution seed-head-feeding species may have been efforts since 2001 have been focused on C. critical for the reductions in the seed bank, achates and Larinus spp. because the which in combination with C. achates has remaining biological control agents are been linked to C. stoebe subsp. micranthos widely distributed. By 2012, C. achates decline in Montana (Story et al., 2008). redistribution continued at C. stoebe Cyphocleonus achates was fi rst released subsp. micranthos sites because of slow in British Columbia in 1987 and expected dispersal but operational distribution of to have the most impact on C. stoebe Larinus spp. is complete excepting a few subsp. micranthos because of the larger isolated areas with Centaurea spp. (V. taproot (Stinson et al., 1994; Bourchier et Miller, Nelson, British Columbia, 2012, al., 2002). It was moved to southern pers. comm.). During this period wide- Alberta from British Columbia in 2003 and scale reductions of C. diffusa populations has established on C. diffusa at a site near in the central interior of British Columbia Lethbridge. Mark–recapture studies were have been documented (Myers et al., 2009; Chapter 44 305

Newman et al., 2011; Gayton and Miller, understand the mechanisms and inter- 2012). actions between agents and why biological In Alberta, L. minutus has been released control may not be effective in all areas. since 2003 as part of a collaborative project Restoration studies are also critical to between the municipal districts of ensure that we do not just replace Cen- Southern Alberta and AAFC for the oper- taurea spp. with another rangeland ational implementation of weed biological invasive species. control. There have been 14 releases of L. minutus with confi rmed overwintering and 44.2 Future Needs establishment in Southern Alberta since 2003. The initial 2003 source populations Future work should include continuing: for L. minutus were from British Columbia near Verigan’s Tomb, Creston, British 1. Characterization of established Larinus Columbia. Nine additional release sites spp. populations using DNA and morpho- were added in 2012 using local Alberta L. logical studies to determine if there are minutus but have not yet been confi rmed habitat associations for Larinus spp., if as established. there is any evidence for hybridization and Larinus minutus from the initial Alberta if there is additional potential for biologi- nurse site near Lethbridge were sub- cal control; sequently moved to Ontario in 2007 and 2. Long-term monitoring of impact by L. Manitoba in 2012. A total of 450 L. minutus and C. achates on Centaurea spp. minutus adults were released on spotted at sites in Alberta and British Columbia; knapweed at two Ontario sites (44.2676°, 3. To expand operational release pro- −79.9013°; 44.2629°, −79.9499°) located at grammes using Larinus spp. and C. achates Canadian Forces Base Borden (P.G. Mason, to assist in limiting the spread of 2012, unpublished results). Establishment Centaurea spp. into areas where these bio- at these sites could not be confi rmed; the logical control agents are not established. insects were released on 19 July but the sites were mowed shortly thereafter and there were no seed heads to sample in the Acknowledgements fall. It is possible L. minutus may have survived and dispersed to other local C. Funds for the on-going research pro- stoebe subsp. micranthos patches. The gramme on knapweeds have been provided Manitoba release in 2012 was conducted by AAFC Peer Review. We thank Ray by the Invasive Species Council of Wilson, Monte Thomson, Stephanie Erb, Manitoba on C. stoebe subsp. micranthos and Michael Crowe, Karma Tiberg and and will be evaluated in 2013 (Cheryl Leah Blair and many student summer Hemming, Winnipeg, Manitoba, 2012 pers. assistants for their help with the project. comm.). Earlier funding for knapweed biological Success in the Centaurea spp. biological control studies was provided by the AAFC control programme has taken a long time. Matching Investment Initiative, British In the past 12 years data have accumulated Columbia Ministry of Forests (Now: from multiple locations in Canada and the Ministry of Forests, Lands and Natural USA that suggests there is reason for Resource Operations Range Branch) and optimism. On-going work is required to Canadian Pacifi c Railway. 306 Chapter 44

References

Bourchier, R.S. and Crowe, M.L. (2011) Role of plant phenology in mediating interactions between two biological control agents for spotted knapweed. Biological Control 58, 367–373. Bourchier, R.S., Mortensen, K. and Crowe, M. (2002) Centaurea diffusa Lamarck, Diffuse Knapweed, and Centaurea maculosa Lamarck, Spotted Knapweed (Asteraceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 302–313. British Columbia Ministry of Forests Lands, Natural Resource Operations and Range (2012) Biocontrol agents currently unavailable for distribution. Available at: http://www.for.gov.bc.ca/ hra/plants/biocontrol/bioagents_primary.htm#CHAC (accessed 26 November 2012). Crowe, M.L. and Bourchier, R.S. (2006) Interspecifi c interactions between the gall-fl y Urophora affi nis Frfl d. Diptera: Tephritidae, and the weevil Larinus minutus Gyll. Coleoptera: Curculionidae, two biological control agents released against spotted knapweed Centaurea stobe L. ssp. micranthos. Biocontrol Science and Technology 16, 417–430. Gayton, D. and Miller, V. (2012) Impact of biological control on two knapweed species in British Columbia. British Columbia Journal of Ecosystems and Management 13(3), 1–14. Groppe, K. (1990) Larinus minutus Gyll. (Coleoptera: Curculionidae), a suitable candidate for the biological control of diffuse and spotted knapweed in North America. In: Final Report CAB International Institute of Biological Control. CAB International, Delémont, Switzerland, pp. 1–25. Groppe, K. (1992) Larinus obtusus Gyll. (Coleoptera: Curculionidae), a candidate for the biological control of diffuse and spotted knapweed in North America. In: Final Report CAB International Institute of Biological Control. CAB International, Delémont, Switzerland, pp. 1–46. Harris, P. and Myers, J.H. (1984) Centaurea diffusa Lam. and Centaurea maculosa Lam. s. lat, Diffuse and Spotted Knapweed (Compositae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 127–137. Knochel, D.G. and Seastedt, T.R. (2010) Reconciling contradictory fi ndings of herbivore impacts on the growth and reproduction of spotted knapweed (Centaurea stoebe). Ecological Applications 20, 1903–1912. Myers, J.H. (2007) How many and what kind of biological control agents: a case study with diffuse knapweed. In: Vincent, C., Goettel, M.S. and Lazarovits, G. (eds) Biological Control: A Global Perspective. CAB International, Wallingford, UK, pp. 70–79. Myers, J.H., Jackson, C., Quinn, H., White, S. and Cory, J.S. (2009) Successful biological control of diffuse knapweed, Centaurea diffusa: the role of Larinus minutus. Biological Control 50, 66–72. Myers, J.H., Cory, J.S., Keever, C. and Bourchier, R. (2011) Using Genetic Techniques to Track Introduction and Distribution of Larinus. Presentation in: Report 17, Invasive Species Council of British Columbia. Responding to Invasive Species. Research Forum Summary. 18–19 October 2011, Richmond, British Columbia, Canada. Available at: http://www.bcinvasives.ca/images/ stories/documents/events_docs/Report17_Research%20Forum%20Sum_Final_2012_03_14.pdf (accessed 26 November 2012). Newman, R.F., Turner, S., Wallace, B.M. and Cesselli, S. (2011) The Decline of Diffuse Knapweed in British Columbia. British Columbia Ministry of Forests, Range and Forest Science Program, Victoria, British Columbia, Technical Report 065, pp. 1–23. Available at: http://www.for.gov. bc.ca/hfd/pubs/Docs/Tr/Tr065.htm (accessed 26 November 2012). Rondeau, K.J. (2007) Dispersal of the biocontrol agent Cyphocleonus achates (Coleoptera: Curculionidae) on the invasive plant diffuse knapweed (Centaurea diffusa) (Asteraceae). MSc thesis. Department of Biological Sciences, University of Alberta, Edmonton, Alberta. Seastedt, T.R., Knochel, D.G., Garmoe, M. and Shosky, S.A. (2007) Interactions and effects of multiple biological control insects on diffuse and spotted knapweed in the Front Range of Colorado. Biological Control 42, 345–354. Smith, L. and Mayer, M. (2005) Field cage assessment of interference among insects attacking seed heads of spotted and diffuse knapweed. Biocontrol Science and Technology 15, 427–442. Stephens, A.E.A. and Myers, J.H. (2012) Resource concentration by insects and implications for plant populations. Journal of Ecology 100, 923–931. Chapter 45 307

Stephens, A.E.A., Krannitz, P.G. and Myers, J.H. (2009) Plant community changes after the reduction of an invasive rangeland weed, diffuse knapweed, Centaurea diffusa. Biological Control 51, 140–146. Stinson, C.S.A., Schroeder, D. and Marquardt, K. (1994) Investigations on Cyphocleonus achates (Fahr.) (Col., Curculionidae), a potential biological control agent of spotted knapweed (Centaurea maculosa Lam.) and diffuse knapweed (C. diffusa Lam.) (Compositae) in North America. Journal of Applied Entomology 117, 35–50. Story, J., Callan, N., Corn, J. and White, L. (2006) Decline of spotted knapweed density at two sites in western Montana with large populations of the introduced root weevil, Cyphocleonus achates (Fahraeus). Biological Control 38, 227–232. Story, J.M., Smith, L., Corn, J.G. and White, L.J. (2008) Infl uence of seed head-attacking biological control agents on spotted knapweed reproductive potential in western Montana over a 30-year period. Environmental Entomology 37, 511–519. Ter-Minasyn, M.E. (1978) Weevils of the subfamily Cleoninae in the fauna of the USSR Tribe Lixini. Academy of Sciences of the USSR. Keys to the USSR Fauna. Zoological Institute, Academy of Sciences of the USSR 95. (Nauka Publishers, Leningrad 1967). Translated and published for USDA by Amerind Publishing, New Delhi, pp. 1–166. Van Hezewijk, B.H. and Bourchier, R.S. (2012) Impact of Cyphocleonus achates on diffuse knapweed and its interaction with Larinus minutus. Biological Control 62, 113–119.

45 Convolvulus arvensis L., Field Bindweed (Convolvulaceae)

Alec S. McClay1 and Rosemarie A. De Clerck-Floate2 1McClay Ecoscience, Sherwood Park, Alberta; 2Agriculture and Agri- Food Canada, Lethbridge, Alberta

45.1 Project Status persisted at a minimum of three release sites in and around Medicine Hat, Alberta The defoliating moth Tyta luctuosa (Denis (50.07°, −110.83°; 49.95°, −110.78°; 50.04°, and Schiffermüller) (Lepidoptera: Noctu- −110.72°). No formal evaluations of impact idae) and the gall mite Aceria malherbae have been done, but infested plants at these Nuzzaci (Trombidiformes: Eriophyidae) sites are often heavily galled and stunted, have been released against Convolvulus comparable to the damage illustrated by arvensis L. (Convolvulaceae) in Canada, but Laurialt et al. (2004) in New Mexico. only A. malherbae is known to be Dispersal from these release sites has not established (McClay and De Clerck-Floate, been studied in detail, but galling damage 2002; De Clerck-Floate and Cárcamo, 2011). has been found up to 1.4 km from one of the Large populations of A. malherbae have sites.

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 308 Chapter 45

Previous releases of A. malherbae made fi eld. It has recently been confi rmed that in 1992–1998 in British Columbia at this species is established in Colorado Kamloops, Grand Forks and Cawston were (Kaltenbach, 2009, 2010), and there are monitored on several occasions from 1999 also reports of populations in Oregon to 2009. Galling was found in 1999 from (Andreas et al., 2012) and Utah (North the 1998 release at Cawston, but no sign of American Moth Photographers Group, establishment has been found subsequently 2012). Pheromone trapping (Cao et al., at any of these sites (S. Turner, Kamloops, 2003) could be useful in confi rming 2012, pers. comm.). whether this species is present, although Two attempts have been made to this was not found to be effective in redistribute A. malherbae from the Colorado (Kaltenbach, 2009). Medicine Hat populations to other C. arvensis infestations since 2000. Infested C. arvensis foliage was released on an organic 45.2 Future Needs farm near Armstrong, British Columbia, in June 2008 and in an irrigated fi eld and a Several further potential biological control nearby roadside at Taber, Alberta, in June agents for C. arvensis were identifi ed by 2009. In both cases, large amounts of galled Tóth and Cagán (2005). Studies on three of tissue containing abundant mites were these, the stem-mining agromyzid fl y released on to vigorous, actively growing Melanagromyza albocilia Hendel (Diptera: stands of C. arvensis. However, no signs of Agromyzidae) and the root-mining fl ea establishment were found at the Armstrong beetles Longitarsus pellucidus Foudras and site when monitored in 2008 and 2009 or L. rubiginosus Foudras (Coleoptera: Chrys- at the Taber sites when monitored in 2012. omelidae) are currently being funded by Continued, sporadic monitoring between the USDA at CABI in Switzerland (Cortat et 2000 and 2012 of two previous releases in al., 2012). If any of these species are Lethbridge, Alberta (i.e. 1994, 1998; approved for release in the USA they could McClay and De Clerck-Floate, 2002) also also be tested in Canada. has turned up no evidence of establish- Therefore, future work should include: ment. Convolvulus arvensis continues to be a 1. Determining the conditions and tech- problematic weed in many parts of Canada niques to promote successful establishment and it would be benefi cial to establish A. of A. malherbae; malherbae more widely. This species has 2. Post-release monitoring better to assess been widely and successfully distributed if T. luctuosa is present at locations where across the western USA (Lauriault et al., it was released; 2004). It is not known if the failures of the 3. Risk assessment of M. albocilia, L. pellu- 2008 and 2009 redistribution releases in cidus and L. rubiginosus under Canadian British Columbia and Alberta were due to conditions if they are found to be suitable environmental conditions at the release as candidate biological control agents. sites, or to problems with release tech- nique. An effective redistribution pro- gramme for this species will depend on a better understanding of the conditions and Acknowledgements techniques required for successful establish- ment. We thank Sandy Cesselli and Susan Turner It is possible that T. luctuosa popu- (BC Ministry of Forests, Lands and Natural lations may still be present at the release Resource Operations) and Fred Beaulieu sites in southern Alberta (McClay and De (Agriculture and Agri-Food Canada) for Clerck-Floate, 2002). As larvae are well information on releases of A. malherbae in camoufl aged and adults are active fl iers, British Columbia and for assistance in they may have escaped detection in the monitoring A. malherbae release sites. Chapter 46 309

References

Andreas, J.E., Coombs, E.M., Milan, J., Piper, G.L. and Schwarzländer, M. (2012) Biological control. In: Peachey, E. (ed.) Pacifi c Northwest Weed Management Handbook. Oregon State University, pp. B1–B6. Cao, W.H., Charlton, R.E., Nechols, J.R. and Horak, M.J. (2003) Sex pheromone of the noctuid moth, Tyta luctuosa (Lepidoptera: Noctuidae), a candidate biological control agent of fi eld bindweed. Environmental Entomology 32, 17–22. Cortat, G., Grosskopf-Lachat, G., Hinz, H.L., Thuis, A. and Tateno, A. (2012) Biological control of fi eld bindweed, Convolvulus arvensis. Annual Report 2011. CAB International, Delémont, Switzerland. De Clerck-Floate, R. and Cárcamo, H. (2011) Biocontrol arthropods: new denizens of Canada’s grassland agroecosystems. In: Floate, K.D. (ed.) Arthropods of Canadian Grasslands, Vol. 2: Inhabitants of a Changing Landscape. Biological Survey of Canada, pp. 291–321. Kaltenbach, J. (2009) Cooperative Agricultural Pest Survey (CAPS) Annual Report Colorado FY 2009. Colorado Department of Agriculture, Plant Industry Division. Kaltenbach, J. (2010) Cooperative Agricultural Pest Survey (CAPS) Annual Report Colorado FY 2010. Colorado Department of Agriculture, Plant Industry Division. Lauriault, L.M., Thompson, D.C., Pierce, J.B., Michels, G.J. and Hamilton, W.V. (2004) Managing Aceria malherbae Gall Mites for Control of Field Bindweed. Cooperative Extension Service Circular 600. New Mexico State University, Las Cruces, New Mexico. McClay, A.S. and De Clerck-Floate, R.A. (2002) Convolvulus arvensis L., fi eld bindweed (Convolvulaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 331–337. North American Moth Photographers Group (2012) Tyta luctuosa. Available at: http:// mothphotographersgroup.msstate.edu/species.php?hodges=9063.1 (accessed 27 August 2012). Tóth, P. and Cagán, L. (2005) Organisms associated with the family Convolvulaceae and their potential for biological control of Convolvulus arvensis. Biocontrol News and Information 26, 17N–40N.

46 Cynoglossum offi cinale (L.), Houndstongue (Boraginaceae)

Rosemarie A. De Clerck-Floate Agriculture and Agri-Food Canada, Lethbridge, Alberta

46.1 Project Status rangelands in the southern interior of British Columbia and south-western Houndstongue, Cynoglossum offi cinale (L.) Alberta in Canada (De Clerck-Floate and (Boraginaceae), is an invasive biennial or Schwarzländer, 2002a). The species is an short-lived perennial of Eurasian origin invader of disturbed sites, such as pad- that has been a problem particularly on docks created through logging for cattle © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 310 Chapter 46

grazing in British Columbia (De Clerck- the province between 1998 and 2002, with Floate, 1997). Until recent success in the some augmentative releases at single sites use of classical biological control, the (Table 46.1). As of the last monitoring year species thrived in dense, large scattered per site, establishment has been confi rmed patches within the forested rangeland at three of ten sites (Table 46.1). In Alberta, habitats of British Columbia (De Clerck- the single release into a propagation plot at Floate and Schwarzländer, 2002a). In Lethbridge, Alberta in 1999 (listed in De Alberta it still occurs in smaller patches on Clerck-Floate and Schwarzländer, 2002a) the Rocky Mountain foothill rangelands or established and then over time moved to within the more mesic micro-habitats various patches of C. offi cinale used in provided by draws or river coulees on dry propagation of M. crucifer. The last con- prairie, but changes in its distribution and fi rmation of its presence was in 2009 abundance are also beginning to happen during a small outbreak of the beetle, but here. Cynoglossum offi cinale is dispersed once M. crucifer had destroyed all known within these habitats mainly through the patches and individuals of C. offi cinale on attachment of its barbed nutlets (burrs) on the propagation plots, L. quadriguttatus to large, grazing animals (De Clerck-Floate, has not been found since. Given how well 1997), which additionally created market- M. crucifer is working by comparison, related concerns for ranchers attempting to continued use of L. quadriguttatus is not auction their burr-covered cattle (Upad- recommended. hyaya and Cranston, 1991). Cynoglossum Confi rmed establishment of M. crucifer, offi cinale also is toxic to livestock because in comparison to L. quadriguttatus, has of its high concentrations of pyrrolizidine proven to be consistently high regardless of alkaloids (Eigenbrode et al., 2008; Stegel- where released, i.e. near 100%, and soon meier, 2011). Consequently, a biological after initial releases of the root weevil in control programme was begun for C. British Columbia there was evidence of offi cinale in Canada in 1988 at the urging impact on large, dense patches of C. of the British Columbia cattlemen (De offi cinale. In an experiment in south- Clerck-Floate and Schwarzländer, 2002a). eastern British Columbia to determine the After nearly 10 years of host-specifi city optimal number of M. crucifer to release to testing by CABI in Europe, fi rst intro- obtain predictable weevil establishment ductions of two biological control agents and C. offi cinale control, 100% of the 20 were made in Canada, beginning with experimental releases became established the root weevil Mogulones crucifer Pallas regardless of release size (100, 200, 300 (=M. cruciger Herbst) (Coleoptera: Curcu- and 400 weevils per site, n=5 replicate lionidae) in 1997 and the root-feeding fl ea sites) (De Clerck-Floate et al., 2005). The beetle Longitarsus quadriguttatus Pontop- established weevils spread quickly to pidan (Coleoptera: Chrysomelidae) in surrounding patches of C. offi cinale, 1998. The biology, circumstances sur- including to three of fi ve control sites (De rounding obtaining regulatory approval for Clerck-Floate et al., 2005; De Clerck-Floate release, and outcomes of early releases in and Wikeem, 2009). Within 3 years of British Columbia and Alberta for both release, M. crucifer had dispersed 1.42 km species were documented in De Clerck- on average through a densely forested Floate and Schwarzländer (2002a). landscape to fi nd its host, and both Of the two available agents, L. quadri- distance from the release patch and the guttatus has been the least redistributed number of M. crucifer released were and the most inconsistently recovered from signifi cant predictors of weevil population release sites. Since its introduction to size within surrounding, newly colonized British Columbia in 1997 (De Clerck-Floate C. offi cinale patches. Within the same and Schwarzländer, 2002a), fi eld releases experiment, M. crucifer populations had of about 4000 beetles in total have been rapidly increased within release patches, made at ten sites in the southern interior of and there was a signifi cant positive Chapter 46 311

Table 46.1. Releases and recoveries of Longitarsus quadriguttatus against Cynoglossum offi cinale in British Columbia, 1998–2002. All releases were of uncaged adults. Release information was obtained from the Invasive Alien Plant Program database (British Columbia Ministry of Forests, Lands and Natural Resource Operations, 2012) and recovery data from provincial biological control agent records held by the British Columbia Ministry of Forests, Lands and Natural Resource Operations, Kamloops. Location Latitude Longitude Year Number Recoveries Osprey Lake 49.71° −120.21° 1998 200 Population found in 1999, 2000–2004, 2006; not found in 2008 and 2009 (last checked) Kamloops 50.67° −120.33° 1999 246 Population found in 2002, 2003; not found in 2000 2001 181 and 2007 (last checked) Westwold 50.47° −119.77° 1999 187 Population found in 2001–2002; not found in 2006 2001 179 and 2007 (last checked) 2002 61 Brookmere 49.82° −120.87° 2000 140 Population found in 2004 only; not found in 2002, 2003, 2005, 2006 and 2008 (last checked) Canford-1a 50.14° −120.99° 2000 200 Population found in 2002–2005; not found in 2006 and 2008 (last checked) Canford-2a 50.14° −120.99° 2000 400 Population found in 2003, 2005 (last checked); not found in 2002 Princeton 49.46° −120.51° 2000 1000 Population found in 2003 only; not found in 2002, 2002 52 2005 and 2008 (last checked) Kingsvale 49.91° −120.91° 2000 500 Population found in 2002 and 2003; not found in 2008 (last checked) Oliver 49.81° −119.55° 2000 328 Population found in 2002 and 2009 (last checked); not found in 2003, 2004, 2006, 2008 Fairview 49.17° −119.60° 2000 337 Population found in 2002, 2005, 2009 (last checked); not found in 2003, 2004, 2006, 2008 aTwo release sites in same area, separated by 2 km. relationship between the number released crucifer (ca. 50:50 sex ratio) for effective and the number of M. crucifer adults and predictable C. offi cinale control (De collected 1 year after release (De Clerck- Clerck-Floate and Wikeem, 2009). Floate and Wikeem, 2009). In terms of Similar rates and levels of C. offi cinale impact, however, C. offi cinale populations control using M. crucifer have consistently were signifi cantly reduced within 2 years and repeatedly been witnessed throughout of release by the same rate and amount the southern interior of British Columbia, regardless of release size. Although a regardless of the biogeoclimatic zone, i.e. drought also was on-going during the variable elevations, moisture and tempera- experiment and generally affected C. ture regimes, soils and plant community offi cinale densities, the reductions in types, and time frame involved. During the density were greater on treatment com- height of M. crucifer dispersal and impact pared to control sites (De Clerck-Floate and in the East Kootenay of British Columbia, Wikeem, 2009). Moreover, when the same i.e. near to the location of above-mentioned sites were resampled 9 years after release, experiment, whole fi elds of dense C. control of C. offi cinale had been sustained, offi cinale were succumbing to attack by with very low densities of C. offi cinale, i.e. dispersing populations of the weevil (R. De typically less than ten plants per site, and Clerck-Floate, 2006, unpublished results). M. crucifer persisting at all sites (R. De In one such ‘houndstongue-fi lled’ fi eld that Clerck-Floate, 2008, unpublished results). was a recently logged clearing of approxi- An important operational recommendation mately 6 ha, M. crucifer was discovered in arising from the study was to use a 2003 on the fi eld’s edge nearest to a release minimum release size of 100 adult M. made in 1999. When revisited in spring 312 Chapter 46

2007, only a few plants remained that were CAN$0.10 to CAN$0.14 per weevil using heavily attacked by M. crucifer. The native, the ‘farming method’ compared to resident species, Lithospermum ruderale CAN$2.65 per weevil when using the more Douglas ex Lehm. and Lappula squarrosa energy- and labour-intensive method of (Retz.) Dumort. (Boraginaceae), however, laboratory rearing M. crucifer (Smith et al., showed no signs of attack by M. crucifer, 2009). Methods also were developed for and their populations appeared to be collecting and sorting the large numbers of thriving. Although not as dramatic or adult weevils produced in spring 2004– rapid, control of C. offi cinale by M. crucifer 2006, which were explained to stake- in southern Alberta also has been evident. holders during extension events. This Between 2009 and 2011, ten release sites suc cessful biological control delivery from 2000 to 2002 were revisited in search project produced over 85,000 insects for of C. offi cinale, and in each location very ranchers and land managers in southern few plants were found relative to patch British Columbia (De Clerck-Floate et al., size at the time of M. crucifer release (R. De 2006; Moyer et al., 2007), and greatly Clerck-Floate, 2009–2011, unpublished accelerated the redistribution of M. cruci- results). Although in need of more rigorous fer. Based on increased propagation efforts quantifi cation, these observations suggest at Lethbridge associated with the project, that M. crucifer has had a profound impact southern Alberta also indirectly benefi ted, on C. offi cinale populations, despite recent and between 2004 and 2012 approximately model predictions that European specialist 16,500 M. crucifer were redistributed to herbivores would be less important than 123 new C. offi cinale sites, mostly on disturbance in driving the population ranches in the southern foothills (R. dynamics of C. offi cinale in its introduced Wilson, Lethbridge and H. Catton, range (Williams et al., 2010). Hypotheses Kelowna, 2012, pers. comm.). on why M. crucifer is effective also require A spin-off from the farm propagation testing, but one possibility is that root project resulted upon learning that the damage caused by M. crucifer larval addition of nitrogen fertilizer signifi cantly feeding is capable of quickly killing C. increased weevil production, partly offi cinale rosettes because C. offi cinale is because the host plants grow larger with on the edge of its ecological limit for fertilization, but also because female moisture requirements in the ‘hot and dry weevils lay about 25% more eggs on summer’ regions of southern British nitrogen-rich plants regardless of plant size Columbia and Alberta. (Van Hezewijk et al., 2008). Using this Once it was realized that M. crucifer knowledge, a fi eld experiment was was showing promise as an effective developed to test the idea of fertilizing biological control agent, demand for its use natural patches of C. offi cinale on by interested stakeholders increased. As a rangelands in British Columbia to boost M. result, a research project was developed to crucifer production for later redistribution investigate the feasibility of using cropping by ranchers, and to potentially accelerate methods to grow C. offi cinale for weevil C. offi cinale control. The addition of production versus laboratory rearing. Set nitrogen to rangeland C. offi cinale (150 kg up on farmland in Creston, British ha−1) signifi cantly increased weevil pro- Columbia and Lethbridge, Alberta (2002– duction, however, M. crucifer worked just 2006), numerous agronomic conditions for as rapidly in controlling C. offi cinale (2 growing healthy C. offi cinale plants for years) regardless of nitrogen addition (R. weevil production were explored, includ- De Clerck-Floate, 2011, unpublished ing use of fertilization, timing, depth and results). Mogulones crucifer worked so spacing of planting, and methods of weed effi ciently in both the farm propagation and disease control within the C. offi cinale and rangeland fertilization projects that ‘crop’. An associated economic analysis they quickly overwhelmed and killed the estimated a 2009 production cost of majority of available C. offi cinale plants, Chapter 46 313

including the trap plants grown for their lations in southern Alberta. A preliminary collection in the former project, and summary of data revealed that non-target forcing an early termination of the latter attack by M. crucifer is low and sporadic experiment (De Clerck-Floate, 2011). relative to its primary host, C. offi cinale, Despite the success with M. crucifer in and appears to be temporary (‘spillover’) in Canada, the weevil species has not occurrence (Catton et al., 2012). obtained regulatory approval for release in the USA and is now a declared plant pest in the USA (United States Department of 46.2 Future Needs Agriculture, Animal and Plant Health Inspection Service, 2010). The concerns Future work should include: outlined in De Clerck-Floate and Schwarz- 1. On-going monitoring of occurrence and länder (2002a) over endangered Boragina- impact of feeding by M. crucifer on non- ceae species listed federally in the USA target Boraginaceae spp. individuals and have not only persisted, but have grown populations at Canadian fi eld sites; with the listing of three more federally 2. Documenting the response of native endangered species since the fi rst release of plant communities as M. crucifer controls M. crucifer in Canada in 1997, i.e. C. offi cinale. Plagiobothrys strictus (Greene) I.M. Johnst. (listed November, 1997), P. hirtus (Greene) No further biological control agents are I.M. Johnst. (listed February, 2000) and required for Canada. Hackelia venusta (Piper) H. St. John (listed March, 2002) (United States Fish and Wildlife Service, 2012). Hackelia venusta, Acknowledgements especially, is of concern because of the occurrence of its small, endemic popu- Information on insect releases and lations in the Cascade Mountains of north- monitoring were gratefully provided by R. central Washington State, which are Bourchier, B. Van Hezewijk, R. Wilson relatively close to potential sources of (Alberta), S. Turner, S. Cesselli, M. DeWolf Canadian M. crucifer. As part of the (British Columbia). E. Pavlik and numerous Canadian biological control programme for summer students are thanked for laboratory C. offi cinale, native Boraginaceae species root dissections, insect rearing efforts and occurring at M. crucifer release sites in help with host specifi city experiments. British Columbia and Alberta continue to Colleagues, participants and friends, J. be monitored to verify previous laboratory Andreas, R. Bourchier, H. Catton, A. Dalcin, and fi eld study results on the weevil’s host R. Lalonde, C. and C. Larson, V. Miller, J. range (De Clerck-Floate and Schwarz- Moyer, G. Roy, M. Schwarzländer, E. Smith, länder, 2002b; Andreas et al., 2008). Both S. Sweet, B. Stewart, B. van Hezewijk, R. fi eld and laboratory testing of the USA Wesselingh and B. Wikeem are thanked for endangered annual, P. hirtus, and a their valuable discussions, observations, Canadian listed endangered annual contributions and insights on the amazing species, Cryptantha minima Rydb. M. crucifer–houndstongue success story. (Boraginaceae) (Government of Canada, Support for houndstongue biological 2012), revealed no risk to these species control research over the past 12 years was from M. crucifer feeding and development provided by: Agriculture and Agri-Food (De Clerck-Floate and Schwarzländer, Canada, Boundary Weed Management 2002b). Furthermore, a long-term fi eld Committee, British Columbia Ministry of experiment was recently conducted (2009– Forests, Range and Natural Resource 2011) to assess and compare feeding and Operations, British Columbia Transmission impact by M. crucifer on the non-target Corporation, Canadian Pacifi c Railway, Hackelia micrantha (Eastw.) J.L. Gentry Creston Valley Beefgrowers Association, (Boraginaceae) and on C. offi cinale popu- Grand Forks Stockbreeder’s Association, 314 Chapter 46

Inter-Ministry Invasive Plant Council, Stockmen’s Association, Terasen Gas, Investment Agriculture Foundation of BC, Tembec Industries Kootenay East Region Kettle River Stockmen’s Association, and Wyoming Weed and Pest Districts Kootenay Livestock Association, Rock Biological Control Steering Committee, and Creek Farmers’ Institute, Southern Interior University of British Columbia Okanagan.

References

Andreas, J.E., Schwarzländer, M. and De Clerck-Floate, R. (2008) The occurrence and potential relevance of post-release, nontarget attack by Mogulones cruciger, a biocontrol agent for Cynoglossum offi cinale in Canada. Biological Control 46, 304–311. British Columbia Ministry of Forests, Lands and Natural Resource Operations (2012) Invasive Alien Plants Program. Available at: http://www.for.gov.bc.ca/hra/plants/index.htm (accessed 12 November 2012). Catton, H., De Clerck-Floate, R.A. and Lalonde, R.G. (2012) Temporary spillover? Patch-level nontarget attack by the biocontrol weevil Mogulones crucifer. In: Wu, Y., Johnson, T., Sing, S., Raghu, S., Wheeler, G., Pratt, P., Warner, K., Center, T., Goolsby, J. and Reardon, R. (eds) Proceedings of the XIII International Symposium on Biological Control of Weeds. Waikoloa, Hawaii, United States, 11–16 September 2011. FHTET-2012-07. US Forest Service Morgantown,West Virginia (in press). De Clerck-Floate, R. (1997) Cattle as dispersers of hound’s-tongue on rangeland in southeastern British Columbia. Journal of Range Management 50, 239–243. De Clerck-Floate, R. (2011) A nose for success: Hound’s-tongue biocontrol weevils work without reward. Beef in BC 46, 46–48. De Clerck-Floate, R.A. and Schwarzländer, M. (2002a) Cynoglossum offi cinale (L.), houndstongue (Boraginaceae). In: Mason P.G. and Huber J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 337–343. De Clerck-Floate, R. and Schwarzländer, M. (2002b) Host specifi city of Mogulones cruciger (Coleoptera: Curculionidae), a biocontrol agent for houndstongue (Cynoglossum offi cinale), with emphasis on testing of native North American Boraginaceae. Biocontrol Science and Technology 12, 293–306. De Clerck-Floate, R. and Wikeem, B. (2009) Infl uence of release size on establishment and impact of a root weevil for the biocontrol of houndstongue (Cynoglossum offi cinale). Biocontrol Science and Technology 19, 169–183. De Clerck-Floate, R.A., Wikeem, B. and Bourchier, R.S. (2005) Early establishment and dispersal of the weevil, Mogulones cruciger (Coleoptera: Curculionidae) for biological control of houndstongue (Cynoglossum offi cinale) in British Columbia, Canada. Biocontrol Science and Technology 15, 173–190. De Clerck-Floate, R.A., Moyer, J.R., Van Hezewijk, B.H. and Smith, E.G. (2006) Farming weed biocontrol agents: a Canadian test case in insect mass-production. In: Clements, D.R. and Darbyshire S.J. (eds) Topics in Canadian Weed Science, Vol. 5, Invasive plants. Canadian Weed Science Society, Sainte-Anne-de Bellevue, Quebec, pp. 111–130. Eigenbrode, S.D., Andreas, J.E., Cripps, M.G., Ding, H., Biggam, R.C. and Schwarzländer, M. (2008) Induced chemical defenses in invasive plants: a case study with Cynoglossum offi cinale L. Biological Invasions 10, 1373–1379. Government of Canada (2012) Species at Risk Public Registry. Available at: http://www.sararegistry. gc.ca/sar/index/default_e.cfm (accessed 1 December 2012). Moyer, J.R., De Clerck-Floate, R.A., Van Hezewijk, B.H. and Molnar, L.J. (2007) Agronomic practices for growing houndstongue (Cynoglossum offi cinale) as a crop for mass-producing a weed biocontrol agent. Weed Science 55, 273–280. Smith, E.G., De Clerck-Floate, R.A., Van Hezewijk, B.H., Moyer, J.R. and Pavlik, E. (2009) Costs of mass-producing the root weevil, Mogulones cruciger, a biological control agent for houndstongue (Cynoglossum offi cinale L.). Biological Control 48, 281–286. Chapter 47 315

Stegelmeier, B.L. (2011) Pyrrolizidine alkaloid-containing toxic plants (Senecio, Crotalaria, Cynoglossum, Amsinckia, Heliotropium, and Echium spp.). Veterinary Clinics of North America: Food Animal Practice 27, 419–428. United States Department of Agriculture, Animal and Plant Health Inspection Service (2010) Pest Alert. Mogulones cruciger. Plant Protection and Quarantine March 2010. Animal and Plant Health Inspection Service, 81-35-014. United States Fish and Wildlife Service (2012) Species Reports, Environmental Conservation Online System. Available at: http://ecos.fws.gov/tess_public/pub/listedPlants.jsp (accessed 1 December 2012). Upadhyaya, M.K. and Cranston, R.S. (1991) Distribution, biology, and control of hound’s-tongue in British Columbia. Rangelands 13, 103–106. Van Hezewijk, B.H., De Clerck-Floate, R.A. and Moyer, J.R. (2008) Effect of nitrogen on the preference and performance of a biological control agent for an invasive plant. Biological Control 46, 332– 340. Williams, J.L., Auge, H. and Maron, J.L. (2010) Testing hypotheses for exotic plant success: Parallel experiments in the native and introduced ranges. Ecology 91, 1355–1366.

47 Euphorbia esula L., Leafy Spurge (Euphorbiaceae)

Rob S. Bourchier1 and Brian H. Van Hezewijk2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2Natural Resources Canada, Canadian Forest Service, Victoria, British Columbia

47.1 Project Status defoliate the plants when the beetles are at high density (Bourchier et al., 2002, 2006; Euphorbia esula L. (Euphorbiaceae) was Kalischuk et al., 2004; Larson et al., 2008). one of the early targets for biological There have been no new biological control control in Canada with the programme agents released for E. esula since 1997, starting in 1962 and the fi rst agent, Hyles when a mixed population of Aphthona euphorbiae (L.) (Lepidoptera: Sphingidae), czwalinae Weise and A. lacertosa Rosen- released in 1965 (Harris, 1984). Bourchier hauer (Coleoptera: Chrysomelidae), col- et al. (2002) and Harris (1984) reviewed the lected from North Dakota, was released at ecology of all of the biological control multiple locations in Alberta, Saska- agents released for E. esula in Canada. The tchewan and Manitoba (Bourchier et al., most successful biological control agents 2002). have been fl ea beetles, Aphthona spp. The primary focus of the spurge (Coleoptera: Chrysomelidae), whose larvae biological control project since 2000 has feed on the roots of E. esula and adults been: (i) characterization of the relative

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 316 Chapter 47

abundance of Aphthona spp. in recently identifi ed the presence of three clades of A. established and historical populations; (ii) lacertosa, suggesting the presence of a understanding the impact and spread of possible cryptic species (Roehrdanz et al., the Aphthona spp.; and (iii) operational 2009). It is possible that one of these clades release programmes to redistribute, estab- is a morphological variant of A. czwalinae. lish and increase Aphthona spp. popu- Specimens from the two Cardston sites lations in all regions affected by E. esula. were selected for study because these sites The fi ve Aphthona spp. and year of fi rst were initial release locations for black- release in Canada are Aphthona cyparis- bodied Aphthona spp. in 1990. Roehrdanz siae (Koch) (1982), A. fl ava Guillebeau et al. (2009) also looked at early release (1982), A. nigriscutis Foudras (1983), A. sites for all three of the brown-bodied czwalinae (1985) and A. lacertosa (1990) beetle species and identifi ed sites with (Julien and Griffi ths, 1998; Bourchier et al., populations that were dominated by A. 2002). The fi rst three species have brown cyparissiae and A. fl ava. This suggests that or golden bodies and the latter two species although A. cyparissiae and A. fl ava have are entirely black. Species identifi cation is not been intentionally or actively based primarily on genitalia, but some redistributed, they are able to persist in external morphological characters are also some locations over long periods (15–20 useful (LeSage and Paquin, 1996). A sixth years since initial releases) and may have species, the brown-bodied Aphthona additional unexploited potential for abdominalis (Duftschmid), has been biological control of E. esula. In 2011–2012 released in the USA but is not known to be additional studies of Aphthona spp. present in Canada (Bourchier et al., 2006). populations were initiated in Alberta, In post-release evaluation of E. esula Saskatchewan and Manitoba to investigate biological control, Aphthona spp. have this potential. Returning to historical been cited as a biological control success black-beetle release sites near Cardston and story because they are having signifi cant using CO1 gene sequences, we have con- impacts on the target plant (Larson et al., fi rmed the presence of the three genetic 2008). Successful biological control of E. clades reported by Roehrdanz et al. (2009) esula, which has resulted in signifi cant in populations of black-bodied beetles and economic benefi ts for producers (Bangsund that these three clades correspond morpho- et al., 1999), has been attributed to pri- logically to A. lacertosa (L. Lesage, Ottawa, marily two of the fi ve species: A. Ontario, 2012, pers. comm.; R. Bourchier nigriscutis in drier, sandy sites and A. and K. Floate, 2012, unpublished results). lacertosa in moister locations (Bourchier et On-going studies will hopefully confi rm al., 2006; Larson et al., 2008). the taxonomic status of these three groups In recent molecular studies of Aphthona of beetles, as well as sampled populations spp. collected from several US states and at redistribution sites across the prairies, Alberta (Roehrdanz et al., 2006, 2009, and provide guidance on their potential for 2011) there was a greater diversity of diversifying the pool of biological control Aphthona spp. than expected. Aphthona agents. czwalinae has been externally differen- Studies on impact and spread of tiated from A. lacterosa by the black colour Aphthona spp. have focused on under- of its hind femur (LeSage and Paquin, standing the density interactions between 1996); based on this character and the beetles and E. esula, initially on a local examination of thousands of beetles since patch scale, with the goal of applying this 1997, A. czwalinae was believed to be very knowledge to understand spread and rare in Canada and the USA (Roehrdanz et dispersal at larger spatial scales. Using al., 2009). However, a population of A. manipulative release experiments in small, czwalinae was found in North Dakota, and isolated patches of E. esula, the local genetic variation based on CO1 sequences dispersal of A. lacertosa individuals in specimens from Cardston, Alberta has been shown to be independent of Chapter 47 317

conspecifi cs at densities between 250 and biological control. The programme initially 2500 beetles m−2 (Van Hezewijk and targeted E. esula and subsequently knap- Bourchier, 2005). This tolerance for a high weed, Centaurea spp. (Asteraceae), toad- degree of crowding is one factor that is fl ax, Linaria spp. (Plantaginaceae), and thought to play a role in the effi cacy of this houndstongue, Cynoglossum offi cinale L. species in reducing E. esula densities at the (Boraginaceae), were added when effective local scale. In two separate experiments, A. biological control agents became available lacertosa were found to develop non- in suffi cient numbers. For E. esula, there random aggregations over time but no clear have been 485 documented and monitored pattern has emerged to explain where these releases of Aphthona beetles between 2001 aggregations form. The density of E. esula and 2012, primarily in southern Alberta, ramets seems to have a positive effect on A. south of the Trans-Canada Highway. The lacertosa aggregation (Van Hezewijk and focus has been on redistribution of A. Bourchier, 2005), but this does not seem to lacertosa because this species was the most translate into increased population growth recent introduction to the area (1997); we (R. Bourchier, 2012, unpublished results). had observed very high-density beetle Based on repeated intensive sampling at populations at some 1997 release sites by one site near Pincher Creek, Alberta, the 2000 (Bourchier et al., 2002); it has a emergence and subsequent redistribution shorter degree-day requirement than other patterns of a population of A. lacertosa was Aphthona spp. (Skinner et al., 2004) and it determined (B. Van Hezewijk and R. appears to be able to establish in a wider Bourchier, 2012, unpublished data). variety of habitats and soil types in Aphthona lacertosa adults were found to southern Alberta than other Aphthona spp. emerge fi rst from areas closest to the initial (Kalischuk et al., 2004; R. Bourchier, 2012, release, and subsequently from areas unpublished results). The key components further away. Across the entire site, A. for the successful establishment rates lacertosa emergence occurred from late (>90% in all years) observed during this June into the third week of August, which project have been that all releases were was a much longer period than expected. done by project staff, which facilitated Although movement was not measured selection of suitable release sites; releases directly, the pattern of redistribution of were planned directly with landowners adults suggests that movement rates are ensuring their ‘ownership’ and thus greatest in the areas of high impact (and preservation of release location; and there lowest spurge density), and A. lacertosa was follow-up and monitoring of beetle movement is arrested at the leading edge of establishment by returning staff. Between the outbreak, resulting in a radial expan- 2001 and 2005, Aphthona spp. were sion of the impact area. Contrary to the sourced from high density populations in predictions of most population spread North Dakota or Montana and thus were models, it appears that in this case the rate expected to include a mixed population of of spread was not constant but acceler- A. lacertosa and A. czwalinae. In 2006 and ating. This might be the result of a fat- thereafter, all releases used Aphthona spp. tailed dispersal kernel (Lewis, 1997) as collected from local nursery sites that had would occur given differential dispersal been developed as part of the project. rates within and beyond the zone of There are now signifi cant, high density impact. Quantifying these rates will be populations of Aphthona spp. that are important for scaling up the small-scale suppressing E. esula at local release sites in population processes to landscape-scale all seven of the initial participating distribution and impact. municipal districts in southern Alberta. On Since 2001 there has been a collabor- a regional scale it is diffi cult to evaluate the ative project between the municipal dis- success of the E. esula biological control tricts of Southern Alberta and AAFC for agents because the area infested in the the operational implementation of weed release zone is a moving target. Since 2001, 318 Chapter 47

there have been two ‘100 year fl ood’ events ution programmes using both US collected in wide areas of southern Alberta, in 2002 beetles (estimated 95,000 beetles imported and 2005. These fl ood events resulted in from North Dakota between 2001 and signifi cant spread and re-colonization of 2009) and local beetles by Department of river fl ats with E. esula along major rivers National Defence–Shilo, and the Rural in the area (R. Bourchier, 2012, unpub- Municipalities in the south-west weed lished results). A scientifi c assessment is district (B. Dunlop, Brandon, Manitoba, further compounded by a lack of regional 2012, pers. comm.). These redistribution baseline data for E. esula distribution, programmes have included mixes of brown which is a key data gap to be addressed and black Aphthona spp. with an emphasis across the prairies. towards brown beetles for sandy soils in In Saskatchewan, there has been an on- areas such as Spruce Woods Provincial going operational redistribution pro- Park and Department of National Defence– gramme of mixed populations of brown Shilo. Thus, with the combination of and black Aphthona spp. for biological populations dispersing from early release control of E. esula. Beetles are distributed sites and multiple sources of redistributed primarily through fi eld days where beetles collected over the past 20 years, the producers, rural municipalities staff, First Aphthona spp. composition in Manitoba Nations groups and government agencies may have a similar diversity to Alberta. responsible for land management attend to Much of the historical point data for E. collect beetles for their own use. Since esula site locations in Manitoba and 2001, an average of 200,000 Aphthona spp. Saskatchewan has been captured in the adults per year have been collected during Prairie Regional Invasive Plants database fi eld days. These beetles have been currently housed at the University of redistributed to at least 80 sites per year. Saskatchewan (PRIPS, 2012). The PRIPS The beetles for these releases were sourced data for both provinces, as well some new from primarily two nursery site locations records up to 2012 for Manitoba, has been in Saskatchewan. However, there were also transferred and is viewable on EDDMapS two supplemental collections of an (2012). Additional consolidation of E. estimated 200,000 Aphthona spp. from esula distribution and biological control Montana and North Dakota that were used agent release data from both provinces and for redistribution, in two separate years current molecular studies will assist to during the 2001 to 2012 period. Follow-up clarify the beetle species composition. on the new release locations resulting from The E. esula biological control pro- fi eld days has been limited because this is gramme is a success in that there are only possible if the landowner submits effective agents established that can reduce their release site details to Saskatchewan weed populations signifi cantly (Kalischuk Agriculture. There is a historical database et al., 2004; Bourchier et al., 2006; Larson of approximately 350 release sites of which et al., 2008) and which provide measurable between 50 and 75 are qualitatively economic benefi ts (Bangsund et al., 1999). monitored each year (Harvey Anderson, Because it was one of the fi rst weed Saskatoon, Saskatchewan, 2012, pers. biological control targets, the E. esula pro- comm.). gramme has had infl uence on other bio- In Manitoba, all of the fi ve Aphthona logical control projects. It was, for spp. were released between 1982 and 1996 example, one of the fi rst to use the now- (Bourchier et al., 2002). There were standard, consortium approach to engage multiple collection trips to the USA, multiple stakeholders to fund the long- primarily North Dakota, by members of the term projects required for successful host- weed control community, e.g. Leafy Spurge range testing of biological control agents. Stakeholders Group, to collect Aphthona Success has taken a long time to develop spp. for redistribution prior to 2000. Since and biological control practices especially 2001 there have been on-going redistrib- those associated with host-range testing Chapter 47 319

have changed dramatically since 1965. to monitor the benefi ts of this weed biolog- New biological control agents would ical control and other management pro- require extensive testing for target impacts grammes. and non-target effects. However, for E. esula, we believe there is signifi cant potential for further improving biological Acknowledgements control by understanding the genetic diversity and impacts of the agents that Funds for on-going research on leafy have already been released. spurge have been provided by AAFC Matching Investments Initiative and AAFC Peer Review funding programmes. We 47.2 Future Needs thank Ray Wilson, Monte Thomson, Stephanie Erb, Karma Tiberg and Leah Future work should include: Blair and many student summer assistants 1. Use of DNA and morphological studies for their help with the project. Thanks to to continue to characterize the species Harvey Anderson (Invasive Alien Group composition of established, historical Planning Advisor, Saskatchewan Agri- release and high density populations of culture) and Bev Dunlop (AAFC – Science Aphthona spp. throughout the prairies in and Technology Branch, Brandon), for order to identify species complexes for gathering information regarding spurge redistribution and nursery sites; biological control activities in Saska- 2. Expanding operational release pro- tchewan and Manitoba, respectively. The grammes to include Manitoba and continue research programme could not have been programmes to redistribute, establish nurs- conducted without the enthusiastic partici- ery sites and increase Aphthona spp. popu- pation in the operational release pro- lations in all Canadian regions affected by gramme by many Alberta Agricultural E. esula; Fieldmen; special thanks to Jon Hood, Rod 3. Consolidation of available data sources Foggin, Kelly Cooley, Ron Mackay and on E. esula distribution to improve esti- Doug Henderson for their early and mates of economic impact of E. esula and continued support.

References

Bangsund, D.A., Leistritz, F.L. and Leitch, J.A. (1999) Assessing economic impacts of biological control of weeds: the case of leafy spurge in the northern Great Plains of the United States. Journal of Environmental Management 56, 35–43. Bourchier, R.S., Erb, S., McClay, A.S. and Gassmann, A. (2002) Euphorbia esula (L.), leafy spurge, and Euphorbia cyparissias (L.), cypress spurge (Euphorbiaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 346–358. Bourchier, R., Hansen, R., Lym, R., Norton, A., Olson, D., Bell Randall, C., Schwarzlaender, M. and Skinner, L. (eds) (2006) Biology and Biological Control of Leafy Spurge. United States Department of Agriculture Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, USDA-FHTET-2005-07, p.138. EDDMapS (2012) EDDMapS Prairie Region Manitoba and Saskatchewan. Available at: http://www. eddmaps.org/prairieregion (accessed 26 November 2012). Harris, P. (1984) Euphorbia esula-virgata complex, leafy spurge and E. cyparissias L., cypress spurge (Euphorbiaceae). In: Kelleher, J.S. and Hulme, M.A. (eds) Biological Control Programmes against Insects and Weeds in Canada 1969–1980. Commonwealth Agricultural Bureaux, Slough, UK, pp. 159–169. 320 Chapter 47

Julien, M.H. and Griffi ths, M.W. (eds) (1998) Biological Control of Weeds. A World Catalogue of Agents and their Target Weeds, 4th edn. CAB International, Wallingford, UK. Kalischuk, A.R., Bourchier, R.S. and McClay, A.S. (2004) Post hoc assessment of an operational biocontrol program: effi cacy of the fl ea beetle Aphthona lacertosa Rosenhauer (Chrysomelidae: Coleoptera), an introduced biocontrol agent for leafy spurge. Biological Control 29, 418–426. Larson, D.L., Grace, J.B. and Larson, J.L. (2008) Long-term dynamics of leafy spurge (Euphorbia esula) and its biocontrol agent, fl ea beetles in the genus Aphthona. Biological Control 47, 250– 256. LeSage, L. and Paquin, P. (1996) Identifi cation keys for Aphthona fl ea beetles (Coleoptera: Chrysomelidae) introduced in Canada for the control of spurge (Euphorbia spp., Euphorbiaceae). The Canadian Entomologist 128, 593–603. Lewis, M.A. (1997) Variability, patchiness, and jump dispersal in the spread of an invading population. In: Tilman, D. and Kareiva, P. (eds) Spatial Ecology: The role of space in population dynamics and interspecifi c interactions. Monographs in Population Biology No. 30. Princeton University Press, Princeton, New Jersey, pp. 46–69. PRIPS (Prairie Regional Invasive Plants) (2012) Website. Available at: http://prips.usask.ca (accessed 26 November 2012). Roehrdanz, R., Olson, D., Bourchier, R., Sears, S., Cortilet, A. and Fauske, G. (2006) Mitochondrial DNA diversity and Wolbachia infection in the fl ea beetle Aphthona nigriscutis (Coleoptera: Chrysomelidae) an introduced biocontrol agent for leafy spurge. Biological Control 37, 1–8. Roehrdanz, R., Olson, D., Fauske, G., Bourchier, R., Cortilet, A. and Sears, S. (2009) New DNA markers reveal presence of Aphthona species (Coleoptera: Chrysomelidae) believed to have failed to establish after release into leafy spurge. Biological Control 49, 1–5. Roehrdanz, R., Bourchier, R., Cortilet, A., Olson, D. and Sears, S. (2011) Phylogeny and genetic diversity of fl ea beetles (Aphthona sp.) introduced to North America as biological control agents for leafy spurge. Annals of the Entomological Society of America 104, 966–975. Skinner, L.C., Ragsdale, D.W., Hansen, R.W., Chandler, M.A. and Moon, R.D. (2004) Temperature- dependent development of overwintering Aphthona lacertosa and A. nigriscutis (Coleoptera: Chrysomelidae): Two fl ea beetles introduced for the biological control of leafy spurge, Euphorbia esula. Environmental Entomology 33, 147–154. Van Hezewijk, B.H. and Bourchier, R.S. (2005) Is two company or a crowd: how does conspecifi c density affect the small-scale dispersal of a weed biocontrol agent? Biocontrol Science and Technology 15, 191–205. Chapter 48 321

48 Fallopia japonica (Houtt.) Ronse Decraene, Japanese Knotweed, Fallopia sachalinensis (F. Schmidt) Ronse Decraene, Giant Knotweed, Fallopia × bohemica (Chrtek & Chrtková) J. P. Bailey, Bohemian Knotweed (Polygonaceae)

Rob S. Bourchier,1 Fritzi Grevstad2 and Richard Shaw3 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2Oregon State University, Corvallis, Oregon, USA; 3CABI, Egham, UK

48.1 Pest Status seeds if there is a pollinator available), male fl owers (producing no seed) and Japanese knotweed, Fallopia japonica hermaphroditic fl owers (producing few (Houtt.) Ronse Decraene (Polygonaceae), is seeds). Although the seeds have high native to East Asia, including Japan, China, germination rates in the laboratory, Korea and Taiwan. Giant knotweed, seedling establishment in the fi eld occurs Fallopia sachalinensis (F. Schmidt) Ronse infrequently (Forman and Kesseli, 2003; Decraene (Polygonaceae), is native to Engler et al., 2011). Field reproduction northern Japan and Sakhalin Island. appears to occur mainly through clonal Hybrid forms of knotweed, Fallopia × fragmentation of stems and rhizomes. bohemica (Chrtek & Chrtková) J. P. Bailey Fallopia spp. have invaded North (Polygonaceae) can be found in Japan at America, Europe, New Zealand and mid-latitudes and F. japonica is primarily Australia and are listed among the ‘world’s found in southern Japan (Shaw et al., worst invasive species’ by the World 2009). Knotweeds are herbaceous per- Conservation Union (Lowe et al., 2000). ennials sprouting each year by midsummer Both F. japonica and F. sachalinensis are to form dense thickets of tall stalks, 1–4 m classed as noxious in British Columbia and high with large leaves (Freeman and Alberta. As concern for invasive plants has Reveal, 2005). Flowering occurs in increased, many jurisdictions are revising September and seeds ripen in October. weed lists (initially drafted based on Fallopia spp. in North America are agricultural concerns) to consider a broader variably reported as either dioecious or spectrum of invasive plants. While F. gynodioecious (Stone, 2010). However, we japonica is listed as noxious for only two have found evidence for subdioecy (or provinces, it is listed as an invasive species ‘leaky dioecy’) in which there are plants of concern in nine provinces. There are with female fl owers (producing copious signifi cant Fallopia spp. populations in

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 322 Chapter 48

Ontario, which are most commonly F. 48.2 Background japonica or hybrids based on fi eld data (Bourchier and Van Hezewijk, 2010; Management of Fallopia spp. through Anderson, 2012). In British Columbia, F. conventional means is generally con- japonica is the most common of the three sidered to be a long-term venture. A UK species based on records in the Invasive meta-analysis reviewing 65 articles and Alien Plant Program (IAPP, 2012), with the considering six categories of intervention number of records for F. sachalinensis and found that none could eradicate F. japonica × F. × bohemica at approximately 10% of or Fallopia bohemica in the short term those for F. japonica. While there may be (Kabat et al., 2006). There were some some cases of misidentifi cation of F. combined treatments of cutting and herbi- japonica sites that are actually hybrids, the cides that were successful in causing relative abundance of Fallopia spp. records statistically signifi cant reductions in F. by species in IAPP has remained consistent japonica abundance in the short term, but between 2008 (Bourchier and Van the authors were still unable to conclude Hezewijk, 2010) and 2012. long-term effi cacy for any control measure Fallopia spp. have signifi cant negative (Kabat et al., 2006). As knotweeds have ecological impacts on native plant been a serious problem in the UK longer (Siemens and Blossey, 2007; Murrell et al., than in North America, there is a large 2011; Urgenson et al., 2012) and database and experience with attempts to invertebrate communities (Beerling and eradicate Fallopia spp., which has been Dawah, 1993; Kappes et al., 2007; Gerber et captured in extensive codes of practice for knotweed management (UK Environment al., 2008; McIver and Grevstad, 2010), soil Agency, 2007). Conventional approaches properties and nutrient cycling (Dasson- for management that have been tested ville et al., 2007; Aguilera et al., 2010). include: cutting, mowing, fi re, root Lacking fi ne roots near the surface, membrane barriers, geotextile fabrics over Fallopia spp. are less able to hold the plants, soil sterilization and chemical surface soil and can cause increased herbicides (Kabat et al., 2006; McHugh, erosion along stream banks (Child et al., 2006; UK Environment Agency, 2007; 1992). Fallopia spp. stems break off and Bashtanova et al., 2009; Anderson, 2012). wash away in winter leaving the soil Current management approaches target the surface exposed and broken stems can also rhizome because of its long persistence and cause dams and fl ooding in streams. because movement of small pieces of Fallopia spp. can cause costly damage to rhizome is the major method of spread for infrastructure with roots and rhizomes the weed. As a rule of thumb the area of capable of cracking concrete and asphalt infestation or spread of the rhizome is 7 m (Shaw and Seiger, 2002). Estimates for the horizontally from the nearest growth of F. cost of Fallopia spp. removal in North japonica that can be seen (UK Environment America are diffi cult to obtain, in part Agency, 2007). There are active control because complete eradication from an area programmes for Fallopia spp. in multiple or river system requires repeated treatment provinces and states. British Columbia and over a very long time. However, costs Ontario (Anderson, 2012) are currently estimated in the UK range between £800 developing or revising Best Management and £8000 per infested square metre. For Practices documents. Wide-scale eradi- the entire UK, annual costs were estimated cation of Fallopia spp. is highly unlikely at over £165m (Williams et al., 2010). The because of the size of the Fallopia spp. size of the infested range in North America invasion in North America, the inaccess- is far larger than in the UK with continuing ibility of some of the infestations and the local and regional expansion of popu- cost and diffi culty of killing the plants. lations likely (Bourchier and Van Effective management is additionally Hezewijk, 2010). limited because Fallopia spp. are often Chapter 48 323

found in riparian zones where application specifi c for further consideration. The of herbicides is undesirable and restricted. beetle Euops chinensis Voss (Coleoptera: In British Columbia, the province with Attelabidae) from China feeds on the edge the most serious Fallopia spp. problem, of knotweed leaves and has been found to broad-spectrum herbicide use is oper- be host specifi c in preliminary testing ationally restricted to 10 m above the high- (Wang et al., 2010). However, the damage water mark in riparian zones (V. Miller, infl icted by this insect is somewhat limited Nelson, British Columbia, 2012, pers. and some key non-target plant species from comm.). Specifi c applications for Fallopia North America have not yet been tested. spp. growing within riparian areas are only Preliminary testing has been carried out on possible using Glyphosate hand wipes or two pathogens: a Puccinia sp. (Puccinia- stem injection and only up to 1 m from the ceae) and a leafspot fungus as part of the high-water mark. These application UK biological control programme. The methods are extremely costly and time Puccinia sp. was not host-specifi c enough intensive. Fallopia spp. are often found (Kurose et al., 2009a) whereas the leafspot, growing right up to the water’s edge, Mycosphaerella polygoni-cuspidati Hara making their long-term management (Mycosphaerellaceae) (Kurose et al., extremely diffi cult. Best management 2009b), is still under investigation, after practices in Ontario, the UK and the USA promising initial results from specifi city all emphasize vigilance to prevent the testing. spread of Fallopia spp. There are many Aphalara itadori (Shinji) (=Psylla areas that are suitable for Fallopia spp. that itadori Shinji) (Hemiptera: Psyllidae) is the are not yet infested (Bourchier and Van most promising arthropod biological Hezewijk, 2010) and careful monitoring to control agent for knotweeds. Burckhardt prevent establishment and rapid response and Lauterer (1997) provide a more recent to new infestations is critical to any long- species description and report that A. term management success. Small isolated itadori is specifi c to F. japonica and F. plants or new Fallopia spp. patches have sachalinensis. Worldwide, the genus been effectively removed by covering them Aphalara has 40 spp. which are restricted for several years with geotextile fabric to plants within the Polygonaceae combined with hand digging (McHugh, including Rumex, Persicaria, Polygonum 2006). This approach is more likely to and Fallopia. The various Aphalara spp. work if the rhizome system is not well are morphologically very similar and often established. identifi ed based on their distinct host ranges (Burckhardt and Lauterer, 1997). The native range of A. itadori occurs 48.3 Biological Control Agents between 31°N and 50°N latitude and includes the southern end of Japan, Korea Because of the scale of the Fallopia spp. and the Kurile and Sakhalin islands problem, biological control offers the best (Burckhardt and Lauterer, 1997). In fi eld hope for ecologically sound and cost- surveys in Japan, A. itadori was found from effective control. Several insects and patho- sea level up to 2150 m (Shaw et al., 2009). gens have been investigated as potential Shaw et al. (2009) describe the basic biological control agents. The leaf beetle biology of A. itadori. All stages of the Gallerucida bifasciata Motschulsky (Cole- knotweed psyllid feed by inserting sucking optera: Chrysomelidae) and two moths, mouthparts into the phloem cells of the Ostrinia ovalipennis Ohno and O. lati- leaves and stems and removing sap. pennis Warren (Lepidoptera: Crambidae), Female psyllids can lay up to 600–700 eggs were of interest because we observed them as adults, primarily on the top and bottoms causing signifi cant damage to the plant at of the leaves and in the sheath at the base fi eld locations in Japan. Unfortunately they of the leaf petiole (Shaw et al., 2009). At were found to be insuffi ciently host 23°C, eggs hatch after about 12 days and 324 Chapter 48

the nymphs pass through fi ve instars. A classical biological control agent for an full generation at 23°C requires 33 days. invasive plant to be released in Europe Nymphs excrete crystallized honeydew (Djeddour and Shaw, 2011; Shaw et al., during feeding that is visible as white 2011). We collected a second (‘northern’) strings or fl akes on the plant surfaces. biotype from F. sachalinensis on the island While adult A. itadori are winged and can of Hokkaido in northern Japan in 2007 fl y it is currently not known how far they (Grevstad et al., 2013). can fl y or whether there is a distinct fl ight Extensive host-range testing in season. The psyllids overwinter as adults. containment facilities in the USA, UK and Many Aphalara spp. use coniferous tree Canada has demonstrated the safety and bark for winter shelter (Hodkinson, 2009) effi cacy of both biotypes of A. itadori and several other species of psyllids, (Grevstad et al., 2013). The Kyushu psyllid including Aphalara spp., can also be performed best in terms of population successfully overwintered on grass tus- growth on F. japonica and F. bohemica socks (Heslop-Harrison, 1937). In Japan, A. whereas the Hokkaido psyllid performed itadori have been found wintering in the best on F. sachalinensis (R. Bourchier and bark of Pinus densifl ora Sieb. and Zucc. F. Grevstad, 2012, unpublished results). (Pinaceae) and Cryptomeria japonica Both were found to be specialized to (Thunb. ex L. f.) D. Don (Cupressaceae) Fallopia spp., with only very low (Miyatake, 1973, 2001; Baba and Miyatake, occurrence of development on a small 1982). Thus A. itadori is expected to use number of related non-target plant species the tree bark of related conifer species in (Grevstad et al., 2013). North America for overwintering. For the three key non-target species We have estimated the number of supporting development, Muehlenbeckia generations of A. itadori in North America axillaris (Hook. f.) Endl., Fallopia cilinodis based on temperature-dependent develop- (Michaux) Holub and Fagopyrum escu- ment studies in containment and simu- lentum Moench (Polygonaceae), additional lation modelling (Bourchier et al., 2012, detailed host-range studies were con- unpublished results). Using (i) a con- ducted. These included multiple-choice servative development threshold of 10°C, oviposition testing, survivorship studies (ii) peak adult emergence and development and generational tests (assessing if a occurring between 15 May and 15 October population of A. itadori could be main- and (iii) weather data from the past 10 tained strictly on these species) and open years, we expect two generations of A. fi eld tests with the Kyushu psyllid in the itadori at over 98% of the reported F. UK (Grevstad et al., 2012). All plant japonica sites in British Columbia species supporting development received (n=2205) and Oregon (n=6091). For careful scrutiny, however the plant of most between 13 and 15% of the sites, usually at concern for non-target impacts was F. lower elevations, there would be at least a esculentum, buckwheat, because of its use partial third generation. The predicted as a crop in North America. Using F. timing of peak adult emergence in North esculentum as an example for the results America is uncertain. Using 15 April, from the additional testing, we are which was the predicted emergence date in confi dent that all species are at very low the UK based on observations in Japan risk from the release of A. itadori in North (Shaw et al., 2009), the percentage of sites America. There is an extreme oviposition having a third generation will increase. preference for Fallopia spp. compared to There are two biotypes of A. itadori. F. esculentum that was demonstrated in The Kyushu (or ‘southern’) biotype was both lab and fi eld experiments. For any collected in southern Japan from F. eggs that were laid on F. esculentum, japonica (Shaw et al., 2009). This biotype survivorship was zero in 2012 UK fi eld has recently been released in the UK after trials and extremely low under optimal extensive safety testing and is the fi rst laboratory conditions. When it did occur, Chapter 48 325

development in the laboratory was at much sachalinensis and Fallopia × bohemica are slower rates (20% longer on F. esculentum more common, the petition is for release of compared to Fallopia spp.), which in the both A. itadori biotypes. A single A. itadori fi eld would further reduce survivorship. In biotype, Kyushu or Hokkaido, will be repeated attempts to rear A. itadori popu- released per watershed depending on the lations on F. esculentum in the benign and dominant Fallopia sp. For all of the initial predator-free laboratory environment, nine North America release locations Fallopia of ten attempts resulted in extinction early spp. identifi cations have been confi rmed on and one lingered into the third using AFLP (J. Gaskin, Sydney, Montana, generation without expanding. Finally, F. 2012, pers. comm.). esculentum is grown as a crop all over Aphalara itadori has the potential to be Japan in close proximity to Fallopia spp. a highly effective biological control agent. populations, yet A. itadori is not recorded As with any classical biological control as a pest of F. esculentum in Japan introduction, the release of A. itadori into (Japanese Society of Applied Entomology North America would not be 100% risk- and Zoology, 1987). free. However, the limited development In impact studies conducted in observed on non-target plants poses a very containment using F. sachalinensis and F. × minimal risk for these species. It falls well bohemica, both biotypes of A. itadori within the range observed for other agents, signifi cantly reduced knotweed growth. including psyllids (Center et al., 2007), that The psyllids caused more than a 50% re- have been released without any harm to duction in biomass after 50 days exposure non-target plants in the fi eld (Blossey et al., as compared to controls (Grevstad et al., 2001; Paynter et al., 2004; Breiter and 2013). Biomass reductions occurred even if Seastedt, 2007; Pratt et al., 2009). In the A. itadori biotype did not reproduce contrast, as seen in the UK, there are particularly well on the target plant. In defi nite ecological risks and economic con- these cases we suspect that feeding by sequences to letting Fallopia spp. continue early instar nymphs, before signifi cant A. to spread in North America and damage itadori mortality occurred, resulted in fragile riparian ecosystems and infra- damage to the meristems and reduced structure. Based on the impact data plant growth. In addition we observed a observed in the laboratory, at a minimum signifi cant twisting of Fallopia spp. leaves, we expect that A. itadori will help slow the which was most pronounced for the spread of Fallopia spp. by making the Hokkaido psyllid on F. sachalinensis . plants less vigorous and less competitive. Patterns of reproductive success for the At best, A. itadori will cause plants to die two biotypes on the two hosts were back both above and below ground, as it inverted. On F. sachalinensis, approxi- does in the laboratory, and Fallopia spp. mately fi ve times more F1 adults of the will be reduced to a level where it is no Hokkaido A. itadori developed than the longer considered a problem. Under either Kyushu psyllid whereas on F. × bohemica, scenario, the economic benefi ts are likely fi ve times more of the Kyushu A. itadori to be very large because of the current high developed. costs of controlling Fallopia spp. Pending approval of regulators, we are proposing to initially release the Kyushu A. itadori biotype in Canada because of its 48.4 Evaluation of Biological demonstrated preference for F. japonica in Control the lab, which is the dominant species in British Columbia. Both A. itadori biotypes No agents have been released for biological will likely be required to effectively control control of Fallopia spp. in North America the wide variety of Fallopia spp. and to date. A joint petition for the release of genotypes that are invasive throughout Aphalara itadori in Canada and the USA North America. In the USA where F. was submitted in October 2012 to the 326 Chapter 48

Canadian Food Inspection Agency and the biotypes of Aphalara itadori in quarantine, USDA-Animal Plant Health Inspection pending release decision. Service.

Acknowledgements 48.5 Future Needs We are very grateful that the North Future work should include: American knotweed programme benefi tted 1. Continued study of established popula- from a huge head start because of work tions of the Kyushu biotype in the UK to conducted in the UK by CABI on behalf of understand the impact of Aphalara itadori ‘Natural Control of Japanese knotweed under fi eld conditions and compare with Project Board’ who also agreed to the impact studies in containment in North provision of starter colonies of the Kyushu America on all three types of Fallopia spp.; psyllid for both Canada and the USA. The 2. Examination of host usage of crossed USDA Forest Service co-fi nanced Phase 1 lines (Kyushu × Hokkaido) of Aphalara ita- of the UK research alongside the Welsh dori in containment; Development Agency (now Welsh Assembly 3. Continuing host-specifi city screening of Government). Subsequent funding for Fallopia spp. pathogens, e.g.: leafspot foreign exploration and host-range research Mycosphaerella polygoni-cuspidati; for the North American project has been 4. Maintaining existing and establishing provided by British Columbia Ministry of additional pre-release Fallopia spp. moni- Forests, Lands and Natural Resource toring sites in western and eastern Canada Operations, Agriculture and Agri-Food and the USA; Canada, Washington State Department of 5. Maintaining rearing colonies of both Agriculture and USDA Forest Service.

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49 Galium spurium L., False Cleavers, and G. aparine L., Cleavers (Rubiaceae)

Alec S. McClay McClay Ecoscience, Sherwood Park, Alberta

49.1 Project Status either series of tests (Sobhian et al., 2004; McClay, 2005). One arthropod biological control agent, the In 2003 and 2004, C. rouhollahi was gall mite Cecidophyes rouhollahi Craemer released on G. spurium in replicated fi eld (Trombidiformes: Eriophyidae), has been plots at Vegreville, Alberta (53.510°, approved for release against Galium −112.100°). Mites were released on to G. spurium L. and G. aparine L. (Rubiaceae) spurium growing alone or in a canola, in Canada. A population of C. rouhollahi Brassica napus L. (Brassicaceae), stand, from France was found to be highly host- either early (at the two leaf-whorl stage of G. specifi c and damaging to the three closely spurium) or late (at the six leaf-whorl stage). related species G. spurium, G. aparine and Further releases were made into plots G. tricornutum Dandy (Rubiaceae), and did seeded with G. spurium later in the season, not attack any other Galium species tested in an effort to obtain winter annual G. (Craemer et al., 1999; Sobhian et al., 2004). spurium plants that would overwinter. In A petition was submitted in March 2001 2003, the latter plots were seeded on 14 July requesting approval for fi eld release of C. and inoculated with mites on 19 September, rouhollahi in Canada (McClay et al., 2001), and in 2004 they were seeded on 10 and approval was received from the September and inoculated on 13 October. Canadian Food Inspection Agency in June In 2003, gall development in the plots 2002. was consistent but light. All plots that Because of a report (Moha, 1972) of a received mites at the six leaf-whorl stage, possible plant virus associated with the and 20 out of 24 that received them at the related species Cecidophyes galii two leaf-whorl stage, showed galling in late (Karpelles) (Trombidiformes: Eriophyidae), July. There were no signifi cant differences virus testing of infested plants from the in G. spurium biomass or seed production greenhouse colony at USDA-ARS, Mont- between any of the C. rouhollahi treat- pellier, was carried out in 1999 and 2000. ments. All plots were checked thoroughly Plant samples from imported colonies of C. on 19 May and 29 June 2004 for possible rouhollahi were also submitted for PCR mite survival over winter. Overwintered or testing to Agdia, Inc. (Elkhart, Indiana, newly germinated G. spurium was found in USA) in April and June 2003 before mites all plots except the canola-only plots. No were released in the fi eld in Alberta. No damage to G. spurium indicating over- evidence of viruses associated with the winter survival of mites was found in any introduced C. rouhollahi was found in of these plots.

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 330 Chapter 49

In 2004, early application of mites led to regrowth between April and June 2005 signifi cantly higher levels of galling than (McClay, 2005). late application. There was a signifi cant A cold temperature storage experiment overall effect of C. rouhollahi treatments was conducted with C. rouhollahi, using on G. spurium total aboveground biomass mites from a greenhouse colony, to deter- (Table 49.1). In plots without canola, G. mine its survival (as assessed by ability to spurium biomass was reduced by 29.3% in initiate galls on G. spurium) after storage the early C. rouhollahi inoculation treat- for different periods at temperatures from 4 ment, compared with uninoculated control to −25°C. From 4 to −8°C mites were able plots. Plots with the late inoculation to successfully initiate galling after 24 days treatment had an intermediate reduction in of storage, the longest period tested. At biomass. A similar trend, although not −15°C and −20°C, C. rouhollahi lost the statistically signifi cant, was seen in plots ability to initiate galling after 3 days of with canola. The effects of C. rouhollahi storage, and mites stored at −25°C were not treatments on G. spurium seed production viable after 1 day (McClay, 2005). As these were similar to those on biomass. Again, tempera tures are well within the range that no sign of overwinter survival of C. could be experienced by overwintering rouhollahi was seen in any of these plots in mites in Alberta, these results suggest that 2005 (McClay, 2005). the tested population of C. rouhollahi is Cecidophyes rouhollahi was also not suffi ciently cold-hardy to survive in the released on G. spurium in a canola fi eld fi eld over winter, at least in Alberta. near Mundare, Alberta (53.761°, A fungal pathogen isolated from G. −112.451°), in July 2003 and in a fi eld of spurium in Alberta, Monographella creeping red fescue, Festuca rubra L. cucumerina (Lindf.) Arx (=Plectosporium (Poaceae), near Spirit River, Alberta tabacinum (J.F.H. Beyma) Palm et al.) (55.957°, −118.992°), in June 2004. No gall (incertae sedis) (American Type Culture development was seen at the Mundare Collection PTA-3463), was also studied as release site, but defi nite galling was seen a potential biological control agent for G. on plants at the Spirit River site in August spurium and G. aparine. Application of 2004. No sign of C. rouhollahi was seen at 107 conidia ml−1 killed G. spurium and G. either of these sites in the year following aparine seedlings, and caused no or minor release. A tray of 15 C. rouhollahi -infested symptoms on 34 other species tested, G. spurium plants in 10 cm square pots including other Galium and Rubiaceae was overwintered outdoors in a garden species and crop species in ten other from October 2004 to June 2005. These families (Zhang et al., 2002a). Studies of plants regrew well after overwintering, but growth requirements for this fungus no sign of mite damage was seen on the showed that potato-dextrose agar was the

Table 49.1. Effects of Cecidophyes rouhollahi on biomass of Galium spurium in fi eld plots at Vegreville, Alberta, 2004.

Galium spurium above ground biomass (g m−2, mean ± s.e.) Stage of mite application In canola Without canola none 55.05 ± 9.39 C 356.34 ± 34.27 A late (6 leaf-whorl) 52.79 ± 11.37 C 328.18 ± 36.67 AB early (2 leaf-whorl) 39.39 ± 8.34 C 251.97 ± 40.01 B

A,B,C,ABMeans followed by different letters are signifi cantly different, P<0.05, Tukey’s HSD test. Chapter 49 331

best medium for spore production and the viable as a biological control agent (K. optimal pH for spore production was 7.0. Bailey, Saskatoon, 2012, pers. comm.). The best medium for submerged liquid culture spore production was Richard’s solution at a pH of 7.0 with a carbon 49.3 Future Needs concentration of 12.6 g l−1 and a C:N ratio of 7.5:1 (Zhang et al., 2001). Effi cacy was Future work should include: strongly dependent on plant growth stage; 1. Exploration for cold-hardy populations G. spurium seedlings older than the one of C. rouhollahi in areas of Europe with leaf-whorl stage were not killed, although more severe winter temperatures; dry weight was reduced in some treat- 2. Development of a bioherbicide for these ments. The best effi cacy was found on Galium spp., through exploration for more cotyledon or one leaf-whorl seedlings of effective pathogens. G. spurium and G. aparine with a dew period of 16 h and a dew temperature of 15°C or above. Delayed dew periods, or multiple shorter dew periods, reduced the Acknowledgements effi cacy of the pathogen (Zhang et al., 2002b). I thank the Alberta Canola Producers Commission for funding support, Dr Rouhollah Sobhian (USDA-ARS, retired) 49.2 Evaluation of Biological Control for collections and shipments of mites from France, Robert B. Hughes for technical Although C. rouhollahi caused signifi cant assistance, Dr James Amrine for identifi - reductions in biomass and seed production cation of mites, Andrea Harness (Agdia of G. spurium in fi eld plots, the tested Inc.) for assistance and advice with virus population of this mite does not appear to testing, Dr Rose DeClerck-Floate, Eva be suffi ciently cold-hardy to be effective as Pavlik and Dr Rob Bourchier (Agriculture a classical biological control agent in and Agri-Food Canada) for quarantine Alberta. It could potentially be useful in assistance, John Mayko, Jennifer Otani, areas with milder winters where G. Alex Skorowodko, Calvin Yoder, Gary spurium or G. aparine are agricultural Ropchan and the Peace Region Forage Seed problems. The tested isolate of M. Association for assistance and support for cucumerina likely does not sporulate fi eld releases, and Dr Paul Watson and Jeff profusely enough, or cause severe enough Newman for assistance with fi eld plots at damage to its host, to be commercially Vegreville.

