Instant download Proceedings of the 5th international symposium on biological control of arthropods
Proceedings of the 5th International Symposium on Biological Control of Arthropods 1st Edition Peter Mason
Visit to download the full and correct content document: https://textbookfull.com/product/proceedings-of-the-5th-international-symposium-on-bi ological-control-of-arthropods-1st-edition-peter-mason/
More products digital (pdf, epub, mobi) instant download maybe you interests ...
Proceedings of the 5th International Conference on Electrical Engineering and Automatic Control 1st Edition Bo Huang
Innovation and Application of Engineering Technology: Proceedings of the International Symposium on Engineering Technology and Application 1st Edition Wenxue Chen
ISBN-13: 9 Commission Editorial ass Production e Way d e OX10 8DE )1491 832111 )1491 833508 o@cabi.org ww.cabi.org CAB ernational 201 al Control of A mmons Attrib record for thi
Internationa 7. Proceeding rthropods is ution-NonCo s book is ava
ning editor: W sistant: Alexan editor: Tracy H
11 8 ard Cooper dra Lainsbur ead a trading nam al, 2017 gs of the 5th I licensed unde ommercial-No ilable from th ry me of CAB In 745 B T: + E-mail: ca
International S er a oDerivatives 4 he British Libr nternational CA 5 Atlantic Ave 8th F oston, MA 02 U +1 (617)682-9 abi-nao@cabi Symposium 4.0 Internation rary, London, ABI enue loor 2111 USA 9015 i.org nal License UK.
SESSION 1: ACCIDENTAL INTRODUCTIONS OF BIOCONTROL AGENTS: POSITIVE AND NEGATIVE ASPECTS
1.1 Accidental Introductions of Natural Enemies: Causes and Implications by D.C. Weber, A.E. Hajek and K.A. Hoelmer ……………………………………………………... 2
1.2 Risks and Benefits of Accidental Introductions of Biological Control Agents in Canada by P.G. Mason, O.O. Olfert, T. Haye, T.D. Gariepy, P.K. Abram and D.R. Gillespie …………………………………………………………………………………… 6
1.3 Adventive vs. Planned Introductions of Trissolcus japonicus Against BMSB: An Emerging Case Study in Real-time by K.A. Hoelmer, D.C. Weber and T. Haye ……….. 9
1.4 Can Native Parasitoids Benefit From Accidental Introductions of Exotic Biological Control Agents? by T. Haye, J.K. Konopka, T.D. Gariepy, J.N. McNeil, P.G. Mason and D.R. Gillespie …………………………………………………………………………….. 12
1.5 Accidental Introduction into Italy and Establishment of Aprostocetus fukutai (Hymenoptera: Eulophidae) in Citrus Longhorned Beetle Infestations by F. Hérard, M. Maspero and M.C. Bon ………………………………………………………….……….. 15
1.6 Inadvertent Reconstruction of Exotic Food Webs: Biological Control Harms and Benefits by J.M. Kaser, A.L. Nielsen, P.K. Abram and G.E. Heimpel …………………... 19
SESSION 2: THE IMPORTANCE OF PRE AND POST RELEASE GENETICS IN BIOLOGICAL CONTROL
2.1 Practical Management of the Genetics of Classical Biocontrol Introductions by R. Stouthamer ……………………………………………………………………………….. 23
2.2 Genetic Diversity of Field and Laboratory Populations of Mastrus ridens and Consequences of Inbreeding During Laboratory Culture by T. Zaviezo, R. Retamal, T. Urvois, X. Fauvergue, K. Toleubayev and T. Malausa ………………………………..… 26
2.3 Effects of Genetic Diversity, Inbreeding and Outbreeding Investigated in Six Reared or Released Biocontrol Agents by T. Malausa, B. Quaglietti, H. Mathé-Hubert and P. Martinez …………………………………………………………………………... 29
2.4 Rapid Biocontrol Evolution in New Zealand’s Species-sparse Pasturelands by S.L. Goldson, F. Tomasetto, J.M.E. Jacobs, B.I.P. Barratt, , S.D. Wratten, R.M. Emberson and J. Tylianakis ……………………………………………………………………………… 32
2.5 Food Webs, Multiple Enemies and Biological Control by J.M. Tylianakis, P. Casanovas and S.L. Goldson …………………………………………………………….. 35
2.6 Benefits of Pre-release Population Genetics: A Case Study Using Psyttalia lounsburyi, a Biocontrol Agent of the Olive Fruit Fly in California by M.C. Bon, L. Smith, K.M. Daane, C. Pickett, X. Wang, A. Blanchet, F. Chardonnet, F. Guermache and K. A. Hoelmer………………………………………………………………………………... 38
SESSION 3: HOW WELL DO WE UNDERSTAND NON-TARGET IMPACTS IN ARTHROPOD BIOLOGICAL CONTROL?
3.1 Introduction and Non-target Effects of Insect Biological Control: Concepts, Examples, and Trends by R.G. Van Driesche and M.S. Hoddle ……………………….. 43
3.2 Displacement of Native Natural Enemies by Introduced Biological Control Agents in Agro-Ecosystems: A Serious Non-target Effect or Not? by S.E. Naranjo …………. 46
3.3 Assessing Host Use and Population Level Impacts on Non-target Species by Introduced Natural Enemies: Can Host Range Testing Provide Insight? by M.G. Wright …………………………………………………………………………………….. 50
3.4 Parasitoid Host Ranges: Comparing Studies From the Laboratory and Field by G.E. Heimpel, K.R. Hopper, J.M. Kaser, J. Miksanek, M. Bulgarella, I. Ramirez and R.A. Boulton
3.5 Can Predictive Models Help to Identify the Most Appropriate Non-target Species for Host-specificity Testing? by J.H. Todd, B.I.P. Barratt and T. Withers …………..… 55
3.6 What Olfactometer Tests Were Able to Tell Us About Non-target Risk That Nochoice and Choice Tests Could Not by G.A. Avila, T.M. Withers and G.I. Holwell ………
SESSION 4: REGULATION AND ACCESS AND BENEFIT SHARING POLICIES RELEVANT FOR CLASSICAL BIOLOGICAL CONTROL APPROACHES
4.1 The New Zealand System to Assess the Environmental Benefits and Risks of Releasing New Biocontrol Agents of Arthropods by G.A.C. Ehlers and K.E. Bromfield
4.2 Practical and Implementable Mechanisms for Compliance with the Nagoya Protocol: Access and Benefit Sharing by D. Smith ……………………………………. 67
4.3 Access and Benefit Sharing: Best Practices for the Use and Exchange of Invertebrate Biological Control Agents by B.I.P. Barratt, P.G. Mason, M.J.W. Cock, J. Klapwijk, J.C. van Lenteren, J. Brodeur, K.A. Hoelmer and G.E. Heimpel ……………... 71
SESSION 5: THE ROLE OF NATIVE AND ALIEN NATURAL ENEMY DIVERSITY IN BIOLOGICAL CONTROL
5.1 Native Coccinellids and Biological Control: A Positive Partnership that can be Threatened by the Invasion of an Alien Species by A.A. Grez, T. Zaviezo, C. González, A. O. Soares and T. Poch ……………………………………………………………………. 76
5.2 Predator Invasion Disrupts the Conservation of Natural Enemy Biodiversity by W.E. Snyder …………………………………………………………………………….… 79
5.3 Impacts of North American Native and Introduced Natural Enemies on Population Dynamics of the Invasive Emerald Ash Borer by J.J. Duan, L.S. Bauer and R. G. Van Driesche …………………………………………………………….……….. 80
5.4 Relationships Between Diversity of Natural Enemy Communities and Pest Predation Levels in Different Farming and Landscape Contexts in Hedgerow Network Landscapes by S. Aviron, E.A. Djoudi, A. Alignier, M. Plantegenest and J. Pétillon ….. 82
5.5 Establishment of Mastrus ridens (Hymenoptera: Ichneumonidae), an Ectoparasitoid of Codling Moth, in New Zealand by M. Sandanayaka, J. Charles, V. Davis, A. Chhagan, P. Shaw, R. Wallis, P. Lo, L. Cole, J. Walker and K. Colhoun …………….. 85
5.6 Exotic or Native? Interspecific Competition in the Parasitization of the Fruit Fly Ceratitis cosyra by E.O. De Souza, P. Ayelo, J. Zannou, A.H. Bokonon-Ganta and M.F. Karlsson ………………………………………………………………………………….. 88
SESSION 6: FRONTIERS IN FOREST INSECT CONTROL
6.1 Investigating the Complex Gall Community of Leptocybe invasa by B.P. Hurley, C. Gevers, G. Dittrich-Schröder and B. Slippers ………………………………………….... 92
6.2 Larval Parasitoids for Biocontrol of Invasive Paropsine Defoliatiors by T.M. Withers, G.R. Allen, S.R. Quarrell and A. Pugh …………………………………………. 95
6.3 Biological Control of the Gonipterus scutellatus Species Complex: Testing the Species, Climatic or Phenological Mismatch Hypotheses by M.L. Schröder, H.F. Nahrung, S. A. Lawson, B. Slippers, M.J. Wingfield and B.P. Hurley ……………….….. 99
6.4 A Successful Case of Classical Biological Control of a Gall Wasp by F. Colombari and A. Battisti …………………………………………………………………………… 102
6.5 Biological Control of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) in Eucalyptus Plantations in Brazil: An Update by C.F. Wilcken, L.R. Barbosa, S.M. Velozo, L.K. Becchi, L.R. Junqueira, L.A.N. de Sá and J.C. Zanuncio …………………. 105
6.6 Ecology and Biological Control of Outbreak Populations of Winter Moth in the Northeastern United States by J.S. Elkinton, G.H. Boettner and H.J. Broadley ……... 108
SESSION 7: BIOCONTROL MARKETPLACE I – FREE TOPICS
7.1 Friend or Foe: The Role of Native, Natural Enemies in the Biological Control of Winter Moth by H.J. Broadley, J.S. Elkinton and G.H. Boettner ……………………... 112
7.2 BiCEP: Progress in a Global Collaboration for the Biological Control of Australian-origin Eucalypt Pests by S.A. Lawson, H. F. Nahrung, M. Griffiths and M. A. Healey …………………………………………………………………………………… 115
7.3 Introduction of Tachardiaephagus somervilli, an Encyrtid Parasitoid, for the Indirect Biological Control of an Invasive Ant on Christmas Island by S.P. Ong, D.J. O’Dowd, T. Detto and P.T. Green …………………………………………………….... 118
7.4 Orius laevigatus Induces Plant Defenses in Sweet Pepper by S. Bouagga, M. PérezHedo, J.L. Rambla, A. Granell and A. Urbaneja ………………………….……………. 121
7.5 The Role of Tomato Plant Volatiles Mediated by Zoophytophagous Mirid Bugs by M. Pérez-Hedo, J.L. Rambla, A. Granell and A. Urbaneja …………………….………. 124
SESSION 8: WEED AND ARTHROPOD BIOLOGICAL CONTROL: MUTUAL BENEFITS AND CHALLENGES
8.1 Arthropod and Weed Biological Control: Mutual Benefits and Common Challenges by H.L. Hinz, M.J.W. Cock, T. Haye and U. Schaffner ………………….… 128
SESSION 9: MAXIMIZING OPPORTUNITIES FOR BIOLOGICAL CONTROL IN ASIA'S RAPIDLY CHANGING
AGRO-ENVIRONMENTS
9.1 From Molecule to Landscape - Integrating Molecular Biology and Landscape Ecology to Open New Opportunities for Biological Control in East Asia by G.M. Gurr and M. You …………………………………………………………………………….... 132
9.2 Phyto-pathogens and Soil Nutrients Shape Biological Control of Invasive Mealybugs in Asia’s Cassava Crops by K.A.G. Wyckhuys …………………………… 135
9.3 Recent Change of Biocontrol Services in Cotton Agro-ecosystem of Northern China by Y. Lu ………………………………………………………………………….. 137
9.4 Know your Enemies: Suppression of Plutella xylostella and Crocidolomia pavonana by Different Predators in West Java, Indonesia by R. Murtiningsih, P.M. Ridland, L.G. Cook and M. J. Furlong ………………………………………………………………… 139
9.5 Biological Control in Vegetable Brassica Pest Management in Tropical Asia: Where Do We Currently Stand? by R. Srinivasan, M-Y. Lin, N.T.T. Hien and V.M. Hai
144
SESSION 10: BIOLOGICAL CONTROL BASED INTEGRATED PEST MANAGEMENT: DOES IT WORK?