References

Craemer, C., Sobhian, R., McClay, A.S. and Amrine, J.W. (1999) A new species of Cecidophyes (Acari: Eriophyidae) from Galium aparine (Rubiaceae) with notes on its biology and potential as a biological control agent for Galium spurium. International Journal of Acarology 25, 255–263. McClay, A.S. (2005) Field Evaluation of a Gall Mite for Biological Control of False Cleavers. Canola Agronomic Research Program Project #AG-2002-20 Final Report. McClay Ecoscience, Sherwood Park, Alberta. McClay, A.S., Sobhian, R., Craemer, C. and Peterschmitt, M. (2001) Petition for fi eld release of the gall mite Cecidophyes rouhollahi Craemer (Acari: Eriophyidae) from southern France for biological control of false cleavers, Galium spurium L. (Rubiaceae), in western Canada. Alberta Research Council, Vegreville, Alberta. 332 Chapter 50

Moha, C. (1972) Sur la présence d’inclusions de type particulier dans les cellules qui bordent la cavité gallaire de la cécidie d’Eriophyes galii Karp sur Galium aparine L. Journal de Microscopie 14, 70a–71a. Sobhian, R., McClay, A., Hasan, S., Peterschmitt, M. and Hughes, R.B. (2004) Safety assessment and potential of Cecidophyes rouhollahi (Acari, Eriophyidae) for biological control of Galium spurium (Rubiaceae) in North America. Journal of Applied Entomology 128, 258–266. Zhang, W., Sulz, M. and Bailey, K.L. (2001) Growth and spore production of Plectosporium tabacinum. Canadian Journal of Botany 79, 1297–1306. Zhang, W.M., Sulz, M. and Bailey, K.L. (2002a) Evaluation of Plectosporium tabacinum for control of herbicide-resistant and herbicide-susceptible false cleavers. Weed Science 50, 79–85. Zhang, W.M., Sulz, M., Bailey, K.L. and Cole, D.E. (2002b) Effect of epidemiological factors on the impact of the fungus Plectosporium tabacinum on false cleavers (Galium spurium). Biocontrol Science & Technology 12, 183–194.

50 Lepidium draba L., L. chalepense L., L. appelianum Al-Shehbaz, Hoary Cresses (Brassicaceae)

Hariet L. Hinz,1 Robert S. Bourchier2 and Mark Schwarzländer3 1CABI, Delémont, Switzerland; 2Agriculture and Agri-Food Canada, Lethbridge, Alberta; 3University of Idaho, Moscow, Idaho, USA

50.1 Pest Status Findlay, 1974). The hoary-cress complex ranks eighth out of 45 most frequently Hoary cresses or whitetops, Lepidium listed noxious weeds in the USA and draba L., L. chalepense L. and L. Canada (Skinner et al., 2000). Lepidium appelianum Al-Shehbaz (Brassicaceae), are draba or the complex of hoary cress deep-rooted, clonal mustards that were species is listed as noxious in Alberta and introduced from Eurasia to North America Saskatchewan and is of regional concern in in the 19th and early 20th centuries as British Columbia and parts of Manitoba. contaminants in seed or in ballast (Francis Lepidium draba is apparently the least and Warwick, 2008). The three species can common of the three species in Canada but be distinguished by the shape of their seed is considered a major concern in the pods (silicles): L. draba pods are heart- Thompson–Okanagan region (Francis and shaped, L. chalepense pods are nearly Warwick, 2008). Lepidium chalepense and round or kidney-shaped and L. appelia- L. appelianum are both abundant in num has completely globular to ellipsoid irrigated areas and are frequently found pods with short simple hairs (Mulligan and together (Francis and Warwick, 2008). All © CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 50 333

three species are weeds of: (i) agricultural plants continue to grow until frost. If land, e.g. grain crops, lucerne, Medicago conditions remain suitable, they can fl ower sativum L. (Fabaceae), hayfi elds, where and produce a second crop of seeds late in they reduce yields; (ii) pastures, where the summer (Sheley and Stivers, 1999). they displace forage species and can cause Seeds can be dispersed in contaminated toxicity problems to cattle; and (iii) natural crop seed and hay, vehicles and equip- ecosystems, e.g. riparian areas, forest ment, in surface runoff and through the margins, grass and shrub lands, where they digestive tracts of animals (McInnis et al., reduce native plant communities (Lyons, 2003). 1998; Sheley and Stivers, 1999; Francis and Warwick, 2008). Disturbed sites are most vulnerable for infestation. Hoary 50.2 Background cresses can also serve as alternative host plants for numerous crop pests (Cripps et Since the 1970s the Lepidium spp. al., 2006a), including the cabbage seedpod complex has been managed at least in weevil, Ceutorhynchus obstrictus (Mar- agricultural areas of the prairie provinces sham) (Coleoptera: Cuculionidae) (Mason by application of phenoxy herbicides et al., 2004), and a bacterial black rot in (Francis and Warwick, 2008). The three Ontario (Francis and Warwick, 2008). Lepidium spp. differ in their susceptibility All three Lepidium spp. are herbaceous, to herbicides with L. draba being the most rhizomatous, perennial plants that repro- resistant, while some strains of L. duce vegetatively and by seed, although chalepense have also developed resistance established populations mostly rely on to 2,4-D (Lyons, 1998). Repeated culti- vegetative reproduction to increase plant vation or grazing by sheep, Ovis aries L., density. Their root system is extensive, and goats, Capra hircus L. (Artiodactyla: consisting of a complex network of vertical Bovidae), has also been shown to provide and lateral roots typically reaching depths control of the three Lepidium spp. How- of 60–150 cm; Selleck (1965) traced the ever, because Lepidium spp. can regenerate root system of L. appelianum to the water from their extensive root system, they table 6.5 m below the soil surface. For L. readily re-establish after control measures. draba at established fi eld sites, over 75% Thus, control efforts must be persistent, of biomass is located below ground (Miller and require at least 2–3 years of follow-up et al., 1994). In Saskatchewan, L. draba work. In general, successful control is most spread up to 3.7 m in the fi rst year and likely achieved with a combination of then increased radially from 0.6 to 0.75 m several control practices, such as herbicide each subsequent year (Mulligan and application and physical removal by Findlay, 1974). Lepidium appelianum hoeing or tilling, followed by planting increased at almost the same rate, while L. competitive species (Lyons, 1998). chalepense was less vigorous. Germination In a review of the European literature to occurs in the spring after a period of assess the potential for biological control of dormancy (McInnis et al., 2003), and the hoary cress complex, 175 phyto- clonal growth occurs from buds on the phagous arthropod species were recorded rhizomes of established plants from spring to be associated with L. draba, while in the onwards. Established plants bolt in early USA only eight species were recorded from spring, fl ower from late April to early June L. draba (Cripps et al., 2006a). During and form seeds in June and July. Seeds are European fi eld surveys, 162 phytophagous produced in silicles, which contain usually species were collected from L. draba, of two (L. draba), one to four (L. chalapense) which 22 species were reared from plants, or zero to four seeds (L. appelianum) whereas the USA fi eld survey resulted in (Mulligan and Findlay, 1974). Single the collection of 45 phytophagous species shoots produce up to 850 silicles (Corns of which two species were reared from the and Frankton, 1952). After fl owering the plants. Polyphagous herbivores were 334 Chapter 50

signifi cantly more abundant in the USA some degree and from 15 of these species than Europe, while specialists were more (ten native to North America) adults or less absent (Cripps et al., 2006b). Host- emerged. None of the commercially grown plant utilization was more complete in Brassicaceae were attacked by C. Europe; root feeders and gall formers were cardariae. In subsequent choice tests with generally absent from the introduced range, 16 test species that had supported gall or which was dominated by generalist sap- adult development under no-choice sucking herbivores. conditions, only the native North Ameri- can Lepidium latipes Hook. (Brassicaceae) was readily attacked. A combined impact 50.3 Biological Control Agents and survival experiment showed that: (i) attack by C. cardariae did not negatively To date, nine European species have been affect L. latipes; and (ii) C. cardariae is not identifi ed as potential biological control able to sustain a population on L. latipes, agents based on records of their restricted or on any other plant species with an host range: fi ve weevils, one fl ea beetle, annual life history. In an open-fi eld test, L. two gall midges and one eriophyid gall latipes was only attacked when exposed in mite. The gall midges Contarinia cardariae close proximity to L. draba. Additional Fedotova and Dasineura cardariae investigations on the fi eld host range of C. Fedotova (Diptera: Cecidomyiidae) have cardariae in its native range demonstrated not been found during fi eld surveys, and that only the European congener Lepidium host-specifi city tests with one of the campestre (L.) W.T. Aiton (Brassicaceae), weevils, Melanobaris sp. near semistriata which is closely related to L. draba, can be (Boheman) (Coleoptera: Curculionidae) and considered as alternative host plant. the shoot-mining fl ea beetle Psylliodes Aceria drabae is an eriophyid mite, wrasei Leonardi & Arnold (Coleoptera: with a wide distribution east across Europe Chrysomelidae), demonstrated that they to central Asia. The mite has been reported are not suffi ciently host specifi c for release in Austria, Bulgaria, the Czech Republic, in North America. Current work is focused Finland, Greece, Hungary, Kazakhstan, on the gall-forming weevils Ceutorhynchus Poland, Romania, Russia, Spain, Sweden cardariae Korotyaev and C. assimilis and Turkey (Lipa, 1976, 1978; Lipa et al., (Paykull), the seed-feeding weevil C. 1998; M. Cristofaro (BBCA), J. Kashefi and turbatus Schultze, the stem-mining weevil R. Sobhian (USDA-ARS), Montpellier, C. merkli Korotyaev (Coleoptera: Curculio- France, 2002, pers. comm.). Aceria drabae nidae) and the gall mite Aceria drabae has multiple generations per year. (Nal.) (Trombidiformes: Eriophyidae). Individuals overwinter on root buds and Ceutorhynchus cardariae is a gall- perhaps in the root crown. As the plant forming weevil native to southern Russia bolts in the spring, A. drabae move into the (Korotyaev, 1992), but has also been found vegetative and fl ower buds, where they in Hungary, Bulgaria, Romania and the induce galls, erineum and other tissue Crimean Peninsula (Cripps et al., 2006a). deformities. Infestations often eliminate or Gall formation by C. cardariae can severely reduce seed production or stunt the plant. stunt individual shoots of L. draba and at Although A. drabae has been reported from high attack rates may kill shoots pre- various plant species in the Brassicaceae maturely. Between 2003 and 2012, 117 (Buhr, 1964; Davis et al., 1982; Bijkerk, plant species and varieties were exposed in 2012; Redfern and Shirley, 2012), other no-choice development tests, including 72 sources suggested that A. drabae is species native to North America. Apart monophagous and reports in the literature from the target weeds, L. draba, L. on other host species seem to have been chalepense and L. appelianum, 22 plant mis-identifi cations or mis-interpretations species supported gall development to of synonymously named organisms (Lipa, Chapter 50 335

1978). No-choice host-specifi city tests with molecular analyses indicate that a 97 taxa confi rmed that A. drabae only haplotype host-specifi c to L. draba exists in attacks L. draba and to a lesser extent L. southern France (Fumanal et al., 2004; appelianum (Littlefi eld et al., 2012). Aceria M.-C. Bon, Montpellier, France, 2012, pers. drabae did not develop on any other test comm.). Host-specifi city tests are on-going. plant species, including some of those listed as host plants in the literature. Petitions for the fi eld release in the USA 50.4 Evaluation of Biological Control of C. cardariae and A. drabae were submitted in December 2011 and March No biological control agents have been 2012, respectively, to the United States released to date in Canada or the USA. Department of Agriculture, Animal and Plant Health Inspection Service. To date no petitions have been submitted for release of 50.5 Future Needs these agents in Canada. Ceutorhynchus turbatus adults feed on Future work should include: the fl owers and developing seed pods of L. 1. Continuing host-specifi city tests with draba, while its larvae develop inside the C. assimilis, C. merkli and C. turbatus; seeds. The species is known from central 2. Establishing and maintaining rearing Asia to central Europe and has recently colonies of C. cardariae and A. drabae in moved to western Europe (Van den Berg quarantine; and van de Sande, 1999). Ceutorhynchus 3. Preparing petitions for release of agents turbatus is the most specifi c of the weevils in Canada for submission to the Canadian studied so far; its development is restricted Food Inspection Agency to supplement to L. draba and the closely related Euro- existing petitions submitted to the USDA- pean L. campestre. To date, host-specifi city APHIS. tests have been conducted with 47 test plant species in the Brassicaceae and completion of investigations will require a few more years. Ceutorhynchus turbatus Acknowledgements has so far not been tested on L. chalepense or L. appelianum since these species are Work on C. cardariae, C. merkli and C. diffi cult to propagate to the reproductive turbatus is conducted by CABI in stage in pots. Switzerland. Work on C. assimilis is shared Ceutorhynchus merkli has been found between CABI, USDA, ARS, EBCL in in south-western Russia, Ukraine, Mol- France (Dr Marie-Claude Bon), USDA-ARS davia and Hungary (Korotyaev, 2000). in Sidney, Montana, USA (Dr Kevin Adults feed on the leaves of L. draba and Delaney) and the University of Idaho, USA larvae mine in the stems. Work with C. (Dr Mark Schwarzländer). Work on A. merkli was postponed because of incon- drabae is conducted by Dr Jeff Littlefi eld at sistent attack of the target weed L. draba Montana State University, USA. We thank during host-specifi city tests. Additional Jeff Littlefi eld for providing data on A. host-specifi city tests are planned in drabae. CABI received funding from: Baker southern Russia to decide whether work County, Oregon; Blaine County Weed with this potential agent will be continued. Control Association (CWCA), Idaho; British Ceutorhynchus assimilis is a root-gall- Columbia, Ministry of Forests, Lands and forming weevil, which is widely distrib- Natural Resource Operations; Idaho uted in Eurasia and northern Africa. Department of Agriculture through the Hoffmann (1954) stated that this weevil is a University of Idaho; Idaho Fish and Game; pest of several Brassicaceae crops. How- Inland Empire County Weed Management ever, preliminary host range tests and Area (IECWMA), Idaho; Montana Weed 336 Chapter 50

Trust Fund through Montana State Uni- Bureau of Indian Affairs; the USDI Bureau versity; Selkirk CWMA, Idaho; University of Land Management; Weedslayer Inc., of Idaho; USDA, APHIS, PPQ, CPHST; Wyoming Biological Control Steering USDA-APHIS Western Region; the USDI Committee.

References

Bijkerk, J. (2012) Plantengallen. Available at: http://www.plantengallen.com/dataengels/gall_mites. htm (accessed 2 February 2012). Buhr, H. (1964) Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pfl anzen Mittel- und Nordeuropas. VEB, Gustav Fischer Verlag, Jena, Germany. Corns, W.G. and Frankton, C. (1952) Hoary cresses in Canada with particular reference to their distribution and control in Alberta. Scientifi c Agriculture 32, 484–495. Cripps, M.G., Hinz, H.L., McKenney, J.L., Harmon, B.L., Merickel, F.W. and Schwarzländer, M. (2006a) Comparative survey of the phytophagous arthropod faunas associated with Lepidium draba in Europe and the western United States, and the potential for biological weed control. Biocontrol Science and Technology 16, 1007–1030. Cripps, M.G., McKenney, J.L., Hinz, H.L., Price, W.J. and Schwarzländer, M. (2006b) Biogeographic comparison of the arthropod herbivore communities associated with Lepidium draba in its native, expanded and introduced ranges. Journal of Biogeography 33, 2107–2119. Davis, R., Fletchemann, C.H.W., Boczek, J.H. and Barke, H.E. (1982) Catalogue of eriophyid mites (Acari: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, Poland. Francis, A. and Warwick, S.I. (2008) The biology of Canadian weeds. 3. Lepidium draba L., L. chalepense L., L. appelianum Al Shehbaz (updated). Canadian Journal of Plant Science 88, 379–401. Fumanal, B., Martin, J.-F., Sobhian, R., Blanchet, A. and Bon, M.-C. (2004) Host range of Ceutorhynchus assimilis (Coleoptera: Curculionidae), a candidate for biological control of Lepidium draba (Brassicaceae) in the USA. Biological Control 30, 598–607. Hoffmann, A. (1954) Faune de France. Vol. 59. Paul Lechevalier, Paris, France. Korotyaev, B.A. (2000) A new species of Ceutorhynchus Germar, 1824 living on Cardaria draba in southeastern Europe (Coleoptera, Curculionidae). Acta Zoologica Academiae Scientiarum Hungaricae 46, 15–18. Lipa, J.J. (1976) A new record of Aceria drabae (Nal.) (Eriophyiidae, Acarina) on a weed Cardaria draba L. (Cruciferae) in Poland. Bulletin de L’Académie Polonaise des Sciences. Série des sciences biologiques Cl. 24, 457–459. Lipa, J.J. (1978) [Preliminary studies on the species Aceria drabae (Nal.) (Acarina, Eriophyiidae) and its potential for the biological control of the weed Cardaria draba L. (Cruciferae).] Prace Naukowe Instytutu Ochrony Roslin 20, 139–155 [In Polish with English summary]. Lipa, J.J., Murillo, J., Castro, F., Vinuela, E., Del Estal, P., Budia, F. and Caballero, P. (1998) Primera cita de Aceria drabae (Nalepa) (Acarina: Eriophyidae) en España. Boletin de Sanidad Vegetal Plagas 24, 797–802 [in Spanish with English summary]. Littlefi eld, J., Kashefi , J., deMeij, A. and Birdsall, J. (2012) A petition for the fi eld release of the gall mite Aceria drabae (Acari: Eriophyidae) for the biological control of hoary cress in North America. United States Department of Agriculture/Animal and Plant Health Inspection Service TAG Petition 2012-03. Lyons, K.E. (1998) Cardaria draba (L.) Desv. Heart-podded hoary cress, Cardaria chalepensis (L.) Hand-Maz. Lens-podded hoary cress and Cardaria pubescens (C.A. Meyer) Jarmolenko Globe- podded hoary cress. Element Stewardship Abstract. The Nature Conservancy, Virginia. Mason, P.G., Baute, T., Olfert, O. and Roy, M. (2004) Cabbage seedpod weevil, Ceutorhynchus obstrictus (Masham) (Coleoptera: Curculionidae) in Ontario and Quebec. Journal of the Entomological Society of Ontario 134, 107–113. McInnis, M.L., Kiemnec, G.L., Larson, L.L., Carr, J. and Sharratt, D. (2003) Heart-podded hoary cress. Rangelands 25, 1823. Chapter 51 337

Miller, R.R., Svejcar, T.J., Rose, J.A. and McInnis, M.L. (1994) Plant development, water relations, and carbon allocation of heart-podded hoary cress. Agronomy Journal 86, 487–491. Mulligan, G.A. and Findlay, J.N. (1974) The biology of Canadian weeds. 3. Cardaria draba, C. chalepensis, and C. pubescens. Canadian Journal of Plant Science 54, 149–160. Redfern, M. and Shirley, P. (2012) Checklist of British Galls. Available at: http://www.british-galls. org.uk/index.htm (accessed 2 February 2012). Selleck, G.W. (1965) An ecological study of lens- and globe-podded hoary cresses in Saskatchewan. Weeds 13, 1–5. Sheley, R.L. and Stivers, J. (1999) Hoary Cress (Whitetop). In: Sheley, R.L. and Pertroff, J.K. (eds) Biology and Management of Noxious Rangeland Weeds. Oregon State University Press, Corvallis, Oregon, pp. 401–407. Skinner, K., Smith, L. and Rice, P. (2000) Using noxious weed lists to prioritize targets for developing weed management strategies. Weed Science 48, 640–644. Van den Berg, C. and van de Sande, J.C. (1999) Ceutorhynchus turbatus new for the Netherlands (Coleoptera: Curculionidae). Entomologische Berichten 59, 157–159.

51 Leucanthemum vulgare Lam., Oxeye Daisy (Asteraceae)

Alec S. McClay,1 Sonja Stutz2 and Urs Schaffner2 1McClay Ecoscience, Sherwood Park, Alberta; 2CABI, Delémont, Switzerland

51.1 Pest Status by seed, and individual plants expand by rooting at the stem bases and by rhizome Leucanthemum vulgare Lamarck (=Chrys- spread (Clements et al., 2004). Leuc- anthemum leucanthemum L.) (Asteraceae) anthemum vulgare was reported to be is a shallow-rooted perennial herb native to naturalized in Quebec by the 18th century Europe. It has a short creeping rootstock (Lavoie et al., 2012). It is widespread that gives rise to erect, simple or slightly across Canada, occurring in all provinces branched stems usually up to 90 cm in and in the Yukon Territory (Clements et al., height, generally one to two per plant but 2004; Bennett and Mulder, 2009) and also sometimes forming larger clumps. Leaves throughout the USA, although less frequent are spatulate or obovate at the base of the in southern states (Strother, 2006; USDA- plant and ligulate higher on the stem. The NRCS, 2012). Some authors separate the fl ower head is a daisy, 2.5–7.5 cm in tetraploid Leucanthemum ircutianum DC. diameter, with a yellow central disk and from the diploid L. vulgare, and AFLP white rays. Leucanthemum vulgare spreads analysis of European material suggests that

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 338 Chapter 51

L. ircutianum is a hybrid of L. vulgare and industrial and other non-crop areas in another, unknown, diploid parent (Ober- Canada. Clements et al. (2004) report prieler et al., 2011). Both diploids and several other herbicides that are effective tetraploids occur in North America on L. vulgare but point out that most of (Clements et al., 2004), but preliminary these will also eliminate legumes and other results on a number of North American desirable broad-leafed species in pastures. populations suggest that most of them are Fertilizing pastures can also be effective in diploid (Stutz et al., 2012). suppressing L. vulgare by stimulating the Leucanthemum vulgare is primarily a growth of grasses and other competing weed of pastures, rangelands and roadside vegetation (Olson and Wallander, 1999; areas, and can form very dense, extensive Clements et al., 2004). populations in pastures, where it is Leucanthemum is a European genus of generally avoided by grazing cattle, and 41 species, most of which, except for the promotes soil erosion because of its widespread L. ircutianum and L. vulgare, shallow root system. Overgrazing often have quite limited distributions in Europe promotes infestations of L. vulgare (Greiner et al., 2012). It belongs to the tribe (Clements et al., 2004). It is usually not Anthemideae and the subtribe Leuc- considered a problem in annual crops, antheminae, which has no native North although it was the fourth most abundant American species (Oberprieler et al., 2009), weed species in a survey of spring cereals so L. vulgare is taxonomically well isolated in New Brunswick in 1986–1987 (Thomas from potential native non-target species. et al., 1994). It is of major concern as a The main non-target taxon of concern is contaminant in grass seed production in the popular horticultural Shasta daisy, the Peace River region of British Columbia Leucanthemum × superbum (Bergmans ex (British Columbia Ministry of Agriculture, J.W. Ingram) D.H. Kent (Asteraceae), a Food and Fisheries, 2002) and cannot be hybrid introduced by the famous American separated from seed of timothy, Phleum plant breeder Luther Burbank in 1901 pratense L. (Poaceae) (Manitoba Agri- (Hawke, 2007). According to Burbank culture, Food and Rural Initiatives, 2012). (1914) its parentage included three Euro- Leucanthemum vulgare is an invasive pean Leucanthemum species, L. vulgare, L. species of concern in natural areas, such as maximum (Ramond) DC. and L. lacustre Riding Mountain National Park, Manitoba (Brot.) Samp. (Asteraceae) and the (Otfi nowski et al., 2007) and Yellowstone Japanese Nipponanthemum nipponicum National Park, USA (Olliff et al., 2001). It is (Franch. ex Maxim.) Kitam (Asteraceae). listed as a provincial noxious weed in However, given that Burbank ‘kept no Alberta, Saskatchewan and Manitoba, and systematic records’ and had ‘unorthodox as noxious in the Cariboo, North Okanagan, views of heredity’ (Crow, 2001), the true Thompson-Nicola and Peace River regions parentage of Shasta daisy must be of British Columbia. Leucanthemum considered unclear. For example, Tahara vulgare is a ‘primary noxious weed seed’ (1921) disputes Burbank’s identifi cation of under the Canada Seeds Act, and there is a N. nipponicum and suggests that the zero tolerance for oxeye daisy seed in most species he used was probably Arct- grades of most seed species sold in Canada anthemum arcticum (L.) Tzvelev (Minister of Justice, 2005). (Asteraceae). Numerous varieties of Shasta daisy are available, most of which fall within L. × superbum but a few of which 51.2 Background are probably selections of L. vulgare (Hawke, 2007). It will be necessary to test a Several herbicides containing amino- range of Shasta daisy cultivars to assess pyralid or aminopyralid + metsulfuron- possible risk to this horticultural plant methyl are currently registered for control from potential biological control agents for of L. vulgare in rangeland, pasture, L. vulgare. Chapter 51 339

Natural enemies of L. vulgare in North sidered as potential biological control America have not been surveyed in detail. agents based on records of their restricted Guillet and Arnason (1995) found the host range: the root-mining moths polyphagous species Argyrotaenia velu- Dichrorampha aeratana (Pierce & Metcalfe) tinana Walk. and Sparganothis sulfureana and D. baixerasana Trematerra, the shoot- (Clemens) (Lepidoptera: Tortricidae) feed- mining moth D. consortana Stephens ing on L. vulgare fl ower heads around (Lepidoptera, Tortricidae), the root-feeding Ottawa, Ontario. The fl ower-head feeding weevils Cyphocleonus trisulcatus (Herbst) weevil Microplontus campestris (Gyllen- and Diplapion stolidum (Germar) (Cole- hal) (=Ceutorhynchus campestris Gyllen- optera, Brentidae) and the fl ower-head hal) (Coleoptera: Curculionidae) has been attacking fl y Tephritis neesii Meigen collected in Ontario on several occasions (Diptera, Tephritidae). since 1971 (Anderson and Korotyaev, Initial in-depth studies on the biology, 2004). Macrosiphoniella leucanthemi host-range and impact of biological control Ferrari and M. sanborni (Gillette) (Hem- candidates focused on D. aeratana, which iptera: Aphididae) are recorded feeding occurs throughout western and central on L. vulgare in North America (Miller Europe. The larvae of D. aeratana feed and Stoetzel, 1997; Stoetzel and Miller, mainly inside the roots, where they also 1999). overwinter. Around March–April, they leave the roots and pupate in the soil. Adult D. aeratana, which have brownish 51.3 Biological Control Agents forewings and a wingspan of 12–16 mm, fl y in May and June. They live for Foreign explorations started in 2008 with approximately 1 week and females lay literature and fi eld surveys. In total, at least about 100 eggs. First results from no-choice 80 insects, 7 nematodes and 16 fungi were larval development tests indicated that the found to be associated with oxeye daisy in fundamental larval host range of D. its native range (Schaffner et al., 2008). aeratana is mainly restricted to the genus Particularly well represented is the genus Leucanthemum, the larvae being able to Dichrorampha (Lepidoptera, Tortricidae), develop on L. vulgare, L. ircutianum and which appears to have undergone speci- on Shasta daisies. A few larvae were also ation on L. vulgare and related plants; in found on other test plant species, but it total, some 15 Dichrorampha spp. have remains to be shown whether the larvae been recorded from Leucanthemum spp. were indeed D. aeratana or whether they (Razowski, 2003). The fl ower head-attack- belonged to other Dichrorampha spp. ing weevil M. campestris was originally (Stutz et al., 2012). Under multiple-choice identifi ed as a potential candidate bio- conditions, L. vulgare and L. ircutianum logical control agent. Adults of this species were attacked signifi cantly more often than start feeding in late April, and mating and Shasta daisies (S. Stutz and U. Schaffner, oviposition into the fl ower heads was Delémont, Switzerland, 2012, unpublished observed from mid-May onwards. Obser- data). vations made during the fi eld surveys and The root-feeding weevil C. trisulcatus, in the laboratory confi rmed that larval which has a scattered distribution through- feeding is restricted to the receptacle and out Europe (Dieckmann, 1983), was also that seeds were not attacked. As a identifi ed as a promising potential bio- consequence, attack by M. campestris was logical control agent in the initial literature shown to have no or minimal impact on survey (Schaffner et al., 2008). Larvae feed seed output of oxeye daisy. Microplontus externally on roots of L. vulgare and L. campestris was therefore dropped from the ircutianum. This species appears to be list of potential biological control agents. quite rare in Europe, and most site records To date, six European species are con- mentioned in the literature are more than 340 Chapter 51

50 years old. However, in 2011 and 2012, 51.4 Evaluation of Biological Control C. trisulcatus was found at several locations in southern Germany and No biological control agents have been southern France, allowing establishment of released to date in Canada or the USA. laboratory rearing and initiation of investigations on the biology of this species. 51.5 Future Needs The fl ower head-attacking fl y T. neesii is very common throughout Europe (White, Future work should include: 1988) and was frequently found during fi eld surveys. Larvae feed in the receptacle 1. Additional molecular and genetic stud- and on the developing seeds, thereby ies to clarify the identity of invasive reducing seed output (Robinson, 2008). Leucanthemum populations in North Tephritis neesii pupate in the fl ower heads America and the relationships between and adults emerge in summer. This species oxeye and Shasta daisy; has one generation per year, and over- 2. Host-specifi city testing with the candi- wintering occurs in the adult stage. Usually date biological control agents D. aeratana, only seed heads collected from plants C. trisulcatus, T. neesii and D. stolidum; fl owering in May or June were infested; 3. Assessing the potential impact on L. vul- seed heads collected later in the year from gare of all candidate biological control plants that had regrown after mowing were agents; not infested. 4. Locating large fi eld populations of D. The root-feeding weevil D. stolidum is baixerasana and D. consortana. considered to be a specialist on L. vulgare (Dieckmann, 1977). During fi eld surveys in southern France, Switzerland, southern Acknowledgements Germany, Czech Republic and southern Poland, L. vulgare plants infested by D. Work on D. aeratana, C. trisulcatus, D. stolidum were found at several locations. stolidum and T. neesii in Switzerland was Adults emerging from fi eld-collected roots funded by the British Columbia Ministry of in July were transferred into plastic Forests, Lands and Natural Resource cylinders containing a cut rosette of L. Operations and the Montana Noxious vulgare. The food was regularly changed Weed Trust Fund, through Montana State and the rosettes checked for eggs. Adults University. We thank J. Gaskin, USDA-ARS hibernated and started to lay eggs in April Sidney, Montana, for conducting the (S. Stutz and U. Schaffner, 2012, unpub- molecular work on Leucanthemum vulgare lished results). and related species.

References

Anderson, R.S. and Korotyaev, B.A. (2004) Some Palaearctic weevils in the subfamily Ceutorhynchinae (Coleoptera, Curculionidae) recently discovered in North America. The Canadian Entomologist 136, 233–239. Bennett, B.A. and Mulder, R.S. (2009) Natives gone wild: climate change and a history of a Yukon invasion. In: Darbyshire, S.J. and Prasad, R. (eds) Proceedings of the 2008 Weeds Across Borders Conference, May 27–30, 2008, Banff, Alberta, pp. 235–248. British Columbia Ministry of Agriculture Food and Fisheries (2002) Guide to Weeds in British Columbia. Open Learning Agency Marketing Department, Burnaby, British Columbia. Burbank, L. (1914) The Shasta Daisy: how a troublesome weed was re-made into a beautiful fl ower. In: Whitson, J., John, R. and Williams, H.S. (eds) Luther Burbank: His Methods and Discoveries and Their Practical Application. Luther Burbank Press, New York and London, pp. 7–38. Chapter 51 341

Clements, D.R., Cole, D.E., Darbyshire, S., King, J. and McClay, A. (2004) The biology of Canadian weeds. 128. Leucanthemum vulgare Lam. Canadian Journal of Plant Science 84, 343–363. Crow, J.F. (2001) Plant Breeding Giants: Burbank, the Artist; Vavilov, the Scientist. Genetics 158, 1391–1395. Dieckmann, L. (1977) Beiträge zur Insektenfauna der DDR: Coleoptera–Curculionidae (Apioninae). Beiträge zur Entomologie 27, 7–143. Dieckmann, L. (1983) Beiträge zur Insektenfauna der DDR: Coleoptera – Curculionidae (Tanymecinae, Leptopiinae, Cleoninae, Tanyrhynchinae, Cossoninae, Raymondionyminae, Bagoinae, Tanysphyrinae). Beiträge zur Entomologie 33, 257–381. Greiner, R., Vogt, R. and Oberprieler, C. (2012) Phylogenetic studies in the polyploid complex of the genus Leucanthemum Mill. (Compositae, Anthemideae) based on cpDNA sequence variation. Plant Systematics and Evolution 298, 1407–1414. Guillet, G. and Arnason, J.T. (1995) Some phytophagous insects found on Rudbeckia hirta and Chrysanthemum leucanthemum in the Ottawa/Hull area. Proceedings of the Entomological Society of Ontario 126, 95–97. Hawke, R.G. (2007) A Report on Leucanthemum × superbum and Related Daisies. Chicago Botanic Garden Plant Evaluation Notes Issue 30. Chicago Botanic Garden, Glencoe, Illinois. Lavoie, C., Saint-Louis, A., Guay, G., Groeneveld, E. and Villeneuve, P. (2012) Naturalization of exotic plant species in north-eastern North America: trends and detection capacity. Diversity and Distributions 18, 180–190. Manitoba Agriculture Food and Rural Initiatives (2012) Timothy Seed Production. Available at: https://www.gov.mb.ca/agriculture/crops/forages/bjb00s05.html (accessed 22 October 2012). Miller, G.L. and Stoetzel, M.B. (1997) Aphids associated with chrysanthemums in the United States. Florida Entomologist 80, 218–239. Minister of Justice (2005) Weed Seeds Order. Available at: http://laws-lois.justice.gc.ca/PDF/SOR- 2005-220.pdf (accessed 22 October 2012). Oberprieler, C., Himmelreich, S., Källersjö, M., Vallès, J., Watson, L.E. and Vogt, R. (2009) Anthemideae. In: Funk, V., Susanna, A., Stuessy, T. and Bayer, R. (eds) Systematics, Evolution, and Biogeography of the Compositae. International Association for Plant Taxonomy, Vienna, pp. 631–666. Oberprieler, C., Eder, C., Meister, J. and Vogt, R. (2011) AFLP fi ngerprinting suggests an allopolyploid origin of two members of the Leucanthemum vulgare aggregate (Compositae, Anthemideae) in central Europe. Nordic Journal of Botany 29, 370–377. Olliff, T., Renkin, R., McClure, C., Miller, P., Price, D., Reinhart, D. and Whipple, J. (2001) Managing a complex exotic vegetation program in Yellowstone National Park. Western North American Naturalist 61, 347–358. Olson, B.E. and Wallander, R.T. (1999) Oxeye daisy. In: Sheley, R.L. and Petroff, J.K. (eds) Biology and Management of Noxious Rangeland Weeds. Oregon State University Press, Corvallis, Oregon, pp. 282–289. Otfi nowski, R., Kenkel, N.C., Dixon, P. and Wilmshurst, J.F. (2007) Integrating climate and trait models to predict the invasiveness of exotic plants in Canada’s Riding Mountain National Park. Canadian Journal of Plant Science 87, 1001–1012. Razowski, J. (2003) Tortricidae (Lepidoptera) of Europe: , Vol. 2. František Slamka, Bratislava, Slovakia. Robinson, J. (2008) The evolution of fl ower size and fl owering behaviour in plants: the role of pollination and pre-dispersal seed predation. MPhil thesis, The University of Southampton, UK. Schaffner, U., Gundelwein, F., Grosskopf, G. and Häfl iger, P. (2008) Prospects for the biological control of oxeye daisy, Leucanthemum vulgare. Annual Report. CAB International, Delémont, Switzerland. Stoetzel, M.B. and Miller, G.L. (1999) Macrosiphoniella leucanthemi (Homoptera: Aphididae): new records and redescriptions of the apterous and alate viviparous females. Entomological News 110, 45–50. Strother, J.L. (2006) Leucanthemum Miller. In: Flora of North America Editorial Committee (ed.) Flora of North America North of Mexico, Vol. 19. Magnoliophyta: Asteridae, Part 6: Asteraceae, Part 1. Oxford University Press, New York, pp. 557–559. Stutz, S., Tateno, A., Hinz, H.L. and Schaffner, U. (2012) Annual Report 2011: Prospects for the biological control of oxeye daisy, Leucanthemum vulgare. CAB International, Delémont, Switzerland. 342 Chapter 52

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52 Linaria dalmatica (L.) Miller, Dalmatian Toadfl ax (Plantaginaceae)

Rosemarie A. De Clerck-Floate1 and Susan C. Turner2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2British Columbia Ministry of Forests, Lands and Natural Resource Operations, Kamloops, British Columbia

52.1 Pest Status et al., 2010), suggesting that it is still spreading and may become a serious weed Dalmatian toadfl ax, Linaria dalmatica (L.) in northern latitudes of Canada as the Mill. (Plantaginaceae), introduced to climate warms. eastern North America from Europe at the Linaria dalmatica continues to be of turn of the 19th century (Alex, 1962; greatest concern in western North America, Vujnovic and Wein, 1997), now occurs where this perennial invades rangelands, widely in Canada and the USA (Wilson et rights-of-way and natural areas. It is al., 2005; United States Department of currently listed as ‘noxious’ in British Agriculture, Natural Resource Conser- Columbia (British Columbia Ministry of vation Service, 2012). In Canada, there are Agriculture, 2012), Alberta (Alberta anecdotal reports of L. dalmatica being Agriculture and Rural Development, 2012) planted as an ornamental at the Central and Manitoba (Government of Manitoba, Experimental Farm in Ottawa, Ontario in 2012). Its shallow, creeping roots, early 1901 (Macoun, 1908; Alex, 1962), however, seasonal growth, prolifi c seed production the fi rst voucher specimen in Canada was (Lajeunesse et al., 1993; Vujnovic and not collected until 1933 in Edmonton, Wein, 1997), but also a high specifi c leaf Alberta (Alex, 1962). More recently, a fi rst- area (Maron and Marler, 2008) are thought time occurrence of L. dalmatica in the to contribute to the invasiveness and Yukon Territory has been reported (Bennett competitiveness of L. dalmatica. Other

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 52 343

perceived risks of L. dalmatica invasions et al., 2010). Work has continued on the are associated with its potential toxicity to overseas testing of additional European grazers, as a reservoir for crop plant insect agents, coinciding with a re- pathogens, e.g. Cucumovirus cucumber examination of the North American mosaic virus (Bromoviridae), and its ability biological control programmes for L. to increase soil erosion (Sing and Peterson, dalmatica and L. vulgaris Mill. (Plantagin- 2011). Linaria dalmatica is adaptable to aceae) (see De Clerck-Floate and McClay, varied or changing environments, demon- Chapter 53, this volume). The latter is in strating increased population and vege- response to new information on the tative growth in response to increased phylogenetics of both plants and insects precipitation and soil nitrogen (Blumen- within this system (Caldara et al., 2008, thal et al., 2008). However, it also thrives 2010; Gaskin et al., 2011; Toševski et al., in dry and nutrient-impoverished habitats 2011). such as in mixed grass prairie (Blumenthal One of the largest changes for the pro- and Hufbauer, 2007; Blumenthal et al., gramme to address has been the move of 2008), or on steep, south-facing slopes in the genus Linaria from the family rangeland landscapes (Blumenthal et al., Scrophulariaceae Dumort to Plantagin- 2012). Within Canada, the densest aceae Dumort; a result of molecular infestations of L. dalmatica encompass an examination of the Scrophulariaceae area of approximately 3 million ha in the (Albach et al., 2005; Oxelman et al., 2005) dry British Columbia interior, and include and subsequent redistribution of the parts of the Thompson River drainage, family’s genera among seven independent Okanagan Valley, Nicola Valley, and West lineages (families) (Tank et al., 2006; and East Kootenay areas (derived from Schäferhoff et al., 2010). In response, British Columbia Ministry of Forests, members of the North American Linaria Lands and Natural Resource Operations, biological control programme revised the 2012). What may be of increasing concern test plant list to be used for host-range associated with the British Columbia determination of new candidate agents for southern interior and the effects of climate both L. dalmatica and L. vulgaris (sub- change is that L. dalmatica populations are mitted for Canadian/US regulatory review resistant to fi re, and can become more in 2011). The recommended list contains invasive after either controlled burning or 87 spp. within 13 families, including the wildfi res via increased plant density, cover recircumscribed Plantaginaceae, of which and reproductive success relative to native 59 species are native to North America. Of plant species (Jacobs and Sheley, 2003; importance to the programme, the critical Dodge et al., 2008; Pearson et al., 2012). tribe Antirrhineae, to which Linaria belongs, was moved intact to Plantagin- aceae during the phylogenetic revision 52.2 Background (Albach et al., 2005; Tank et al., 2006), and there continues to be no Linaria spp. Since the last review of the Canadian native to North America (Sutton, 1988). biological control programme for L. Thus, the impact on host specifi city testing dalmatica (De Clerck-Floate and Harris, of candidate Linaria agents has been 2002), no new agents have been approved minimal, and if anything, has streamlined for release. However, biological control as the process by allowing us to confi dently a major tool for L. dalmatica mitigation has focus on native plant species of been accepted, especially in British phylogenetic relevance (Gaskin et al., Columbia (Turner, 2008), where the stem 2011). The revised list is currently being weevil, Mecinus janthinus Germar (Cole- used to test a stem-galling weevil, Rhinusa optera: Curculionidae), has been successful brondelii (Brisout) (=R. hispida (Brullé)) in reducing densities (De Clerck-Floate and (Coleoptera: Curculionidae) (Caldara et al., Harris, 2002; Carney, 2003; Van Hezewijk 2008), and an undetermined, stem-mining 344 Chapter 52

Mecinus sp. (Coleoptera: Curculionidae) aligned biotypes of Linaria-feeding insects for L. dal matica (Toševski et al., 2009). (MacKinnon et al., 2005, 2007; Caldara et Although the systematics is being al., 2010; Toševski et al., 2011), it becomes quickly elucidated at the higher taxonomic obvious that determining the genetic levels through DNA analyses, it is at the identity of North America’s Linaria spp., in species level where there remains some conjunction with that of their host-specifi c ambiguity, with implications for the insects, will be crucial to the biological Linaria biological control programmes control programmes for these plants. (Toševski et al., 2011). Two subspecies of L. dalmatica are recognized by taxonomic authorities based on European bio- 52.3 Biological Control Agents geography; Linaria dalmatica subsp. dalmatica (L.) Miller, which is widespread Previous reviews of L. dalmatica biological in Eurasia, and L. dalmatica subsp. control in Canada and North America have macedonica (Griseb.) D.A. Sutton (Plan- listed and described the insect agents tagin aceae), which has a narrower distrib- involved in the joint Canadian–US pro- ution in the mountains of southern gramme (De Clerck-Floate and Harris, Macedonia (Alex, 1962; Integrated 2002; Sing et al., 2005; Wilson et al., 2005). Taxonomic Information System, 2012). Of the fi ve insect agents tested and Linaria dalmatica subsp. dalmatica is what intentionally introduced for L. dalmatica is believed to be present in Canada and biological control in Canada since the throughout most of the USA, whereas L. programme’s fi rst fi eld release of an agent dalmatica subsp. macedonica is not in 1963 (De Clerck-Floate and Harris, 2002; presently recorded in Canada, despite Wilson et al., 2005), three have established being listed for Washington State (United on L. dalmatica: M. janthinus; Rhinusa States Department of Agriculture, Natural antirrhini (Paykull) (=Gymnetron antirrhini Resources Conservation Service, 2012). (Paykull)) (Coleoptera: Curculionidae); and Furthermore, hybridization among Linaria Calophasia lunula (Hufnagel) (Lepi- spp. has long been known to be common doptera: Noctuidae) (De Clerck-Floate and (Chater et al., 1972), and natural Linaria Cárcamo, 2011), and will be assessed in spp. hybrids have been documented for this chapter for their current relevance to North America using molecular analysis, the programme. Although previously i.e. L. dalmatica × L. vulgaris Mill. reported that the root moth Eteobalea (Plantaginaceae) (Ward et al., 2009). There intermediella (Riedl) (Lepidoptera: Cos- also remains uncertainty as to how to mopterigidae) had established within clearly differentiate between L. dalmatica propagation plots at Kamloops, British and L. genistifolia (L.) Miller, broomleaf Columbia (50.67°, −120.33°) based on a toadfl ax (Plantaginaceae), or their hybrids, 1998 release (De Clerck-Floate and Harris, which are collectively treated as a species 2002), the colony only survived to 2002 complex in Europe (Toševski et al., 2011). (S.C. Turner, 2012, unpublished results). The confusion is refl ected in the early No further attempts have been made to taxonomic treatment of L. dalmatica as a establish E. intermediella, so it will not be subspecies of L. genistifolia (Chater et al., discussed further. Similarly, the status of 1972) before acceptance of L. dalmatica as the root-galling weevil Rhinusa linariae a separate but closely related species to L. (Panzer) (=Gymnetron linariae Panzer; genistifolia (Hartl, 1974; Davis, 1978). In Caldara et al., 2010) will not be discussed summary, it is not clear what type or here because it established on L. vulgaris amount of genetic introgression among instead of L. dalmatica (De Clerck-Floate Linaria spp. may have occurred before or and Harris, 2002) (see De Clerck-Floate and after their introduction to North America. McClay, Chapter 53, this volume). As more evidence surfaces on the existence The stem-boring weevil M. janthinus of host species, or species-complex, was given regulatory approval for release Chapter 52 345

against both L. dalmatica and L. vulgaris in at Agriculture and Agri-Food Canada, Canada in 1991 (De Clerck-Floate and Lethbridge, and now are listed in Table Harris, 2002; McClay and De Clerck-Floate, 52.1. Some of the Mecinus sp. received in 2002; also see De Clerck-Floate and British Columbia in 1991 and 1992 were McClay, Chapter 53, this volume). Sub- kept at the provincial weed biological sequently, what was thought to be one control agent propagation facility in species of Mecinus was imported to Kamloops (operated by the British Canada in 1991–1992 as collections mainly Columbia Ministry of Forests, Lands and from L. vulgaris in western Europe, but Natural Resource Operations) for outdoor, also from L. dalmatica subsp. macedonica caged rearing prior to redistribution. It was in Macedonia (Toševski et al., 2011). The material of unknown origin from this time M. janthinus collected from both Linaria that established well on L. dalmatica, and spp. and shipped to Canada during this was subsequently used for the mass- period became mixed during pre-release redistribution of Mecinus sp. that occurred propagation by Agriculture and Agri-Food in British Columbia in 1994. During 1994, it Canada and provincial collaborators, and is estimated that close to 7000 weevils were individuals from the mixed populations produced from one tented plot and released became the originating genetic material for at 27 L. dalmatica sites in British Columbia what subsequently established on either L. (S.C. Turner, 2012, unpublished results), dalmatica or L. vulgaris, and then was ranging from William’s Lake (52.14°, either purposely redistributed or had −122.14°) in the Cariboo Region to Grand dispersed on its own in Canada and the Forks (49.03°, −118.44°) in the West USA. Kootenay (De Clerck-Floate and Harris, Recently, however, it was revealed 2002). The majority of these releases through molecular and biological studies established, and sites where Mecinus sp. that European M. janthinus is composed of populations were beginning to reach two separate, host-affi liated, cryptic outbreak levels were designated by the species: M. janthinus, associated with L. British Columbia Ministry of Forests, Lands vulgaris, and M. janthiniformis Toševski & and Natural Resource Operations as fi eld Caldara (Coleoptera: Curculionidae), collection sites for further redistributions to associated with the L. dalmatica/L. new L. dalmatica sites in the province genistifolia spp. complex (Toševski et al., (Table 52.2). Between 1996 and 2012, 2011). In light of these results, a molecular approximately 219,000 M. janthinus were investigation is in progress to confi rm the redistributed to 771 L. dalmatica sites in identity of the Mecinus spp. that have British Columbia, with the peak movement established on invasive Linaria spp. in occurring in 2001 (Table 52.2). During 2001, North America (research led by I. Toševski, almost half of the redistributed weevils Belgrade, Serbia, 2012). Although the data (15,700/35,100) came from one fi eld site in have not been fully analysed, it may be that William’s Lake, i.e. 5 years after its the Mecinus sp. currently established on L. establishment in 1994 (S.C. Turner, 2012, dalmatica in North America originated unpublished results). Mecinus sp. from from a single shipment of M. janthiniformis British Columbia collection sites also were to Canada in 1992 ‘of about 200 provided to the USA for fi eld release after specimens’, mentioned by Toševski et al. 1995, i.e. when the USA obtained regulatory (2011) as being collected in Macedonia approval for the release of M. janthinus, and from L. dalmatica. periodically to Alberta for research and fi eld Initial fi eld releases of purported M. releases (Table 52.1). Some of those shipped janthinus were made on L. dalmatica to Alberta were used to initiate a L. beginning in 1991 in British Columbia and dalmatica biological control release and 1992 in Alberta (De Clerck-Floate and monitoring programme in the southern Harris, 2002). Records of a few additional region of the province starting in 2005, led early releases have been uncovered recently by R. Bourchier, Agriculture and Agri-Food 346 Chapter 52

Table 52.1. Initial fi eld releases (1992–2002) and updated recoveries of Mecinus janthinusa against Linaria dalmatica in southern Alberta. All releases were of uncaged adults. Source: original/ Location Latitude Longitude Year immediate Number Recoveries Lundbreck 49.58° −114.21° 1992 Unknown/AAFC 30 None; last checked in (Pincher Creekb) Reginac 1994 Scandiab 50.22° −111.99° 1992 Unknown/AAFC 29 1993−1999; present in Reginac 2012 when collection made for molecular analysis Calgary 50.93° −114.06° 1994 Unknown/AAFC 51 1995 found; not Lethbridgec monitored since Lundbreck 49.58° −114.15° 1995 Unknown/AAFC 36 None; last checked in Lethbridgec 2009 Del Bonita 49.03° −112.78° 1996 Unknown/AAFC 74 None; last checked in Lethbridgec late summer 1996 Milk River 49.01° −112.15° 1997 Unknown/ARC 503 Not monitored Vegrevilled Milk River 49.15° −112.08° 1997 Unknown/AAFC 100 None; last checked Lethbridgec 1998, released 526 more in 1998 (below) 1998 Unknowne/ fi eld 526 Not monitored collected in BC ex L. dalmatica Lundbreckf 49.58° −114.21° 2000 Unknowne/ fi eld 1) 300 1) 2001–2004 in low collected in 2) 300 numbersg BC ex L. 2) 2001–2002 in low dalmatica numbersg. In 2003, no toadfl ax present to sample Fort Macleod 49.72° −113.39° 2001 Unknowne/ fi eld 100 2002 found in low collected in numbersg, so BC ex L. released 1000 more dalmatica weevils (below) 2002 Unknowne/ fi eld 1000 2003–2004 found, but collected in remained in low BC ex L. numbersg dalmatica a At the time of releases, it was believed that the species involved was Mecinus janthinus, but an on-going investigation to ascertain the identity of Mecinus spp. established at previous North American release sites may reveal the species to be otherwise. b Releases reported in De Clerck-Floate and Harris (2002). c Original shipments from different European sources made in 1991–1992 had been mixed for rearing at Agriculture and Agri-Food Canada, Regina and Lethbridge on both hosts before redistribution. Molecular analyses are on-going to determine origin. d Greenhouse colony maintained at Alberta Research Council, Vegreville, Alberta, from 1995 to 2002; source material believed to be collections from Rhine Valley, France. e Unknown source of original European populations shipped in 1991–1992, but molecular analyses are on- going to determine origin. f Two releases ca. 1 km apart along railway. g Mean number of adult weevils per dissected toadfl ax stalk (n = 15–30 stalks/site) was generally <5 for all years sampled. Chapter 52 347

Table 52.2. Redistributions of Mecinus janthinusa on Linaria dalmatica in British Columbia using weevils collected from previously established releases on L. dalmatica. Listed information was obtained from biological control agent propagation facility records (Kamloops) held by the British Columbia Ministry of Forests, Lands and Natural Resource Operations (1996–2000) and the Invasive Alien Plant Program database (2001–2012) (British Columbia Ministry of Forests, Lands and Natural Resource Operations, 2012).

Total number of Number of new Average release size Year weevils redistributed releases (±S.E.) Release size range 1996 1,000 7 142.9 (20.2) 100–200 1997 3,430 21 163.3 (10.7) 100–200 1998 13,814b 42 328.9 (18.6) 100–550 1999 24,994c 90 277.7 (13.4) 100–600 2000d 25,700 115 223.5 (13.0) 50–500 2001 35,100 93 377.4 (16.7) 200–1,150 2002 23,497 105 223.8 (16.7) 100–1,262 2003 26,856 87 308.7 (15.2) 100–800 2004 8,830 34 259.7 (17.8) 100–400 2005 19,499 50 390.0 (27.3) 100–1,000 2006 12,100 39 310.3 (16.3) 100–600 2007 8,300 29 286.2 (67.8) 100–2,000 2008 4,342 21 206.8 (30.8) 100–600 2009 2,850 12 237.5 (42.2) 100–500 2010 1,700 9 188.9 (11.1) 100–200 2011 3,550 13 273.1 (77.3) 150–1,200 2012 3,400 4 850.0 (50.0) 800–1,000 a At the time of releases, it was believed that the species involved was Mecinus janthinus, but an on-going investigation to ascertain the identity of Mecinus spp. established at previous North American release sites may reveal the species to be M. janthiniformis. b Total number redistributed in 1998 includes 789 weevils from the Kamloops propagation facility. Remain- der was obtained from British Columbia fi eld collection sites. c Total number redistributed in 1999 includes 2630 weevils from the Kamloops propagation facility. Remainder was obtained from British Columbia fi eld collection sites. d In 2000, the M. janthinus propagation plots in Kamloops were dismantled and all weevils were dispersed for fi eld release. Records of the number of weevils redistributed after 2000 may be less accurate as the pro- gramme became more operational and involved more collaborators.

Canada, Lethbridge, Alberta. From 2005 to interior from the Cariboo region, e.g. Prince 2010, 7332 M. janthinus from British George (53.92°, −122.78°) and Clinton, Columbia were released on L. dalmatica at British Columbia (51.09°, −121.59°), to 19 sites in southern Alberta. near the USA–Canada border in the West The original shipments of the L. Kootenay, e.g. Rock Creek, British dalmatica biotype of R. antirrhini received Columbia (44.05°, −118.99°) (Turner, 2008). and released in British Columbia (1993– The R. antirrhini shipped from Europe and 2000) (De Clerck-Floate and Harris, 2002) released in a garden plot of L. dalmatica at produced offspring for redistribution the Agriculture and Agri-Food Canada, within the province. Approximately 17,000 Lethbridge Research Centre, Lethbridge, R. antirrhini were released at 43 L. Alberta (49.69°, −112.84°) in 1994 and dalmatica fi eld sites between 1996 and 1997 for propagation had not established 2007 by the British Columbia Ministry of (De Clerck-Floate and Harris, 2002) and no Forests, Lands and Natural Resource further attempts have been made to Operations (S.C. Turner, 2012, unpublished introduce the biotype to Alberta. results). Releases ranged in geographic The defoliating moth C. lunula was the latitude within the British Columbia fi rst biological control agent released 348 Chapter 52

against Linaria spp. in Canada in the 1960s establishment ‘blitz’, and then pro- (De Clerck-Floate and Harris, 2002). gressively spreading on the landscape Although released on L. dalmatica in both through both natural dispersal and targeted Alberta and British Columbia, it is only redistribution to new L. dalmatica infest- recorded as established on this species in ations. On average, established M. jan- the southern regions of British Columbia thinus populations took 8 years to peak in (De Clerck-Floate and Harris, 2002; De density (Van Hezewijk et al., 2010), which Clerck-Floate and Cárcamo, 2011) due to allowed for a lengthy period of collection climatic restrictions (McClay and Hughes, for redistribution as outbreaks built on 1995). There have been no organized individual sites. The geospatial data of efforts to redistribute C. lunula in Canada releases and dispersals of M. janthinus since 2000. (also in relation to L. dalmatica distrib- The adventive fl ower beetle Brachyptero- ution on the British Columbia landscape) lus pulicarius (L.) (Coleoptera: Nitidulidae) were incorporated into the Invasive Alien and seed capsule weevil Rhinusa neta Plant Program application, which was (Germar) (=Gymnetron netum (Germar)) launched online in 2005 (Turner, 2008; (Coleoptera: Curculionidae) occur in British Columbia Ministry of Forests, western Canada (De Clerck-Floate and Lands and Natural Resource Operations, Harris, 2002; Wilson et al., 2005). Recent 2012). The program is useful as an inter- studies have confi rmed the existence of active and predictive tool in invasive plant host Linaria sp. biotypes within B. puli- management and biological control fi eld carius (MacKinnon et al., 2005, 2007) and operations, e.g. it can be applied in fi nding R. antirrhini (Hernández-Vera et al., 2010) new collection or release sites. To aid on- with caveats for successful agent redistrib- the-ground operations, methods were ution (MacKinnon et al., 2007). However, developed for monitoring M. janthinus neither B. pulicarius nor R. neta has been population increases and for collecting and actively redistributed on L. dalmatica in distributing weevils. Methods of sexing M. Canada in recent years. During 2002–2010, janthinus also were developed (Carney et the province of British Columbia has al., 2004; Schat et al., 2007), although these documented the adventive occurrence of R. were not used operationally in British neta at 50 L. dalmatica sites (S.C. Turner, Columbia. 2012, unpublished results). Both R. neta The impact of M. janthinus was fi rst and B. pulicarius are considered wide- obvious at the individual plant scale spread in British Columbia, and thus during weevil outbreaks at British unqualifi ed for active redistribution Columbia fi eld sites, and complete (British Columbia Ministry of Forests, suppression of fl owering and severe Lands and Natural Resource Operations, stunting of L. dalmatica shoot growth was 2012). documented (De Clerck-Floate and Harris, 2002; Carney, 2003). Although it was initially hypothesized that it was feeding 52.4 Evaluation of Biological Control by large numbers of spring-emerging adults on the apices of growing L. dalmatica The L. dalmatica biological control pro- shoots that produced the damage (De gramme can be considered one of Canada’s Clerck-Floate and Harris, 2002), recent success stories in invasive plant mitigation studies in Montana have indicated that owing to M. janthinus (tentatively = M. both adult and larval feeding are janthiniformis) in British Columbia. The responsible for the observed impact (Schat provincial propagation and redistribution et al., 2011). Mecinus janthinus feeding programme in itself reveals the sheer size was found to affect the physiological and momentum of the success as M. processes of L. dalmatica by reducing janthinus populations began increasing in photosynthesis, water conductance and 1998 (Table 52.2) after the 1994 release and transpirational rates (Schat, 2008), and the Chapter 52 349

effects were measureable at a threshold poor results and was to be terminated in density of only fi ve M. janthinus larvae per 2011; however, in 2012 there was news of stem (Schat et al., 2011). In a comparative two sites in the Alberta foothills with study, Peterson et al. (2005) also deter- outbreaking populations of M. janthinus mined that M. janthinus had a deleterious (R. Wilson, Lethbridge, Alberta, 2012, pers. effect on L. dalmatica physiology, whereas comm.). C. lunula larval feeding did not, thus Climate effects may help explain the suggesting that the latter may be relatively difference in M. janthinus success between ineffective as a biological control agent. British Columbia and Alberta. Perhaps Evidence of M. janthinus impact at the degree-day larval development require- local level quickly translated to a larger ments are not suffi cient, especially on the regional scale as the weevils spread over Alberta plains (McClay and Hughes, 2007), the southern British Columbia landscape. or M. janthinus may be affected by drought Major changes in the density of L. (Sing et al., 2008). Overwinter survival also dalmatica became apparent at several has been evoked as a potential reason for locations where M. janthinus was in the poor performance in Alberta, especially outbreak between 1998 and 2003, e.g. given that the adults that overwinter in William’s Lake (Turner, 2008) and the West exposed L. dalmatica stalks do not survive Kootenay beginning in 2003 (R. De Clerck- temperatures below −28°C (De Clerck- Floate, 2003, unpublished results), which Floate and Miller, 2002). High overwinter coincided with the peak period of M. mortality of M. janthinus on L. dalmatica janthinus redistribution (Table 52.2). The has been documented at sites on the east regional changes were confi rmed in an side of the Rocky Mountains for both analysis of historical survey data from the Alberta (De Clerck-Floate and Miller, 2002) Invasive Alien Plant Program (British and Montana (Sing et al., 2008), and low Columbia Ministry of Forests, Lands and and variable densities in Colorado Natural Resource Operations, 2012) to- (Jamieson et al., 2012) relative to the same gether with local scale data on L. dalmatica M. janthinus metrics in the southern and M. janthinus densities across a 40,000 British Columbia interior where winter km2 area in southern British Columbia temperatures are milder. (Van Hezewijk et al., 2010). It was There also is the possibility that the determined that between 2000 and 2007, L. wrong Mecinus sp. was released on L. dalmatica decreased in stem length and dalmatica at some sites in Alberta. The plant density as M. janthinus density realization that two cryptic Mecinus spp. increased. Furthermore, L. dalmatica were likely shipped to Canada in 1991– patches became more frag mented in time 1992 and then mixed during early with M. janthinus attack, with 15% of the propagation prior to fi eld release (Table patches totally disappearing. 52.1), may help explain what was observed The success of M. janthinus in British as poor establishment and population Columbia, however, has not transferred to growth of M. janthinus on L. dalmatica for southern Alberta. The early releases of M. at least some of the releases. As mentioned janthinus on L. dalmatica in Alberta have with respect to the L. vulgaris biological had mixed results for those sites monitored control programme (see De Clerck-Floate (Table 52.1), but in many cases where and McClay, Chapter 53, this volume), a re- establishment has been documented, examination of potential causes for success weevil densities have remained low, e.g. an or failure is needed once it is determined average of <5 weevils per stem (Table 52.1), which species of Mecinus has established, versus 25 or more weevils per stem during on what host and where (Toševski et al., an outbreak (De Clerck-Floate and Miller, 2011). 2002). Similarly, the release and moni- The only other released biological toring programme for M. janthinus begun control agent that is demonstrating good in southern Alberta in 2005 has produced establishment and population increase on 350 Chapter 52

L. dalmatica is R. antirrhini. Out of the 43 thiniformis ex L. dalmatica in relation to fi eld releases of R. antirrhini made between M. janthinus ex L. vulgaris; 1996 and 2007 in British Columbia, 26 are 5. Assessing the population dynamics and documented as established, 6 have not host impact of the L. dalmatica biotype of established and 11 have yet to be moni- R. antirrhini where it has established in tored. There are also 29 confi rmed British Columbia, and make recommenda- dispersal sites, to where R. antirrhini has tions for further releases in Canada; spread on its own from release sites (S.C. 6. Completing the screening of further Turner, Kamloops, 2012, unpublished European agents for L. dalmatica if results). The province of British Columbia required (e.g. R. brondelii) and petition for has tracked the releases and distribution of release in Canada. R. antirrhini using the Invasive Alien Plant Program (British Columbia Ministry of Forests, Lands and Natural Resource Oper- Acknowledgements ations, 2012) and have confi rmed a broad biogeoclimatic range for R. antirrhini, We acknowledge the release and/or including the ability to survive from monitoring efforts of R. Bourchier, A. elevations of 290 to 1205 m (Turner, 2008). McClay, B. Van Hezewijk, R. Wilson However, there is no information yet on (Alberta), V. Miller, S. Cesselli and M. the impact of the seed-feeding R. antirrhini DeWolf (British Columbia). E. Pavlik, J. on L. dalmatica populations. Given that L. Otani, T. Larsen and J. Qureshi are dalmatica is not seed limited, and studies thanked for laboratory stem dissections have suggested that available seed-feeding and insect rearing efforts. V. Carney is biological control insects are unlikely to acknowledged for her valuable research on infl uence L. dalmatica density (Grieshop M. janthinus in the West Kootenay, British and Nowierski, 2002), it remains to be seen Columbia, which contributed greatly to whether R. antirrhini will help control its our understanding of the weevil’s host plant. interaction with L. dalmatica. A. Dalcin (Canadian Pacifi c Railway) was an excellent fi eld assistant and companion 52.5 Future Needs during tours of Alberta and British Columbia (2000–2004) to monitor M. Future work should include: janthinus, and V. Miller also is thanked for 1. Continuing use of molecular analyses to her enthusiasm, wisdom and support. I. identify Mecinus spp. and host Linaria spp. Toševski and A. Gassmann (CABI in at previous Canadian release sites where Europe) are acknowledged for their weevil establishment has been successful; passionate push to solve the genetic 2. Further monitoring of Mecinus spp. puzzles of the toadfl ax biological control releases, particularly on L. dalmatica in programme. Support for Canadian research southern Alberta, to determine population over the past 12 years was provided by size and assess impact where appropriate; Agriculture and Agri-Food Canada, British 3. Determining the role of climate in the Columbia Ministry of Forests, Lands and success or failure of Mecinus spp. once Natural Resource Operations, British species identities have been clarifi ed; Columbia Grazing Enhancement Fund and 4. Re-examining the host range of M. jan- Canadian Pacifi c Railway. Chapter 52 351

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Grieshop, M.J. and Nowierski, R.M. (2002) Selected factors affecting seedling recruitment of dalmatian toadfl ax. Journal of Range Management 55, 612–619. Hartl, D. (1974) Familie Scrophulariaceae. In: Hegi, G., Hartl, D. and Wagenitz, G. (eds) Illustrierte Flora von Mittleleuropa, 2nd edn, Bd. VI, Part 1. Carle Hanser, Munich, Germany, pp. 73–94. Hernández-Vera, G., Mitrovic ´ , M., Jovic ´ , J., Toševski, I., Caldara, R., Gassmann, A. and Emerson, B.C. (2010) Host-associated genetic differentiation in a seed parasitic weevil Rhinusa antirrhini (Coleoptera: Curculionidae) revealed by mitochondrial and nuclear sequence data. Molecular Ecology 19, 2286–2300. Integrated Taxonomic Information System (2012) Scrophulariaceae – Taxonomic Serial No. 33005. Available at: http://www.itis.gov (accessed 27 November 2012). Jacobs, J.S. and Sheley, R.L. (2003) Prescribed fi re effects on dalmation toadfl ax. Journal of Range Management 56, 193–197. Jamieson, M.A., Knochel, D., Manrique, A. and Seastedt, T.R. (2012) Top-down and bottom-up controls on Dalmatian toadfl ax (Linaria dalmatica) performance along the Colorado Front Range, USA. Plant Ecology 213, 185–195. Lajeunesse, S.E., Fay, P.K., Cooksey, D., Lacey, J.R., Nowierski, R.M. and Zamora, D. (1993) Dalmatian and Yellow Toadfl ax: Weeds of Pasture and Rangeland. Extension Service, Montana State University, Bozeman, Montana. MacKinnon, D.K., Hufbauer, R.A. and Norton, A.P. (2005) Host-plant preference of Brachypterolus pulicarius, an inadvertently introduced biological control insect of toadfl axes. Entomologia Experimentalis et Applicata 116, 183–189. MacKinnon, D.K., Hufbauer, R.A. and Norton, A.P. (2007) Evaluating host use of an accidentally introduced herbivore on two invasive toadfl axes. Biological Control 41, 184–189. Macoun, W.T. (1908) List of herbaceous perennials tested in the arboretum and botanic garden, Central Experimental Farm, Ottawa, Canada with descriptions of fl owers, and other notes. Bulletin (Canada. Dept. of Agriculture) series 2, number 5. Government Printing Bureau, Ottawa, Ontario, Canada, p. 70. Maron, J.L. and Marler, M. (2008) Field-based competitive impacts between invaders and natives at varying resource supply. Journal of Ecology 96, 1187–1197. McClay, A.S. and De Clerck-Floate, R.A. (2002) Linaria vulgaris Miller, yellow toadfl ax (Scrophulariaceae). In: Mason P.G. and Huber J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 375–382. McClay, A.S. and Hughes, R.B. (1995) Effects of temperature on developmental rate, distribution and establishment of Calophasia lunula (Lepidoptera: Noctuidae), a biocontrol agent for toadfl ax (Linaria spp.). Biological Control 5, 368–377. McClay, A.S. and Hughes, R.B. (2007) Temperature and host-plant effects on development and population growth of Mecinus janthinus (Coleoptera: Curculionidae), a biological control agent for invasive Linaria spp. Biological Control 40, 405–410. Oxelman, B., Kornhall, P., Olmstead, R.G. and Bremer, B. (2005) Further disintegration of Scrophulariaceae. Taxon 54, 411–425. Pearson, D., Ortega, Y. and Sears, S. (2012) Darwin’s naturalization hypothesis up-close: Intermountain grassland invaders differ morphologically and phenologically from native community dominants. Biological Invasions 14, 901–913. Peterson, R.K.D., Sing, S.E. and Weaver, D.K. (2005) Differential physiological responses of Dalmatian toadfl ax, Linaria dalmatica L. Miller, to injury from two insect biological control agents: implications for decision-making in biological control. Environmental Entomology 34, 899–905. Schäferhoff, B., Fleischmann, A., Fischer, E., Albach, D.C., Borsch, T., Heubl, G. and Müller, K.F. (2010) Towards resolving Lamiales relationships: insights from rapidly evolving chloroplast sequences. BMC Evolutionary Biology 10, 352–374. Schat, M. (2008) The impacts of a stem boring weevil, Mecinus janthinus, on Dalmatian Toadfl ax, Linaria dalmatica. PhD thesis, Montana State University, Bozeman, Montana. Schat, M., Sing, S.E. and Peterson, R.K.D. (2007) External rostral characters for differentiation of sexes in the biological control agent Mecinus janthinus (Coleoptera: Curculionidae). Canadian Entomologist 139, 354–357. Chapter 52 353

Schat, M., Sing, S.E., Peterson, R.K.D., Menalled, F.D. and Weaver, D.K. (2011) Growth inhibition of Dalmatian toadfl ax, Linaria dalmatica (L.) Miller, in response to herbivory by the biological control agent Mecinus janthinus Germar. Journal of Entomological Science 46, 232–246. Sing, S.E. and Peterson, R.K. (2011) Assessing environmental risks for established invasive weeds: Dalmatian (Linaria dalmatica) and yellow (L. vulgaris) toadfl ax in North America. International Journal of Environmental Research and Public Health 8, 2828–2853. Sing, S.E., Peterson, R.K.D., Weaver, D.K., Hansen, R.W. and Markin, G.P. (2005) A retrospective analysis of known and potential risks associated with exotic toadfl ax-feeding insects. Biological Control 35, 276–287. Sing, S.E., Weaver, D.K., Nowierski, R.M. and Markin, G.P. (2008) Long-term fi eld evaluation of Mecinus janthinus releases against Dalmatian toadfl ax in Montana (USA). In: Julien, M.H., Sforza, R., Bon, M.C., Evans, H.C., Hatcher, P.E., Hinz, H.L. and Rector, B.G. (eds) Proceedings of the XII International Symposium on Biological Control of Weeds. La Grande Motte, France, 22-27 April 2007. CAB International, Wallingford, UK, pp. 620–624. Sutton, D.A. (1988) A Revision of the Tribe Antirrhineae. British Museum of Natural History, Oxford University Press, London. Tank, D.C., Beardsley, P.M., Kelchner, S.A. and Olmstead, R.G. (2006) L.A.S. Johnson Review No. 7: Review of the systematics of Scrophulariaceae s.l. and their current disposition. Australian Systematic Botany 19, 289–307. Toševski, I., Gassmann, A., Desanc ˇic ´, M. and Jovic ´, J. (2009) Biological control of Dalmatian and yellow toadfl axes, Linaria dalmatica and L. vulgaris. CAB International Annual Report, Delémont, Switzerland. Toševski, I., Caldara, R., Jovic ´ , J., Hernández-Vera, G., Baviera, C., Gassmann, A. and Emerson, B.C. (2011) Morphological, molecular and biological evidence reveal two cryptic species in Mecinus janthinus Germar (Coleoptera, Curculionidae), a successful biological control agent of Dalmatian toadfl ax, Linaria dalmatica (Lamiales, Plantaginaceae). Systematic Entomology 36, 741–753. Turner, S.C. (2008) Post-release evaluation of invasive plant biological control agents in BC using IAPP, a novel database management platform. In: Julien, M.H., Sforza, R., Bon, M.C., Evans, H.C., Hatcher, P.E., Hinz, H.L. and Rector, B.G. (eds) Proceedings of the XII International Symposium on Biological Control of Weeds. La Grande Motte, France, 22–27 April 2007. CAB International, Wallingford, UK, pp. 625–630. United States Department of Agriculture, Natural Resource Conservation Service (2012) The PLANTS Database. National Plant Data Team, Greensboro, North Carolina 27401-490. Available at: http://plants.usda.gov (accessed 20 November 2012). Van Hezewijk, B.H., Bourchier, R.S. and De Clerck-Floate, R.A. (2010) Regional-scale impact of the weed biocontrol agent Mecinus janthinus on Dalmatian toadfl ax (Linaria dalmatica). Biological Control 55, 197–202. Vujnovic, K. and Wein, R.W. (1997) The biology of Canadian weeds. 106. Linaria dalmatica (L.) Mill. Canadian Journal of Plant Science 77, 483–491. Ward, S.M., Fleischmann, C.E., Turner, M.F. and Sing, S.E. (2009) Hybridization between invasive populations of Dalmatian toadfl ax (Linaria dalmatica) and yellow toadfl ax (Linaria vulgaris). Invasive Plant Science and Management 2, 369–378. Wilson, L.M., Sing, S.E., Piper, G.L., Hansen, R.W., De Clerck-Floate, R., MacKinnon, D.K. and Randall, C. (2005) Biology and Biological Control of Dalmatian and Yellow Toadfl ax. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, FHTET-05-13. 354 Chapter 53

53 Linaria vulgaris Mill., Yellow Toadfl ax (Plantaginaceae)

Rosemarie A. De Clerck-Floate1 and Alec S. McClay2 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2McClay Ecoscience, Sherwood Park, Alberta

53.1 Pest Status A risk analysis of L. vulgaris (and L. dalmatica (L.) Miller (Plantaginaceae)) for Yellow toadfl ax, Linaria vulgaris Mill. North America pointed out the scarcity of (Plantaginaceae), is a herbaceous perennial evidence for environmental impact (Sing native to Europe and northern Asia, which and Peterson, 2011), but recent obser- arrived with the fi rst European colonists to vations and studies suggest that L. vulgaris eastern North America in the mid-1700s is a growing problem in natural habitats. It (Mack, 2003). Beginning in the mid-1800s, is increasingly noticeable on the southern it quickly spread throughout temperate interior rangelands of British Columbia North America (Mack, 2003), where it is (British Columbia Ministry of Forests, now an invader of cultivated lands and Lands and Natural Resource Operations, pastures, particularly on the Canadian 2012), foothill fescue rangelands of Prairies (Leeson et al., 2005). In the 1970s, southern Alberta (R. De Clerck-Floate, L. vulgaris was described as the most 2012, unpublished results) and on forest troublesome perennial broad-leaved weed reserves and rangelands of the north- in Alberta (Darwent et al., 1975), with a eastern Rocky Mountains of the USA, e.g. province-wide survey revealing that 30% Colorado and Montana (Pauchard et al., of annual crops, 30% of perennial forage 2003; Sutton et al., 2007; Lehnhoff et al., crops, 20% of pastures and 20% of non- 2008). Recent incursions of L. vulgaris have agricultural land were infested. Crop occurred in protected areas, e.g. Yellow- surveys conducted in Alberta, Saska- stone National Park (Pauchard et al., 2003), tchewan and Manitoba in 2000–2004 including sensitive, subalpine habitats, reported L. vulgaris as a continuing prob- where signifi cant impacts have been lem for spring wheat, Triticum aestivum L., documented on phenology and abundance barley, Hordeum vulgare L., oats, Avena of fl owering in native plant communities sativa L. (Poacaeae), canola/rapeseed, (Wilke and Irwin, 2010). Brassica napus L., B. rapa L., mustard, Invasions by L. vulgaris are facilitated Sinapis alba L. (Brassicaceae), and fi eld by either natural or human disturbances peas, Pisum sativum L. (Fabaceae), in the such as fi re (Fornwalt et al., 2010), and the Peace River Lowland of Alberta and the weed is an effective invader at both local Aspen Parkland ecoregion of the prairie and landscape scales due to its clonal provinces (Leeson et al., 2005). growth from creeping roots (Nadeau et al.,

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 53 355

1991) and ability to disperse and establish used for host-range determination of new via seed in a wide range of climates and candidate agents for L. vulgaris and L. habitats (Pauchard et al., 2003; Pauchard dalmatica (submitted for Canadian/US and Shea, 2006). In Canada, L. vulgaris can regulatory review in 2011). The recom- establish at elevations greater than 2000 m mended list contains 87 species within 13 and latitudes of up to 65°N (Saner et al., families, including the recircumscribed 1994). It was recently found on Sable Plantaginaceae, of which 59 species are Island off the western coast of Nova Scotia native to North America. Of note however, (Catling et al., 2009), indicating its is that the critical tribe Antirrhineae, to continuing spread. On native rangelands, which Linaria belongs, was moved in its L. vulgaris can displace valued forage entirety to Plantaginaceae during the species used by both domestic and native phylogenetic revision (Albach et al., 2005; ungulates (see Pauchard et al., 2003), and Tank et al., 2006), and there continues to may be found unpalatable by grazers due be no Linaria spp. native to North America to the presence of iridoid glycosides (Sutton, 1988). The revisit of the test plant (Mitich, 1993). species list has actually streamlined testing by focusing on native species of phylo- genetic relevance (Gaskin et al., 2011). The 53.2 Background revised list is currently being used to test a more cold-tolerant species of stem-mining Biological control agent releases and moni- weevil, Mecinus heydeni Wencker (Cole- toring in Canada for L. vulgaris have been optera: Curculionidae) (Toševski et al., minimal since the last report (McClay and 2005), for L. vulgaris, and was recently De Clerck-Floate, 2002), mostly due to the used to test the stem-galling weevil lacklustre performance of the majority of Rhinusa pilosa (Gyllenhal) (Coleoptera: available agents on this target host. Curculionidae), which was petitioned in However, since 2000, additional European 2012 for release in Canada and the USA insects have been investigated as candidate (response pending as of November 2012). biological control agents, and a re- Rhinusa pilosa is a promising biological examination of the North American control agent for L. vulgaris because of its biological control programme (for both L. high host specifi city, robustness during vulgaris and L. dalmatica; see De Clerck- rearing, evidence of negative impact on Floate and Turner, Chapter 52, this host growth and reproduction through volume) is under way, particularly in light galling (Barnewall, 2011; Barnewall and De of new information on the phylogenetics of Clerck-Floate, 2012), and expected popu- the plants and insects involved (Caldara et lation release from the effects of a Euro- al., 2008, 2010; Gaskin et al., 2011; pean gall intruder, the inquiline weevil Toševski et al., 2011). Rhinusa eversmanni (Rosenschöld) (Cole- As described in Chapter 52, the genus optera: Curculionidae) (I. Toševski, Bel- Linaria has been transferred from the grade, Serbia, 2008–2012, pers. comm.). family Scrophulariaceae Dumort into the Plantaginaceae Dumort. This was a result of molecular examination of the former 53.3 Biological Control Agents taxonomic group’s phylogeny through DNA sequencing (Albach et al., 2005; Both adventively and purposely intro- Oxelman et al., 2005) and subsequent duced European insects for the control of redistribution of its genera into seven L. vulgaris have been previously listed in independent lineages (families) (Tank et summaries of the North American pro- al., 2006; Schäferhoff et al., 2010). This gramme (McClay and De Clerck-Floate, prompted participants in the North 2002; Sing et al., 2005; Wilson et al., 2005). American Linaria biological control pro- Although there have been no new gramme to revise the test plant list to be biological control agents released against L. 356 Chapter 53

vulgaris in Canada since 1997 (De Clerck- 52, this volume). Subsequently, what was Floate and Cárcamo, 2011), a brief status believed to be one species of Mecinus was report on all existing biological control imported to Canada in 1991–1992 as insects will be given for the period 2000– collections mainly from L. vulgaris in 2012, including any changes in taxonomic western Europe, but also from L. dalmatica nomenclature that have occurred. ssp. macedonica (Grisebach) D.A. Sutton The adventive fl ower-feeding beetle in Macedonia (Toševski et al., 2011). What Brachypterolus pulicarius (L.) (Coleoptera: was shipped at this time is believed to be Nitidulidae) and seed-feeding weevils the originating genetic material of what Rhinusa antirrhini (Paykull) (= Gymnetron subsequently established on either L. vul- antirrhini (Paykull)) and R. neta (Germar) garis or L. dalmatica, and then was either (=Gymnetron netum (Germar)) (Coleoptera: purposely redistributed or had dispersed Curculionidae) (Caldara et al., 2010) on its own in Canada and the USA. continue to be widespread on L. vulgaris in However, molecular and biological evi- North America (Sing et al., 2005; Wilson et dence has recently shown that populations al., 2005), including in western Canada (De known as M. janthinus in Europe are Clerck-Floate and Cárcamo, 2011). Thus, composed of two separate, host-affi liated, no redistribution of these agents on L. cryptic species, M. janthinus, associated vulgaris was done in Canada during 2000– with L. vulgaris, and M. janthiniformis 2012. Toševski & Caldara (Coleoptera: Curcu- The defoliating moth Calophasia lunula lionidae), associated with L. dalmatica and (Hufnagel) (Lepidoptera: Noctuidae) is also L. genistifolia (L.) Miller (Toševski et al., dispersing on its own. Originally released 2011). In light of these results, an on L. dalmatica in British Columbia in investigation is under way to confi rm the 1963, it was not released on L. vulgaris identity of the Mecinus spp. that have until 1965 in Saskatchewan and 1985 in established on invasive Linaria spp. in Alberta, and in neither case has it North America. established (De Clerck-Floate and Cárcamo, From 1994 to 2000, releases of 2011). However, since 2000, larvae of C. purported M. janthinus were made on L. lunula have been observed on L. vulgaris vulgaris mainly in Alberta, but also in in the Southern Interior of British Saskatchewan and Nova Scotia (McClay Columbia (British Columbia Ministry of and De Clerck-Floate, 2002). In 2001–2002, Forests, Lands and Natural Resource a further 23 releases were made on L. Operations, 2012), which fi ts with pre- vulgaris in Alberta. Material for these dictions for its spread based on degree-day releases came mainly from a colony requirements for development (McClay and maintained at Vegreville, Alberta, and Hughes, 1995). It is suspected that some originating from L. vulgaris in the French populations of C. lunula found on L. Rhine Valley (Table 53.1). However, several vulgaris have moved from nearby colonies releases in Alberta and British Columbia on L. dalmatica (De Clerck-Floate and on L. vulgaris in the mid-2000s used Cárcamo, 2011). No new information is weevils redistributed from populations on available for eastern Canada, although C. L. dalmatica (Table 53.1). There also was a lunula was reported as common in Nova peculiar case of Mecinus sp. appearing on a Scotia in 2000 (McClay and De Clerck- L. vulgaris infestation that had invaded a Floate, 2002). successful houndstongue, Cynoglossum The stem-boring weevil Mecinus jan- offi cinale (L.) (Boraginaceae), biological thinus Germar (Coleoptera: Curculionidae) control site in south-eastern British was approved for release against both L. Columbia sometime between 2000 and vulgaris and L. dalmatica in Canada in 2002. Mecinus sp. was fi rst noticed feeding 1991 (De Clerck-Floate and Harris, 2002; on L. vulgaris at the site in 2004 and is McClay and De Clerck-Floate, 2002; also suspected to have moved from nearby see De Clerck-Floate and Turner, Chapter releases made on L. dalmatica in 2000 Chapter 53 357

Table 53.1. Releases and recoveries of Mecinus janthinusa against Linaria vulgaris in Canada, 2001–2002, and information on some releases made in 2000* which were previously unreported. All releases were of uncaged adults.

Location Latitude Longitude Year Source: original/immediate Number Recoveries

Alberta Kinsella 52.94 −110.52 1996, France/ARCb 720 Population still present in 1997 2007 Rosalind 52.74 −112.50 1996 France/ARCb 194 44.9d; population still present in 2012 Kinsella 53.00 −111.43 1997 France/ARCb 200 Noned Tofi eld 53.53 −112.59 1997 France/ARCb 200 Noned Edmonton 53.48 −113.61 1997 France/ARCb 533 1.0d Edmonton 53.48 −113.56 1998 France/ARCb 200 2.6d Edmonton 53.48 −113.48 1998 France/ARCb 200 Noned Edmonton 53.48 −113.47 1998 France/ARCb 200 0.8d (larvae only) Kinsella 53.00 −111.53 1998 France/ARCb 200 Noned Fairview 55.96 −118.36 1998 France/ARCb 200 Could not locate release point Fairview 56.03 −118.68 1998 France/ARCb 200 Noned Fairview 56.04 −118.10 1998 France/ARCb 200 Site cultivated Brownvale 56.13 −117.89 1999 France/ARCb 60 Noned Edmonton 53.48 −113.55 1999 France/ARCb 100 4.7d; no population found in 2008 Edmonton 53.53 −113.57 1999 France/ARCb 100 15.2d; population still present in 2012 Langdon 50.80 −113.70 1999 France/ARCb 60 5.6d Derwent 53.72 −110.99 2000 France/ARCb 200 Noned Kinsella 53.02 −111.43 2000 France/ARCb 200 Noned Pine Lake 52.04 −113.38 2000 France/ARCb 400 2 closely spaced releases; Noned Fairview 56.10 −118.42 2000 France/ARCb 200 Noned Whitelaw 55.94 −117.99 2000 France/ARCb 200 Noned Grande Prairie 55.21 −118.79 2000 France/ARCb 200 Noned Longview* 50.51 −114.19 2000 Unknownc/fi eld collected Grand 200 None; checked in 2002 Forks, BC ex L. dalmatica Maycroft* 49.82 −114.24 2000 Unknownc/fi eld collected Grand 200 None; checked in 2002 Forks, BC ex L. dalmatica Breton 53.09 −114.49 2001 France/ARCb 200 84.4d Berwyn 56.08 −117.67 2001 France/ARCb 100 2.1d Peace River 56.16 −117.43 2001 France/ARCb 100 Noned Peace River 56.19 −117.35 2001 France/ARCb 100 Noned Grimshaw 56.15 −117.50 2001 France/ARCb 100 Noned Paradise Valley 53.12 −110.41 2001 France/ARCb 400 4.1d (mean of 4 closely spaced releases) Hines Creek 56.16 −118.79 2001 France/ARCb 100 2.1d (larvae only) Whitelaw 56.16 −118.03 2001 France/ARCb 100 1.5d (larvae only; mean of 2 closely spaced releases) Grande Prairie 55.29 −118.85 2001 France/ARCb 300 62.3d (larvae only) Strome 52.91 −112.13 2002 France/ARCb 200 Not monitored Kelsey 52.77 −112.63 2002 France/ARCb 200 Not monitored Fairview 56.04 −118.68 2002 France/ARCb 200 Not monitored Fairview 55.93 −118.36 2002 France/ARCb 200 Not monitored Whitelaw 56.16 −118.03 2002 France/ARCb 200 Not monitored Whitelaw 56.16 −118.03 2002 France/ARCb 200 Not monitored

Continued 358 Chapter 53

Table 53.1. Continued

Location Latitude Longitude Year Source: original/immediate Number Recoveries Whitelaw 56.16 −118.05 2002 France/ARCb 200 Not monitored Hines Creek 56.16 −118.79 2002 France/ARCb 200 Not monitored Vegreville 53.50 −112.10 2002 France/ARCb 220 Not monitored British Columbia Donald* 51.30 −116.95 2000 Unknownc/fi eld collected Grand 400 None; checked in 2001, Forks, BC ex L. dalmatica 2004, 2010 Blaeberry* 51.43 −117.05 2000 Unknownc/fi eld collected Grand 400 None; checked in 2001, Forks, BC ex L. dalmatica 2010 a Note that at the time of releases, it was believed that the species involved was Mecinus janthinus, but an on-going investigation to ascertain the identity of Mecinus spp. established at previous North American release sites may reveal otherwise. b Greenhouse colony maintained at Alberta Research Council, Vegreville, Alberta, from 1995 to 2002; source material believed to be collections from Rhine Valley, France. c Original shipments from different European sources made in 1991–1992 had been mixed for rearing on both hosts before redistribution, but molecular analyses are on-going to determine origin. d Live Mecinus per 100 stems in samples taken September 2001.

(ca. 2.5 km away), which were at outbreak 2010) was approved for release in Canada levels in 2003 (R. De Clerck-Floate, 2003, against L. vulgaris in 1995 (McClay and De unpublished results). The identity of the Clerck-Floate, 2002). After repeated Mecinus established at this site, and also of attempts to establish garden populations the host plant (a hybrid Linaria sp. may be on L. vulgaris for propagation at Leth- involved), are currently being investigated bridge, Alberta (1996, 1997) and Kamloops, using molecular analysis. British Columbia (1997, 1998) using The root moth Eteobalea serratella imported R. linariae from the Rhine Valley, (Treitschke) (Lepidoptera: Cosmopteri- Europe, success fi nally was achieved at gidae) was fi rst introduced to Canada in Kamloops (McClay and De Clerck-Floate, 1992 specifi cally for the biological control 2002). Using insects from the Kamloops of L. vulgaris (McClay and De Clerck- propagation plots, fi eld releases of R. Floate, 2002). However, after repeated linariae on L. vulgaris in British Columbia failed attempts to establish this diffi cult-to- began in 2001 (British Columbia Ministry rear insect in Alberta (1992, 1995, 1996), of Forests, Lands and Natural Resource British Columbia (1992, 1995), Saska- Operations, 2012; Table 53.2). Because tchewan (1993) and Nova Scotia (1992, populations are slow to build up, col- 1995) (McClay and De Clerck-Floate, 2002), lections from the plots for redistribution no further introductions were made for the have been made every 2–4 years (S. Turner, purposes of either development of propa- Kamloops, 2012, pers. comm.). Insects gation methods or fi eld release. The 1995 from the Kamloops plots also have been E. serratella release site at Kinsella, shared with the USA in 2008 (British Alberta, where larvae were found 1 year Columbia Ministry of Forests, Lands and after release, was resampled in 2007 and Natural Resource Operations, 2012) and no larvae or signs of root damage were Lethbridge in 2010 (145 weevils to start a found. A PCR-based method for separating garden colony). E. serratella and E. intermediella Riedl (Lepidoptera: Cosmopterigidae) has been developed (Mitchell et al., 2005). 53.4 Evaluation of Biological Control The root-galling weevil Rhinusa linariae (Panzer) (=Gymnetron linariae Panzer) As noted in De Clerck-Floate and Turner (Coleoptera: Curculionidae) (Caldara et al., (Chapter 52, this volume), evaluation of Chapter 53 359

Table 53.2. Releases and recoveries of Rhinusa linariae against Linaria vulgaris in British Columbia, 2001– 2012. All releases were of uncaged adults except for galls with larvae released in Kamloops in 2012.* Location Latitude Longitude Year Number Recoveries Pritchard 50.57 −119.85 2001 200 Population found in 2002, 2003, 2008; not found in 2012 Barrière 51.13 −120.12 2001 100 Population found in 2003, 2004, 2005, 2008, 2010, 2011; not found in 2009 Bull River 49.51 −115.49 2002 200 Population found in 2004, not checked since Westwold 50.44 −119.82 2006 200 Population found in 2008; not found in 2007, 2012 Barrière 51.24 −119.95 2006 200 Population found in 2008, 2009, 2010, 2011, 2012; not found in 2007 Chase 50.83 −119.94 2006 200 Population found in 2008, 2010, 2011, 2012; not found in 2007 Kamloops 50.67 −120.67 2009 348 Population found in 2010, 2012 2012 50 Not monitored 2012 1417* Not monitored 100 Mile House 51.82 −121.57 2010 115 Population not found 2011, 2012 100 Mile House 51.82 −121.57 2012 127 Not monitored Westwold 51.79 −119.89 2012 70 Not monitored agent establishment and impact for both L. Alberta (Table 53.1) and Nova Scotia (G. vulgaris and L. dalmatica in Canada and Sampson, Truro, 2009, pers. comm.; the USA has been slowed as we clarify the R. DeClerck-Floate, 2009, unpublished identities of the insects and host plants results). Only a few releases in Alberta involved. In some situations, poor have been monitored since 2001. However, establishment and/or impact may be due to at a site where M. janthinus was released the inadvertent release of the wrong in 1996 near Rosalind, Alberta, and which species or biotype, which we expect to be was checked visually in October 2012, L. revealed with on-going molecular analyses. vulgaris had declined to very low density, Such information not only will help with the few remaining stems heavily determine potential causes for success or infested with M. janthinus (A. McClay, failure of agent releases, but also introduce 2012, unpublished results). future effi ciencies in biological control The revelation that two cryptic Mecinus programmes. For instance, recent studies spp. were likely released in North America on B. pulicarius (MacKinnon et al., 2005, in 1991–1992 may help explain what was 2007) and R. antirrhini (Hernández-Vera et observed as poor establishment and al., 2010) are revealing the presence of host population growth of the weevil on L. biotypes, with implications for agent vulgaris relative to what was occurring redistribution if successful biological with releases on L. dalmatica (McClay and control is to be achieved (MacKinnon et De Clerck-Floate, 2002). Particularly in al., 2007). Molecular information on the British Columbia, the majority of fi eld presence of viable and fertile natural releases of the weevil on L. dalmatica hybrids of L. vulgaris and L. dalmatica starting in 1994 had established and (Ward et al., 2009) and high levels of quickly built to outbreak levels (De Clerck- intraspecifi c genetic variation of L. vulgaris Floate and Harris, 2002; Carney, 2003). (Ward et al., 2008) also will need to be Although climatic differences in habitats taken into account when assessing bio- where L. dalmatica versus L. vulgaris tend logical control outcomes. to grow can also be invoked as an There currently are confi rmed popu- explanation for differential weevil success lations of M. janthinus on L. vulgaris in at release sites (McClay and Hughes, 2007), 360 Chapter 53 any previous conclusions now require re- thinus ex L. vulgaris in relation to M. jan- examination once it is determined which thiniformis ex L. dalmatica; species of Mecinus has established, on 5. Assessing the population dynamics and what host and where (Toševski et al., impact of R. linariae on L. vulgaris where it 2005). For instance, it is now realized that has established in British Columbia, and the failure of releases on L. vulgaris using make recommendations for further releases Mecinus redistributed from L. dalmatica in in Canada; British Columbia (Table 53.1) were likely 6. Obtaining regulatory approval for fi eld the result of matching the wrong species release of the stem-galling weevil R. pilosa, (M. janthiniformis) to target host (R. De make fi rst fi eld releases of laboratory- Clerck-Floate, 2012, unpublished results). reared weevils on L. vulgaris in Canada, Within an experiment to model degree-day and assess establishment. Conducting requirements for development of then laboratory experiments in development of identifi ed ‘M. janthinus’ on both L. vulgaris optimal strategies for release of the weevil; and L. dalmatica, there also was an 7. Completing the screening of further unexplained high mortality of the weevil European agents for L. vulgaris, e.g. cold- on the latter host (McClay and Hughes, tolerant stem weevil, M. heydeni, and peti- 2007). tion for release in Canada. The root-galling weevil R. linariae has clearly established on L. vulgaris in British Columbia based on repeated monitoring at Acknowledgements most sites (Table 53.2). However, there is no information yet on the population We acknowledge the release and/or dynamics or impact of the agent on its host. monitoring efforts of R. Hughes (Alberta), S. Turner, S. Cesselli (British Columbia) and G. Sampson, S. Sing (Nova Scotia). 53.5 Future Needs Emily Barnewall (MSc, University of Lethbridge) is acknowledged for her Future work should include: research contributions on R. pilosa biology, 1. Continuing use of molecular analyses to rearing, impact and host specifi city. Ivo identify Mecinus spp. and host Linaria spp. Toševski and André Gassmann (CABI in at previous Canadian release sites where Europe) are acknowledged for their weevil establishment has been successful; passionate push to solve the genetic 2. Further monitoring of Mecinus spp. puzzles of the toadfl ax biological control releases particularly on L. vulgaris, to programme. John Gaskin (USDA-ARS) is determine population size and assess thanked for molecular analyses of L. impact where appropriate; vulgaris samples. Support for Canadian 3. Determining the role of climate in the research on R. pilosa was provided by success of Mecinus spp. once species iden- British Columbia Ministry of Forests, tities have been clarifi ed; Lands and Natural Resource Operations 4. Re-examining the host range of M. jan- and Agriculture and Agri-Food Canada.

References

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Barnewall, E. and De Clerck-Floate, R. (2012) A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod-Plant Interactions 6, 449–459. British Columbia Ministry of Forests, Lands and Natural Resource Operations (2012) Invasive Alien Plants Program. Available at: http://www.for.gov.bc.ca/hra/plants/index.htm (accessed 12 November 2012). Caldara, R., Desanc ˇic ´ , M., Gassmann, A., Legarreta, L., Emerson, B.C. and Toševski, I. (2008) On the identity of Rhinusa hispida (Brullé) and its current synonyms (Coleoptera: Curculionidae). Zootaxa 1805, 61–68. Caldara, R., Sassi, D. and Toševski, I. (2010) Phylogeny of the weevil genus Rhinusa Stephens based on adult morphological characters and host plant information (Coleoptera: Curculionidae). Zootaxa 2627, 39–56. Carney, V.A. (2003) Ecological interactions of biological control agent, Mecinus janthinus Germar, and its target host, Linaria dalmatica (L.) Mill. MSc thesis, University of Lethbridge, Lethbridge, Canada. Catling, P., Lucas, Z. and Freedman, B. (2009) Plants and insects new to Sable Island, Nova Scotia. Canadian Field-Naturalist 123, 141–145. Darwent, A.L., Lobay, W., Yarish, W. and Harris, P. (1975) Distribution and importance in Northwestern Alberta of toadfl ax and its insect enemies. Canadian Journal of Plant Science 55, 157–162. De Clerck-Floate, R. and Cárcamo, H. (2011) Biocontrol arthropods: new denizens of Canada’s grassland agroecosystems. In: Floate, K. (ed) Arthropods of Canadian Grasslands, Vol. 2: Inhabitants of a Changing Landscape. Biological Survey of Canada Monograph Series No. 4, Biological Survey of Canada, Canada, pp. 291–321. De Clerck-Floate, R.A. and Harris, P. (2002) Linaria dalmatica (L.) Miller, Dalmatian toadfl ax (Scrophulariaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 368–374. Fornwalt, P.J., Kaufmann, M.R. and Stohlgren, T.J. (2010) Impacts of mixed severity wildfi re on exotic plants in a Colorado ponderosa pine-Douglas-fi r forest. Biological Invasions 12, 2683– 2695. Gaskin, J.F., Bon, M.-C., Cock, M.J.W., Cristofaro, M., Biase, A., De Clerck-Floate, R., Ellison, C.A., Hinz, H.L., Hufbauer, R.A., Julien, M.H. and Sforza, R. (2011) Applying molecular-based approaches to classical biological control of weeds. Biological Control 58, 1–21. Hernández-Vera, G., Mitrovic ´ , M., Jovic ´ , J., Toševski, I., Caldara, R., Gassmann, A. and Emerson, B.C. (2010) Host-associated genetic differentiation in a seed parasitic weevil Rhinusa antirrhini (Coleoptera: Curculionidae) revealed by mitochondrial and nuclear sequence data. Molecular Ecology 19, 2286–2300. Leeson, J.Y., Thomas, A.G., Hall, L.M., Brenzil, C.A., Andrews, T., Brown, K.R. and Van Acker, R.C. (2005) Prairie Weed Survey. Cereal, Oilseed and Pulse Crops 1970s to the 2000s. Weed Survey Series Publication 05-1. Agriculture and Agri-Food Canada, Saskatoon, Canada. Lehnhoff, E.A., Rew, L.J., Maxwell, B.D. and Taper, M.L. (2008) Quantifying invasiveness of plants: a test case with yellow toadfl ax (Linaria vulgaris). Invasive Plant Science and Management 1, 319–325. Mack, R.N. (2003) Plant naturalizations and invasions in the Eastern United States: 1634-1860. Annals of the Missouri Botanical Garden 90, 77–90. MacKinnon, D.K., Hufbauer, R.A. and Norton, A.P. (2005) Host-plant preference of Brachypterolus pulicarius, an inadvertently introduced biological control insect of toadfl axes. Entomologia Experimentalis et Applicata 116, 183–189. MacKinnon, D.K., Hufbauer, R.A. and Norton, A.P. (2007) Evaluating host use of an accidentally introduced herbivore on two invasive toadfl axes. Biological Control 41, 184–189. McClay, A.S. and De Clerck-Floate, R.A. (2002) Linaria vulgaris Miller, yellow toadfl ax (Scrophulariaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 375–382. McClay, A.S. and Hughes, R.B. (1995) Effects of temperature on developmental rate, distribution and establishment of Calophasia lunula (Lepidoptera: Noctuidae), a biocontrol agent for toadfl ax (Linaria spp.). Biological Control 5, 368–377. McClay, A.S. and Hughes, R.B. (2007) Temperature and host-plant effects on development and population growth of Mecinus janthinus (Coleoptera: Curculionidae), a biological control agent for invasive Linaria spp. Biological Control 40, 405–410. 362 Chapter 53

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54 Lythrum salicaria L., Purple Loosestrife (Lythraceae)

Jim Corrigan,1 Dave R. Gillespie,2 Rosemarie De Clerck-Floate3 and Peter G. Mason4 1British Columbia Ministry of Forests, Lands and Natural Resource Operations, Vernon, British Columbia; 2Agriculture and Agri-Food Canada, Agassiz, British Columbia; 3Agriculture and Agri-Food Canada, Lethbridge, Alberta; 4Agriculture and Agri-Food Canada, Ottawa, Ontario

54.1 Project Status (2002). The establishment and increase of two leaf beetles, Galerucella calmariensis Purple loosestrife, Lythrum salicaria L. L. and G. pusilla Duftschmid (Coleoptera: (Lythraceae), is an invasive wetland per- Chrysomelidae), is well documented ennial of Eurasian origin that occurs in all (Lindgren et al., 2002; Denoth and Myers, Canadian provinces. Biological control is 2005). The root weevils Nanophyes an important strategy for its long-term marmoratus Goeze and Hylobius trans- management. Lindgren et al. (2002) pro- versovittatus Goeze (Coleoptera: Curcu- vided details on its environmental impact, lionidae) were released at various locations biological control agents introduced, and in Canada (Lindgren et al. 2002), and the documented releases and recoveries to status of these two species in Canada is not 1999. Further studies by Blossey et al. known, although McAvoy et al. (2002) (2001) demonstrated that the invasion of L. reported establishment of H. transverso- salicaria into freshwater wetlands alters vittatus in Virginia, USA. decomposition rates and nutrient cycling, Lindgren et al. (2002) recommended leads to reductions in wetland plant that future work in Canada should include: diversity, reduces pollination and seed (i) assessing the establishment of H. output of the native Lythrum alatum Pursh transversovittatus and N. marmoratus; (ii) (Lythraceae) and reduces habitat suitability long-term monitoring of G. calmariensis for specialized wetland bird species. A and G. pusilla and changes in L. salicaria recent study by Hovik et al. (2011) populations; (iii) documenting the demonstrated that L. salicaria mono- response of native plant communities; and cultures decrease colonization of wetlands (iv) developing integrated strategies to by native plants compared to monocultures manage L. salicaria. Here we report on of the native broadleaf cattail, Typha progress related to the second recom- latifolia L. (Typhaceae). mendation. Introductions of four agents were made In British Columbia, Denoth and Myers at various locations across Canada, and (2005) studied the spatial and temporal these were documented in Lindgren et al. variability in G. calmariensis feeding and

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 364 Chapter 54 the effects of feeding on L. salicaria a 17-week period. In contrast, G. pusilla populations in the lower mainland where numbers decreased over the study and no >4000 individuals of this biological control larvae or adults were produced in the third agent were released from 1993 to 1997. year of the study, indicating a failure to They found that G. calmariensis were not establish. present in tidal locations, but at non-tidal In 2004, a survey was conducted to sites beetles were present and in some determine the status of G. calmariensis and cases there was a rapid increase in feeding G. pusilla at locations where these species damage from low levels to complete had been released from 1992 to 1997 defoliation within a year. These high levels during the Ontario Biological Control of defoliation once attained were generally Program against Purple Loosestrife sustained in subsequent years. Where (Corrigan, 2005). A total of 148 samples populations were high, G. calmariensis containing adult Galerucella spp. were larval feeding reduced fl ower-bud densities taken at or near release sites established in of infl orescences, decreased the length of 1994–1997 (Fig. 54.1). From these samples, infl orescences and reduced per m2 dry 2638 adult Galerucella spp. were pinned, biomass of L. salicaria. The presence of labelled, sexed and identifi ed to species; generalist predators was considered to be a >91% (1309ƂƂ, 1093ƃƃ) were identifi ed factor that may delay or hinder G. as G. calmariensis and 8.6% (110ƂƂ, calmariensis outbreaks (Denoth and Myers, 118ƃƃ) were G. pusilla. Two additional 2005). Galerucella spp. (8 specimens) comprised a A similar scenario was found at a site small proportion of the total collection. where it was believed that a mix of G. Introduced Galerucella spp. were present calmariensis and G. pusilla from the at 175 of the 194 original release sites Agriculture and Agri-Food Canada, visited (90%). Adult specimens of one or Lethbridge Research Centre, Alberta, was both of G. calmariensis and G. pusilla were released in 1998 near Edmonton, Alberta collected at 160 of these 175 release sites, (53.41°, −113.82°). In 2000, outbreak levels adult G. calmariensis were found at 157 of of the beetle were found along with 160 of these locations (98%) and adult G. extensive feeding damage to >90% of the L. pusilla were found at 34 sites (21%). salicaria occurring within a 1 ha area (J. The results show that G. calmariensis Motta, Edmonton, Alberta, 2000, pers. has dispersed extensively, and is the comm.). Beetles from this site were dominant species in most regions of subsequently redistributed to a new L. Ontario (Corrigan, 2005). Galerucella salicaria infestation in the region, and calmariensis was recovered at virtually samples collected in 2010 from the original every site where adult beetles were col- release site were confi rmed to be composed lected, including many of the release sites of only G. calmariensis (n=18) (R. De originally initiated with populations of G. Clerck-Floate, 2012, unpublished results). pusilla. In contrast, G. pusilla was A recent revisit of the site in 2011 recovered only in the immediate vicinity of confi rmed heavy larval feeding by G. locations where populations of this species calmariensis on only a few, scattered L. had been released in the 1990s, with the salicaria plants, the majority of which were exceptions of several small areas of the not fl owering (A. McClay, Sherwood Park, Grand River watershed in Cambridge, and Alberta, 2011, pers. comm.). in the eastern part of the Niagara Peninsula In Ontario, Dech and Nosko (2002) where several samples taken near Niagara studied populations of G. calmariensis and Falls were dominated by G. pusilla. G. pusilla introduced in 1995 near North Furthermore, G. pusilla was not collected Bay (46.35°, −79.43°). They found that over at release sites initiated exclusively with a 3-year period (1996–1998) G. cal- populations of fi eld-collected beetles mariensis numbers increased signifi cantly, which formed the basis of the Ontario and producing three generations of adults over Grand River Release Programs in 1996 and Chapter 54 365

G. calmariensis G. pusilla

Fig. 54.1. Galerucella spp. collected in southern Ontario in 2004 at locations where releases were made from 1994 to 1997.

1997. Only two of these ‘redistributed’ populations of L. salicaria in many regions beetle release sites hosted G. pusilla in of Ontario. Furthermore, the 2004 survey 2004, and both of these can be linked to provided fundamental infor mation about releases made from the laboratory colony how this plant/herbivore complex has in 1996. Galerucella pusilla were not developed from the initial biological control recovered at a number of locations where agent introductions to its present status as a both G. calmariensis and G. pusilla were successful area-wide biological control released at sites that had been in the initiative. This new information will also vanguard of beetle activity in Ontario in allow for the design of more effective the mid-1990s. These ‘vanguard’ sites release programmes in the future. (Speed River, Guelph; Mercer’s Glen, Royal Botanical Gardens, Burlington; Grand River at Highway 7, Kitchener; Dixie Rd, 54.2 Future Needs Mississauga) were among the fi rst release locations in Ontario where effective Future work should include: Galerucella spp. populations developed. It 1. On-going monitoring of distribution and is known that G. pusilla had established impact of Galerucella calmariensis, G. populations at all of these sites, and it was pusilla, H. transversovittatus and N. mar- believed that the ‘dual-species’ status of moratus in all provinces; these releases had contributed to the 2. Documenting the response of native impact caused by the beetles. The absence plant and wetland communities; of G. pusilla in 2004, both at these 3. Developing integrated strategies to man- vanguard sites and at ‘redistributed’ release age L. salicaria. sites, suggests that sustainable populations of G. pusilla were no longer present at these dual-species release sites by 1996. The observations made in 2004 indicated Acknowledgements that populations of the biological control agents G. calmariensis and G. pusilla have Funding for the 2004 survey was provided been responsible for profound reductions in by the Ontario Ministry of Natural 366 Chapter 54

Resources. Beth Brownson and Christine how to collect, preserve and label the beetle Ali, Invasive Species Specialists with specimens so a voucher collection could be OMNR, provided continued support and established. We also acknowledge the encouragement for biological control of monitoring and/or provision of information purple loosestrife. Dr Steve Marshall and on Galerucella releases in Alberta by Bill Dr Matthias Buck of the University of Barr, Alec McClay, Jamie Motta, Chris Guelph Insect Collection loaned collecting Saunders and Jim Tansey. Andrea Brauner materials and provided valuable advice on constructed the distribution map, Fig. 54.1.

References

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55 Malva pusilla Smith, Round-leaved Mallow (Malvaceae)

Paul D. Hildebrand,1 Cheryl Konoff2 and Klaus I.N. Jensen1 1Agriculture and Agri-Food Canada, Kentville, Nova Scotia; 2Environment Canada, Dartmouth, Nova Scotia

55.1 Pest Status throughout the season, it has a deep taproot, indeterminate growth and pro- Round-leaved mallow, Malva pusilla Sm. duces numerous prostrate branches that also called M. rotundifolia L. (Malvaceae) can exceed 1 m in length. It is diffi cult to (Makowski and Morrison, 1989), is native control, except in early seedling stages, to Eurasia, occurs throughout Canada, and because of its tolerance to many common is especially a problem in western Canada herbicides once it is established (Makowski (Mortensen and Bailey, 2002). Roland and and Morrison, 1989). For greatest effi cacy, Smith (1969) described the weed as ‘rather herbicides must be applied at the 1–6 leaf rare in Nova Scotia’, but a weed survey stage. Applications at later growth stages conducted in 1994 by provincial weed may result in temporary knock down, but inspectors (L. Casey, 1994, Kentville, Nova normal growth resumes. Cultivation can Scotia, pers. comm.) found round-leaved kill M. pusilla if the taproot is severed mallow on almost half of the 350 farms below the crown. The weed can also be visited. There was concern at the time that problematic in turf since mowing or the weed should be regulated under the grazing will temporarily stunt the plant but provincial Weed Control Act. The increas- vigorous regrowth usually takes place ing prevalence of M. pusilla appeared to be below the severed stems. related to importation of contaminated feed Several insects feed on the foliage of grains from western Canada as it was round-leaved mallow in addition to several mainly associated with poultry and live- fungal pathogens that parasitize the leaves, stock production, and its occurrence in but only the host-specifi c pathogen Col leto- orchards, pastures and grain fi elds trichum gloeosporioides (Penzig) Penzig & appeared related to manure spreading. Saccardo f. sp. malvae (Glomerellaceae) has proven to have any signifi cant impact on the weed (Mortensen and Bailey, 2002). 55.2 Background

Mortensen and Bailey (2002) and Makowski 55.3 Biological Control Agents and Morrison (1989) have previously pro- vided comprehensive summaries of the Round-leaved mallow was the target of challenges faced when attempting to Canada’s fi rst registered bioherbicide, a control round-leaved mallow. It is an conidial preparation of C. gloeosporioides aggressive annual weed that germinates f. sp. malvae (hereafter referred to as

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 368 Chapter 55

Cg-malvae). The bioherbicide was not in apple orchards and later observations commercialized due to limited market size suggested that the pathogen persisted on (Cross and Polonenko, 1996; Mortensen, old test sites and occurred naturally 1996; Mortensen and Bailey, 2002; Bailey elsewhere (K.I.N. Jensen, 1999, Kentville, et al., 2010). The pathogen was originally Nova Scotia, unpublished observations). discovered and tested in Saskatchewan Subsequent epidemiological studies at where inundative inoculation with coni- orchard sites where the pathogen occurred dial sprays under favourable moisture and naturally indicated that disease initiation temperature regimes provided effective and intensity were related to density of control under both controlled environment round-leaved mallow stands (Konoff, and fi eld conditions (Mortensen, 1988; 2004). Disease began earlier in the season Makowski and Mortensen, 1989; Makow- and was more intense in stands with ski, 1993). After infection, Cg-malvae pro- higher weed density than in stands of duces necrotic lesions on stems, leaves and lower density. Consequently, seed pro- fl owers and lesions may coalesce and duction was signifi cantly lower in high girdle the stems. Gelatinous masses of density stands. This is not surprising since conidia are produced in acervuli within host density can be an important factor lesions and are disseminated by rain- infl uencing the epidemiology of a patho- splash or other physical means, resulting gen. High densities may alter humidity, in repeated cycles of secondary infection. leaf wetness duration and temperature to Colletotrichum gloeosporioides exists as favour infection and sporulation and the a number of host-specifi c form species that closer proximity among plants results in cause debilitating diseases on many increased effi ciency of spore transfer economically important hosts, including (Cousens and Croft, 2000). Dispersal of weed species. Some of these have been conidia of Colletotrichum spp. is generally studied as inundative biological control considered to be rain-splashed, but within agents, although few have been suc cess- a habitat such as an orchard row, transport fully commercialized (Auld and Morin, of gelatinous conidia could also occur by 1995; Mortensen and Bailey, 2002). Under many other physical means including favourable conditions, naturally occurring insects and other fauna, foot traffi c, epidemics can also provide signifi cant mowers and other equipment. Injury to control of some weed species (Butler, 1951; plant tissue by these agents may also Morrison et al., 1998). Throughout Nova reduce the need for optimum leaf wetness Scotia, for example, high levels of St John’s conditions for infection (Morrison et al., wort, Hypericum perforatum L. (Hyper- 1998). icaceae), control is achieved by the widely Colletotrichum gloeosporioides f. sp. occurring fungal species Colletotrichum malvae was able to persist in infected seed gloeosporioides (Penzig) Penzig & Saccardo and stem pieces under maritime con- f. sp. hyperici in non-tilled habitats such as ditions. The incidence of diseased seed- lowbush blueberry fi elds, pastures and lings arising from overwintered seed was roadsides (Hildebrand and Jensen, 1991; only about 1% of the total number of Morrison et al., 1998). In non-tilled habi- seedlings that emerged and when seedlings tats the infection cycle is not interrupted from disease-free seed emerged through a nor are sources of inoculum incorporated litter of diseased stem pieces, the incidence into the soil by cultivation. of infection reached about 3% (Konoff, 2004). This low incidence of carry-over is consistent with observations in the fi eld where lesions and conidia are typically 55.4 Evaluation of Biological Control fi rst observed on a few scattered seedlings in the cotyledon to 1- or 2-leaf stage in Field testing in the mid-1990s of conidial early spring. These diseased seedlings sprays of Cg-malvae gave excellent control evidently are the source of secondary of M. pusilla under Nova Scotia conditions inoculum that spreads to adjacent plants. Chapter 55 369

Interestingly, disease on round-leaved without augmentation (Mortensen, 1988). mallow at orchard sites appeared to be However, under generally cooler, moister delayed and reduced by fungicides applied maritime conditions, and in non-tilled for control of apple diseases, but disease on habitats where inoculum is not incorpor- the weed nevertheless progressed to high ated into the soil, natural epidemics of Cg- levels by the end of the season (Konoff, malvae occur annually and appear to be 2004). keeping the weed at tolerable levels. The A cursory survey in Nova Scotia found introduction of Cg-malvae in Nova Scotia Cg-malvae on 74% of 58 farms visited with was largely unintended but its spread and round-leaved mallow (Konoff, 2004). persistence further supports the potential Initially identifi ed as a rapidly spreading usefulness of Colletotrichum spp. as weed of concern, it was concluded that it ‘classical’ biological control agents (Morri- no longer required regulation under the son et al., 1998) that could be exploited in Weed Control Act because of the effective- suitable environments. ness and distribution of the pathogen in Nova Scotia. Although Cg-malvae occurs naturally in 55.5 Future Needs annual fi eld crops in western Canada, Future work should include: persistence through the winter is low (Makowski, 1987) and the pathogen does 1. Evaluation of Colletotrichum spp. as not provide effective nor timely control classical biological control agents.

References

Auld, B.A. and Morrin, L. (1995) Constraints in the development of bioherbicides. Weed Technology 9, 638–652. Bailey, K.L., Boyetchko, S.M. and Längle, T. (2010) Social and economic drivers shaping the future of biological control: a Canadian perspective on the factors affecting the development and use of microbial biopesticides. Biological Control 52, 221–229. Butler, F.C. (1951) Anthracnose and seedling blight of Bathurst burr caused by Colletotrichum xanthii Halst. Australasian Journal of Agricultural Science 2, 240–410. Cousens, R. and Croft, A.M. (2000) Weed populations and pathogens. Weed Research 40, 63–82. Cross, J.V. and Polonenko, D.R. (1996) An industry perspective on registration and commercialization of biocontrol agents in Canada. Canadian Journal of Plant Pathology 18, 446– 454. Hildebrand, P.D. and Jensen, K.I.N. (1991) Potential for the biological control of St. John’s wort (Hypericum perforatum) with an endemic strain of Colletotrichum gloeosporioides. Canadian Journal of Plant Pathology 13, 60–70. Konoff, C. (2004) Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. f. sp. malvae as a classical biological control agent for round-leaved mallow (Malva pusilla Sm.) in noncultivated habitats. MSc thesis, Dalhousie University, Halifax and the Nova Scotia Agricultural College, Truro, Canada. Makowski, R.M.D. (1987) The evaluation of Malva pusilla Sm. as a weed and its pathogen Colletotrichum gloeosporioides (Penz.) Sacc. f. sp. malvae as a bioherbicide. PhD thesis, University of Saskatchewan, Saskatoon, Canada. Makowski, R.M.D. (1993) Effect of inoculum concentration, temperature, dew point and plant growth stage on disease of round-leaved mallow and velvetleaf by Colletotrichum gloeosporioides f. sp. malvae. Phytopathology 83, 1229–1234. Makowski, R.M.D. and Morrison, I.N. (1989) The biology of Canadian weeds. 91. Malva pusilla Sm. (=M. rotundifolia). Canadian Journal of Plant Science 69, 861–879. 370 Chapter 56

Morrison, K.D., Reekie, E.G. and Jensen, K.I.N. (1998) Biocontrol of common St. John’s wort (Hypericum perforatum) with Chrysolina hyperici and a host-specifi c Colletotrichum gloeosporioides. Weed Science 12, 426-435. Mortensen, K. (1988) The potential of an endemic fungus, Colletotrichum gloeosporioides, for biological control of round-leaved mallow (Malva pusilla) and velvetleaf (Abutilon theophrasti). Weed Science 36, 473–478. Mortensen, K. (1996) Constraints in development and commercialization of a plant pathogen, Colletotrichum gloeosporioides f.sp. malvae in biological weed control. In: Proceedings of the 2nd International Weed Control Conference, Copenhagen, Denmark, pp. 1297–1300. Mortensen, K. and Bailey, K.L. (2002) Malva pusilla Smith, round-leaved mallow (Malvaceae). In: Mason, P.G. and Huber, J.T. (eds) Biological Control Programmes in Canada, 1981–2000. CAB International, Wallingford, UK, pp. 391–394. Roland, A.E. and Smith, E.C. (1969) The Flora of Nova Scotia. Nova Scotia Museum, Halifax, Canada.

56 Setaria viridis (L.) Beauvois, Green Foxtail (Poaceae)

Susan M. Boyetchko,1 Gary Peng,1 Russell K. Hynes1 and Paul Y. de la Bastide2 1Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 2Department of Biology, University of Victoria, Victoria, British Columbia

56.1 Pest Status environments and habitats. Green foxtail, S. viridis, is a cosmopolitan weed in Weeds belonging to the Setaria species temperate zones and at higher elevations of group in the Poaceae, including giant, the subtropics, and is considered the Setaria faberi Herrm., green, S. viridis (L.) weedy progenitor species that expanded P. Beauvois, yellow, S. pumilla (Poir.) into Eurasia and was fi nally introduced to Roem. & Schult., knotroot, S. geniculata P. the New World via human emigration Beauvois, and bristly foxtail, S. verticillata during the last fi ve centuries. Setaria (L.) P. Beauvois (Poaceae) (Defelice, 2002; viridis is therefore believed to be the main Dekker, 2003), are considered amongst the source of the weedy Setaria spp. world’s worst weeds. The Setaria group is established in North American agriculture believed to have originated from Africa, and its dominance and economic import- from where it spread into Eurasian ance to countries in North and South countries and adapted to a broader range of America, Australia and Asia can be

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 56 371 attributed to the close relationship between soil for 5–15 years, but has been known to humans, disturbance, agriculture and land survive for more than 30 years. Seed management (Douglas et al., 1985; Dekker, mortality decreases with increasing depth 2003). Interestingly, S. viridis is believed to in soil. Optimum germination occurs at have been domesticated as foxtail millet, soil depths of 1.5–2.5 cm (Douglas et al., Setaria italic (L.) P. Beauvois (Poaceae), in 1985; Thomas et al., 1986; Van Acker, ancient China during the 6th millennium 2009). Setaria viridis is a C4 photo- BC (Zohary and Hopf, 2000) and several synthetic plant species, i.e. warm season taxonomists now believe that foxtail millet grass, that emerges late in the spring in the should be classifi ed as a variety of green Canadian prairies at temperatures ranging foxtail and not a separate species. Setaria from 20 to 35°C (Blackshaw et al., 1981; viridis is currently a weed in 29 crops in 35 Holm et al., 1991; Dekker, 2003). However, countries around the world (Holm et al., soil moisture often plays a more important 1977; Douglas et al., 1985) and considered role in seed germination than soil tempera- a serious weed in countries such as Iran, ture. Spain and the USA and a principal weed in Canada, Japan and the former USSR. Setaria viridis is distributed in all 56.2 Background Canadian provinces but is most abundant in the prairies. Weed surveys conducted in Management of S. viridis often involves the western Canada have shown that S. viridis application of herbicides along with other is ranked as the most abundant weed cultural weed control tactics. Several species, occurring in over 50% of culti- synthetic herbicides belonging to Group 1 vated fi elds (Leeson et al., 2005). It has (acetyl-CoA carboxylase (ACCase)) and become established in numerous agri- Group 3 (dinitroanilines) herbicides are cultural crops (wheat, Triticum aestivum generally used to control S. viridis. L., barley, Hordeum vulgare L., maize, Zea However, S. viridis has demonstrated a mays L., sorghum, Sorghum bicolor (L.) high incidence of herbicide-resistant (HR) Moench (Poaceae), canola, Brassica napus biotypes in the prairie region of Canada L. (Brassicaceae), fl ax, Linum usitatissi- and is ranked amongst the top HR weeds mum L. (Linaceae), soybean, Glycine max (Beckie et al., 1999, 2008a). Resistance to (L.) Merr. (Fabaceae)), fallow fi elds, Group 1 (ACCase) herbicides occurs most pastures, roadside ditches, waste places, frequently, relative to other herbicide railroads, gardens, sidewalks and other groups, and results in a broad cross- disturbed areas (Holm et al., 1977, 1991; resistance to Group 3 herbicides (Beckie et Douglas et al., 1985; Leeson et al., 2005). al., 2008a). The incidence of resistance to Economic losses due to S. viridis arise more than one herbicide group, although from: (i) crop yield reductions due to weed less frequent than that of wild oat, competition; (ii) dockage, cleaning costs, Chasmanthium latifolium (Michx.) H.O. lower crop grade and quality associated Yates, or Avena fatua L. (Poaceae), popu- with seed contamination; and (iii) costs lations, was relatively high in Saska- associated with chemical and cultural tchewan and Manitoba (Beckie et al., 1999, control, all of which have been estimated 2008a). Cross resistance to Group 1 and 3 at over CAN$500m annually (O’Donovan et herbicides have been reported at much al., 2005; Leeson et al., 2006). lower incidence (Beckie and Morrison, Setaria viridis is a prolifi c seed producer 1993; Morrison and Devine, 1994; Beckie (Douglas et al., 1985) and the abundance of et al., 1999). the weed over the last few decades has The presence of HR biotypes of S. been attributed to its persistence in the viridis can increase the cost of weed seed bank and thus its invasive traits control for growers, requiring the use of (Buhler et al., 1997; Dekker, 1999; Van different herbicides and modifi ed rotation/ Acker, 2009). The weed seed can survive in crop management strategies, especially in 372 Chapter 56 the case of multiple HR biotypes; and the of insects and plant-pathogenic fungi, additional cost to growers in managing HR bacteria and viruses associated with S. S. viridis in Manitoba and Saskatchewan is viridis. In Saskatchewan, insects identifi ed estimated at over CAN$4m annually as being associated with the weed include (Beckie et al., 1999). From 2007 to 2009, Lygus borealis (Kelton), Stenodema vici- HR S. viridis infested 84.5% of over 2.5 num (Provancher) (Hemiptera: Miridae), million acres surveyed (H. Beckie, Saska- Hebecephalus occidentalis Beamer and toon, Saskatchewan, 2012, pers. comm.). Tuthill, H. rostratus Beamer and Tuthill, The higher incidence in these recent Helochara communis Fitch, Latalus surveys compared to those conducted 10 personatus Beirne (Hemiptera: Cicadel- years previously would suggest that the lidae) and various Chrysomelidae, cost for managing HR S. viridis has Melyridae (Coleoptera), Agromyzidae, increased. In a study to examine the Anthomy zidae, Chloropidae (Diptera) and association between farm management parasitic wasps (Hymneoptera: Chalci- practices and the occurrence of Group 1 doidea). Pathogenic fungi reported on HR weeds, Beckie et al. (2008b) deter- green foxtail include Fusarium equiseti mined that the risk of weed resistance was (Corda) Saccardo (Nectriaceae), Pyricularia greatest in fi elds with cereal-based grisea Sarccardo (Magnaporthaceae), rotations and in conservation tillage Pythium debaryanum Hesse, P. graminicola systems, but least in fi elds with forage Subramaniam (Pythiaceae) and Sclerospora crops, fallow, or where three or more crop graminicola Saccardo Schroeter (Perono- types were grown. Agricultural practices, sporaceae) (Conners, 1967). These fungi are especially weed control, should be re- also reported pathogens of various crops evaluated in terms of how they may affect including cereals and thus are unlikely the incidence of HR biotypes. Weed control candidates for biological control. strategies will benefi t from the develop- ment and use of an effective biological herbicide, as it will provide unique modes of action (Boyetchko and Peng, 2004). 56.3 Biological Control Agents Non-chemical control measures for S. viridis include crop rotation, crop com- 56.3.1 Bacteria petition and improved crop emergence and establishment (Blackshaw et al., 2007). An extensive screening programme was Selection of crops with life cycles that initiated to identify bacterial strains with differ from the target weed are used to weed-suppressive activity against S. viridis prevent weed establishment, which also (Boyetchko, 1997). Over 3000 bacterial can result in reductions of the weed seed strains and their metabolites with >80% bank. Weed suppression can be enhanced weed suppression using a Tier 1 agar by manipulation of crop competitiveness, bioassay method were evaluated (S. including the selection of crop cultivars Boyetchko, 2012, unpublished results). with greater competitive traits. Com- This was followed by a Tier 2 growth petition from weeds has also been manipu- pouch bioassay using whole bacterial lated through early seeding and uniform cultures. Small-plot fi eld effi cacy trials to crop establishment and by increasing the evaluate strains and dose response resulted crop stand by decreasing row spacing and in the selection of fi ve leading bacterial thus increasing crop density. Delayed crop candidates, which also controlled both seeding may be used to avoid a fl ush of susceptible and HR S. viridis populations: weeds early in the growing season, but this Group 1 (ACCase inhibitor) and Group 3 practice is often not utilized because (trifl uralin resistant) (S. Boyetchko, 2012, emergence patterns vary amongst weed unpublished results). These bacteria species. achieved over 70–80% reduction in weed Douglas et al. (1985) reported a number emergence and biomass in the fi eld at Chapter 56 373 multiple geographical locations (Daigle et rostratum were initially investigated as al., 2002) with broad-spectrum activities part of a multiple pathogen strategy to against other grass weed species (wild oat, control several grass weeds in Florida C. latifolium, crabgrass, Digitaria spp., (Chandramohan and Charudattan, 2001). annual ryegrass, Lolium multifl orum Lam., The results indicated their potential for use barnyard grass, Echinochloa crus-galli (L.) in Florida and that they had restricted host P. Beauvois, yellow foxtail, S. pumilla range with no risk to non-target crops, (Poaceae)) without harming cereal crops. including cereals. Research conducted in As a result, US and Canadian patents were Canada revealed that D. gigantea and E. issued for use of these bacteria as pre- rostratum were also very effective at emergent bioherbicides against S. viridis controlling S. viridis; the application of (Boyetchko et al., 2005, 2006). Chemical these fungi formulated in a humectant analyses of extracts from bacterial resulted in 100% weed mortality in less metabolites (strains BRG100 and 189) than 7 days (Boyetchko et al., 2003). indicated that these bacteria produce Pyricularia setariae is indigenous to different UV-active metabolites (Quail et Canada and showed high host specifi city, al., 2002; Pedras et al., 2003). HPLC and with little negative impact on 28 plant NMR spectroscopy showed that the active species tested, including many fi eld crop products are a complex mixture of cyclic species such as wheat, barley and oat, peptides and x-ray crystallography allowed Avena sativa L. (Poaceae). Infection by this the determination of the chemical structure fungus is more rapid at a temperature of two antifungal peptides from BRG100 around 26°C, and weed control is more named pseudophomin A and pseudo- effective when the fungus is applied at a phomin B. These are complex cyclic high inoculum concentration (>107 spores peptides with nine amino acid residues ml−1) and at younger plant growth stages and lipophilic portion; the most active (1–4 leaf stage) (Peng et al., 2004). Under components are water-soluble peptides. controlled-environment conditions, the Additional fermentation and formulation effi cacy was comparable to the herbicide research led to proof-of-concept that sethoxydim but was much more effective Pseudomonas fl uorescens (Flügge) Migula on HR populations, resulting in 80% weed (Pseudomonadaceae) BRG100 strain had control as opposed to 17% by the herbicide high potential for commercialization. This alone (Peng et al., 2004). Further studies resulted in the selection of an industry indicated that conidia of both P. setariae partner, MycoLogic (Victoria, British and D. gigantea germinated well at Columbia), to register this bacterial strain temperatures above 15°C, but 23–25°C were as a pre-emergent bioherbicide for grass optimum temperatures for appressorial weed control. Additional research is formation and maximum infection occurred required to generate data for registration at 25°C for P. setariae and 32°C for D. with Health Canada. gigantea (Peng and Boyetchko, 2006). Viability of both fungi decreased when 4-h leaf wetness was followed by a 20-h dry 56.3.2 Fungi period or after an 8-h delay in leaf wetness following inoculation (Green et al., 2004). The fungal pathogens Pyricularia setariae A thermogradient plate was used to Nisikado (Magnaporthaceae), Drechslera evaluate these fungal pathogens under gigantea S. Ito and Exserohilum rostratum fl uctuating daily temperature regimes to (Drechsler) Leonard and Suggs (Pleo- determine their bioherbicidal properties on sporaceae) have been studied as candidates S. viridis under cooler and more variable for biological control of S. viridis Canadian prairie temperature conditions. (Boyetchko et al., 2003; Green et al., 2004; This unique method permitted the investi- Peng et al., 2004; Peng and Boyetchko, gation of ‘habitat-matching’ studies in order 2006). The fungi D. gigantea and E. to establish the utility of these fungal agents 374 Chapter 56 in different environments and geographical A granular formulation based on an oat locations. Drechslera gigantea appeared fl our matrix (called ‘pesta’) was developed more promising in terms of virulence on to deliver P. fl uorescens BRG100 to the soil green foxtail under lower dew-temperature (Daigle et al., 2002) and modifi cations to conditions (Peng and Boyetchko, 2006). the formulation to promote disintegration Extensive host-range tests of D. gigantea and dispersion of the bioherbicide were were subsequently conducted on a variety reported (Hynes and Boyetchko, 2011). of crops (over 30 crops with at least two Low water activity (aw) of 0.1–0.3 contrib- cultivars from each crop) to determine non- uted to extension of the shelf life for 16 target effects (S. Boyetchko and G. Peng, months by promoting the survival of a 2012, unpublished results). Slight patho- stable population of P. fl uorescens at about −1 genicity on some cereal cultivars that was 9 log10 cfu g while reducing microbial not previously revealed during an initial contaminants (Hynes and Boyetchko, study in Florida (Chandramohan and 2011). The addition of starch, particularly Charudattan, 2001) raised serious questions pea, Pisum sativum L. (Fabaceae), starch, about the safety of using this bioherbicide promoted faster disintegration of the agent in Canada. Additional studies on the granules. The ability to produce granular susceptibility of cereal cultivars at different formulations with different release rates of growth stages confi rmed this issue; appli- the biological control agent provides cations at the 3–5 leaf stage (common spray additional control for the end user when timing for weed control in western Canada) managing crop pests such as S. viridis. will cause damage on certain cereal cultivars commonly grown in Canada. The research therefore clearly demonstrates that 61.4.2 Fungi this fungus has no utility as a bioherbicide in the Canadian prairies. US and Canadian As a domestic organism, P. setariae was patents were issued for the use of P. studied extensively for potential utility as a setariae, for control of foxtail weeds (Peng biological control agent of S. viridis. One of and Byer, 2008, 2010). the defi ciencies for biological control of S. viridis is poor effi cacy on emerging young leaves. The meristem of many grasses is 56.4 Evaluation of Biological Control protected by a leaf sheath (Greaves and MacQueen, 1992) and younger tissues 56.4.1 Bacteria appeared more tolerant to the infection by Pyricularia pathogens (Moss and Treva- The green fl uorescent protein gene was than, 1987). Additionally, the top S. viridis introduced into P. fl uorescens BRG100 to leaf is vertically positioned, which makes permit the visualization and monitoring of it a poor target for retaining spray droplets root colonization and environmental fate (Wolf and Caldwell, 2004). As a result, S. when introduced into soils under various viridis treated with P. setariae alone often environmental conditions (Hanson, 2008; recovered from initial injuries, unless Caldwell et al., 2012). BRG100 bacteria are extremely high fungal doses were applied released from the granular formulation and in high carrier volumes (Peng et al., 2005). establish colonies on the S. viridis root, Several herbicides at reduced rates were proving that the granular formulation synergistic with P. setariae, boosting the disperses the bacteria to the target weed. fungal virulence substantially by targeting However, soil moisture and temperature young grass leaves or the growing point have an impact on the dispersal properties (Peng and Byer, 2005). For example, of the formulation; therefore, improved sethoxydim inhibits cell division and is dispersion through formulation amend- particularly toxic to actively growing ments were required to improve bio- young grass tissues (Jain and Vanden Born, herbicidal activity (Hanson, 2008). 1989). Greenhouse trials showed that Chapter 56 375

sethoxydim at 0.1× label rate killed S. improve spray retention on S. viridis and viridis completely when synergized with a several products increased the retention by low dose of P. setariae. In the fi eld, 58–185% relative to water suspensions however, sethoxydim at 0.25× the label rate (Peng and Wolf, 2008). Although mecha- was required for a noticeable impact on S. nisms for increasing the retention were not viridis and for suffi cient weed control determined, these adjuvants would possibly when tank-mixed with P. setariae (Peng have an impact on spray quality, which in and Wolf, 2008). Pyricularia setariae turn might affect retention effi ciency on S. caused only slight infection on S. faberi viridis (Peng et al., 2005). Most of the and S. glauca, but when applied with adjuvants that showed substantial sethoxydim at 0.25× label rate, it killed S. improvement on spray retention appeared faberi completely while injuring S. glauca compatible with P. setariae conidia (Peng only slightly (Peng and Wolf, 2011). This and Wolf, 2008). This indicated that these demonstrates that synergy can not only products would be suitable for tank mixing enhance the virulence of P. setariae on S. with the fungus for control of S. viridis. viridis, but also help expand the target of this biological control agent to S. faberi. A water/oil/water (W/O/W) emulsion 56.5 Future Needs formulation was developed to deliver spores of P. setariae to the foliage of S. Future work should include: viridis effi ciently. W/O/W formulated P. setariae spores were as effi cacious on S. 1. Development of strain-specifi c DNA viridis as non-formulated P. setariae, indi- markers to assist with studies of environ- cating that none of the formulation com- mental fate, quality control monitoring and ponents interfered with bioherbicide the evaluation of biosafety of bacterial activity (Hynes et al., 2005). products; Extensive studies were conducted to 2. Optimization of fermentation and for- improve spray retention effi ciency for P. mulation technologies for scale-up produc- setariae. Although impractical, the initial tion and manufacturing of bacterial study using air-brush spraying until runoff bioherbicides; likely maximized retention volumes on 3. Completion of multi-site fi eld trials plants (Peng et al., 2005). Reducing droplet examining effi cacy of the improved bac- size from 325 +m (VMD) to 207 +m by terial formulation at different rates; simply changing spray nozzles enhanced 4. Preparation and submission of appli- the retention by approximately 40% on S. cations for product registration to the Pest viridis when the application volume was Management Regulatory Agency of leading kept the same (Byer et al., 2006). This bacterial candidates; potentially represents 40% saving on the 5. Development of formulations for foliar biological control agent inoculum. A large application of P. setariae that promote number of adjuvants were evaluated to activity and extend shelf life.

References

Beckie, H.J. and Morrison, I.N. (1993) Effective kill of trifularin-susceptive and -resistant green foxtail (Setaria viridis). Weed Technology 7, 15–22. Beckie, H.J., Thomas, A.G. and Légère, A. (1999) Nature, occurrence, and cost of herbicide-resistant green foxtail (Setaria viridis) across Saskatchewan ecoregions. Weed Technology 13, 626–631. Beckie, H.J., Leeson, J.Y., Thomas, A.G., Brenzil, C.A., Hall, L.M., Holzgang, G., Lozinski, C. and Shirriff, S. (2008a) Weed resistance monitoring in the Canadian Prairies. Weed Technology 22, 530–543. Beckie, H.J., Leeson, J.Y., Thomas, A.G., Hall, L.M. and Brenzil, C.A. (2008b) Risk assessment of weed resistance in the Canadian Prairies. Weed Technology 22, 741–746. 376 Chapter 56

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57 Tanacetum vulgare L., Common Tansy (Asteraceae)

Alec S. McClay1 and André Gassmann2 1McClay Ecoscience, Sherwood Park, Alberta; 2CABI, Delémont, Switzerland

57.1 Pest Status rats, rabbits and humans, blocks pain sensation in mice, and stimulates por- Tanacetum vulgare L. (Asteraceae) is a phyrin production in chick embryo liver vigorous, strongly aromatic perennial, cells. It acts by blocking receptor sites for native to Europe. It was introduced into the neurotransmitter GABA (Scientifi c North America as a medicinal and culinary Committee on Food, 2003). Tanacetum herb, and escaped from cultivation over vulgare plants vary in their production of 200 years ago (Mitich, 1992). It forms large _-thujone: in a survey in Alberta the clumps that spread out gradually by proportion of plants producing _-thujone growth of the root crown, and also spreads in samples from various municipalities by prolifi c seed production. It is now ranged from 0 to 50% (McClay et al., 2002). widely naturalized across Canada and the Tanacetum vulgare reduces the pro- northern USA, and is typically found in ductivity of pastures, displaces native uncultivated areas such as roadsides, vegetation in natural areas and can hinder fencelines, pastures, riparian zones, forest forest regeneration in logged areas. margins and parks, but is also spreading in Tanacetum vulgare is listed as a noxious forested areas, such as along the Athabasca weed under provincial weed control River in northern Alberta (Alberta Sustain- legislation in Alberta, Saskatchewan and able Resource Development, 2005). Tana- Manitoba, and in the Bulkley-Nechako, cetum vulgare contains a number of Central Kootenay, Columbia-Shuswap, East pharmacologically active secondary com- Kootenay and North Okanagan regions of pounds, some of which are quite toxic to British Columbia, as well as under various humans and livestock. In traditional regulatory categories in the US states of medicine, T. vulgare is used to control Colorado, Minnesota, Montana, North and nervousness, eliminate intestinal worms, South Dakota, Washington and Wyoming. stimulate menstruation and induce abortions. There have been human deaths from overdoses of T. vulgare extracts or 57.2 Background teas (Mitich, 1992; Olasky, 1992; Lahlou et al., 2008). There are also anecdotal reports An extensive study of Tanacetum and of abortions induced in cattle by grazing on related species of the tribe Anthemideae T. vulgare (Keindorf and Keindorf, 1978). (Sonboli et al., 2012), using nuclear and The major toxic constituent is _-thujone, chloroplast DNA data, found that sequence which causes convulsions and seizures in divergence within the genus was low, and

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 57 379 many phylogenetic relationships within vulgare populations exhibited high chemo- the genus could not be resolved. However, type variation, with nine chemotypes the separation of Tanacetum from other occurring on both continents. However, members of the subtribe Anthemidinae, plants of invasive origin had higher such as Anthemis, Archanthemis, Cota, terpene and volatile compound concen- Nananthea and Tripleurospermum was trations than their native counterparts. confi rmed, while the south-west European Wolf et al. (2012a) also found an indication Tanacetum microphyllum DC (Asteraceae) for higher genetic diversity in plants of the was found to be phylogenetically distant introduced population compared to popu- from the rest of the genus and was placed lations in the native range. Analyses of in a new genus Vogtia. volatile profi les of the same plant indi- Tanacetum vulgare has relatively few viduals indicated similarly high chemical close relatives in the native North Ameri- diversities in native and introduced can fl ora. Congeneric native North Ameri- populations, with a considerable amount of can species have been described under the unique geno- and chemotypes on both names T. huronense Nutt., T. camphoratum continents. No signifi cant relation between Less. and T. douglasii DC, but these are all the genetic and chemical data could be considered in the Flora of North America detected. In brief, the high intraspecifi c treatment as Tanacetum bipinnatum (L.) fi ne-scaled mosaic of variation in genetic Sch.Bip. (Asteraceae) (Watson, 2006). In composition and quantitative and qualita- the USA, native Tanacetum spp. are state tive composition of terpenes may facilitate listed under the name T. huronense as the invasion process of T. vulgare. ‘threatened’ in Michigan and ‘endangered’ In a survey of arthropod populations in in Wisconsin, and under the name T. north-central Alberta between 1993 and bipinnatum as ‘special concern’ in Maine. 1995, White (1997) found few polyphagous These populations are on the southern insects feeding on T. vulgare, with none edge of the North American range of T. abundant enough to infl ict serious damage. bipinnatum, which is widespread across Macrosiphoniella tanacetaria (Kaltenbach) Canada and considered ‘secure’ (Canadian (Hemiptera: Aphididae) is common in Endangered Species Conservation Council, Alberta, and cercopids, thrips and other 2011). The native North American aphids were observed feeding on the plant. Tanacetum spp. are important non-target Eupithecia satyrata dodata Taylor and species for host-specifi city testing, but their Synchlora albolineata Packard (Lepi- taxonomy and relationships to T. vulgare doptera: Geometridae) feed on the fl owers, are still unclear. According to Oberprieler and the monophagous Aceria calathinus (2004), T. huronense is sister to T. vulgare, (Nalepa) (Trombidiformes: Eriophyidae) while Sonboli et al. (2012) place the closest was collected from the terminal buds. A relatives of T. bipinnatum as the Russian rust, Puccinia tanaceti DC (Pucciniaceae), species T. millefolium (L.) Tzvel. and T. and a powdery mildew, Erysiphe cichora- sclerophyllum H. Krasch. Genetic analysis cearum DC (Erysiphaceae), were found on using AFLPs suggests that T. bipinnatum foliage late in the season (White, 1997; ssp. huronense, T. camphoratum and T. Newcombe, 2003). douglasii form a closely related group that Following an initial survey in 1996 is sister to T. vulgare; however, further (Freise and Schroeder, 1997), European sampling is needed to resolve possible exploration for potential biological control species-level differences within this group agents began in 2006. From 166 herbivore (J. Gaskin, Sidney, Montana, 2011, pers. species recorded in the literature, 29 comm.). species are restricted to the genus Tana- In a study including 13 native European cetum and about ten were thought to be and nine introduced North American potentially host specifi c (Gassmann et al., populations of T. vulgare, Wolf et al. (2011) 2007). Candidate insects subsequently showed that both native and invasive T. studied include the leaf-feeding beetle 380 Chapter 57

Cassida stigmatica Suffrian (Coleoptera: be detected when reared on the different Chrysomelidae), the shoot-boring longhorn chemotypes. beetle Phytoecia nigricornis (Fabricius) Phytoecia nigricornis is a univoltine (Coleoptera: Cerambycidae), the shoot- shoot-boring cerambycid, which over- boring weevil Microplontus millefolii winters in the adult stage in a pupal cell in (Schultze) (Coleoptera: Curculionidae), the the shoot base of its host. Preliminary host- root-boring fl ea-beetle Longitarsus sp. near range studies have shown that this species noricus Leonardi (Coleoptera: Chrys- is likely not host specifi c. omelidae) and the fl ower-feeding moth Microplontus millefolii is a univoltine Isophrictis striatella (Denis & Schiffer- shoot miner, which overwinters in the müller) (Lepidoptera: Gelechiidae). Fungi adult stage. According to Dieckmann have not yet been surveyed in Europe. (1972), M. millefolii is monophagous on T. vulgare and occurs in the central and southern parts of northern Europe. Ovi- 57.3 Biological Control Agents position usually occurred at the uppermost leaf node and the larvae mine down into Cassida stigmatica occurs widely in the shoot. The number of M. millefolii Europe, and material from Germany, Russia larvae recorded in the shoots of T. vulgare and Ukraine has been used in host- after exposure in a fi eld cage for 3 weeks specifi city tests. The beetle overwinters as ranged from one to seven, with a mean of an adult. Newly emerged adults do not 2.3 larvae per attacked shoot. Preliminary reproduce until late winter or early spring host-range studies using material from of the following year. A small percentage of Russia and Ukraine indicate a narrow host each C. stigmatica generation may survive range for M. millefolii. The native North more than 2 years in rearing conditions American T. camphoratum supports pro- and these beetles can remain active during longed adult longevity and is accepted in the third year. Eggs are laid singly, or in no-choice tests and in single-choice tests pairs, on the lower leaf surface and larvae with T. vulgare, but is a less suitable host develop within 1 month at room tempera- than T. vulgare for larval development. ture. Neonate larvae of C. stigmatica Tanacetum camphoratum was not attacked develop successfully to the adult stage on in a multiple-choice open fi eld test in the native North American T. bipinnatum Russia with T. vulgare and Achillea alpina species complex as well as on other species L. (Asteraceae), although the attack rate such T. balsamita L., T. parthenium (L.) was low on the control T. vulgare plant. Sch. Bip., Chamaemelum nobile (L.) All. A root-feeding fl ea beetle tentatively and a North American population of named Longitarsus sp. near noricus Achillea millefolium L. (Asteraceae). In a Leonardi has been collected from T. preliminary multiple-choice fi eld cage test, vulgare near St Petersburg, Russia, and some oviposition was recorded on all Kiev, Ukraine. Longitarsus noricus is tested species that were suitable for larval reported mostly from central Europe development. Cassida stigmatica reared on (Leonardi, 1976); its biology is unknown T. huronense had a similar fecundity to but it is closely related to L. succineus those reared on T. vulgare. In a study on (Foudras), which has been associated with the ability of C. stigmatica to select for various species in the Asteraceae (Freude certain chemotypes of T. vulgare, Wolf et et al., 1966). Sequencing of mtDNA COI al. (2012b) found that overall, C. stigmatica suggests that the species collected from T. females showed a clear preference for the vulgare is distinct from both L. noricus and pure `-thujone chemotype over the mixed L. succineus, both of which also emerged chemotypes containing camphor, but were as contaminants from experimental larval able to use all offered chemotypes for transfer tests. From larval transfer tests oviposition and feeding. No differences in carried out in 2010 with L. sp. near noricus larval survival and adult body mass could from Russia, adults emerged in 2011 from Chapter 57 381

T. vulgare, T. balsamita, T. macrophyllum 57.5 Future Needs (Waldst. & Kit.) Sch. Bip. (Asteraceae), T. parthenium, C. nobile and the native North Future work should include: American Achillea alpina. The identity of 1. Completion of host specifi city testing emerging adults was confi rmed by COI with M. millefolii and I. striatella; sequencing. This species appears to be 2. Open-fi eld multiple choice tests to oligophagous on Anthemideae, and thus assess the fi eld host-specifi city of C. stig- not specifi c enough for use as a biological matica; control agent. A phylogenetic study is 3. Evaluation of other potential candidate needed to clarify the taxonomic position of agents: the root-feeding beetle Meliboeus these morphologically closely related graminoides Abeille (Coleoptera: Bupresti- small, bright-brown fl ea beetles of the L. dae), the shoot/root-boring moth Platyptilia noricus-succineus species complex. ochrodactyla (Denis & Schiffermüller) Early larval instars of I. striatella feed (Lepidoptera: Pterophoridae), the plant bug and develop within the receptacle of the Oncotylus punctipes Reuter (Hemiptera: fl ower head. Later instars usually leave the Miridae) and the leaf/shoot-galling midge fl ower heads during winter and move into Rhopalomyia tanaceticola (Karsch) the lower part of dry stems for over- (Diptera: Cecidomyiidae). wintering. However, the larvae can also spend their whole life cycle in the dry fl ower heads before emerging the fol- lowing summer. Isophrictis striatella can Acknowledgements very occasionally have a partial 2-year life cycle. Larvae are extremely mobile and, as We gratefully acknowledge the fi nancial described by Freise (1997) for a Northern support in the USA of the Minnesota German population of the species, it is Department of Agriculture, the Montana possible that completion of larval feeding Noxious Weed Trust Fund through in spring may occur in the newly growing Montana State University, and UPM shoots, or in the roots. Oviposition and Blandin Paper Mill, and in Canada of the larval development occurred only on Agriculture and Food Council of Alberta T. vulgare in no-choice oviposition tests (Advancing Canadian Agriculture and with six plant species in the tribe Agri-Food and Canadian Agricultural Anthemideae. Adaptation Program), the Alberta Beef Producers, Alberta Sustainable Resource Development, the British Columbia 57.4 Evaluation of Biological Control Ministry of Forests, Lands and Natural Resource Operations, Canadian Pacifi c, When the project started in 2006, priority Cenovus FCCL Ltd, Enbridge Pipelines was given to beetles and internal feeders, Inc., Marksmen Vegetation Management since these two groups of biological control Inc., Saskatchewan Agriculture and Food agents have proven to be the most effi cient (Agriculture Development Fund), Saddle in the biological control of temperate Hills County (Alberta), Suncor Energy Inc. weeds (Gassmann, 1995; Syrett et al., and TransCanada. We also thank Ivo 1996). Although most potential biological Toševski for the DNA analysis of control agents studied have not yet been Longitarsus; Dr John Gaskin for DNA tested in choice conditions, a number of studies on Tanacetum spp.; Prof. Caroline them might not have the level of specifi city Müller and the University of Bielefeld for required for release into North America. supervising and supporting the PhD Results to date suggest that the most research by Vera Wolf; Dr Margarita promising agents from a host specifi city Dolgovskaya and Dr Sergey Reznik viewpoint studied so far are M. millefolii (Russian Academy of Sciences, St Peters- and I. striatella. burg) for facilitating and accompanying the 382 Chapter 57

fi eld trips to northern Russia; Prof. Sergei the fi eld trips in Ukraine; and Dr Wojciech L. Mosyakin and Andrew Mosyakin (M.G. Paul (W. Szafer Institute of Botany, Polish Kholodny Institute of Botany, Kiev, Academy of Sciences, Krakow) for Ukraine) for facilitating and accompanying facilitating work in Poland.