10.1 Successful Integrated Pest Management with Biological Control: Case of the Diamondback Moth in Malaysia by A. Sivapragasam ……………………………….. 148
10.2 A Practice of Trichogramma-based IPM of Rice Insect Pests by M. Hou, K. Ko, L. Guo, M. Kang, H. Peng, D. Babendreier, F. Zhang, R. Tang and K. Song …………….. 151
10.3 Conservation Biological Control and IPM Practices in Brassica Vegetable Crops in China: A Step Further by Y.Q. Liu and S.S. Liu ………………………………….. 154
10.4 Biological Control of Olive Fruit Fly in California – Release, Establishment and Impact of Psyttalia lounsburyi and Psyttalia humilis by K.M. Daane, X.G. Wang, C.P. Pickett, A. Blanchet, D. Nieto, K.A. Hoelmer, M.C. Bon and L. Smith ………………… 156
10.5 Biological Control using Predators and Parasitoids in Vietnam: From Successful Participatory Approaches to Potential Challenges by A. Costa, H.T. Dao and D.H. Tran
159
SESSION 11: EXPLORING THE COMPATIBILITY OF ARTHROPOD BIOLOGICAL CONTROL AND PESTICIDES: MODELS AND DATA
11.1 How Differential Stage Susceptibility to Pesticides Affects the Success of Biocontrol Agents by J.D. Stark, J.E. Banks and R.I. Vargas ………………….……… 164
11.2 Orchard Pesticides and Natural Enemies: Lessons from the Lab and Field by N.J. Mills
11.3 Pesticide Use and Floral Resources Differentially Affect Communities of Predators, Parasitoids, and Pests in a Regional Survey by C. Blubaugh and W.S. Snyder
11.4 Integration of Biopesticides with Natural Enemies for Control of Tropical Fruit Flies (Diptera: Tephritidae) by R.I. Vargas, S. Souder, L. Leblanc, J.E. Banks and J. Stark
11.5 Protecting Assemblages of Biocontrol Species: Modeling a Surrogate Species Approach by J.E. Banks, J.D. Stark, R.I. Vargas, A. Veprauskas and A. Ackleh …………………………………………………………………………………………… 175
11.6 Disruption of Biological Control Due to Non-target Effects of Pesticides in Australian Grains by M. Hill, M. Nash, P. Umina and S. Macfadyen ……………….... 178
SESSION 12: SUCCESSES AND UPTAKE OF ARTHROPOD BIOLOGICAL CONTROL IN DEVELOPING COUNTRIES
12.1 Classical Biological Control of Insects in Developed and Developing Countries: a Comparison Using BIOCAT Database by M.J.W. Cock and U. Kuhlmann …………. 181
12.2 Plantwise Data on Extension and the Uptake of Augmentative Biological Control using Arthropods by J. Dougoud, U. Kuhlmann, S. Edgington and M.J.W. Cock ….. 185
12.3 The Importance of Local Production to Foster the Uptake of Augmentative Biological Control in Developing Countries by F. Zhang, S.X. Bai, H.K. Tai, Y.Y. Myint, N.N. Htain, B. Soudmaly, L. Zheng, Z.Y. Wang, U. Wittenwiler, M. Grossrieder and U. Kuhlmann ……………………………………………………………………………….. 188
12.4 Understanding the Ecology and Impact of Parasitoids of the Whitefly (Bemisia tabaci Complex: Aleyrodidae) in Cassava Landscapes of East Africa by S. Macfadyen, A. Kalyebi, Y. Tembo, K. Katono, A. Polaszek, W.T. Tay, C. Paull and J. Colvin …………………………………………………………………………………………… 192
12.5 Success and Failures of IPM in Africa and Asia: the Significance of Biocontrol by S.T. Murphy, J. Lamontagne-Godwin, B. Taylor and E. Thompson ……………………. 195
SESSION 13: SOCIO-ECONOMIC IMPACTS OF BIOLOGICAL CONTROL
13.1 Success and Impact in Classical Biological Control: Some Examples from Developing Countries by R.K. Day, M.J.W. Cock and U. Kuhlmann …………………. 201
13.2 Cost of Biological Control of Invasive Arthropods by K.M. Jetter ………..…….205
13.3 Assessment of the Economic and Poverty Impacts of Biological Control of Cereal Stemborers in Kenya using the Economic Surplus Modelling Approach by S. Midingoyi, A. Hippolyte, M. Ibrahim, B. Muriithi, G. Ong’amo and L. Bruno ……….... 208
13.4 Socio-economic Impacts and Extension Process of Conservation Biological Control in Mango Orchards in Réunion Island by J.P. Deguine, M. Jacquot, E. Frago, P. Laurent, L. Vanhuffel, D. Vincenot and J.N. Aubertot ………..…………………...… 211
13.5 Chronicling the Socio-economic Impact of Integrating Biological Control, Technology, and Knowledge over 25 Years of IPM in Arizona by P.C. Ellsworth, A. Fournier, G. Frisvold and S.E. Naranjo ………………………………………………... 214
SESSION 14: MARKETPLACE II – FREE TOPICS
14.1 Do GM Plants with Stacked Insecticidal Traits Pose an Increased Risk to Biological Control? by J. Romeis and M. Meissle …………………………………...… 218
14.2 Initial Evaluation of Two Native Egg Parasitoids for the Control of Bagrada hilaris, an Invasive Stink Bug in Western USA by R.F.H. Sforza, M.C. Bon, G. Martel, M. Augé, M. Roche, R. Mahmood and L. Smith ………………………………………… 221
14.3 Old and New Host-parasitoid Associations: Parasitism of the Native African and Invasive Fruit flies Species by S.A. Mohamed, S. Ekesi, R. Wharton, S.A. Lux and W. A. Overholt …………………………………………………………………………………. 224
14.4 Harnessing of Floral and Faunal Biodiversity of Rice Ecosystems for Pest Management by C. Shanker, K. Shabbir, B. Jhansi Rani, S. Amudhan and G. Katti …………………………………………………………………………………………… 228
14.5 Population dynamics of Plutella xylostella (Lepidoptera: Plutellidae) and Its Parasitoids Along Altitudinal Gradients of the Eastern Afromontane by B.V. Ngowi, H.E. Z. Tonnang, F. Khamis, E.M. Mwangi, B. Nyambo, P. N. Ndegwa and S. Subramanian
231
POSTER PRESENTATIONS
Poster 1: Discovery of Phasmarhabditis hermaphrodita (Nematoda) in the USA and its Potential Importance in the Biological Control of Invasive Gastropods by R.J. Mc Donnell, I. Tandingan De Ley, D.R. Denver and T.D. Paine …………………………... 236
Poster 2: Feeding Behavior of Rumina decollata (Gastropoda) Raises Questions about Its Efficacy as a Biocontrol Agent of the Pestiferous Brown Garden Snail, Cornu aspersum (Gastropoda) by R.J. Mc Donnell, R. Santangelo, T.D. Paine and M.S. Hoddle
237
Poster 3: Genetic Diversity and Origins of Halyomorpha halys in the U.S. and of Its Potential Biocontrol Agent Unexpectedly Recovered from the Wild in the United States by M.C. Bon, K. A. Hoelmer, E. J. Talamas, M.L. Buffington, F. Guermache and D. C. Weber ………………………………………………………………..……………….. 240
Poster 4: Variable Performance and Improvement by Crossing in Commercial Populations of the Pirate Bug Orius majusculus by L.B. Rasmussen, K. Jensen, J.G. Sørensen, J. Overgaard, M. Holmstrup and T.N. Kristensen ……………….………….. 243
Poster 5: Parasitoids of Drosophila in Switzerland and Their Potential for Biological Control of the Invasive Drosophila suzukii by J. Collatz, V. Knoll, T. Ellenbroek and J. Romeis ……………………………………………………………………………….….. 245
Poster 6: Native North American vs. Asian Parasitoid Natural Enemies of Invasive Brown Marmorated Stink Bug by P.K. Abram and K.A. Hoelmer …………………... 248
Poster 7: Insect Natural Enemies: Review and Future Application for CPB Management in Cocoa by N. Maisin ………………... 251
Poster 8: Do Invasive Alien Species Affect Diversity of Local Communities? by P. Kindlmann, A. Honěk and Z. Martinková ………………………………………………. 254