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58 Taraxacum offi cinale F.H. Wigg, Dandelion (Asteraceae)

Alan K. Watson1 and Karen L. Bailey2 1McGill University, Ste Anne de Bellevue, Québec; 2Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan

58.1 Pest Status uniformity and density, reduces crop yields, causes slower drying of hay, is an Dandelion, Taraxacum offi cinale F.H. Wigg alternative host for several insect pests and (Asteraceae), is a herbaceous perennial diseases and its pollen is allergenic plant. Common dandelion is native to (Stewart-Wade et al., 2002b). Although T. Eurasia, and now is naturalized throughout offi cinale is considered a major weed temperate regions of North America, species, especially in turfgrass environ- southern Africa, South America, New ments, it has historically been used as a Zealand, Australia and India. It occurs in medicinal herb and as food. Taraxacum all Canadian provinces and all 50 states of offi cinale is commonly used as a salad the USA. It can be found growing in green and is being promoted in organic lawns, parks, gardens, pastures, hayfi elds, markets. orchards, roadsides, vegetable gardens, Leaves of T. offi cinale are highly fi eld crops, reduced tillage fi elds and horti- variable (Holm et al., 1997). The plants are cultural crops (Holm et al., 1997; Stewart- sessile, and give rise to several fl ower Wade et al., 2002a). Taraxacum offi cinale shoots. Each fl ower produces up to 250 is an aesthetic problem during fl owering seeds. When released, the seeds can be and seed production. It interrupts turfgrass spread by the wind up to several hundred

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 384 Chapter 58 metres from their source and the seeds are competitive of six turf species, perennial also a common contaminant in crop and ryegrass, Lolium perenne L. (Poaceae), was forage seeds. The plants are adaptable to the most competitive and increased most soils and the seeds do not require a amounts of nitrogen fertilizer suppressed T. cold treatment before they will germinate. offi cinale in all turfgrass swards (Tripp, Taraxacum offi cinale is unaffected by day 1997). Grass competition under frequent length and can fl ower at any time of the close mowing did not prevent T. offi cinale year. from surviving and spreading (Timmons, Taraxacum offi cinale are simple per- 1950). ennials. They spread by seed and have no natural means of spreading vegetatively, but can readily regenerate from small por- 58.3 Biological Control Agents tions of their fl eshy taproots. In perennial plants, basal rosettes of leaves are pro- 58.3.1 Insects duced each year above those of the previous season, but the root undergoes a There has been limited effort in biological periodic longitudinal contraction up to control of T. offi cinale with insects. The 30% of its length, ensuring the leaf rosette fi rst occurrence of the European dandelion remains at ground level, a feature that leaf-gall midge, Cystiphora taraxaci Kieffer enables T. offi cinale to suppress other (Diptera: Cecidomyiidae), in north-central plants in short turf. Saskatchewan was recorded by Peschken et al. (1993). This midge induces purple-red pustule galls on the upper surfaces of 58.2 Background leaves. In the USA, Glocianus punctiger (Sahlberg) (=Ceutorhynchus punctiger Repeated applications of herbicides such Gyllenhall) (Coleoptera: Curculionidae) as 2,4-D (2,4-dichlorophenoxy acetic attacks T. offi cinale infl orescence buds, acid), mecoprop ((9/)-2-(4-chloro-2-methyl- seeds and leaves (McAvoy et al., 1983). phenoxy) propanoic acid), dicamba (3,6-dichloro-2-methoxybenzoic acid), or combination products have been widely 58.3.2 Fungi used for T. offi cinale control (Anonymous, 2005). Environmental and public health Numerous fungi occur on T. offi cinale in concerns about pesticides, especially the Canada and several have been evaluated as use of chemical herbicides in turfgrass for potential bioherbicides. Sclerotinia sclero- aesthetics, have led to bans or severe tiorum (Lib.) de Bary and S. minor Jagger restrictions on the use of pesticides in (Sclerotiniaceae) have been investigated as many regions of Canada. Consequently, possible biological control agents for T. alternatives to chemical herbicides are offi cinale (Ciotola et al., 1991; Riddle et al., being sought (Brière et al., 1992; Neumann 1991; Brière et al., 1992; Stewart-Wade et Brebaum and Boland, 2002; Stewart-Wade al., 2002b; Abu-Dieyeh and Watson, 2005, et al., 2002b; Zhou et al., 2004). Mech- 2006). Several Phoma species, including P. anical removal of T. offi cinale plants has taraxaci Hofsten, P. exigua Desm., P. limited success, due to the regenerative herbarum Westend. and P. macrostoma var. capacity of the long taproot. Integrated pest macrostoma Montagne (incerti sedis), have management strategies for T. offi cinale in also been considered as potential biological turf include the selection of competitive control agents for T. offi cinale (Neumann turfgrass species, application of increased Brebaum and Boland, 1999; Graupner et al., quantities of fertilizers, and mechanical 2003). Signifi cant progress in the biological control by mowing or removal. Studies in control of T. offi cinale has been obtained Ontario showed that Kentucky bluegrass, with two fungal isolates, S. minor IMI Poa pratensis L. (Poaceae), was the least 344141 and P. macrostoma isolate 94-44B. Chapter 58 385

Sclerotinia minor IMI 344141 is an normal lawn maintenance operations such asporogenic plant pathogen that has as mowing, fertilization and irrigation. biological control activity on T. offi cinale The IMI 344141 isolate was obtained and other broadleaf weeds without damage from a lettuce, Lactuca sativa L. to turfgrass species (Ciotola et al., 1991; (Asteraceae), fi eld in Sherrington, Quebec Riddle et al., 1991; Brière et al., 1992; but the life cycle, mode of action, moisture Stewart-Wade et al., 2002b; Abu-Dieyeh and temperature requirements and host and Watson, 2005). Earlier work with S. range of S. minor IMI 344141 were not minor IMI 344141 (under the code Mac1) different from S. minor ‘sensu lato’ resulted in the discovery and screening of (Watson, 2007). However, persistence, sur- numerous fungi, to the fi eld evaluation and vival and dissemination are very different formulation of a single candidate bio- when S. minor IMI 344141 is employed as herbicide isolate (Stewart-Wade et al., an integrated biological control product. 2002b). Several factors led to the dis- Isolate IMI 344141 can be phenotypically continuation of the project including distinguished from the other tested S. changes in research priorities and direction minor (Shaheen et al., 2010) and a strain- of industrial sponsors, uncertain market specifi c molecular marker was developed size, poor performance during warm and to detect and monitor the S. minor IMI dry periods, intermittent sclerotia 344141 bioherbicide strain (Pan et al., production, need for refrigeration storage 2010). When applied as a bioherbicide, S. and costs of scale-up production (Stewart- minor (IMI 344141) did not persist into the Wade et al., 2002b). following spring season in turf environ- Prospects for a biological control market ments. This molecular detection method improved in 2001, when the Supreme provides a mechanism to distinguish this Court of Canada endorsed the right of isolate from related organisms and a tool to municipalities to regulate pesticides in the selectively monitor behaviour of the bio- interest of a community’s health and logical control agent in the environment. welfare, leading to bans of products like When applied to turfgrass, S. minor IMI 2,4-D. The survival of the herbicide-intense 344141 rarely produces sclerotia (melan- lawn care industry was threatened. ized survival structures) and these sclerotia In 2004, Sarritor Inc. (4260864 Canada do not survive over winter (Stewart-Wade Inc.) was incorporated as a spin-off com- et al., 2002b; Pan et al., 2010). Mycelia of pany from McGill University and included S. minor IMI 344141 that emerge from a consortium of Lawn Care Operators bioherbicide granules do not survive (LCOs) as partners. Sarritor Inc. was beyond 10 days in the turfgrass granted an exclusive licence to com- environment. Field and greenhouse studies mercialize S. minor IMI 344141. McGill confi rmed that turfgrass species are not researchers and Sylvan BioProducts engin- susceptible to S. minor IMI 344141. eers overcame technical problems and Independent toxicological studies have achieved a cost-effective production of the established that S. minor IMI 344141 is Sarritor bioherbicide (Teshler et al., 2007). neither toxic nor pathogenic to humans, The fungus is cultured on ground barley birds, fi sh, daphnia, Daphnia spp. and the bioherbicide granules are (Cladocera: Daphniidae), honey bees, Apis broadcast-applied to weed-infested turf. mellifera L. (Hymenoptera: Apidae), earth- Favourable conditions for germination and worms (Megadrilaceae), or other animals. infection include 15–24°C temperatures The effect of S. minor IMI 344141 on T. and 95+% relative humidity. Disease offi cinale survival was evaluated under develops quickly and complete kill of T. different mowing heights and compared offi cinale and other broadleaf weeds can be with the commonly used herbicide achieved within 7 days, about twice as fast KillexTM (Abu-Dieyeh and Watson, 2005, as the standard chemical herbicide 2006). In the greenhouse, the onset of KillexTM. The product is compatible with symptoms was more rapid, foliar damage 386 Chapter 58 was more severe, and the reduction of competition (Abu-Dieyeh and Watson, aboveground biomass and root biomass 2007a). The grass sward provides a was greater for the bioherbicide than the microenvironment favouring the success of herbicide. The bioherbicide reduced root S. minor as a biological control agent of T. biomass ≥10-fold compared with untreated offi cinale. Thus, appropriate management plants (Abu-Dieyeh and Watson, 2005). of the turfgrass environment will be Under high weed infestation levels in complementary to the effi cacy of S. minor. the fi eld, S. minor IMI 344141 provided In a 3-year fi eld study, spring or early greater initial reduction of T. offi cinale autumn treatments with S. minor IMI density than did the herbicide during the 344141 were equally effective in sup- fi rst 2 weeks post-application period, pressing T. offi cinale as the herbicide although reductions were greater in treatment, 2 weeks after application (Abu- herbicide-treated plots by 6 weeks after Dieyeh and Watson, 2007c). By the second application (Abu-Dieyeh and Watson, year, weed control from two applications 2006). Over the growing season, S. minor per year of S. minor IMI 344141 was IMI 344141 and the herbicide had similar equivalent to the herbicide. In the third suppressive effects on T. offi cinale density year, weed control from one spring appli- except under the closest mowing height cation of S. minor IMI 344141 was (3–5 cm). Taraxacum offi cinale biological equivalent to the herbicide. Populations of control with the fungus at the two higher birds-foot trefoil, Lotus corniculatus L., mowing heights was as effective as with white clover, Trifolium repens L. the chemical herbicide. Close mowing (Fabaceae), broadleaf plantain, Plantago favoured T. offi cinale seedling recruitment major L. (Plantaginaceae), and common since the biological control agent has no ragweed, Ambrosia artemisiifolia L. residual activity. Close mowing may be (Asteraceae), were controlled to a similar detrimental for S. minor IMI 344141 extent by the S. minor IMI 344141 and the applications on heavily infested domestic herbicide treatments. lawns and amenity grassland areas. When Although prostrate knotweed, Poly- T. offi cinale populations in fl ower were gonum aviculare L. (Polygonaceae), is treated with S. minor IMI 344141, fructifi - susceptible to S. minor, it appears to cation accelerated, seeds were smaller and escape infection due to its prostrate habit, free of the fungus and germination rate was which limits contact with bioherbicide reduced by 50% (Abu-Dieyeh et al., 2005). granules (Abu-Dieyeh et al., 2010). Mul- Despite the signifi cant morphologic and tiple growing points proliferate from the meristic differences among the 14 T. crowns and P. aviculare extends hori- offi cinale accessions collected from differ- zontally with tough woody stems and ent locations in North America and small leaves. The microclimate around Europe, all the accessions were similarly susceptible P. aviculare may be less moist susceptible to the S. minor IMI 344141 and therefore less conducive to the growth granular formulation (Abu-Dieyeh and of, and infection by, S. minor. In contrast, Watson, 2007a). Above- and below-ground the saucer-shaped rosette habits of T. biomass were reduced by 94% and 96%, offi cinale and P. major tend to gather respectively, with no difference among the granules into the centre of the rosette and 14 accessions. direct contact with the meristematic Foliar damage and T. offi cinale mortality crown. The importance of direct physical caused by S. minor IMI 344141 was contact was affi rmed by covering the affected by plant age and the presence of treated plots with jute fabric for 3 con- grass competition. Taraxacum offi cinale secutive days (Abu-Dieyeh and Watson, plants up to the 6-leaf stage were killed by 2009). Under cover, S. minor growth was S. minor IMI 344141 and T. offi cinale of all very rapid and abundant due to high ages were more severely affected by S. humidity and this enabled intimate contact minor IMI 344141 in the presence of grass of the plant parts with fungal mycelia, Chapter 58 387 consequently providing faster and better (clovers, Trifolium spp., medic, Medicago control even with lower rates of S. minor. spp.) were the next most susceptible When S. minor was combined with families with important weed species. The grass overseeding, at application or 10 days most resistant hosts were Poaceae (grasses, after application, the T. offi cinale popu- cereals), Linaceae (fl ax, Linum usitatissi- lation was reduced 70–80% in the fi rst mum L.), Cucurbitaceae (pumpkin, Cucur- year, increasing to 95% in the following bita moschata Duchesne, watermelon, year, in the absence of further treatments Citrullus lanatus (Thunberg) Matsum. & (Abu-Dieyeh and Watson, 2007b). Grass Nakai), Solanaceae (tomato, Solanum overseeding alone did not improve grass lycopersicum L., pepper, Capsicum quality or reduce T. offi cinale population annuum L.), Pinaceae (fi r trees, Abies spp.) densities in a low-maintained turf environ- and several other ornamentals. Based on ment. Turfgrass visual appearance and host-range testing, P. macrostoma was quality signifi cantly and continuously further investigated as a biological control improved up to 80%, compared with 10– for T. offi cinale and other broadleaved 20% in the control plots. When S. minor weeds in turfgrass and cereals. was applied with grass overseeding, Genetic characterization of several P. densities of T. repens and fi eld bindweed, macrostoma isolates showed that only Convolvulus arvensis L. (Convolvulaceae), those isolates originating from C. arvense were also signifi cantly reduced compared possessed the bioherbicidal trait (Zhou et with the bioherbicide alone treatment. al., 2005). The bioherbicidal isolates had There were no adverse effects of direct S. two chromosomal karyotypes that were minor contact on turfgrass seed germin- geographically distributed across Canada. ation, seedling emergence, or seedling Phoma macrostoma has no known telo- establishment. morph (Boerema et al., 2004) and limited Phoma macrostoma isolate 94-44B, intraspecifi c variation, thereby limiting the derived from the coelomycete fungus P. risk of introducing novel alleles in the macrostoma was originally isolated from population. Cirsium arvense (L.) Scopoli (Asteraceae) The environmental fate of P. macro- and shown to cause intense bleaching of stoma is limited in soil due to restricted leaves and root growth inhibition of T. mobility and survival. When granules were offi cinale when applied to the soil. These applied to soil at high doses (500g m−2), symptoms were the result of host sus- DNA of the fungus was detected in the ceptibility to the fungal production of roots, in the soil profi le at 1–8 cm deep, novel phytotoxins called macrocidins but not at 30 cm distance from the margin (Graupner et al., 2003, 2006). The infection of placement (Zhou et al., 2004). Over process confi rmed that fungal mycelia time, DNA of the fungus was detected in penetrated the host roots and grew towards plant roots and soil for up to 9 weeks, only the vascular trachea, whereby macrocidins in soil for up to 4 months, and not detected were released and taken up by the host at all after 12 months. (Bailey et al., 2011b). Phoma macrostoma is formulated as a Host-range testing of agricultural, horti- granule for broadcasting on soil or turf- cultural, ornamental and weedy plant grass. The amount applied and the fre- species showed that 57 species from 28 quency of applications depends on families were resistant and 38 species from whether it is being used on T. offi cinale 12 families were susceptible (Bailey et al., emerging as seedlings or T. offi cinale that 2011a). Asteraceae was the most sus- have already established. On turfgrass, a ceptible plant family, which includes single pre-emergent application at the rate weeds such as T. offi cinale, ragweed, of 16 g m−2 consistently reduced the common groundsel, Senecio vulgaris L. number of T. offi cinale seedlings emerging and Canada thistle. Brassicaceae (wild by >80% compared to untreated controls in mustard, Sinapis arvensis L.) and Fabaceae 14 out of 21 trials and by >60% in 19 out of 388 Chapter 58

21 trials. Post-emergent applications at the Management Regulatory Agency granted rate of 60 g m−2 with two applications temporary registration for the sale and use spaced 1 month apart consistently reduced of FeHEDTA as a reduced risk product to the number of established T. offi cinale by control several broadleaved weed species >80% in 14 of 30 trials and >60% in 23 of in turf. Products containing FeHEDTA 30 trials. However, doubling the post- quickly arrived on the list of permitted emergent rate reduced the number of T. pesticides in several provinces. offi cinale by >80% in 23 out of 30 trials. Sarritor, Sclerotinia minor IMI 344141, Preliminary research in agricultural is a living entity and requires appropriate settings has shown a 68% reduction in T. temperature and moisture conditions as offi cinale numbers when applied as a per label instructions and may not be single, pre-emergent application at 64 g compatible with commercial LCOs. Due to m−2. Other factors affecting effi cacy the nature of the lawn-care industry and included granule formulation, precipi- their large customer base, Sarritor was tation volume and soil type. Better effi cacy often applied in too hot or too dry con- was obtained with small granules (400– ditions and did not survive. When label 1200 μm) that disintegrated rapidly in instructions are followed, excellent control water (Bailey et al., 2010b). Effi cacy was of T. offi cinale and other broadleaf weeds is reduced after receiving 250 mm of obtained. The future of Sarritor Inc. and simulated rainfall and the loss of activity the Sarritor bioherbicide are uncertain. was more pronounced in sandy soils than Phoma macrostoma isolate 94-44B was in clay (Bailey et al., 2010c). registered by The Scotts Company as a bioherbicide for control of T. offi cinale and other broadleaved weed species in turf- 58.4 Evaluation of Biological grass in Canada in 2011 and in the USA in Control 2012. At the time of writing, develop- mental research continues to scale-up the Sclerotinia minor IMI 344141 received production process to commercial levels. temporary registration as a bioherbicide in Its signifi cance in the market place may Canada in 2007 and full registration in only be determined after the product is 2010 for the control of T. offi cinale and commercially available (Bailey and Falk, other broadleaf weeds in turfgrass. 2011). Registration is pending in the USA. The Bioherbicides are now recognized as an fi rst biological, 100% natural (non-chem- important weed management tool. Changes ical), selective lawn weed killer to control in societal values with respect to the use of T. offi cinale was available for the com- conventional herbicides on food products mercial and domestic markets and Sarritor and in our day-to-day environment, sup- was compliant with all municipal by-laws. ported by government bans on the use of In 2009, approximately 300 t of com- herbicides in our urban centres, have mercial product was sold in Canada to created a need for these new weed man- professional lawn-care companies and agement tools (Bailey et al., 2010a). This is municipalities in Canada. The domestic particularly evident with T. offi cinale and product was launched in the spring of 2010 other weeds occurring in turfgrass in urban in some retail stores across Canada. At that areas. The key challenges for the develop- time, over 400 t of freshly prepared pre- ment of both S. minor and P. macrostoma ordered commercial product was available were related to late-stage product develop- in a distribution facility in Ontario, but ment and commercialization, specifi cally Sarritor Inc’s LCO partners abandoned in acquiring funding for developing com- their pre-ordered commitment of the mercially viable fermentation and formu- Sarritor product in favour of FeHEDTA – lation strategies, controlling product purity iron chelated with hydroxyethylenedia- and shelf life, controlling costs of pro- mine triacetic acid (HEDTA). The Pest duction for competitive consumer pricing, Chapter 58 389 and limited availability of commercial 5. Continuing to modify regulatory and infrastructure for microbial manufacturing legislative environments to encourage (Bailey, 2010). biopesticide development.

58.5 Future needs Acknowledgements Glare et al. (2012) have provided several We thank Agriculture & Agri-Food Canada recommendations that they believe will Matching Investment Initiatives, Natural help all biopesticides develop to their full Science and Engineering Council, Saska- potential. tchewan Agriculture and Food–Agri- Thus, future work should include: cultural Development Fund, Canada Wheat 1. Improving delivery and persistence of Board, Saskatchewan Alfalfa Seed Pro- biopesticides; ducers Development Commission, Alberta 2. Understanding the chemistry of the bio- Alfalfa Seed Commission, Canadian Turf- active component; grass Research Foundation, The Scotts 3. Making strategic selection of target pests Company, Sylvan BioProducts and Sarritor in addition to T. offi cinale and markets; Inc. (4260864 Canada Inc.) for funding the 4. Continuing investment in discovery, research and development of these two development and implementation; bioherbicides.

References

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59 Tripleuro spermum inodorum (L.) Sch. Bip., Scentless Chamomile (Asteraceae)

Alec S. McClay,1 Gary Peng,2 Karen L. Bailey,2 Russell K. Hynes2 and Hariet L. Hinz3 1McClay Ecoscience, Sherwood Park, Alberta; 2Agriculture and Agri- Food Canada, Saskatoon, Saskatchewan; 3CABI, Delémont, Switzerland

59.1 Pest Status perennial crops, pastures, wasteland, road- sides and ditches (Woo et al., 1991), and Scentless chamomile, Tripleurospermum germinates readily under conditions of inodorum (L.) Sch. Bip. (=Matricaria periodic fl ooding, becoming abundant perforata Mérat) (Asteraceae) is an annual around sloughs, low areas and along or short-lived perennial plant of European ditches (Saskatchewan Agriculture and origin that has become naturalized in Food, 2004). Tripleurospermum inodorum Canada, and is a serious weed of disturbed can become abundant in urban and and agricultural land in the prairie prov- industrial areas, and along pipeline and inces (Woo et al., 1991). It occurs widely in utility rights-of-way, forming a reservoir for the black, grey and dark brown soil zones further infestation of agricultural land. of Alberta and Saskatchewan, and can Plants germinating before mid-July usually spread rapidly because of its profuse seed show an annual life cycle, bolting and production, up to 1.8 million seeds m−2 in fl owering within the same growing season, dense populations. It occurs in a wide whereas plants germinating from mid-July variety of habitats, including annual and onwards usually show a winter annual life

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) 392 Chapter 59 cycle, developing into an overwintering without disturbance (by removal of all rosette, which bolts and fl owers the post-fl owering T. inodorum and plants of following summer. Most plants die after other species in September), indicated that fl owering and setting seed, but a small disturbance was the most important factor percentage may survive over winter and for population build-up (Hinz, 1999; Hinz regrow from the base to fl ower again in the and McClay, 2000). However, on disturbed following season. In central Alberta, plots (i.e. reduced interspecifi c com- fl owering usually begins in early to mid- petition), a reduction in herbivory through July and seed is set from early August to application of insecticide nearly doubled freeze-up (Blackshaw and Harker, 1997). the yearly rate of population increase, h. Tripleurospermum inodorum can cause This occurred mainly through an increase signifi cant yield losses by competing with in the number of seedlings that established, cereal crops (Douglas et al., 1991, 1992), but also an increase in the survival rate of and losses are likely higher in less biennial rosettes. This study concluded competitive crops such as lentils, Lens that disturbance in and around mono- culinaris Medik. (Fabaceae ), and fl ax, specifi c stands of T. inodorum should be Linum usitatissimum L. (Linaceae) (Saska- reduced and biological control agents that tchewan Agriculture and Food, 2004). attack the rosettes of T. inodorum would be Tripleurospermum inodorum is listed as a the most effective. noxious weed in British Columbia, Alberta, In addition, a density-dependent model Saskatchewan and Manitoba. indicated that full control of T. inodorum will be diffi cult to achieve, due to strong over-compensating density dependence, at least in monospecifi c stands. Severe and 59.2 Background sustained reductions in fecundity and reductions in late season survival are there- With its diversity of life histories, T. fore necessary for management regimes to inodorum can be a diffi cult weed to con- be effective (Buckley et al., 2001). trol: practices that control summer annual De Camino-Beck (2006) and De Camino- seedlings may not be effective against Beck and Lewis (2009) used fi eld data on winter annual or perennial plants. It seeds seed dispersal from T. inodorum plants to prolifi cally throughout the growing season, develop a coupled map lattice model for and the seeds are easily dispersed and can the spread of this species across a germinate at any time of year. Many heterogeneous landscape. Estimated rates herbicides registered for in-crop use will of spread from this model ranged from not control T. inodorum beyond the seed- around 11 to 16 m year−1. This relatively ling stage, and the plant’s dense fi brous slow rate suggests that passive seed dis- root system can allow larger plants to persal is not the most important mech- survive tillage, especially in moist soil anism of spread for T. inodorum in real (Saskatchewan Agriculture and Food, landscapes. Models incorporating stocha- 2004). After the rapid spread of T. ino- stic dispersal may be useful in simulating dorum in the 1970s and 1980s (Saska- the interactions between biological control tchewan Agriculture and Food, 2004), it agents and pioneer weed species such as T. was selected as a target for biological inodorum, where the weed forms a control (Peschken et al., 1990), and a ‘moving target’ and the appearance and number of European insects were studied decline of new host patches and the as potential biological control agents dispersal of agents both play a major role (McClay et al., 2002). (De Camino-Beck et al., 2004). A study on the population dynamics of In crop fi elds, a microbial-bioherbicide T. inodorum in artifi cially established plots approach may be appropriate for control of in the native range, with or without regular T. inodorum because frequent disturbance application of insecticide and with or may hamper establishment of insect Chapter 59 393 bio logical control agents. A project was August 2011 and held in emergence boxes initiated to survey and evaluate indigenous for collection of adult parasitoids. One and exotic fungi for biological control of T. female Eupelmus vesicularis (Retzius) inodorum. Field surveys were conducted (Hymenoptera, Eupelmidae) and three in Saskatchewan and in west-central female Mesopolobus sp. (Hymenoptera, Europe in 2000 and 2001, and 706 fungal Pteromalidae) emerged (G. Gibson, Ottawa, isolates were tested for weed control Ontario, 2012, pers. comm.). Larvae of M. potential under controlled environment edentulus were sometimes found at Vegre- conditions. While the majority of the organ- ville developing in the base of the fl ower isms appeared ineffective, many isolates of heads of T. inodorum, feeding in receptacle Colletotrichum truncatum (Schwein.) tissue without damaging the developing Andrus & W.D. Moore (Glomerellaceae) ovules; this mode of feeding was not showed moderate to high potential for reported by Hinz et al. (1996). weed control (Peng et al., 2005). Omphalapion hookerorum was fi rst released in 1992 and R. tripleurospermi in 1999. Both species are now widely 59.3 Biological Control Agents established in Alberta, Saskatchewan, and parts of north-eastern British Columbia. In The seed weevil Omphalapion hookerorum central Alberta they are found on virtually (Kirby) (= Apion hookeri Kirby or Ompha- every patch of T. inodorum. Majka et al. lapion hookeri (Kirby); see Wanat, 1994) (2007) also note that O. hookerorum has (Coleoptera: Brentidae), the stem-mining expanded its range in Nova Scotia and is weevil Microplontus edentulus (Schultze) now abundant on the north shore of the (Coleoptera: Curculionidae) and the gall province. midge Rhopalomyia tripleurospermi Both rapid natural dispersal and re- Skuhravá & Hinz (Diptera: Cecidomyiidae), distribution efforts contributed to the all from Europe, have been released and spread of these agents. From 1996 to 2002, established against T. inodorum in Canada the dispersal of both species from their (McClay et al., 2002) initial release sites at Vegreville, Alberta, Microplontus edentulus, fi rst released in was mapped by searching the surrounding 1997, is still only confi rmed to be estab- area in a grid pattern, inspecting patches of lished at one site, at Vegreville, Alberta T. inodorum and recording locations where (53.51°, −112.09°), and appears to have either insect was found, using GPS. spread very little in 13 years after release. Omphalapion hookerorum initially dis- In August 2010, stems containing M. persed fairly slowly, and up to 3 years after edentulus larvae were collected from a release was found only 180 m from the roadside clump of T. inodorum at Vegre- release plots. Its spread then began to ville; however, no larvae emerged from accelerate, and from 1996 to 2002 it stems sampled in a similar population only dispersed at a fairly uniform rate with a 2.6 km away to the south-east. Approxi- mean of 2.8 km year−1. Initial dispersal of mately 140 mature larvae from the R. tripleurospermi was much more rapid Vegreville population were shipped to than that of O. hookerorum; from 1999 to British Columbia in late summer 2010 for 2002 it spread at a mean rate of about 5.2 rearing to the adult stage and release in km year−1 (Fig. 59.1). The rapid spread of spring of 2011. These were released near R. tripleurospermi was also aided by its Kleena Kleene, British Columbia (51.95°, multivoltine life history. Periodic sampling −124.83°), but establishment has not yet from fi eld plots at Vegreville indicated that been confi rmed (S. Turner, Kamloops, 2012, R. tripleurospermi underwent three gener- pers. comm.). As ectoparasitic Hymen- ations per year in 2000 and 2001 (McClay, optera larvae had been observed on M. 2003). Two unidentifi ed Mesopolobus spp. edentulus larvae, further stems were (Hymenoptera: Pteromalidae) emerged as collected from the Vegreville population in parasitoids from fi eld-collected galls in 394 Chapter 59

18

16

14 Omphalapion 12 Rhopalomyia 10

8

Dispersal (km) 6

4

2

0 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 Year

Fig. 59.1. Maximum observed dispersal distances of Omphalapion hookerorum and Rhopalomyia tripleurospermi from releases made at Vegreville, Alberta, in 1993 and 1999, respectively.

Vegreville in 2000 and 2001 (G. Gibson, (56.12°, −120.35°) from releases made in Ottawa, 2002, pers. comm.). 1992, 1998 and 2002, and some re- Both O. hookerorum and R. tripleuro- distribution has been done in this region. spermi have been extensively redistributed. Observations from 2009 to 2012 confi rm In Alberta most redistribution was done on that O. hookerorum is present throughout a fee-for-service basis, through the Alberta the area from Fort St John east 50 km to the Research Council from 2000 to 2004, and Alberta border and (from redistribution in by McClay Ecoscience since then. Between 2009) in a smaller area about 80 km south, 2000 and 2012 there were approximately near Dawson Creek (55.77°, −120.23°). 140 releases of O. hookerorum and 135 of Rhopalomyia tripleurospermi was also R. tripleurospermi in Alberta, with redistributed to the same area but has not additional releases of both species sent to become as noticeable (K. Clark, Dawson British Columbia and Saskatchewan, and Creek, 2012, pers. comm.). A few releases releases of only R. tripleuro spermi sent to of R. tripleurospermi were made around Manitoba. Omphalapion hookerorum was Erickson and Minnedosa, Manitoba (50.50°, released in lots of 200–500 adults, in early −99.91°), in 2009, but the results are not or late summer (McClay and De Clerck- known (J. Thornton, Souris, 2012, pers. Floate, 1999), whereas R. tripleurospermi comm.). was released by transplanting groups of Figure 59.2 shows the estimated nine galled rosette-stage plants into fi eld distribution of O. hookerorum and R. sites in early summer. Releases of adult R. tripleurospermi in British Columbia, tripleurospermi are not feasible due to their Alberta and Saskatchewan, based on sites short lifespan (Hinz, 1998). In Saska- where establishment has been confi rmed tchewan there was also extensive re- and the observed rates of spread for each distribution and monitoring by provincial species at Vegreville (McClay, 2003). This agencies, with 152 releases of O. may underestimate the actual distribution, hookerorum and 132 of R. tripleurospermi as location and monitoring data were not up to 2008 (H. Ander son, Saskatoon, 2011, available for all releases. pers. comm.). Both species are established Colletotrichum truncatum is a common around Fort St John, British Columbia fungal pathogen causing anthracnose on Chapter 59 395 served at in British Columbia, Alberta and in British Columbia, Rhopalomyia tripleurospermi (b) and (b) Omphalapion hookerorum Release sites and establishment of (a) (a) Fig. 59.2. Vegreville, Alberta. Some locations are approximate. Vegreville, Saskatchewan. Shaded area shows estimated distribution as of 2012, based on release locations and dates, rates spread ob 396 Chapter 59 many plant species, including fi eld crops followed by development of primary such as lentil (Morrall, 1988), fi eld pea, infection hyphae within these epidermal Pisum sativum L. (Gossen et al., 2009), cells. The onset of host tissue necrosis lucerne, Medicago sativa L. (Graham et al., seemed to coincide with the development 1976), soybean, Glycine max (L.) Merr., of secondary hyphae. This initial intra- (Manandhar et al., 1985; Roy, 1982) and cellular, hemibiotrophic infection pattern mung bean, Vigna radiata (L.) R.Wilczek may be relevant to host specifi city of this (Fabaceae) (Han and Lee, 1995). Many biological control agent. There was also a Colletotrichum spp. have developed strong low level of latent infection of lentil by the preferences for a particular plant species or C. truncatum BCI, although the impact even a type of tissue (Bailey et al., 1992), appeared to be transient and some cultivars especially within C. truncatum, making resisted the infection with a hypersensitive them good candidates as bioherbicides reaction (Forseille et al., 2009). (Boyette, 1991). Most C. truncatum isolates obtained from T. inodorum in either Saskatchewan or Europe showed high 59.4 Evaluation of Biological Control pathogenicity only on their original host and not on 13 other plant species, A factorial fi eld plot experiment was set up including fi eld crops commonly grown in at Vegreville in 2001 to evaluate the impact western Canada, and related Asteraceae of all three insect agents on the growth and (Peng et al., 2005). These C. truncatum seed production of T. inodorum plants in 1 isolates could not be reliably separated m3 screened fi eld cages (McClay, 2003). from isolates from lentil or fi eld pea based Signifi cant effects were observed for R. on conidial morphology, but ribosomal tripleurospermi on mean stem height and DNA sequencing of a large number of number of open fl owers, for O. hookerorum Colletotrichum spp. isolates showed that on number of open fl owers, number of seed all the T. inodorum isolates fell within a heads and total seed weight, and for M. single cluster regardless of their geographic edentulus on number of seed heads (Table origin. They are most closely related to C. 59.1). The effect of R. tripleurospermi on truncatum isolates from lentil, and less mean stem height and number of open closely to pea and soybean isolates. PCR fl owers confi rms results of pre-release primers based on the rDNA sequences of impact studies (Hinz and Müller-Schärer, different C. truncatum isolates separated 2000), and is to be expected from the type of the isolates effectively (Forseille et al., damage caused by R. tripleurospermi, as 2011). galling on terminal buds tends to stunt the Because C. truncatum causes anthrac- growth of main stems and delay fl ower nose on lentil and fi eld pea, two important production. The reduction in seed weight fi eld crops in western Canada, there was due to O. hookerorum is also not concern about the safety of the C. unexpected, as O. hookerorum directly truncatum isolates from T. inodorum for reduces seed production by larval feeding. pulse crops when applied at high doses. The effects of O. hookerorum and M. On detached leaves and young plants, edentulus on open fl ower and seed head isolates from T. inodorum caused infection numbers (Table 59.1) are less easy to symptoms only on the original host and understand. Possibly, feeding by these showed no pathogenicity on lentil or fi eld insects increases stress on the plant, leading pea (Forseille et al., 2009), whereas lentil to more rapid maturation of fl ower heads. isolates caused severe disease on both Due to good growing conditions and lentil and fi eld pea but no symptoms on T. lack of competition, the plants in this inodorum. The biological control isolates experiment grew extremely large and (BCI) showed typical hemibiotrophic vigorous, each plant virtually fi lling its infection: infection vesicles were produced cage by the time the experiment was in epidermal cells shortly after penetration, harvested in September. The biological Chapter 59 397

Table 59.1. Least squares means for treatment effects in 2001 fi eld plot impact experiment. Only main effects signifi cant at P<0.05 shown. Mean without Mean with Standard Insect treatment Response variable insect insect error P R. tripleurospermi mean stem height (cm) 115.0 105.8 3.0 0.0360 number of open fl owers 1327.8 830.3 110.3 0.0036 O. hookerorum number of open fl owers 1243.1 914.9 110.3 0.0439 number of seed heads 918.3 1326.6 97.3 0.0083 total seed weight (g) 113.8 80.0 10.0 0.0223 M. edentulus number of seed heads 961.8 1283.1 97.3 0.0332

con trol agents may have a greater impact head (S) in 2007 was signifi cantly reduced on the less vigorous plants typical of by both insects, and was given by: natural situations where T. inodorum S = 182 – 60R – 6.1H grows in competition with other plant (n = 50; r2 = 0.269) (59.1) species. Hinz and Schroeder (2003), in fi eld plot experiments in Germany, found where R (= 0 or 1) indicates presence or that root herbi vory by Diplapion confl uens absence of R. tripleurospermi galling, and Kirby and Coryssomerus capucinus (Beck) H is number of O. hookerorum per head. (Cole optera: Curculionidae) reduced the There was no interaction between the number of shoots of T. inodorum when effects of O. hookerorum and R. tripleuro- growing in competition with wheat, spermi. In 2008 seed head volume was Triticum aestivum L. (Poaceae), but not measured as a covariate; there was no when grown alone. The impact of the signifi cant effect of R. tripleurospermi and agents established in Canada has not been seed production was given by: evaluated quantita tively on a fi eld scale. S = 148 + 0.48V – 9.4H However, plants of T. inodorum are (n = 40; r2 = 0.254) (59.2) frequently heavily galled by R. tripleurospermi. In early summer large where V is seed head volume in mm3. galls often develop at the tips of bolting Based on these samples, mean seed stems, stunting their growth and inhibiting production per head at this site was normal branching and fl owering, which reduced by 19% and 17% by the combined may reduce competitiveness with crops effects of the biological control agents in and other vegetation. Galls of R. tripleuro- 2007 and 2008, respectively. spermi can develop on all above-ground The virulence of Canadian and Euro- parts of T. inodorum, including fl owers. pean C. truncatum isolates on T. inodorum There has been very limited post-release varied: most of the European isolates assessment of the effects of these two showed relatively high weed suppression agents. Seed-head samples were taken in (based on disease severity and plant fresh- 2007 and 2008 at a suburban park site in weight reduction), while Canadian isolates Sherwood Park, Alberta (53.52°, −113.26°), were more variable (Peng et al., 2005). where O. hookerorum and R. tripleuro- Nevertheless, several Canadian isolates spermi occurred as a result of natural showed the same effi cacy as their European dispersal. In 2007, 72% of seed heads were counterparts when tested under the same attacked by O. hookerorum, with a mean of conditions. Leaf wetness duration >20 h is 2.7 weevils per head (range 0–15) and 32% generally required for maximum infection by R. tripleurospermi. In 2008, 78% of by C. truncatum at 20°C, but the infection heads were attacked by O. hookerorum may be enhanced under higher dew- (mean 3.9 per head, range 0–17) and 15% temperature conditions ranging from 20 to by R. tripleurospermi. Seed production per 25°C (Graham et al., 2006a). Increasing the 398 Chapter 59 inoculation dose of C. truncatum may also h prior to fungal inoculation or as a tank- improve weed suppression. mix application. In the greenhouse, In initial trials, C. truncatum BCI alone metribuzin at 1× recommended rate caused provided only modest suppression of T. slight phytotoxicity on lentil, with most inodorum, especially against bigger plants plants exhibiting slight to moderate and under fi eld conditions. Potential syn- chlorosis. However, this phytotoxicity did ergy of the fungus with synthetic herbi- not increase the infection on lentil inocu- cides was investigated using tank-mix lated with C. truncatum BCI when applications to enhance weed suppression. compared to controls inoculated with the Many herbicide products are not com- fungus. In fi eld trials, lentil plots were patible with the fungal spores, but infested with T. inodorum at 25 plants m−2. clodinafop, glufosinate, MCPA and 2,4-D Metribuzin also caused damage to lentil are relatively benign and only delayed plants although most of the affected plants spore germination slightly (Graham et al., recovered within 2–3 weeks. No disease 2006b). When applied under greenhouse symptoms were observed on lentil plants conditions at 7×106 spores ml−1 with treated with metribuzin and C. truncatum selected herbicides at 1× and 0.1× regis- whereas a modest level of disease occurred tered label rates, C. truncatum BCI showed on T. inodorum receiving the same treat- synergistic interactions with MCPA, 2,4-D ment (Peng et al., 2007). Further results ester, clopyralid and metribuzin at the 1× showed that metribuzin plus C. truncatum rate, resulting in substantially improved did not affect lentil biomass relative to control relative to C. truncatum or the untreated controls 4 weeks after treatment herbicides applied alone. (Table 59.2). Interestingly, C. truncatum did There was a concern about crop safety not seem to progress beyond the initial for use of the C. truncatum BCI with infection phase in lentil leaves treated with herbicide because slight latent infection on metribuzin (Peng et al., 2007). Thus even lentil by this fungus was observed. It was with the herbicide, C. truncatum still was not clear if the companion herbicide metri- not able to cause substantial infection on buzin, a recommended herbicide for con- lentil plants. trol of broadleaf weeds in pulse crops, In the same fi eld trials, the biomass of would predispose lentil to infection by the T. inodorum was reduced by all treatments C. truncatum BCI. This was assessed in relative to non-treated controls, but the greenhouse as well as fi eld conditions by herbicide plus C. truncatum treatment applying the herbicide to lentil seedlings 24 tended to be more effective than either

Table 59.2. Effect of Colletotrichum truncatum (CT) in tank mixes with the herbicide metribuzin on T. inodorum and lentil in fi eld trials.

Mean plant biomass a T. inodorum Lentil Treatment g/plant g/plot b Non-treated control 141 a 33 c Weed-free control N/A 66 a CT alone 119 b 36 c Metribuzin alone 80 c 44 b Metribuzin + CT (Tank mix) 63 d 46 b Metribuzin + CT (split applications) 70 cd 47 b

a Means followed by the same letter do not differ (LSD, P = 0.05). b Plants were cut from two central 50-cm rows and averaged over eight plots (two trials). Chapter 59 399 component applied alone (Table 59.2). The 1. Redistribution of O. hookerorum and R. highest lentil biomass was observed in tripleurospermi to any areas of T. inodorum weed-free plots. The synergy between C. infestation where they are not yet estab- truncatum and the herbicide metribuzin lished; against T. inodorum was demonstrated in 2. Quantitative impact assessment of O. these two fi eld trials, and the results hookerorum and R. tripleurospermi in fi eld confi rmed the prior observations under situations, in particular focusing on popu- controlled-environment conditions (Graham lation level impacts and effects on the com- et al., 2006b). Use of this synergy may petitiveness of T. inodorum with other widen the window for fi eld applications; vegetation; the effectiveness of C. truncatum or herbi- 3. Further assessment of the establishment cides generally declines with increasing and possible impact of M. edentulus; growth stages of T. inodorum (Graham et 4. Completion of the screening of candi- al., 2006b, 2007), but combining C. trun- date agents previously studied, such as catum with the herbicide provides an Napomyza sp. near lateralis (Fallén) option for controlling larger T. inodorum (Diptera: Agromyzidae) and Botanophila plants in crop fi elds that otherwise would sp. near spinosa (Rondani) (Diptera: not be controlled suffi ciently. The synergy Anthomyiidae) (McClay et al., 2002), if may also reduce the requirement for a high evaluation indicates that O. hookerorum C. truncatum dose, substantially saving on and R. tripleurospermi do not have suffi - the cost of the fungal inoculum (Peng and cient impact; Wolf, 2011). 5. An improved fermentation process for Tripleurospermum inodorum has fi nely more effi cient and economical production divided leaves with a limited surface area of C. truncatum conidia; for intercepting spray droplets. Under 6. An improved formulation to encourage controlled environmental conditions, fi ne rapid germination of C. truncatum conidia sprays (volume median diameter (VMD) on T. inodorum and infection of the host <207 μm) resulted in better spray retention for more consistent fi eld performance. and more effective control of T. inodorum by C. truncatum than medium (267 μm) or coarse (325 μm) sprays (Byer et al., 2006a, b). Hynes et al. (2010) developed a com- Acknowledgements plex coacervate formulation for C. trun- catum in non-refi ned vegetable oil, using We thank the Alberta Agricultural Research soy lecithin as an emulsifi er and 1% Institute and the Agriculture Development gelatin and 2% gum arabic as the wall Fund, Saskatchewan, for fi nancial support; ingredient. This formulation was sub- Robert B. Hughes, Cara Kirkpatrick, Dr stantially more effective in greenhouse James Tansey, Lucille Kowalchuk, Kathy trials than an aqueous suspension in 0.1% Taxbock, Kelly Byer and Margaret Molloy Tween 80. The application technology with for technical assistance; Kerry Clark and optimized spray adjuvants and parameters Susan Turner for information on fi eld also aids in control of T. inodorum using releases and recoveries of agents in British tank mixtures of a synergistic herbicide Columbia; Harvey Anderson and Jane and C. truncatum (Peng and Wolf, 2011). Thornton for information on releases in Saskatchewan and Manitoba, respectively; Dr Gary Gibson (AAFC, Ottawa) for 59.5 Future Needs identifi cations of parasitoids; and Dr Lloyd Dosdall for assistance with the parasitoid Future work should include: sampling with M. edentulus. 400 Chapter 59

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60 Vincetoxicum nigrum (L.) Moench, V. rossicum (Kleopow) Barbar., Swallow-Worts, Dog Strangling Vine (Apocynaceae)

Rob S. Bourchier,1 Aaron Weed,2,6 Richard Casagrande,2 André Gassmann,3 Sandy M. Smith4 and Naomi Cappuccino5 1Agriculture and Agri-Food Canada, Lethbridge, Alberta; 2University of Rhode Island, Kingston, Rhode Island, USA; 3CABI, Delémont, Switzerland; 4University of Toronto, Toronto, Ontario; 5Carleton University, Ottawa, Ontario; 6Current address: Dartmouth College, Hanover, New Hampshire, USA

60.1 Pest Status ling down small trees and smothering vegetation planted at restoration sites European populations of swallow-worts, (Christen sen, 1998) and pine plantations in Vincetoxicum nigrum (L.) Moench and V. Ontario (DiTommaso et al., 2005). rossicum (Kleopow) Barbar. (Apocyna- Vincetoxicum spp. are long-lived, herb- ceae), have become established in north- aceous perennial plants that produce eastern North America, where there are no multiple shoots from overwintering root effective arthropod herbivores to suppress buds each spring. They fl ower beginning in populations and deter further spread late spring and continue until late August. (Sheeley, 1992; Sheeley and Raynal, 1996; Flowers are insect- or self-pollinated and Christensen, 1998; Lawlor, 2000; Milbrath, produce one to two elongate seedpods 2010). Vincetoxicum spp. display superior containing about 20 seeds. The poly- competition for resources among native embryonic seeds have fi brous tufts that aid plants and often form dense monocultures in wind dispersal and can germinate in a variety of habitats (Cappuccino, 2004). during late summer to autumn or in the They are a threat to native species and following spring (DiTommaso et al., 2005). habitats, and negatively affect farming The two species of concern, V. nigrum practices, livestock and ornamental land- and V. rossicum, are now widely distrib- scapes. Vincetoxicum spp. contain the uted along the Atlantic coast of the USA haemolytic glycoside vincetoxin, which is and in Ontario and Quebec in Canada. toxic to humans and most other mammals Vincetoxicum nigrum is native to Mediter- (DiTommaso et al., 2005). In addition to ranean regions of France, Italy and Spain; disrupting agricultural crops such as no-till V. rossicum is naturally distributed in maize, Zea mays L. (Poaceae), Vincetoxi- south-east Ukraine and Russia. The earliest cum spp. have been reported as a major record for V. rossicum in Canada was from pest in tree nurseries. The twining vines of British Columbia in 1885; however, this swallow-worts have been documented pul- species has not persisted in that province

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 60 403

(Douglas et al., 1998, as cited by usually compensate by sending up mul- DiTommaso et al., 2005). The earliest tiple axillary shoots (DiTommaso et al., record for Ontario was 1889 (DiTommaso 2005; McKague and Cappuccino, 2005). et al., 2005). Vincetoxicum nigrum is less In Ontario, at least two applications of common in Canada, primarily occurring in glyphosate in mid-June and early August localized patches in Ontario; early records were required to reduce V. rossicum cover were often confused with V. rossicum. It by 90% the following year (Christensen, has however been confi rmed to be in 1998). However, after treatment, the sites Ontario since the early 1950s (DiTommaso were open for successful colonization by et al., 2005). Despite the long history of another invasive plant, sweet white clover, Vincetoxicum spp. presence in North Melilotus albus Medik. (Fabaceae), which America, they have only become a signifi - replaced V. rossicum as the dominant vege- cant problem in recent decades due to tation (Christensen, 1998). In New York, range expansion and unhindered popu- one treatment of triclopyr (1.9 kg a.i. ha−1) lation growth (Lawlor, 2000). reduced V. rossicum cover and stem density by 56% and 84% after 2 years (Averill et al., 2008). However, despite 60.2 Background these results, the authors cautioned that long-term control could only be sustained Substantial efforts in the use of con- by repeated applications and active restor- ventional control methods such as mow- ation. ing, hand pulling and herbicides have All current control measures are largely been unsuccessful in eliminating generally only effective in the short term, established infestations of Vincetoxicum require substantial resources or labour and (Lawlor and Raynal, 2002; DiTommaso et could have collateral impacts on native al., 2005; McKague and Cappuccino, 2005; species in the surrounding habitats Averill et al., 2008; Douglass et al., 2009). (Lawlor, 2000). The use of biological con- The only method to ensure long-term con- trol agents is likely the only viable option trol of Vincetoxicum spp. requires ex- for long-term reductions in Vince toxicum cavation of entire plants because root spp. populations. Surveys of native herbi- crown fragments left behind can root in the vores on Vincetoxicum spp. have found a soil and produce additional shoots limited fauna of primarily generalist (DiTommaso et al., 2005). Hand picking species with limited potential to control seedpods from plants to limit spread is the plant (Ernst and Cappuccino, 2005; another control measure where digging and Milbrath, 2010). herbicides are not an option, such as in rocky habitats or protected natural areas. However, removal of seedpods is only 60.3 Biological Control Agents effective at reducing seed pressure if it is repeated throughout the growing season Field surveys in Europe identifi ed fi ve (Lawlor, 2000). potential biological control agents for Repeated mowing was shown to reduce Vincetoxicum spp.: two leaf-feeding the average stem height of V. rossicum but caterpillars, two leaf-feeding chrysomelid did not decrease overall cover (Christen- beetles, one of which also feeds on the sen, 1998). Subsequent studies found little roots of the plant as a larva, and a seed- or no effect of mowing or clipping on plant feeding tephritid fl y (Weed et al., 2011b). biomass, stem cover, density, or seedpod An initial test-plant list for swallow-wort production, with some variation associated biological control agents, drafted with a with the timing of the treatment in the North American perspective that included season (McKague and Cappuccino, 2005; Canada and Mexico, was developed by Averill et al., 2008). When the primary Milbrath and Biazzo (2007) and approved aerial stem is damaged, swallow-worts by the United States Department of 404 Chapter 60

Agriculture/Animal and Plant Health demonstrated, using similar conditions to Inspection Agency Technical Advisory the European tests, that a very closely Group (TAG) on Biological Control of related North American beetle species, Weeds. During the testing process, Chrysochus auratus (Fabricius) (Coleoptera: additional plant species were added to Chrysomelidae), can also complete increase representation in groups of concern development on Asclepias spp. (R. DeJonge, and the fi nal list of tested plants included 2012, unpublished results). However, this 83 species (Casagrande et al., 2012). species is a specialist on dogbane, Chrysolina asclepiadis asclepiadis Apocynum cannabinum L. (Apocynaceae), (Villa) (Coleoptera: Chrysomelidae) is a and does not attack Asclepias in the fi eld univoltine leaf beetle that is found on (Dobler and Farrell, 1999). Work is on-going white swallow-wort, Vincetoxicum hirun- to characterize better the host range of C. dinaria Medik. (Apocynaceae), in the west- auratus and C. cobaltinus LeConte ern Alps (Weed and Casagrande, 2011). (Coleoptera: Chrysomelidae), two North Eggs overwinter in the leaf litter and both American species that occupy the same the larvae and the adults feed on the niche as the European C. asclepiadeus, and leaves. In initial no-choice testing using 37 test if there is potential to use them for plant species, beetle larvae completed Vincetoxicum spp. biological control. This development on nine species within the work may also lead to a reassessment of genera Artemisia and Tanacetum (Astera- host-range testing results of the European ceae) and Asclepias and Vincetoxicum species C. asclepiadeus. (Apocynaceae). The host range for adult Euphranta connexa (Fabricius) (Diptera: feeding was even broader with 13 plant Tephritidae) is a pre-dispersal seed species within fi ve genera receiving sus- predator of V. hirundinaria and is one of tained feeding. Based on these results this the most broadly distributed and common species was dropped from further con- herbivores of Vincetoxicum in Eurasia. sideration as a potential biological control Populations of this species have been agent in North America (Weed and Casa- collected from Germany, Switzerland, grande, 2011). France and Ukraine. Adults oviposit in Chrysochus (Eumolpus) asclepiadeus developing seedpods of V. hirundinaria. Pallas (Coleoptera: Chrysomelidae) has a The larvae feed on the developing seeds, broader distribution in Europe than C. bore out of the seedpod at maturity and asclepiadis asclepiadis with populations pupate in the surrounding soil (Solbreck, found on V. nigrum in France, V. hirun- 2000). Euphranta connexa successfully dinaria in Switzerland and V. rossicum in attacks and completes development on Ukraine. There has been particular interest seedpods of the target weeds (Weed et al., in this species because adults feed on the 2011b). The initial focus of the dog leaves of the plant and larvae feed on the strangling vine project was on biological roots, causing signifi cant damage to the control agents that could directly affect plant (Weed et al., 2011a). The life cycle of plant biomass, thus efforts to characterize C. asclepiadeus varies between 1 and 3 the host range of E. connexa were initially years and this may be associated with delayed. However, as limiting seed spread regional population differences. The mean is a desirable outcome in North America, genetic divergence between specimens from additional studies on biology and host- France and Ukraine was 3%. Thus, the two range testing for E. connexa were initiated populations should be treated at least at the in 2011. The insect is challenging to test level of a well-differentiated subspecies because multiple non-target species must (Gassmann et al., 2011). Work on this insect be reared to produce seed. To date fi ve has been suspended because larvae can species, A. cannabinum, Asclepias tuber- complete development on four North osa L., A. curassavica L., Amsonia American Asclepias spp. (Gassmann et al., tabernaemontana Walter and A. illustris 2011). Additional studies in Canada have Woodson (Apocynaceae), have been tested Chapter 60 405 for oviposition response by E. connexa Monophagy on Vincetoxicum spp. was (Gassmann et al., 2013). Oviposition only confi rmed with a population collected occurred on three out of ten replicates of from V. hirundinaria in Ukraine, using the the ornamental A. curassavica. No ovi- same test-plant list as for H. opulenta position occurred on 22 replicates of the (Weed, 2010; Hazlehurst, 2012). A draft native North American A. tuberosa. petition has been prepared for A. Hypena opulenta (Christoph) (Lepi- asclepiadis; however, the petition for the doptera: Erebidae) was collected from V. release of H. opulneta has been submitted hirundinaria in Ukraine in a shaded forest fi rst because multiple overlapping gener- habitat (Weed et al., 2011b). It is a multi- ations of this species are expected to have voltine species with overlapping gener- higher impact on Vincetoxicum spp. than ations (Weed and Casagrande, 2010), which univoltine or bivoltine populations of A. indicates it will infl ict sustained attack on asclepiadis. Both species may be required Vincetoxicum spp. throughout the growing in North America for suppression of season. Impact studies conducted in Vincetoxicum in all habitats because H. containment determined that all tested opulenta was initially found exclusively at larval densities (2–8 larvae per plant) forested sites in Ukraine (Weed et al., signifi cantly reduced above-ground bio- 2011a). mass, seedpod production and seed pro- duction of V. rossicum (Weed and Casagrande, 2010). Host-range testing, 60.4 Evaluation of Biological Control completed with a test-plant list of 82 species, indicated that the insect is a No agents have been released for biological specialist on Vincetoxicum spp. (Hazle- control of Vincetoxicum spp. in North hurst et al., 2012). A joint petition for the America to date. A joint petition for the release of this insect in Canada and the release of Hypena opulenta in Canada and USA was submitted in November 2011. the USA was submitted in November 2011. Supplementary data requested by the Supplementary data requested by the United States Department of Agriculture, United States Department of Agriculture, Animal and Plant Health Inspection Ser- Animal and Plant Health Inspection vice, Technical Advisory Group was sub- Service, Technical Advisory Group was mitted in January 2013. submitted in January 2013. Abrostola asclepiadis (Denis and Schiffermüller) (Lepidoptera: Noctuidae) is broadly distributed across Europe and 60.5 Future Needs primarily associated with V. hirundinaria. Like the tephritid E. connexa, A. Future work should include: asclepiadis attacks plants in both open and forested habitats (Weed et al., 2011b). 1. Continuing host-specifi city tests with Abrostola asclepiadis usually completes seed-feeder E. connexa; one generation per year in northern lati- 2. Continuing assessment of host selection tudes, but bivoltine populations are known biology of potential native biological con- from Italy. The larvae of A. asclepiadis feed trol agents (Chrysochus spp.) that may on the leaves of Vincetoxicum spp. and attack and damage Vincetoxicum spp., and impact studies in Europe demonstrated compare results with European Chrysochus complete defoliation of plants at low larval spp.; densities (Weed et al., 2011a). Host-range 3. Maintaining colonies of H. opulenta and records for A. asclepiadis indicate that the A. asclepiadis in quarantine, pending species is monophagous on V. hirundinaria release decision; in the western part of its native range 4. Preparing a North America release peti- (Förare, 1995); other Vincetoxicum spp. tion for A. asclepiadis for submission to likely serve as hosts in eastern Europe. the Canadian Food Inspection Agency and 406 Chapter 60 the United States Department of Agri- initial host-plant test list and shared test- culture, Animal and Plant Health plant material. Additional studies on Inspection Service. Eumolpus asclepiadeus and Vincetoxicum genetics have involved collaboration between CABI, and USDA, ARS, EBCL in Acknowledgements France (Dr René Sforza, Marie-Claude Bon). Funding for foreign exploration and Host-plant testing and experimental work host-range research has been provided by: for Vincetoxicum was conducted at CABI Agriculture and Agri-Food Canada, Ontario Delémont in Switzerland and the Ministry of Natural Resources, Ontario University of Rhode Island, USA. Lindsey Invasive Species Centre, USDA North- Milbrath (USDA-ARS) developed the eastern IPM Program.

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Lawlor, F.M. (2000) Herbicidal treatment of the invasive plant Cynanchum rossicum and experimental post control restoration of infested sites. MS thesis, State University of New York, College of Environmental Science and Forestry, Syracuse, New York. Lawlor, F.M. and Raynal, D.J. (2002) Response of swallow-wort to herbicides. Weed Science 50, 179– 185. McKague, C.I. and Cappuccino, N. (2005) Response of pale swallow-wort, Vincetoxicum rossicum, following aboveground tissue loss: implications for the timing of mechanical control. Canadian Field Naturalist 119, 525–531. Milbrath, L.R. (2010) Phytophagous arthropods of invasive swallow-wort vines (Vincetoxicum spp.) in New York. Environmental Entomology 39, 68–78. Milbrath, L.R. and Biazzo, J. (2007) Proposed host specifi city test plant list for testing potential biological control agents of swallow-worts. Test plant list submitted to United States Department of Agriculture-Animal and Plant Health Inspection Service. Sheeley, S.E. (1992) Life history and distribution of Vincetoxicum rossicum (Asclepiadaceae): an exotic plant in North America. MS thesis, Syracuse University of New York, College of Environmental Science and Forestry, Syracuse, New York. Sheeley, S.E. and Raynal, D.J. (1996) The distribution and status of species of Vincetoxicum in eastern North America. Bulletin of the Torrey Botanical Club 123, 148–156. Solbreck, C. (2000) Ecology and biology of Euphranta connexa (Fabr.) (Diptera: Tephritidae) – a seed predator of Vincetoxicum hirundinaria Med. (Asclepiadaceae). Entomologisk Tidskrift 121, 23–30. Weed, A.S. (2010) Biology and ecology of European natural enemies of swallow-worts (Vincetoxicum) and the potential for biological control. PhD dissertation, University of Rhode Island, Kingston, Rhode Island. Weed, A.S. and Casagrande, R.A. (2010) Biology and larval feeding impact of Hypena opulenta (Christoph) (Lepidoptera: Noctuidae): a potential biological control agent for Vincetoxicum nigrum and V. rossicum. Biological Control 53, 214–222. Weed, A.S., and Casagrande, R.A. (2011) Evaluation of host range and larval feeding impact of Chrysolina aurichalcea asclepiadis (Villa): considerations for biological control of Vincetoxicum in North America. Environmental Entomology 40, 1427–1436. Weed, A.S., Gassmann, A. and Casagrande, R.A. (2011a) Effects of leaf and root herbivory by potential insect biological control agents on the performance of invasive Vincetoxicum spp. Biological Control 56, 50–58. Weed, A.S., Casagrande, R.A., Gassmann, A. and Leroux, A. (2011b) Performance of potential European biological control agents of Vincetoxicum spp. with notes on their distribution. Journal of Applied Entomology 135, 700–713. 408 Chapter 61

61 Erwinia amylovora (Burrill) Winslow et al., Fire Blight (Enterobacteriaceae)

Antonet M. Svircev,1 Julie Boulé,2 Peter Sholberg2 and Alan J. Castle3 1Agriculture and Agri-Food Canada, Vineland, Ontario; 2Agriculture and Agri-Food Canada, Summerland, British Columbia; 3Brock University, St Catharines, Ontario

61.1 Pest Status concentration of bacterial cells and plant- associated sugars. Bacterial cells are Fire blight, Erwinia amylovora (Burrill) dissipated into the orchard environment by Winslow et al. (Enterobacteriaceae), is a rain, wind and insects. Primary E. bacterial pathogen of plant species belong- amylovora infections are initiated once ing to the Rosaceae, such as apple, Malus bacterial cells land on the stigmata of open domestica Borkhhausen, and pear, Pyrus blossoms. Throughout the blossom blight communis L. Disease symptoms commonly stage, the bacterial population increases on associated with infection include wilt, the fl ower stigma, especially within the tissue necrosis and cankers. In severe optimal temperature range from 20 to 27°C. disease outbreaks the entire orchard In the presence of free water and/or high canopy may appear wilted and necrotic. relative humidity, the bacterial cells stream The appearance of black and shrivelled into the open fl ower cups or hypanthia. tissues has resulted in the name of ‘fi re Once E. amylovora reaches the hypan- blight’ since trees appear scorched and thium it easily passes into the internal burned. In Canada, all commercially grown tissues of the tree. Upon reaching the apples, apple rootstocks and pear cultivars internal tissue E. amylovora cannot be are moderately to highly susceptible to this controlled by streptomycin and/or bio- pathogen. The routine use of high density logical control agents. Under optimal plantings and fi re blight-susceptible dwarf- temperatures blossom infections may pro- ing rootstocks has contributed to extreme gress to shoots and rootstock. Erwinia susceptibility of trees to E. amylovora amylovora is an orchard epiphyte, there- infections. To date, dwarfi ng rootstocks fore trees remain susceptible during highly resistant to fi re blight pathogen are vigorous growth periods where chewing not available to the industry. The principal insects or hail damage may create openings sources of E. amylovora inoculum are fi re for the bacterial ingression into healthy blight cankers located on woody portions tissue. The internal survival of E. amylo- of the trees that were infected in the vora is not well understood, trees infected previous growing season(s). Warm spring in the previous growing season may show temperatures and high relative humidity symptoms in subsequent years. Tree age, leads to the production of bacterial ooze on cultivar susceptibility, management prac- canker margins. The ooze contains a high tices and climatic conditions all play an

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 61 409 intricate role in the development of fi re unavailable), Pseudomonas fl uorescens blight in the orchard. (Flügge) Migula (Pseudomonadaceae) A506 (BlightBan®, Nufarm) and Bacillus subtilis (Erhenberg) Cohn (Bacillaceae) (Serenade® 61.2 Background MAX, AgraQuest). The mechanism of action associated with the biological control In Canada, streptomycin has been available agents includes competition for space and for the effective control of blossom blight nutrients and/or the production of anti- since the 1960s. In Ontario, streptomycin is microbial substances such as antibiotics. limited to three applications within a The control of E. amylovora by bacterio- single bloom period (Anonymous, 2012). phages has been considered by a number of Bacterial resistance to streptomycin has researchers since the 1960s (Svircev et al., been reported in the USA north-west 2010). Phage effi cacy was generally tested (Coyier and Covey, 1975), Michigan under laboratory conditions or in vivo (McGhee et al., 2011) and British Colum- bioassays on fruit surface or fl ower bia, Canada (Sholberg et al., 2001) and bioassays. Erskine (1973) recognized that more recently in New York State (Russo et non-pathogenic orchard epiphytes could be al., 2008). Prohexadione-calcium (Apogee, used to deliver the lysogenized phages to BASF) was registered in Canada for fi re the fl ower surface. Pantoea agglomerans is blight control in apples. Prohexadione- now being developed as a vehicle for lytic calcium is a plant hormone that inhibits phages. The development of a phage- the green adventitious growth, resulting in mediated control of E. amylovora has terminal growth that is more sensitive to focused on obtaining effi cacies comparable mechanical damage and subsequent to streptomycin in bioassays and fi eld- infection by E. amylovora. This product is based trials. an important fi re blight management tool The Erwinia sp. phages were collected since it reduces the incidence and severity from the orchard environment in British of fi re blight symptoms in the apple Columbia (Boulé et al., 2011) and orchard. Current rootstock trials in the Vineland, Ontario (Gill et al., 2003). The 45 USA have demonstrated that many Geneva bacteriophages that constitute the Agri- series rootstocks are demonstrating culture and Agri-Food Canada, Vineland improved resistance to fi re blight pathogen Collection (Ontario) have been char- when compared to the Malling M9 and acterized by restriction fragment length M26 (Auvil et al., 2011). The future polymorphisms (RFLP), host range and availability of resistant rootstocks will be transmission electron microscopy (Gill et an important tool for fi re blight manage- al., 2003). All Ontario Erwinia sp. phages ment. are tailed (Caudoviridales), belonging to six distinct RFLP groups: Myoviridae (10 isolates, Group 1), Siphoviridae (2 isolates, 61.3 Biological Control Agents Group 2) and Podoviridae (38 isolates, Groups 3–6) (Svircev et al., 2002, 2011; In 2007, the Pest Management Regulatory Gill et al., 2003). In British Columbia, the Agency (PMRA, Health Canada) registered eight isolated Erwinia sp. phages belonged a number of commercial biological control to the Myoviridae and Podoviridae. The agents that can be used for the control of E. eight phage British Columbia collection amylovora in the orchard (Kabaluk et al., has two new RFLP groups, named Group 7 2010). The registered biologicals include and 8 (Boulé et al., 2011). Using the plaque Pantoea agglomerans (Ewing and Fife) assay (Adams, 1959), the host ranges of the Gavini et al. E325 (Bloomtime™, North- phages were established using wild-type west Agricultural Products), Pantoea isolates of E. amylovora from British vagans Brady et al. (Enterobacteriaceae) Columbia, Ontario and Nova Scotia (Gill et C9-1 (BlightBan®, Nufarm – currently al., 2003; Boulé et al., 2011). All the phages 410 Chapter 61

from British Columbia and Ontario reached densities greater than 105 pfu ml−1 demonstrated a wide host range. Current (Lehman, 2007). work in progress uses quantitative real- Further laboratory-based studies have time PCR (qPCR) procedures to determine focused on the optimization of the phage– host range with a global collection of E. carrier system and the eventual amylovora and 100 wild-type isolates of P. development of phage mixtures. Phage– agglomerans. In this procedure, host range host–carrier interactions can be monitored is characterized by the number of virions by multiplex real-time PCR. In this pro- produced in the phage–host combination. tocol we can simultaneously detect phage Bacteriophages are sensitive to UV and (Myoviridae or Podoviridae), pathogen and desiccation and require the presence of carrier in infected fl owers and/or liquid host cells to increase their population on cultures. The ability of bacteriophages to the fl ower surface. The use of P. agglo- transfer genetic information between bac- merans as a phage carrier would ensure terial species has often been cited as a phage survival and replication under fi eld serious problem with phage therapy in conditions. In vivo blossom assays and agriculture. To date, Erwinia sp. bacterio- fi eld-based trials were conducted from phages that have been fully sequenced do 2005 to 2008 to evaluate the effi cacy of not carry genes for lysogeny. Using the real phage-carrier combination against the time PCR probe-primers for Myoviridae pathogen. Streptomycin was used as the and Podoviridae, 100 wild-type isolates of positive control to evaluate the biological P. agglomerans and 250 global isolates of E. versus antibiotic effi cacy (Lehman, 2007; amylovora were screened for presence of Boulé et al., 2011). The phage-carrier was prophages and there were no lysogens generally applied at 50–75% full bloom detected in this collection of host bacteria and the pathogen was introduced 2–3 days (Roach, 2011). Our data indicate that E. later at a disease threshold concentration of amylovora lysogens are diffi cult to produce 106 cfu ml−1. All Ontario fi eld trials from under laboratory conditions and to locate 2005 to 2008 used a single phage-carrier in wild-type host collections (Roach, 2011). combination. In 2005, 6 of 12 treatments Additionally, bacterial exopolysaccharides consisting of E. amylovora phages and P. play a key role in the ability of the Podo- agglomerans Pa21-5 as the carrier signifi - viridae phages to infect E. amylovora cantly reduced the incidence of fi re blight. (Roach et al., 2011; Sjaarda, 2012). Under- The control afforded by these treatments standing the role of phage receptors on the was not statistically different from that ability of phages to infect E. amylovora afforded by streptomycin (Lehman, 2007). will impact the mixture of phage that will In British Columbia, two phages reduced be used in the fi nal preparation of the infection by 84–96% in blossom assay biological control agent. when applied in conjunction with the P. agglomerans carrier. Additionally, using potted trees and a single phage-carrier 61.4 Evaluation of Biological Control Pa21-5 system, 56% effi cacy was obtained when compared to streptomycin (Boulé et Our collective fi eld experiments, potted al., 2011). The population dynamics of the plant, in vivo blossom assays and lysogeny phage, carrier and pathogen was monitored studies indicate that the phage–carrier with qPCR over the bloom period. In fi eld- system should be pursued and further trial treatments that exhibited signifi cantly tested on a large scale using a complex reduced incidence of fi re blight, the mixture or cocktail of bacteriophages. average blossom population of E. amylo- The foremost challenge with biological vora was reduced to pre-experiment epi- control programmes is the wildly fl uctu- phytic levels (Lehman, 2007). Control of E. ating effi cacies from season to season. The amylovora on the blossom surface was application of biological control agents achieved when the phage population is challenging, since carrier and phage Chapter 61 411

populations must be established on the vide the ‘double punch’ where the carrier blossom prior to the arrival of the pathogen. is a biological control organism and the The unpredictable weather conditions, the phages are an additional control measure. presence of epiphytic populations of Heavy reliance on streptomycin can lead to E. amylovora and emergence of strepto- the development of bacterial resistance; mycin resistance has resulted in serious 2. Integration of biological control agents challenges for controlling this pathogen. into disease management programmes to reduce the incidence of antibiotic resist- ance in future bacterial populations. 61.5 Future Needs

Future work on fi re blight disease control Acknowledgements will need to: 1. Incorporate novel biological control Research was supported by funding from agents such as bacteriophages that can pro- Agriculture and Agri-Food Canada.

References

Adams, M.H. (1959) Bacteriophages. Interscience Publishers, New York. Anonymous (2012) Ontario Ministry of Agriculture Food and Rural Affairs, Guide to Fruit Production 2012-13, Publication 360. Available at: http://www.omafra.gov.on.ca/english/crops/ pub360/p360toc.htm (accessed 10 October 2012). Auvil, T.D., Schmidt, T.R., Hanrahan, I., Castillo, F., McFerson, J.R. and Fazio, G. (2011) Evaluation of dwarfi ng rootstocks in Washington apple replant sites. Acta Horticulturae 903, 265–271. Boulé, J., Sholberg, P.L., Lehman, S.M., O’Gorman, D.T. and Svircev, A.M. (2011) Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada. Canadian Journal of Plant Pathology 33, 308–317. Coyier, D.L. and Covey, R.P. (1975) Tolerance of Erwinia amylovora to streptomycin sulfate in Oregon and Washington. Plant Disease Reporter 59, 849–852. Erskine, J.M. (1973) Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemiology of fi re blight. Canadian Journal of Microbiology 19, 837–845. Gill, J.J., Svircev, A.M., Smith, R. and Castle, A. (2003) Bacteriophages of Erwinia amylovora. Applied and Environmental Microbiology 69, 2133–2138. Kabaluk, J.T., Svircev, A.M., Goettel, M.S. and Woo, S.G. (2010) The use and regulation of microbial pesticides in representative jurisdictions worldwide. Available at: http://www.IOBC-Global.org (accessed 10 October 2012). Lehman, S.M. (2007) Development of a bacteriophage-based biopesticide for fi re blight. PhD thesis, Brock University, St Catharines, Ontario. McGhee, G.C., Guasco, J., Bellomo, L.M., Blumer-Schuette, S.E., Shane, W.W., Irish-Brown, A. and Sundin, G.W. (2011) Genetic analysis of streptomycin-resistant (Sm-R) strains of Erwinia amylovora suggests that dissemination of two genotypes is responsible for the current distribution of Sm-R E. amylovora in Michigan. Phytopathology 101, 182–191. Roach, D.W. (2011) Erwinia amylovora bacteriophage resistance. PhD thesis, Brock University, St Catharines, Ontario. Roach, D.W., Sjaarda, D., Castle, A.J. and Svircev, A.M. (2011) Bacteriophages as biopesticides: role of bacterial exopolysaccharides. Acta Horticulturae 896, 449–455. Russo, N.L., Burr, T.J., Breth, D.I. and Aldwinckle, H.S. (2008) Isolation of streptomycin-resistant isolates of Erwinia amylovora in New York. Plant Disease 92, 714–718. Sholberg, P.L., Bedford, K.E., Haag, P. and Randall, P. (2001) Survey of Erwinia amylovora isolates from British Columbia for resistance to bactericides and virulence on apple. Canadian Journal of Plant Pathology 23, 60–67. 412 Chapter 62

Sjaarda, D.R. (2012) Role of exopolysaccharides and monosaccharides in Erwinia amylovora resistance to bacteriophages. MSc thesis, Brock University, St Catharines, Ontario. Svircev, A.M., Smith, R., Gracia-Garza, J.A., Gill, J.J. and Schneider, K. (2002) Biocontrol of Erwinia with bacteriophages. Bulletin OILB/SROP Working Group ‘Biological Control of Fungal and Bacterial Plant Pathogens’, Proceedings of the meeting Infl uence of A-Biotic and Biotic Factors on Biocontrol Agents at Pine Bay, Kusadasi (Turkey), 22–25 May 2002 25(10), 139–142. Svircev, A.M., Castle, A.J. and Lehman, S.M. (2010) Bacteriophages for control of phytopathogens in food production systems. In: Sabour, P.M. and Griffi ths, M.W. (eds) Bacteriophages in the Control of Food- and Waterborne Pathogens. ASM Press, Washington, pp. 79–102. Svircev, A.M., Lehman, S.M., Roach, D. and Castle, A.J. (2011) Phage biopesticides and soil bacteria: multilayered and complex interactions. In: Witzany, G. (ed.) Biocommunications in Soil Microorganisms. Springer-Verlag, Berlin Heidelberg, Soil Biology 23, 215–235.

62 Fusarium graminearum Schwabe (teleomorph Gibberella zeae (Schwein.) Petch.), Fusarium Head Blight Disease (Nectriaceae)

Jianwei He,1,2 Greg J. Boland1 and Ting Zhou2 1University of Guelph, Guelph, Ontario; 2Agriculture and Agri-Food Canada, Guelph, Ontario

62.1 Pest Status (Nectriaceae), can also cause FHB in North America (Clear and Patrick, 2010). Fusarium head blight (FHB, scab) on Fusarium graminearum not only causes wheat, Triticum spp. (Poaceae), and serious crop damage but also produces Gibberella ear rot on maize, Zea mays L. mycotoxins such as zearalenone and (Poaceae), are two of the most econom- trichothecenes (most commonly, deoxyni- ically important crop diseases in Canada. valenol or DON), creat ing food safety risks The most prevalent causal agent of these (Nelson et al., 1993; Canadian Grain two diseases is the fungus Fusarium Commission, 2008). graminearum Schwabe (teleomorph: Gib- The characteristic disease symptom of berella zeae (Schwein.) Petch.) (Nectria- Gibberella ear rot of maize is the pink ceae). Other Fusarium spp., for example F. mould in/on kernels. In infected wheat, culmorum (Wm. G. Sm.) Sacc, F. avena- the fi rst characteristic symptom of FHB is ceum (Fries) Saccardo and F. crook- bleaching on spikelets, which can develop wellense Burgess, Nelson & Toussoun early after fl owering. As the disease

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 62 413

progresses, the bleaching can spread to the Larsen et al., 2004; Llorens et al., 2004; entire head. White or pinkish mould can Ramirez et al., 2004, 2006; Beyer et al., be found on the rachis and glumes of 2005). Germination of ascospores and spikelets under moist and warm macroconidia required a minimum relative conditions. humidity (RH) of 53% and 80%, respect- Fusarium graminearum overwinters on ively. DON production increased as the RH plant debris and in soil as perithecia and increased (Beyer et al., 2005). Tempera- sporodochia, which release ascospores and tures that allow two Argentinean strains of macroconidia, respectively, which are the F. graminearum to grow at a water activity most important inoculum sources of (_w) of 0.900 were in the range 15–25°C. Fusarium. Hyphae and chlamydospores At 25°C, the range of _w for optimal F. can also serve as inoculum. Wind, rainfall, graminearum growth was 0.950–0.995 and insects and birds play important roles in the _w for maximum growth was at 0.995. dispersion of these spores. Usually, infec- DON production was dependent on both tion of maize ears and wheat spikes occurs temperature and _w. The range of _w for at anthesis and silking, respectively. As optimal DON production was 0.950–0.995. the growth progresses of the pathogen on DON was produced more rapidly at 25°C infected wheat spikes, seeds, maize ears, than at other temperatures tested, how- leaf sheaths and stems, ascospores and ever, the maximum amount was detected macroconidia are produced and will at 30°C with an _w of 0.995 (Ramirez et al., become the inoculum for secondary infec- 2006). tions (Sutton, 1982). Infection and colonization can occur right after inoculum becomes attached to 62.2 Background the susceptible plant organs if the environ- mental conditions are warm, windy and 62.2.1 Cultivation practices humid. After ascospores or macroconidia of the pathogen are deposited on wheat Agriculture practices such as crop rotation, spikes and germinate, hyphae can develop soil tillage, fertilizer applications and on the surfaces of fl orets and glumes to insect control infl uence Fusarium infection form a mycelial network, which then and mycotoxin production (Obst et al., grows toward stomata, penetrates and 1997; Schaafsma et al., 2001; Edwards, colonizes the ovary, and then infects fl oral 2004). Crop rotation can reduce the inci- bracts (Pritsch et al., 2000). Wheat is most dence of FHB and reduce DON con- susceptible to infection at the fl owering tamination of grains (Obst et al., 1997; stage (Bai and Shaner, 1994). Choline in Dill-Macky and Jones, 2000; Schaafsma et fresh anthers stimulates conidial germin- al., 2001; Maiorano et al., 2008). Soil ation and elongation of germ tubes of F. tillage reduced FHB by removal, graminearum (Li and Wu, 1994). In maize, destruction or burial of infected crop the silking stage of plant development is residues (Obst et al., 1997; Dill-Macky and sensitive to infection and the infection is Jones, 2000). Fertilizer can also infl uence similar to that of wheat. In addition, disease severity of FHB and DON content wounds made on maize by insects and in crops. Disease incidence of FHB birds also aid infection. Trichothecene increased as the amount of nitrogen fertil- myco toxins have phytotoxic effects on izer was increased. Furthermore, different plant tissues and contribute to virulence of forms of nitrogen fertilizers can also affect Fusarium spp. (Desjardins et al., 1996). disease severity of FHB and DON pro- Warm and moist environmental con- duction (Teich, 1987; Martin et al., 1991; ditions favour both infection and myco- Yi et al., 2001). Consequently, Blandino et toxin production by the pathogen F. al. (2008) suggested that a balanced N graminearum (Martins and Martins, 2002; fertilizer application might ensure low 414 Chapter 62

incidence and severity of FHB and reduced 62.2.3 Chemical control production of mycotoxins. Weed and insect management may also reduce severity of Fungicides prothioconazole, chlorothalanil, FHB (Holmes, 1983; Teich and Nelson, tebuconazole and metconazole are cur- 1984; Jenkinson and Parry, 1994). Some rently registered for management of FHB evidence has shown that insect control can on wheat, maize, barley, Hordeum vulgare result in reduced Gibberella ear rot in L., oats, Avena sativa L., rye, Secale cereale maize and contamination by several L., and triticale, × Triticale hexaploide Lart. mycotoxins (Munkvold et al., 1999; Bakan (Poaceae), in Canada (Health Canada, et al., 2002; Schaafsma, 2002). 2012). Some of these registered pesticides have also claimed reduction of DON levels in treated crops (Pest Management Regu- 62.2.2 Breeding for FHB resistance latory Agency, 2006, 2007, 2011). The lack of effi cient and consistent Wheat, Triticum aestivum L. (Poaceae), mycotoxin reduction may be considered as cultivars resistant to FHB have been widely a possible drawback of chemical control, as used as parents in breeding in China, applications of pesticides have not always Japan, the USA and other countries (Bai resulted in suppression of FHB disease and Shaner, 2004), and resistance in wheat development and/or reduction of myco- to FHB has been improved with new toxin production. In some cases, stimu- breeding strategies (Bai and Shaner, 2004). lation of mycotoxin production was Transgenic techniques have also been used observed (D’Mello et al., 1998; Simpson et for enhancing FHB resistance. A rice al., 2001; Magan et al., 2002; Ramirez et thaumatin-like protein gene was trans- al., 2004; Blandino et al., 2006). Fungicide ferred into wheat and the resulting plants activities, i.e. control of FHB disease and developed FHB symptoms more slowly reduction of mycotoxin, were infl uenced (Chen et al., 1999). The gene FsTri101 by interactions among water activity, encoding trichothecene acetyltransferase temperature, fungicide concentrations and was inserted to the regenerable wheat time of inoculation (Ramirez et al., 2004). cultivar ‘Bobwhite’. Transformed plants Reduction of growth of Fusarium or FHB resisted the spread of F. graminearum in disease severity by fungicides was not inoculated wheat heads; consequently, always associated with reduction in myco- these plants had signifi cantly less disease toxin production in the fi eld (Edwards et and mycotoxin content than the non- al., 2001; Ioos et al., 2005). These results transformed parents (Okubara et al., 2002). indicate that chemical control is not However, commercial wheat cultivars that consistently effective, and that the are highly resistant to FHB are not cur- suppression of FHB by fungicides is not rently available (Bushnell et al., 1998; Bai always associated with reduced DON et al., 2000; Hollins et al., 2003). Moreover, levels in grains. the development of transgenic techniques is limited by public concerns associated with transgenic plants (Bai and Shaner, 62.3 Biological Control Agents 2004). Current research about quantitative trait loci (QTL) mapping and marker- Biological control is a promising approach assisted selection for FHB resistance in for the management of FHB, especially in wheat was recently reviewed (Buerstmayr cases where the target pathogens are et al., 2009). Discovery of more diagnostic resistant to fungicides (Schisler et al., markers for the most repeatable QTL 2002a; da Luz et al., 2003; Khan et al., associated with resistance genes will aid 2004). Biological control agents for FHB the adoption of marker-assisted selection have been developed based on two control by plant breeders. strategies: (i) reduction of inoculum from Chapter 62 415

soil and crop residues; and (ii) inhibition 62.3.1.2 Inhibition of colonization of pathogen colonization and disease Cryptococcus sp. OH 71.4 and Crypto- development on crops. coccus nodaensis Sato et al. (Tremellaceae) OH 182.9 reduced FHB severity on a tested 62.3.1 Fungi wheat cultivar ‘Renville’. Cryptococcus sp. OH 71.4 and C. nodaensis OH 182.9 62.3.1.1 Reduction of inoculum from soil and reduced disease severity by 57% in fi eld crop residues trials conducted in Peoria, Illinois, and Cryptococcus sp. OH 181.1 reduced Infested crop residues are the main disease severity by 59% in Langdon, North inoculum source for epidemics of FHB Dakota. However, none of these tested (Sutton, 1982), and the fungal antagonists strains reduced the DON content of grain Trichoderma harzianum Rifai (Hypocreae- in the trial in Peoria. From these tests, the ceae), Microsphaeropsis sp. (Montagnula- yeasts Cryptococcus sp. OH 71.4, Crypto- ceae) and Clonostachys rosea f. rosea coccus sp. OH 181.1 and C. nodaensis OH (Link) Schroers et al. (Bionectreaceae) have 182.9 were likely the most promising been evaluated for effi cacy in reducing antagonists to reduce FHB on durum perithecial and ascospore production of F. wheat, Triticum durum Desf. (Poaceae), in graminearum on wheat, oat and maize in the fi eld (Schisler et al., 2002b). The same laboratory and fi eld conditions (Fernandez, research group conducted a series of fi eld 1992; Bujold et al., 2001; Luongo et al., trials in different locations in the USA 2005; Inch and Gilbert, 2007). In fi elds of from 1998 to 2000 (Schisler et al., 2002b; wheat and black oat treated with T. Khan et al., 2004). The three Cryptococcus harzianum, incidence of F. graminearum species/strains also reduced disease on straw residues was signifi cantly lower severity in most trials. The most effi cient (19–21% in wheat and 27–49% in black treatment was C. nodaensis OH 182.9, oat) than untreated fi elds (63–68% in which reduced disease severity by 55% wheat and 53–60% in black oat) (Schisler et al., 2002b; Khan et al., 2004). (Fernandez, 1992). In wheat crops where Clonostachys rosea is a potential straw residue was treated postharvest with biological control agent for reduction of a T. harzianum conidial suspension, pro- inoculum, but can also inhibit duction of perithecia of G. zeae was colonization and disease development on reduced by up to 96% at 30 days and 92% crops. When sprayed on wheat heads, this at 60 days following the treatment (Inch fungal antagonist signifi cantly reduced and Gilbert, 2007). infected spikelets by 64%, and Fusarium- Microsphaeropsis sp. signifi cantly damaged kernels by 65% in greenhouse reduced ascospore production by F. grami- conditions; and FHB index by 58%, nearum on wheat and maize residues. infected spikelets by 46%, Fusarium- Immature and/or mature perithecia formed damaged kernels by 49% and DON level on spikelets and straw were found to be in kernels by 21% in fi eld conditions (Xue signifi cantly reduced after treatments with et al., 2009). Microsphaeropsis sp. under different application conditions (Bujold et al., 2001). In a separate study, C. rosea was the most promising biological control agent tested in 62.3.2 Bacteria several experiments, and signifi cantly inhibited the sporulation of several 62.3.2.1 Inhibition of colonization Fusarium spp. on wheat straw and maize Bacillus subtilis (Ehrenberg) Cohn (Bacil- stalks in bio-assays, as well as the laceae) AS 43.3, B. subtilis AS 43.4 and B. colonization of stalk pieces under fi eld subtilis OH 131.1 reduced FHB disease conditions (Luongo et al., 2005). severity on wheat by up to 95% in 416 Chapter 62 greenhouse and fi eld evaluations (Schisler 62.4 Evaluation of Biological Control et al., 2002a). In greenhouse experiments, B. subtilis AS 43.3 and B. subtilis AS 43.4 FHB can be a challenging disease to reduced FHB severity on cultivar ‘Ren- manage and currently relies on an ville’, and three of the four microorganisms integrated approach of several methods. tested reduced severity on cultivar ‘Ben’. Biological controls can contribute to man- The most effi cient treatment that reduced agement of this disease, particularly when disease severity by 90% was with B. fungicide resistance is present, or fungi- subtilis strain AS 43.3 (Schisler et al., cides are not available. Currently, no bio- 2002b; Khan et al., 2004). The antifungal logical pesticides are registered for FHB activities of two strains of Lactobacillus but research has resulted in several bac- plantarum (Orla-Jensen) Bergey et al. terial and fungal organisms that are effec- (Lactobacillaceae) against Fusarium spp. tive under experimental conditions (both were studied in laboratory-scale malting of greenhouse and/or fi eld). Applications of naturally contaminated barley. Lactobacil- biological control agents to foliage and lus plantarum E76 reduced contamination crop debris, and during crop processing are of strains of F. graminearum, F. avena- being compared as strategies to improve ceum, F. culmorum and F. oxysporum control effi cacy. Schlechtend (Nectriaceae) by more than Current methods for the control of FHB 20% over 3 years of evaluations. However, rely primarily on cultural practices and in the fourth year of the evaluations, the foliar applications of fungicides, and these effi cacy of the treatment with L. plantarum practices have been increasingly effective was limited because of heavy contamin- in reducing disease incidence, disease ation with Fusarium spp. on the barley severity and/or the concentration of DON (Laitila et al., 2002). A bacterial antagonist, in harvested grains. However, the effi cacy Lysobacter enzymogenes Christensen and of these practices can be infl uenced by Cook (Xanthomonadaceae) strain C3, pro- weather, pesticide application, fungicide duced lytic enzymes and caused induced deposition and effi cacy etc., and these resistance to FHB (Jochum et al., 2006). In practices need to be integrated with other greenhouse experiments, chitin broth cropping practices and disease prediction cultures of this strain reduced FHB severity models. to less than 10%, whereas disease sever- In contrast, the development of resistant ities in the control treatments were above crop varieties and biopesticide products 80%. are in earlier stages of research and In a unique approach, more than 250 develop ment, and resistant crop varieties microbial isolates were assessed using up or effective biopesticides are not yet to fi ve in vitro assays including: a co- registered for FHB in Canada. However, culture and dual-culture assay, an indirect research is progressing rapidly towards impedance assay, a wheat fl oret assay, and making such products available. assays assessing DON pro duction on whole wheat fl our and wheat fl orets, respectively (He et al., 2009). Two Paenibacillus poly- 62.5 Future Needs myxa (Prazmowski) Ash et al. Future research should: (Paenibacillaceae) isolates reduced colon- ization of wheat heads by F. graminearum 1. Continue to identify and develop in- by 58.8% and 62.4%, disease severity by novative strategies for biopesticide 56.5% and 55.4%, DON pro duction by development. Such new strategies must 84.8% and 89.4%, and increased evaluate potential biopesticide pro ducts 100-kernel weights by 56.6 and 66.9%, concurrently for both reduction of FHB respectively, in a greenhouse evaluation incidence and/or severity, and DON con- (He et al., 2009). centration, as the effi cacy of some products Chapter 62 417

has been shown to affect these vari ables applied accurately to the target site of fl ow- differentially. This is an important con- ering wheat heads); sideration during the assessment stages for 3. Work towards commercial-scale pro- identifying promising biopesticide organ- duction and formulation, and registration isms for FHB; of products. The increasing number of 2. Emphasize the feasibility of integrating commercial biopesticides that have those biopesticides that appear to be prom- become available in recent years has con- ising at early stages of research into the tributed to an expanding expertise in these crop production and disease management areas. The identifi cation of specifi c genes practices of individual crops because this associated with mechanisms of action of integration will often require selection of individual biopesticides would also enable some strategies over others, such as the use improved understanding of such traits, of fungicides or fungal biopesticides, and the development of more-rapid and unless these products can be integrated to high-throughput systems for detection of achieve an additive effect on suppression favourable combinations of genes in iso- of FHB or DON (additional effort will need lates recovered from environmental sam- to be placed on sprayer technology to ples. ensure fungicides or biopesticides can be

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63 Heterobasidion irregulare Garbel. & Otrosina, Annosus Root Rot (Bondarzewiaceae)

Gaston Lafl amme1 and Mike T. Dumas2 1Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec; 2Natural Resources Canada, Canadian Forest Service, Great Lake Forestry Centre, Sault Ste Marie, Ontario

63.1 Pest Status in 1989 approximately 40 km from the Larose Forest (Lafl amme and Blais, 1993). The annosus root disease, Heterobasidion From the fi rst infection in southern Ontario irregulare Garbel. & Otrosina (Bondarze- until its most northern observation at wiaceae), attacking pines, Pinus spp. Saint-Jean-de-Matha, Quebec, in 2007, the (Pinaceae), was fi rst diagnosed and disease has spread northward at an annual described by Hartig (1874) in Europe. He rate of 10 km (Lafl amme, 2011). demonstrated that the disease is trans- The fungus Heterobasidion irregulare mitted from tree to tree by root contact, (Otrosina and Garbelotto, 2010), known creating characteristic ‘circles of mortality’ until recently under the name of the most (Hartig, 1900). In eastern Canada, the common European species H. annosum disease was fi rst detected at St Williams, (Fries) Brefeld (=Fomes annosus (Fries) southern Ontario, in 1955. It was infecting Cooke), is a causal agent of annosus root a red pine plantation thinned 26 years rot in North America (Linzer et al., 2008). previously (Jorgenson, 1956). In 1968, the In Canada, it is restricted to Quebec and root disease was detected in Larose Forest Ontario. The behaviour of the other species near Ottawa (Lafl amme, 1994). In Quebec, found in western Canada, H. occidentalis the fi rst case of this disease was discovered Otrosina & Garbelotto (Bondarzewiaceae),

© CAB International 2013. Biological Control Programmes in Canada 2001–2012 (eds P.G. Mason and D.R. Gillespie) Chapter 63 421

is quite different from H. irregulare; it window of opportunity varies depending causes a heart rot of roots and basal stem. on host and climate and can range from a Recently, other new species have also been few days to 3 or 4 weeks. However, infec- described in Europe (Niemelä and tion rarely occurs more than 2 weeks after Korhonen, 1998), H. parviporum Niemelä felling (Hodges, 1969). & Korhonen (Bondarzewiaceae) on spruce, Picea spp. (Pinaceae), and H. abietinum Niemelä & Korhonen (Bondarzewiaceae) 63.2 Background on fi r, Abies spp. (Pinaceae). Because Heterobasidion spp. cause extensive dam- Mechanical eradication of infected trees age worldwide, this genus is considered to has been the sole method to partially stop include some of the most destructive the spread of H. annosum. As of 2011, no pathogens in evergreen forests. commercial formulations, chemical or bio- Disease caused by the species of the logical, were registered for use in Canada. genus Heterobasidion occurs in over 170 Rishbeth (1963) was the fi rst to experiment tree species worldwide. Although the successfully with biological control against extent of damage varies with species, the H. annosum. He observed that untreated greatest damage occurs in conifers. In stumps were often colonized by the sapro- eastern Canada, red pine, Pinus resinosa phytic fungus Phlebiopsis gigantea (Fries) Ait. (Pinaceae), is the most affected Jülich (=Peniophora gigantea (Fries) species, but all pine species can be Massee) (Phanerochaetaceae). Once estab- affected. Other species growing near red lished, this fungus prevented H. annosum pines infected with H. irregulare, such as from infecting the stump. Phlebiopsis balsam fi r, Abies balsamea (L.) Mill. gigantea has the additional advantage of (Pinaceae), have also been found to be producing large quantities of spores when infected with the pathogen but they do not cultivated in the laboratory. Like many appear to be hosts for primary infections other woodrotting fungi, P. gigantea on stumps. spreads by spores produced on fruiting Rishbeth (1951) discovered that H. bodies made of a thin and porous layer on annosum becomes established in a stand the surface of the substratum colonized by by spores that colonize freshly cut stumps. the fungus. This resupinate form of fruiting Heterobasidion irregulare spreads the same body produces millions of spores. way. The discovery of this key element in Although other potential microorganisms the propagation of the disease made it have been tested (Holdenrieder and Greig, possible to develop methods aimed at 1998), P. gigantea is the only one that has controlling its introduction into forests been commercialized (Korhonen et al., through stump treatment. Various chemical 1994). products were then tested and Rishbeth Although the North American and (1963) was the fi rst to use biological European strains of P. gigantea show some control, with promising results. differentiation, they can be regarded as The basidiospores are capable of belonging to the same species (Grillo et al., travelling long distances. Rishbeth (1959) 2005). The isolates of P. gigantea used for found viable spores over the ocean more the Verdera formulation Rotstop, registered than 300 km from the closest possible in a few European countries (Korhonen et source of infection. After being transported al., 1994), could thus be used in North by wind, the basidiospores settle on freshly America. But to reduce the impact on cut stump surfaces and germinate. Such microbial biodiversity in Canada, a com- surfaces are selective for a number of mercial formulation for use in eastern microorganisms, including H. irregulare. Canada should be produced with a Therefore, spores must colonize the stump Canadian isolate, and could also make it surface soon after the tree is felled and easier to register the biological product. before other microorganisms move in. The Moreover, an isolate selected in the same 422 Chapter 63

ecological region where it will be used 30°C. Finally, Dumas and Lafl amme (2012, would be better adapted to the hosts and to Sault Ste Marie, unpublished data) were climatic conditions. able to inoculate H. irregulare on fresh jack pine, Pinus banksiana Lamb. (Pinaceae), stumps, which means that H. 63.3 Biological Control Agents irregulare can establish in P. banksiana stands. In western Quebec, Bussières et al. (1996) In northern Europe, spruce and pine evaluated the potential of P. gigantea for stumps can be colonized by H. parviporum use in P. resinosa plantations to control and H. annosum, respectively. Both tree annosus root rot. Their results showed that species are treated with P. gigantea to P. gigantea colonized the majority of P. prevent Heterobasidion colonization. In resinosa stumps 12 months following eastern Canada, only pine stumps have to application of the inoculum. Natural be treated as only H. irregulare, the colonization of stumps by P. gigantea did equivalent of the European H. annosum, is not provide adequate protection against present. infection by H. irregulare. However, the application of P. gigantea on the fresh stumps ensures its presence there and 63.4 Future Work results in a more extensive colonization of this saprophyte. Lafl amme and Dumas Future work should include: (2007) have done an effi cacy trial with two Canadian isolates in four P. resinosa 1. Formulate and commercialize a Can- plantations and both isolates colonized all adian isolate of P. gigantea for use on pine 120 stumps per isolate inoculated without stumps of all species; any presence of H. irregulare on treated 2. Test the effi cacy of the Canadian isolate ones while 12% of the untreated stumps formulation on pine species other than P. were colonized by H. irregulare. Dumas resinosa, for registration purposes; (2011) demonstrated that the effi cacy of P. 3. Adapt techniques used in the Scandin- gigantea could be enhanced when ammo- avian countries to apply the biological con- nium lignosulfonate was added to spore trol product; suspensions and inoculated in P. resinosa 4. Evaluate manual treatment for small- stumps. This is a real advantage when scale operations, and devices that can be stump treatments are performed under fi tted on a tree harvester, making the treat- extreme conditions (hot, sunny and dry) ment completely mechanized for largescale because spore germination occurs in 8 h at operations (Thor, 1997).

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Hodges, C.S. (1969) Modes of infection and spread of Fomes annosus. Annual Review of Phytopathology 7, 247–266. Holdenrieder, O. and Greig, B.J.W. (1998) Biological Method of Control. In: Woodward, S., Stenlid, J., Karjalainen, R. and Hüttermann, A. (eds) Heterobasidion annosum: Biology, Ecology, Impact and Control. CAB International, Wallingford, UK, pp. 235–258. Jorgenson, E. (1956) Fomes annosus (Fr.) Cke. on red pine in Ontario. Forestry Chronicle 32, 87–88. Korhonen, K., Lipponen, K., Bendz, M., Johansson, M., Ryen, L., Venn, K., Seiskari, P. and Niemi M. (1994) Control of Heterobasidion annosum by stump treatment with ‘Rotstop’, a new commercial formulation of Phlebiopsis gigantea. In: Johansson, M. and Stenlid, J. (eds) Proceedings of the Eighth International Conference on Root and Butt Rot, Sweden and Finland, 9–16 August 1993, pp. 675–685. Lafl amme, G. (1994) Annosus root rot caused by Heterobasidion annosum. Natural Resources Canada, Canadian Forest Service, Quebec Region, Information Leafl et LFC 27. Lafl amme, G. (2011) Spread of Heterobasidion irregulare in eastern Canada towards northern natural forests of Pinus banksiana. Proceedings of XIII Conference – Root and Butt Rots of Forest Trees, IUFRO WP-7.01.01. September 2011, Florence, Italy (in press). Lafl amme, G. and Blais, R. (1993) Première mention de Heterobasidion annosum au Québec. Phytoprotection 74, 171. Lafl amme, G. and Dumas, M.T. (2007) Development of a biological treatment with Phlebiopsis gigantea for the control of the root rot pathogen Heterobasidion annosum and impact of microbial biodiversity. Internal Report: Enhanced Pest Management Methods, Science and Technology Program. Canadian Forest Service, Natural Resources Canada. Linzer, R.E., Otrosina, W.J., Gonthier, P., Bruhn, J., Lafl amme, G., Bussières, G. and Garbelotto, M. (2008) Inferences on the phylogeography of the fungal pathogen Heterobasidion annosum, including evidence of interspecifi c horizontal genetic transfer and of human-mediated, long- range dispersal. Molecular Phylogenetics and Evolution 46, 844–862. Niemelä, T. and Korhonen, K. (1998) Taxonomy of the Genus Heterobasidion. In: Woodward, S., Stenlid, J., Karjalainen, R. and Hüttermann, A. (eds) Heterobasidion annosum: Biology, Ecology, Impact and Control. CAB International, Wallingford, UK, pp. 27–33. Otrosina, W.J. and Garbelotto, M. (2010) Heterobasidion occidentale sp. nov. and Heterobasidion irregulare nom. nov.: a disposition of North American Heterobasidion biological species. Fungal Biology 114, 16–25. Rishbeth, J. (1951) Observations on the biology of Fomes annosus with particular reference to East Anglian pine plantations. II. Spore production, stump infection, and saprophytic activity in stumps. Annals of Botany 15, 1–21. Rishbeth, J. (1959) Dispersal of Fomes annosus Fr. and Peniophora gigantea (Fr.) Massee. Transactions of the British Mycological Society 42, 243–260. Rishbeth, J. (1963) Stump protection against Fomes annosus III. Inoculations with Peniophora gigantea. Annals of Applied Biology 52, 63–77. Thor, M. (1997) Stump treatment against Heterobasidion annosum: techniques and biological effect in practical forestry. Licentiate’s dissertation, SkogForsk, Science Park, Uppsala, Sweden. 424 Chapter 64

64 Monilinia vaccinii-corymbosi (Reade) Honey, Mummy Berry (Monilinia Blight) (Sclerotiniaceae)

James A. Traquair,1 Paul D. Hildebrand,2 Donna H. Langdon3,4 and Greg J. Boland4 1Agriculture and Agri-Food Canada, London, Ontario; 2Agriculture and Agri-Food Canada, Kentville, Nova Scotia; 3Brampton, Ontario; 4University of Guelph, Guelph, Ontario

64.1 Pest Status tends to be more severe in lowbush blueberry than in highbush blueberry. Mummy berry disease caused by Monilinia Conidia are produced on grey-coloured vaccinii-corymbosi (Reade) Honey (Sclero- tufts on the blighted tissues and secondary tinia ceae) attacks both highbush, Vacci- infection occurs during the bloom period. nium corymbosum L., and lowbush, V. Conidia are dispersed by blowing rain and angustifolium Aiton (Ericaceae), blue- insects, germinate on stigmas, and grow berries in Canada and the USA (Caruso and down the styles into the ovaries of open Ramsdell, 1995). The disease can be very fl owers (Caruso and Ramsdell, 1995). In- severe depending on levels of inoculum fected ovaries develop into mummy berries and environmental conditions. The fi rst that become salmon-pink, shrivelled and symptom in the spring (late April to early hard as ripening ensues later in the May) is a drooping of shoots and leaves summer. These mummifi ed fruits drop to followed by a blighting (browning) of the the ground and overwinter in the leaf litter. midrib and lateral veins of leaves (Caruso They can survive several growing seasons and Ramsdell, 1995). Shoots, leaves and in undisturbed blueberry fi elds (Caruso developing fl ower clusters are killed and Ramsdell, 1995). The mummy berry shortly after discoloration appears and phase tends to be more severe in highbush usually drop off. This early primary infec- blueberry than in lowbush blueberry. tion is caused by ascospores released from stalked apothecia produced on over- wintered mummifi ed berries (pseudo- 64.2 Background sclerotia). Cold (2–14°C), wet conditions are required for ascospore germination and Preventative, non-biological control of infection, both of which can be stimulated blight and mummy berry disease in by frost damage to blueberry tissues lowbush blueberry is focused on the (Hildebrand and Braun, 1991). This phase destruction of inoculum in leaf litter by the of the disease is often referred to as burning of new blueberry sites (Caruso and Monilinia blight and the resulting crop loss Ramsdell, 1995). Pruning with fi re can be

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 64 425

an effective cultural practice for reducing organisms is illustrated in studies of the the viability of mummy berries in lowbush suppression of Alternaria fruit rot and blueberry fi elds (Lambert, 1990). Burn Colletotrichum anthracnose by Burk- pruning was traditionally practised for holderia cepacia (Palleroni & Holmes) many decades by spreading straw and Yabuuchi et al. (Burkholderiaceae) and igniting it to allow a free burn, or by several bacteria, yeasts and fungi washed tractor-drawn fl ame throwers known as from highbush blueberry surfaces in New Woolery blueberry burners. However, in Jersey (Stretch, 1988) and by studies of the the late 1980s fl ail mowing began to biological control of anthracnose and fruit replace burning as a pruning practice and rot by fruit-borne wild yeasts in Michigan by the 2000s there were very few fi elds that (Sabaratnam et al., 2004). were burn-pruned. The benefi ts of burning for control of mummy berry and several other diseases, insects and weeds are now 64.3 Biological Control Agents being rediscovered by growers. Growers are beginning to use sickle bar mowers to Published research on the biological cut the blueberry stems during the autumn control of blueberry diseases deals mainly and then ignite the debris during the with problems on highbush blueberry following spring to obtain a cost-effective where conidial infection of fruit by Alter- free burn. naria tenuissima (Kunze) Wiltshire (Pleop- The management of ascospore germin- sporaceae), of stems and fruit by ation and leaf infection entails the timely Phomopsis vaccinii Shear, N.E. Stevens & applications (usually two) of fungicide H.F. Bain (Diaporthaceae), of fruit by (triforine or propiconazole) in early spring Colletotrichum acutatum J.H. Simmonds at vegetative bud break and during early and C. gloeosporioides (Penz.) Penz. & bloom stages (Caruso and Ramsdell, 1995). Sacc. (Glomerellaceae), and of shoots and A forecast of potential Monilinia blight fruit by M. vaccinii-corymbosi are sup- severity based on fi eld temperature and pressed by the application of bacteria, moisture is used to guide timing of hyphomycetous fungi or wild yeasts. fungicide applications (Hildebrand and Burkholderia cepacia and Pseudomonas Braun, 1991; Hildebrand and McRae, syringae Van Hall (Pseudomonadaceae) 1995). Fungicides are used also in the were effective bacterial antagonists of management of this disease in highbush Alternaria fruit rot in storage in New Jersey blueberry, but in this case, secondary (Stretch, 1988). Aureobasidium pullulans infection of fl owers by conidia is the focus (de Bary) G. Arnuad (Dothioraceae) and (Caruso and Ramsdell, 1995). Clean tillage Cryptococcus magnus (Lodder & Kreger) of soil in highbush blueberry fi elds Baptist & Kurtzman (Tremellaceae) were involves light surface cultivation and reported to be good yeasts for the disturbance of mummy berries and apoth- inhibition of P. vaccinii and C. acutatum in ecial rhizoids causing apothecia to shrivel vitro and on stored fruit in Michigan and die (Caruso and Ramsdell, 1995). (Sabaratnam et al., 2004; Jordon et al., Biological control of the ascospore and 2006). Isolation of wild yeasts on leaves conidial phases of mummy berry disease in and fruit of highbush blueberry in Ontario lowbush blueberry have received only and identifi cation using molecular tech- limited research attention (Langdon, 2008). niques showed a wide range of pink and Overwintered mummy berries that produce white yeasts. Many of these yeasts have the apothecia in leaf litter and soil would be potential to be blueberry disease antagon- the targets of attack by antagonistic bacteria ists such as species of Rhodotorula and fungi. Ascospores and conidia are the (incertae sedis), Sporobolomyces (Spori- targets of antagonism by bacteria and fungi dio bolaceae), Cryptococcus and Bullero- on developing leaves and fl owers. The myces (Tremellaceae) (Traquair et al., antagonistic potential of epiphytic micro- 2012). More wild yeasts were found on 426 Chapter 64 fruit than on leaves and pink basidio- 64.4 Evaluation of Biological Control mycetous yeasts predominated over white basidiomycetous yeasts. Gliocladium Yeasts and bacteria have been tested as catenulatum J.C. Gilman and E.V. Abbott biological control agents for Monilinia (Hypocreaceae) formulated as Prestop® blight of lowbush blueberry in Canada. and Trichoderma harzianum Rifai (Hypo- Two wild yeasts were the only isolates of creaceae) formulated as PlantShield® were 24 yeasts and 24 bacteria from washings of shown to be effective commercial bio- shoots and fruit surfaces that were capable fungicides for Colletotrichum anthrac nose of reducing Monilinia blight incidence by on potted and fi eld-grown highbush 50% or greater on lowbush blueberry leaf blueberry plants in British Columbia buds after artifi cial inoculation with (Verma et al., 2006). Early work on ascospore suspensions and incubation at mummy berry biological control in the 10°C for 24 h and then at 20°C for 9–10 fi eld using sprays of Gliocladium roseum days in controlled environment chambers Bainier and Trichoderma viride Pers. (Langdon, 2008). These antagonistic yeasts (Hypocreaceae) applied to fl owering high- were identifi ed using molecular tech- bush blueberry plants in the Pacifi c niques, i.e. modifi ed whole cell DNA Northwest over a 2-year period showed amplifi cation, sequencing of D1/D2 gene disease reduction but failed to prevent domains of the large rDNA subunit and major crop loss (Bristow and Windham, BLAST searches in GenBank (Lachance et 1995). Bacillus subtilis (Ehrenberg) Cohn al., 1999) as Cryptococcus victoriae (Bacillaceae) formulated as Serenade® Montes et al. (Tremellaceae) and (strain QRD137) was reported to be a very Rhodotorula graminis DiMenna (incertae promising biofungicide for control of sedis) (Langdon, 2008). Cold-tolerant mummy berry in Georgia based on bac- strains of these two yeasts suppressed terial applications to detached highbush Monilinia blight on lowbush blueberry blueberry fl owers subsequently inoculated shoots incubated at 10°C in controlled with conidia (Scherm et al., 2004). This environment chambers (Langdon, 2008; effi cacy was confi rmed in highbush blue- Traquair et al., 2012). Various bacteria and berry fi elds (Dedej et al., 2004) by using other yeast species (Traquair et al., 2012) caged plants and bumblebees to deliver B. were antagonistic to growth of various subtilis to blueberry fl owers. Recent fungi in vitro at 24°C but were ineffective research highlights the strong potential for at suppressing disease on plants in the B. subtilis formulated as Serenade® Max to fi eld largely because of their inability to biologically control Monilinia shoot blight grow at low temperatures (Langdon, 2008; and mummy berry of lowbush (wild) Traquair et al., 2012). blueberry in Nova Scotia, Canada (Langdon Three bacteria and three fungi formu- et al., 2006; Langdon, 2008). lated as registered biofungicide products Chemical residues resulting from available in Canada and/or the USA were fungicidal disease control have the poten- evaluated for the suppression of Monilinia tial to be barriers to export of blueberries blight in lowbush blueberry under con- and blueberry products to some countries. trolled environment and fi eld conditions at Biofungicides such as Serenade® Max will three sites in Nova Scotia (Langdon et al., continue to be important disease manage- 2006; Langdon, 2008). Pseudomonas ment tools for organic growers seeking to fl uorescens (Flügge) Migula (Pseudomona- fi nd alternatives or at least supplements to da ceae) (BlightBan® strain A506), Pantoea the minimal use of chemical fungicides for agglomerans (Ewing and Fife) Gavini et al. integrated disease management strategies. (Enterobacteriaceae) (BlightBan® strain Serenade® Max is currently registered in C91), Streptomyces lydicus De Boer et al. Canada for use on highbush and lowbush (Actinovate®) and S. griseoviridis Ander- blueberries to control mummy berry son et al. (Streptomycetaceae) (Mycostop®) disease (Anonymous, 2011). were ineffective at suppressing infection of Chapter 64 427 blueberry buds at both 5°C and 20°C 64.5 Future Needs (Langdon, 2008). However, G. catenulatum, (Prestop®), Clonostachys rosea f. rosea Future work should include: (Link) Schroers et al. (Bionectriaceae) (Endofi ne®), Pseudozyma fl occulosa 1. Developing biological control strategies (Traquair, Shaw and Jarvis) Boekhout and aimed at antagonism of overwintering inoc- Traquair (Ustilaginaceae), (Sporodex®) and ulum on mummy berries in the litter of B. subtilis (Serenade® Max strain QST 713) lowbush blueberry; suppressed bud infection by more than 2. Investigating cold-tolerant yeasts from 50%. Serenade® Max applied at 0.08 g the surface of blueberry as these show ml−1 was the most effective product under promise for biological control of the blight controlled environment conditions and phase of M. vaccinii-corymbosi on lowbush artifi cial inoculation with ascospore sus- blueberry and various other fungal patho- pensions (Langdon, 2008). gens that cause rots of blueberry and cran- Field testing spray applications at three berry in storage; sites in Nova Scotia and using challenge 3. Determining the compatibility of biofun- inoculation with ascospore suspensions gicidal agents such as B. subtilis (Sere- showed that two applications of Serenade® nade® Max) and wild yeasts, with other Max at the most effective rate of 8 kg ha−1 bacterial and fungal biological control reduced vegetative bud infection signifi - agents and with chemical pesticides that cantly in an amount that was comparable are used in standard integrated pest and to the standard fungicide, propiconazole disease management programmes for small (Langdon, 2008; Langdon et al., 2009). fruits. Activity dropped off over time and with simulated rain treatments, but addition of a surfactant did not enhance activity of the Acknowledgements Serenade® Max (Langdon, 2008). When bacteria were fi ltered out of the formu- Evaluation of biological control agents was lation, lipopeptides in the fi ltrate sup- funded in part by the Pest Management pressed blight symptoms on lowbush Centre, AAFC Ottawa, through the Pesti- blueberry leaves. These results are con- cide Risk Reduction Programme. Sere- sistent with reports for the fungitoxic nade® Max was provided by AgraQuest, mechanism of activity for B. subtilis stain Inc., Davis California, USA. Actinovate® QST 713 (Marrone, 2002). However, failure was provided by Natural Industries, Inc., to show inhibition of ascospore germin- Houston Texas, USA. EndoFine® was ation on treated blueberry leaves (Langdon, provided by Adjuvants Plus, Kingsville, 2008; Langdon et al., 2009) indicates an Ontario, Canada. Sporodex® was provided additional mechanism, probably induced by R. Bèlanger, Laval University, Quebec host resistance based on mechanisms City, Quebec, Canada. Prestop® was described by Marrone (2002). provided by Verdera Oy, Helsinki, Finland.

References

Anonymous (2011) Serenade® Max Wettable Powder Biofungicide, Bacillus subtilis strain QST713, Product Label, Registration No. 28549, Pest Control Products Act, Pest Management Regulatory Agency, Health Canada, Ottawa, Ontario. Bristow, P.R. and Windham, G.E. (1995) Biological control of the berry infection stage of mummy berry. Biological and Cultural Tests for Control of Plant Diseases 10, 54. Caruso, F.L. and Ramsdell, D.C. (eds) (1995) Compendium of Blueberry and Cranberry Diseases. American Phytopathological Society Press, St Paul, Minnesota. 428 Chapter 64

Dedej, S., Delaplane, K.S. and Scherm, H. (2004) Effectiveness of honey bees in delivering the biocontrol agent Bacillus subtilis to blueberry fl owers to suppress mummy berry disease. Biological Control 31, 422–427. Hildebrand, P.D. and Braun, P.G. (1991) Factors affecting infection of lowbush blueberry by ascospores of Monilinia vaccinii-corymbosi. Canadian Journal of Plant Pathology 13, 232–240. Hildebrand, P.D. and McRae, K.B. (1995) Protectant and postinfection activity of triforine against ascospore infections of Monilinia vaccinii-corymbosi in lowbush blueberries. Canadian Journal of Plant Pathology 17, 215–222. Jordon, S.A., Sabaratnam, S., Catal, M. and Schilder, A. (2006) Partial characterization of epiphytic microorganisms on blueberry fruit, enzyme production and biocontrol potential. Phytopathology 96, S57. Lachance, M.-A., Bowles, J.M., Starmer, W.T. and Barker, J.S.F. (1999) Kodamaea kakaduaensis and Candida tolerans, two new yeast species from Australian Hibiscus fl owers. Canadian Journal of Microbiology 45, 172–177. Lambert, D.H. (1990) Effects of pruning method on the incidence of mummy berry and other lowbush blueberry diseases. Plant Disease 74, 199–201. Langdon, D.H. (2008) Biological control of Monilinia and Botrytis blights in lowbush blueberries. MSc thesis, University of Guelph, Guelph, Ontario. Langdon, D., Traquair, J., Hildebrand, P. and Boland, G. (2006) Screening commercial biocontrol agents for inhibition of Monilinia blight (mummy berry) on lowbush blueberry. Canadian Journal of Plant Pathology 28, 355–356. Langdon, D., Hildebrand, P.D., Traquair, J.A. and Boland, G.J. (2009) Effi cacy of the biological control agent Serenade® Max against Monilinia vaccinii-corymbosi in lowbush blueberry. Canadian Journal of Plant Pathology 31, 124. Marrone, P.G. (2002) An effective biofungicide with novel modes of action. Pesticide Outlook 13, 193–194. Sabaratnam, S., Dickman, J. and Schilder, A. (2004) Blueberry fruit surface microfl ora: search for potential biological control agents for fruit rot pathogens. Phytopathology 94, S91. Scherm, H., Ngugi, H.K., Savelle, A.T. and Edwards, J.R. (2004) Biological control of infection of blueberry fl owers caused by Monilinia vaccinii-corymbosi. Biological Control 29, 199–206. Stretch, A.W. (1988) Biological control of blueberry and cranberry fruit rots (Vaccinium corymbosi L. and V. macrocarpon Aist.). In: Strang, E.J. (ed.) Acta Horticultureae 241, 301–306. Traquair, J.A., Hildebrand, P.D., Langdon, D.H., Boland, G.J. and Sabaratnam, S. (2012) Preliminary survey of blueberry yeasts and their potential for biocontrol. Phytopathology 102, S4.121. Verma, N., MacDonald, L. and Punja, Z.K. (2006) Inoculum prevalence, host infection and biological control of Colletotrichum acutatum: causal agent of blueberry anthracnose in British Columbia. Plant Pathology 55, 442–450. Chapter 65 429

65 Plasmodiophora brassicae Woronin, Clubroot of Crucifers (Plasmodiophoraceae)

Gary Peng,1 Rachid Lahlali,1 Russell K. Hynes,1 Susan M. Boyetchko,1 Bruce D. Gossen,1 Sheau-Fang Hwang,2 Denis Pageau,3 Mary Ruth McDonald4 and Steven E. Strelkov5 1Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 2Alberta Agriculture and Rural Development, Edmonton, Alberta; 3Agriculture and Agri-Food Canada, Normandin, Quebec; 4University of Guelph, Kettleby, Ontario; 5University of Alberta, Edmonton, Alberta

65.1 Pest Status Pageau, 2012, unpublished results). In contrast, P. brassicae is not an important Clubroot, caused by Plasmodiophora disease of canola in Ontario. brassicae Woronin (Plasmodiophoraceae), The life cycle of P. brassicae consists of is a serious disease of Brassica spp. a primary infection phase in root hairs and (Brassicaceae) crops worldwide (Dixon, a secondary phase in the root cortex 2009). In western Canada, clubroot was (Buczacki, 1983). It starts with the reported on canola, Brassica napus L., B. germination of resting spores and release of rapa L. (Brassicaceae), in Alberta for the the primary zoospores, infection of root fi rst time in 2003 (Tewari et al., 2005) and hairs and formation of primary plasmodia. has since been found in more than 800 The primary plasmodia further results in fi elds in Alberta (Strelkov et al., 2012). secondary zoospores, which can infect Recently, clubroot was also reported from either root hairs to restart the primary two fi elds in Saskatchewan (Dokken- phase, or infect roots to initiate the Bouchard et al., 2012). The spread of secondary phase in root tissues. The char- clubroot disease is a threat to canola acteristic clubbing symptom is a con- production in western Canada because sequence of hyperplasia and hyper trophy substantial yield losses have been observed of the infected root tissues (Ludwig-Müller in heavily diseased fi elds (Hwang et al., et al., 1999). Under optimal conditions, the 2012). In eastern Canada, P. brassicae production of secondary zoospores peaks causes damage on cruciferous vegetable between 7 and 14 days after seeding crops. Soil liming and crop rotation are (Sharma et al., 2011). The population of recommended for management of P. resting spores can build up quickly in the brassicae in cruciferous vegetables, with soil when susceptible crops are grown variable success (McDonald et al., 2004). In repeatedly, and resting spores can persist Quebec, P. brassicae was fi rst reported on in the soil for many years (Niwa et al., canola in 1997 (Pageau et al., 2006), and 2008). The primary and secondary zoo- since then the disease has been found in spores are fragile and short-lived, and many canola fi elds in the province (D. appear to be a weak link in the pathogen

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 430 Chapter 65 life cycle (Dixon, 2006), so P. brassicae 65.3 Biological Control Agents management strategies tend to target the zoospores. Previous studies have demonstrated the potential of using naturally occurring microorganisms to reduce clubroot severity 65.2 Background (Narisawa et al., 1998; Cheah et al., 2000; Joo et al., 2004). Some of these biological Until recently, effective options for control control agents (BCAs) produce anti- of P. brassicae on canola in western Canada microbial metabolites (Arie et al., 1998; were lacking. The impact of agronomic Kim et al., 2004), while others colonize measures such as crop rotation were roots (Hashiba et al., 2003; Usuki and unknown or inadequate (Wallenhammar, Narisawa, 2007) and induce resistance to 1996), and all of the commercial cultivars clubroot (Morita et al., 2003). So far, no were highly susceptible to P. brassicae biofungicide is available for clubroot con- pathotype 3, which is a dominant pathogen trol but several commercial biofungicides, strain in the region (Strelkov et al., 2006). including Serenade®, Bacillus subtilis Four pathotypes of P. brassicae are present (Ehrenberg) Cohn (Bacillaceae) strain QST in Alberta (Strelkov et al., 2007; Xue et al., 713, Prestop®, Clonostachys rosea f. 2008). Knowledge of the pathotype catenulata (Gilman & Abbott) Schroers (= composition in a region is important Gliocladium catenulatum Gilman & because genetic resistance to P. brassicae is Abbott.) (Bionectriaceae), Mycostop®, generally race specifi c (Diederichsen et al., Strepto myces griseoviridis Anderson et al. 2006) and can be eroded rapidly when (Streptomycetaceae) strain K61, and Root virulent strains increase in the pathogen Shield®, Trichoderma harzianum Rifai population (Oxley, 2007). (Hypocreaceae), are registered in Canada In 2009, the fi rst P. brassicae-resistant for control of other soil-borne diseases. canola cultivar for western Canada was From 2009 to 2012, a study was released, and additional resistant cultivars conducted to search for soil micro- were brought to market shortly after. The P. organisms from western Canada with the brassicae resistance in each of these potential to control clubroot. A total of resistant cultivars is likely controlled by a 5152 bacterial and fungal isolates were single gene, but it is not known if the obtained from the rhizosphere or the resistance in all of these cultivars is derived interior of canola roots collected from the from the same source (LeBoldus et al., 2012; provinces of Alberta and Saskatchewan. Deora et al., 2013). However, none of the Each of these isolates was screened for resistant cultivars is immune to P. brassicae potential antagonism or competition (Peng et al., 2011a; Deora et al., 2013) and against P. brassicae in a two-tiered evalu- repeated exposure of a resistant cultivar to ation system. The majority of the bacterial the same pathogen population can cause a isolates were not identifi ed, but generally rapid decline in the level of resistance grew well on nutrient agar. The common (LeBoldus et al., 2012). Therefore, cultivar fungal isolates associated with canola roots resistance should be employed judiciously, included Clonostachys rosea f. rosea (Link) and an integrated approach is recom- Schroers et al. (Bionectriaceae), Epicoccum mended for sustainable management of nigrum Link (Pleosporaceae), T. harzianum clubroot (Dixon, 2003; Donald and Porter, and Fusarium spp. (Nectriaceae). Add- 2009). Other measures may include soil itionally, the endophytic fungus Hetero- nutrient management (Webster and Dixon, conium chaetospira (Grove) M.B. Ellis 1991a, b; Dixon and Page, 1998), cultural (Herpotrichiellaceae) strain B2HB1 isolated practices (McDonald and Westerveld, 2008; from forest soils in British Columbia, Gossen et al., 2009, 2012), crop rotation Canada was grown on autoclaved barley (Wallenhammar, 1996) and fungicides grain, ground to about 0.5-mm granules (Suzuki et al., 1995; Cheah et al., 1998). after drying, and applied via soil Chapter 65 431 incorporation. The commercial biofungi- soil drench to saturate growth medium cides Mycostop® (Verdera Oy, Finland), infested with P. brassicae resting spores, Prestop® (Verdera Oy), Root Shield® showed no substantial effi cacy against (BioWorks Inc., USA), Actinovate®, clubroot, except for three endophytic Streptomyces lydicus De Boer et al. fungal isolates and four rhizobacterial (Streptomycetaceae) strain WYEC 108, isolates which reduced clubroot severity by Natural Industries Inc. USA, and Sere- >75% relative to the control (Table 65.1). nade® (AgraQuest Inc. USA) were evalu- An additional ten fungal and bacterial ated as a soil drench treatment (as per isolates reduced disease severity by 50– registrants’ recommendation) against club- 75%. Overall, the results of the screening root on both canola and cruciferous method using P. ultimum were correlated vegetable crops. The synthetic fungicides with clubroot control on canola (r = 0.75, P Allegro® (fl uazinam) and Ranman® (cya- <0.05). The fact that a large number of zofamid) were included in these trials as a candidate isolates were ineffective in the commercial control. clubroot test may be due to a relatively low bar of effi cacy (>30%) used for initial selection. 65.4 Evaluation of Biological Control The granular formulation of H. chaeto- spira, when incorporated into the growth The initial assessments of the biofungi- medium prior to inoculation with P. cides and indigenous organisms were brassicae, reduced clubroot severity by conducted under controlled environment >80% relative to the non-treated control conditions. Of the 5152 indigenous micro- (Lahlali et al., 2012). However, applying bial isolates tested on agar media for the granular formulation into pathogen- antibiosis and competition, 390 were infested growth medium resulted in much selected from the fi rst tier of screening lower effi cacy. It appears that root based on >30% inhibition of Pythium colonization is required for H. chaetospira ultimum Trow (Pythiaceae) (an indicator to effectively reduce clubroot and the pathogen) in vitro and in vivo. As in P. colonization may take time because brassicae, Pythium spp. can infect roots H. chaetospira grows slowly. More exten- with motile zoospores in response to sive root colonization by H. chaetospira environmental stimuli including root resulted in greater suppression of exudates (Dandurand et al., 1995). In the P. brassicae infection and subsequent second tier of the assessment, most of the clubroot development (Lahlali et al., 2012). selected microbial isolates, applied as a Profi ling of the gene expression in canola

Table 65.1. Number of indigenous soil microorganisms exhibiting a level of suppression (%) of clubroot disease caused by soils infestation with Plasmodiophora brassicae under controlled environmental conditions.a

Range of clubroot suppression (%)d Microbial isolates 26–50 50–75 75–100 Fungi Endophyteb 71 3 Rhizospherec 13 2 0 Bacteria Endophytea 71 0 Rhizosphereb 57 4

a Out of 390 microbial isolates evaluated b Microorganisms isolated from the inside of roots c Microorganisms isolated from the rhizosphere d Disease suppression as measured by disease severity index (DSI) 432 Chapter 65 roots based on a microarray assay found increased with increasing soil bulk density up-regulation of several defence-related (Kasinathan, 2012). genes, especially those that control the Based on the overall effi cacy and jasmonic-acid (JA)/ethylene (Et) pathways potential readiness for use on canola, the (Lahlali et al., 2012). The transcriptional biofungicides Serenade and Prestop were expression of JA and Et genes were pursued in further studies on canola. Both enhanced by four- and two-fold, respect- biofungicides contain secondary meta- ively, relative to those in non-treated bolites, which alone reduced clubroot by plants, thus implying that the endophytic up to 60% relative to the controls in root colonization by H. chaetospira controlled-environment studies. The stimulated gene expression that regulates formulated product (containing the BCA host defence-related pathways (Lahlali et plus the secondary metabolites) of each al., 2012). The requirement for applying biofungicide suppressed clubroot by over H. chaetospira 1 week prior to exposure to 90%. Although the metabolites play a role P. brassicae makes the BCA impractical for in the effi cacy of both biofungicides, they controlling clubroot on canola. However, may not be the only active component this application timing may be feasible on (Lahlali et al., 2011a; R. Lahlali and G. vegetable transplants because the treatment Peng, unpublished results). can be applied to seedlings in the The impact of suppressing initial greenhouse before they are transplanted infection and subsequent clubroot develop- into infested fi elds. ment was demonstrated when the amount The biofungicides Serenade and Prestop of P. brassicae DNA in canola roots was provided 85–100% effi cacy against P. assessed at 2 weeks after treatment using brassicae when applied as a soil drench qPCR (Sundelin et al., 2010). In these (Peng et al., 2011b), which was similar to trials, the measurements on pathogen DNA the effi cacy of the synthetic fungicides was strongly correlated with subsequent fl uazinam and cyazofamid. However, the clubroot severity; the lower the amount of biofungicides were less effective than the pathogen DNA, the less clubroot severity synthetic fungicides when disease pressure later on. Neither biofungicide reduced the was high (Peng et al., 2011b). Also, the germination nor viability of pathogen BCAs B. subtilis and C. rosea were less resting spores substantially (Lahlali et al., effective when applied as a seed-dressing 2011a, b), so the biological control activity treatment than as a soil drench. In contrast likely resulted from the suppression of to the results on canola, Mycostop and root-hair and/or root-cortex infection by Actinovate were more effective on primary and secondary zoospores of Shanghai pak choy, B. rapa ssp. chinensis P. brassicae. Additionally, genes encoding (L.) Hanelt (Brassicaceae). However, none JA (BnOPR2), Et (BnACO) and phenyl- of the biofungicides were effective on propanoids (BnOPCL and BnCCR) were Shanghai pak choy under fi eld conditions substantially up-regulated in canola plants (Adhikari, 2010; Kasinathan, 2012). treated with either biofungicide, indicating When the biofungicides were evaluated potential induction of defence reactions. in different soil types under controlled This host response was translocated to environmental conditions, both Serenade leaves, where it reduced infection by the and Prestop reduced clubroot levels in fungal pathogen Leptosphaeria maculans muck soil, mineral soil and sand, but soil (Fuckel) Ces. & de Not (Leptosphaeriaceae) type had an important impact on the (Lahlali et al., 2013). In the same studies, relative effi cacy of the two biofungicides, both BCAs were observed to colonize with the pattern of response being canola roots extensively. This intimate generally similar on canola (inoculated contact between the BCA and canola roots with pathotype 3) and pak choy (inocu- may induce or enhance resistance to club- lated with pathotype 6). Levels of clubroot root via modulation of the JA/Et and disease were low in soil-less mix, but phenylpropanoid pathways. Chapter 65 433

From 2009 to 2011, several fi eld trials Chinese cabbage is not known. At the trial were conducted to assess the effi cacy of site where the treatments were effective, Serenade and Prestop against clubroot on clubroot severity was lower than at the canola in central Alberta and northern other site. These biofungicides were much Quebec and on Chinese cabbage, B. rapa L. more effective at moderate than at high ssp. pekinensis (Lour.) Hanelt (Brassica- disease pressure under controlled environ- ceae), in southern Ontario. Pathotype 3 of mental conditions, so disease pressure may P. brassicae was predominant at the have an impact on the success of bio- Alberta sites (Strelkov et al., 2007), and fungicide treatments. pathotypes 6 and 2 were predominant in Clubroot disease pressure was generally Ontario and northern Quebec, respectively high in all of the trials where the (Cao et al., 2009). biofungicide granular formulations were Subsequent fi eld trials evaluated tested, with DSI ranging from 69% to 98% B. subtilis applied as a granular formu- on the susceptible canola cultivar. None of lation or as a seed-dressing, and these two the biofungicide formulations (or the delivery approaches would be more synthetic fungicides) reduced clubroot practical for commercial canola pro- severity, but DSI in the resistant cultivar duction. Two granular formulations were was consistently <15% and the seed yield applied in-furrow to a resistant and was double that of the susceptible cultivar susceptible canola cultivar: one was based (Fig. 65.1) in six fi eld trials over 2 years. on a corn starch–peat mixture that dis- Biofungicide seed dressing did not reduce integrates rapidly in water and ensures clubroot level, regardless of the application quick release of B. subtilis into the soil rate or crop rotation. Longer crop rotation (Hynes and Boyetchko, 2011) and the reduced disease pressure (inoculum second consisted of B. subtilis infused into density), with the 11-year-break treatment corn-cob grits. The seed-dressing treatment showing the lowest amount of pathogen in was applied using standard industrial the soil based on qPCR and bioassay methods and equipment at the Seed- analyses of soil samples. The DSI for all of Treatment Lab (Regina, Saskatchewan), the rotation treatments was high, with the Bayer CropScience Canada. Each of the 1-year break at or near 100%. However, formulations showed moderate effi cacy clubroot symptoms on the roots were against P. brassicae under controlled slightly lower (clubs were smaller) in the 3- environmental conditions. However, in the and 11-year-break treatments, and above- fi eld trials where the biofungicides were ground symptoms (stand thinning, stunting applied as a liquid to canola, none of the and premature ripening) were less severe treatments (including the synthetic fungi- than in the 1-year break treatment. cides) reduced clubroot severity sub- Similarly, seed yields in the 3- and 11-year stantially. There was a period of 4 weeks break treatments were substantially higher without rain immediately after seeding, than that of the 1-year-break treatment in and this dry soil condition likely reduced both trials (Peng et al., 2012). the effi cacy of the biofungicides (Peng et The biofungicide Serenade® showed al., 2011b). In contrast, each of the treat- consistent effi cacy against clubroot on ments in the initial Chinese-cabbage trial canola when applied as a soil drench suppressed clubroot on the susceptible under moderate disease pressure. This cultivar and reduced DSI by 54–84%. The method of application is impractical for biofungicides were as effective as the canola crops because of the large water synthetic fungicides in this trial. Unfortu- volumes required. However, it may have a nately, the biofungicides and synthetic role in vegetable production. Similarly, fungicides did not control clubroot signifi - application of H. chaetospira to vegetable cantly when the trial was repeated (G. seedlings prior to transplanting shows Peng, 2012, unpublished results). The promise. Despite encouraging results under cause for the inconsistent performance on controlled conditions, biofungicides or 434 Chapter 65

100

80

60

40

20

0 5 45H28 - S 4 45H29 - R

3

2

Yield (kg seed/plot)Yield 1 (%) index Disease severity

0

Allegro (grits) Ranman (grits) Serenade (grits) Non-treated (CK)

Serenade (granules) Treatment

Seeding date: May 28, 2011

Fig. 65.1. Effect of Serenade biofungicide or synthetic fungicide (Allegro or Ranman) application on clubroot severity (DSI) and subsequent seed yield of a susceptible (S) and a resistant (R) canola cultivar at Leduc, Alberta (2011). Capped lines represent standard error.

fungicides have performed poorly in under fi eld conditions – seed dressing may canola fi eld trials. deserve special attention as part of bio- fungicide formulation, because this deliery approach would be highly practical for 65.5 Future Needs canola production; 2. Further investigation of biological con- Future work should include: trol in combination with crop rotation and varietal resistance as these methods can 1. Development of formulations of promis- reduce P. brassicae inoculum in the soil ing agents, e.g. Serenade®, H. chaetospira, and effectively alleviate the impact of club- that extend product longevity and activity root on canola, respectively. Chapter 65 435

Acknowledgements McGregor and D. Hupka for technical assistance. We also thank SaskCanola, We thank Dr K. Narasawa (College of Alberta Crop Industry Development Fund, Agriculture, Ibarakii University, Japan) for Canola Council of Canada (PCARP) and the providing the isolate H. chaetospira strain AAFC Pest Management Centre for B2HB1, and G.D. Turnbull, V.P. Manolii, L. fi nancial support.

References

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66 Pythium aphanidermatum (Edson) Fitzpatrick and Pythium ultimum Trow (Pythiaceae), Seedling Damping-off and Root and Crown Rot

Pervaiz A. Abbasi Agriculture and Agri-Food Canada, London, Ontario

66.1 Pest Status These oomycete pathogens are common soil inhabitants and they can infect seed Pythium ultimum Trow, Pythium aphani- soon after planting. Germinating seeds and der matum (Edson) Fitzpatrick and other growing roots release chemicals such as Pythium spp. (Pythiaceae) are soil-borne phenolic compounds that act as growth pathogens causing seedling damping-off stimulants and attractants for Pythium and root and crown rot diseases in young spores, allowing them to grow quickly and seedlings of several horticultural and infect roots, and these compounds pre- vegetable crops in both greenhouse and dispose the host to infection (Owen-Going fi eld production systems (Howard et al., et al., 2012). Pythium spores germinate and 1994; Paulitz and Bélanger, 2001). These penetrate feeder roots directly. In pre- pathogens generally attack the juvenile emergence damping-off, seed may be tissues of bedding plants (Gravel et al., decayed or rot under the soil surface soon 2009), greenhouse transplants and fl oral after infection when moisture penetrates crops (Howard et al., 1994; Moorman et al., the seedcoat or when the radicle begins to 2002) and direct-seeded fi eld crops (Hwang extend, resulting in a poor and uneven et al., 2000, 2001; Paulitz, 2006; Leisso et seedling stand. In post-emergence al., 2009). Damping-off and root rot damping-off, cotyledons of the infected diseases are also widespread and destruc- plant may break the soil surface and soon tive on seedlings in forest nurseries (Huang wither and die, or healthy looking seed- and Kuhlman, 1990). Pythium spp. cause lings may suddenly fall over. The seedling infection in cool, wet and poorly-drained will discolour or wilt suddenly, or simply soils, and young seedlings of direct-seeded collapse and die. Weak seedlings also plantings may be killed before or soon after become vulnerable to attack by other soil- they emerge, leading to inadequate stand borne pathogens. Pythium spp. can survive establishment. No-till agriculture practices as thick-walled mycelia or oospores for also increased root diseases caused by several years in soil and plant debris, and Pythium spp. and other soil-borne are the main source of disease inoculum in pathogens (Paulitz, 2006; Schroeder and the soil. Paulitz, 2008).

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 66 439

66.2 Background ceae) diseases. Phosphorus acid is a biofungicide since it is categorized as a Pythium spp. are always present in the soil natural product. We investigated the and their effects can be considerably effectiveness of a new formulation of reduced if their initial attack is stopped or phosphonate fungicide (Calirus 150, Bro- slowed. This can be achieved by some mine Compounds Ltd, Beer Sheva, Israel) cultural and chemical control options. to suppress damping-off and root rot Planting undamaged high-quality seed diseases of cucumber, Cucumis sativus L. treated with fungicides in well-drained (Cucurbitaceae), caused by Pythium spp. soils may improve emergence and stand and Phytophthora capsici Leonian (Perono- establishment. Reseeding of the damaged sporaceae) (Abbasi and Lazarovits, 2005, or patchy areas in the fi eld may be the 2006a; Abbasi et al., 2011). Both pre- most cost-effective option. Some targeted planting and post-planting drench appli- crop rotation is also possible (Lawrence cations and seed treatments of this product and Harvey, 2006), but in general it may effectively reduced damping-off of not be a suitable management option due cucumber seedlings. The product was also to the wide host range of Pythium spp. and effective in micro-plot and fi eld trials, their long-term viability as thick-walled however, the amount and frequency of mycelia or oospores. Disease resistance irrigation and rainfall can affect the disease may be available against some Pythium suppression. Drench applications of phos- spp. but not always in the most desirable phonate were also effective in reducing crop cultivars. Fumigants can be effective seedling damping-off and clubroot of bok but such compounds are expensive and choy, Brassica rapa var. chinensis (L.) can be dangerous to apply. Seed treatment Kitam., and cabbage, Brassica oleracea L. with fungicides such as captan, thiram, (Brassicaceae) (Abbasi and Lazarovits, iprodione, fenaminosulf, fosetyl-Al and 2006b), and Phytophthora blight of bell metalaxyl generally provides effective pepper, Capsicum annuum L. (Solanaceae) control but there is growing public (Abbasi et al., 2011). concern with the application of chemical pesti cides. Seed treatment with some of these fungicides, however, may not always 66.3 Biological Control be effective. Healthy undamaged pea, Pisum sativum L. (Fabaceae), seed treated 66.3.1 Microbial agents with metalaxyl improved emergence and stand establishment in commercial fi elds, Damping-off and root rots caused by but inoculation by Pythium spp. and Pythium spp. are good model diseases to mech anical damage to the seed reduced evaluate microbial biofungicides for their seedling emergence, seedling size and seed disease control effect. These are also very yield (Hwang et al., 2001). Although common diseases affecting young seedlings fungicide seed treatment reduced the of a wide array of plants. Several different impact of seed damage, it did not always bacteria, fungi and yeasts have been restore seedling emergence and seed yield evaluated as biological control agents to the same level as for undamaged seed. against these diseases, mostly under In fi eld trials in Montana, the mefenoxam controlled but also under fi eld conditions. seed treatment of chickpeas, Cicer The bacteria used include rhizobacteria, arietinum L. (Fabaceae), was the most pseudomonads, bacilli and actinomycetes, effective treatment in reducing Pythium whereas fungal agents include Tricho- damping-off and increasing plant growth derma spp. (Hypocreaceae), Clonostachys (Leisso et al., 2009). spp. (Bionectriaceae), Gliocladium spp. Phosphonates and phosphites are (Hypocreaceae) and Muscodor spp. phosphorus acid-based fungicides effective (Xylariaceae). Several of the biofungicides against Phytophthora spp. (Peronospora- discussed below are now available as 440 Chapter 66 commercial products against these patho- cides are now commercially available, gens. The effectiveness of the biofungicides including Actinovate® and Mycostop®. is low to moderate depending on the level Several bacilli are also known biological of disease and the condition of the control agents of plant pathogens. These assessment. bacteria were effective in reducing root rot Non-pathogenic rhizobacteria are of lettuce, Lactuca sativa L. (Asteraceae), potential biological control agents of caused by P. aphanidermatum. The disease several soil-borne pathogens and these are was managed by vermiculite-based formu- also good root colonizers. These rhizo- lations of Bacillus subtilis (Ehrenberg) bacteria can protect cucumber roots from Cohn (Bacillaceae) (Amer and Utkhede, Pythium root and crown rot disease by 2000) or B. subtilis and some nutrient colonizing them and inducing systemic supplements (Utkhede et al., 2000). resistance (Chen et al., 1999, 2000). In Some fungal antagonists, which are cucumber roots the bacteria also com mon soil inhabitants and non- stimulated the activity of plant defence pathogens, also gained interest as potential enzymes, such as phenylalanine ammonia- biofungicides with some products avail- lyase, peroxidase and polyphenol oxidase. able commercially. A wettable powder Seed treat ment with rhizobacteria formu lation of Clonostachys rosea f. collected from southern and central catenulata (J.C. Gilman & E.V. Abbott) Alberta reduced Pythium damping-off of Schroers (= Gliocladium catenulatum sugarbeet, Beta vulgaris L. (Amarantha- Gilman and Abbott) (Bionectriaceae) ceae), canola, Bras sica napus L., B. rapa L. reduced damping-off in bedding plant (Brassicaceae), saffl ower, Carthamus seedlings grown in a peat-based substrate tinctorius L. (Asteraceae), and dry pea, artifi cially infested with P. ultimum Pisum sativum L. (Fabaceae) (Bardin et al., (McQuilken et al., 2001). The biofungicide 2003). A strain of Pseudomonas was applied as a pre-plant or drench chlororaphis (Guignard and Sauvageau) application. In most cases, the damping-off (Pseudomonadaceae) suppressed Pythium reduction by the antagonist was root rot and promoted plant growth in comparable to fungicide drenches of hydroponic cucumbers (Zheng et al., 2000) propamocarb HCl or tolclofos-methyl. and in hydroponic peppers (Sopher and Survival of G. catenulatum in the Sutton, 2011). The bacteria introduced formulation and subsequent ability to into the nutrient solution prior to the reduce damping-off was not affected by pathogen inoculation delayed root brown- storage at low temperature for 48 weeks. ing in both cucumber and pepper. An isolate of C. rosea f. catenulata is also Similarly, an isolate of Pseudomonas available commercially as a formulated putida Trevisan (Pseudomonada ceae) biological control agent (Prestop® WP and protected hydroponic cucumbers against Prestop® Mix) with broad-spectrum activ- Pythium root rot, possibly through ity against plant pathogens. Application of production of antifungal phenolics away Prestop® was shown to reduce root from the point of treatment (Ongena et al., diseases caused by P. aphanidermatum on 2000). Fluorescent pseudomonad bacteria greenhouse cucumber (Punja and Yip, produce antifungal antibiotics during root 2003). Clonostachys rosea f. catenulata colonization and elicit induced systemic also reduced damping-off on ginseng, resistance in the host plant or interfere Panax quinquefolius L. (Araliaceae), seed- specifi cally with patho genicity factors lings caused by a complex of soil-borne (Haas and Défago, 2005). pathogens (Rahman and Punja, 2007). The Nonpathogenic streptomycetes and effectiveness of this antagonist as a other actinomycetes are common soil biological control agent may be due to this inhabitants and several are now known fungus being a very good rhizosphere- biological control agents of plant patho- competent, rapid root colonizer (Chat- gens. Many Streptomyces-based biofungi- terton et al., 2008) that also produces Chapter 66 441 glucanase in the colonized roots (Chat- growth even in combination with fungi- terton and Punja, 2009). cides (Leisso et al., 2009). Muscodor albus Worapong et al. (Xylariaceae) is an endophytic fungus isolated from tropical trees and vines. It has broad-spectrum antimicrobial activity, 66.3.2 Organic amendments which is achieved through an array of volatile organic compounds it produces. Soil-less media, consisting mainly of peat- Fresh rye, Secale cereale L. (Poaceae), based substrates and composts, are culture of M. albus when incorporated into extensively used by the greenhouse peat-based potting mix suppressed industry for transplant production. damping-off of broccoli, Brassica oleracea Although these substrates are usually L. convar. oleracea (Brassicaceae), seed- pathogen-free, peat-based potting sub- lings and Phytophthora root rot of bell strates are generally considered as disease peppers depending on the rate of inoculum conducive and compost-amended sub- of the fungus used (Mercier and Manker, strates are considered as disease sup- 2005). Disease control became inconsistent pressive (Hoitink and Boehm, 1999). This as the inoculum of the fungus was reduced. may, however, depend greatly upon the This fumigant fungus produced volatiles composition of the mixes and their such as isobutyric acid in soil and potting biological activity. Planting mixes that are mix, which played a major role in disease naturally disease suppressive have been control (Mercier and Jiménez, 2009). considered to be rich in microorganisms Similarly, a starch-based formulation of M. that induce biological control (Hoitink and albus provided control of seedling disease Boehm, 1999; Abbasi et al., 2007b). In of sugarbeet caused by P. ultimum general, where suppression has been (Grimme et al., 2007). Another isolate of obtained, it has been attributed to the this fungus was effective in improving increased microbial activity in the germination of kale, Brassica oleracea var. amended substrate. Compost-amended acephala DC (Brassicaceae), seedlings in P. mixes containing peat moss, sawdust, ultimum-infested soil (Worapong and chitin waste or cow manure, and shrimp Strobel, 2009). waste, prepared in a biphasic composting Field effi cacy is very critical for process, reduced incidence of cucumber development of new microbial-based pro- damping-off caused by P. ultimum (Labrie ducts and will always be a challenge. et al., 2001). The composting process also Leisso et al. (2009) evaluated commercially induced population of Gram-positive available Bacillus pumilus Meyer and bacteria. Similarly, Carisse et al. (2003) Gottheil (Bacillaceae) GB34 (Yield observed more diverse bacterial popu- Shield®), B. subtilis GB03 (Kodiak®), B. lations in compost from paper mill sludge subtilis MBI 600 (Subtilex®), Streptomyces than in composts from plant waste or lydicus De Boer et al. WYEC 108 manure. Some of these bacteria suppressed (Actinovate®), S. griseoviridis Andersen, cucumber damping-off. McKellar and Ehrlich, Sun and Burkholder (Strepto- Nelson (2003) provided evidence for the mycetaceae) K61 (Mycostop®), Tricho- role of fatty-acid-metabolizing bacteria derma harzianum Rifai (Hypocreaceae) from leaf composts in suppression of KRL-AG2 (T-22 Planter Box®) and fungi- Pythium damping-off of cotton, Gossypium cide (fl udioxonil and mefenoxam) seed herbaceum L. (Malvaceae). They found treatments applied alone or in com- that bacteria colonized cottonseeds within binations for their effects on Pythium the fi rst few hours and suppressed P. damping-off in two chickpea cultivars ultimum sporangium germination and seed under greenhouse and fi eld conditions. colonization and protected cotton None of the biological seed treatments transplants from damping-off. Gravel et al. reduces damping-off and increases plant (2009) noted a synergic effect of benefi cial 442 Chapter 66 microorganisms and an organic source of adding FE. There was also a signifi cant fertilizer in growth stimulation of increase in soil bacteria after addition of FE geranium, Pelargonium spp. (Geraniaceae) in muck soil. plants. These plants were also less colon- The effi cacy of FE to suppress damping- ized by P. ultimum. off of cucumber seedlings in peat-based Utilizing a cucumber–Pythium growth- mix may have been due to an increase in room plant bioassay, we have been the resident microbial activity of the investigating the effects of various organic amended mix (Abbasi et al., 2004). amendments on seedling damping-off and Therefore, it is expected that the disease root rot diseases in artifi cially infested protection can vary from batch to batch of peat-based substrates and agricultural soils the mix depending on the pathogen and (Abbasi et al., 2004). Fish emulsion (FE) microbial activity for general or specifi c derived from Atlantic menhaden, suppression (Hoitink and Boehm, 1999). Brevoortia tyrannus (Latrobe), and Gulf Suppression of Pythium or Phytophthora menhaden, Brevoortia patronus Goode damping-off and root rot diseases by (Clupeiformes: Clupeidae), is an organic organic matter-mediated general microbial foliar fertilizer with disease-suppressing activity is a good example of general sup- activity (Lazarovits et al., 2009; Abbasi, pression, whereas the suppression of 2011). It can be used to enrich and enhance diseases caused by Rhizoctonia solani microbial activity in the amended sub- Kühn (Ceratobasidiaceae) and Fusarium strates or soils. Incorporation of FE into oxysporum Schltdl. (Nectriaceae) is gener- pathogen-infested substrate and incubation ally considered to be specifi c through the for 1–4 weeks prior to planting cucumber activities of one or several specifi c organ- seeds reduced incidence and severity of isms (Hoitink and Boehm, 1999). A careful damping-off. Seedlings produced in the analysis of the type of microbial popu- peat-based mix incubated for only 1 day lations induced in the mix after FE with FE were often as highly diseased as amendment can provide further insight the control treatments, although occasion- into the general or specifi c nature of ally signifi cant disease reduction was seen disease suppression by FE. FE also con- (Abbasi et al., 2004). In the peat-based mix tains large amounts of organic acids and treated with 2 and 4% FE 7 days prior to they may also have a role in disease seeding, 60–70% of the seedlings remained suppression depending on the soil and disease-free and when treated 28 days prior substrates (Abbasi et al., 2009a). to seeding even the 1% rate of FE provided Maize, Zea mays L. (Poaceae), distil- similar high levels of protection. The lation products or condensed distiller equivalent levels of inorganic N-P-K treat- solubles (CDS) are co-products remaining ment provided no disease control (Abbasi after the removal of ethyl alcohol by et al., 2004). distillation from yeast fermentation of Fish emulsion also provided disease maize and condensing the thin stillage control in naturally infested organic or fraction to a semi-solid. CDS is a good muck soil (Abbasi et al., 2004). When nutrient source for enriching and planted with cucumber seeds, samples of enhancing microbial activity. The effect of muck soil from commercial Ontario CDS pre-plant amendment to muck soil to vegetable fi elds naturally infested with suppress damping-off and root rot disease Pythium spp. showed a high damping-off of cucumber seedlings was investigated in incidence and severity among the a growth room (Abbasi et al., 2007a). The cucumber seedlings. FE (1 and 2% mass/ muck soil from a commercial fi eld was mass soil) provided immediate protection naturally-infested with Pythium spp. CDS of cucumber seedlings from damping-off in (0.25, 0.5 and 1%) provided protection of this infested muck soil and disease cucumber seedlings from damping-off protection was consistent when planting immediately after incorporation, but the was delayed for 1, 2 and 4 weeks after maximum protection was seen after 1 Chapter 66 443 week with all three rates. The number of 66.5 Future Needs total bacteria was enhanced in the CDS- amended muck soil. In the micro-plots, Further work should include: CDS (0.5 and 1%) as an amendment to 1. Characterizing benefi cial microbial com- muck soil 2 weeks before planting munities from the plant rhizosphere after improved the percentage of healthy enriching with organic substrates; cucumber seedlings and fresh plant 2. Elucidating the role of microbial com- weight compared to the control. CDS munities in both suppression of damping- contains low levels of some organic acids off and root rot pathogens and in plant that may have a role in disease growth; suppression in muck and sandy-loam soils 3. Re-introducing selected microorganisms (Abbasi et al., 2009b). with an organic substrate to confi rm and further enhance their role in disease sup- pression; 66.4 Evaluation of Biological 4. Evaluating a holistic approach including Control several management options to reduce overall losses from Pythium spp.-induced Biological control has a promising role in and other plant diseases and to improve suppressing damping-off and root rot the consistency in fi eld effectiveness of diseases and several studies have reported biofungicides for disease management. great success under controlled conditions. Several commercial biofungicides are now available against damping-off and root rot Acknowledgements diseases, however, consistent fi eld effective- ness of these biofungicides remains a Many individuals including technicians, challenge. Biological control agents can be term employees and co-op students have introduced as drench applications or as made signifi cant contributions to this seed treatments. Organic substrates can research in several ways during the past also be used as carriers for biological con- several years. Technical assistance of Brian trol agents. Indigenous microbial com- Weselowski, Igor Lalin and Rebecca Earl, munities in potting substrates and and the collaborative work of Dr George agricultural soils can greatly contribute to Lazarovits and Dr Kenneth L. Conn is disease suppression by reducing and highly appreciated and acknowledged. This competing with pathogen populations. research was funded by grants from Omega Organic substrates can infl uence these Protein, Commercial Alcohol Inc., Agricare communities and enhance their biological Ltd. and the Agriculture and Agri-Food control potential. Canada Matching Investment Initiative.

References

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67 Rhizoctonia solani Kühn (Anamorphic S tate of Thanatephorus cucumeris (A.B. Frank) Donk), Damping-off, Root and Crown Rot, Blight, Leaf Spot, Stem Canker and Tuber Scurf (Ceratobasidiaceae)

James A. Traquair,1 Russell K. Hynes,2 Siva Sabaratnam3 and Pervaiz A. Abbasi1 1Agriculture and Agri-Food Canada, London, Ontario; 2Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan; 3British Columbia Ministry of Agriculture, Abbotsford, British Columbia

67.1 Pest Status scurf is a widespread disease of potato, Solanum tuberosum L. (Solanaceae), tubers, Rhizoctonia solani Kühn (Ceratobasidia- seed pieces and potato sprouts in Canada ceae) is a cosmopolitan plant pathogen that and the USA (Stevenson et al., 2001; infects a wide range of hosts and causes Anonymous, 2005). Rhizoctonia diseases diverse symptoms depending upon the are also widespread and destructive on host, the part of the plant affected and potted seedlings in forest nurseries (Huang environmental conditions. Seedling blights, and Kuhlman, 1990; Camporota and web blight, damping-off, root rot, leaf spot, Perrin, 1998). stem canker and scurf symptoms are The quality and marketability of tomato, reported on many different horticultural, Solanum lycopersicum L. (Solanaceae), vegetable and fi eld crops and on trans plants and subsequent stand establish- ornamentals including turf grass in Canada ment in tomato fi elds can be seriously and throughout the world (Martens et al., compromised by R. solani infection and 1984; Smiley et al., 1992; Howard et al., disease incidences of 10–50% in plug trays 1994; O’Brien et al., 2008). Seedlings of have been reported (Howard et al., 1994). fi eld-grown crops and transplants of vege- Prolonged cool, moist soil conditions tables and ornamentals raised in the follow ing seeding contributes to yield greenhouse are particularly susceptible to losses due to Rhizoctonia diseases that can pre-emergent root rot, crown rot and be substantial in fi eld crops such as canola, damping-off caused by R. solani. Leaf spots Brassica napus L. (Brassicaceae) (Martens and stem cankers appear on seedling et al., 1984). Klein-Gebbinck and Woods sprouts such as mung bean, Vigna radiata (2002) reported that canola plant weight, (L.) R. Wilczek (Fabaceae) (O’Brien et al., seed yield, harvest index, seed size but not 2008), and on older plants of a wide range oil content, were reduced on plants with of crops (Martens et al., 1984), while black completely decayed roots. Canola yield

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 67 447 losses can be as high as 65–85% under 67.2 Background fi eld plot conditions (S.F. Hwang, Crop Diversifi cation Centre, Brooks, Alberta, For Rhizoctonia diseases in greenhouse- 2012, pers. comm.). Canola roots with and the fi eld-grown plants, chemical girdling and sunken lesions had seed yield fungicides are registered in Canada but reduced by 17% while plants with decayed control is diffi cult. Protectant fungicides taproots had seed yield reduced by 65% such azoxystrobin, iprodione, fl udioxinol, (Klein-Gebbinck and Woods, 2002). Crop mancozeb, thiram, thiophanate-methyl and rotation and tillage intensity infl uenced thiabendazole can be used as seed Rhizoctonia girdling and root rot of canola treatments, soil drenches, foliar sprays and (Soon et al., 2005). Tillage practice also dips/sprays to stored roots and tubers factored into wheat, Triticum aestivum L. (Anonymous, 1996, 1997, 2005, 2012). (Poaceae) production in the Pacifi c North- Seed treatment with fungicides may not west of the USA where the incidence and always be effective. For example, seed severity of R. solani on roots was reported treatments with various combinations of to be greatest in the no-till treatments seven formulated fungicides did not (Schillinger et al., 2010). Emergence and increase soybean, Glycine max L. (Faba- establishment of vegetable crops such as S. ceae), emergence or yield in R. solani- tuberosum can be reduced by widespread infested fi eld (Xue et al., 2007). and low to high infection of sprouts on Cultural measures such as strict tuber seed-pieces, leading to serious yield sanitation and sterilization of potting losses (20–30%) annually (Stevenson et al., medium and plug trays are very effective 2001; Anonymous, 2005). in the greenhouse (Howard et al., 1994) The presence of sterile, web-like while seedling depth, tillage, plant mycelium on infected plant tissues is the density, crop rotation, weed control, usual evidence of Rhizoctonia disease fertilization and timing of irrigation (leaf (Traquair and Smith, 1981). The vegetative wetness) are important for discouraging hyphae are hyaline to brownish-coloured, Rhizoctonia diseases in fi elds and turf have characteristic right-angle branching (Traquair and Smith, 1981; Smiley et al., and produce sclerotial initials that consist 1992; Kharbanda and Tewari, 1996). of compact aggregations of moniliform cells. Resistance in fi eld and vegetable crops is These aggregations develop into brown to limited but there is a low to moderate black sclerotia on plant surfaces and degree of tolerance in selected cultivars blackish, thick-walled microsclerotia within (Howard et al., 1994; Kharbanda and infected plant cells (Howard et al., 1994; Tewari, 1996; Stevenson et al., 2001; Stevenson et al., 2001). Sclerotia and Anonymous, 2005). Composted agri- microsclerotia allow the pathogen to cultural, household and industrial wastes survive in soil and on diseased plant debris. (Tuitert et al., 1998), fi sh meal and maize More rarely, surface mycelium on infected distillate solids (Abbasi et al., 2007b; stems such as potato and tomato in cool, Lazarovits et al., 2009; Abbasi, 2011) and moist conditions, may form an in- green manures (Huang and Huang, 1993) conspicuous grey, waxy and membranous have shown considerable promise as (corticoid) hymenium producing hyaline, organic soil amendments for controlling R. pip-shaped basidiospores that are spread in solani and other soil-borne diseases. the wind to other host plants (Stevenson et Allelochemicals in these amendments al., 2001). In canola and other crops, R. such as allyl isothiocyanates in mustard solani infects hypocotyls and roots of seed- greens, can act directly to kill R. solani lings by dome-shaped infection cushions and other pathogens or they can stimulate and macerates the cortical and vascular disease-suppressive bacteria and fungi in tissues with the aid of wall-degrading the soil (Huang et al., 1993; Chung et al., enzymes (Kataria and Verma, 1992). 2002). 448 Chapter 67

67.3 Biological Control Agents peat-based substrate artifi cially infested with R. solani (McQuilken et al., 2001). Commercial, peat-based potting mixtures Muscodor albus Worapong, Strobel & Hess available in Canada (Premier Horticulture, (Xylariaceae) is an endophytic biological Ltd, Rivière-du-Loup, Quebec, Canada) are control fungus isolated from tropical trees now routinely spiked with disease-sup- and vine species. It has broad-spectrum pressive bacteria against R. solani and antimicrobial activity, which is achieved other fungal pathogens of greenhouse crops through an array of volatile organic and plug transplants (Anonymous, 2007). compounds. Fresh rye, Secale cereale L. Products such as Premier® Pro-Mix® HP (Poaceae), culture of M. albus incorporated and Pro-Mix® PGX with biofungicide con- into peat-based potting mix suppressed tain the active ingredient Bacillus subtilis Rhizoctonia damping-off of broccoli, (Ehrenberg) Cohn (Bacillaceae) MBI 600 (as Brassica oleracea L. (Brassicaceae), seed- Subtlex®) while others such as Premier® lings (Mercier and Manker, 2005). Volatiles Pro-Mix® HP with Mycorise Pro® contain such as isobutyric acid produced by this the benefi cial, growth-promoting endo- fungus in soil and potting mix play a major mycorrhizal fungus Glomus intraradices role in disease biological control (Mercier Schenck and Smith (Glomeraceae). and Jiménez, 2009). A wide range of soil- and root-borne bacteria and their microbial products have been isolated and screened in vitro for 67.4 Evaluation of Biological Control potential to biologically control R. solani in fi eld crops and greenhouse transplants Development and commercialization of (De Freitas et al., 1999). A streptomycetous cost-effective biofungicides for Rhizoctonia bacterium from a S. lycopersicum rhizo- diseases require a good understanding of sphere in Ontario was shown to be an markets, target crops, implementation effective antagonist of R. solani in dual strategies and microbial production tech- cultures and on S. lycopersicum trans- nologies (Bailey et al., 2010). Effi cacy, plants in the greenhouse (Sabaratnam, shelf-life, delivery methods, disease 1999). Streptomyces griseoviridis Anderson etiology and epidemiology, formulation, et al. (Streptomycetaceae) is commercially ecology, environmental risk and persist- available as Mycostop® for managing root ence of the product are important con- rot and damping-off by R. solani and other siderations by Canadian researchers. fungi in the greenhouse (Sabaratnam and Individual microbial biological control Traquair, 1998). Trichoderma and Glio- agents being developed in Canada include cladium spp. (Hypocreaceae) have been bacterial and fungal antagonists of R. shown frequently to suppress Rhizoctonia solani causing damping-off and root rot in damping-off and root rot of many crops by tomato transplants and seedlings of fi eld seed treatments and soil amendments and vegetable crops such as canola, beans (Lumsden et al., 1993). Trichoderma and potatoes. Various Rhizoctonia-sup- harzianum Rifai (Hypocreaceae) is com- pressive organic amendments and the mercially available in Canada and the USA consequent stimulation of antagonistic, as RootShield® for biological control of naturally occurring bacteria and fungi in Rhizoctonia diseases. Clonostachys rosea f. soil are being explored for fi eld vegetable catenulata (Gilman & Abbot) Schroers production and protection. (Bionectriaceae) is also available com- The mechanism of antagonism by a mercially as a formulated biological control Streptomyces isolate (Di944) from a S. agent (Prestop® WP and Prestop® Mix) with lycopersicum rhizosphere has been investi- broad-spectrum activity against plant gated intensively (Sabaratnam, 1999). pathogens. A wettable powder formulation Spore germination and mycelial growth of of C. rosea f. catenulata reduced damping- several common, fungal root pathogens, off in bedding plant seedlings grown in a including Fusarium oxysporum Schlech- Chapter 67 449

tend: Fries f. sp. radicis-lycopersici W.R. (Wallr.) S.J. Hughes (Glomerellaceae) and T. Jarvis and Shoemaker (Nectriaceae), basicola. The active agent Di944 identifi ed Thielaviopsis basicola (Berk. and Broome) as Streptomyces griseocarneus Benedict Ferraris (Ceratocystideaceae), Botrytis (Streptomycetaceae) by 16S DNA sequenc- cinerea Pers. (Sclerotinaceae) and ing (Hynes et al., 2008) is being formulated Verticillium dahlia Kleb. (Plectosphaerella- by microencapsulation to facilitate its ceae), were shown to be inhibited in vitro application as sprays to plant surfaces by a pentaene macrolide extracted from while maintaining effi cacy to biologically culture fi ltrates of the Di944 isolate control Rhizoctonia diseases. Micro- (Sabaratnam, 1999). The inhibition was encapsulation of S. griseocarneus Di944 equal to or better than that of other using a novel, complex co-acervation antifungal polyenes such as amphotericin protocol was developed as a means of B, fi lipin, nystatin and candicidin tested in formulating and delivering the bacterial comparison (Sabaratnam, 1999). Fungus biological control agent. Experiments were wall-degrading enzymes, such as chitinase conducted to select compatible micro- and glucanase, are also produced by this encapsulation ingredients including two bacterium and contribute to fungicidal oppositely charged colloids and to activity (Sabaratnam, 1999). Inhibition of determine suitable concentrations of each mycelial growth of a wide range of for favourable development of co-acervates pathogens (Fusarium, Verticillium, Botrytis, (Hynes et al., 2008). Using a similar Thielaviopsis, Pythium (Pythiaceae) and process to microencapsulate Colleto- Phytophthora (Peronospoaceae) spp.) in trichum truncatum (Schwein.) Andrus and dual cultures with isolate Di944 was W.D. Moore (Glomerellaceae), a complex reported (Sabaratnam, 1999). Subsequent co-acervation consisting of an aqueous studies have shown that this Streptomyces suspension of vegetative cells of S. isolate (Di944) can also suppress these root griseocarneus Di944 emulsifi ed with pathogens in tomato plug transplants in the surfactant and non-refi ned vegetable oil greenhouse, if applied as amendments to (the formulation core), is micro- the potting medium prior to inoculation encapsulated in gelatin-gum arabic (the (Traquair et al., 2012). formulation shell) (Hynes et al., 2010). Numerous formulations and delivery Stachybotrys elegans (Pidopl.) W. Gams methods have been evaluated for the (incerta sedis) and binucleate, non- rhizosphere streptomycete Di944 (Sabarat- pathogenic strains of Rhizoctonia (Cerato- nam, 1999). Freeze-dried vegetative propa- basidium) sp. (Ceratobasidiaceae) are being gules from liquid fermentations were tested investigated in Quebec for biological as a talcum powder, durum fl our (starch- control of R. solani on potato and other pesto) and alginate bead formulations crops (Benyagoub et al., 1994). Binucleate (Sabaratnam and Traquair, 2002). Low Rhizoctonia spp. have been reported as temperature (4°C) storage enhanced the potential biological control agents of R. shelf life of formulations. Delivery to solani that cause seedling damping-off in tomato transplants by seed coating or by cotton, Gossypium hirsutum L. (Malva- amendment to the peat-based potting mix ceae) (Jabaji-Hare and Neate, 2005). Based were examined. Talcum powder formu- on the fundamental knowledge of the lations were shown to be the most stable in mechanism of antagonism for the myco- storage and the most effective in biological parasite S. elegans (Morissette et al., 2006; control of Rhizoctonia damping-off, if Chamoun and Jabaji, 2011), powerful PCR applied by seed coating (Sabaratnam and and molecular gene expression tech- Traquair, 2002). Older tomato transplants nologies are being employed to detect R. stressed by drought and nutrient defi ciency solani and S. elegans (Morissette et al., are also susceptible to infection by root 2008) in the natural environment. Fungal rotting fungi such as F. oxysporum f. sp. cell wall-degrading enzymes such as radicis-lycopersici, Colletotrichum coccodes chitinases and glucanases are being 450 Chapter 67

induced and activated in S. elegans in improved the percentage of healthy radish response to exposure to R. solani seedlings established (22–72% healthy (Chamoun and Jabaji, 2011). Real-time PCR seedlings compared to 2% in the untreated and marker genes are being used to control) (Abbasi et al., 2007a). Levels of expedite detection and quantifi cation of Rhizoctonia suppression increased with the biological control agents, including S. incubation time prior to planting. Disease elegans and non-pathogenic binucleate suppression in peat-based mix amended Rhizoctonia (Ceratobasidium) isolates with CDS is believed to be due to microbial (Wen et al., 2005; Morissette et al., 2008). activity in the potting medium and not by Utilizing radish-Rhizoctonia growth direct toxicity of organic acids present in room plant bioassay, Abbasi et al. (2004) the CDS (Abbasi et al., 2009b). Suppression have been investigating the effects of effi cacy of peat-based potting medium various organic amendments on seedling amended with CDS was increased also by damping-off and root rot in artifi cially addition of the biological control agent T. infested peat-based substrates and agri- hamatum 382 (Abbasi et al., 2009b). cultural soils. Fish emulsion (FE) derived from menhaden fi sh, an organic foliar fertilizer with disease-suppressing activity, 67.5 Future Needs can enrich fertility and enhance microbial activity in potting substrates or soils Future work should include: (Lazarovits et al., 2009; Abbasi, 2011). In 1. Tailoring the biological control agent to peat-based potting mix treated with 4% FE the physical, chemical and biological con- 7 days prior to seeding, 70–80% of the text into which it is introduced, as recom- seedlings remained disease-free, while mended by Handelsman (2002) as the best potting mix treated 28 days prior to seeding approach to address the challenges of con- with 1% FE provided similar high levels of sistency of the biological control effi cacy, protection (Abbasi et al., 2004). Adding sustainability of bioactive agents and com- 0.5% FE into a R. solani-infested sandy- patibility with the microbial community; loam soil 5 days prior to planting radish 2. Modern molecular and biochemical seed suppressed Rhizoctonia damping-off approaches to enable the fundamental eco- similarly (Abbasi et al., 2004). Increased logical studies of subtle interactions taking microbial activity and the addition of large place in these microenvironments on or amounts of fungitoxic organic acids have near plant surfaces in order to facilitate the major roles in Rhizoctonia suppression in development of more effective formula- FE-amended soil and potting substrates tions of biological control organisms and (Abbasi et al., 2004, 2009a). To address organic amendments; concerns about variability and consistent 3. The use of biological agents and organic effi cacy in different batches of industrial amendments with wide host ranges or use organic amendments, the effect of spiking of combinations of biological agents and with known biological control agents was organic amendments in order to control explored. Trichoderma hamatum (Bonord.) more than one disease simultaneously, Bainier (Hypocreaceae) 382 was added to a reduce variability and inconsistency, non-suppressive batch of the peat-based increase effi cacy and enhance cost effec- mix and 1% FE in a growth room bioassay. tiveness of biological control measures. The combination of T. hamatum 382 and FE increased the percentage of healthy seedlings and reduced damping-off severity (Abbasi, 2011). Corn distillate solids (CDS) Acknowledgements are also effective pre-planting amendments in growth room assays. Amendment of a R. The research collaborations of Dr George solani-infested peat-based mix with 1–4% Lazarovits and Dr Ken Conn are gratefully CDS 1 week before planting seeds acknowledged. Research was funded in Chapter 67 451

part by grants from Omega Protein, and Engineering Research Council of Commercial Alcohol Inc., Agricare Ltd, the Canada and the Ontario Research Agriculture and Agri-Food Matching Enhancement Programme operated by Investment Initiative, the Natural Sciences Agriculture and Agri-Food Canada.