Poster 9: Introduction to FAO Guide: Classical Biological Control of Insect Pests in Forestry: A Practical Guide by F. Colombari, B. P. Hurley, M. Kenis, S.A. Lawson, S. Sathyapala, J. Sun, R. Weeks and C. Wilcken …………………………………………... 257
Poster 10: Diversity of Edible Saturniids (Lepidoptera: Saturniidae) and Their Parasitoids in Kenya by S. Subramanian, C.M. Tanga, E. Kusia, P. Cerretti, F. Khamis, R.S. Copeland, C. Borgemeister and S. Ekesi …………………………………………... 260
Poster 11: Action of Bacillus thuringiensis on Eucalyptus Snout Beetle Gonipterus platensis (Coleoptera: Curculionidae) Larvae by A.B. Horta, C. Jordan, M.F. Ribeiro, M.V.F. Lemos, J.A. Desidério and C.F. Wilcken ……………………………………….. 263
Poster 12: Host Specificity Testing of Psyllaephagus bliteus, an Accepted Biocontrol Agent of Glycaspis brimblecombei, Reveals a New Host by S.J. Bush, B. Slippers and B.P Hurley …………………………………………………………………………………… 266
Poster 13: Potential of Entomopathogenic Hyphomycetes for Control of Forest and Urban Lepidoptera in Georgia by M. Burjanadze, A. Supatashvili, M. Arjevanidze, K. Koridze, T. Abramishvili, N. Kunelauri and V. Vachadze ……………………………… 267
Poster 14: Diversity of Entomopathogenic fungi from forest ecosystem of Georgia by K. Koridze and M. Burjanadze .…………………. 270
Poster 15: Innate Positive Chemotaxis to Pollen from Crops and Banker Plants in Predaceous Biological Control Agents: Towards New Field Lures? by S. Li and F. Zhang …………………………………………………………………….……………… 273
Poster 16: Estimating Parasitoid Suppression of Aphid Populations in the Field by A. Leblanc and J. Brodeur …………………………………………………….…………… 274
Poster 17: Does Patch-guarding Behaviour in Parasitoids Deter or Attract Arthropod Egg Predators? by J. Doyon, P.K. Abram and J. Brodeur …………………………….. 275
Poster 18: The Behavioural Type of a Top Predator Drives the Short-term Dynamic of Intraguild Predation by R. Michalko and S. Pekár ……………………………………. 276
Poster 19: The Effect of Plant Resistance on Biological Control of Insect Pests by D. Weber, P. A. Egan, L. E. Ericson, A. Muola and J. A. Stenberg ……………………….. 278
Poster 20: Promoting Cotesia rubecula, an antagonist of Pieris rapae by S. Fataar, S. Leist, T. Oberhänsli and H. Luka …………………………………………………….…. 281
Poster 21: Cold Acclimation Increases Cold- and Starvation Tolerance but Reduces Predation Rate and Reproduction in the Predatory Mite Gaeolaelaps aculeifer by K. Jensen …………………………………………………………………………………... 284
Poster 22: Mass-rearing Optimization of the Parasitoid Psyttalia lounsburyi for Biological Control of the Olive Fruit Fly by F. Chardonnet, A. Blanchet, B. Hurtel, F. Marini, M.C. Bon, K.M. Daane, C. Pickett, X. Wang and L. Smith …………….………. 286
Poster 23: Evaluation of Sixspotted Thrips, Scolothrips sexmaculatus, for Biological Control of Spider Mites in California Almonds by D. Haviland …………………….. 290
Poster 24: Area Wide Integrated Pest Management Incorporating the Sterile Insect Technique: Gut Microbiota Impacts on Tephritid Fitness and Performance by L.A. Shuttleworth, A.T. Deutscher, T. Osborne, M.A.M. Khan, D. Collins, C. Burke, T. Chapman, A. Darling, M. Riegler and O.L. Reynolds ………………………………….. 292
Poster 25: Non-target Impacts of Isaria fumosorosea (Hypocreales: Cordycipitaceae) on Natural Enemies of Arthropod Pests by R. Zemek, E. Prenerová, L. Volter, M. Awad, F. Weyda, H. M. Hussein, O. Habuštová Skoková and V. Půža ………………………... 294
Poster 26: Releases of Trissolcus japonicus and Anastatus sp. for Suppression of Halyomorpha halys in Kiwifruit Orchards by Q.Q. Mi, J.P. Zhang, Y.X. Han, Y.C Yan, B.X. Zhang, D.S. Li and F. Zhang
Poster 27: Caught on Camera: Confirmation of Natural Enemies Attacking Pest Leafrollers in Kiwifruit Orchards by J.H. Todd, J. Poulton, C. McKenna and L.A. Malone
Poster 28: Telenomus sp., a Potential Biocontrol Agent Against the Cabbage Moth Mamestra brassicae by G. Barloggio, L. Tamm, T. Oberhänsli, P. Nagel and H. Luka
Poster 29: Alteration of Predatory Behavior of a Generalist Predator by Exposure to Two Insecticides by B. Petcharad, O. Košulič, S. Bumrungsri and R. Michalko ………302
Poster 30: Impact of Plant Extracts of Embelia ribes and two Commercial Pesticides on Mortality and Predator Activity of a Generalist Predator, Oxyopes lineatipes by O. Košulič, P. Vichitbandha, T. Pung and R. Michalko ………………………………........ 304
Poster 31: Vespula Biocontrol in New Zealand Revisited by B. Brown and R. Groenteman ……………………………………………………………………………... 306
Poster 32: The Rich Tapestry of Biological Control Targets and Agents in Sweetpotato Production Systems of Papua New Guinea by J. Liu, B. Wilson, T. Guaf, W. Wau, B. Komolong, S. Sar, R. Dotoana, Y. Jeffery, W. Sirabis, R. Akkinapally, R. Fujinuma, G. Kirchhoff, A. Agiwa, R. Geno, R. Culas, P. Brown, S. Bang and G.M. Gurr …...……… 309
Poster 33: Acerophagus papayae Noyes and Schauff (Hymenoptera: Encyrtidae) as a Biocontrol Agent of Paracoccus marginatus Williams and Granara de Willink (Hemiptera: Pseudococcidae) in Barbados by Y. Colmenarez, C.F. Wilcken, I. Gibbs and L.W. De Chi …………………
313
Poster 34: Economic Impact of Biological Control of Mango-infesting Fruit Flies: A Case Study of Kenya by B.W. Muriithi, S.A. Mohamed and S. Ekesi ………………….... 317
Poster 35: ‘Nothing Kills Insects’, or How Public and Farmer Perceptions Affect Success Rates of Biological Control by K.A.G. Wyckhuys, J. Bentley, M. Fredrix and R. Lie
320
Poster 36: Evolution and Potential Non-target Effect of the Introduced Biological Control Agent Cryptolaemus montrouzieri by H.S. Li ……………………………….. 323
Poster 37: Bioassay and Scanning Electron Microscopic Observations Reveal High Virulence of Entomopathogenic Fungus, on the Onion Maggot by Z. Lei, H. Wang, S. Wu, L. Li and H. Zhang………………………………………………………………….. 324
Poster 38: Cattle Fever Tick, Rhipicephalus annulatus (Acari: Ixodidae), and the Quest for Discovery of Its Natural Enemies in the Balkan Region by J. Kashefi, S. Demir, J. Goolsby, L. Smith and A. Chaskopoulou ……………………………………... 327
PREFACE
The 5th International Symposium on Biological Control of Arthropods, held in Langkawi –Malaysia, continues the series of international symposia on the biological control of arthropods organized every four years. The first meeting was in Honolulu, Hawaii – USA during January 2002, followed by the Davos - Switzerland meeting during September 2005, the Christchurch – New Zealand meeting during February 2009, and the Pucón – Chile meeting during March 2013. The goal of these symposia is to create a forum where biological control researchers and practitioners can meet and exchange information, to promote discussions of up to date issues affecting biological control, particularly pertaining the use of parasitoids and predators as biological control agents. This includes all approaches to biological control: conservation, augmentation, and importation of natural enemy species for the control of arthropod targets, as well as other transversal issues related to its implementation.