References

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68 Streptomyces scabies Lambert and Loria, Common Scab or Potato Scab (Streptomycetaceae), and Verticillium dahliae Klebahn, Verticillium albo-atrum Reinke and Berthhold, Verticillium Wilt (Plectosphaerellaceae)

Pervaiz A. Abbasi Agriculture and Agri-Food Canada, London, Ontario

68.1 Pest Status (Goyer et al., 1996; Loria et al., 1997, 2006) of which S. scabies Lambert and Loria (= S. Common scab of potato, Solanum scabiei Lambert and Loria) (Plectosphaerel- tuberosum L. (Solanaceae), or potato scab laceae) is the predominant causal agent is caused by multicellular, soil-inhabiting, (Lambert and Loria, 1989; St-Onge et al., fi lamentous Gram-positive actinobacteria 2008). The pathogenic strains of Strepto- belonging to several Streptomyces spp. myces spp. also cause scab symp toms on

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 454 Chapter 68

the fl eshy roots of beet, Beta vulgaris L. aubergine, Solanum melongena L. (Solana- (Amaranthaceae), carrot, Daucus carota ceae), and other broadleaf crops (Rowe and subsp. sativus Schülb. and M. Martens, Powelson, 2002; Powelson and Rowe, parsnip, Pastinaca sativa L. (Apiaceae), 1993). Typical symptoms of verticillium radish, Raphanus sativus L., turnip, wilt include chlorosis, stunting, premature Brassica rapa var. rapa L. (Brassicaceae), defoliation and wilting. The fungus can and other taproot crops (Howard et al., survive as microsclerotia in soil or as 1994). The pathogen attacks the newly mycelium on plant debris in soil for developing young tubers through lenticels several years in the absence of susceptible and infection can lead to shallow, raised, hosts and poses a long-term threat to potato or deep-pitted lesions on tubers depending production in infested soils (Schnathorst, on the Streptomyces strain and the soil 1981). Microsclerotia are the principal environment (Goyer et al., 1996; Loria et source of inoculum and their germination al., 1997, 2006). The pathogenic strains of in rhizosphere soil or its vicinity is Streptomyces spp. produce the phytotoxin stimulated by root exudates. After germin- thaxtomin A, which is essential for ation, the mycelium penetrates plant roots induction of common scab symptoms in and moves to the vascular tissues, blocking potato (King et al., 1991; Babcock et al., the movement of water (Schnathorst, 1993; Goyer et al., 1996; Kers et al., 2005). 1981). Pathogen inoculum is spread by The pathogen survives as mycelia or spores contaminated tuber pieces and infested soil on infected plant tissues in the soil and the by farm equipment and/or irrigation water inoculum is spread by rain and wind- (Howard et al., 1994). It is believed that blown soil or by infected or contaminated plant-parasitic root-lesion nematodes also tubers (Kritzman and Grinstein, 1991; play an important role in enhancing the Howard et al., 1994). Scab is generally incidence and severity of verticillium wilt most severe in dry soils at soil disease in potatoes (Powelson and Rowe, temperatures of 20–22°C. Potato scab has 1993; Back et al., 2002; Rowe and become increasingly important in recent Powelson, 2002; Rotenberg et al., 2004). years due to the demand for a blemish-free, high-value product and low tolerances for pathogen presence in seed tubers. 68.2 Background Verticillium wilt is caused by the soil- borne fungi Verticillium dahliae Klebahn There is no single effective strategy and V. albo-atrum Reinke and Berthhold currently available to control either potato (Plectosphaerellaceae). Both species may scab or verticillium wilt. Fumigation with be present in the same fi eld or even on the chemical sterilants such as metam sodium, same plant (Howard et al., 1994). chloropicrin and other chemicals (Rowe Verticillium dahliae produces thick-walled and Powelson, 2002; Goicoechea, 2009) microsclerotia whereas V. albo-atrum can reduce soil populations of these patho- produces dark resting mycelium instead of gens, which may lead to disease sup- microsclerotia. Although V. albo-atrum is pression. These chemicals, however, are generally considered more pathogenic than not always available, can be expensive, V. dahliae, it is not the more widespread or potentially dangerous to apply and predominant of the two species, particu- environ mentally undesirable. Their larly in Canada. It may, however, have application may also lower populations of simply been overlooked since it is not non-target benefi cial soil microorganisms, known to produce microsclerotia. World- which could lead to increased pathogen wide, the disease causes early dying of populations as antagonism and com- leaves and stems leading to severe yield petition are eliminated. Foliar sprays of reductions in a variety of important crops some chemicals are reported to inhibit including potato, tomato, Solanum lyco- common scab symptoms on tubers (Tegg et pericum L., peppers, Capsicum annum L., al., 2008, 2012) but they also reduce yield. Chapter 68 455

Some cultivars with good to intermediate potato scab and increased tuber yield in resistance against common scab are plots rotated with barley under-seeded available, but resistant cultivars have not with rye prior to planting potatoes. In a replaced the most widely grown cultivars. recent study, green manure rotations with No cultivars with good resistance against disease-suppressive crops such as high- both species of the verticillium wilt glucosinolate mustard blend or sorghum- pathogen are currently available (Howard sudangrass hybrid modestly reduced et al., 1994). Several other management verticillium wilt in the subsequent potato practices can reduce these diseases crop compared to the standard barley, including: increasing soil pH, irrigation Hordeum vulgare L. (Poaceae), control during tuber setting, soil amendment with (Larkin et al., 2011). Potato tubers green manures and composts, crop harvested from plots amended with the rotations and biological control. Some of mustard blend also had less common scab. these methods may be costly or not Their study suggested that multiple years practical. of these crops may be needed prior to Green manuring with a variety of plant planting potatoes to substantially reduce species has been used to manage soil-borne disease in heavily infested fi elds. In a pathogens of potato scab and verticillium greenhouse study, potato plants produced wilt. Soil amendment using a combination in soils amended with vegetable compost of soybean, Glycine max (L.) Merr. and wood-chip polyacrylamide cores (Fabaceae), green manuring with partially showed signifi cantly lower infection rates decomposed wheat, Triticum aestivum L. of V. dahliae compared to manure and (Poaceae), straw effectively reduced potato vegetable composts alone (Entry et al., scab with a decrease of 57% in disease 2005). It is known that utilization of severity and 55% in disease incidence, organic amendments, crop residues, or accompanied by a 14% increase in tuber green manures can also dramatically affect yield (Mishra and Srivastava, 2004). soil microbial communities and dynamics Wiggins and Kinkel (2005) used green (Garbeva et al., 2004; Mazzola, 2007; manures of buckwheat, Fagopyrum Larkin et al., 2011; Bernard et al., 2012) esculentum Moench (Polygonaceae), and thereby serving as important components canola, Brassica napus L. (Brassicaceae), in establishing and maintaining soil interspersed with rotations of maize, Zea suppressiveness. mays L. (Poaceae), and lucerne, Medicago sativa L. (Fabaceae), to reduce verticillium wilt and potato scab and increase tuber 68.3 Biological Control yields. Similarly, soil incorporation of high rates of residues of broccoli, Brassica 68.3.1 Microbial agents oleracea L. convar. oleracea (Brassicaceae) (Ochiai et al., 2007), or other plant species Biological control with microbial agents (Ochiai et al., 2008) in fi eld plots used for has potential for the management of potato potato production reduced verticillium scab and verticillium wilt. Suppressiveness wilt disease. Larkin and Griffi n (2007) against these pathogens can develop noted a modest reduction (25%) of naturally in potato fi elds. Streptomyces common scab on potato tubers produced in strains are common soil inhabitants and fi eld plots rotated with Indian mustard, the majority of them are non-pathogenic. Brassica juncea (L.) Czern. (Brassicaceae), These non-pathogenic strains are generally as green manure prior to planting potatoes. found in soils suppressive to potato scab In fi eld trials with biological amendments and have shown some success in reducing and various crop rotations, Larkin (2008) common scab on progeny tubers (Neeno- showed that soil application of a Eckwall et al., 2001; Prévost et al., 2006; combination of compost tea and a mixture Hiltunen et al., 2009). These strains are of benefi cial microorganisms reduced often isolated from potato tuber tissues or 456 Chapter 68

even from scab lesions and some may 68.3.2 Organic soil amendments produce antibiotics to inhibit the growth of pathogenic S. scabies (Neeno-Eckwall et Biological control can also be accom- al., 2001). Attempts have also been made to plished by adding organic amendments use bacteriophages for scab control. In an that stimulate the activity of resident in vivo study, McKenna et al. (2001) biological control agents, leading to the applied a polyvalent phage that infected S. establishment of natural disease-sup- scabies as seed tuber treatment to suppress pressive conditions (Hoitink and Boehm, seed-borne infection of common scab. 1999; Abbasi et al., 2007b; Diallo et al., However, fi eld suppression of common 2011). While organic soil amendments scab has yet to be shown. from agriculture-related industry have been Rhizosphere bacteria may play a key used for centuries as fertilizers, their role in biological control of these soil- effects on plant diseases have also been borne pathogens. The bacteria isolated noticed. In general, plant diseases caused from rhizospheres of potato or other plant by soil-borne plant pathogens are less species have shown antagonistic activity severe in soils receiving organic amend- against soil-borne potato pathogens (Berg et ments (Davis et al., 2001; van Bruggen and al., 2002, 2006; Krechel et al., 2002) and Temorshuizen, 2003), and such organic may play a role in soil suppressiveness. In soils generally have had higher biological greenhouse and fi eld trials, Uppal et al. diversity (van Diepeningen et al., 2006). It (2008) showed that soil or seed application is also well known that these organic of some plant extracts and biological amendments increase the activity and control bacteria can reduce verticillium diversity of resident microbial com- wilt in potatoes. An extract of Canada milk munities by increasing the organic matter vetch, Astragalus canadensis L. (Faba- content of the amended soil (Mäder et al., ceae), showed the highest level of pro- 2002), which is an important soil com- tection against verticillium wilt and also ponent for improving soil and plant health induced very high levels of the fl avonol- (Magdoff and Weil, 2004). glycoside rutin in the tuber tissues (El Organic amendments can also revitalize Hadrami et al., 2011). Coating of potato potato soils depleted in organic matter due seed piece tubers with Pseudomonas sp. to intensive cultivation. They can also LBUM 223 prior to planting in S. scabies- retain and provide nutrients to plants, infested soil protected progeny tubers improve soil physical, chemical and against common scab disease (St-Onge et biological properties, and increase soil al., 2011). Recently in a fi eld study from buffering capacity (Grandy et al., 2002; New Brunswick, Al-Mughrabi (2010) Carter et al., 2004). Such changes can reported a reduction in scab severity on create conditions that are suppressive to potato tubers harvested from fi eld plots soil-borne plant pathogens (Davis et al., grown from tuber seed pieces treated with 2001; Bailey and Lazarovits, 2003). the biological control bacteria Pseudo- Agricultural soils naturally suppressive to monas fl uorescens (Flügge) Migula soil-borne plant pathogens have been (Pseudomonadaceae) and Enterobacter identifi ed worldwide (Alabouvette, 1999; cloacae (Jordan) Hormaeche and Edwards Weller et al., 2002). The basis of sup- (Enterobacteriaceae). Although manage- pressiveness in most cases has been ment of potato soil-borne diseases with attributed to biological activity (Weller et microbial agents has great potential, the al., 2002), but soil chemical and physical main concern is lack of consistent results, factors may also play a role. While it is particularly under fi eld conditions. It may possible to artifi cially create sup- be more useful to combine the use of pressiveness in soils, conditions may be biological control agents with other control specifi c and unique for each soil. For options as part of an integrated disease instance, incorporating most organic management system. amendments into soil can lead to this long- Chapter 68 457 term effect. The decomposition of some Ammonium lignosulfonate (ALS), neem organic amendments can also result in the cake and maize distillation products are generation of compounds that kill plant among the plant-based products tested for pathogens (Lazarovits, 2001; Abbasi et al., suppression of potato scab and/or 2005, 2007b; Lazarovits et al., 2005). The verticillium wilt. ALS, derived from spent short-term effects that result in an sulfi te liquors produced during the wood immediate reduction of pathogen inoculum pulping process, applied as a pre-plant soil may be more specifi c to a particular type of amendment provided control of potato amendment (Tenuta and Lazarovits, 2002; scab and verticillium wilt in several Mazzola et al., 2007). For example, high commercial fi elds in Ontario and Prince nitrogenous and volatile fatty acid (VFA)- Edward Island (Soltani et al., 2002). Single containing amendments elicit an almost application of ALS reduced the incidence immediate reduction in pathogen popu- of verticillium wilt and potato scab in all lations via short-lived toxic metabolites locations in the year of application (Soltani (Tenuta et al., 2002; Conn et al., 2005; et al., 2002; Lazarovits et al., 2008). Disease Lazarovits et al., 2005, 2009; Abbasi et al., severity remained lower in subsequent 2009; Abbasi, 2011). years in some locations when potatoes Using potato as a model system, we were replanted into the same soils without have investigated the effects of various further addition of ALS. The reduction of organic soil amendments on common scab potato scab or verticillium wilt was not and verticillium wilt, which are often site- or soil-specifi c. ALS treatment also found in the same potato fi eld. Most of the increased total microbial populations and organic material in our investigations was diversity, particularly that of fungi (Soltani sourced from agriculture-related industry et al., 2002); any specifi c role in disease and included by-products of animal, reduction was, however, not investigated. poultry or fi sh processing, plant-based Neem cake is a high nitrogen-containing products and manures or composts. Use of (6.4%) organic material derived from seed organic soil amendments such as animal of the neem tree, Azadirachta indica A. manures and composts is a common Juss. (Meliaceae). Addition of neem cake to practice in organic agriculture, and one of agricultural soils before planting reduced the long-term effects of adding these the viability of microsclerotia of V. dahliae, materials to agricultural soils is enhanced depending upon the rates of neem cake and biological control of soil-borne plant the soil types (Abbasi et al., 2005). Adding pathogens by increasing the number and higher rates of neem cake to soil may not diversity of resident microbial com- be economical and may, indeed, be munities. As described below, the disease- phytotoxic. Maize distillation products or suppressing effects of these organic condensed distillers’ solubles (CDS) are amendments were either assessed in products remaining after the removal of commercial potato fi elds with a history of ethyl alcohol by distillation from yeast these two diseases or in greenhouse trials fermentation of maize and condensing the or micro-plots with soils from these fi elds. thin stillage fraction to a semi-solid. These In general, the rates of these organic products have been utilized as cattle feed. amendments used in suppression of potato CDS is a promising material for increasing scab and verticillium wilt were very high soil organic matter content, improving soil and may not be economically feasible for physical properties and retaining soil commercial application. Unfortunately, nutrients. Addition of CDS to a potato soil long-term studies with low application 2 weeks before planting aubergine reduced rates of these and other organic soil verticillium wilt disease (Abbasi et al., amendments at the same fi eld locations are 2007a). Similarly, a CDS pre-plant soil rare. These specifi c studies are needed to amendment reduced potato scab severity in monitor and exploit the potential of natural a potato soil with medium levels of disease biological control. pressure under greenhouse and micro-plot 458 Chapter 68 conditions, but was not as effective in the compared to control plots (Abbasi et al., fi eld. However, numbers of marketable 2006). Although FE signifi cantly reduced tubers (<5% surface scab) were signifi - petiole infection by V. dahliae in only one cantly increased under all three conditions. soil, a similar trend of reduced petiole Soil incorporation of an organic fertil- infection was observed in most soils. In izer made from poultry feathers (Nature fi eld trials at two sites located in grower Safe®,10-2-8) at a broadcast rate of 8.6 t ha−1 fi elds, soil incorporation of FE at 20,000 l in two commercial potato fi elds in Prince ha−1 reduced scab severity, increased the Edward Island 3 weeks before planting percentage of disease-free tubers by 132– potatoes reduced scab severity; 90% of the 366%, and increased marketable tuber harvested tubers were marketable in the yield by two-fold compared to control plots year of application at both sites (Lazarovits at both sites (Abbasi et al., 2006). FE et al., 2008). The amendment effect reduced potato scab and verticillium wilt persisted for a second year, but in the third in soils of different characteristics and pH. year after the amendment incorporation the The results, however, also indicated that FE scab severity on tubers from the treated may not be effective in soils showing very plots was not different from that recorded high scab severity on tubers. Uniform in control plots (Lazarovits et al., 2008). It incorporation of organic material into fi eld is further recommended that this product plots may be a key to consistent fi eld should only be applied in the furrows to effectiveness in disease suppression. Most reduce the total N on a per hectare basis. recent long-term studies indicated that Fish emulsion (FE) derived from economically feasible and ten-fold lower menhaden fi sh, Brevoortia patronus Goode rates (2000 l ha−1) of FE can also provide and B. tyrannus (Latrobe) (Clupeiformes: effective suppression of soil-borne potato Clupeidae), is an organic foliar fertilizer diseases and improve marketable and total with disease-suppressing activity against tuber yields (Abbasi, 2013). This potato soil-borne pathogens (Abbasi et al., 2004). disease suppression by low rates of FE is The effects of FE as a pre-plant soil most likely due to biological control. FE amendment on verticillium wilt and potato may be a promising material for increasing scab in various soils of different soil organic matter content and for characteristics (pH 5.2–7.2, organic matter changing the disease profi le of a potato soil. 1.0–3.7%) from commercial potato fi elds in Ontario, New Brunswick, and Prince Edward Island with a history of 68.5 Evaluation of Biological Control verticillium wilt and scab were examined in greenhouse, micro-plot and fi eld Although several studies have documented experiments (Abbasi et al., 2006). In some success, the use of biological control greenhouse trials, FE pre-plant amendment agents for control of potato scab and (0.5 and 1% mass/mass soil) to an infested verticillium wilt is still in its infancy. potato soil protected aubergine from Seed-potato tubers offer an ideal avenue in verticillium wilt and reduced disease terms of surface area to introduce high incidence by 77–89% and disease severity densities of biological control agents. by 2.1–2.2 units relative to control (Abbasi Organic amendments can also be used as et al., 2006). In micro-plots consisting of carriers for biological control agents. plastic drainage tiles (25 cm × 25 cm) Indigenous soil microbial communities buried into a sandy-loam soil, FE was generally contribute to disease suppression applied to 11 soils from commercial potato by reducing and competing with pathogen fi elds from three provinces. The 1% FE populations. Organic soil amendments can treatment signifi cantly reduced potato scab infl uence these communities and enhance severity in seven soils with low to medium their biological control effectiveness. Man- scab disease pressure and increased total agement of these benefi cial microbial tuber yield by 41–170% in nine soils communities for suppression of soil-borne Chapter 68 459 potato diseases and plant growth pro- production and management approach to motion through the use of organic soil reduce overall losses from multiple plant amendments has great potential. As diseases; described above, very high broadcast rates 3. Creating disease-suppressing conditions of some of these organic amendments were in infested soils with more frequent appli- required for effective disease control. cation of very low rates of these organic While high application rates of organic materials; amendments may not be practical or 4. Establishing long-term fi eld studies uti- economically feasible for commercial use, lizing various soil amendments for disease they may not be required to establish long- management on the same fi eld plots to term biological control. It may be monitor changes in disease profi le and soil economical if the disease control effect microbial communities. persists for multiple years after a single soil application. In addition, the costs could possibly be lowered by applying the Acknowledgements material only in-furrow or in bands precisely targeting the root zones. Many individuals including technicians, term employees, summer and co-op students, fi eld crews and potato growers 68.6 Future Needs have made signifi cant contributions to this research in several ways during the past Further work should include: several years. Technical assistance of Brian 1. Characterizing benefi cial microbial com- Weselowski, Igor Lalin, Jackie Hill and munities from the potato rhizosphere after Rebecca Earl, and the collaborative work of enrichment with organic substrates and Dr George Lazarovits, Dr Kenneth L. Conn elucidating their role in suppression of and Mr Bruce Reynolds is highly soil-borne pathogens and in plant growth appreciated and acknowledged. This promotion – a consortium of the selected research was funded by grants from De organisms can then be reintroduced with Cloet Ltd, Omega Protein, Commercial an organic substrate to confi rm and further Alcohol Inc. and the Agriculture and Agri- enhance their role in disease suppression; Food Canada Matching Investment 2. Developing and applying a holistic crop Initiative.

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Hoitink, H.A.J. and Boehm, M.J. (1999) Biocontrol within the context of soil microbial communities: a substrate dependent phenomenon. Annual Review of Phytopathology 37, 427–446. Howard, R.J., Garland, J.A. and Seaman, W.L. (1994) Diseases and Pests of Vegetable Crops in Canada. Canadian Phytopathological Society and Entomological Society of Canada, Ottawa, Ontario. Kers, J.A., Cameron, K.D., Joshi, M.V., Bukhalid, R.A., Morello, J.E., Wach, M.J., Gibson, D.M. and Loria, R. (2005) A large, mobile pathogenicity island confers plant pathogenicity on Streptomyces species. Molecular Microbiology 55, 1025–1033. King, R.R., Lawrence, C.H. and Clark, M.C. (1991) Correlation of phytotoxin production with pathogenicity of Streptomyces scabies isolates from scab infected potato tubers. American Potato Journal 68, 675–680. Krechel, A., Faupel, A., Hallmann, J., Ulrich, A. and Berg, G. (2002) Potato-associated bacteria and their antagonistic potential towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Canadian Journal of Microbiology 48, 772– 786. Kritzman, G. and Grinstein, A. (1991) Formalin application against soil-borne Streptomyces. Phytoparasitica 19, 248. Lambert, D.H. and Loria, R. (1989) Streptomyces scabies sp. nov., nom. rev. International Journal of Systematic Bacteriology 39, 387–392. Larkin, R.P. (2008) Relative effects of biological amendments and crop rotations on soil microbial communities and soilborne diseases of potato. Soil Biology and Biochemistry 40, 1341–1351. Larkin, R.P. and Griffi n, T.S. (2007) Control of soilborne potato diseases using Brassica green manures. Crop Protection 26, 1067–1077. Larkin, R.P., Honeycutt, C.W. and Olanya, O.M. (2011) Management of Verticillium wilt of potato with disease-suppressive green manures and as affected by previous cropping history. Plant Disease 95, 568–576. Lazarovits, G. (2001) Management of soilborne plant pathogens with organic soil amendments: a disease control strategy salvaged from the past. Canadian Journal of Plant Pathology 23, 1–7. Lazarovits, G., Conn, K.L., Abbasi P.A. and Tenuta, M. (2005) Understanding the mode of action of organic soil amendments provides the way for improved management of soilborne plant pathogens. Acta Horticulturae 698, 215–225. Lazarovits, G., Conn, K.L., Abbasi P.A., Soltani, N., Kelly, W., MacMillan, E., Peters, R.D. and Drake, K.A. (2008) Reduction of potato tuber disease with organic soil amendments in two Prince Edward Island fi elds. Canadian Journal of Plant Pathology 30, 215–225. Lazarovits, G., Abbasi, P.A., Conn, K.L., Hill, J. and Hemmingsen, S.M. (2009) Fish emulsion and liquid swine manure: model systems for development of organic amendments as fertilizers with disease suppressive properties. In: Bettiol, W. and Morandi, M.A.B. (eds) Biocontrole de Doenças de Plantas: Uso e Perspectivas. Embrapa Meio Ambiente Jaguariúna, São Paulo, Brazil, pp. 49–67. Loria, R., Bukhalid, R.A., Fry, B.A. and King, R.R. (1997) Plant pathogenicity in the genus Streptomyces. Plant Disease 81, 836–846. Loria, R., Kers, J. and Joshi, M. (2006) Evolution of plant pathogenicity in Streptomyces. Annual Review of Phytopathology 44, 469–487. Mäder, P., Fliessbach, A., Dubois, D., Gunst, L., Fried, P. and Niggli, U. (2002) Soil fertility and biodiversity in organic farming. Science 296, 1694–1697. Magdoff, F. and Weil, R.R. (2004) Soil organic matter management strategies. In: Magdoff, F. and Weil R.R. (eds) Soil Organic Matter in Sustainable Agriculture. CRC Press, Boca Raton, Florida, pp. 45–65. Mazzola, M. (2007) Manipulation of rhizosphere bacterial communities to induce suppressive soils. Journal of Nematology 39, 213–220. Mazzola, M., Brown, J., Izzo, A.D. and Cohen, M.F. (2007) Mechanism of action and effi cacy of seed meal-induced pathogen suppression differ in a brassicaceae species and time-dependent manner. Phytopathology 97, 454–460. McKenna, F., El-Tarabily, K.A., Hardy, G.E.St and Dell, B. (2001) Novel in vivo use of a polyvalent Streptomyces phage to disinfest Streptomyces scabies-infected seed potatoes. Plant Pathology 50, 666–675. 462 Chapter 68

Mishra, K.K. and Srivastava, J.S. (2004) Soil amendments to control common scab of potato. Potato Research 47, 101–109. Neeno-Eckwall, E.C., Kinkel, L.L. and Schottel, J.L. (2001) Competition and antibiosis in the biological control of potato scab. Canadian Journal of Microbiology 47, 332–340. Ochiai, N., Powelson, M.L., Dick, R.P. and Crowe, F.J. (2007) Effects of green manure type and amendment rate on verticillium wilt severity and yield of Russet Burbank potato. Plant Disease 91, 400–406. Ochiai, N., Powelson, M.L., Crowe, F.J. and Dick, R.P. (2008) Green manure effects on soil quality in relation to suppression of Verticillium wilt of potatoes. Biology and Fertility of Soils 44, 1013– 1023. Powelson, M.E. and Rowe, R.C. (1993) Biology and management of early dying of potatoes. Annual Review of Phytopathology 31, 111–126. Prévost, K., Couture, G., Shipley, B., Brzezinski, R. and Beaulieu, C. (2006) Effect of chitosan and a biocontrol streptomycetes on fi eld and potato bacterial communities. BioControl 51, 533–546. Rotenberg, D., MacGuidwin, A.E., Saeed, I.A.M. and Rouse, D.I. (2004) Interaction of spatially separated Pratylenchus penetrans and Verticillium dahliae on potato measured by impaired photosynthesis. Plant Pathology 53, 294–302. Rowe, R.C. and Powelson, M.L. (2002) Potato early dying: management challenges in a changing production environment. Plant Disease 86, 1184–1193. Schnathorst, W.C. (1981) Life cycle and epidemiology of Verticillium. In: Mace, M.E., Bell, A.A. and Beckman, C.H. (eds) Fungal Wilt Diseases of Plants. Academic Press, New York, pp. 81–111. Soltani, N., Conn, K.L., Abbasi, P.A. and Lazarovits, G. (2002) Reduction of potato scab and verticillium wilt with ammonium lignosulfonate soil amendment in four Ontario potato fi elds. Canadian Journal of Plant Pathology 24, 332–339. St-Onge, R., Goyer, C., Coffi n, R. and Filion, M. (2008) Genetic diversity of Streptomyces spp. causing common scab of potato in eastern Canada. Systematic and Applied Microbiology 31, 474–484. St-Onge, R., Gadker, V.J., Arseneault, T., Goyer, C. and Filion, M. (2011) The ability of Pseudomonas sp. LBUM223 to produce phenazine-1-carboxylic acid affects the growth of Streptomyces scabies, the expression of thaxtomin biosynthesis genes and the biological control potential against common scab of potato. FEMS Microbiology Ecology 75, 173–183. Tegg, R.S., Gill, W.M., Thompson, H.K., Davies, N.W., Ross, J.J. and Wilson, C.R. (2008) Auxin- induced resistance to common scab disease of potato linked to inhibition of thaxtomin A toxicity. Plant Disease 92, 1321–1328. Tegg, R.S., Corkrey, R. and Wilson, C.R. (2012) Relationship between the application of foliar chemicals to reduce common scab disease of potato and correlation with thaxtomin A toxicity. Plant Disease 96, 97–103. Tenuta, M. and Lazarovits, G. (2002) Ammonia and nitrous acid from nitrogenous amendments kill the microsclerotia of Verticillium dahliae. Phytopathology 92, 255–264. Tenuta, M., Conn, K.L. and Lazarovits, G. (2002) Volatile fatty acids in liquid swine manure can kill microsclerotia of Verticillium dahliae. Phytopathology 92, 548–552. Trüper, H.G. and dè Clari, L. (1997) Taxonomic note: necessary correction of specifi c epithets formed as substantives (nouns) ‘in apposition’. International Journal of Systematic Bacteriology 47, 908–909. Uppal, A.K., El Hadrami, A., Adam, L.R., Tenuta, M. and Daayf, F. (2008) Biological control of potato verticillium wilt under controlled and fi eld conditions using selected bacterial antagonists and plant extracts. Biological Control 44, 90–100. van Bruggen, A.H.C. and Termorshuizen, A.J. (2003) Integrated approaches to root disease management in organic farming systems. Australasian Plant Pathology 32, 141–156. van Diepeningen, A.D., de Vos, O.J., Korthals, G.W. and van Bruggen, A.H.C. (2006) Effects of organic versus conventional management on chemical and biological parameters in agricultural soils. Applied Soil Ecology 31, 120–135. Weller, D.M., Raaijmakers, J.M., McSpadden Gardener, B.B. and Thomashow, L.S. (2002) Microbial populations responsible for specifi c soil suppressiveness to plant pathogens. Annual Review of Phytopathology 40, 309–348. Wiggins, B.E. and Kinkel, L.L. (2005) Green manures and crop sequences infl uence potato diseases and pathogen inhibitory activity of indigenous streptomycetes. Phytopathology 95, 178–185. Chapter 69 463

69 Taphrina deformans (Berk.) Tul., Peach Leaf Curl (Taphrinaceae)

James A. Traquair1 and Antonet M. Svircev2 1Agriculture and Agri-Food Canada, London, Ontario; 2Agriculture and Agri-Food Canada, Vineland, Ontario

69.1 Pest Status infect delicate leaf tissues throughout the bud-break period in cool (less than 20°C), Taphrina deformans (Berk.) Tul. (Taphrina- wet weather. Mature leaves in the summer ceae) causes leaf curl disease of peach, are not susceptible but ascospores and Prunus persica (L.) Batsch, and nectarine, yeast-like blastoconidia can survive the P. persica var. nucipersica Dippel (Rosa- winter at low frequencies (Buck et al., ceae), and is a persistent fungal pathogen 1998) on twig bark and bud scales to re- in all the major peach production areas of infect emerging leaves during the following Canada. Major losses can be expected if spring (Jones and Sutton, 1984; Ogawa et protective control measures are not taken. al., 1995; Rossi et al., 2007). Symptoms fi rst appear on young develop- ing leaves in the spring, shortly after fl owering. Yellow to reddish leaf patches 69.2 Background thicken and pucker progressively and cause the developing leaves to curl. Peach leaf curl can be controlled effect- Swollen reddish patches take on a grey, ively by a single, preventative spray of felted appearance as asci develop below chemical fungicide during the dormancy of the puckered leaf cuticle. Green shoots the tree in the autumn after leaf drop or in and, more rarely, green fruits can be the spring before bud-break. Registered infected also. Premature defoliation products include Ferbam® (dithiocarba- compromises fruit set and winter survival mate) and Bravo® (chlorothalonil) for com- of trees (Jones and Sutton, 1984; Ogawa et mercial growers and lime-sulfur for home al., 1995). gardeners (Ogawa et al., 1995; Anonymous, Ascospores are forcibly ejected from a 2012). There are no immune varieties of palisade-like layer of asci produced on peach although cv. Redhaven and its intercellular mycelium just below the derivatives have a low degree of tolerance. cuticle of infected and swollen epidermal Sanitation has no impact on leaf curl tissues. They quickly bud as blastoconidia management. Any attempts to control leaf and are washed by spring rains to infection curl after symptoms are observed are sites on emerging leaves. These blasto- ineffective. The vigour of infected trees conidia and ascospores are carried in water must be carefully managed by proper fi lms to new infection sites and continue to fertilization and irrigation.

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 464 Chapter 69

69.3 Biological Control Agents ferbam. For greater disease pressure, two applications of the recommended rate Natural microbial competitors occur on were required to match the control by peach bark. Early microbial analysis of ferbam (Traquair et al., 2008). Harvest peach bark revealed culturable antagonistic yields of peaches were increased by use of bacteria and fungi in the cracks and the biological control agent Serenade® fi ssures of the bark of peach twigs at all Max (Traquair et al., 2008). Production of a times of the year (Wensley, 1971). diffusible antifungal substance appeared to Populations were especially high in the be the mechanism of suppression based on summer months but by isolating from observation of cleared inhibition zones surface-sterilized and unsterilized twigs, around B. subtilis isolated from the the microbes were shown to be mainly on Serenade® Max formu lation spot- the bark surface. Subsequent isolations in oculated on overlays of budding showed diverse populations of wild Taphrina blastoconidia on yeast-malt- basidiomycetous yeasts, various potentially glucose agar in Petri dishes (Traquair et antagonistic hyphomycetous fungi, and al., 2008). These observations and epiphytic bacteria in addition to T. interpretations are consistent with the deformans on peach bark, particularly in antagonistic effects of lipoproteins the summer months (Buck et al., 1998). reported for the QST713 strain of B. Microbial competition is likely to subtilis and known to be in the Serenade® contribute to the poor survival of T. Max formulation (Marrone, 2002). deformans in summer months and to lack of infection of new leaves during the summer period. 69.5 Future Needs

Peach leaf curl is managed effectively by 69.4 Evaluation of Biological Control one timely application of fungicide during the dormancy period. However, Serenade® Bacillus subtilis (Ehrenberg) Cohn (Bacilla- Max is a potentially useful biofungicidal ceae) (Serenade® Max, strain QST713) alternative to chemicals and it is an developed by AgraQuest, Inc. in Davis, important tool for organic growers even California, USA, was tested over a 2-year though more than one application may be period in an Ontario orchard (Agriculture required under severe disease pressures. and Agri-food Canada, Vineland Station, Serenade® Max is registered in Canada for Ontario) on two peach cultivars, ‘Loring’ use on pome and stone fruits for other and ‘Elberta’, naturally infested with diseases such as Podosphaera powdery peach leaf curl. Serenade® Max mildew and Monilinia brown rot, respect- (Anonymous, 2011) was sprayed in the ively, caused by fungal pathogens (Anony- early dormant spring period prior to fl ower mous, 2011). Therefore, future work bud-break at half the label recommended should include: rate and the recommended rate in one or two appli cations and compared to stand- 1. Expansion of the Serenade® Max biofun- ard ferbam sprays and water controls. gicide registration to include peach leaf Incidence of leaf curl symptoms in early curl; summer and harvest yield in late summer 2. Inclusion of Serenade® Max biofungi- for Serenade® Max, ferbam and water cide as a useful disease management tool controls were compared. For light disease for organic growers and for integrated dis- pressure, one application of Serenade® ease control strategies for fungal pathogens Max at the recommended 6.8 kg ha−1 rate currently requiring repeated applications controlled peach leaf curl as well as did of chemical fungicides. Chapter 69 465

Acknowledgements through the Risk Reduction and Bio- pesticides Initiative. AgraQuest, Inc., The testing was funded in part by the Pest Davis, California, provided the Serenade® Management Centre (AAFC Ottawa) Max.

References

Anonymous (2011) Serenade® Max, a Wettable Powder Biofungicide. Pest Management Regulatory Agency, Health Canada, Ottawa, Ontario. Anonymous (2012) Publication 360, Guide to Fruit Production 2012–13. Ontario Ministry of Agriculture and Food and Rural Affairs, Toronto, Ontario. Buck, J.W., Lachance, M.-A. and Traquair, J.A. (1998) Mycofl ora of peach bark: population dynamics and composition. Canadian Journal of Botany 76, 345–354. Jones, A.L. and Sutton, T.B. (1984) Diseases of Tree Fruits. Cooperative Extension Service, Michigan State University, East Lansing, Michigan. Marrone, P.G. (2002) An effective biofungicide with novel modes of action. Pesticide Outlook, 13, 193–194. Ogawa, J.M., Zehr, E.I., Bird, G.W., Ritchie, D.F., Uriu, K. and Uyemoto, J.K. (eds) (1995) Compendium of Stone Fruit Diseases. American Phytopathological Society Press, St Paul, Minnesota. Rossi, V., Bolognesi, M. and Giosuè, S. (2007) Seasonal dynamics of Taphrina deformans inoculum in peach orchards. Phytopathology 97, 352–358. Traquair, J.A., Svircev, A. and Singh, B. (2008) Biological control of peach leaf curl with Bacillus subtilis. Phytopathology 98, S158. Wensley, R.N. (1971) The microfl ora of peach bark and its possible relation to perennial canker (Leuscostoma cincta (Fr.) von Hohnel (Valsa cincta)). Canadian Journal of Microbiology 17, 333– 337. 466 Chapter 70

70 Xanthomonas euvesicatoria Jones et al., Xanthomonas perforans Jones et al., Xanthomonas vesicatoria (ex Doidge) Vauterin et al., Xanthomonas gardneri (ex Šutic ˇ) Jones et al., Bacterial Spot of Tomato and Pepper (Xanthomonadaceae)

Diane A. Cuppels and Pervaiz A. Abbasi Agriculture and Agri-Food Canada, London, Ontario

70.1 Pest Status and tip. On pepper leaves, the fi rst symptoms of the disease are small, The majority (90%) of Canadian fi eld greenish, pustular lesions that eventually tomatoes, Solanum lycopersicum L, and develop into large, angular, water-soaked, approximately one-half of Canadian fi eld light reddish brown lesions. Severely peppers, Capsicum annuum L. (Solana- infected plants will defoliate. On tomato ceae), are grown in Ontario; they have fruit, lesions are dark brown to black, may estimated 5-year average annual farm reach a diameter of 4–6 mm and sometimes values (Canada-wide) of approximately appear scabby. On pepper fruit, the CAN$81m and CAN$31m, respectively pathogen forms light brown lesions with a (Agriculture and Agri-Food Canada, 2012). roughened appearance. Major crop loss is The Ontario Processing Vegetable Growers, primarily from the shedding of blossoms the Ontario Field Tomato Committee and and young developing fruit and a reduction the Ontario Minor Use Program have in marketable fruit due to severe fruit identifi ed control of bacterial diseases of spotting. tomato and pepper, particularly bacterial Infested seed is thought to be the spot, as one of their top research priorities primary inoculum source for bacterial spot (Chaput, 2012). Bacterial spot, a disease infection of tomato and pepper plug that is favoured by warm, moist conditions, seedlings and the main avenue for intro- can affect all above-ground parts of the duction of a new race or form of the tomato or pepper plant (LeBoeuf et al., pathogen into Ontario tomato and pepper- 2005). Currently, the predominant species growing areas. The pathogens can persist of the bacterial spot pathogen found in on seed for long periods of time (Bashan et Ontario is X. gardneri (ex Šutic ˇ) Jones et al. al., 1982; Cuppels, 2007). Common seed (Xanthomonadaceae) (Cuppels et al., 2006). treatments to reduce or eliminate these On tomato leaves, these pathogens produce pathogens include thermotherapy (hot irregular, dark brown to black lesions, water, dry heat, or aerated steam), acid which tend to concentrate on the leaf edges dips, antibiotic soaks and chlorination

© Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 70 467

(Cuppels, 2004). Once the pathogen gains to this chemical (Cooksey et al., 1990). entry to a plug greenhouse, it will move Fortunately, copper resistance is not yet through that house very quickly. Disease prevalent among Ontario strains of these may spread from pepper seedlings to pathogens (D. Cuppels, 2009, unpublished tomato seedlings, or vice versa, within the results). Although the use of antibiotics to same greenhouse. Transplants infected control bacterial diseases on fi eld tomatoes with disease-causing bacteria may go and peppers has not been encouraged, undetected because of the lack of visible kasugamycin is currently under review by symptoms or because of diffi culties in the Pest Management Regulatory Agency distinguishing bacterial lesions from those for registration as a minor use pesticide to of other diseases and nutritional and control bacterial spot on greenhouse as physiological disorders. Symptomless but well as fi eld peppers and tomatoes. This infested tomato plug seedlings, which may aminoglycoside antibiotic, originally harbour as many as 100,000 pathogenic isolated in 1965 from Streptomyces bacteria g−1 of tissue (Cuppels and Elm- kasugaensis (Okanishi, Ohta & Umezawa) hirst, 1999), could become an important (Streptomycetaceae), has low toxicity for inoculum source for fi eld epiphytotics. mammals and is not used to treat diseases Additional, potentially important inocu- of humans or animals. Recent US studies lum sources for fi eld plants are volunteer indicate that this antibiotic may have value tomato and pepper plants and weeds found if used at a reduced rate and alternated near tomato fi elds (Jones et al., 1986). with another product in an integrated Xanthomonas gardneri has been found in control programme (Vallad et al., 2010). samples of quackgrass, Elymus repens (L.) The use of chemicals that activate the Gould (Poaceae), and goldenrod, Solidago defence system of the host plant (Hunt et canadensis L. (Asteraceae), from Ontario al., 1996) is another alternative to copper- fi elds that were heavily infected with based pesticide sprays. Typically, these bacterial spot in the previous year (Cuppels biochemical pesticides have activity et al., 2008). Xanthomonas gardneri also is against a wide variety of fungal, bacterial capable of surviving on plant debris in and viral diseases of plants. Syngenta Crop Ontario tomato fi elds over one but not two Protection Inc. has developed an activator winters (Cuppels et al., 2008). called acibenzolar-S-methyl (Actigard™ 50WG). It has been extensively tested as a foliar spray for bacterial spot both in the 70.2 Background USA and Canada (Louws et al., 2001; Abbasi et al., 2002a, b) and has shown At present, there are no bacterial spot- considerable promise. Canadian regis- resistant tomato cultivars available to tration of this compound occurred in 2011 Canadian growers. Although several (Syngenta, 2011). pepper cultivars have tolerance to the Acidic electrolysed water (AEW), or pathogens, there are strains of the electrolysed oxidizing water, has gained pathogens that can overcome all of the signifi cant attention from the food, medical currently known resistance genes (Ritchie, and agricultural industries for use as a 2007). Disease control relies upon using sanitizing agent (Izumi, 1999; Kim et al., treated seed, disease-free transplants, crop 2000a, b). The electrolysis process leads to rotation, cultural methods that eradicate or the generation of reactive oxygen species reduce the inoculum, and a vigorous spray and toxic radicals such as O−, Cl− and OH−, programme with copper-based bacteri- which contribute to the germicidal cides. Unfortunately, spray intervals of properties of AEW (Kim et al., 2000a; Buck greater than 5–7 days or periods of heavy et al., 2002). Electrochemically generated or frequent rainfall drastically reduce their AEW is an environmentally-safe pathogen effectiveness. Furthermore, heavy use of management tool as it is not phytotoxic copper can lead to widespread resistance and has no known residual effects. A 2-min 468 Chapter 70

exposure to AEW, obtained by electrolysis fortifi ed with the biocontrol agent Tricho- of a diluted aqueous solution of 0.045% derma hamatum (Bonord.) Bainier (Hypo- sodium chloride (pH 2.3–2.6, oxidation- creaceae) 382 (FCPB), composted cow reduction potential 1007–1025 mV, and manure mix, or a steam-treated compost- free active chlorine concentration 27–35 amended greenhouse soil and then ppm), reduced the viability of X. inoculated with X. vesicatoria were less vesicatoria cells by 4–8 log units (Abbasi severely diseased than plants grown in and Lazarovits, 2006). Immersion of tomato commercial peat mix or vermiculite. The seed from infected fruit in AEW for 1 or 3 effect varied among the batches of FCPB min signifi cantly reduced surface but not mix used and was lost when the mix was internal X. vesicatoria populations; it had autoclaved. This work suggests that no adverse effect on seed germination. growing tomato transplant seedlings in a Applied as a foliar spray, it also reduced X. compost-based mix such as FCPB, vesicatoria populations and disease although incurring an increased cost to the severity on greenhouse-grown tomato grower, may provide suffi cient initial plants. In the fi eld, multiple sprays of AEW protection to lessen disease development consistently reduced disease severity on both in the greenhouse and the fi eld. tomato foliage. Although its effect on However, more studies are needed to disease incidence and severity on fruit was understand the mechanisms involved and not consistent, fruit yield was either to reduce the level of variability. enhanced or not affected by the AEW In greenhouse and fi eld trials, Abbasi et sprays. Thus, AEW may prove to be a al. (2003) tested foliar applications of fi sh convenient and economical way of emulsion (FE) derived from menhaden disinfesting the surfaces of seeds, fruit, fi sh, Brevoortia patronus Goode and B. foliage and plant cuttings. tyrannus (Latrobe) (Clupeiformes: Clupeidae), and neem oil (NO) extracted from the seed kernels of the neem tree, Azadirachta indica A. Juss. (Meliaceae), 70.3 Biological Control Agents against bacterial spot on tomato and pepper plants. FE, which is used mainly as 70.3.1 Organic extracts a fertilizer, is water-soluble and thus is an ideal product for application as a spray or Composts or compost-amended substrates, with drip irrigation. Greenhouse-grown which can induce systemic resistance, are plants sprayed with an aqueous used to manage diseases in nurseries, but suspension (0.5%, v/v) of either NO or FE the effect can be variable against foliar and then inoculated with the bacterial spot diseases (Zhang et al., 1998; Abbasi et al., pathogen had less disease than the water- 2002a; Pharand et al., 2002; Krause et al., treated controls; however, NO also was 2003). Water extracts of composted cow phytotoxic to the test plants. In the 2-year manure, composted pine bark, organic fi eld study, weekly foliar sprays (0.5%, farm compost and composted yard waste, v/v) of NO and FE consistently reduced applied as foliar sprays on greenhouse- disease severity on the foliage of grown tomato transplants, resulted in a inoculated tomato and pepper plants with moderate reduction in the severity of no signs of phyto toxicity. Although these bacterial spot; composted cow manure treatments signifi cantly reduced disease extract also was shown to suppress foliar severity on pepper fruit, their effect on X. vesicatoria populations (Al-Dahmani et disease incidence on both tomato and al., 2003). Sprays of compost water extract pepper fruit was variable. A signifi cant did not reduce disease severity in fi eld increase in the yield of disease-free trials. In a later report (Aldahmani et al., peppers with NO treatment occurred in 2005), this research group showed that both years. FE contains large quantities of plants grown in composted pine bark mix organic acids that are toxic to pathogens Chapter 70 469

(Abbasi et al., 2009) and it is possible that 70.3.3 Microorganisms these organic acids may have played a role in disease suppression. However, other A number of microorganisms have been mechanisms, such as induced systemic tested for their ability to limit the growth of resistance, may be involved and thus the bacterial spot pathogen X. vesicatoria additional studies focusing on how FE and to lessen the severity of this disease on suppresses disease should be initiated. both greenhouse- and fi eld-grown plants Phosphorus-containing materials such (Byrne et al., 2005). After a preliminary as potassium phosphate fertilizers are greenhouse screening of potential reported to be effective foliar fungicides microbial biological control agents by that can induce disease resistance researchers at Auburn University (Gottstein and Kuc ´, 1989; Reuveni and (Alabama, USA), the most promising of Reuveni, 1998). Ammonium lignosulfonate these strains were fi eld-tested at various (ALS), derived from the spent sulfi te North American locations, including liquors produced during the wood pulping London, Ontario. The highest mean process, also reduces plant disease when reduction in foliar disease occurred when applied as a soil amendment (Soltani et al., plants were sprayed with either Pseudo- 2002). Greenhouse-grown tomato plants monas syringae Van Hall strain Cit7 treated with 2 or 4% (v/v) ALS, 25 mM KP, (28.9% (S.D. = 11.6)) or Pseudomonas or 2% ALS plus 10 mM KP and then putida Trevisan (Pseudomonadaceae) inoculated with the bacterial spot pathogen strain B56 (23.1% (S.D. = 12.2)); but had signifi cantly less disease than the neither treatment consistently reduced water controls (Abbasi et al., 2002b). In a disease incidence on fruit. Although 3-year fi eld study, weekly foliar appli- Pseudomonas fl uorescens (Flügge) Migula cations of these products signifi cantly (Pseudomonadaceae) strain A506 was reduced foliar disease severity on inocu- moderately effective under greenhouse lated fi eld-grown tomato and pepper conditions, it did not consistently suppress plants. disease under fi eld conditions. In a second study (Cuppels and Traquair, 2005), this strain signifi cantly reduced in vitro growth 70.3.2 Bacteriophages of all four bacterial spot-causing xantho- monad species as well as their disease Mixtures of bacteriophages specifi c for the severity under greenhouse conditions. bacterial spot pathogens have been tested When fi eld-tested for activity against X. extensively for their ability to control this vesicatoria and X. gardneri, its perform- disease (Jones et al., 2007). OmniLytics, ance was not consistent. None of the Inc. currently sells bacteriophage in UV- strains tested gave a level of control that protective formulations (AgriPhage™) to merited their use as the sole agent for US growers. Challenges to the routine use disease control. However, they may have of bacteriophage include their extreme value when combined with plant growth- sensitivity to environmental factors such promoting rhizobacteria (PGPR), plant as UV radiation, and the development of resistance activators, or bacteriophage in bacterial resistance. AgriPhage™ is an integrated disease management pro- thought to have the most potential when gramme. combined with other biological control Bacillus subtilis (Ehrenberg) Cohn agents or resistance activators such as (Bacillaceae) strain QST 713 is registered acibenzolar-S-benzolar (Obradovic et al., in Canada for use on a number of key crops 2004). Currently this product is listed as to suppress several commonly occurring an active URMULE (User Requested Minor diseases including bacterial diseases of Use Label) project for use on Canadian tomato and pepper. Serenade® Max™, greenhouse tomatoes. which is a wettable powder, and Serenade® 470 Chapter 70

ASO™, which is an aqueous suspension, 2011). In vitro, Mycostop® but not can be used for bacterial spot on fi eld Actinovate® strongly inhibited the bacterial tomatoes and peppers, while Rhapsody® spot pathogens. In planta studies showed ASO™ is registered for use on greenhouse that Actinovate®, applied as a spray, and pepper (AgraQuest Inc., Davis, California, Mycostop®, applied as drench, consistently USA). In a 2-year study, Abbasi and and signifi cantly reduced bacterial spot on Highland (2009) demonstrated that foliar greenhouse seedlings without adversely sprays of both the dried and aqueous affecting the weight and size of the plants. formulations of this biological control In a 4-year fi eld study, neither strepto- strain reduced bacterial spot severity on mycete consistently and signifi cantly tomato foliage, with the aqueous reduced bacterial spot foliar disease suspension being more effective. Although severity; the amount of control appeared to this biopesticide alone did not reduce be dependent on seasonal conditions. disease incidence or severity on fruit, a tank mix of this microbe with copper hydroxide (Kocide® 2000) signifi cantly 70.3.4 Combinations enhanced healthy and total fruit yields. Thus this biological control agent may Various combinations of biological control have the most value if integrated into a agents, such as resistance activators, sustainable disease management strategy microbial antagonists, bacteriophage and that employs both conventional practice, plant growth-promoting rhizobacteria have such as spraying with copper bactericide, been tested for their ability to control and biologically based methodologies. bacterial spot on fi eld tomatoes (Obradovic The streptomycetes are known for their et al., 2004, 2005). In a 4-year fi eld study, ability to produce antimicrobial agents and Cuppels and Traquair (2011) found that to induce local and systemic resistance to spraying plants with both Actinovate® and plant pathogens (Schrey and Tarkka, 2008). BlightBan® A506, a treatment that had Mycostop® (Verdera Oy, Kurjenkellontie, consistently controlled bacterial spot in Finland) is a streptomycete-based bio- growth chamber assays, effectively reduced control product registered for use in not only foliar disease severity but also the Canada and over 15 other countries against AUDPC (area under the disease progress several root-rot and wilt fungi. The active curve) in two of these years. Although this agent is Streptomyces griseoviridis Ander- treatment was not as effective as Kocide® sen et al. (Streptomycetaceae) strain K61 2000-Bravo®500 at reducing foliar disease (Verdera, 2009). Actinovate® SP (Natural severity, it was superior to this standard Industries, Houston, Texas) is registered in control treatment in curtailing bacterial the USA and Canada for foliar and soil- spot lesion numbers on fruit. Furthermore, borne fungal diseases of greenhouse and this combination was also more consistent fi eld-grown crops. The bacterium Strepto- than Kocide® 2000-Bravo®500 at sup- myces lydicus De Boer et al. (Strepto- pressing the fungal disease anthracnose on mycetaceae) strain WYEC108 not only fruit in a separate but parallel set of fi eld suppresses phytopathogenic fungi but also trials. promotes plant growth (Yuan and Craw- ford, 1995). Because these two strepto- mycetes are capable of suppressing a 70.4 Evaluation of Biological Control number of plant diseases in a number of different ways, a study was initiated to Much progress has been made in determine if either biological control agent evaluating various biological control-based would be of value in a biological control methods for suppressing the tomato and programme focusing on bacterial spot, pepper disease bacterial spot. Unfortu- early blight and anthracnose in fi eld nately, the majority lack consistency when tomatoes (Cuppels and Traquair, 2005, used as the sole control agent in the fi eld Chapter 70 471

where conditions may vary considerably the effect of this treatment on other tomato depending upon the geographic location, diseases; the weather, the year and farming prac- 2. Determining the epiphytic fi tness of S. tices. When and how a biological control lydicus WYEC108 and P. fl uorescens A506 agent for bacterial spot is to be applied will on fi eld tomato plants and optimizing signifi cantly impact its ability to survive application methods to extend their sur- and maintain a critical population density vival and enhance their antagonistic activ- and thus be effective at controlling the ities; pathogens. Perhaps, the best strategy for 3. Additional testing of various com- controlling bacterial spot is to integrate a binations of biological control agents and combination of biological control agents timings, such as tomato transplant treat- that have different modes of action into ment with compost water extract followed conventional control practices. As an by fi eld tomato treatment with a resistance example, application of a biological control activator in combination with bacterio- agent fortifi ed compost-amended potting phage or a microbial antagonist. mix to greenhouse tomato transplants may be followed by application of acibenzolar- S-methyl and Agriphage™ in the fi eld. Acknowledgements Whatever strategy is followed, more effort Technical assistance was provided by Terry should be directed at understanding the Ainsworth, Brian Weselowski, Rebecca specifi c mechanism(s) involved, as well as Earl, and several summer and Co-op the ecological requirements of the students. The collaborative work of Dr biological control agents under con- George Lazarovits and Dr Jim Traquair, sideration. Agriculture and Agri-Food Canada is appreciated and acknowledged. This research was funded by grants from 70.5 Future Needs AgraQuest Inc., Omega Protein, the Ontario Tomato Research Institute, the Agriculture Further work should include: and Agri-Food Canada Matching Invest- 1. Determining the effi cacy of acibenzolar- ment Initiative, and the Improved Farming S-methyl and Agriphage™ for controlling Systems and Practices Initiative of the X. gardneri-caused bacterial spot under Agriculture and Agri-Food Canada Pest Ontario fi eld conditions and determining Management Centre.

References

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71 Invasive Alien Species and Future Biological Control Targets

Dave R. Gillespie1 and Peter G. Mason2 1Agriculture and Agri-Food Canada, Agassiz, British Columbia; 2Agriculture and Agri-Food Canada, Ottawa, Ontario

71.1 Introduction ant in ecosystems, and induce large and obvious changes in natural and managed Through human migration, commerce and ecosystems and in human conditions natural processes, many species have been (Colautti and MacIssac, 2004; Wheeler and moved from ranges where they are native Hoebecke, 2009). Their impacts cost to new regions where they are exotic. billions of dollars annually (Pimentel et al., These are generally described as exotic, 2001, 2005; Dawson, 2002; Colautti et al., adventive, alien, or introduced species. 2006). They arrive – accidentally, deliberately, or Many of the IAS that are serious threats naturally – from other places, and establish in Canada originate from Eurasia. As noted breeding populations in their new range. by Diamond (1999), much of contemporary They can be almost any species of life: human culture originates from the east– microorganisms, insects, mites, slugs and west axis of Eurasia, and his observation other invertebrates, birds, mammals and regarding agriculture and forestry relates fi sh (Elton, 1958). However, most of these also to IAS. Due to recent evolutionary adventive species are either benefi cial or history, IAS originating from this broad neutral to human interests, and the over- region are likely to be especially adapted to whelming majority do not increase in both anthropogenic disturbance and to abundance to the extent that they cause phoresy on human transportation systems. signifi cant concerns (Elton, 1958; William- Due to their presence in human trans- son and Fitter, 1996). Those that do are portation, IAS have the ability to re-invade, considered to be invasive alien species and many species are intercepted (IAS). repeatedly by CFIA inspectors. They tend Clearly, the mere fact of appearance in a to be highly plastic, due to their distrib- new range does not warrant identifi cation ution across a wide range of habitats on the as an invasive alien species (Wheeler and east–west Eurasian axis. Hoebecke, 2009). IAS share a suite of When the fi rst biological control impacts and biological traits that brings attempts were made, ships moved species them into confl ict with human interests. between continents and IAS spread from They affect human health, infrastructure origins in North America that were centred and food production, and disrupt eco- around ports. Railways provided corridors system services, biodiversity and eco- for their spread, through the provision of system integrity. IAS spread widely from avenues and through the movement of their point of introduction, become domin- settlers into new regions. Ships had to © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada 2013 Chapter 71 475 either transport breeding populations of IAS, the presence of a research community IAS on board, or the IAS needed resting that is able to recognize (taxonomic stages that allowed them to endure expertise) and respond (pest management transport. Today, container shipping and expertise) to new IAS threats is also aircraft can generate random founder essential to the long-term IAS strategies in populations without the pest needing to Canada. breed in transport or survive with a resting Once an IAS is established in Canada, stage. The distribution of wood-boring responses can take many forms. Economic beetle species in wire spools and dunnage and social adaptations may accommodate is one example (Humble, 2010). A second the presence of a disruptive species; example is brown marmorated stink bug however, more usually, active management Halyomorpha halys (Stål) (Hemiptera: strategies are developed, including the on- Pentatomidae), which appears regularly in going use of chemical pesticides. Of the warehouses, having been shipped from possible responses to IAS, classical bio- places in North America where it is well logical control, and other biologically established (T. Gariepy, 2012, London, based management strategies, offer good Ontario, pers. comm.). Modern commerce potential for the long-term reduction of the is essentially comprised of ship-sized undesirable impacts and the associated units, in 19th-century scales, that can be economic costs of IAS. placed anywhere in the world in less than 30 days. Container-based shipping is becoming more common in the air-freight 71.2 Invasive Alien Species in Canada industry as well. Given the costs that arise from the What is the rate at which species are being impacts of IAS, strategies for their introduced to, and becoming invasive in management should be a priority for Canada and where are they coming from? governments. IAS strategies roughly divide These questions are important for into fi ve categories: preparedness, preven- determining the level of resources that tion, detection, response and recovery (Sy, federal and provincial governments must 2009). In Canada, in the agriculture and devote to responding to IAS. Determining forestry sectors, the Canadian Food the origins of and rates at which new Inspection Agency (CFIA) has the primary adventive species and new potential IAS responsibility for the fi rst three strategies. appear is important for long-term planning The identifi cation of species that would to ensure that knowledge of their biology likely become IAS if introduced to Canada, and ecology can be developed before a i.e. pest-risk assessment, is a key IAS crisis arises. strategy. In general, CFIA has the fi rst Almost all of the arthropod and disease responsibility for response to IAS, i.e. to IAS of pest signifi cance have been conduct eradication programmes following introduced accidentally (Mack et al., 2000; the identifi cation of a newly arrived Pimentel et al., 2005). Conversely, many of species as an IAS threat. This responsi- the weed species that are IAS have been bility mostly shifts to the research and introduced intentionally (Mack et al., extension community once the IAS is 2000) as part of the global plant trade, or inextricably established in Canada. How- have been initially grown as garden crops ever, most IAS that are present in Canada and later as ornamentals (Mack, 2003). have not been identifi ed a priori, and have The overwhelming majority of the key only been recognized as such when the pests, diseases and weeds of agriculture in research and extension community dis- Canada are exotic (P.G. Mason and D.R. covers them spreading and causing wide- Gillespie, 2012, unpublished results), spread damage in ecosystems. Although which is not surprising given that most preparedness, prevention and detection crop species are themselves exotic. Most of programmes demonstrably help to mitigate these are IAS, in the sense that they have 476 Chapter 71

spread widely and invaded natural and cance have been imported through wood managed ecosystems. The situation is products used in shipping. Emerald ash somewhat different in forestry, where some borer, Agrilis planipennis Fairmaire (Cole- of the major pests, diseases and weeds are optera: Buprestidae), and Asian longhorn native species (e.g. Ives and Wong, 1988; beetle, Anoplophora glabripennis (Mot- Natural Resources Canada, 2012) that schulsky) (Coleoptera: Cerambycidae), are attack native trees. None the less, many examples that have been addressed as IAS are of strategic importance in forestry biological control targets, and reports on and silviculture (summarized by Hendrick- progress in these programmes are included son, 2002). Among alien patho gens: (i) in this volume (see Lyons, Chapter 7, this chestnut blight, Cryphonectria parasitica volume; Turgeon and Smith, Chapter 11, (Murrill) Barr (Cryphonectraceae), devas- this volume). tated forests dominated by the American In annual reports to the Agriculture and chestnut, Castanea dentata (Marsh.) Borkh. Agri-Food Canada, Biological Control (Fagaceae), affecting wildlife dependent on Working Group over the past decade (D. its fruits and driving several insect species Parker, Ottawa, Ontario, unpublished data, to extinction; (ii) white pine blister rust, 2001–2011), CFIA entomologists note the Cronartium ribicola J.C. Fisch. (Cronartia- presence of 12 newly present IAS threats in ceae), has affected Pinus spp. important as Canada: leek moth, Acrolepiopsis assec- wildlife habitat and has inhibited the tella (Zeller) (Lepidoptera: Acrolepiidae), development of commercial plantations of brown spruce longhorn beetle, Tetropium eastern white pine, Pinus strobus L. fuscum (F.) (Coleoptera: Cerambycidae), (Pinaceae); and (iii) Dutch elm disease, Asian longhorn beetle (starry sky beetle), Ophiostoma ulmi (Buisman) Nannf. and O. Anoplophora glabripennis (Motschulsky) novo-ulmi Brasier (Ophiostomataceae), has (Coleoptera: Cerambycidae), swede midge, destroyed white elm, Ulmus americana L. Contarinia nasturtii Kieffer, (Diptera: (Ulmaceae), an important shade tree. Cecidomyiidae), emerald ash borer, Agrilus Among the more than 180 alien woody planipennis Fairmaire (Coleoptera: plant-feeding insects established in Buprestidae), sudden oak death, Phyto- Canada, pine shoot beetle, Tomicus phthora ramorum Werres et al., piniperda (L.) (Coleoptera: Curculionidae: (Pythiaceae), golden nematode, Globodera Scolytinae), balsam woolly adelgid, rostochiensis (Wollenweber) Behrens Adelges piceae (Ratzburg) (Hemipera: (Tylen chida: Heteroderidae), apple clear- Adelgidae), Diprion similis Hartig wing, Duponchelia fovealis (Zeller) (Hymenoptera: Diprionidae), pine false (Lepidoptera: Crambidae), tomato looper, webworm, Acantholyda erythrocephala Chrysodeixis chalcites (Esper) (Lepi- (L.) (Hymenoptera: Pamphiliidae), birch doptera: Noctuidae), Sirex noctilio casebearer, Coleophora serratella L. (Lepi- Fabricius (Hymenoptera: Siricidae), banana doptera: Coleophoridae), and gypsy moth, moth, Opogona sacchari Bojer (Lepi- Lymantira dispar (L.) (Lepidoptera: Lyman- doptera: Tineidae), and spotted wing triidae), are serious economic pests; and drosophila, Drosophila suzukii Matsumura among alien plants, Scotch broom, Cytisus (Diptera: Drosophilidae). This is by no scoparius (L.) Link (Fabaceae), interferes means a complete list of the new IAS in with seedling establishment of Douglas fi r, Canada; however, these are species with Pseudotsuga menziesii (Mirb.) Franco potential to become extremely invasive, (Pinaceae), and garlic mustard, Alliaria and many have already involved a petiolata (Bieb.) Cavara and Grande response on the part of CFIA, i.e. (Brassicaceae), threatens rare native plants monitoring and eradication programmes. in the Carolinian forests. Of these introductions, nine were new In recent years, many wood-boring introductions to the continent and fi ve beetles (Coleoptera: Buprestidae, Ceramby- spread north from the USA. Eradication cidae and Curculionidae) of IAS signifi - programmes were developed for nine Chapter 71 477

species and have been successful in fi ve Table 71.1. Potential IAS intercepted by CFIA cases, however, three of these were against inspectors in 2010/2011 that represent ten or more pests of greenhouse agriculture that were interceptions. unable to sustain populations outside of No. of greenhouses. Pest risk assessments con- Order Family interceptions ducted by CFIA, and experience, suggest Coleoptera Bostrichidae 46 that most of the remainder are IAS of Coleoptera Cerambycidae 22 signifi cance to managed and natural eco- systems. Many other species of potential Coleoptera Chrysomelidae 13 IAS signifi cance have certainly been Coleoptera Curculionidae 43 introduced in the past decade. Although Coleoptera Dermestidae 12 eradication is the best and most cost- Coleoptera Nitidulidae 11 effective approach to management of newly Hemiptera Anthocoridae 15 established IAS, most eradication attempts Hemiptera Aphididae 11 will fail. Moreover, adventive species that are destined to become IAS may not be Hemiptera Pentatomidae 15 recognized as such initially. Hemiptera Pseudococcidae 12 The interception reports of the CFIA Hymenoptera Formicidae 13 provide useful information regarding Lepidoptera Noctuidae 52 future IAS. In 2010/2011, the most recent Lepidoptera Pyralidae 24 year for which data are available, Lepidoptera Tortricidae 24 inspectors made 805 interceptions. The taxonomic families with ten or more Mollusca Helicidae 10 interceptions (Table 7.1) represented 47% Mollusca Succineidae 19 of interceptions, and all families except the Thysanoptera Thripidae 36 Anthocoridae (Hemiptera) contain species that are known IAS. Many of the interceptions are of wood-boring beetles, interceptions in 2010/2011, China was as which have special signifi cance as IAS in large a potential source of IAS in Canada as Canadian forests. Most of the Noctuidae Europe. Vegetables, plants, cut fl owers and (Lepidoptera) originated from shipments fruit accounted for 67% of the from the USA. Because inspectors gener- commodities on which interceptions were ally fi nd immature stages of pests, many made and 117 interceptions (over 14%) interceptions are only identifi ed to the were made in dunnage, wood and logs. To family level, which makes it diffi cult to use a very large degree, interceptions refl ect the interception records as predictors of trading patterns and volumes of com- particular IAS. Even for relatively well- modities that are imported. known families such as Tortricidae Recent invasions of pests of agricultural (Lepidoptera), 17 of the 24 interceptions signifi cance generally support the analysis are only identifi ed to family. above. Several invasive pests of signifi - The majority (over 50%) of the cance to agriculture, forestry and environ- interceptions came from California (USA), ment in Canada and North America have China, India, South Africa and Florida invaded from Asia in the last two decades. (USA), with almost 30% of interceptions Of note are the soybean aphid, Aphis from Florida alone. The USA as a whole glycines Matsumura (Hemiptera: Aphi- accounted for 368 interceptions, and 81 didae) (Brodeur, Chapter 12, this volume), interceptions (10%) originated from spotted wing drosophila, Drosophila Europe, which has been the traditional suzukii Matsumura (Diptera: Droso- source of IAS in North America. China has philidae) (Thistlewood et al., Chapter 21, been identifi ed as a likely source of IAS in this volume), the emerald ash borer, the USA, due to increased volumes of trade Agrilus planipennis Fairmaire (Coleoptera: (National Research Council, 2002). With 75 Buprestidae) (Lyons, Chapter 9, this 478 Chapter 71

volume), and the Asian longhorned beetle, down regulation from natural enemies. Anoplophora glabripennis (Motschulsky) Researchers now have a much more (Coleoptera: Cerambycidae) (Turgeon and extensive toolkit for biological control. In Smith, Chapter 11, this volume). In the the early history of the fi eld, all biological past two decades, Asian knotweeds, control was essentially classical biological Fallopia spp. (Polygonaceae), have become control, that is, regulation of IAS popu- invasive weeds of national concern (see lations by introduction of exotic natural Bourchier et. al., Chapter 48, this volume). enemies from their area of origin. In the However, these recent invasions from Asia present volume are not only examples of do not refl ect a shift in origin of invasive successful classical biological control, but pests. Rather, they refl ect an addition to also examples of successful programmes North American trade patterns, since IAS using inundative biological control, con- continue to arrive from European origins as servation biological control and biological well. Examples from Europe are the leek control through utilization of metabolic moth, Acrolepiopsis assectella (Zeller) products of natural enemies. (Lepidoptera: Acrolepiidae) (see Mason et Once it is established that a species has al., Chapter 8, this volume), the swede signifi cant negative impacts and that other midge, Contarinia nasturtii Kieffer (Dip- options for control are ineffective or tera: Cecidomyiidae) (see Abram et al., environmentally unsafe, the feasibility of Chapter 18, this volume), and the apple biological control as a good management clearwing moth, Synanthedon myopae- option can be assessed (De Clerck-Floate et formis (Borkhausen) (Lepidoptera: al., 2006). Barbosa and Segarra-Carmona Sesiidae) (see Cossentine et al., Chapter 41, (1993) and Peschken and McClay (1995) this volume). Because new invasive alien proposed criteria with scoring systems that species, which are also potential biological would generate a numerical score for control targets, arrive in North America feasibility. The weakness of assigning from both Asian and European origins, numerical values is that they are often there is a need to prioritize targets no arbitrarily assigned and thresholds can be matter where IAS arrive from and to changed to suit particular interests. De develop the long-term biological control Clerck-Floate et al. (2006) modifi ed the solutions that are necessary. criteria and proposed a ‘yes/no’ evaluation to determine if a species should be targeted for biological control. These approaches 71.3 Selecting Targets for Biological categorize the information under three Control areas, Economic, Environmental and Feasibility for Biological Control; Barbosa Not all pest species are suitable targets for and Segarra-Carmona (1993) add a fourth biological control. Introductions of exotic category, Capacity to Conduct the Work. A species against vertebrate pests have strength of such standardized approaches proven to be disastrous (Courchamp et al., is that they can provide feedback to 2003), thus vertebrates should not ever be determine areas of strength or weakness of considered appropriate target species. a potential project as well as an estimate of Invertebrates, microorganisms and plants the costs to undertake a project (Barbosa may be suitable targets for biological and Segarra-Carmona, 1993). While these control and there are numerous examples approaches can provide the justifi cation for of successes against pests in these groups. selecting a target based on current impact, For a biological control programme to be ‘upstream’ considerations could also be considered, it is important that there be useful to determine early on whether a negative economic, environmental and/or particular species should be a target for social impacts that cannot be safely biological control. ameliorated by other means. It is also Knowledge of the fl ora and fauna of essential that the IAS be vulnerable to top- countries with which we trade would help Chapter 71 479

to fl ag species that pose risk. The recent probability of success for target IAS for spate of invasions from Asian regions has which natural enemies are signifi cant highlighted the need for comprehensive factors in restraining densities (Van knowledge of the biodiversity of the world. Driesche and Bellows, 1996). Parasitoid, Checklists and catalogues of species in a predator and pathogen communities can region provide a good starting point. ‘A full regulate pest arthropods, while herbivores catalogue gives information concerning all and pathogens can reduce weed popu- published names within a group, their lations and antagonist organisms can have classifi cation, taxonomic history, means of impacts on plant pathogens. The species identifi cation, references to taxonomic acts, richness of natural enemy communities type material, detailed distribution, may indicate the probability of fi nding habitat, natural history, and so on’ (Löbl appropriate biological control agents. and Smetana, 2003). To have such Pemberton (2002) suggests that for weeds, information enables risk assessments that the size of geographic range, abundance aim to determine the potential for a species within the range, number of congener to become a pest, hence a potential target species and complexity of plant archi- for biological control. We propose that this tecture may indicate herbivore species is the stage at which species identifi ed as richness; and the greater the number of having high potential as IAS should be species the more likely that suitable and evaluated as targets for biological control. successful agents will be found. This ‘off-shore’ approach would allow Knowledge of which life stages of a target early biological control implementation, IAS are most vulnerable to attack can also rather than the ‘wait-until-there-is-a-crisis- increase the probability of success (Rhagu and-attempt-to-eradicate-fi rst’ strategy that et al., 2006; Mills, 2009). For example, for appears to be the norm. Thus, the criteria houndstongue, Cynoglossum offi cinale (L.) for feasibility for biological control become (Boraginaceae), the roots appear to be the the focus, the economic/environmental Achilles heel as evidenced by the dramatic aspects having been considered in the risk reductions of weed populations by the assessment process. root-feeding Mogulones crucifer Pallas In addition to the above, taxonomic and (Coleoptera: Curculionidae) (see De Clerck- phylogenetic relationships between the Floate, Chapter 46, this volume). target IAS and close North American It is easier to recognize suitable relatives are important considerations. biological control targets in natural systems Species that have few close relatives in as opposed to agricultural systems, where North America are highly suitable targets alternative and economically viable for classical biological control, because strategies, such as pesticides, may be specialist natural enemies – which by available. However, as noted by Floate et defi nition have a host range that is al. (2002), pesticide resistance is a major constrained to a few, closely related consideration. In a number of chapters in species in the same genus – are less likely this volume, the failure of pesticide-based to attack distantly related, non-target IPM programmes, or the incompatibility of species in North America. Unfortunately, pesticide-based management practices with such phylogenetically isolated IAS are IPM programmes for other pests, has been relatively rare. Therefore, a fundamental the essential driver behind the develop- understanding of the evolutionary and ment of a biological control approach for a ecological parameters that determine host pest. The European red mite, Panonychus range in herbivores, predators and ulmi (Koch) (Trobidiformes: Tetrany- parasitoids in general would provide some chidae), is a key pest of fruit orchards that guidance as to what type of non-target rapidly evolves resistance to pesticides, species may be at risk (see Gariepy and and these pesticides disrupt management Roitberg, Chapter 4, this volume). programmes based on conservation bio- Biological control has a higher logical control (see Thistlewood et al., 480 Chapter 71

Chapter 34, this volume). Therefore, other arthropod) natural enemies with inun- IAS in fruit orchards become suitable dative biological control agents based on targets for biological control, e.g. the strains of common pathogens that are European apple sawfl y, Hoplocampa selected and formulated to provide impact testudinea (Klug) (Hymenoptera: Tenthre- on the target that is comparable to many of dinidae) (Vincent et al., Chapter 27, this the common herbicides. volume), and the apple clearwing moth, In their analysis of biological control of Synanthedon myopaeformis (Borkhausen) insects in Canada, Turnbull and Chant (Lepidoptera: Sesiidae) (Cossentine et al., (1961) advocated that targets for biological Chapter 41, this volume). Furthermore, control be limited to indirect pests, which inaccessibility of habitats such as range- feed on plant parts other than that which is lands affected by the IAS also drives the harvested, and where there are reasonably need to develop biological control high thresholds for injury and a large programmes (see Bourchier et al., Chapter number of individuals are required to 48, this volume; De Clerck-Floate, Chapter damage the crop. They hypothesized that 46, this volume; De Clerck-Floate and direct pests would not make suitable targets Turner, Chapter 52, this volume; De Clerck- because relatively small numbers of insects, Floate and McClay, Chapter 53, this and small amounts of damage, would cause volume). For IAS that invade agricultural the loss of the commodity. We point out systems, the presence of IPM systems that that this analysis was made before IPM manage pesticide inputs and consider became the standard approach for natural enemy impacts are conducive to managing pests of agriculture in Canada, in the development of biological control an era when broad spectrum pesticides solutions. Pests of greenhouse crops (see were more-or-less the sole approach to Buitenhuis et al., Chapter 13, this volume) managing pests. In modern IPM, monitor- are good examples, and the biological ing pest and natural enemy populations is, control focus of the industry has been a key or should be, the best-management prac- driver in the pursuit of biological control tice. Reduced-risk pesticides, physical approaches for cabbage loopers, Tricho- barriers, pheromone disruption and sterile- plusia ni Hübner (Lepidoptera: Noctuidae) insect programmes are now standard IPM (see Erlandson, Chapter 42, this volume), practices and most of these are highly and the tomato/potato psyllid, Bactericera compatible with biological control. In this cockerelli (Sulc) (Hemiptera: Triozidae) setting, biological control by management (see McGregor, Chapter 14, this volume). of pests with natural enemies can be highly In many cases, a biological control successful. Biological control programmes strategy has emerged that merges classical, for codling moth, Cydia pomonella (L.) inundative and conservation biological (Lepidoptera: Tortricidae), a direct pest of control approaches with other reduced-risk apples, are showing promise (see Cos- IPM approaches. For example, the recent sentine and Vincent, Chapter 19, this invasion of leek moth, A. assectella, volume). Similarly, biological control of threatened the garlic and leek industry in orange wheat blossom midge, Sitodiplosis Ontario (Mason et al., Chapter 8, this mosellana (Géhin) (Diptera: Cecido- volume). The long-term strategy that myiidae), a direct pest of wheat kernels, is emerged is based on classical biological extremely successful (Doane et al., Chapter control through introduction and establish- 39, this volume). ment of a European parasitoid, combined with use of microbial and reduced-risk insecticides and physical exclusion using 71.4 Challenges and Constraints row covers. Increasingly, programmes for biological control of annual and crop Once a suitable target is identifi ed, the weeds, as described in Chapters 43–60 of biological control programme generally this volume, integrate herbivorous (mostly faces a number of serious challenges and Chapter 71 481

constraints, and these are evident in the of pest populations, increases in habitat chapters in this volume. The identifi cation quality and/or crop yield, and reductions and testing of non-target communities in costs of control, and impacts of (Mason et al., Chapter 1 this volume) is agricultural practices on the Canadian often identifi ed as an important issue; environment and ecosystem services however, it is only one of many problems attached to those environments. In respect faced by biological control researchers. of the long-term nature of biological Increasingly, countries around the world control programmes, the community of are adopting ‘Access and Benefi t Sharing’ scientists and professors in Canada is legislation (see Mason and Brodeur, aging, and it is essential to develop the Chapter 2, this volume) that threatens to resources and to identify and fi ll key restrict the ability of classical biological positions in this fi eld. control researchers to access and survey the natural enemy diversity of target pests in their native ranges. Another challenge 71.5 Opportunities faced by researchers is the need for models based on both Research and Development Current knowledge of molecular physi- and business considerations, which are ology, the identifi cation of genomes and an increasingly essential for success (see emerging understanding of phylogeny and Boyetchko and Svircev, Chapter 5, this evolution of life on this planet, means that volume). For inundative biological control, biological control scientists have incredible it is no longer suffi cient to demonstrate resources available (Gariepy and Roitberg, impacts on targets in laboratory experi- Chapter 4, this volume). These resources ments – increasingly, these approaches aid in developing biological control pro- demand a business plan, business partners grammes and can be useful in identifying and investment from both government and and solving old problems. The cabbage industry. seedpod weevil, Ceutorhynchus obstrictus Biological control of target IAS is, like (Marsham) (Coleoptera: Curculionidae) is most technological innovations in biology, one of the oldest of the biological control a very long-term process, and success can programmes, and has been described take decades to emerge. This is especially (Turnbull and Chant, 1961) as a mediocre true in classical biological control pro- success due to the failure of established grammes. Biological control programmes agents to control the target. An improved for leafy spurge, Euphorbia esula L. understanding of the systematics of the (Euphorbiaceae) (Bourchier and Van agents and recent research (Gibson et al., Hezewijk, Chapter 47, this volume), and 2005, 2006; Haye et al., Chapter 16, this knapweeds, Centaurea spp. (Asteraceae) volume) have breathed new life into this (see Bourchier and Van Hezewijk, Chapter programme, with a promise of a solution to 44, this volume), were among the earliest a pest that causes millions of dollars of of the biological control programmes damage to Canadian canola crops annually. against weeds in Canada. These have Similarly, molecular analysis of toadfl ax emerged in the past decade as huge success Linaria spp. (Plantaginaceae) has led to a stories, and the reduction of these weeds in re-investigation of the agents and releases rangeland and pasture is producing made in Canada (see De Clerk-Floate and signifi cant benefi ts for both livestock Turner, Chapter 52, this volume, and De production and habitat quality for native Clerck-Floate and McClay, Chapter 53, this species. Long-term programmes, however, volume) with a likelihood of proceeding to require long-term commitments to new releases. Revisions of the phylogeny of personnel, and in fact some programmes plants based on molecular evidence have have spanned more than one scientist’s resulted in improved risk assessment career, from inception to fi nal success. The through enabling development of more benefi ts are long-term and stable reduction relevant non-target test lists. 482 Chapter 71

The development of inexpensive and (Lythriaceae) (see Corrigan et al., Chapter sophisticated molecular approaches to 54, this volume) shows clearly that the identifying strains and species of micro- releases of Galerucella calmariensis L. and organisms has led to an astounding array of G. pusilla Duftschmidt (Coleoptera: Chrys- successful inundative and conservation omelidae) have been responsible for the approaches to biological control of plant reduction of populations of this weed. pathogens (see Chapters 61–70, this The understanding of the biodiversity of volume). Two decades ago, the knowledge Canada and the ecology and biology of and technology needed for these successful species is increasingly important to these innovations was not available, so the programmes and taxonomy is basic to the advances are striking. success of biological control. New classifi - Biological control is simultaneously a cations are being developed using the latest research programme in fundamental and techniques and major changes have applied ecology of IAS, and a programme occurred for plants, e.g. the new of innovation that leads to the deployment standardized family names consisting of of new technology and techniques to the type genus and the suffi x –aceae (S. control and regulate pests. These pro- Darbyshire, Ottawa, Ontario, 2012, pers. grammes are highly infl uenced by evolving comm.). Major changes are imminent for societal values. In the middle of the 20th the taxonomy of fungi (A. Levesque, century, the notion of non-target effects Ottawa, Ontario, 2012, pers. comm.), was constrained to the potential for which have traditionally been named economic (non-target) impacts of biological based on the teleomorph or anamorph control agents on crops, and non-target stages of the life cycle. Taxonomic expert- studies were exclusively performed on ise is linked to identifi cation of target potential agents against weeds. Today, due species and biological control agents and to increased concern for biodiversity and taxonomists are the ones who have habitat quality, all biological control agents developed the authoritative electronic data- are examined for potential for non-target bases, e.g. ‘Tropicos’, ‘Species Fungorum’, impacts, and rare and endangered organ- ‘Universal Chalcidoidea Database, ‘Taxa- isms are necessarily part of the con- pad’ etc., that are essential to standardizing siderations. The previously unrecognized names such as for this volume. risk of impact of a highly successful The advances in and success of biological control agent for houndstongue, biological control programmes that are Cynoglossum offi cinale (L.) (Boraginaceae), documented in this volume constitute an on native plants (De Clerk-Floate, Chapter outline of a biological control strategy for 46, this volume) has generated a need to Canada. The Acts supporting biological understand the nature and meaning of host control activities lay good foundations, and range and the implications of transient serve the development of innovations in herbivory for rare and endangered species. support of Canadian agriculture, forestry Paradoxically, successful biological con- and environment. The current advances trol programmes may simply not be and successes, and the promise for the recognized by the public. The release of future, are the fruits of decades-long leaf-feeding beetles against purple loose- support of biological control programmes strife, Lythrum salicaria L. (Lythraceae), in by government and funding agencies, and Canadian wetlands has recently been in the case of inundative biological criticized in the press and reductions of the controls and microbial pesticides, by weed attributed to adaptations of the weed companies and venture capital. The to the Canadian wetland habitats (‘Once- foundations of the strategy are as follows: feared purple peril fades away’, Tom Spears, Ottawa Citizen, 21 November, 1. An effective inspection service (the 2012). Evidence from the recent research CFIA) that not only inspects and intercepts on purple loosestrife, Lythrum salicaria L. at borders, but anticipates IAS threats to Chapter 71 483

Canada, and liaises with the research com- logical control agents for suitable target munity when IAS are intercepted to ensure pests; awareness, and facilitate the development 4. The ability to develop and deploy all of of action plans; the biological control approaches (classi- 2. National collections representing the cal, inundation and conservation) in an biodiversity of Canada, and the world, pro- IPM framework. viding the foundation for exploration for biological control agents and development of the knowledge of the ecology and biol- ogy of non-target species; Acknowledgements 3. A community of researchers in govern- ment, universities and industry that col- Naomi Cappuccino provided helpful laborate with one-another to solve comments on an earlier version of this problems and develop appropriate bio- contribution.

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abbreviatus, Hypnoidus Adelgidae – order Hemiptera abdominalis, Aphthona adstrictus, Pterostichus Abies – family Pinaceae Aedes – family Culicidae Abies spp. 387, 421 Aedes aegypti (L.) 49–50 Abies balsamea (L.) Mill. 203, 421 aegypti, Aedes abietinum, Heterobasidion aenea, Amara abietis, Neodiprion aeneoviridis, Catolaccus Abrostola – family Noctuidae Aeolus – family Elateridae Abrostola asclepiadis (Denis & Schiffermüller) Aeolus mellillus (Say) 73 405 aequalis, Irenimus Acantholyda – family Pamphiliidae aeratana, Dichrorampha Acantholyda erythrocephala (L.) 54–55, 476 aeripennis, Selatosomus Acer – family Sapindaceae (Aceraceae) aeripennis destructor, Ctenicera Acer spp. 83, 84, 87 aerogenes, Enterobacter Acer mono Maxim. 83 Aesculus – family Sapindaceae 83 Acer negundo L. 85 aestivum, Triticum Acer pseudosieboldianum (Pax.) Kom. 83 aethiops, Perilitus Acer rubrum L. 88 affi nis, Dibrachys Acer saccharum Marshall 88 affi nis, Urophora Acer tegmentosum Maxim. 83 African violet (Saintpaulia spp.) 100 Acer truncatum Bunge 83 Agamermis – family Mermithidae Aceria – family Eriophyidae Agamermis sp. 170 Aceria calathinus (Nalepa) 379 Agelastica – family Chrysomelidae Aceria drabae (Nalepa) 334–335 Agelastica alni (L.) 210 Aceria malherbae Nuzacci 307–308 Ageniaspis – family Encyrtidae acetosa, Rumex Ageniaspis bicoloripes (Girault) 245 achates, Cyphocleonus agglomerans, Pantoea Achillea – family Asteraceae Agistemus – family Stigmaeidae Achillea alpina L. 380, 381 Agistemus fl eschneri Summers 239 Achillea millefolium L. 380 Agonum – family Carabidae Achromobacter – family Alcaligenaceae Agonum cupreum Dejean 172 Achromobacter spp. 173 Agonum placidum (Say) 172 AcMNPV (Autographa californica multiple agonus, Limonius nucleopolyhedrovirus) 231, 292–293, agrili, Oobius 294 agrili, Spathius Acrididae – order Orthoptera Agrilus – family Buprestidae Acrolepiidae – order Lepidoptera Agrilus spp. 64, 65 Acrolepiopsis – family Acrolepiidae Agrilus angelicus Horn 66 Acrolepiopsis assectella (Zeller) 56–61, 476, Agrilus anxius Gory 66, 67 478, 480 Agrilus bilineatus (Weber) 66 acrolophi, Chaetorellia Agrilus granulatus liragus Barter & Brown 66 acronyctae, Cotesia Agrilus planipennis Fairmaire 62–68, 476, 477 aculeifer, Gaeolaelaps Agriotes – family Elateridae Aculops – family Eriophyidae Agriotes spp. 72, 73–74, 75, 78, 79, 80 Aculops lycopersici (Massee) 100 Agriotes criddlei Van Dyke 73 Aculus – family Eriophyidae Agriotes lineatus (L.) 72, 73, 75–78 Aculus schlechtendali (Nalepa) 240 Agriotes mancus (Say) 73 acuminatum, Fusarium Agriotes obscurus (L.) 72, 73, 75–79 acutatum, Colletotrichum Agriotes sputator (L.) 73, 75–78 Adelges – family Adelgidae Agromyzidae – order Diptera 115, 372 Adelges piceae (Ratzeburg) 476 Agropyron – family Poaceae 115

485 486 Index

Agrypon – family Ichneumonidae alticola, Protapanteles Agrypon fl aveolatum (Gravenhorst) 7 alyssum (Lobularia maritima) 259 Agulla – family Raphidiidae Amara – family Carabidae Agulla xanthostigma (Schummel) 158 Amara aenea Degeer 122 alaskensis, Rhyssa Amara apricaria (Paykull) 172 alatum, Lythrum Amara avida (Say) 172 alba, Sinapis Amara ellipsis (Casey) 172 albicans, Cyzenis Amara latior (Kirby) 172 albicans, Hexamermis Amara ovata F. 122 albifrons, Conura Amara patruelis Dejean 172 albipes, Grypocentrus Amara quenseli (Schönherr) 172 albitarsus, Euderus Amara similata Gyllenhall 122, 145 Albizia – family Fabaceae 83 Amara torrida (Panzer) 172 albo-atrum, Verticillium ambermarked birch leafminer (Profenusa albocilia, Melanagromyza thomsoni) 175–180 albolineata, Synchlora ambiguella, Eupoecilia Albugo tragopogonis (DC) Gray see Pustula ambiguus, Erigorgus tragopogonis (Pers.) Thines Amblydromalus limonicus (Garman & McGregor) albus, Melilotus see Typhlodromalus limonicus (Garman albus, Muscodor & McGregor) Alcaligenes – family Alcaligenaceae Amblyseius – family Phytoseiidae alcaligenes, Pseudomonas Amblyseius andersoni (Chant) 104 Alcaligenes faecalis Castellani & Chalmers 86 Amblyseius californicus (McGregor) see alder buckthorn (Frangula alnus) 153 Neoseiulus californicus (McGregor) aldrichi, Gonia Amblyseius cucumeris (Oudemans) see Aleochara – family Staphylinidae Neoseiulus cucumeris (Oudemans) Aleochara spp. 144, 145 Amblyseius degenerans (Berelese) see Iphesius Aleochara bilineata (Gyllenhall) 144, 145–147 degenerans Berelese Aleochara bipustulata (L.) 144, 145–148 Amblyseius fallacis Garman see Ne oseiulus Aleochara verna Say 144, 147 fallacis (Garman) Aleyrodidae – order Hemiptera 291 Amblyseius montdorensis (Schicha) 104 algens, Tachina Amblyseius swirskii Athias-Henriot 102, Aliolus – family Braconidae 103–104 Aliolus curculionis (Fitch) 216 Amblytylus – family Miridae Allantonematidae – order Tylenchida 250 Amblytylus nasutus (Kirschbaum) 223 Alliaria – family Brassicaceae Ambrosia – family Asteraceae Alliaria petiolata (Bieb.) Cavara & Grande 124, Ambrosia artemisiifolia L. 296–300, 386, 476 387 alliariae, Ceutorhynchus American chestnut (Castanea dentata) 476 Allium – family Amaryllidaceae American serpentine leafminer (Liriomyza Allium spp. 56 trifolii) 100 Allium cepa L. 56 americana, Fraxinus Roth 56 americana, Sorbus Allium porrum L. 56, 57, 59, 480 americana, Trichomalopsis Allium sativum L. 56, 57, 480 americana, Ulmus Nutt.ex Ker Gawl. 56 americanus, Echinothrips Allothrombium – family Trombidiidae americolimbata, Nabicula Allothrombium spp. 279 amoena, Rhyssa Allurus – family Braconidae Amphimermis – family Mermithidae Allurus muricatus (Haliday) 278, 279 Amphimermis elegans Kab. & Imam. 250 allynii, Brasema amputatus, Harpalus almond (Prunus dulcis) 156 Amsonia – family Apocynaceae alni, Agelastica Amsonia illustris Woodson 404 alnus, Frangula Amsonia tabernaemontana Walter 404 Alphabaculovirus – family Baculoviridae 229, Amylostereum – family Amylostereaceae 292 Amylostereum areolatum (Chaillet ex Fr.) Boidin alpina, Achillea 264, 265, 268 Alternaria – family Pleosporaceae amylovora, Erwinia Alternaria tenuissima (Kunze) Wiltshire 425 Anagrus – family Mymaridae alternata, Villa Anagrus sp. 216 alternatus, Nabis Anagyrus – family Encyrtidae Altica – family Chrysomelidae Anagyrus sp. 31 Altica brevicollis Foudras 210 Anagyrus lopezi (DeSantis) 7 Index 487

x ananassa, Fragaria Aphelinus certus Yasnosh 95, 96 Anaphes – family Mymaridae Aphididae – order Hemiptera 193, 291, 477 Anaphes sp. 210, 211 aphidimyza, Aphidoletes Anaphes cotei Huber 216 Aphidius – family Braconidae Anaphes diana Girault 279 Aphidius spp. 105 Anaphes fl avipes (Foerster) 234 Aphidoletes – family Cecidomyiidae Anaphes iole Girault 222 Aphidoletes spp. 103 Anaphes listronoti Huber 216 Aphidoletes aphidimyza (Rondani) 105 Anaphes sordidatus (Girault) 216 Aphis – family Aphididae Anaphes victus Huber 216 Aphis glycines Matsumura 93–96, 193, 477 anaplophorae, Aprostocetus Aphis gossypii Glover 98 Anchomenus – family Carabidae Aphis pomi DeGeer 132 Anchomenus dorsalis Pontoppidan 122 Aphria – family Tachinidae andersoni, Amblyseius Aphria ocypterata Townsend 165 Anethum – family Apiaceae Aphthona – family Chrysomelidae Anethum graveolens L. 214 Aphthona spp. 315, 317–319 angelicus, Agrilus Aphthona abdominalis (Duftschmid) 316 angustifolia, Elaeagnus Aphthona cyparissiae (Koch) 316 angustifolium, Vaccinium Aphthona czwalinae Weise 315, 316, 317 anisopliae, Metarhizium Aphthona fl ava Guillebeau 316 annosum, Heterobasidion Aphthona lacertosa Rosenhauer 315, 316–317 annosus root rot (Heterobasidion irregulare) Aphthona nigriscutis Foudras 316 420–422 apiculatus, Diphyus annual canary grass (Phalaris canariensis) 273 Apidae – order Hymenoptera annual rye grass (Lolium multifl orum) 217, 373 Apion hookeri Kirby see Omphalapion annulata, Campoletis hookerorum (Kirby) annuum, Capsicum Apis – family Apidae annuus, Helianthus Apis mellifera L. 385 Anopheles – family Culicidae Apium – family Apiaceae Anopheles gambiae Giles 48 Apium graveolens L. 214 Anopheles stephensi Liston 48 Apium petroselinum L. 214 Anoplophora – family Cerambycidae Apocynum – family Apocynaceae Anoplophora chinensis (Förster) 85 Apocynum cannabinum L. 404 Anoplophora glabripennis (Motschulsky) Apophua – family Ichneumonidae 82–88, 476, 478 Apophua simplicipes (Cresson) 131, 132 Anthocoridae – order Hemiptera 109, 238, 477 appelianum, Lepidium Anthomyiidae – order Diptera 372 apple blotch leafminer (Phyllonorycter Anthonomus – family Curculionidae crataegella) 244 Anthonomus eugenii Cano 101 apple clearwing (Duponchelia fovealis) 101, 476 antirrhini, Rhinusa apple clearwing moth (Synanthedon anxius, Agrilus myopaeformis) 285–288, 478, 480 Anystidae – order Trombidiformes 238 apple (Malus domestica) 130, 139–140, 156, Anystis – family Anystidae 192, 198–201, 238–240, 241, 244–246, Anystis spp. 242, 279 285–288, 408–409, 480 Anystis baccarum L. 239 apple scab (Venturia inaequalis) 200, 245–246 Aoplus – family Ichneumonidae apricaria, Amara Aoplus velox (Cresson) 204 apricot (Prunus armeniaca) 156, 285 Apanteles – family Braconidae Aprostocetus – family Eulophidae Apanteles carpatus (Say) 7 Aprostocetus sp. 86, 154 Apanteles impurus (Nees) 58 Aprostocetus anaplophorae Delvare 85 Apanteles laevigatus (Ratzeburg) 158 Aptesis – family Ichneumonidae Apanteles polychrosidis Viereck 131, 132 Aptesis nigrocincta Gravenhorst 200 Apanteles sp. nr. fl avovariatus (Muesebeck) 204 Aptesis segnis (Provancher) 179, 180 aparine, Galium aquatilis, Rahnella Aphaereta – family Braconidae aquifolium, Mahonia Aphaereta spp. 144, 146 Arctanthemum – family Asteraceae Aphaereta brevis Tobias 58, 60 Arctanthemum arcticum (L.) Tzvelev 338 Aphaereta pallipes (Say) 185 arcticum, Arctanthemum Aphalara – family Psyllidae Arctiidae – order Lepidoptera Aphalara itadori (Shinji) 323–326 arctos horribilis, Ursus aphanidermatum, Pythium Arenetra – family Ichneumonidae Aphelinidae – order Hymenoptera 245 Arenetra canadensis Cresson 169 Aphelinus – family Aphelinidae Arenetra fumipennis Townes 169 488 Index

Arenetra rufi pes Cresson 169 Aulacidae – order Hymenoptera areolatum, Amylostereum Aulacorthum – family Aphididae Argentine stem weevil (Listronotus bonariensis) Aulacorthum solani (Kaltenbach) 98, 99, 104, 216–217 105 argentipes, Phlebotomus aulicae, Entomophaga Argyrotaenia – family Tortricidae auratus, Chrysochus Argyrotaenia velutinana Walk. 339 aurea, Leskia aries, Ovis Aureobasidium – family Dothioraceae arietinum, Cicer Aureobasidium pullulans (de Bary) G. Arnuad armeniaca, Prunus 425 army cutworm (Euxoa auxiliaris) 164–173 aureum, Ribes Arsenophonus – family Enterobacteraceae auricularia, Forfi cula Arsenophonus spp. 43–44, 45, 47, 185, 186 australis, Campoletis Artemisia – family Asteraceae 404 Autographa – family Noctuidae artemisiifolia, Ambrosia Autographa californica (Speyer) 231 arvense, Cirsium Autographa californica multiple arvense, Trifolium nucleopolyhedrovirus – family arvensis, Convolvulus Baculoviridae 231, 292–293, 294 arvensis, Sinapis autumnalis, Musca Ascidae – order Megostigmata auxiliaris, Euxoa asclepiadeus, Chrysochus Avena – family Poaceae asclepiadis, Abrostola Avena fatua L. 371 asclepiadis asclepiadis, Chrysolina Avena sativa L. 273, 278, 354, 373, 414 Asclepias – family Apocynaceae avenaceum, Fusarium Asclepias spp. 404 aviculare, Polygonum Asclepias curassavica L. 404 avida, Amara Asclepias tuberosa L. 404 avium, Prunus Asian knotweeds (Fallopia spp.) 321–323, axillaris, Muehlenbeckia 324–326, 478 axyridis, Harmonia Asian ladybird beetle (Harmonia axyridis) 94, Azadirachta – family Meliaceae 132, 136, 192–196 Azadirachta indica A. Juss. 209, 457, 468 Asian longhorn beetle (Anoplophora azurea, Cassida glabripennis) 82–88, 476, 478 Asiatic lilies (Lilium spp.) 208 Asobara – family Braconidae baccarum, Anystis Asobara tabida Nees von Esenbeck 154 Bacillus – family Bacillaceae asparagi, Crioceris Bacillus cereus Frankland & Frankland 173 assectella, Acrolepiopsis Bacillus pumilus Meyer & Gottheil 441 assimilis, Ceutorhynchus Bacillus sphaericus Meyer & Neide 173 astigma, Leluthia Bacillus subtilis (Ehrenberg) Cohn 409, Astragalus – family Fabaceae 415–416, 426, 427, 430, 432, 433, 440, Astragalus canadensis L. 456 441, 448, 464, 469–470 Atanycolus – family Braconidae Bacillus thuringiensis Berliner 37–38, 57, 144, Atanycolus spp. 67 228, 229, 258, 286, 292, 294 Atanycolus cappaerti Marsh & Staznac 65–66 Bacillus thuringiensis Berliner serovar. Atanycolus hicorae Shenefelt 65–66 darmstadiensis 186 Atanycolus longicauda Shenefelt 65–66 Bacillus thuringiensis Berliner serovar. Atanycolus nigriventris Vojjnovskaja-Krieger 65 israelensis 136 Atanycolus nigropyga Shenefelt 65 Bacillus thuringiensis Berliner serovar. kurstaki Atanycolus simplex (Cresson) 65 59, 101, 103, 130–131, 132, 186, 204, Atanycolus tranquebaricae Shenefelt 65 229, 258, 292, 294 Atheta coriaria Kraatz see Dalotia coriaria Bacillus thuringiensis Berliner serovar. (Kraatz) tenebrionis 87 Athrycia – family Tachinidae Bacillus thuringiensis Berliner serovar. Athrycia cinerea (Coquillette) 228 thompsoni 186 atkinsoni, Campoletis Bacillus thuringiensis Berliner serovar. Atlantic menhaden fi sh (Brevoortia tyrannus) thuringiensis 186 442, 458 Bacillus thuringiensis Berliner serovar. tolworthi atopovirilia, Trichogramma 186 atripes, Eurytoma bacterial spot of tomato and pepper Attelabidae – order Coleoptera (Xanthomonas spp.) 466–471 aubergine, eggplant (Solanum melongena) 100, Bactericera – family Triozidae 454 Bactericera cockerelli (Sulc) 101, 107–111, 480 Index 489

bacteriophora, Heterorhabditis bilineatus, Agrilus baixerasana, Dichrorampha bilineatus, Mesochorus bakeri, Copidosoma bilineatus, Stictopisthus Balaustium – family Erythraeidae bimaculatum, Bembidion Balaustium sp. 239, 242 Binodoxys – family Braconidae Balcha – family Eupelmidae Binodoxys communis (Gahan) 95–96 Balcha indica (Mani & Kaul) 66 bipinnatum, Tanacetum balsam fi r (Abies balsamea) 203, 421 bipustulata, Aleochara balsam fi r sawfl y (Neodiprion abietis) 55 birch (Betula spp.) 83, 175–177 balsam woolly adelgid (Adelges piceae) 476 birch casebearer (Coleophora serratella) 476 balsamea, Abies birch leafminer (Fenusa pumila) 175–176, balsamita, Tanacetum 178–180 banana moth (Opogona sacchari) 476 birds-foot trefoil (Lotus corniculatus) 386 Banchus – family Ichneumonidae black ash (Fraxinus nigra) 63 Banchus fl avescens Cresson 228 black swallow-wort (Vincetoxicum nigrum) 402, banksiana, Pinus 403, 404 barley (Hordeum vulgare) 273, 354, 371, 373, blackberry (Rubus fructicosus) 152 414, 455 blackburni, Microchelonus barnyard grass (Echinochloa crus-galli) 373 blancardella, Phyllonorycter basicola, Thielaviopsis blue ash (Fraxinus quadrangulata) 63 bassiana, Beauveria blue elderberry (Sambucus cerulea Raf. var. batychrus, Leptacinus cerulea) 153 Beauveria – family Cordycipitaceae blue stain fungus (Leptographium wingfi eldii, Beauveria spp. 67, 75, 87 Ophiostoma minor) 267 Beauveria bassiana (Balsamo) Vuillemin 67, 68, blueberry (Vaccinium spp.) 152 74, 75, 78, 85, 86, 87, 103, 104, 110, 131, Bohemian knotweed (Fallopia x bohemica) 321, 144, 215, 222, 236, 279, 286, 287–288 322, 324, 325 Beauveria brongniartii (Saccardo) Petch 87 x bohemica, Fallopia beet, sugar beet (Beta vulgaris) 72, 441, 454 Bombus – family Apidae Beet pseudo-yellows virus – family Bombus spp. 103 Closteroviridae 99 Bombyliidae – order Diptera Begonia – family Begoniaceae bonariensis, Listronotus Begonia spp. 100 Bonnetia – family Tachinidae Bembidion – family Carabidae Bonnetia comta (Fallén) 165 Bembidion bimaculatum (Kirby) 172 borealis, Lygus Bembidion canadianum Casey 172 Boreioglycaspis – family Psyllidae Bembidion mutatum Gemminger & Harold 172 Boreioglycaspis melaleucae Moore 24 Bembidion nitidum (Kirby) 172 Bos – family Bovidae Bembidion obscurellum (Motschoulsky) 172 Bos taurus L. 182–183, 186, 187–188, 309–310, Bembidion quadrimaculatum (L.) 145, 147, 278, 378 281 Bostrichidae – order Coleoptera 477 Bembidion quadrimaculatum oppositum Say Botanophila – family Anthomyiidae 172, 216 Botanophila sp. near spinosa (Rondani) 399 Bembidion rupicola (Kirby) 172 Bothrideridae – order Coleoptera Bembidion versicolor (LeConte) 172 botrana, Lobesia Bemisia – family Aleyrodidae Botrytis – family Sclerotinaceae Bemisia tabaci (Gennadius) 99–100, 102, 103 Botrytis cinerea Pers. 449 berolinensis, Phalacrotophora Bovidae – order Artiodactyla bertha armyworm (Mamestra confi gurata) Brachypterolus – family Nitidulidae 228–231 Brachypterolus pulicarius (L.) 348, 356, 359 Beta – family Amaranthaceae Bracon – family Braconidae Beta vulgaris L. 72, 440, 441, 454 Bracon cephi (Gahan) 113, 114, 115, 116 Bethylidae – order Hymenoptera Bracon furtivus Fyles 59 Betula – family Betulaceae Bracon lissogaster (Muesebeck) 113, 114 Betula spp. 83, 175–177 Braconidae – order Hymenoptera 154, 245 bicolor, Hypnoidus Bradynema – family Allantonematidae bicolor, Sorghum Bradynema listronoti Zeng et al. 215, 217 bicolor, Townselitis Bradysia – family Sciaridae bicolorata, Zygogramma Bradysia spp. 101, 104 bicoloripes, Ageniaspis Brasema – family Eupelmidae bifasciata, Gallerucida Brasema allynii (French) 114, 115 big-eyed bug (Geocorus bullatus) 250 Brassica – family Brassicaceae bilineata, Aleochara Brassica spp. 124, 429 490 Index

Brassica carinata Braun 257 brown spruce longhorn beetle (Tetropium Brassica juncea (L.) Czern 142, 249, 257, 260, fuscum) 476 455 bruchophagi, Mesopolobus Brassica napus L. 16, 119, 120, 121, 124, 134, brumata, Operophtera 143, 146–147, 164, 221, 228, 248, 257, brunneum, Metarhizium 273, 329–330, 354, 371, 429, 440, 446, Brussels sprouts (Brassica oleracea var. 455 gemmifera) 134, 142 Brassica napus var. napobrassica (L.) Rchb. 142, Bryobia – family Tetranychidae 143, 144 Bryobia spp. 45 Brassica oleracea L. 142, 257, 439, 448 Bt (Bacillus thuringiensis) 37–38, 144, 228, 229, Brassica oleracea L. convar. oleracea 441 258, 286, 292, 294 Brassica oleracea var. acephala DC 441 Bti (Bacillus thuringiensis serovar. israelensis) Brassica oleracea var. botrytis L. 134 136 Brassica oleracea var. capitata L. 134, 298 Btk (Bacillus thuringiensis serovar. kurstaki) 59, Brassica oleracea var. gemmifera (DC) Zenker 101, 103, 130–131, 132, 186, 204, 229, 134 258, 292, 294 Brassica oleracea var. italica Plenk 134 buckthorn (Rhamnus spp.) 93–94 Brassica rapa L. 16, 119, 120, 121, 124, 134, buckwheat (Fagopyrum esculentum) 324–325, 164, 214, 221, 228, 248, 257, 273, 354, 455 429, 440 bullatus, Geocoris Brassica rapa ssp. oleifera (DC) Metzger 142 Bulleromyces – family Tremellaceae 425 Brassica rapa subsp. chinensis (L.) Hanelt 432, bumble bees (Bombus spp.) 103 439 Buprestidae – order Coleoptera 476 Brassica rapa subsp. pekinensis (Lour.) Hanelt Burkholderia – family Glomerellaceae 433 Burkholderia cepacia (Palleroni & Holmes) Brassica rapa var. rapa L. 454 Yabuuchi et al. 425 Brassicaceae – order Capparales 249, 256, 257 bursa-pastoris, Capsella brassicae, Mamestra brassicae, Plasmodiophora brassicae, Trichogramma Ca. Liberibacter – family Rhizobiaceae Brazilian pepper tree (Schinus terebinthifolius) Ca. Liberibacter psyllaurous 108 25 Ca. Phytoplasma – family Acholeplasmataceae Brentidae – order Coleoptera Ca. Phytoplasma oryzae 48 brevicollis, Altica cabbage (Brassica oleracea var. capitata) 134, breviforceps, Gonia 142, 298, 439 brevinucleata, Entomophthora cabbage looper (Trichoplusia ni) 101, 103, brevior, Vrestovia 291–294, 480 Brevipalpus – family Tenuipalpidae cabbage maggot, cabbage root fl y (Delia radicum) Brevipalpus phoenicis (Geijskes) 45 142–148 brevipetiolatus, Leiophron cabbage seedpod weevil (Ceutorhynchus brevipetiolatus, Perilitus obstrictus) 48–49, 119–125, 333, 481 brevis, Aphaereta cacoeciae, Trichogramma brevis, Deraeocoris Cactoblastis – family Pyralidae Brevoortia – family Clupeidae Cactoblastis cactorum (Berg) 17 Brevoortia patronus Goode 442, 458, 468 cactorum, Cactoblastis Brevoortia tyrannus (Latrobe) 442, 458 calathinus, Aceria bristly foxtail (Setaria verticillata) 370 calcitrans, Stomoxys broad mites (Polyphagotarsonemus latus) 100, calidum, Calosoma 101 californica, Autographa broad nosed weevils (Sitona spp.) 277–281 californicus, Limonius broadleaf cattail (Typha latifolia) 363 californicus, Neoseiulus broadleaf plantain, common plantain (Plantago caliginosus, Harpalus major) 214, 386 Callosobruchus – family Curculionidae broccoli (Brassica oleracea var. italica, convar. Callosobruchus maculatus (Fabricius) 217 oleracea) 134, 142, 441, 448, 455 calmariensis, Galerucella Bromus – family Poaceae 115 Calophasia – family Noctuidae brondelii, Rhinusa Calophasia lunula (Hufnagel) 344, 347–348, brongniartii, Beauveria 349, 356 bronze birch borer (Agrilus anxius) 66, 67 Calophyla – family Calophylidae broomleaf toadfl ax (Linaria genistifolia) 344, Calophyla spp. 25 345, 356 Calophylidae – order Hemiptera brown marmorated stinkbug (Halyomorpha Calosoma – family Carabidae halys) 101, 475 Calosoma calidum (Fabricius) 171, 172 Index 491

Camereria – family Gracillariidae Cardinium spp. 43, 44, 45 Camereria ohridella Deschka & Dimiü 26 carinata, Brassica cameroni, Spalangia carinifer, Diaparsis campestre, Lepidium carnea, Chrysoperla campestris, Microplontus carolinus, Melanerpes camphoratum, Tanacetum carota, Daucus Campogaster exigua Meigen see Microsoma carpatus, Apanteles exigua (Meigen) Carpinus – family Betulaceae 83 Campoletis – family Ichneumonidae carpocapsae, Steinernema Campoletis sp. 169 carrot (Daucus carota subsp. sativus) 72, Campoletis annulata (Gravenhorst) 58 214–216, 217, 298, 454 Campoletis atkinsoni (Viereck) 169 carrot weevil (Listronotus oregonensis) 214–218 Campoletis australis (Viereck) 169 Carthamus – family Asteraceae Campoletis fl avicincta (Ashmead) 169 Carthamus tinctorius L. 440 Campoletis sonorensis (Cameron) 169 cassava mealybug (Phenacoccus manihoti) 7 Campoplex – family Ichneumonidae Cassida – family Chrysomelidae Campoplex capitator Aubert 160–161, 162 Cassida azurea Fabricius 235–236 Campoplex difformis (Gmelin) 158, 160, 162 Cassida stigmatica Suffrian 380, 381 Campoplex dubitator Horstmann 158–161 Castanea – family Fagaceae Campoplex mutabilis Holmgren 158 Castanea dentata (Marsh.) Borkh. 476 Canada milk vetch (Astragalus canadensis) 456 castrans, Strongwellsea Canada thistle (Cirsium arvense) 387 catenulatum, Gliocladium canadense, Lilium Catogenus – family Passandridae canadensis, Arenetra Catogenus rufus (F.) 63 canadensis, Astragalus Catolaccus – family Pteromalidae canadensis, Leidyana Catolaccus aeneoviridis (Girault) 121, 259 canadensis, Populus Catolaccus cyanoideus Burks 259 canadensis, Solidago catoptron, Collyria canadianum, Bembidion cattle (Bos taurus) 182–183, 186, 187–188, canariensis, Phalaris 309–310, 378 candefacta, Tarachidia caudiglans, Typhlodromus Canidae – order Carnivora caulifl ower (Brassica oleracea var. botrytis) 134, Canis – family Canidae 142 Canis lupus familiaris L. 182 Cecidomyiidae – order Diptera cannabinum, Apocynum Cecidophyes – family Eriophyidae canola (Brassica napus, B rapa) 16, 119–120, Cecidophyes galii (Karpelles) 329 122–125, 134, 135, 142, 143, 144, 145, Cecidophyes rouhollahi Craemer 329–330, 331 147, 164, 221, 228, 231, 248–249, celery (Apium graveolens) 214 251–252, 257, 258, 259, 260, 273, 354, Celtis – family Cannabaceae 83 429–434, 440 Centaurea – family Asteraceae canus, Limonius Centaurea spp. 317, 481 capitata, Ceratitis Centaurea diffusa Lamarck 302–305 capitator, Campoplex Centaurea maculosa Lamarck see Centaurea cappaerti, Atanycolus stoebe subsp. micranthos (S.G. Gmel. ex Capra – family Bovidae Gugler) Hayek Capra hircus L. 333 Centaurea stoebe subsp. micranthos (S.G. Gmel. Capsella – family Brassicaceae ex Gugler) Hayek 302–305 Capsella bursa-pastoris (L.) Medik. 124, 257 Centistes – family Braconidae capsici, Phytophthora Centistes lituratus (Haliday) 278, 279 Capsicum – family Solanaceae cepa, Allium Capsicum annuum L. 99, 100, 101, 108, 109, cepacia, Burkholderia 111, 291, 387, 439, 440, 441, 454, cephi, Bracon 466–470 Cephidae – order Hymenoptera capucinus, Coryssomerus Cephus – family Cephidae Carabidae – order Coleoptera 94–95, 260, 274 Cephus cinctus Norton 112–116 Carabus – family Carabidae Cephus hyalinatus Konow see Cephus cinctus Carabus serratus Say 172 Norton Carabus taedatus Fabricius 172 Cephus pygmaeus (L.) 112, 114, 115, 116 Cardaria draba (L.) Desv. see Lepidium draba L. Cerambycidae – order Coleoptera 476, 477 cardariae, Ceutorhynchus Ceraphron – family Ceraphronidae cardariae, Contarinia Ceraphron sp. 154 cardariae, Dasineura Ceraphronidae – order Hymenoptera Cardinium – family Bacteroidaceae cerasus, Prunus 492 Index

Ceratitis – family Tephritidae chickpeas (Cicer arietinum) 439, 441 Ceratitis capitata (Wiedemann) 188 chili thrips (Scirtothrips dorsalis) 99 Cerceris – family Crabronidae chinensis, Anoplophora Cerceris fumipennis Say 63–64 chinensis, Euops Cercidiphyllum – family Cercidiphyllaceae 83 Chinese cabbage (Brassica rapa subsp. cereal leaf beetle (Oulema melanopus) 7, pekinensis) 433 233–236 Chlorocytus – family Pteromalidae cereale, Secale Chlorocytus sp. 121, 124 cereus, Bacillus Chloropidae – order Diptera 372 cernuum, Allium Choristoneura – family Tortricidae certus, Aphelinus Choristoneura rosaceana (Harris) 130–133 cerulea, Sambucus Chromatomyia – family Agromyzidae Ceutorhynchus – family Curculionidae Chromatomyia syngenesiae (Hardy) 100 Ceutorhynchus alliariae Brisout 124 Chrysanthemum – family Asteraceae Ceutorhynchus assimilis (Paykull) 121, 124, Chrysanthemum spp. 98, 100, 102, 103 334, 335 Chrysanthemum leucanthemum L. see Ceutorhynchus campestris Gyllenhal see Leucanthemum vulgare Lam. Microplontus campestris (Gyllenhal) Chrysanthemum morifolium Ramat 99 Ceutorhynchus cardariae Korotyaev 124, 334, chrysanthemum aphid (Macrosiphoniella 335 sanborni) 98, 339 Ceutorhynchus constrictus Marsham 123, 124 chrysanthemum leafminer (Chromatomyia Ceutorhynchus erysimi (Fabricius) 124, 217 syngenesiae) 100 Ceutorhynchus merkli Korotyaev 335 chrysocephala, Phyllotreta Ceutorhynchus neglectus Blatchley 122 Chrysocharis – family Eulophidae Ceutorhynchus obstrictus (Marsham) 48–49, Chrysocharis laricinellae (Ratzeburg) 7 119–125, 333, 481 Chrysochus – family Chrysomelidae Ceutorhynchus pleurostigma (Marsham) 121, Chrysochus (Eumolpus) asclepiadeus Pallas 404 124 Chrysochus auratus (Fabricius) 404 Ceutorhynchus punctiger Gyllenhall see Chrysochus cobaltinus LeConte 404 Glocianus punctiger (Sahlberg) Chrysodeixis – family Noctuidae Ceutorhynchus quadridens (Panzer) 121 Chrysodeixis chalcites (Esper) 476 Ceutorhynchus roberti Gyllenhall 124 Chrysolina – family Chrysomelidae Ceutorhynchus turbatus Schultze 123, 124, 334, Chrysolina asclepiadis asclepiadis (Villa) 404 335 Chrysolina hyperici (Förster) 8 Ceutorhynchus typhae (Herbst) 123, 124 Chrysolina quadrigemina (Suffrian) 8 Chaetocnema – family Chrysomelidae Chrysomela – family Chrysomelidae Chaetocnema spp. 252 Chrysomela populi L. 210 Chaetorellia – family Tephritidae Chrysomela tremula Fabricius 210 Chaetorellia acrolophi White 304 Chrysomelidae – order Coleoptera 372, 477 chaetospira, Heteroconium Chrysoperla – family Chrysopidae Chagas disease (Trypanosoma cruzii) 48 Chrysoperla spp. 109 Chalcididae – order Hymenoptera Chrysoperla carnea (Stephens) 110, 250 Chalcidoidea (superfamily) – order Chrysoperla rufi labris (Burmeister) 110 Hymenoptera 183, 372 Chrysopidae – order Neuroptera 109 chalcites, Chrysodeixis chrysostictos, Diadegma chalepense, Lepidium Cicadellidae – order Hemiptera chalybeus, Macroglenes Cicer – family Fabaceae Chamaemelum – family Asteraceae Cicer arietinum L. 439, 441 Chamaemelum nobile (L.) All. 380, 381 cichoracearum, Erysiphe Chasmanthium – family Poaceae cilinodis, Fallopia Chasmanthium latifolium (Michx.) H.O. Yates cimbicis, Sarcophaga 371, 373 cinctipes, Schlettererius cheiranthoides, Erysimum cinctus, Cephus Chelonus – family Braconidae cinerea, Athrycia Chelonus insularis Cresson 167 cinerea, Botrytis cherry bark tortrix (Enarmonia formosana) cinerosa, Periscepsia 156–162 Cirsium – family Asteraceae cherry (Prunus avium) 130, 152, 156, 159, 162, Cirsium arvense (L.) Scopoli 387 285 citri, Planococcus chestnut blight (Cryphonectria parasitica) 476 Citrullus – family Cucurbitaceae Chetogena – family Tachinidae Citrullus lanatus (Thunberg) Matsum. & Nakai Chetogena claripennis (Macquart) 165 387 Chetogena edwardsii (Williston) 166 citrus mealybug (Planococcus citri) 101 Index 493

claripennis, Chetogena coloradensis, Telenomus cleavers (Galium aparine) 329, 330–331 Colorado potato beetle (Leptinotarsa Cleridae – order Coleoptera decemlineata) 27, 235 Clivina – family Carabidae common toadfl ax, yellow toadfl ax (Linaria Clivina fossor L. 216 vulgaris) 25, 343, 344, 345, 349, cloacae, Enterobacter 354–360 Clonostachys – family Bionectriaceae communa, Ophraella Clonostachys spp. 439 communis, Binodoxys Clonostachys rosea f. catenulata (Gilman & communis, Helochara Abbott) Schroers 430, 440, 448 communis, Melanotus Clonostachys rosea f. rosea (Link) Schroers et al. communis, Pyrus 415, 427, 430 comta, Bonnetia clover root curculio (Sitona fl avescens, S. concinna, Stobaera hispidulus) 277, 278, 279 confi gurata, Mamestra clover root weevil (Sitona cylindricollis) 277, confl uens, Diplapion 278, 279, 280, 281 connexa, Euphranta clovers (Trifolium spp.) 277, 281, 387 Conotrachelus – family Curculionidae clubroot of crucifers (Plasmodiophora brassicae) Conotrachelus nenuphar Herbst 199 429–434 conquisitor, Itoplectis Clupeidae – order Clupeiformes consobrina, Ernestia coagulatus, Melanotrichus consortana, Dichrorampha cobaltinus, Chrysochus constrictus, Ceutorhynchus Coccinella – family Coccinellidae Contarinia – family Cecidomyiidae Coccinella septempunctata L. 94, 132, 136, 195 Contarinia cardariae Fedotova 334 coccinellae, Dinocampus Contarinia nasturtii Kieffer 134–136, 476, Coccinellidae – order Coleoptera 46, 94, 109, 478 238, 274 Contarinia tritici (Kirby) 274 Coccipolipus – family Podapolipidae contemplator, Pimpla Coccipolipus spp. 195 Conura – family Chalcididae coccodes, Colletotrichum Conura albifrons (Walsh) 59, 121, 259 Coccoidea (superfamily) – order Hemiptera 193 Conura torvina (Cresson) 121, 259 cockerelli, Bactericera convergens, Hippodamia codling moth (Cydia pomonella) 110, 130, Convolvulus – family Convolvulaceae 139–141, 161, 480 Convolvulus arvensis L. 307–308, 387 cognatus, Trichocellus Copidosoma – family Encyrtidae Coleomegilla – family Coccinellidae Copidosoma bakeri (Howard) 168, 170–171 Coleomegilla maculata lengi Timberlake 94, 195 cordubensis, Trichogramma Coleophora – family Coleophoridae Coreidae – order Hemiptera Coleophora malivorella Riley 7 coriaria, Dalotia Coleophora serratella L. 476 corn rootworm (Diabrotica virgifera virgifera) Coleophoridae – order Lepidoptera 27, 46 collaris, Diadromus corniculatus, Lotus Colletotrichum – family Glomerellaceae corticis, Lonchaea Colletotrichum acutatum J.H. Simmonds 425 Corvidae – order Passeriformes Colletotrichum coccodes (Wallr.) S.J. Hughes Corvus – family Corvidae 449 Corvus spp. 75 Colletotrichum gloeosporioides (Penzig) Penzig corymbosum, Vaccinium & Saccardo 425 Coryssomerus – family Curculionidae Colletotrichum gloeosporioides (Penzig) Penzig Coryssomerus capucinus (Beck) 397 & Saccardo f. sp. hyperici 368 Cosmopterigidae – order Lepidoptera Colletotrichum gloeosporioides (Penzig) Penzig cossi, Proctolaelaps & Saccardo f. sp. malvae 367–369 cotei, Anaphes Colletotrichum truncatum (Schwein.) Andrus & Cotesia – family Braconidae W.D. Moore 393, 394, 396, 397–399, 449 Cotesia spp. 260 Collops – family Melyridae Cotesia acronyctae (Riley) 167 Collops vittatus (Say) 250 Cotesia griffi ni (Viereck) 167 Collyria – family Ichneumonidae Cotesia laeviceps Ashmead 167 Collyria calcitrator (Gravenhorst) see Collyria Cotesia marginiventris (Cresson) 293, 294 coxator (Villers) Cotesia vanessae (Reinhard) 167 Collyria catoptron Wahl 116 cotton (Gossypium herbaceum, G. hirsutum) Collyria coxator (Villers) 115–116 222, 441, 449 Colobopyga – family Halimococcidae cotton aphid (Aphis gossypii) 98 Colobopyga pritchardiae Beardsley 27 coxator, Collyria 494 Index

CpGV (Cydia pomonella granulosus virus) culinaris, Lens 139–140, 141 culmorum, Fusarium crabapple (Malus sylvestris) 285 cupreum, Agonum crabgrass (Digitaria spp.) 373 cupreus, Poecilus Crabronidae – order Hymenoptera curassavica, Asclepias cracca, Vicia Curculionidae – order Coleoptera 476, 477 Crambidae – order Lepidoptera curculionis, Aliolus crataegella, Phyllonorycter curtus, Lemophagus Crataegus – family Rosaceae cyanoideus, Catolaccus Crataegus spp. 156, 285 Cyclamen – family Primulaceae creeping red fescue (Festuca rubra) 330 Cyclamen persicum Mill. 100 crevieri, Rhyssa cyclamen mite (Phytodromus pallidus) 100–101 criddlei, Agriotes Cyclogastrella – family Pteromalidae Crioceris – family Chrysomelidae Cyclogastrella simplex (Walker) 159 Crioceris asparagi (L.) 210 Cydia – family Tortricidae Crioceris duodecimpunctata (L.) 235 Cydia pomonella (L.) 110, 130, 139–141, 161, Crioceris quatuordecimpunctata (L.) 210 480 crispum, Petroselinum Cydia pomonella granulosus virus – family crispus, Rumex Baculoviridae 139–140, 141 Cronartium – family Cronartiaceae Cydonia – family Rosaceae Cronartium ribicola J.C. Fisch. 476 cylindricollis, Sitona crookwellense, Fusarium cylindriformis, Sylvanelater crows (Corvus spp.) 75 cylindrosporum, Tolypocladium crucifer, Mogulones Cynipidae – order Hymenoptera crucifer fl ea beetle (Phyllotreta cruciferae) Cynips – family Cynipidae 248–253 Cynips quercusfolii L. 29 cruciferae, Phyllotreta Cynoglossum – family Boraginaceae crus-galli, Echinochloa Cynoglossum offi cinale (L.) 309–313, 317, 356, cruzii, Trypanosoma 479, 482 Cryphonectria – family Cryphonectraceae cyparissiae, Aphthona Cryphonectria parasitica (Murrill) Barr 476 Cyphocleonus – family Curculionidae Cryptantha – family Boraginaceae Cyphocleonus achates Fahraeus 303, 304, 305 Cryptantha minima Rydb. 313 Cyphocleonus trisulcatus (Herbst) 339–340 Cryptococcus – family Tremellaceae Cystiphora – family Cecidomyiidae Cryptococcus magnus (Lodder & Kreger) Baptist Cystiphora taraxaci Kieffer 384 & Kurtzman 425 Cystosporogenes – family Glugeidae Cryptococcus nodaensis Sato et al. 415 Cystosporogenes sp. 67 Cryptococcus victoriae Montes et al. 426 Cytisus – family Fabaceae Cryptomeria – family Cupressaceae Cytisus scoparius (L.) Link 476 Cryptomeria japonica (Thunb. ex L. f.) D. Don Cyzenis – family Tachinidae 324 Cyzenis albicans (Fallén) 7 Ctenicera – family Elateridae czwalinae, Aphthona Ctenicera aeripennis destructor (Brown) 78 Ctenicera pruinina (Horn) 76–78 Cubocephalus – family Ichneumonidae Dacnusa – family Braconidae Cubocephalus sp. 66 Dacnusa pubescens (Curtis) 146 cucumber (Cucumis sativus) 99, 100, 101, 291, dahliae, Verticillium 439, 440, 441, 442–443 Dalapius – family Elateridae cucumber beetle (Diabrotica spp.) 101 Dalapius vagus Brown 73 cucumber mosaic virus (Cucumovirus cucumber Dalmatian toadfl ax (Linaria dalmatica) 25, 26, mosaic virus) 98, 343 342–350, 354, 355, 356, 359, 360 cucumerina, Monographella dalmatica, Linaria cucumeris, Neoseiulus Dalotia – family Staphylinidae cucumeris, Thanatephorus Dalotia coriaria (Kraatz) 104 Cucumis – family Cucurbitaceae dandelion (Taraxacum offi cinale) 383–389 Cucumis sativus L. 99, 100, 101, 291, 439, 440, Daphnia – family Daphniidae 441, 442–443 Daphnia spp. 385 Cucumovirus – family Bromoviridae Daphniidae – order Cladocera Cucumovirus cucumber mosaic virus 98, 343 darksided cutworm (Euxoa messoria) 164–173 Cucurbita – family Cucurbitaceae Dasineura – family Cecidomyiidae Cucurbita spp. 93, 192 Dasineura cardariae Fedotova 334 Cucurbita moschata Duschesne 387 Dastarcus – family Bothrideridae Culicidae – order Diptera 47 Dastarcus helophoroides (Fairmaire) 86, 87 Index 495

Daucus – family Apiaceae Dichrorampha baixerasana Trematerra 339, 340 Daucus carota L. 214 Dichrorampha consortana Stephens 339, 340 Daucus carota subsp. sativus Schülb. & M. Dicyphus – family Miridae Martens 72, 214–216, 217, 298, 454 Dicyphus hesperus Knight 103, 110, 293 debaryanum, Pythium difformis, Campoplex decemlineata, Leptinotarsa diffusa, Centaurea deformans, Taphrina diffuse knapweed (Centaurea diffusa) 302–305 degenerans, Iphesius Digamasellidae – order Megostigmata deilephilae, Winthemia Digitaria – family Poaceae deion, Trichogramma Digitaria spp. 373 Deladenus – family Neotylenchidae Digitonthophagus – family Scarabeidae Deladenus (Beddingia) siricidicola Bedding Digitonthophagus (Onthophagus) gazella 24–25, 265–266, 267–268 (Fabricius) 187–188 Delia – family Anthomyiidae digoneutis, Peristenus Delia brassicae (Bouché) see Delia radicum (L.) dill (Anethum graveolens) 214 Delia fl oralis (Fallén) 142 dimidiatus, Meteorus Delia radicum (L.) 142–148 Dinocampus – family Braconidae Delphacidae – order Hemiptera Dinocampus coccinellae Schrank 195 deltoides, Populus dioica, Urtica Dendrocopos – family Picidae Diospilus – family Braconidae Dendrocopos major (L.) 86, 87 Diospilus oleraceus Haliday 122 Dendrolaelaps – family Digamasellidae Diphyus – family Ichneumonidae Dendrolaelaps sp. 86 Diphyus apiculatus (Walkley) 169 densifl ora, Pinus Diphyus euxoae Heinrich 169 dentata, Castanea Diphyus nuncius (Cresson) 169 Deraeocoridae – order Hemiptera 238 Diphyus subfuscus (Cresson) 169 Deraeocoris – family Miridae Diplapion – family Brentidae Deraeocoris brevis (Uhler) 110 Diplapion confl uens Kirby 397 Dermestidae – order Coleoptera 477 Diplapion stolidum (Germar) 339, 340 Descurainia – family Brassicaceae Diprion – family Diprionidae Descurainia sophia (L.) Webb ex Prantl 257 Diprion similis Hartig 476 detrita, Endromopoda Diprionidae – order Hymenoptera Diabrotica – family Chrysomelidae discoideus, Sitona Diabrotica spp. 101 dispar, Lymantria Diabrotica virgifera virgifera LeConte 27, 46 dog (Canis lupus familiaris) 182 Diadegma – family Ichneumonidae dogbane (Apocynum cannabinum) 404 Diadegma sp. 157 dolabrata, Leptopterna Diadegma chrysostictos (Gmelin) 57 Dolichogenidea – family Braconidae Diadegma fenestrale (Holmgren) 57, 58, 60 Dolichogenidea impura (Nees) 60 Diadegma insulare (Cresson) 258–259, 260 Dolichogenidea laeviagata Ratzeburg 158 Diadromus – family Ichneumonidae Dolichomitus – family Ichneumonidae Diadromus collaris (Gravenhorst) 58, 60 Dolichomitus sp. 66 Diadromus pulchellus Wesmael 57, 58, 59–60 Dolichomitus vitticrus Townes 66 Diadromus subtilicornis (Gravenhorst) 258, 259, domestica, Malus 260 domestica, Musca Diadromus varicolor Wesmael 58, 60 domestica, Prunus diamondback moth (Plutella xylostella) 60, donovani, Leishmania 256–260, 292 dorsalis, Anchomenus diana, Anaphes dorsalis, Scirtothrips Diaparsis – family Ichneumonidae Douglas fi r (Pseudotsuga menziesii) 476 Diaparsis carinifer (Thomson) 234 douglasii, Tanacetum Diaparsis jucunda (Holmgren) 209, 210, 211, downy woodpecker (Picoides pubescens) 63 212 draba, Lepidium Diapriidae – order Hymenoptera drabae, Aceria diaspidicola, Encarsia Drechslera – family Pleosporaceae Diaspididae – order Hemiptera Drechslera gigantea S. Ito 373–374 Dibrachys – family Pteromalidae droozi, Telenomus Dibrachys affi nis Masi 159 Drosophila – family Drosophilidae Dibrachys microgastri (Bouché) 185 Drosophila hydei Sturtevant 46 Dichrorampha – family Tortricidae Drosophila melanogaster Meigen 44, 46, 49, Dichrorampha spp. 339 153 Dichrorampha aeratana (Pierce & Metcalfe) 339, Drosophila neotestacea Grimaldi, James & Jaenik 340 46 496 Index

Drosophila simulans Sturtevant 44, 46 173 Drosophila suzukii (Matsumura) 101, 152–154, Enterobacter cloacae (Jordan) Hormaeche & 241, 476, 477 Edwards 173, 456 drosophilae, Spalangia Entomophaga – family Entomophthoraceae Drosophilidae – order Diptera 47 Entomophaga aulicae (E. Reichardt) Humber dubia, Trichomalopsis 204 dubitator, Campoplex Entomophthora – family Entomophthoraceae dubius, Phyllobaenus Entomophthora brevinucleata Keller & Wilding dulcis, Prunus 274 duodecimpunctata, Crioceris Entomophthora muscae (Cohn) Fresenius 144 Duponchelia – family Crambidae Entomophthora sphaerosperma Fresenius 204 Duponchelia fovealis (Zeller) 101, 476 entomopox viruses – family Poxviridae 173 durum, Triticum enzymogenes, Lysobacter durum wheat (Triticum durum) 415 epambrosiae, Septoria Dutch elm disease (Ophiostoma ulmi, Epiblema – family Tortricidae O. novo-ulmi) 476 Epiblema strenuana Walker 297–298 Epicoccum – family Pleosporaceae Epicoccum nigrum Link 430 earthworms (order Megadrilacea) 385 epilobii, Pnigalio eastern hemlock looper (Lambdina fi scellaria Equidae – order Perissodactyla fi scellaria) 203 equiseti, Fusarium Echinochloa – family Poaceae Equus – family Equidae Echinochloa crus-galli (L.) P.Beauvois 373 Equus ferus L. 182 Echinothrips – family Thripidae Erebidae – order Lepidoptera Echinothrips americanus (Morgan) 99 Eretmocerus – family Aphelinidae edentulus, Microplontus Eretmocerus mundus Mercet 103 edwardsii, Chetogena Erigorgus – family Ichneumonidae eggplant, aubergine (Solanum melongena) 100, Erigorgus ambiguus (Norton) 170 454 Erioischia brassicae (Bouché) see Delia radicum Elaeagnus – family Eleagnaceae (L.) Elaeagnus angustifolia L. 83, 85 Eriophyidae – order Trombidiformes Elateridae – order Coleoptera Ernestia – family Tachinidae elderberry (Sambucus spp.) 153 Ernestia consobrina (Meigen) 228 elegans, Amphimermis errabundus, Lemophagus elegans, Stachybotrys error, Euxestonotus elisus, Lygus erucarum, Habrobracon ellipsis, Amara Erwinia – family Enterobacteraceae Elymus – family Poaceae Erwinia amylovora (Burrill) Winslow et al. Elymus repens (L.) Gould 467 408–411 emarginata, Prunus erysimi, Ceutorhynchus emarginatoria, Megarhyssa Erysimum – family Brassicaceae emerald ash borer, -(Agrilus planipennis) 62–68, Erysimum cheiranthoides L. 257 476, 477 Erysiphe – family Erysiphaceae Enarmonia – family Tortricidae Erysiphe cichoracearum DC 379 Enarmonia formosana Scopoli 156–162 Erythraeidae – order Trombidiformes 238 Encarsia – family Aphelinidae erythrocephala, Acantholyda Encarsia diaspidicola Silvestri 27 esculentum, Fagopyrum Encarsia hispida De Santis 45 esula, Euphorbia Encyrtidae – order Hymenoptera 245 Eteobalea – family Cosmopterigidae endius, Spalangia Eteobalea intermediella (Riedl) 344, 358 Endromopoda – family Ichneumonidae Eteobalea serratella (Treitschke) 358 Endromopoda detrita Holmgren 114, 115 eubius, Pediobius Endromopoda nigricoxis (Ulbricht) 58 Euderus – family Eulophidae English ash (Fraxinus excelsior) 63 Euderus sp. 245 English laurel (Prunus laurocerasus) 156 Euderus glaucus Yoshimoto 121 Enicospilus – family Ichneumonidae eugenii, Anthonomus Enicospilus sp. 169 Eulophidae – order Hymenoptera 245 Enoclerus – family Cleridae Euops – family Attelabidae Enoclerus sp. 63 Euops chinensis Voss 323 Enoclerus sphegeus (Fabricius) 287 Eupelmidae – order Hymenoptera ensator, Lathrolestes Eupelmus – family Eupelmidae Enterobacter – family Enterobacteraceae Eupelmus allynii (French) see Brasema allynii Enterobacter aerogenes Hormaeche & Edwards (French) Index 497

Eupelmus pini Taylor 66 faberi, Setaria Eupelmus vesicularis (Retzius) 114, 115, 121, face fl y (Musca autumnalis) 185 185, 393 faecalis, Alcaligenes Euphorbia – family Euphorbiaceae faecalis, Streptococcus Euphorbia esula L. 315–319, 481 Fagopyrum – family Polygonaceae Euphorbia pulcherrima Willd. ex Klotzsch 99, Fagopyrum esculentum Moench 324–325, 455 102 Fagus – family Fagaceae 83 euphorbiae, Hyles falcatus, Pygostolus euphorbiae, Macrosiphum fallacis, Neoseiulus Euphranta – family Tephritidae Fallopia – family Polygonaceae Euphranta connexa (Fabricius) 404–405 Fallopia spp. 321–323, 324–326, 478 Eupithecia – family Geometridae Fallopia cilinodis (Michaux) Holub 324 Eupithecia satyrata dodata Taylor 379 Fallopia japonica (Houtt.) Ronse Decraene Eupoecilia – family Tortricidae 321–322, 323, 324, 325 Eupoecilia ambiguella Hübner 160 Fallopia sachalinensis (F. Schmidt) Ronse European apple sawfl y (Hoplocampa testudinea) Decraene 321, 322, 323, 324, 325 198–201, 480 Fallopia x bohemica (Chrtek & Chrtková) J. P. European black elderberry (Sambucus nigra) Bailey 321, 322, 324, 325 153 false cleavers (Galium spurium) 329–331 European corn borer (Ostrinia nubilalis) 38, 101 farinosa, Isaria European earwig (Forfi cula auricularia) 287 farinosus, Paecilomyces European grape berry moth (Eupoecilia fasciata, Phalacrotophora ambiguella) 160 fasciatus, Trichomalus European grapevine moth (Lobesia botrana) fastidiosa, Xylella 160–161 fatua, Avena European red mite (Panonychus ulmi) 238–242, febriculosus, Homoporus 479 feltiae, Microplitis European stem sawfl y (Cephus pygmaeus) 112, feltiae, Steinernema 114, 115, 116 fenestrale, Diadegma europeator, Itoplectis Fenusa – family Tenthredinidae Eurytoma – family Eurytomidae Fenusa pumila Leach 175–176, 178–180 Eurytoma sp. 66 Fenusa pusilla (Lepeletier) see Fenusa pumila Eurytoma atripes Gahan 114, 115 Leach Eurytoma tylodermatis Ashmead 121 Fenusella – family Tenthredinidae Eurytomidae – order Hymenoptera Fenusella nana (Klug) 180 Euseius – family Phytoseiidae ferus, Equus Euseius ovalis (Evans) 104 Festuca – family Poaceae Eutanyacra – family Ichneumonidae Festuca rubra L. 330 Eutanyacra suturalis (Say) 170 Ficus – family Moraceae euvesicatoria, Xanthomonas Ficus sp. 153 Euxestonotus – family Platygastridae fi eld bindweed (Convolvulus arvensis) 307–308, Euxestonotus error (Fitch) 274–275 387 Euxoa – family Noctuidae fi eld cricket (Gryllus pennsylvanicus) 250 Euxoa auxiliaris (Grote) 164–173 fi eld peas (Pisum sativum) 277, 278, 354, 374, Euxoa messoria (Harris) 164–173 396, 439, 440 Euxoa ochrogaster (Guenée) 164–173 fi g (Ficus sp.) 153 euxoae, Diphyus Figitidae – order Hymenoptera 154 eversmanni, Rhinusa fi r (Abies spp.) 387, 421 excelsior Fraxinus fi reblight (Erwinia amylovora) 408–411 Exetastes – family Ichneumonidae fi rethorn (Pyracantha spp.) 156 Exetastes lasius Cushman 170 fi scellaria, Lambdina Exetastes obscurus Cresson 170 fl ava, Aphthona exigua, Microsoma fl aveolatum, Agrypon exigua, Phoma fl avescens, Banchus eximius, Macroglenes fl avescens, Sitona exitiosa, Synanthedon fl avicaudis, Nedyus Exserohilum – family Pleosporaceae fl aviceps, Stictopisthus Exserohilum rostratum (Drechsler) Leonard & fl avicincta, Campoletis Suggs 373 fl avipes, Anaphes Flavobacterium – family Flavobacteriaceae Flavobacterium spp. 43, 45 faba, Vicia fl avotibiae, Telenomus faba bean (Vicia faba) 277, 278 fl avovariatus, Apanteles 498 Index

fl ax (Linum usitatissimum) 164, 273, 371, 387, Fusarium oxysporum Schlechtend: Fries f. sp. 392 radicis-lycopersici W.R. Jarvis & fl eschneri, Agistemus Shoemaker 448–449 fl ixweed (Descurainia sophia) 257 Fusarium pseudograminearum O’Donnell & fl occulosa, Pseudozyma T. Aoki 115 fl oralis, Delia Fusarium head blight (FHB), Gibberella ear rot fl oridanus, Spathius (Fusarium graminearum) 412–417 fl uorescens, Pseudomonas fuscicollis, Gonia Fomes annosus (Fries) Cooke see Heterobasidion fuscum, Tetropium annosum (Fries) Brefeld Forfi cula – family Forfi culidae Forfi cula auricularia (L.) 287 Gaeolaelaps – family Laelapidae Forfi culidae – order Dermaptera Gaeolaelaps aculeifer (Canestrini) 27, 104 Formicidae – order Hymenoptera 477 Gaeolaelaps gillespiei Beaulieu 104 formosana, Enarmonia Galendromus – family Phytoseiidae fossor, Clivina Galendromus occidentalis (Nesbitt) 239 fovealis, Duponchelia Galerucella – family Chrysomelidae foxglove aphid (Aulacorthum solani) 98, 99, Galerucella calmariensis L. 235, 363–365, 482 104, 105 Galerucella pusilla Duftschmid 363, 364–365, foxtail millet (Setaria italic) 371 482 Fragaria – family Rosaceae galii, Cecidophyes Fragaria x ananassa Duschesne ex Rozier 152, galinae, Spathius 222, 223 Galium – family Rubiaceae Frangula – family Rhamnaceae Galium aparine L. 329, 330–331 Frangula alnus Mill. 153 Galium spurium L. 329–331 Frankliniella – family Thripidae Galium tricornutum Dandy 329 Frankliniella occidentalis (Pergande) 99, 102, Gallerucida – family Chrysomelidae 103, 105 Gallerucida bifasciata Motschulsky 323 Franklin’s gull (Leucophaeus pipixcan) 171 gambiae, Anopheles fraternus, Horismenus Ganaspis – family Figitidae Fraxinus – family Oleaceae Ganaspis sp. 154 Fraxinus spp. 63, 83 Ganaspis xanthopoda (Ashmead) 154 Fraxinus americana L. 63 gardneri, Xanthomonas Fraxinus excelsior L. 63 garlic (Allium sativum) 56, 57, 480 Fraxinus latifolia Benth. 63 garlic mustard (Alliaria petiolata) 124, 476 Fraxinus nigra Marsh. 63 Gastrophysa – family Chrysomelidae Fraxinus pennsylvanica Marsh. 63, 66 Gastrophysa polygoni (L.) 235 Fraxinus profunda (Bush) Bush 63 gazella, Digitonthophagus Fraxinus quadrangulata Michx. 63 Gelechiidae – order Lepidoptera 59 Fritillaria – family Liliaceae Gelis – family Ichneumonidae Fritillaria spp. 208 Gelis longicauda (Thomson) 159 fructicosus, Rubus gemellus, Mesopolobus fulviana, Villa geniculata, Setaria fumator, Phygadeuon geniculatum, Odontocolon fumipennis, Arenetra genistifolia, Linaria fumipennis, Cerceris Geocoridae – order Hemiptera 109 fumosorosea, Isaria Geocoris – family Geocoridae funerarius, Harpalus Geocoris spp. 109 fungus gnats (Bradysia spp.) 101, 104 Geocoris bullatus (Say) 250 furtivus, Bracon Geolaelaps – family Laelapidae Fusarium – family Nectriaceae Geolaelaps aculeifer (Canestrini) see Fusarium spp. 430 Gaeolaelaps aculeifer (Canestrini) Fusarium acuminatum Ell. & Ev. sensu Gordon Geolaelaps sp. nr. aculeifer (Canestrini) see 115 Gaeolaelaps gillespiei Beaulieu Fusarium avenaceum (Fries) Saccardo 115, 412, Geometridae – order Lepidoptera 416 geranium (Pelargonium spp.) 442 Fusarium crookwellense Burgess, Nelson & Gerbera – family Asteraceae Toussoun 412 Gerbera jamesonii Adlam 99, 100 Fusarium culmorum (Wm. G. Sm.) Sacc 115, giant foxtail (Setaria faberi) 370, 375 412, 416 giant knotweed (Fallopia sachalinensis) 321, Fusarium equiseti (Corda) Saccardo 372 322, 323, 324, 325 Fusarium graminearum Schwabe 17, 412–417 Gibberella – family Nectriaceae Fusarium oxysporum Schlechtend 416, 442 Gibberella zeae (Schwein.) Petch. 412, 415 Index 499

gigantea, Drechslera green foxtail (Setaria viridis) 370–375 gigantea, Phlebiopsis green peach aphid (Myzus persicae) 98, 99, 105 gillespiei, Gaeolaelaps greenhouse whitefl y (Trialeurodes ginseng (Panax quinquefolius) 440 vaporariorum) 99, 100, 102 glabripennis, Anoplophora griffi ni, Cotesia glassy winged soldier bug (Hyaloides grisea, Pyricularia vitripennis) 241 griseocarneus, Streptomyces glauca, Setaria griseoviridis, Streptomyces glaucus, Euderus grizzly bear (Ursus arctos horribilis) 171, 173 Gliocladium – family Hypocreaceae groundsel, common (Senecio vulgaris) 387 Gliocladium spp. 439, 448 Gryllidae – order Orthoptera Gliocladium catenulatum J.C. Gilman & E.V. Gryllus – family Gryllidae Abbott 426, 427, 430, 440 Gryllus pennsylvanicus Bermeister 250 Gliocladium roseum Bainier 426 Grypocentrus – family Ichneumonidae globata, Microgaster Grypocentrus albipes Ruthe 176, 178, 179, 180 Globodera – family Heteroderidae guani, Scleroderma Globodera rostochiensis (Wollenweber) Behrens Gulf menhaden fi sh (Brevoortia patronus) 442, 476 458, 468 Glocianus – family Curculionidae gulls (Laridae) 75 Glocianus punctiger (Sahlberg) 384 Gymnetron – family Curculionidae gloeosporioides, Colletotrichum Gymnetron antirrhini (Paykull) see Rhinusa Glomus – family Glomeraceae antirrhini (Paykull) Glomus intraradices Schenck & Smith 448 Gymnetron linariae Panzer see Rhinusa linariae gloxinia (Sinningia speciosa) 100 (Panzer) Glugeidae – order Microsporidia Gymnetron netum (Germar) see Rhinusa neta Glycine – family Fabaceae (Germar) Glycine max (L.) Merr. 93–94, 95–96, 193, 297, Gymnetron tetrum Fabricius 217 298, 371, 396, 447, 455 gypsy moth (Lymantria dispar) 476 glycines, Aphis Gyranusoidea – family Encyrtidae Glypta – family Ichneumonidae Gyranusoidea tebyg Noyes 31 Glypta variegata Dasch 131 goats (Capra hircus) 333 golden currant (Ribes aureum) 153 Habrobracon – family Braconidae golden nematode (Globodera rostochiensis) 476 Habrobracon erucarum Cushman 167 goldenrod (Solidago canadensis) 467 Habrocytus – family Pteromalidae Gonia – family Tachinidae Habrocytus (Pteromalus) sp. 122 Gonia spp. 166 Hackelia – family Boraginaceae Gonia aldrichi Tothill 166 Hackelia micrantha (Eastw.) J.L. Gentry 313 Gonia breviforceps Tothill 166 Hackelia venusta (Piper) H. St. John 313 Gonia fuscicollis Tothill 166 Hadrobunus – family Sclerosomatidae gordius, Sympiensis Hadrobunus maculosus (Wood) 173 gossypii, Aphis Haematobia – family Muscidae Gossypium – family Malvaceae Haematobia irritans L. 182–183, 185–187 Gossypium herbaceum L. 222, 441 haematobiae, Spalangia Gossypium hirsutum L. 449 hairy woodpecker (Picoides villosus) 63 gracilis, Stenomalina halcyon, Poecilanthrax Gracillariidae – order Lepidoptera Halimococcidae – order Hemiptera grackle, common (Quiscalus quiscula) 171, 173 Halyomorpha – family Pentatomidae graminearum, Fusarium Halyomorpha halys (Stål) 101, 475 graminicola, Pythium halys, Halyomorpha graminicola, Sclerospora hamatum, Trichoderma graminis, Rhodotorula Harmonia – family Coccinellidae graminoides, Meliboeus Harmonia axyridis (Pallas) 94, 132, 136, granulatus liragus, Agrilus 192–196 granuloviruses – family Baculoviridae 173, 292 Harpalus – family Carabidae grape (Vitis vinifera) 48, 153, 192, 193–195, 238, Harpalus amputatus Say 172 240–241 Harpalus caliginosus (Fabricius) 171, 172 graveolens, Anethum Harpalus funerarius Csiki 172 graveolens, Apium harzianum, Trichoderma great-spotted woodpecker (Dendrocopos major) hawthorn (Crataegus spp.) 156, 285 86, 87 Hebecephalus – family Cicadellidae green apple aphid (Aphis pomi) 132 Hebecephalus occidentalis Beamer & Tuthill green ash (Fraxinus pennsylvanica) 63, 66 372 500 Index

Hebecephalus rostratus Beamer & Tuthill 372 Histeridae – order Coleoptera Helianthus – family Asteraceae hoary cress, whitetop (Lepidium draba, L. Helianthus annuus L. 164 chalapense, L. appelianum) 124, Helicidae – order Mollusca 477 332–335 Helochara – family Cicadellidae hoferi, Rhyssa Helochara communis Fitch 372 Hololepta – family Histeridae helophoroides, Dastarcus Hololepta sp. 86 helymus, Periscepsia Homalotylus – family Encyrtidae Hemerobiidae – order Neuroptera Homalotylus spp. 195 Hemicrepidius – family Elateridae Hominidae – order Primates Hemicrepidius memnonius (Herbst) 73 Homo – family Hominidae hemipteron, Theroscopus Homo sapiens L. 182, 192, 296, 378 Hemiteles – family Ichneumonidae Homoporus – family Ichneumonidae Hemiteles inimicus Gravenhorst 158 Homoporus febriculosus (Girault) 114, 115 hemlock looper (Lambdina fi scellaria) 203–206 honey bee (Apis mellifera) 385 herbaceum, Gossypium honeysuckle (Lonicera sp.) 153 herbarum, Phoma hookerorum, Omphalapion hertingi, Myxexoristops Hoplocampa – family Tenthredinidae hesperus, Dicyphus Hoplocampa testudinea (Klug) 198–201, 480 hesperus, Lygus Hordeum – family Poaceae hesperus, Pimpla Hordeum vulgare L. 273, 354, 371, 373, 414, Heterathrus – family Tenthredinidae 455 Heterathrus nemoratus (Fallén) 180 Horismenus – family Eulophidae Heterobasidion – family Bondarzewiaceae Horismenus fraternus (Fitch) 245 Heterobasidion abietinum Niemelä & Korhonen horn fl y (Haematobia irritans) 182–183, 421 185–187 Heterobasidion annosum (Fries) Brefeld 420, horse-chestnut leaf miner (Camereria ohridella) 421, 422 26 Heterobasidion irregulare Garbel. & Otrosina horse (Equus ferus) 182 420–422 horticola, Phylloptera Heterobasidion occidentalis Otrosina & hospes, Microgaster Garbelotto 420–421 houndstongue (Cynoglossum offi cinale) Heterobasidion parviporum Niemelä & 309–313, 317, 356, 479, 482 Korhonen 421, 422 house fl y (Musca domestica) 182–188 Heteroconium – family Herpotrichiellaceae Howardula – family Allantonematidae Heteroconium chaetospira (Grove) M.B. Ellis Howardula phyllotreta Oldham 250 430, 431–432, 433–434 howdenorum, Rhyssa Heteroderidae – order Tylenchida hudsonianum, Ribes heterophylla, Tsuga huidobrensis, Liriomyza Heterorhabditidae – order Rhabiditida huronense,Tanacetum Heterorhabditis – family Heterorhabditidae Hyaloides – family Miridae Heterorhabditis spp. 78, 79, 87, 161 Hyaloides vitripennis (Say) 241 Heterorhabditis bacteriophora Poinar 136, 215, Hyalomyodes – family Tachinidae 279–280, 288 Hyalomyodes triangulifera Loew 278, 279 heterotoma, Leptopilina hydei, Drosophila Heterotylenchus – family Sphaerulariidae Hylemya brassicae (Bouché) see Delia radicum Heterotylenchus sp. 144 (L.) Hexamermis – family Mermithidae Hyles – family Sphingidae Hexamermis albicans Steiner 250 Hyles euphorbiae (L.) 315 hexaploide, x Triticale Hylobius – family Curculionidae heydeni, Mecinus Hylobius transversovittatus Goeze 363, 365 hicorae, Atanycolus Hypena – family Erebidae highbush blueberry (Vaccinium corymbosum) Hypena opulenta (Christoph) 405 424, 425, 426 Hypera – family Curculionidae Hippodamia – family Coccinellidae Hypera postica (Gyllenhal) 280 Hippodamia convergens (Say) 109 hyperici, Chrysolina hircus, Capra Hypericum – family Hypericaceae hirsutum, Gossypium Hypericum perforatum L. 8, 368 hirtus, Plagiobothrys hyperodae, Microctonus hirundinaria, Vincetoxicum Hypnoidus – family Elateridae hispae, Scambus Hypnoidus abbreviatus (Say) 73 hispida, Encarsia Hypnoidus (Hypolithus) bicolor (Eschscholtz) hispidulus, Sitona 73, 78 Index 501