To this end, 14 sessions have been organized in order to address the most relevant and current topics in the field of biological control of arthropods, delivered by invited speakers, contributed talks and poster presentations. Some of these topics have remained as important issues since the first meeting, for example, the understanding of non-target impacts in arthropod biological control and biological control as the cornerstone of successful integrated pest management programmes, underlined by an understanding of the compatability of biological control with pesticide applications. Since the beginning we have also talked about the importance of regulation and risk assessment methodology. This still remains an important topic, but today biological control practioners also need to be better prepared for implementing access and benefit sharing policies relevant for classical biological control practices. But also, as new tools and environmental concerns arise, some fresh interdisciplinary topics have emerged. These days the importance of ensuring that baseline data are in place is far better recognised in order to be able to assess the impact of biological control programmes. This is not only a cost-benefit anaylsis, it also looks at the socio-economic impact of biological control and the effect on livelihoods. In this context, it is also rather important to understand the uptake of existing biological control solutions in low and lower middle income countries in order to be able to formulate strategies to replace the use of highly hazardous pesticides through the use of biological control agents. Ecological questions also remain at the forefront of biological control research. Topics that are currently high on the agenda include understanding the role of native and exotic natural enemies, as well as the importance of pre- and post-genetics in biological control.
Another important goal of these meetings has been to be truly international, and this is why every conference so far has been organized in a different continent. This year we are holding the meeting in Asia for the first time ever and again we have around 150 participants from around the world. As a result, this meeting represents an opportunity for creating and expanding networks between researchers worldwide, in particular researchers from South-East Asia who have not been in the position to attend the preceding meetings. Thus we expect that the 5th International Symposium on Biological Control of Arthropods will be an important milestone in maintaining forward momentum with arthropod biological control research and practice. In doing so, this will contribute towards improving the sustainability of managed systems and protecting biodiversity on the planet, thus contributing towards the Sustainable Development Goals (Transforming our world: the 2030 Agenda for Sustainable Development).
ACKNOWLEDGEMENTS
We are very grateful to the following individuals for their help in organizing ISBCA 5.
SCIENTIFIC
SESSION
ORGANIZING COMMITTEE MEMBERS
Session 1: Donald C. Weber (USDA-ARS, USA and Tim Haye (CABI, SWITZERLAND). Session 2: Richard Stouthamer (University of California – Riverside, USA) and Stephen L. Goldson (AgResearch Limited, NEW ZEALAND). Session 3: Roy G. Van Driesche (University of Massachusetts, USA) and Mark S. Hoddle (University of California –Riverside, USA). Session 4: Peter G. Mason (Agriculture and Agri-Food, CANADA) and Barbara I.P. Barratt (AgResearch Limited, NEW ZEALAND). Session 5: Tania Zaviezo (Universidad Católica de Chile, CHILE) and Audrey A. Grez (University of Chile, CHILE). Session 6: Brett P. Hurley (University of Pretoria, SOUTH AFRICA) and Simon A. Lawson (University of Sunshine Coast, AUSTRALIA). Session 7: Yelitza Colmenarez (CABI, BRAZIL) and R. Srinivasan (World Vegetable Center, TAIWAN). Session 8: Hariet L. Hinz (CABI, SWITZERLAND) and George E. Heimpel (University of Minnesota, USA). Session 9: Kris A. G. Wyckhuys (International Center for Tropical Agriculture, VIETNAM) and Yanhui Lu (Chinese Academy of Agricultural Sciences, CHINA). Session 10: Mohamad Roff (MARDI, MALAYSIA) and Fang-Hao Wan (Chinese Academy of Agricultural Sciences, CHINA). Session 11: John E. Banks (California State University – Monterey Bay, USA). Session 12: Ulrich Kuhlmann (CABI, SWITZERLAND) and Matthew J.W. Cock (CABI, UK). Session 13: Steve E. Naranjo (USDA – ARS, USA) and Jörg Romeis (Agroscope, SWITZERLAND). Session 14: Sunday Ekesi (International Center of Insect Physiology and Ecology, KENYA) and Wai Hong Loke (CABI, MALAYSIA).
SCIENTIFIC COMMITTEE
Members of the Scientific Committee are thanked for providing input into session themes and other aspects of the meeting. The Committee: Barbara I.P. Barratt (AgResearch Ltd., NEW ZEALAND), Jacques Brodeur (University of Montreal, CANADA), Mark S. Hoddle (University of California – Riverside, USA), Ulrich Kuhlmann (CABI, SWITZERLAND), Nick J. Mills (University of California – Berkeley, USA), Tania Zaviezo (Universidad Católica, CHILE) and Matthew J.W. Cock (CABI, UK).
REGIONAL ORGANIZERS
We thank Regional Organizers for coordinating ISBCA V advertising, soliciting interest in the conference, and for helping with local inquiries. Regional Coordinators included: EUROPE: Patrick De Clercq (Ghent University, BELGIUM). USA: Charles Pickett (California Department of Food and Agriculture, USA). CANADA: Peter G. Mason (Agriculture and Agri-Food Canada, CANADA); WEST AND CENTRAL AFRICA: Manuele Tamo (International Institute of Tropical Agriculture, BENIN). EAST AFRICA: Sunday Ekesi (International Centre of Insect Physiology and Ecology, KENYA). SOUTHERN AFRICA: Brett P. Hurley (Department of Zoology and Entomology, University of Pretoria, SOUTH AFRICA). AUSTRALIA AND NEW ZEALAND: Barbara I.P. Barratt (AgResearch Ltd., NEW ZEALAND). CHINA: Fang-Hao Wan (Chinese Academy of Agricultural Sciences, CHINA). INDIA: Malvika Chaudhary (CABI, INDIA). TAIWAN: R. Srinivasan (World Vegetable Center, TAIWAN). SOUTHEAST ASIA: A.
Sivapragasam (CABI, MALAYSIA). SOUTH AMERICA: Yelitza Colmenarez (CABI, BRAZIL).
LOCAL ORGANIZATION
COMMITTEE
Wai-Hong Loke (CABI, MALAYSIA), A. Sivapragasam (CABI, MALAYSIA), Dr. Mohamad Roff (MARDI, MALAYSIA) and John M. Chan (MEJUSTIF, MALAYSIA). Heike Kuhlmann, KCS Convention Service, for setting up the website, informational recourses and accounts, and to the proceedings editors Peter G. Mason, David R. Gillespie, Charles Vincent (Agriculture and Agri-Food Canada), for their diligent and thorough work.
CONFERENCE LOGO
Sarah Hillier (CABI, UK).
SPONSORSHIP
Ministry of Tourismn and Culture, Malaysia; Malaysia Convention and Exhibition Bureau (MyCEB); CAB International (CABI), Malaysian Agricultural Research and Development Institute (MARDI) and Agriculture and Agri-Food Canada (AAFC).
Session 1: Accidental Introductions of Biocontrol Agents: Positive and Negative Aspects
Donald C. WEBER
USDA-ARS, Beltsville, Maryland, USA
Tim HAYE
CABI, Delémont, SWITZERLAND
1.1 Accidental Introductions of Natural Enemies: Causes and Implications
D.C. Weber1, A.E. Hajek2 and K.A. Hoelmer3
1United States Department of Agriculture – Agricultural Research Service, Newark, Beltsville, Maryland, USA, don.weber@ars.usda.gov, 2Department of Entomology, Cornell University, Ithaca, New York, USA, aeh4@cornell.edu, 3United States Department of Agriculture – Agricultural Research Service, Newark, Delaware, USA, kim.hoelmer@ars.usda.gov
Accidental introductions of natural enemies, including parasitoid and predatory groups, may exceed species introduced intentionally. Several factors favor this: a general surge in international trade; lack of surveillance for species that are not associated with live plants or animals; inability to intercept tiny organisms such as parasitoids; huge invasive host populations in source and/or receiving areas that allow rapid establishment; and lack of aggressive screening for pests already established. Recent frequent and surprisingly rapid accidental natural enemy introductions call into question the regulatory emphasis on a rigorous and protracted process for classical biological control (CBC) introductions, when adventives have a high probability to displace or disrupt this planned process. We provide an overview with three brief case studies.
The volume of global international trade is staggering, and it continues to increase. International shipping moves 127 million containers (TEUs, each ~40m³ in volume and weighing ~14 tonnes) per year between countries, the majority between continents, for a total of ~5 billion m³ of freight (2014 totals; World Shipping Council, 2017). About 4x this amount moves domestically in coastal shipping. Additionally, 3.2 billion passenger trips take place by air, and air freight amounts to ~185 million tonnes (about 1/50th of the weight shipped by boat, but delivered in <1 day) (2014 totals; World Bank, 2017). A single adult parasitoid weighs about 1 mg (Harvey et al., 2006), or approximately 70 parts per trillion of a single shipping container – less than a needle in a haystack – and 350,000 such haystacks arrive from foreign ports worldwide per day!
Given this massive exchange of merchandise, invading natural enemies are of low to vanishing priority for national authorities inspecting imports for harmful organisms and other threats. Primary concerns are plant and animal pests and pathogens that will do the most serious and immediate damage, not to mention a host of other non-biological concerns such as terrorism, hazardous substances, and material that is illegal, smuggled, and/or counterfeit. In the US Department of Agriculture, the very name APHIS PPQ (Animal and Plant Health Inspection Service, Plant Protection and Quarantine) reflects these priorities, and, aside from known plant and animal pests and pathogens, and their associated carriers, very little else attracts the attention of border patrol inspectors.
Reece Sailer, in a prescient perspective, estimated the number of “beneficial immigrant species” to the US, determining that nearly half (134 of 287=47%) had been accidentally introduced (numbers from his Figure 6, not his text). “As an entomologist specialized in
introduction of beneficial insects, I find it disconcerting...” (Sailer, 1978). He cited as “valuable” many of the accidentally-introduced species such as San Jose scale parasitoid, Prospaltella perniciosi Tower (Hymenoptera: Aphelinidae), and the alfalfa leafcutter bee, Megachile rotundata (F.) (Hymenoptera: Megachilidae). A few years later, Sailer (1983) provided a breakdown of the 232 alien “beneficial Hymenoptera,” of which 82 (35%) had arrived accidentally; of the remaining 150, 10 had entered the US from Canada after being introduced intentionally there, and the remainder were intentionally introduced to the US by USDA and University of California scientists.