Hypoaspis aculeifer (Canestrini) see Gaeolaelaps Isadelphus – family Ichneumonidae aculeifer (Canestrini) Isadelphus inimicus (Gravenhorst) 158, 159 Hypoaspis miles (Berlese) see Stratiolaelaps Isaria – family Cordycipitaceae scimitus (Wormersley) Isaria farinosa (Holmskjold) Fries (Paecilomyces Hypoaspis sp. nr. aculeifer (Canestrini) see farinosus) 67, 86, 87 Gaeolaelaps gillespiei Beaulieu Isaria fumosorosea (Wize) 67, 104, 110 Isophrictis – family Gelechiidae Isophrictis striatella (Denis & Schiffermüller) Ibalia – family Ibaliidae 380, 381 Ibalia spp. 265 itadori, Aphalara Ibalia jakowlewi Jacobson 266 italic, Setaria Ibalia leucospoides ensiger Norton 266 Itoplectis – family Ichneumonidae Ibalia leucospoides leucospoides (Hochenwarth) Itoplectis conquisitor (Say) 59, 204, 260 265, 266, 267 Itoplectis europeator Aubert 58 Ibalia montana Cresson 266 Itoplectis maculator (Fabricius) 57 Ibalia rufi collis Cameron 266 Itoplectis quadricingulata (Provancher) 157, 260 Ibalia rufi pes drewseni Borries 266 Itoplectis tunetana (Schmiedeknecht) 58 Ibalia rufi pes rufi pes Cresson 266 Ibaliidae – order Hymenoptera Ichneumon – family Ichneumonidae jack pine (Pinus banksiana) 264, 422 Ichneumon longulus Cresson 171 Jacobaea – family Asteraceae Ichneumonidae – order Hymenoptera 115, 245 Jacobaea vulgaris Gaertn. 8 Icteridae – order Passeriformes jacobaeae, Tyria idaeus, Rubus jakowlewii, balia illustris, Amsonia jamesonii, Gerbera Impatiens – family Balsaminaceae janthiniformis, Mecinus Impatiens spp. 100 janthinus, Mecinus impatiens necrotic spot virus – family Japanese knotweed (Fallopia japonica) 321–322, Bunyaviridae 99 323, 324, 325 impiger, Phaeogenes japonica, Cryptomeria impiger, Tycherus japonica, Fallopia impostor, Iphiaulax jucunda, Diaparsis impura, Dolichogenidea julis, Tetrastichus impurus, Apanteles juncea, Brassica inaequalis, Venturia incertus, Lyrcus incompletus, Macrocentrus kale (Brassica oleracea var. acephala) 441 inconstans, Spilichneumon kasugaensis, Streptomyces Indian mustard (Brassica juncea) 142, 249, 257, keltoni, Lygus 260, 455 Kentucky bluegrass (Poa pratensis) 384 indica, Azadirachta kewleyi, Microplitis indica, Balcha Klebsiella – family Enterobacteriaceae inimicus, Hemiteles Klebsiella pneumonia (Schroeter) Trevisan 173 inimicus, Isadelphus Kleidotoma – family Figitidae inodorum, Tripleurospermum Kleidotoma sp. 154 Inostemma – family Platygastridae knapweeds (Centaurea spp.) 302–305, 317, 481 Inostemma opacum Thomson 136 knotroot (Setaria geniculata) 370 insulare, Diadegma Kochia – family Amaranthaceae insularis, Chelonus Kochia scoparia (L.) Schrad. 16 intermediella, Eteobalea Koelreuteria – family Sapindaceae 83 intraradices, Glomus invadens, Rastrococcus inyoense, Trichogramma lacertosa, Aphthona iole, Anaphes Lactobacillus – family Lactobacillaceae Iphesius – family Phytoseiidae Lactobacillus plantarum (Orla-Jensen) Bergey Iphesius degenerans Berelese 104 et al. 416 Iphiaulax – family Braconidae Lactuca – family Asteraceae Iphiaulax impostor (Scopoli) 86 Lactuca sativa L. 291, 385, 440 ircutianum, Leucanthemum lacustre, Leucanthemum Irenimus – family Curculionidae Laelapidae – order Megostigmata Irenimus aequalis Broun 216 laeviagata, Dolichogenidea irregulare, Heterobasidion laeviceps, Cotesia irritans, Haematobia laevigata, Periscepsia 502 Index

laevigatus, Apanteles Leishmania donovani Laveran & Mesnil 48 Lambdina – family Geometridae Leluthia – family Braconidae Lambdina fi scellaria (Guenée) 203–206 Leluthia astigma (Ashmead) 66 Lambdina fi scellaria fi scellaria (Guenée) 203 Lema – family Chrysomelidae Lambdina fi scellaria lugubrosa (Hulst) 203 Lema trilineata (Olivier) 210 Lambdina fi scellaria somniaria (Hulst) 203 Lemophagus – family Ichneumonidae lanatus, Citrullus Lemophagus curtus (Townes) 234 lance-leaf plantain (Plantago lanceolata) 214 Lemophagus errabundus (Gravenhorst) 209, lanceolata, Plantago 210, 211, 212 Lappula – family Boraginaceae Lemophagus pulcher (Szepligeti) 210, 211 Lappula squarrosa (Retz.) Dumort. 312 Lens – family Fabaceae laricinellae, Chrysocharis Lens culinaris Medik. (lentil) 392, 396, 398–399 Laridae – order Charadriiformes 75 Lepidium – family Brassicaceae Larinus – family Curculionidae Lepidium appelianum Al-Shehbaz 332, 333, Larinus minutus Gyllenhal 303–305 334, 335 Larinus obtusus Gyllenhal 303 Lepidium campestre (L.) W.T. Aiton 334, 335 Lasioseius – family Ascidae Lepidium chalepense L. 332, 333, 334, 335 Lasioseius ometes (Oudemans) 86 Lepidium draba L. 124, 332–335 Lasioseius sp. 86 Lepidium latipes Hook. 334 Lasius – family Formicidae lepidus, Sitona lasius, Exetastes Leptacinus – family Staphylinidae Lasius niger neoniger Emery 172 Leptacinus batychrus (Gyllenhal) 172 Latalus – family Cicadellidae Leptinotarsa – family Chrysomelidae Latalus personatus Beirne 372 Leptinotarsa decemlineata Say 27, 235 lateralis, Napomyza Leptographium – family Ophiostomataceae lateralis, Villa Leptographium wingfi eldii M. Morelet 267 Lathrolestes – family Ichneumonidae Leptopilina – family Figitidae Lathrolestes spp. 179 Leptopilina heterotoma (Thomson) 46 Lathrolestes ensator Brauns 199–201 Leptopterna – family Miridae Lathrolestes luteolator (Gravenhorst) see Leptopterna dolabrata (L.) 223 Lathrolestes thomsoni Reshchikov Leptosphaeria – family Leptosphaeriaceae Lathrolestes nigricollis (Thomson) 176, 178–179 Leptosphaeria maculans (Fuckel) Ces. & De Not. Lathrolestes soperi Reshchikov 179 432 Lathrolestes thomsoni Reshchikov 176–180 Leskia – family Tachinidae laticollis, Phratora Leskia aurea (Fallén) 158 latifolia, Fraxinus lettuce (Lactuca sativa) 291, 385, 440 latifolia, Typha leucanthemi, Macrosiphoniella latifolium, Chasmanthium Leucanthemum – family Asteraceae latior, Amara Leucanthemum ircutianum DC 337–338, 339 latipennis, Ostrinia Leucanthemum lacustre (Brot.) Samp. 338 latipes, Lepidium Leucanthemum maximum (Ramond) DC. 338 latus, Polyphagotarsonemus Leucanthemum × superbum (Bergmans ex J.W. laurocerasus, Prunus Ingram) D.H. Kent 338, 339, 340 leafy spurge (Euphorbia esula) 315–319, 481 Leucanthemum vulgare Lam. 337–340 Lecanicillium – family Cordycipitaceae Leucoma – family Lymantriidae Lecanicillium spp. 67 Leucoma salicis (L.) 7 Lecanicillium lecanii (Zimmerman) Zare & W. Leucophaeus – family Laridae Gams 110, 144 Leucophaeus pipixcan (Wagler) 171, 173 lecanii, Lecanicillium leucospoides, Ibalia leek (Allium porrum) 56, 57, 59, 480 lilacinum, Purpureocillium leek moth (Acrolepiopsis assectella) 56–61, 476, lilii, Lilioceris 478, 480 Lilioceris – family Chrysomelidae Leidyana – family Leidyanidae Lilioceris lilii (Scopoli) 208–212, 235 Leidyana canadensis Clopton & Lucarotti 204 Lilioceris merdigera L. 210 Leiobunum – family Phalangiidae Lilioceris tibialis Villa 210 Leiobunum vittatum (Say) 173 Lilium – family Liliaceae Leiophron – family Braconidae Lilium spp. 208 Leiophron spp. 222 Lilium canadense L. 208 Leiophron lygivorus (Loan) 222 Lilium martagon L. 209 Leiophron solidaginis Loan 222 Lilium philadelphicum L. 208 Leiophron sp. near brevipetiolatus Loan 222 Lilium superbum L. 208 Leiophron uniformis (Gahan) 222 lily leaf beetle (Lilioceris lilii) 208–212, 235 Leishmania – order Trypanosomatida limitata, Pandemis Index 503

limonicus, Typhlodromalus Longitarsus sp. near noricus Leonardi 380–381 Limonius – family Elateridae Longitarsus succineus (Foudras) 380 Limonius agonus Say 73 longulus, Ichneumon Limonius californicus (Mannerheim) 73 Lonicera – family Caprifoliaceae Limonius canus LeConte 73, 76–78 Lonicera sp. 153 Limonius pectoralis LeConte 73 Lonicera tatarica L. 153 Linaria – family Plantaginaceae lopezi, Anagyrus Linaria spp. 25–26, 317, 343, 344, 350, 355, 356, Lotus – family Fabaceae 360, 481 Lotus corniculatus L. 386 Linaria dalmatica (L.) Miller 25, 26, 342–350, lowbush blueberry (Vaccinium angustifolium) 354, 355, 356, 359, 360 424–425, 426–427 Linaria dalmatica subsp. dalmatica (L.) D.A. lucerne (Medicago sativa) 195, 221, 222, 223, Mill. 344 224, 277, 278, 280, 333, 396, 455 Linaria dalmatica subsp. macedonica (Griseb.) lucidus, Trichomalus D.A. Sutton 344, 345, 356 luctuosa, Tyta Linaria dalmatica x Linaria vulgaris Miller 344 lucublandus, Pterostichus Linaria genistifolia (L.) Miller 25, 344, 345, 356 lunula, Calophasia Linaria vulgaris Miller 25, 343, 344, 345, 349, lupus familiaris, Canis 354–360 lycopersici, Aculops linariae, Rhinusa lycopersicum, Solanum linearis, Macrocentrus Lyctocoris – family Anthocoridae lineatus, Agriotes Lyctocoris sp. 86 lineatus, Sitona lydicus, Streptomyces lineellus, Sitona lygivorus, Leiophron lineolaris, Lygus Lygus – family Miridae lineolata, Rhyssa Lygus spp. (lygus bugs) 16, 221–224 Linum – family Linaceae Lygus borealis (Kelton) 221, 372 Linum usitatissimum L. 164, 273, 371, 387, 392 Lygus elisus (Van Duzee) 221 Liriomyza – family Agromyzidae Lygus hesperus Knight 221 Liriomyza huidobrensis (Blanchard) 100 Lygus keltoni Schwartz 221 Liriomyza trifolii (Burgess) 100 Lygus lineolaris (Palisot) 101, 221–224 lissogaster, Bracon Lygus shulli Kelton 221 Lissonota – family Ichneumonidae Lymantria – family Lymantriidae Lissonota sp. 159 Lymantria dispar (L.) 476 Lissonota versicolor Holmgren 158 Lymantriidae – order Lepidoptera listronoti, Anaphes Lyrcus – family Pteromalidae listronoti, Bradynema Lyrcus incertus (Ashmead) 121 Listronotus – family Curculionidae Lyrcus maculatus (Gahan) 121 Listronotus bonariensis Kuschel 216–217 Lyrcus perdubius (Girault) 121 Listronotus maculicollis Kirby 217 Lysobacter – family Xanthomonadaceae Listronotus oregonensis (LeConte) 214–218 Lysobacter enzymogenes Christensen &Cook 416 Listronotus sparsus Say 217 Lythrum – family Lythraceae Lithospermum – family Boraginaceae Lythrum alatum Pursh 363 Lithospermum ruderale Douglas ex Lehm. 312 Lythrum salicaria L. 363–365, 482 lituratus, Centistes Lobesia – family Tortricidae Lobesia botrana (Denis & Schiffermüller) 160– MacoNPV-A (Mamestra confi gurata 161 nucleopolyhedrovirus-A) 230–231 Lobularia – family Brassicaceae MacoNPV-B (Mamestra confi gurata Lobularia maritima (L.) Desv. 259 nucleopolyhedrovirus-B) 230, 231 Lolium – family Poaceae Macrocentrus – family Braconidae Lolium multifl orum Lamark 217, 373 Macrocentrus incompletus Muesebeck 167 Lolium perenne L. 384 Macrocentrus linearis (Nees) 131, 132 Lonchaea – family Lonchaeidae Macroglenes – family Pteromalidae Lonchaea corticis (Taylor) 145 Macroglenes chalybeus Haliday 136 Lonchaeidae – order Diptera Macroglenes eximius (Haliday) 136 longicauda, Atanycolus Macroglenes penetrans (Kirby) 15, 274, 275 longicauda, Gelis macrophyllum,Tanacetum Longitarsus – family Chrysomelidae Macrosiphoniella – family Aphididae Longitarsus pellucidus Foudras 308 Macrosiphoniella leucanthemi Ferrari 339 Longitarsus quadriguttatus Pontoppidan 310, Macrosiphoniella sanborni (Gillette) 98, 339 311 Macrosiphoniella tanacetaria (Kaltenbach) 379 Longitarsus rubiginosus Foudras 308 Macrosiphum – family Aphididae 504 Index

Macrosiphum euphorbiae (Thomas) 98 Mecinus spp. 344, 345, 349, 350, 356, 358, macrostoma, Phoma 359–360 maculans, Leptosphaeria Mecinus heydeni Wencker 355, 360 maculata lengi, Coleomegilla Mecinus janthiniformis Toševski & Caldara 345, maculator, Itoplectis 347, 348, 350, 356, 360 maculatus, Callosobruchus Mecinus janthinus Germar 25–26, 343, 344–347, maculatus, Lyrcus 348–349, 350, 356, 357–358, 359, 360 maculicollis, Listronotus mediator, Microplitis maculipes, Pnigalio medic (Medicago spp.) 278, 387 maculiventris, Podisus Medicago – family Fabaceae maculosus, Hadrobunus Medicago spp. 278, 387 madidus, Pterostichus Medicago sativa L. 195, 221, 222, 223, 224, 277, magnus, Cryptococcus 278, 280, 333, 396, 455 Mahonia – family Berberidaceae Mediterranean fruit fl y (Ceratitis capitata) 188 Mahonia aquifolium (Pursh) Nutt. 153 Megadrilacea (earthworms) 385 maize, corn (Zea mays) 46, 74, 195, 297, 371, Megarhyssa – family Ichneumonidae 402, 412–415, 442, 455 Megarhyssa spp. 265 major, Dendrocopos Megarhyssa emarginatoria (Thunberg) 266 major, Plantago Megarhyssa nortoni (Cresson) 265 malaheb, Prunus Megarhyssa nortoni nortoni (Cresson) 266 Malaheb cherry (Prunus mahaleb) 153 Megarhyssa nortoni quebecensis (Provancher) malherbae, Aceria 266 mali, Zetzellia Megastigmus – family Torymidae malivorella, Coleophora Megastigmus stigmatizans Fabricius 29 Malus – family Rosaceae Megischus – family Stephanidae Malus spp. 156, 192, 198–201, 238–240, 241, Megischus sp. 266 244 Meigenia – family Tachinidae Malus domestica Borkhausen 130, 139–140, Meigenia simplex Tschorsnig and Herting 210, 244–246, 285–288, 408–409, 480 211 Malus sylvestris Mill. 285 Meigenia uncinata Mesnil 210, 211 Malva – family Malvaceae Melaleuca – family Myrtaceae Malva pusilla Sm. 367–369 Melaleuca quinquenervia (Cav.) S.T.Blake 24 Malva rotundifolia L. see Malva pusilla Sm. melaleucae, Boreioglycaspis Mamestra – family Noctuidae Melanagromyza – family Agromyzidae Mamestra brassicae L. 230 Melanagromyza albocilia Hendel 308 Mamestra confi gurata (Walker) 228–231 melanarius, Pterostichus Mamestra confi gurata nucleopolyhedrovirus – Melanerpes – family Picidae family Baculoviridae 228–229 Melanerpes carolinus (L.) 63 Mamestra confi gurata nucleopolyhedrovirus-A Melanobaris – family Curculionidae 230–231 Melanobaris sp. near semistriata (Boheman) 334 Mamestra confi gurata nucleopolyhedrovirus-B melanogaster, Drosophila 230, 231 Melanoplus – family Acrididae man (Homo sapiens) 182, 192, 296, 378 Melanoplus sanguinipes (Fabricius) 16 mancus, Agriotes melanopus, Microctonus mango mealybug (Rastrococcus invadens) 31 melanopus, Oulema manihoti, Phenacoccus Melanotrichus – family Miridae maples (Acer spp.) 83, 87, 88 Melanotrichus coagulatus (Uhler) 223 marcescen s, Serratia Melanotus – family Elateridae marginiventris, Cotesia Melanotus communis (Gyllenhal) 73 maritima, Lobularia Melanotus similis (Kirby) 73 marmoratus, Nanophyes melianae, Microplitis martagon, Lilium Meliboeus – family Buprestidae Mastrus – family Ichneumonidae Meliboeus graminoides Abeille 381 Mastrus sp. 159 Melilotus – family Fabaceae Mastrus pilifrons (Provancher) 140 Melilotus albus Medik. 403 Mastrus ridibundus (Gravenhorst) 140 Melilotus offi cinalis (L.) Lamarck 277, 278, 280 Matricaria perforata Mérat see mellea, Zele Tripleurospermum inodorum (L.) Sch. mellifera, Apis Bip. mellillus, Aeolus max, Glycine mellipes, Ontsira maximum, Leucanthemum melon/cotton aphid (Aphis gossypii) 98 mays, Zea melongena, Solanum Mecinus – family Curculionidae Melyridae – order Coleoptera 372 Index 505

memnonius, Hemicrepidius Microplitis feltiae Muesebeck 168 menhaden fi sh (Brevoortia spp.) 442, 450, 458, Microplitis kewleyi Muesebeck 168 468 Microplitis mediator Haliday 228, 229 menziesii, Pseudotsuga Microplitis melianae Viereck 168 merdigera, Lilioceris Microplitis plutellae (Muesebeck) 258–259, 260 Merisus febriculosus Girault see Homoporus Microplontus – family Curculionidae febriculosus (Girault) Microplontus campestris (Gyllenhal) 339 merkli, Ceutorhynchus Microplontus edentulus (Schultze) 393, Mermithidae – order Mermithida 75, 250 396–397, 399 Mesochorus – family Ichneumonidae Microplontus millefolii (Schultze) 380, 381 Mesochorus sp. 260 Microsoma – family Tachinidae Mesochorus bilineatus Thomson 260 Microsoma exigua (Meigen) 279, 280 Mesopolobus – family Pteromalidae Microsphaeropsis – family Montagnulaceae Mesopolobus spp. 121, 393–394 Microsphaeropsis sp. 415 Mesopolobus bruchophagi Gahan 121 Milichiidae – order Diptera 86 Mesopolobus gemellus Bauer & Muller 121 militaris, Protapanteles Mesopolobus moryoides Gibson 121, 123 millefolii, Microplontus Mesopolobus morys (Walker) 122, 123–124, 125 millefolium, Achillea messoria, Euxoa millefolium,Tanacetum Metapelma – family Eupelmidae minima, Cryptantha Metapelma spectabile Westwood 66 minor, Ophiostoma Metarhizium – family Clavicipitaceae minor, Sclerotinia Metarhizium spp. 67, 75, 78, 80 minutus, Larinus Metarhizium anisopliae (Metschnikoff) Sorokin Miridae – order Hemiptera 109, 238 67, 74, 76–78, 79, 87, 104, 110, 144–145, Mogulones – family Curculionidae 215 Mogulones crucifer Pallas 310–313, 479 Metarhizium anisopliae (Metschnikoff) Sorokin Mogulones cruciger Herbst see Mogulones sensu lato 74, 80 crucifer Pallas Metarhizium brunneum Petch 67, 74–75, 78–79, mongolica,Tilia 287–288 Monilinia – family Sclerotinaceae Metaseiulus occidentalis (Nesbitt) see Monilinia vaccinii-corymbosi (Reade) Honey Galendromus occidentalis (Nesbitt) 424–427 Meteorus – family Braconidae mono, Acer Meteorus dimidiatus (Cresson) 167 Monographella cucumerina (Lindf.) Arx Meteorus pendulus (Müller) 168 incertae sedis 330 Meteorus rubens (Nees) 168 montana, Ibalia micrantha, Hackelia montdorensis, Amblyseius Microbracon – family Braconidae morifolium, Chrysanthemum Microbracon sp. 216 moryoides, Mesopolobus Microchelonus – family Braconidae morys, Mesopolobus Microchelonus blackburni (Cameron) 58 moschata, Cucurbita Microctonus – family Braconidae mosellana, Sitodiplosis Microctonus spp. 251–252 mountain ash (Sorbus spp.) 83, 156, 285 Microctonus aethiopoides (Loan) see Perilitus Muehlenbeckia – family Polygonaceae aethiops Nees Muehlenbeckia axillaris (Hook. f.) Endl. 324 Microctonus aethiops (Nees) see Perilitus multifl orum, Lolium aethiops Nees mummy berry disease (Monilinia vaccinii- Microctonus hyperodae Loan 216–218 corymbosi) 424–427 Microctonus melanopus (Ruthe) 120–121, 122 mundus, Eretmocerus Microctonus punctulatae Loan &Wylie 252 mung bean (Vigna radiata) 396, 446 Microctonus pusillae Muesebeck 252 muricatus, Allurus Microctonus secalis (Haliday) 279 Musca – family Muscidae Microctonus sitonae Mason 278, 279 Musca autumnalis DeGeer 185 Microctonus vittatae Mueseback (Perilitus Musca domestica L. 182–188 brevipetiolatus) 250, 252, 253 muscae, Entomophthora Microgaster – family Braconidae Muscidae – order Diptera 49 Microgaster globata (L.) 58 Muscidifurax – family Pteromalidae Microgaster hospes Marshall 58 Muscidifurax spp. 189 microgastri, Dibrachys Muscidifurax raptor Girault & Saunders Micromus – family Hemerobiidae 183–185, 188 Micromus variegatus Fabricius 104 Muscidifurax raptorellus Kogan & Legner microphyllum, Tanacetum 183–184 Microplitis – family Braconidae Muscidifurax zaraptor Kogan & Legner 183–185 506 Index

Muscina – family Muscidae Netelia sp. 170 Muscina stabulans (Fallén) 165 ni, Trichoplusia Muscodor – family Xylariaceae niger, Pristaulacus Muscodor spp. 439 niger neoniger, Lasius Muscodor albus Worapong et al. 441, 448 nigra, Fraxinus mustard, Indian mustard (Brassica juncea) 142, nigra, Populus 249, 257, 260, 455 nigra, Prunus mutabilis, Campoplex nigra, Sambucus mutatum, Bembidion nigra, Spalangia Mycosphaerella – family Mycosphaerellaceae nigricollis, Lathrolestes Mycosphaerella polygoni-cuspidati Hara 323, nigricornis, Phytoecia 326 nigricoxis, Endromopoda myles, Synopeas nigriscutis, Aphthona Mymaridae – order Hymenoptera nigriventris, Atanycolus myopaeformis, Synanthedon nigroaenea, Spalangia Myoviridae 409–410 nigrocincta, Aptesis Myxexoristops – family Tachinidae nigropyga, Atanycolus Myxexoristops hertingi Mesnil 54, 55 nigrum, Epicoccum Myzus – family Aphididae nigrum, Vincetoxicum Myzus persicae (Sulzer) 98, 99, 105 Nipponanthemum – family Asteraceae Nipponanthemum nipponicum (Franch. ex Maxim.) Kitam 338 Nabicula – family Nabidae nipponicum, Nipponanthemum Nabicula americolimbata (Carayon) 250 Nitidulidae – order Coleoptera 477 Nabidae – order Hemiptera 109 nitidum, Bembidion Nabis – family Nabidae nobile, Chamaemelum Nabis alternatus Parshley 250 noctilio, Sirex nana, Fenusella Noctuidae – order Lepidoptera 59, 477 Nanophyes – family Curculionidae nodaensis, Cryptococcus Nanophyes marmoratus Goeze 363, 365 nodding onion (Allium cernuum) 56 Napomyza – family Agromyzidae nonoccluded viruses – family Baculoviridae Napomyza sp. near lateralis (Fallén) 399 173 napus, Brassica noricus, Longitarsus Nasonia – family Pteromalidae northern black currant (Ribes hudsonianum var. Nasonia vitripennis (Walker) 183, 184, 185, 186 petiolare) 153 nasturtii, Contarinia nortoni, Megarhyssa nasutus, Amblytylus Nosema – family Nosematidae NeabNPV (Neodiprion abietis Nosema sp. 173, 204 nucleopolyhedrovirus) 55 novo-ulmi, Ophiostoma Necremnus – family Eulophidae nubilalis, Ostrinia Necremnus tidius (Walker) 121, 122, 124–125 Nucleopolyhedrovirus – family Baculoviridae nectarine (Prunus persica var. nucipersica) 153, Nucleopolyhedrovirus (nuclear polyhedrosis 463 virus) – family Baculoviridae 131, 171, Nedyus – family Curculionidae 173, 229, 292 Nedyus fl avicaudis Boheman 217 nuncius, Diphyus neem tree (Azadirachta indica) 209, 457, 468 neesii, Tephritis neglectus, Ceutorhynchus oak gall wasp (Cynips quercusfolii) 29 negundo, Acer oats (Avena sativa) 273, 278, 354, 373, 414 nemoratus, Heterathrus obliquebanded leafroller (Choristoneura nenuphar, Conotrachelus rosaceana) 130–133 Neodiprion – family Diprionidae oblonga, Cydonia 285 Neodiprion abietis (Harris) 55 obscurellum, Bembidion Neodiprion abietis nucleopolyhedrovirus obscurus, Agriotes (NeabNPV) 55 obscurus, Exetastes Neoseiulus – family Phytoseiidae obstrictus, Ceutorhynchus Neoseiulus californicus (McGregor) 104 obtusifolius, Rumex Neoseiulus cucumeris (Oudemans) 103 obtusus, Larinus Neoseiulus fallacis (Garman) 239, 240–241 occidentalis, Frankliniella neotestacea, Drosophila occidentalis, Galendromus Neotylenchidae – order Tylenchida occidentalis, Hebecephalus neta, Rhinusa occidentalis, Heterobasidion Netelia – family Ichneumonidae occidentalis, Philonthus Index 507

occidentis, Winthemia Oscheius (Rhabditis) sp. 67 ochrodactyla, Platyptilia Ostrinia – family Pyralidae ochrogaster, Euxoa Ostrinia latipennis Warren 323 ocypterata, Aphria Ostrinia nubilalis (Hübner) 38, 101 Odiellus – family Phalangiidae Ostrinia ovalipennis Ohno 323 Odiellus pictus (Wood) 173 Oulema – family Chrysomelidae Odontocolon – family Ichneumonidae Oulema melanopus (L.) 7, 17, 233–236 Odontocolon geniculatum (Kreichbaumer) 266 ovalipennis, Ostrinia offi cinale, Cynoglossum ovalis, Euseius offi cinale, Taraxacum ovata, Amara offi cinalis, Melilotus Ovis – family Bovidae ohridella, Camereria Ovis aries L. 333 oleracea, Brassica oxeye daisy (Leucanthemum vulgare) 337–340 oleraceus, Diospilus oxysporum, Fusarium ometes, Lasioseius Omphalapion – family Brentidae Omphalapion hookeri (Kirby) see Omphalapion Pachycrepoideus – family Pteromalidae hookerorum (Kirby) Pachycrepoideus vindemmiae (Rondani) Omphalapion hookerorum (Kirby) 393–395, 153–154, 185 396–397, 399 Paecilomyces – family Trichocomaceae Oncotylus – family Miridae Paecilomyces spp. 67 Oncotylus punctipes Reuter 381 Paecilomyces farinosus (Holmsk.) A.H.S. Br. & onion (Allium cepa) 56 G. Sm. (Isaria farinosa) 86 Onthophagus – family Scarabeidae Paenibacillus – family Paenibacillaceae Onthophagus taurus (Schreber) 187–188 Paenibacillus polymyxa (Prazmowski) Ash et al. Ontsira – family Braconidae 416 Ontsira mellipes (Ashmead) 88 pale swallow-wort, dog strangling vine Oobius – family Encyrtidae (Vincetoxicum rossicum) 402–403, 404, Oobius agrili Zhang & Huang 65, 67, 68 405 Oobius zahaikevitshii Trjpitzin 65 pallidus, Phytodromus opacum, Inostemma pallipes, Aphaereta Operophtera – family Geometridae pallipes, Peristenus Operophtera brumata (L.) 7 pallipes, Pnigalio Ophiostoma – family Ophiostomataceae palm scale (Palmarioccocus (Colobopyga) Ophiostoma minor (Hedgecock) H. & P. Sydow pritchardiae) 27 267 Palmarioccocus – family Halimococcidae Ophiostoma novo-ulmi Brasier 476 Palmarioccocus pritchardiae Stickney 27 Ophiostoma ulmi (Buisman) Nannf. 476 Pamphiliidae – order Hymenoptera Ophraella – family Chrysomelidae Panax – family Araliaceae Ophraella communa LeSage 298–299, 300 Panax quinquefolius L. 440 Ophraella slobodkini Futuyma 299–300 Pandemis – family Tortricidae opilio, Phalangium Pandemis limitata (Robinson) 130 Opogona – family Tineidae Panonychus – family Tetranychidae Opogona sacchari Bojer 476 Panonychus ulmi (Koch) 238–242, 479 opulenta, Hypena Pantoea – family Enterobacteriaceae Opuntia – family Cactaceae Pantoea agglomerans (Ewing and Fife) Gavini et Opuntia spp. 17 al. 48, 86, 409–410, 426 orange wheat blossom midge, wheat midge Pantoea vagans Brady et al. 409 (Sitodiplosis mosellana) 15, 272–275, Panzeria – family Tachinidae 480 Panzeria spp. 166 Oregon ash (Fraxinus latifolia) 63 paper bark tea tree (Melaleuca quinquenervia) Oregon grape (Mahonia aquifolium) 153 24 oregonensis, Listronotus parasitica, Cryphonectria Orius – family Anthocoridae parsley (Petroselinum crispum) 214 Orius spp. 103, 293 parsnip (Pastinaca sativa) 214, 454 ornamental cherries (Prunus serrulata) 156, 161, Parthenium – family Asteraceae 162 Parthenium hysterophorus L. (parthenium weed) ornigis, Pholetesor 297 Orthizema – family Ichneumonidae parthenium,Tanacetum Orthizema sp. 66 parviporum, Heterobasidion oryzae, Ca. Phytoplasma Passandridae – order Coleoptera osaces, Synopeas Pastinaca – family Apiaceae Oscheius – family Rhabditidae Pastinaca sativa L. 214, 454 508 Index

Patasson lameerei Debauche see Anaphes diana persica, Prunus Girault persicae, Myzus patientia, Rumex Persicaria – family Polygonaceae 323 patronus, Brevoortia persicum, Cyclamen patruelis, Amara persimilis, Phytoseiulus pea (Pisum sativum) 277, 278, 354, 374, 396, personatus, Latalus 439, 440 persuasoria persuasoria, Rhyssa pea leaf miner (Liriomyza huidobrensis) 100 petiolata, Alliaria pea leaf weevil (Sitona lineatus) 277–278, Petroselinum – family Apiaceae 279–281 Petroselinum crispum (Mill.) Fuss 214 peach (Prunus persica) 152, 156, 238, 463–464 petroselinum, Apium peach leaf curl (Taphrina deformans) 463–464 Phaenopria – family Diapriidae peach tree borer (Synanthedon exitiosa) 286 Phaenopria sp. 153 pear (Pyrus communis) 139, 156, 244, 285, 408 Phaeogenes – family Ichneumonidae pectinicornis, Pnigalio Phaeogenes impiger Wesmael 60 pectoralis, Limonius Phalacrotophora – family Phoridae pedias, Pholetesor Phalacrotophora berolinensis Schmitz. 195 Pediobius – family Eulophidae Phalacrotophora fasciata (Fallén) 195 Pediobius eubius (Walker) 114, 115 Phalangiidae – order Opiliones Pediobius saulius (Walker) 26 Phalangium – family Phalangiidae Pelargonium – family Geraniaceae Phalangium opilio (L.) 173 Pelargonium spp. 442 Phalaris – family Poaceae Peleteria – family Tachinidae Phalaris canariensis L. 273 Peleteria rubescens Robineau-Desvoidy 166 Phaseolus – family Fabaceae Peleteria texensis Curran 166 Phaseolus vulgaris L. 93 pellucidus, Longitarsus Phasgonophora – family Chalcididae pendulus, Meteorus Phasgonophora sulcata Westwood 66, 67 penetrans, Macroglenes Phenacoccus – family Pseudococcidae Peniophora gigantea (Fries) Massee see Phenacoccus manihoti Matile-Ferrero 7 Phlebiopsis gigantea (Fries) Jülich philadelphicum, Lilium pennsylvanica, Fraxinus Philonthus – family Staphylinidae pennsylvanicus, Gryllus Philonthus occidentalis Horn 172 pentagona, Pseudaulacaspis Phlaeothripidae – order Thysanoptera Pentatomidae – order Hemiptera 477 Phlebiopsis – family Phanerochaetaceae pepper weevil (Anthonomus eugenii) 101 Phlebiopsis gigantea (Fries) Jülich 421–422 peppers, bell, sweet (Capsicum annuum) 99, Phlebotomus – family Psychodidae 100, 101, 108, 109, 111, 291, 387, 439, Phlebotomus argentipes Annandale & Brunette 440, 441, 454, 466–470 48 perdubius, Lyrcus Phleum – family Poaceae perenne, Lolium Phleum pratense L. 338 perennial rye grass (Lolium perenne) 384 phoenicis, Brevipalpus perfectus, Trichomalus Pholetesor – family Braconidae perforans, Xanthomonas Pholetesor ornigis (Weed) 245 perforatum, Hypericum Pholetesor pedias (Nixon) 245 perforatum, Tripleurospermum Phoma sp. incertae sedis 299 Perilitus – family Braconidae Phoma exigua Desm. 384 Perilitus aethiops Nees 278, 279, 280, 281 Phoma herbarum Westend. 384 Perilitus brevipetiolatus Thomson 250 Phoma macrostoma var. macrostoma Mont. Perilitus cerealium Haliday see Microctonus 384, 387–388 secalis (Haliday) Phoma taraxaci Hofsten 384 Perilitus rutilus (Nees) 278, 279, 280 Phomopsis – family Pleosporaceae Periscepsia – family Tachinidae Phomopsis vaccinii Shear, N.E. Stevens & H.F. Periscepsia cinerosa (Coquillett) 166 Bain 425 Periscepsia helymus (Walker) 166 Phoridae – order Diptera Periscepsia laevigata (Wulp) 166 Phratora – family Chrysomelidae Peristenus – family Braconidae Phratora laticollis Suffrian 210 Peristenus spp. 222, 223, 224 Phygadeuon – family Ichneumonidae Peristenus digoneutis Loan 16, 222–225 Phygadeuon spp. 144, 146, 147 Peristenus pallipes (Curtis) 222 Phygadeuon fumator Gravenhörst 184, 185 Peristenus pseudopallipes (Loan) 222 Phygadeuon tini 159 Peristenus relictus (Ruthe) 222–223 Phygadeuon trichops Thompson 146 Peristenus stygicus Loan see Peristenus relictus Phyllobaenus – family Cleridae (Ruthe) Phyllobaenus dubius (Wolcott) 115 Index 509

Phyllonorycter – family Gracillariidae pistol case bearer (Coleophora malivorella) 7 Phyllonorycter spp. 245 Pisum – family Fabaceae Phyllonorycter blancardella (Fabricius) 46, Pisum sativum L. 277, 278, 354, 374, 396, 439, 244–246 440 Phyllonorycter crataegella (Clemens) 244 placidum, Agonum Phylloptera – family Scarabeidae Plagiobothrys – family Boraginaceae Phylloptera horticola (Col.) 78 Plagiobothrys hirtus (Greene) I.M. Johnst. 313 Phyllotreta – family Chrysomelidae Plagiobothrys strictus (Greene) I.M. Johnst. 313 Phyllotreta chrysocephala (L.) 250 planipennis, Agrilus Phyllotreta cruciferae (Goeze) 248–253 planipennisi, Tetrastichus Phyllotreta striolata (Fabricius) 248–253 Planococcus – family Pseudococcidae Phyllotreta undulata Kutsch. 250 Planococcus citri (Risso) 101 Phyllotreta vittata Chen see Phyllotreta striolata Plantago – family Plantaginaceae (Fabricius) Plantago spp. (plantains) 164 phyllotreta, Howardula Plantago lanceolata L. 214 Phytodromus – family Tarsonemidae Plantago major L. 214, 386 Phytodromus pallidus (Banks) 100–101 plantarum, Lactobacillus Phytoecia – family Cerambycidae Plasmodiophora – family Plasmodiophoraceae Phytoecia nigricornis (Fabricius) 380 Plasmodiophora brassicae Woronin 429–434 Phytophthora – family Peronosporaceae Plasmodium – family Plasmodiidae Phytophthora spp. 442 Plasmodium spp. 48 Phytophthora capsici Leonian 439, 441 Platanus – family Platanaceae 83 Phytophthora ramorum Werres et al. 476 Platygaster – family Platygastridae Phytoseiidae – order Megostigmata 238 Platygaster sp. 136, 275 Phytoseiulus – family Phytoseiidae Platygaster tuberosula Kieffer 274–275 Phytoseiulus persimilis Athias-Henriot 8 Platygastridae – order Hymenoptera Picea – family Pinaceae Platyptilia – family Pterophoridae Picea spp. 421 Platyptilia ochrodactyla (Denis & Schiffermüller) piceae, Adelges 381 piceus, Rhoptrocentrus Plectosporium tabacinum (J.F.H. Beyma) Palm et Picidae – order Piciformes 267 al. see Monographella cucumerina Picoides – family Picidae (Lindf.) Arx Picoides pubescens (L.) 63 pleurostigma, Ceutorhynchus Picoides villosus (L.) 63 Pleutropis utahensis Crawford see Pediobius pictus, Odiellus eubius (Walker) Pierce’s disease (Xylella fastidiosa) 48 plum (Prunus domestica, P. nigra) 153, 156, 285 pilifrons, Mastrus plum curculio (Conotrachelus nenuphar) 199 pilosa, Rhinusa Plutella – family Plutellidae Pimpla – family Ichneumonidae Plutella xylostella (L.) 60, 256–260, 292 Pimpla contemplator (Müller) 159 plutellae, Microplitis Pimpla detrita Holmgren see Endromopoda Plutellidae – order Lepidoptera detrita Holmgren pneumonia, Klebsiella Pimpla hesperus (Townes) 157 Pnigalio – family Eulophidae Pimpla spuria Gravenhorst 159 Pnigalio epilobii Bouþek 245 Pimpla turionellae (L.) 159 Pnigalio maculipes (Crawford) 245 Pimpla varians (Townes) 287 Pnigalio pallipes (Provancher) 245 pine false webworm (Acantholyda Pnigalio pectinicornis (L.) 57 erythrocephala) 54–55, 476 Pnigalio soemius (Walker) 57 pine shoot beetle (Tomicus piniperda) 476 Poa – family Poaceae pini, Eupelmus Poa pratensis L. 384 piniperda, Tomicus Podapolipidae – order Trombidiformes Pinus – family Pinaceae Podisus – family Pentatomidae Pinus spp. 263–264, 420, 476 Podisus maculiventris (Say) 250, 293 Pinus banksiana Lamb. 264, 422 Podoviridae 409–410 Pinus densifl ora Sieb. & Zucc. 324 Poecilanthrax – family Bombyliidae Pinus resinosa Aiton 54–55, 264, 421, 422 Poecilanthrax halcyon (Say) 165 Pinus strobus L. 54, 264, 476 Poecilanthrax willistoni (Coquillet) 165 Pinus sylvestris L. 264 Poecilus – family Carabidae pipixcan, Leucophaeus Poecilus cupreus L. 122 Pirene eximia Haliday see Macroglenes eximius poinsettia (Euphorbia pulcherrima) 99, 102 (Haliday) polychrosidis, Apanteles Pissodes – family Curculionidae polygoni, Gastrophysa Pissodes strobi Peck 145 polygoni-cuspidati, Mycosphaerella 510 Index

Polygonum – family Polygonaceae Pseudomonas spp. 173, 456 Polygonum spp. 323 Pseudomonas alcaligenes Monias 86 Polygonum aviculare L. 386 Pseudomonas fl uorescens (Flügge) Migula 373, polymyxa, Paenibacillus 374, 409, 426, 456, 469, 471 Polyphagotarsonemus – family Tarsonemidae Pseudomonas putida Trevisan 86, 440, 469 Polyphagotarsonemus latus (Banks) 100, 101 Pseudomonas stutzeri (Lehmann & Neumann) pomi, Aphis Sijderius 86 pomonella, Cydia Pseudomonas syringae Van Hall 86, 425, 469 populi, Chrysomela pseudopallipes, Peristenus Populus – family Salicaceae Pseudorhyssa – family Ichneumonidae Populus spp. 83, 87 Pseudorhyssa rufi coxis (Kriechbaumer) 266 Populus canadensis Moench 83 pseudosieboldianum, Acer Populus deltoides W. Bartram ex Marshall 83 Pseudothrips – family Phlaeothripidae Populus nigra L. 83 Pseudothrips spp. 25 porrum, Allium Pseudotsuga – family Pinaceae postica, Hypera Pseudotsuga menziesii (Mirb.) Franco 476 potato aphid (Macrosiphum euphorbiae) 98 Pseudozyma – family Ustilaginaceae potato (Solanum tuberosum) 72, 74, 75, 79, 93, Pseudozyma fl occulosa (Traquair, Shaw & Jarvis) 107–108, 110, 447, 448, 453–459 Boekhout & Traquair 427 potato scab (Streptomyces scabies) 453–459 Psychodidae – order Diptera prairie onion (Allium stellatum) 56 Psylla itadori Shinji see Aphalara itadori Praleurocerus – family Encyrtidae (Shinji) Praleurocerus sp. 245 psyllaurous, Ca. Liberibacter pratense, Phleum Psyllidae – order Hemiptera pratense, Trifolium Psylliodes – family Chrysomelidae pratensis, Poa Psylliodes punctulata Melsheimer 252 Pristaulacus – family Aulacidae Psylliodes wrasei Leonardi & Arnold 334 Pristaulacus niger (Shuckard) 266 Pteromalidae – order Hymenoptera 47, 183, pritchardiae, Colobopyga 245 pritchardiae, Palmarioccocus Pteromalus – family Pteromalidae Proctolaelaps – family Ascidae Pteromalus spp. 121, 124 Proctolaelaps cossi Dugés 86 Pteromalus semotus Walker 259 Profenusa – family Tenthredinidae pterophori, Scambus Profenusa thomsoni (Konow) 175–180 Pterophoridae – order Lepidoptera profunda, Fraxinus Pterostichus – family Carabidae prolixus, Rhodnius Pterostichus adstrictus Eschscholtz 172 Propylea – family Coccinellidae Pterostichus lucublandus Say 172 Propylea quatuordecimpunctata L. 94 Pterostichus madidus (Fabricius) 122 prostrate knotweed (Polygonum aviculare) 386 Pterostichus melanarius (Illiger) 94, 95, 122, Protapanteles – family Braconidae 216, 278 Protapanteles alticola Ashmead 168 pubescens, Dacnusa Protapanteles militaris (Walsh) 168 pubescens, Picoides pruinina, Ctenicera Puccinia – family Pucciniaceae Prunus – family Rosaceae Puccinia sp. 323 Prunus spp. 83 Puccinia tanaceti DC 379 Prunus armeniaca L. 156, 285 pulchellus, Diadromus Prunus avium (L.) L. 130, 152, 156, 162, 285 pulcher, Lemophagus Prunus cerasus L. 130, 152 pulcherrima, Euphorbia Prunus domestica L. 153, 285 pulicarius, Brachypterolus Prunus dulcis (Mill.) D.A. Webb 156 pullulans, Aureobasidium Prunus emarginata (Douglas) Eaton 162 pumila, Fenusa Prunus laurocerasus L. 156 pumilla, Setaria Prunus mahaleb L. 153 pumilus, Bacillus Prunus nigra Aiton 156 pumpkin (Cucurbita spp.) 93, 192, 387 Prunus persica (L.) Batsch 152, 156, 238, pumpkin ash (Fraxinus profunda) 63 463–464 punctiger, Glocianus Prunus persica var. nucipersica Dippel 153, 463 punctipes, Oncotylus Prunus serrulata Lindl. 156, 161, 162 punctulata, Psylliodes Pseudaulacaspis – family Diaspididae punctulatae, Microctonus Pseudaulacaspis pentagona (Targioni) 27 pura, Xenocrepis Pseudococcidae – order Hemiptera 477 purple loosestrife (Lythrum salicaria) 363–365, pseudograminearum, Fusarium 482 Pseudomonas – family Pseudomonadaceae Purpureocillium – family Ophiocordycipitaceae Index 511

Purpureocillium lilacinum (Thom) Luangsa-ard raphanistrum, Raphanus et al. 67 Raphanus – family Brassicaceae pusilla, Galerucella Raphanus raphanistrum L. 124 pusilla, Malva Raphanus sativus L. 454 pusillae, Microctonus Raphidiidae – order Neuroptera Pustula – family Albuginaceae raptor, Muscidifurax Pustula tragopogonis (Pers.) Thines 299 raptorellus, Muscidifurax putida, Pseudomonas raspberry (Rubus idaeus) 130, 152, 192 pygmaeus, Cephus Rastrococcus – family Pseudococcidae Pygostolus – family Braconidae Rastrococcus invadens Williams 31 Pygostolus falcatus (Nees) 278, 279, 280, 281 red-bellied woodpecker (Melanerpes carolinus) Pyracantha – family Rosaceae 63 Pyracantha spp. 156 red oak (Quercus rubra) 66 Pyralidae – order Lepidoptera 477 red pine (Pinus resinosa) 54–55, 264, 421, 422 pyri, Typhlodromus redbacked cutworm (Euxoa ochrogaster) Pyricularia – family Magnaporthaceae 164–173 Pyricularia grisea Sarccardo 372 redbellied clerid (Enoclerus sphegeus) 287 Pyricularia setariae Nisikado 373, 374–375 Reduviidae – order Hemiptera Pyrus – family Rosaceae relictus, Peristenus Pyrus communis L. 130, 139, 156, 244, 285, repens, Elymus 408 repens, Trifolium Pythium – family Pythiaceae resinosa, Pinus Pythium aphanidermatum (Edson) Fitzpatrick Rhabditidae – order Rhabiditida 438, 440 Rhabditis – family Rhabditidae Pythium debaryanum Hesse 372 Rhabditis (Oscheius) sp. 67 Pythium graminicola Subramaniam 372 Rhamnus – family Rhamnaceae Pythium ultimum Trow 431, 438–443 Rhamnus spp. 93–94 Rhinusa – family Curculionidae Rhinusa antirrhini (Paykull) 344, 347, 348, 350, quackgrass (Elymus repens) 467 356, 359 quadrangulata, Fraxinus Rhinusa brondelii (Brisout) 343, 350 quadricingulata, Itoplectis Rhinusa eversmanni (Rosenschöld) 355 quadridens, Ceutorhynchus Rhinusa hispida (Brullé) see Rhinusa brondelii quadrigemina, Chrysolina (Brisout) quadriguttatus, Longitarsus Rhinusa linariae (Panzer) 344, 358, 359, 360 quadrimaculatum, Bembidion Rhinusa neta (Germar) 348, 356 quadripustulata, Winthemia Rhinusa pilosa (Gyllenhal) 355, 360 quatuordecimpunctata, Crioceris Rhizobium – family Rhizobiaceae quatuordecimpunctata, Propylea Rhizobium spp. 277, 278 quenseli, Amara Rhizoctonia – family Ceratobasidiaceae Quercus – family Fagaceae Rhizoctonia spp. 449 Quercus rubra L. 66 Rhizoctonia solani Kühn 442, 446–450 quercusfolii, Cynips Rhodnius – family Reduviidae quince (Cydonia oblonga) 156, 285 Rhodnius prolixus Stål 48 quinquefolius, Panax Rhodotorula incertae sedis 425 quinquenervia, Melaleuca Rhodotorula graminis DiMenna 426 Quiscalus – family Icteridae Rhopalomyia – family Cecidomyiidae Quiscalus quiscula (L.) 171, 173 Rhopalomyia tanaceticola (Karsch) 381 quiscula, Quiscalus Rhopalomyia tripleurospermi Skuhravá & Hinz 393, 394, 395, 396–397, 399 Rhoptrocentrus – family Braconidae radiata, Vigna Rhoptrocentrus piceus Marshall 88 radicum, Delia Rhyssa – family Ichneumonidae radish (Raphanus sativus) 142, 450, 454 Rhyssa spp. 265 ragweed, common (Ambrosia artemisiifolia) Rhyssa alaskensis Ashmead 266 296–300, 386, 387 Rhyssa amoena (Gravenhorst) 266 Rahnella – family Enterobacteraceae Rhyssa crevieri (Provancher) 266 Rahnella aquatilis Izard et al. 78 Rhyssa hoferi Rohwer 266 ramorum, Phytophthora Rhyssa howdenorum Townes 266 rapa, Brassica Rhyssa lineolata (Kirby) 265, 266 rapae, Trybliographa Rhyssa persuasoria persuasoria (L.) 265, 266 rapeseed (Brassica napus) 329–330, 371, 446, Ribes – family Grossulariaceae 448, 455 see also canola Ribes aureum Pursh 153 512 Index

Ribes hudsonianum var. petiolare (Douglas) Saintpaulia – family Gesneriaceae Jancz. 153 Saintpaulia spp. 100 ribicola, Cronartium salicaria, Lythrum Rickettsia – family Rickettsiaceae salicis, Leucoma Rickettsia spp. 43, 44, 45 Salix – family Salicaceae ridibundus, Mastrus Salix spp. 83, 87 roberti, Ceutorhynchus Sambucus – family Adoxaceae Rogas – family Braconidae Sambucus spp. 153 Rogas sp. 168 Sambucus cerulea Raf. var. cerulea 153 root rot, blight, damping-off, leaf spot, stem Sambucus nigra L. 153 canker and tuber scurf (Rhizoctonia sanborni, Macrosiphoniella solani) 446–450 sand fl y (Phlebotomus argentipes) 48 Rosa – family Rosaceae sanguinipes, Melanoplus Rosa spp. 100 sapiens, Homo rosaceana, Choristoneura Sarcophaga – family Sarcophagidae rose (Rosa spp.) 100 Sarcophaga cimbicis (Town) 165 rosea, Clonostachys sarcophagae, Trichomalopsis roseum, Gliocladium Sarcophagidae – order Diptera rossicum, Vincetoxicum satin moth (Leucoma salicis) 7 rostochiensis, Globodera sativa, Avena rostratum, Exserohilum sativa, Lactuca rostratus, Hebecephalus sativa, Medicago rouhollahi, Cecidophyes sativa, Pastinaca round-leaved mallow (Malva pusilla, M sativum, Allium rotundifolia) 367–369 sativum, Pisum rubens, Meteorus sativus, Cucumis rubescens, Peleteria sativus, Raphanus rubiginosus, Longitarsus satyrata dodata, Eupithecia rubra, Festuca saulius, Pediobius rubra, Quercus scab see apple scab; potato scab rubrum, Acer scabies, Streptomyces Rubus – family Rosaceae scales – order Hemiptera (superfamily Rubus fructicosus L. 152 Coccoidea) 193 Rubus idaeus L. 130, 152, 192 Scambus – family Ichneumonidae ruderale, Lithospermum Scambus hispae (Harris) 59 rufi collis, Ibalia Scambus pterophori (Ashmead) 59 rufi coxis, Pseudorhyssa Scarabeidae – order Coleoptera 187–188, 189 rufi labris, Chrysoperla Scelionidae – order Hymenoptera 245 rufi pes, Arenetra scentless camomile (Tripleurospermum rufi pes, Ibalia inodorum) 391–393, 396–399 rufi pes, Urolepis Schinus – family Anacardiaceae rufopicta, Winthemia Schinus terebinthifolius Raddi 25 rufus, Catogenus schlechtendali, Aculus Rumex – family Polygonaceae Schlettererius – family Stephanidae Rumex spp. 323 Schlettererius cinctipes (Cresson) 266 Rumex acetosa L. 214 Sciaridae – order Diptera Rumex crispus L. 214 scimitus, Stratiolaelaps Rumex obtusifolius L. 214 Scirtothrips – family Thripidae Rumex patientia L. 214 Scirtothrips dorsalis Hood 99 rupicola, Bembidion Scleroderma – family Bethylidae rutabaga (Brassica napus var. napobrassica) Scleroderma guani (Xiao & Wu) 86, 87 142, 143, 144 sclerophyllum, Tanacetum rutilus, Perilitus Sclerosomatidae – order Opiliones rye (Secale cereale) 272, 414, 441, 448 Sclerospora – family Peronosporaceae Sclerospora graminicola Saccardo Schroeter 372 sacchari, Opogona Sclerotinia – family Sclerotiniaceae Saccharopolyspora – family Sclerotinia minor Jagger 384–387, 388 Pseudonocardiaceae Sclerotinia sclerotiorum (Lib.) de Bary 384 Saccharopolyspora spinosa Mertz & Yao 132 sclerotiorum, Sclerotinia saccharum, Acer Scolioneura – family Tenthredinidae sachalinensis, Fallopia Scolioneura vicina Konow 180 saffl ower (Carthamus tinctorius) 440 scoparia, Kochia Index 513

scoparius, Cytisus Sinningia speciosa (G. Lodd.) Hiern 100 Scotch broom (Cytisus scoparius) 476 Siphoviridae 409 Scots pine (Pinus sylvestris) 264 Sirex – family Siricidae scrofa domestica, Sus Sirex noctilio Fabricius 24–25, 263–268, 476 Secale – family Poaceae Siricidae – order Hymenoptera Secale cereale L. 272, 414, 441, 448 siricidicola, Deladenus secalis, Microctonus Sitodiplosis – family Cecidomyiidae seedling damping-off, root rot, crown rot Sitodiplosis mosellana (Géhin) 15, 272–275, 480 (Pythium spp.) 438–443 Sitona – family Curculionidae segnis, Aptesis Sitona spp. Germar 277–281 Selatosomus – family Elateridae Sitona cylindricollis (Fahraeus) 277, 278, 279, Selatosomus aeripennis aeripennis (Kirby) 73 280, 281 Selatosomus aeripennis destructor (Brown) 73 Sitona discoideus 279, 280 semistriata, Melanobaris Sitona fl avescens (Marshall) 277, 278, 279 semotus, Pteromalus Sitona hispidulus (Fabricius) 277, 278, 279 Senecio – family Asteraceae Sitona humeralis Stephens see Sitona Senecio vulgaris L. 387 discoideus septempunctata, Coccinella Sitona lepidus Gyllenhal 216 Septoria – family Mycosphaerellaceae Sitona lineatus (L.) 16, 277–278, 279–281 Septoria epambrosiae D.F. Farr, Sydowia 300 Sitona lineellus (Bonsdorff) 277, 278, 279, 280 sericeicornis, Sympiensis Sitona scissifrons Say see Sitona lineellus serratella, Coleophora (Bonsdorff) serratella, Eteobalea sitonae, Microctonus Serratia – family Enterobacteriaceae Sium – family Apiaceae Serratia marcescens Bizio 86 Sium suave Walter 214 serratus, Carabus slobodkini, Ophraella serrulata, Prunus snap bean (Phaseolus vulgaris) 93 Sesiidae – order Lepidoptera soemius, Pnigalio Setaria – family Poaceae solani, Aulacorthum Setaria faberi Herrm. 370, 375 solani, Rhizoctonia Setaria geniculata P. Beauvois 370 Solanum – family Solanaceae Setaria glauca (Pennisetum glaucum (L.) R. Br.) Solanum lycopersicum L. 100, 101, 103, 375 107–111, 291, 387, 446, 448, 449, 454, Setaria italic (L.) P. Beauvois 371 466–471 Setaria pumilla (Poir.) Roem. & Schult. 370, 373 Solanum melongena L. 100, 454 Setaria verticillata (L.) P. Beauv. 370 Solanum tuberosum L. 72, 74, 75, 79, 93, Setaria viridis (L.) Beauvois 370–375 107–108, 110, 446, 447, 448, 453–459 setariae, Pyricularia solidaginis, Leiophron setifer, Tetrastichus Solidago – family Asteraceae 7-spotted ladybird (Coccinella septempunctata) Solidago canadensis L. 467 94, 132, 136, 195 sonorensis, Campoletis Shanghai pak choy (Brassica rapa subsp. soperi, Lathrolestes chinensis) 432, 439 sophia, Descurainia Shasta daisy (Leucanthemum × superbum) 338, Sorbus – family Rosaceae 339, 340 Sorbus spp. 83, 156 sheep (Ovis aries) 333 Sorbus americana Mars. 285 shepherd’s purse (Capsella bursa-pastoris) 124, sordidatus, Anaphes 257 Sorghum – family Poaceae shulli, Lygus Sorghum bicolor (L.) Moench (sorghum) 371 sibericum, Trichogramma Sorosporella uvella (Krass.) Giard incertae sedis similata, Amara 173 similis, Diprion sour cherry (Prunus cerasus) 130, 152 similis, Melanotus soybean (Glycine max) 93–94, 95–96, 193, 297, simillimus, Spathius 298, 371, 396, 447, 455 simplex, Atanycolus soybean aphid (Aphis glycines) 93–96, 193, 477 simplex, Cyclogastrella Spalangia – family Pteromalidae simplex, Meigenia Spalangia spp. 184, 185, 188 simplicipes, Apophua Spalangia cameroni Perkins 49, 183, 184, 185, simulans, Drosophila 187, 188 Sinapis – family Brassicaceae Spalangia drosophilae Ashmead 185 Sinapis alba L. 120, 142, 143, 249, 257, 258, 354 Spalangia endius Walker 183, 185 Sinapis arvensis L. 257, 387 Spalangia haematobiae Ashmead 185 Sinningia – family Gesneriaceae Spalangia nigra Latreille 185 514 Index

Spalangia nigroaenea Curtis 185 Stethorus spp. 238 Spalangia subpunctata Förster 185 Stictopisthus – family Ichneumonidae Sparganothis – family Tortricidae Stictopisthus bilineatus (Thomson) 245 Sparganothis sulfureana (Clemens) 339 Stictopisthus fl aviceps (Provancher) 245 sparsus, Listronotus Stigmaeidae – order Trombidiformes 238 Spathius – family Braconidae stigmatica, Cassida Spathius spp. 66 stigmatizans, Megastigmus Spathius agrili Yang et al. 64–65, 67, 68 stinging nettle (Urtica dioica) 109 Spathius fl oridanus (simillimus) Ashmead 66 Stobaera – family Delphacidae Spathius galinae Belokobylskij & Strazanac 65 Stobaera concinna (Stäl) 297 Spathius simillimus (fl oridanus) Ashmead 66 stoebe, Centaurea speciosa, Sinningia stolidum, Diplapion spectabile, Metapelma Stomoxys – family Muscidae sphaericus, Bacillus Stomoxys calcitrans (L.) 182–186 sphaerosperma, Entomophthora Stratiolaelaps – family Laelapidae Sphaerulariidae – order Tylenchida Stratiolaelaps scimitus (Wormersley) 104 sphegeus, Enoclerus strawberry (Fragaria x ananassa) 152, 222, 223 Sphingidae – order Lepidoptera strenuana, Epiblema spiders (order Araneae) 274 Streptococcus – family Streptococceae Spilichneumon – family Ichneumonidae Streptococcus faecalis Andrewes & Horder 173 Spilichneumon inconstans (Cresson) 170 Streptomyces – family Streptomycetaceae Spilichneumon superbus (Provancher) 170 Streptomyces spp. 448–449 spined soldier bug (Podisus maculiventris) 250 Streptomyces griseocarneus Benedict 449 spinosa, Botanophila Streptomyces griseoviridis Andersen et al. spinosa, Saccharopolyspora 426–427, 430, 441, 470 Spiroplasma – family Spiroplasmataceae Streptomyces kasugaensis (Okanishi, Ohta & Spiroplasma spp. 43, 44, 45, 46 Umezawa) 467 Sporobolomyces – family Sporidiobolaceae 425 Streptomyces lydicus De Boer et al. 426–427, spotted knapweed (Centaurea stoebe subsp. 431, 441, 470, 471 micranthos) 302–305 Streptomyces scabies Lambert & Loria 453–459 spotted tentiform leafminer (Phyllonorycter striatella, Isophrictis blancardella) 46, 244–246 strictus, Plagiobothrys spotted wing drosophila (Drosophila suzukii) striolata, Phyllotreta 101, 152–154, 476, 477 striped fl ea beetle (Phyllotreta striolata) spruce (Picea spp.) 421 248–253 spuria, Pimpla strobi, Pissodes spurium, Galium strobus, Pinus sputator, Agriotes Strongwellsea – family Entomopthoraceae squarrosa, Lappula Strongwellsea castrans Batko & Weiser 144 squash, pumpkin (Cucurbita spp.) 93, 192, 387 Sturnidae – order Passeriformes St. John’s wort (Hypericum perforatum) 8, 368 Sturnus – family Sturnidae stable fl y (Stomoxys calcitrans) 182–186 Sturnus vulgaris L. 171, 173 stabulans, Muscina stutzeri, Pseudomonas Stachybotrys elegans (Pidopl.) W. Gams incertae suave, Sium sedis 449–450 subfuscus, Diphyus Staphylinidae – order Coleoptera 274 subpunctata, Spalangia starling, common (Sturnus vulgaris) 171, 173 subtilicornis, Diadromus Steinernema – family Steinernematidae Succineidae – order Mollusca 477 Steinernema spp. 78, 79 succineus, Longitarsus Steinernema carpocapsae (Weiser) 87, 140, 161, sudden oak death (Phytophthora ramorum) 476 162, 215, 279–280, 288 sugar beet (Beta vulgaris) 441 Steinernema feltiae (Filipjev) 57, 87, 104, 145, sugarcane whiteleaf disease (Ca. Phytoplasma 161, 162, 215, 250, 279–280, 287 oryzae) 48 Steinernematidae – order Rhabiditida Suidae – order Artiodactyla stellatum, Allium sulcata, Phasgonophora Stenodema – family Miridae sulfureana, Sparganothis Stenodema vicinum (Provancher) 372 sunfl ower (Helianthus annuus) 164 Stenomalina – family Pteromalidae superbum, Lilium Stenomalina gracilis (Walker) 121, 122–123, × superbum, Leucanthemum 124, 125 superbus, Spilichneumon Stephanidae – order Hymenoptera Sus – family Suidae stephensi, Anopheles Sus scrofa domestica Erxleben 182 Stethorus – family Coccinellidae suturalis, Eutanyacra Index 515

suturalis, Zygogramma Tanacetum macrophyllum (Waldst. & Kit.) Sch. suzukii, Drosophila Bip. 381 swallow-worts (Vincetoxicum spp.) 402–405 Tanacetum microphyllum DC 379 swede midge (Contarinia nasturtii) 134–136, Tanacetum millefolium (L.) Tzvel 379 476, 478 Tanacetum parthenium (L.) Sch. Bip. 380, 381 sweet clover (Melilotus offi cinalis) 277, 278, Tanacetum sclerophyllum H. Krasch 379 280 Tanacetum vulgare L. 378–381 sweet white clover (Melilotus albus) 403 tansy, common/garden (Tanacetum vulgare) swine (Sus scrofa domestica) 182 378–381 swirskii, Amblyseius tansy ragwort (Jacobaea vulgaris) 8 Sylvanelater – family Elateridae Taphrina – family Taphrinaceae Sylvanelater cylindriformis (Herbst) 73 Taphrina deformans (Berk.) Tul. 463–464 sylvestris, Malus Tarachidia – family Noctuidae sylvestris, Pinus Tarachidia candefacta Hübner 297 Sympiensis – family Eulophidae taraxaci, Cystiphora Sympiensis spp. 245 taraxaci, Phoma Sympiensis gordius (Walker) 245 Taraxacum – family Asteraceae Sympiensis marylandensis (Girault) see Taraxacum offi cinale F.H. Wigg 383–389 Sympiensis gordius (Walker) tarnished plant bug (Lygus lineolaris) 101, Sympiensis sericeicornis (Nees) 245 221–224 Synacra – family Diapriidae Tarsonemidae – order Trombidiformes Synacra sp. 185 tatarica, Lonicera Synanthedon – family Sesiidae Tatrian honeysuckle (Lonicera tatarica) 153 Synanthedon spp. 286 taurus, Bos Synanthedon exitiosa (Say) 286 taurus, Onthophagus Synanthedon myopaeformis (Borkhausen) tebyg, Gyranusoidea 285–288, 478, 480 tegmentosum, Acer Synanthedon tipuliformis (Clerck) 286 Telenomus – family Scelionidae Synchlora – family Geometridae Telenomus spp. 205–206 Synchlora albolineata Packard 379 Telenomus coloradensis Crawford 205 syngenesiae, Chromatomyia Telenomus droozi Muesebeck 205 Synopeas – family Platygastridae Telenomus fl avotibiae Pelletier 205 Synopeas myles Walker 136 Tenebriodes – family Trogossitidae Synopeas osaces Walker 136 Tenebriodes sp. 63 Synopeas ventrale Westwood 136 Tenthredinidae – order Hymenoptera syringae, Pseudomonas Tenuipalpidae – order Trombidiformes Syrphidae – order Diptera 109, 274 tenuissima, Alternaria Tephritidae – order Diptera Tephritis – family Tephritidae tabaci, Bemisia Tephritis neesii Meigen 339, 340 tabaci, Thrips terebinthifolius, Schinus tabernaemontana, Amsonia testudinea, Hoplocampa tabida, Asobara Tetranychidae – order Trombidiformes tabidus, Trachelus Tetranychus – family Tetranychidae Tachina – family Tachinidae Tetranychus urticae Koch 8, 46, 100, 104, 239, Tachina algens Wiedemann 166 240, 241 Tachinidae – order Diptera Tetrastichus – family Eulophidae Tachyporus – family Staphylinidae Tetrastichus spp. 195, 245 Tachyporus sp. 172 Tetrastichus julis (Walker) 7, 233, 234–236 taedatus, Carabus Tetrastichus planipennisi Yang 64–65, 67, 68 Tamarixia – family Eulophidae Tetrastichus setifer Thomson 209, 210, 211–212 Tamarixia (Tetrastichus) triozae (Burks) 109, Tetropium – family Cerambycidae 110 Tetropium fuscum (Fabricius) 476 tanacetaria, Macrosiphoniella tetrum, Gymnetron tanaceti, Puccinia texensis, Peleteria tanaceticola, Rhopalomyia Thanatephorus – family Ceratobasidiaceae Tanacetum – family Asteraceae Thanatephorus cucumeris (A.B. Frank) Donk Tanacetum balsamita L. 380, 381 446 Tanacetum bipinnatum (L.) Schultz-Bip. 379, Theroscopus – family Ichneumonidae 380 Theroscopus hemipteron (Riche) 159 Tanacetum camphoratum Less. 379, 380 Thielaviopsis – family Ceratocystidaceae Tanacetum douglasii DC 379 Thielaviopsis basicola (Berk. & Broome) Ferraris Tanacetum huronense Nutt. 379, 380 449 516 Index

thomsoni, Lathrolestes Trichogramma spp. 33, 49, 293, 294 thomsoni, Profenusa Trichogramma atopovirilia Oatman & Platner 49 three-lined leafroller (Pandemis limitata) 130 Trichogramma brassicae Bezdenko 49, 293, 294 Thripidae – order Thysanoptera (thrips) 274, Trichogramma cacoeciae Marchal 157, 161–162 291, 477 Trichogramma cordubensis Vargas & Cabello 49 Thrips – family Thripidae Trichogramma deion Pinto & Oatman 49 Thrips tabaci Lindeman 99 Trichogramma inyoense Pinto & Oatman 228, thuringiensis, Bacillus 229 tibialis, Lilioceris Trichogramma sibericum Sorkina 293, 294 tidius, Necremnus Trichogrammatidae – order Hymenoptera 47 Tilia – family Tiliaceae Trichomalopsis – family Pteromalidae Tilia mongolica Maxim. 83, 85 Trichomalopsis spp. 185 timothy (Phleum pratense) 338 Trichomalopsis americana (Gahan) 185 tinctorius, Carthamus Trichomalopsis dubia (Ashmead) 185 Tineidae – order Lepidoptera Trichomalopsis sarcophagae (Gahan) 44, tini, Phygadeuon 183–185, 187, 188–189 tipuliformis, Synanthedon Trichomalopsis viridescens (Walsh) 185 TnMNPV (Trichoplusia ni multiple Trichomalus – family Pteromalidae nucleopolyhedrovirus) 292 Trichomalus spp. 123 TnSNPV (Trichoplusia ni single Trichomalus fasciatus (Thomson) 122 nucleopolyhedrovirus) 292–293 Trichomalus lucidus (Walker) 121, 122, 123, 124 toadfl ax (Linaria spp.) 25–26, 317, 343, 344, Trichomalus perfectus (Walker) 121–122, 350, 355, 356, 360, 481 123–124, 125 Tolypocladium – family Ophiocordycipitaceae Trichoplusia – family Noctuidae Tolypocladium cylindrosporum Gams 75 Trichoplusia ni (Hübner) 101, 103, 229, 291– tomato (Solanum lycopersicum) 100, 101, 103, 294, 480 107–111, 291, 387, 446, 448, 449, 454, Trichoplusia ni multiple nucleopolyhedrovirus – 466–471 family Baculoviridae 292 tomato looper (Chrysodeixis chalcites) 476 Trichoplusia ni single nucleopolyhedrovirus – tomato/potato psyllid (Bactericera cockerelli) family Baculoviridae 292–293 101, 107–111, 480 Trichopria – family Diapriidae tomato russet mite (Aculops lycopersici) 100 Trichopria spp. 54–55, 144 Tomato spotted wilt virus – family trichops, Phygadeuon Bunyaviridae 99 tricornutum, Galium Tomicus – family Curculionidae trifolii, Liriomyza Tomicus piniperda (L.) 476 Trifolium – family Fabaceae torrida, Amara Trifolium spp. 387 Tortricidae – order Lepidoptera 477 Trifolium arvense L. 277 torvina, Conura Trifolium pratense L. 277 Torymidae – order Hymenoptera Trifolium repens L. 277, 386, 387 Townselitis – family Braconidae trilineata, Lema Townselitis bicolor (Wesmael) 250–251, 252– triozae,Tamarixia 253 Triozidae – order Hemiptera Trachelus – family Cephidae tripleurospermi, Rhopalomyia Trachelus tabidus F. 115 Tripleurospermum – family Asteraceae tragopogonis, Pustula Tripleurospermum inodorum (L.) Sch. Bip. tranquebaricae, Atanycolus 391–393, 396–399 transversovittatus, Hylobius Tripleurospermum perforatum (L.) Sch. Bip. tremula, Chrysomela 124 Trialeurodes – family Aleyrodidae trisulcatus, Cyphocleonus Trialeurodes vaporariorum (Westwood) 99, 100, triticale – family Poaceae 102 x Triticale hexaploide Lart. 272, 414 triangulifera, Hyalomyodes x Triticosecale Witt. ex A. Camas 233 Trichocellus – family Carabidae tritici, Contarinia Trichocellus cognatus (Gyllenhal) 172 Triticum – family Poaceae Trichoderma – family Hypocreaceae Triticum aestivum L. 75, 112–113, 116, 164, Trichoderma spp. 439, 448 233, 272–273, 275, 354, 371, 373, 397, Trichoderma hamatum (Bonord.) Bainier 450, 412–417, 447, 455, 480 468 Triticum durum Desf. 272–273, 415 Trichoderma harzianum Rifai 415, 426, 430, Triticum turgidum convar. durum (Desf.) 441, 448 Bowden 164 Trichoderma viride Pers. 426 Trogossitidae – order Coleoptera Trichogramma – family Trichogrammatidae Trombidiidae – order Trombidiformes Index 517

truncatum, Acer Urophora affi nis (L.) 302 truncatum, Colletotrichum Ursidae – order Carnivora Trybliographa – family Figitidae Ursus – family Ursidae Trybliographa spp. 144, 146, 154 Ursus arctos horribilis Ord 171, 173 Trybliographa rapae (Westwood) 144, 146 Urtica – family Urticaceae Trypanosoma – order Trypanosomatida Urtica dioica L. 109 Trypanosoma cruzii Chagas 48 urticae, Tetranychus Tsuga – family Pinaceae usitatissimum, Linum Tsuga heterophylla (Raf.) Sarg. 203 uvella, Sorosporella tuberosa, Asclepias tuberosula, Platygaster tuberosum, Solanum vaccinii, Phomopsis tunetana, Itoplectis vaccinii-corymbosi, Monilinia turbatus, Ceutorhynchus Vaccinium – family Ericaceae turgidum, Triticum Vaccinium spp. 152 turionellae, Pimpla Vaccinium angustifolium Aiton 424–425, turnip (Brassica rapa var. rapa) 142, 214, 454 426–427 Tuta – family Gelechiidae Vaccinium corymbosum L. 424, 425, 426 Tuta absoluta (Meyrick) 101 vagans, Pantoea twelve-spotted asparagus beetle (Crioceris vagus, Dalapius duodecimpunctata) 235 vagus, Tycherus two-spotted spider mite (Tetranychus urticae) 8, vanessae, Cotesia 46, 100, 104, 239, 240, 241 vaporariorum, Trialeurodes Tycherus – family Ichneumonidae varians, Pimpla Tycherus impiger (Wesmael) 58 varicolor, Diadromus Tycherus vagus (Berthoumieu) 159 variegata, Glypta tylodermatis, Eurytoma variegatus, Micromus Typha – family Typhaceae varipes, Zaglyptus Typha latifolia L. 363 velox, Aoplus typhae, Ceutorhynchus velutinana, Argyrotaenia Typhlodromalus – family Phytoseiidae ventrale, Synopeas Typhlodromalus limonicus (Garman & Venturia – family Venturiaceae McGregor) 104 Venturia inaequalis (Cooke) G. Winter 200, Typhlodromips montdorensis (Schicha) see 245–246 Amblyseius montdorensis (Schicha) venusta, Hackelia Typhlodromips swirskii (Athias-Henriot) see Verbena – family Verbenaceae Amblyseius swirskii Athias-Henriot Verbena spp. 100 Typhlodromus – family Phytoseiidae verna, Aleochara Typhlodromus caudiglans Schuster 239, 240 versicolor, Bembidion Typhlodromus occidentalis (Nesbitt) see versicolor, Lissonota Galendromus occidentalis (Nesbitt) verticillata, Setaria Typhlodromus pyri Scheuten 239, 240–241 Verticillium – family Plectosphaerellaceae tyrannus, Brevoortia Verticillium albo-atrum Reinke & Berthhold 454 Tyria – family Arctiidae Verticillium dahliae Kleb. 449, 454–455, 457, Tyria jacobaeae (L.) 8 458 Tyta – family Noctuidae Verticillium lecanii (Zimmerman) Viégas see Tyta luctuosa (Denis & Schiffermüller) 307, 308 Lecanicillium lecanii (Zimmerman) Zare & W. Gams verticillium wilt (Verticillium dahliae, ulmi, Ophiostoma V. albo-atrum) 454–459 ulmi, Panonychus vesicatoria, Xanthomonas Ulmus – family Ulmaceae vesicularis, Eupelmus Ulmus spp. 83, 87 vetches (Vicia spp.) 277 Ulmus americana L. 476 Vicia – family Fabaceae ultimum, Pythium Vicia cracca L. 277 uncinata, Meigenia Vicia faba L. 277, 278 undulata, Phyllotreta vicina, Scolioneura uniformis, Leiophron vicinum, Stenodema Urolepis – family Pteromalidae victoriae, Cryptococcus Urolepis spp. 185 victus, Anaphes Urolepis rufi pes (Ashmead) 183–185, 186–187 Vigna – family Fabaceae Urophora – family Tephritidae Vigna radiata (L.) R. Wilczek 396, 446 Urophora spp. 303 Villa – family Bombyliidae 518 Index

Villa alternata (Say) 165 white swallow-wort (Vincetoxicum Villa fulviana (Say) 165 hirundinaria) 404, 405 Villa lateralis (Say) 165 whitefl ies (family Aleyrodidae) 291 villosus, Picoides wild carrot (Daucus carota) 214 Vincetoxicum – family Apocynaceae wild mustard (Sinapis arvensis) 257, 387 Vincetoxicum spp. 402, 405 wild oat (Avena fatua, Chasmanthium Vincetoxicum hirundinaria Medik. 404, 405 latifolium) 371, 373 Vincetoxicum nigrum (L.) Moench 402, 403, 404 wild parsnip (Apium petroselinum) 214 Vincetoxicum rossicum (Kleopow) Barbarich willistoni, Poecilanthrax 402–403, 404, 405 wingfi eldii, Leptographium vindemmiae, Pachycrepoideus winter moth (Operophtera brumata) 7 vinifera, Vitis Winthemia – family Tachinidae virgifera virgifera, Diabrotica Winthemia deilephilae (Osten Sacken) 166 viride, Trichoderma Winthemia occidentis Reinhard 204 viridescens, Trichomalopsis Winthemia quadripustulata Fabricius 166 viridis, Setaria Winthemia rufopicta (Bigot) 167 Vitis – family Vitaceae wireworms, click beetles (Agriotes spp.) 72–80 Vitis vinifera L. 48, 153, 192, 193–195, 238, Wolbachia – family Rickettsiaceae 240–241 Wolbachia spp. 28, 43–50, 185, 186–187 vitripennis, Hyaloides woodpeckers (Picidae) 267 vitripennis, Nasonia woodwasp (Sirex noctilio) 24–25, 263–268, vittatae, Microctonus 476 vittatum, Leiobunum wormseed mustard (Erysimum cheiranthoides) vittatus, Collops 257 vitticrus, Dolichomitus wrasei, Psylliodes Vrestovia – family Pteromalidae Vrestovia brevior Boucek 153–154 vulgare, Hordeum Xanthomonas – family Xanthomonadaceae vulgare, Leucanthemum Xanthomonas euvesicatoria Jones et al. 466 vulgare,Tanacetum Xanthomonas gardneri (ex Šutiþ) Jones et al. vulgaris, Beta 466, 467, 469, 471 vulgaris, Jacobaea Xanthomonas perforans Jones et al. 466 vulgaris, Linaria Xanthomonas vesicatoria (ex Doidge) Vauterin vulgaris, Phaseolus et al. 466, 468, 469 vulgaris, Senecio xanthopoda, Ganaspis vulgaris, Sturnus xanthostigma, Agulla Xenocrepis – family Pteromalidae Xenocrepis pura Mayr 122 water parsnip (Sium suave) 214 Xylella – family Xanthomonadaceae watermelon (Citrullus lanatus) 387 Xylella fastidiosa Wells et al. 48 western fl ower thrips (Frankliniella occidentalis) xylostella, Plutella 99, 102, 103, 105 western hemlock (Tsuga heterophylla) 203 western hemlock looper (Lambdina fi scellaria yellow foxtail (Setaria pumilla) 370, 373 lugubrosa) 203 yellow toadfl ax (Linaria vulgaris) 25, 343, 344, western oak looper (Lambdina fi scellaria 345, 349, 354–360 somniaria) 203 wheat, spring wheat, winter wheat (Triticum aestivum) 75, 112–113, 116, 164, 233, Zaglyptus – family Ichneumonidae 272–273, 275, 354, 371, 373, 397, Zaglyptus varipes (Gravenhorst) 58 412–417, 447, 455, 480 zahaikevitshii, Oobius wheat midge (Sitodiplosis mosellana) 15, zaraptor, Muscidifurax 272–275, 480 Zea – family Poaceae wheat stem sawfl y (Cephus cinctus) 112–116 Zea mays L. 46, 74, 195, 297, 371, 402, white ash (Fraxinus americana) 63 412–415, 442, 455 white clover (Trifolium repens) 277, 386, 387 zeae, Gibberella white elm (Ulmus americana) 476 Zele – family Braconidae white mustard, yellow mustard (Sinapis alba) Zele mellea (Cresson) 168 120, 249, 257, 258, 354 Zetzellia – family Stigmaeidae white peach scale (Pseudaulacaspis pentagona) Zetzellia mali (Ewing) 239, 240 27 Zygogramma – family Chrysomelidae white pine (Pinus strobus) 54, 264, 476 Zygogramma bicolorata Pallister 297 white pine blister rust (Cronartium ribicola) 476 Zygogramma suturalis Fabricius 297, 298