Roy et al. (2011) provide a very thorough recent analysis for alien arthropod predators and parasitoids, based on the DAISIE database for European alien species. Of the estimated 1590 species of arthropods introduced to Europe, 513 (32%) are predatory or parasitic. Of these, 66% were introduced unintentionally. This survey includes a number of groups that would never be considered for CBC introductions, e.g., ticks, fleas, spiders, and social Hymenoptera. Of the parasitoid Hymenoptera, 60 (28%) of the 212 recorded alien species were accidental (unintentional) introductions (Roy et al., 2011-Table 1).
From these two assessements, widely separated in space and time, at least one-third of alien natural enemy species appear to have been introduced accidentally. This is probably an underestimate, given the paucity of knowledge of these faunal groups. Furthermore, the proportion of accidentally introduced species has increased recently, as the number of intentional introductions has decreased, due to more stringent criteria for CBC introductions (Roy et al., 2011-Fig. 3; Hajek et al., 2016a).
Several major invasive pests have been associated with accidental introductions of their natural enemies, with varying outcomes, some still unclear. Below is a brief overview of three examples: gypsy moth, brown marmorated stink bug, and kudzu bug.
Since its discovery in northern Georgia (USA) in 2009, kudzu bug, Megacopta cribraria (F.) (Hemiptera: Plataspidae), has been considered a very serious threat to the US soybean, Glycine max (L.) Merrill (Fabaceae) crop. Overwintering on kudzu, Pueraria montana var. lobata (Willdenow) Maesen & S.M. Almeida ex Sanjappa & Predeep (Fabaceae), an invasive woody vine native to Asia, it colonized soy crops and reached very high densities (Gardner et al., 2013) which were very damaging to yields, unless pesticides were applied. In 2013, the scelionid Paratelenomus saccharalis (Dodd) (Hymenoptera: Scelionidae) was detected in northern Georgia, and the next year, in 4 additional states (Gardner and Olson, 2016). The origin is unknown and is presumed accidental (Gardner et al., 2013). A CBC assessment for P. saccharalis was underway in quarantine at the time of appearance of this adventive population, which was shown to be distinct from the quarantine rearings (W. Jones, personal communication). Meanwhile, as early as 2010 (Ruberson et al., 2013), the cosmopolitan generalist fungal entomopathogen, Beauveria bassiana (Balsamo-Crivelli) Vuillemin (Clavicipitaceae) was noted as attacking kudzu bug, and in 2015, many locations had outbreaks of this pathogen. The pathogen, possibly complemented by P. saccharalis, is thought to have caused greatly reduced regional kudzu bug populations (Gardner and Olson, 2016; Blount et al., 2017). It remains to be seen if kudzu bug is vanquished or will rise again in North America.
A second example of a scelionid egg parasitoid accidental introduction is covered in detail by Hoelmer et al. (this volume, 1.3). Nearly twenty years after the introduction and spread of the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America, the Asian scelionid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) oviposited in three sentinel BMSB egg masses in Maryland, USA (Talamas et al., 2015), and has since been detected in several other eastern and western USA. Bon et al. (this volume, 2.6) document at least 3 separate lineages,
corresponding to separate accidental introductions of T. japonicus into North America. None of these match with cultures held in quarantine for study under a CBC program. Native parasitism has been sporadic and mostly low (Hoelmer et al, this volume). However, population declines have been noted in BMSB rearings and in the field, and some of these may be due to a newly-discovered microsporidian, native to North America and pre-dating the introduction of BMSB (Hajek et al., in review). Once again, the plot thickens!
Classical biological control using pathogens (including nematodes) has been infrequently practiced, relative to arthropod CBC introductions. Worldwide, only 70 pathogen species have been introduced for CBC, with a correspondingly low number of 7 species accidentally introduced (Hajek et al., 2016b). However, two of these accidental introductions have played a large role in biological control of invasive gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae) populations in northeastern USA. The first was the introduction of Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV), thought to have been introduced in the early 20th century with parasitoids or plant material, as part of an extended and extensive arthropod CBC effort. During most of the 20th century, this virus, which was later mass-produced and formulated for application by the USDA Forest Service and APHIS, caused epizootics in high-density defoliating gypsy moth populations, resulting in rapid population crashes, and spreading naturally with the host population (Hajek and Tobin, 2011).
The source of the second introduction was initially surrounded by some uncertainty (Hajek et al., 1995). The source of this pathogen was addressed using molecular techniques as well as historical data (Nielsen et al., 2005; Weseloh, 1998) that showed with near certainty that this was an accidental introduction. In 1989, Entomophaga maimaiga Humber, Shimazu & Soper (Entomophthorales: Entomophthoraceae) was found in 7 states of the northeastern US. Within 5 years, this fungus had spread to all contiguous states infested by gypsy moth, and host populations in many areas have remained low for most years since. Although released intentionally in 1910-1911, there was no evidence that it established then, and there were many favorable chances to observe the effects of the pathogen in the US between 1911 and 1989 (Hajek et al., 1995; Weseloh, 1998). Another effort resulted in releases in 1985 and 1986, but these were shown to be a different strain and were geographically distant from the 1989 epizootics when E. maimaiga was first found in the US (Nielsen et al., 2005).
With the increased focus on guarding against nontarget effects of CBC comes the cost of delay and reduction in number of projects carried out (Hajek et al., 2016a). While this may in some cases prevent negative ecological consequences, criticisms of long-past classical biological control mistakes are today largely misplaced. Calls for more regulation and involvement of all stakeholders (e.g., Blossy, 2016) set up the perfect as the enemy of the good. Practical CBC should strike a balance to solve problems as much as it should seek to avoid creating new problems. With increased delay, perhaps CBC agents and plans may be optimized over more time, and native natural enemies may adapt or intersect with the targeted invasive pest in the interim. More certain though, is the prospect of prolonged and even irreversible ecological and economic disruption from pest damage, pesticide applications, and lost ecological services. Along with delay comes the prospect that accidental introductions of potentially suboptimal natural enemies occur, removing the chance to address pest invasions in a timely manner through best scientific practices.
References
Blossey, B. (2016) The future of biological control: a proposal for fundamental reform. In: Van Driesche, R., Simberloff, D., Blossey, B., Causton, C., Hoddle, M.S., Marks, C.O., Heinz, K.M., Wagner, D.L. and Warner, K.D. (eds.), Integrating Biological Control Into Conservation Practice, John Wiley and Sons Limited, Hoboken, New Jersey, USA, pp. 314–328.
Blount, J.L., Roberts, P.M., Toews, M.D., Gardner, W.A., Buntin, G.D., Davis, J.W. and All, J. N. (2017) Seasonal population dynamics of Megacopta cribraria (Hemiptera: Plataspidae) in kudzu and soybean, and implication for insecticidal management in soybean. Journal of Economic Entomology, 110, 157–167.
Gardner, W.A., Blount, J.L., Golec, J.R., Jones, W.A., Hu, X.P., Talamas, E.J., Evans, R.M., Dong, X., Ray, C.H. Jr., Buntin, G.D., Gerardo, N.M. and Couret, J. (2013) Discovery of Paratelenomus saccharalis (Dodd), an egg parasitoid of Megacopta cribraria F. in its expanded North American range. Journal of Entomological Science, 48, 355–359.
Gardner, W. and Olson, D.M. (2016) Population census of Megacopta cribraria (Hemiptera: Plataspidae) in kudzu in Georgia, USA, 2013–2016. Journal of Entomological Science, 51, 325–328.
Hajek, A.E., Hurley, B.P., Kenis, M., Garnas, J.R., Bush, S.J., Wingfield, M.J., van Lenteren, J.C. and Cock, M.J.W. (2016a) Exotic biological control agents: A solution or contribution to arthropod invasions? Biological Invasions, 18, 953–969.
Hajek, A.E., Gardescu, S. and Delalibera Júnior, I. (2016b) Classical Biological Control of Insects and Mites: A Worldwide Catalogue of Pathogen and Nematode Introductions. US Forest Service, Forest Health Technology Enterprise Team , USDA Forest Service, Morgantown, West Virginia, USA, FHTET-2016-06.
Hajek, A.E., Humber, R.A. and Elkinton, J.S. (1995) Mysterious origin of Entomophaga maimaiga in North America. American Entomologist, 41, 31–42.
Hajek, A.E. and Tobin, P.C. (2011) Introduced pathogens follow the invasion front of a spreading alien host. Journal of Animal Ecology, 80, 1217–1226.
Harvey, J.A., Vet, L.E., Witjes, L.M. and Bezemer, T.M. (2006) Remarkable similarity in body mass of a secondary hyperparasitoid Lysibia nana and its primary parasitoid host Cotesia glomerata emerging from cocoons of comparable size. Archives of Insect Biochemistry and Physiology, 61, 170–183.
Nielsen, C., Milgroom, M.G. and Hajek, A.E. (2005) Genetic diversity in the gypsy moth fungal pathogen Entomophaga maimaiga from founder populations in North America and source populations in Asia. Mycological Research, 109, 941–950.
Roy, H.E., Roy, D.B. and Roques, A. (2011) Inventory of terrestrial alien arthropod predators and parasites established in Europe. BioControl, 56, 477–504.
Ruberson JR, Takasu K, Buntin, G.D., Eger, J.E. Jr., Gardner, W.A., Greene, J.K., Jenkins, T.M., Jones, W.A., Olson, D.M., Roberts, P.M., Suiter, D.R. and Toews, M.D. (2013) From Asian curiosity to eruptive American pest: Megacopta cribraria and prospects for its biological control. Applied Entomology and Zoology, 48, 3–13.
Sailer, R. (1978) Our immigrant insect fauna. Bulletin, Entomological Society of America, 24, 3–11. Sailer, R. (1983) History of insect introductions. In C.L. Wilson and C.L. Graham (eds.) Exotic Plant Pests and North American Agriculture. Academic Press, New York, USA, pp.15–38.
Talamas, E.J., Herlihy, M.V., Dieckhoff, C., Hoelmer, K.A., Buffington, M.L., Bon, M.-C. and Weber, D.C. (2015) Trissolcus japonicus (Ashmead) emerges in North America. Journal of Hymenoptera Research, 43, 119–128.
Weseloh R.M. (1998) Possibility for recent origin of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in North America. Environmental Entomology, 27, 171–177.
World Bank (2017) Container port traffic and air transport. Available at: www.data.worldbank.org/indicator/IS.SHP.GOOD.TU (accessed 7 July 2017).
World Shipping Council (2017) About the industry: global trade. Available at: www.worldshipping.org/about-the-industry/global-trade/trade-statistics (accessed 7 July 2017).
1.2 Risks and Benefits of Accidental Introductions of Biological Control Agents in Canada
P.G. Mason1, O.O. Olfert2, T. Haye3, T.D. Gariepy4, P.K. Abram5 and D.R. Gillespie5
1Agriculture and Agri-Food Canada, Ottawa, Ontario, CANADA, Peter.Mason@agr.gc.ca, 2Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan, CANADA, Owen.Olfert@agr.gc.ca, 3CABI Switzerland, Delémont, Jura, SWITZERLAND, t.haye@cabi.org, 4Agriculture and Agri-Food Canada, London, Ontario, CANADA, Tara.Gariepy@agr.gc.ca, 5Agriculture and Agri-Food Canada, Agassiz, British Columbia, CANADA, Paul.Abram@canada.ca, gillespieroad@gmail.com
Introduction of natural enemies associated with invasive alien species is probably more common than conventional wisdom suggests. Such introductions are usually detected well after the host has established in new regions, sometimes even during or after host range studies have been initiated. In Canada, during the last 30 years, at least seven accidental introductions of natural enemies have occurred in arthropod pest systems (Table 1.2.1). Some introductions have resulted in unforeseen benefits to management of invasive alien species, but also pose potential risks to native biodiversity. Here we focus on two examples of accidental natural enemy introductions of arthropod pests that have had positive effects and potential risks.
Table 1.2.1. Accidental introductions of natural enemies associated with arthropod pests reported in agricultural systems in Canada during the last 30 years.
Agent
Euxestonotus error (Fitch)
Macroglenes penetrans (Kirby)
Synopeas myles (Walker)
Platygaster demades (Walker)
Trichomalus perfectus (Walker)
Mesopolobus gemellus Baur & Muller
Necremnus tidius (Walker)
Probable year of introduction
1800’s
Host
Sitodiplosis mosellana
1800’s [1954 MB; 1984 SK] Sitodiplosis mosellana
2000’s [2015 SK; 2016 ON] Contarinia nasturtii
2016 BC
2009 ON, QC
2007 ON, QC
1998 BC; 2003 AB, SK; 2007 ON, QC
Dasineura mali
Ceutorhynchus obstrictus
Ceutorhynchus obstrictus
Ceutorhynchus obstrictus
Macroglenes penetrans (Kirby) (Hymenoptera: Pteromalidae) is a key parasitoid that reduces populations of orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), in western Canada. First reported in the 1950’s after a wheat midge outbreak in Manitoba and later in the 1980’s after a major outbreak in Saskatchewan, conservation of M. penetrans has had economic and environmental benefits by reducing
pesticide use. Although formal host range studies have not been conducted, M. penetrans appears to be specific to wheat midge (Doane et al., 2013).
Management of wheat midge incorporates M. penetrans parasitism levels (25-46% in Saskatchewan, Doane et al., 2013) into models (Fig. 1.2.1) that provide growers with forecasts of potential crop damage during the growing season. Thus, the accidental introduction of M. penetrans has provided benefits through reduced input costs, fewer pesticides being applied, and adoption of practices that conserve natural enemies.
Fig. 1.2.1. Forecast models of wheat midge area infested before (left) and after (right) data where viable cocoons were reduced by Macroglenes penetrans to below economic threshold levels (<600/m2).
Trichomalus perfectus (Walker) (Hymenoptera: Pteromalidae) is an important parasitoid of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), in its native European range and was the focus of more than 15 years of intensive research to assess its potential as a biological control agent. Trichomalus perfectus attacks the larval stages of hosts that are concealed within developing siliques of Brassicaceae plants. Non-target species for testing potential impacts of candidate biological control agents were chosen using a multi-criteria selection method (Haye et al., 2015). Parasitism levels (host acceptance by parasitoids) varied among Ceutorhynchus spp. and feeding niche (Table 1.2.2). Of the 17 non-target species tested in no-choice laboratory experiments, parasitism by T. perfectus of four species was similar to that of the target host C. obstrictus. Parasitism of a further five species was lower than that of C. obstrictus, and six other species were not attacked at all. Ecological host range surveys in Europe corroborated the prediction that T. perfectus would attack C. cardariae at similar levels to C. obstrictus
In North America, T. perfectus was first discovered in 2009, attacking C. obstrictus in Quebec and Ontario and more recently, in a field population of the native weevil C. omissus, confirming the prediction that this species is a suitable host. Therefore, based on host range studies, accidental introduction of T. perfectus poses a medium to high risk to native Ceutorhychus spp., particularly those feeding in the siliques of Brassica plants.
Table 1.2.2. Risk of attack by Trichomalus perfectus females to non-target weevil species in Europe and North America based on percentage of non-target and target larvae accepted (parasitized) in small arena no-choice tests (host acceptance was compared using Fisher’s Exact Test, P< 0.05 (see Haye et al., 2015): high = ns; medium = P<0.05 – P<0.0001; low = P<0.0001; nil = not attacked).
Non-target hosts
Europe
Feeding niche
Risk of attack
Ceutorhynchus typhae (Herbst) seeds in silique medium
Ceutorhynchus constrictus (Marsham) seeds in silique medium
Ceutorhynchus turbatus Schultze seeds in silique high
Ceutorhynchus peyerimhoffi Hustache seeds in silique nil
Mogulones borraginis (Fabricius) seeds in nutlet nil
Ceutorhynchus sp. nr. nodipennis Dietz seeds in silique medium
Ceutorhynchus querceti (Gyllenhal) seeds in silique high
Mononychus vulpeculus (Fabricius) seeds in pod nil
Furthermore, C. constrictus and C. cardariae – which are candidates for introduction as biological control agents of weeds – are also at risk. Thus, although T. perfectus may be narrowly oligophagous, monitoring its impact on species at risk will be essential to refine predictions and develop new hypotheses with regards to risks associated with adventive introductions of arthropod biological control species.
Adventive introductions of biological control agents carry both benefits or risks. Understanding the host range of key natural enemies and monitoring them once they are present in the invaded region is essential in managing invasive alien species.
References
Doane, J.F., Olfert, O.O., Elliott, R.H., Hartley, S. and Meers, S. (2013) Sitodiplosis mosellana (Géhin), orange wheat blossom midge (Diptera: Cecidomyiidae). In: Mason, P.G. and Gillespie, D.R. (eds.) Biological control Programmes in Canada 2001–2012. CAB International, Wallingford, UK, pp. 272–276.
Haye, T., Mason, P.G., Gillespie, D.R., Miall, J.H., Gibson, G.A.P., Diaconu, A., Brauner, A.M. and Kuhlmann, U. (2015) Determining the host specificity of the biological control agent Trichomalus perfectus (Hymenoptera: Pteromalidae): the importance of ecological host range. Biocontrol Science and Technology, 25, 21–47.
1.3 Adventive vs. Planned Introductions of Trissolcus japonicus Against BMSB: An Emerging Case Study in Real-time
K.A.
Hoelmer1, D.C. Weber2 and T. Haye3
1United States Department of Agriculture – Agricultural Research Service, Newark, Delaware, USA, kim.hoelmer@ars.usda.gov, 2United States Department of Agriculture –Agricultural Research Service, Beltsville, Maryland, USA, don.weber@ars.usda.gov, 3CABI, Delémont, Jura, SWITZERLAND, t.haye@cabi.org
The invasive brown marmorated stink bug (BMSB), Halyomorpha halys Stål (Hemiptera: Pentatomidae), has been responsible for widespread damage to fruit, nut and vegetable crops since its establishment in North America and Europe in the past decade. Further spread to continents that are currently free of BMSB remains a serious risk (Kriticos et al., 2017). Although this insect can also be a pest in its native range in northeastern Asia, its severity appears to be less there than in the newly invaded regions (Lee et al., 2013), and natural enemies of BMSB in Asia are thought to be an important regulating factor. Abram et al., (2017) reviewed surveys for indigenous natural enemies that attack BMSB in the invaded regions, which show that parasitism and predation rates are typically too low to suppress BMSB. Several studies have suggested that these indigenous parasitoids are often physiologically incapable of overcoming host BMSB defenses (Abram et al., 2014, Haye et al., 2015). Successful egg parasitism in particular is much lower than in the native Asian range, suggesting that a classical biocontrol approach to manage this pest may be appropriate. The egg parasitoid Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) (also in literature as T. halyomorphae Yang; Yang et al., 2009; Talamas et al., 2013, 2015b) is a key natural enemy of BMSB in its native Asian range (Yang et al., 2009; Qui et al., 2010; Zhang et al., 2017). It has been under evaluation as a candidate biocontrol agent for introduction against BMSB into North America and elsewhere.
Trissolcus japonicus has been reared from several other pentatomid hosts in Asia besides BMSB (Zhang et al., 2015; Matsuo et al., 2016; Kim et al., 2017; Zhang et al., 2017). Laboratory host range testing conducted with no-choice tests in China showed that T. japonicus attacked and developed in most of the non-target Asian stink bug hosts tested (Zhang et al., 2017). Similar tests in the U.S. have shown that it will also attack a number of native American hosts, although there is a wide range of developmental success. Choice tests reveal preferences for BMSB in many, but not all, paired comparisons (Hedstrom et al., 2017, KAH unpublished data). Behavioral cues result in additional host selectivity during the process of searching for hosts (Hedstrom et al., 2017).
Recently, several adventive populations of T. japonicus were discovered in North America, on the U.S. east coast in 2014 (Talamas et al., 2015a; Herlihy et al., 2016), on the west coast in 2015 (Hedstrom et al., 2017; Milnes et al., 2016), and in 2016, a second population in the northeastern U.S. (Fig. 1.3.1). All three populations are genetically distinct (M.C. Bon, unpublished data). It is not known how they arrived in North America
Session 1: Adventive vs. Planned Introductions of Trissolcus japonicus – K. Hoelmer et al. (2017)
but they have established and are expanding their range. Their establishment will allow researchers the valuable opportunity to simultaneously: (1) assess the capacity of T. japonicus to impact BMSB populations in an invaded range, (2) determine the host and habitat preferences and fidelity of T. japonicus under natural conditions and contrast field results with laboratory evaluations, and (3) study how this introduced parasitoid will interact with resident parasitoids and influence trophic webs.
Fig. 1.3.1. Documented field occurrence of adventive Trissolcus japonicus in North America (as of December 2016).
References
Abram, P.K., Gariepy, T.D., Boivin, G. and Brodeur, J. (2014) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biological Invasions, 16, 1387–1395.
Abram, P.K., Hoelmer, K.A., Acebes-Doria, A., Andrews, H., Beers, E.H., Bergh, J.C., Bessin, R., Biddinger, D., Botch, P., Buffington, M.L., et al. (2017) Review of indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. Journal of Pest Science, doi 10.1007/s10340-017-0891-7.
Haye, T., Fischer, S., Zhang, J. and Gariepy, T. (2015) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe?
Journal of Pest Science, 88, 693–705.
Hedstrom, C., Lowenstein, D., Andrews, H., Bai, B. and Wiman, N. (2017) Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon.
Journal of Pest Science, doi 10.1007/s10340-017-0892-6.
Herlihy, M.V., Talamas, E.J. and Weber, D.C. (2016) Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS ONE, 11, e0150275. doi:10.1371/journal.pone.0150275
Kim, K-Y., Choi, D-S., Choi, J-Y. and Hong, K-J. (2017) Host records of Trissolcus (Hymenoptera: Platygasteridae: Telenominae) parasitizing eggs of stink bugs in Korea. Korean Journal of Applied Entomology, 56, 87–92.
Kriticos, D.J., Kean, J.M., Phillips, C.B., Senay, S.D., Acosta, H. and Haye, T. (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. Journal of Pest Science, doi:10.1007/s10340-017-0869-5.
Lee, D.H., Short, B.D., Joseph, S.V., Bergh, J.C. and Leskey, T.C. (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environmental Entomology, 42, 627–641.
Matsuo, K., Honda, T., Itoyama, K., Toyama, M. and Hirose, Y. (2016) Discovery of three egg parasitoid species attacking the shield bug Glaucias subpunctatus (Hemiptera: Pentatomidae) Japanese Journal of Applied Entomology and Zoology, 60, 43–46.
Milnes, J.M., Wiman, N.G., Talamas, E.J., Brunner, J.F., Hoelmer, K.A., Buffington, M.L. and Beers, E.H. (2016) Discovery of an exotic egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål) in the Pacific Northwest. Proceedings of the Entomological Society of Washington, 118, 466–470.
Qiu, L.F. (2010) Natural enemy species of Halyomorpha halys and control effects of the parasitoids species in Beijing. Northern Horticulture [Beifang Yuanyi, in Chinese with English abstract] 9, 181–183.
Talamas, E.J, Buffington, M. and Hoelmer, K.A. (2013) New synonymy of Trissolcus halyomorphae Yang. Journal of Hymenoptera Research, 33, 113–117.
Talamas, E.J., Herlihy, M.V., Dieckhoff, C., Hoelmer, K.A., Buffington, M.L., Bon, M.C. and Weber, D.C. (2015a) Trissolcus japonicus (Ashmead) emerges in North America. Journal of Hymenoptera Research, 43, 119–128.
Talamas, E.J., Johnson, N.F. and Buffington, M.L. (2015b) Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae). Journal of Hymenoptera Research, 43, 45–110.
Yang, Z-Q., Yao, Y-X., Qiu, L-F. and Li, Z-X. (2009) A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Annals of the Entomological Society of America, 102, 39–47.
Zhang, J-P., Zhang, F., Zhong, Y-Z., Yang, S-Y., Zhou, C-Q. and Zhang, Z-N. (2015) Biocontrol and research status of Halyomorpha halys (Stål). Chinese Journal of Biological Control, 31, 166–175.
Zhang, J-P., Zhang, F., Gariepy, T.D., Mason, P.G., Gillespie, D.R., Talamas, E.J. and Haye, T. (2017) Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. Journal of Pest Science, doi:10.1007/s10340-017-0863-y.
1.4 Can Native Parasitoids Benefit From Accidental Introductions of Exotic Biological Control Agents?
T. Haye1, J.K. Konopka2, T.D. Gariepy3, J.N. McNeil2, P.G. Mason4 and D.R. Gillespie5
1CABI Switzerland, Delémont, Jura, SWITZERLAND, t.haye@cabi.org, 2Department of Biology, Western University, London, Ontario, CANADA, jkonopk@uwo.ca, jmcneil2@uwo.ca, 3Agriculture and Agri-Food Canada, London, Ontario, CANADA, Tara.Gariepy@agr.gc.ca, 4Agriculture and Agri-Food Canada, Ottawa, Ontario, CANADA, Peter.Mason@agr.gc.ca, 5Agriculture and Agri-Food Canada, Agassiz, British Columbia, CANADA, gillespieroad@gmail.com
Interspecific interactions between native and exotic parasitoids can impact community structure and are relevant not only from an ecological standpoint, but also from a biological control standpoint. A thorough understanding of these interactions is critical to estimate the range of potential direct and indirect effects, positive or negative, associated with the establishment of an exotic parasitoid, irrespective of whether its introduction was intentional or accidental.
Exotic pests can be exploited by native natural enemies (food source diversification and/or novel host); however, this exploitation is only adaptive for the native species if it results in enhanced survival and/or reproduction. In environments that have undergone rapid change, previously reliable cues for survival and reproductive success may no longer be associated with adaptive outcomes, resulting in an evolutionary trap that reduces the fitness and reproductive success of the native organism (Schlaepfer et al., 2002). If, for example, a native parasitoid accepts an invasive species as a host but fails to complete development, then the host becomes an evolutionary trap for the native species (Abram et al., 2014). This evolutionary trap could benefit native host species by reducing overall parasitoid numbers, and thus, parasitoid load in those host populations. However, phenotypic plasticity can permit escape from an evolutionary trap if the organism in question learns avoidance behaviour, undergoes morphological changes, or overcomes defensive barriers to development in the host (Berthon, 2015).
The potential occurrence of an evolutionary trap has been associated with the widespread establishment of the invasive pest, Halyomorpha halys Stål (Hemiptera: Pentatomidae), in Europe and North America. In invaded areas, H. halys eggs are readily attacked by native Scelionidae, but are unsuitable for parasitoid offspring development (Abram et al., 2014; Haye et al., 2015). To further increase the complexity of the current system, the exotic Asian parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is being considered for introduction as a classical biological control agent for H. halys in recently invaded countries, and has already been documented as an adventive introduction in the USA (Talamas et al., 2015).
Another random document with no related content on Scribd:
solved, for I saw from Doctor Feng’s manner that he knew the truth, and would at last disclose it.
When at last the hour passed and we returned to the Beau Site, Thelma took me up in the lift to a comfortable private suite where, in the sitting-room, Feng was standing before the window which gave a wide view of the Mediterranean, calm in the amber glow of late afternoon.
“Let us sit down,” he said, and I noticed how much more marked his slight American accent had become. “What I have to tell you, Yelverton, will take some little time. It will surprise you too, for it is a remarkable and complicated story—an amazing hotchpotch of love, hate, avarice, and a callous, cruel cunning perfectly devilish. I may as well begin at the beginning.”
I took an easy chair and the old man went on with his strange history.
“First of all,” he said, “it is necessary to go back to the days when Thelma’s father was alive and on the China station. You will remember I told you he was able to render a very great service to Sung-tchun, who was one of the leaders of the Thu-tseng. Exactly what that service was we shall never know—the secret would involve too many men who are still alive.
“But whatever it was, it was very important—very much more than a mere matter of organizing the escape of Sung-tchun from Siberia. That, of course, was important, but, after all, it was only a matter of one man’s life. There must have been something far greater, of which we shall probably never learn.
“Do you remember my once saying to you that the arm of the Thutseng was long?”
I nodded. I remembered perfectly the old chap’s grave look as he spoke the words. I had little suspected their tremendous import.
“Well,” Feng continued, “you and Thelma have to thank the Crystal Claw for the fact that you are alive today. Had I not been at Mürren when it arrived, had I not know its significance, the devilish plot planned by Humphreys must have succeeded.
“I did not know when I arrived at Mürren any of the facts that soon after came into my possession. That I should have been there was one of the wonderful instances of the working of Providence.
“The arrival of the Crystal Claw fairly staggered me. Never before has it been bestowed upon a European. I knew at once that around Mrs. Audley some tremendous story must hang. I am not unknown in the Thu-tseng and I determined to get at the truth. What I learned in reply to my cables both surprised and alarmed me. It showed me that Mrs. Audley was in terrible danger. It put me at once on my guard with reference to Hartley Humphreys. From that time forward he was under almost incessant supervision.
“Now here are the essential facts. Sung-tchun was an extremely wealthy man—how wealthy no one exactly knew. He made a very remarkable will, in which he left the whole of his vast fortune to Miss Thelma Shaylor.”
Thelma started violently. “Left a fortune to me!” she burst out. “Why I never heard a word about it.”
“No,” said Feng, “there was a proviso in the will that except for some grave reason, of which the trustees were to be the judges, you were not to be told until you reached the age of twenty-one. Sung-tchun was anxious that you should not be exposed to the advances of mere fortune-hunters until you were old enough to have had a reasonable experience of the world.
“Now if the will had contained nothing else there would have been no difficulty: you would have been perfectly safe. Unfortunately Sungtchun added a codicil which was, as events proved, to bring you into terrible peril.
“That codicil provided that if you died childless the vast bulk of Sungtchun’s wealth should devolve upon a Chinese named Chi-ho who was living in New York. Now here is a crucial fact. Chi-ho was hopelessly in the power of Hartley Humphreys.
“Humphreys learned of the provisions of Sung-tchun’s will. He had lived in China; he knew the country well and he was very wealthy. By the treachery of an official of the Thu-tseng he learned of that fatal
codicil. It was an amazing instance of leakage of information for which the history of the Thu-tseng knows no parallel and the offender has expiated his crime by the forfeit of his life.
“Chi-ho probably never realized the vastness of the sum to which he would be entitled if Thelma died childless. Humphreys, no doubt, only told him part of the truth. Chi-ho, in consideration of getting his freedom from Humphreys made over to the latter, in strictly legal form, all his interests under the will of Sung-tchun. That document was found among Humphreys’ papers after his death, of which Thelma has already told you.
“Very soon after that document was signed Chi-ho died—stabbed to death in what was said to be a tong feud in the Chinatown district of New York. I cannot say with certainty that the whole thing was arranged by Hartley Humphreys but Chi-ho’s death was very convenient to him.
“Now you have this interesting position: only Thelma’s life stood between Hartley Humphreys and the Sung-tchun fortune.
“All these facts came to me by cable—in code, of course, from Canton. I did not think it necessary or desirable to tell you and of course I had no permission to reveal the fact that Thelma was a great heiress. But I was keenly on the watch. My Canton correspondent warned me very specifically to beware of Hartley Humphreys, whose secret record in China—outwardly he was of the highest respectability—was appalling. And the Thu-tseng knew all there was to know about him.
“That will explain to you, Yelverton, Humphreys’ alarm when he saw the Crystal Claw. He knew it might mean anything—for instance that Thelma was being watched over and guarded by the agents of the most powerful secret society in the world. If that were the case, he knew, a single false step would mean his certain ruin—perhaps even his death.”
“You didn’t seem much concerned about his alarm when I told you,” I interrupted.
“No,” said the doctor with a smile, “it wasn’t necessary I should not have been surprised if the sight of the Crystal Claw had frightened him off his scheme. But his avarice was evidently so unbounded that he was willing to run any risk for the sake of money.
“Now comes a curious part of the story that I think Mrs. Audley had better tell herself.” He turned to Thelma. “Please tell Mr. Yelverton about your marriage,” he said.
“Well,” said Thelma, hesitatingly. “I was introduced to Stanley Audley at a dance at Harrogate. He was an electrical engineer and was apparently also possessed of considerable means. We met frequently. Twice I had tea at his rooms in London and one day at the Savoy he introduced me to Harold Ruthen who, I understood, was a newly formed acquaintance of his.
“Mother rather liked Stanley, who always spoke enthusiastically of his firm, Messrs. Gordon & Austin, the great electrical supply company, and of his eagerness for advancement. When we became engaged mother raised no objection, for he was so keen and enthusiastic in everything. One day he motored me down to a place called ‘Crowmarsh,’ near Wallingford, where I found he possessed a fine old-world house, where we were to live when we married. I was charmed with it and we both spent a glorious day there. Three weeks later we were, as you know, quietly married at St. James’ church in Piccadilly, and went at once out to Switzerland for our honeymoon, where we met you both.
“Then one morning Stanley received a telegram. When he read it he became both confused and alarmed. He did not show me the message, but told me that it was imperative that he should return to London at once. I now recollect that we were in the hall of the Kürhaus when the concierge handed him the message, and seated in his invalid chair, near the big stove on the right, was old Mr. Humphreys, whom I did not then know, but who was no doubt watching us intently.”
“He had followed you to Mürren with a very definite object,” Feng went on. “He must have been watching you for some months
beforehand, and I have no doubt your sudden marriage was a severe blow to his plans.
“I had serious difficulty in making friends with him. Of course he knew I was a Chinese and I really believe that he suspected at first that I was an agent of the Thu-tseng. It was only when he found that I had been at Mürren some time before Thelma and Audley arrived— and therefore, he thought, could not be specially interested in them —that I succeeded in getting inside his guard. Of course, by posing as his friend, I was able much more easily to keep track of his movements.
“Do you remember your escape from the avalanche?”
“Rather!” said Thelma and I simultaneously.
“Perhaps you will be surprised to learn that that avalanche was not the unaided work of Nature,” said the doctor “You did not notice a man some hundreds of feet above you?”
“No,” I said, “but what do you mean?”
“It’s a very easy thing to start an avalanche,” said Feng with a smile. “There was a man above you that day and the avalanche was started deliberately. Your guide John found out the truth afterwards. But the would-be assassin—I have no doubt he was in the pay of Humphreys—was never traced and the matter was hushed up. It would not have done to let Humphreys know that the truth was suspected. As a matter of fact I did suspect it and implored John to investigate.
“But with regard to Stanley Audley I confess I was completely misled. When he received that telegram recalling him to London I believed that the story he had told you about his profession as electrical engineer, was a true one. Only when it was proved to be without foundation did I see that I, like yourself, had been cleverly bamboozled. Until then I had believed Audley to be what he represented himself to be. I never dreamed of the truth. Hartley Humphreys, a crook to his finger tips, possessed a master-mind, obsessed by criminality, and having no idea of my actual purpose he
acted with such amazing cunning and forethought that he must be placed among the list of the master-criminals of the world.”
“Of course I had no suspicion,” said Thelma. “I didn’t even know that I was an heiress.”
“And I was fool enough to think that Humphreys was my friend and you were my enemy, Doctor,” I said with some shame as I thought of how completely I had been deceived.
“Well,” laughed Feng, “that’s all over now. But I’m glad I was able to deceive you because it helped me to deceive Humphreys. He was quite aware of your feeling towards me. You are fairly transparent, Yelverton, if you don’t mind my saying so!”
“The position was very extraordinary. Humphreys got Audley out of the way—I will explain that later—and that, he thought, would leave Thelma unprotected. But he never expected your interest in the bride. You became a very unwelcome bit of grit in a very well-oiled machine. You were constantly with Thelma, she was never left alone for a moment—and you were in the way.”
And the shrewd old man smiled mysteriously.
CHAPTER XXII
THE SECRET DISCLOSED
“B what was the mystery of Audley’s disappearance?” I asked Feng, in breathless eagerness, now that the enigma was in course of solution.
“Well, Humphreys at first did his level best to prevent the marriage, but finding that impossible he went very cleverly to work. Audley, who was a young man of means—though he pretended that his profession was that of electrical engineer—had, Humphreys discovered, fallen into the hands of a man named Graydon, a friend of his, who lived in the same house as Audley and who was one of a gang of note forgers.
“By clever means this gang had used Audley for their own purposes, even to the extent of sometimes inducing him to assume Graydon’s identity. Harold Ruthen was one of Graydon’s accomplices in passing spurious notes, hence old Humphreys knew of Audley’s connection with the forgers. After Thelma’s marriage which he had tried in vain to prevent, it was highly necessary for the furtherance of Humphreys’ sinister plan, to get her husband away. He therefore caused to be sent to him at Mürren a veiled message that the police were making inquiries in London and that he had better at once efface himself, even from his wife. This he did, leaving Thelma in your care.”
“But was Stanley really a forger?” I asked.
“At first I thought so, but later I found that the poor fellow had acted in all innocence. He was being blackmailed by the gang and thus forced to assist them, until he received that warning and fled,” replied Feng. “I was all the time watching the very deep game played by the wily old crook who posed as an invalid. With Audley out of the way he expected that it would be easy to complete his plans. Instead, to
his great chagrin, you came forward as the bride’s companion and protector. It was then that he determined, if you still continued to watch over the girl, from whose husband he had contrived to part her, that your activities should be suppressed. It then became my active duty to keep guard over both of you, which I did to the best of my ability.
“It was, of course, a difficult task. Had he been in New York you would both have been watched night and day by men of the Thutseng. The Chinese make the finest ‘shadowers’ in the world and in New York they are so very numerous that I could employ them with impunity. In London they are too conspicuous. It was really through this that Humphreys nearly beat me at the finish.
“But I will give you an instance of how narrowly you escaped. Do you remember one night when we all had supper with Humphreys at a Chinese restaurant near Piccadilly Circus?”
“Yes,” I nodded.
“And you remember that I signalled to you not to eat the cold soup that was served?”
“Yes,” I replied. “I thought you meant it was something I should not like.”
“You would have been dead in five days if you had eaten it,” said Feng grimly. “It was by a miracle of luck that I saw Humphreys drop into it a tiny pellet as he reached his hand out for some bread. The Chinese waiter took your soup away. Humphreys did not notice the Chinese remark I made to the waiter, but that soup was preserved and analyzed. It contained a virulent culture of the germs of typhoid fever. The Chinese waiter, of course, was an agent of the Thu-tseng. I daresay you will meet him some day. He happens to be a doctor and a great friend of mine. He analyzed the soup for me. If you had taken a spoonful of it while Humphreys was telling the funny stories at which you were laughing, you would have been dead in five days —of perfectly natural causes.”
“But, Thelma. Did you know anything of all this?” I asked turning to her, astounded and muddled.
“Some of the facts I knew, but not all,” she replied. “I hope you will forgive me, but I acted all along upon Doctor Feng’s instructions. At Mürren I knew nothing, and was entirely unsuspicious of the plot against us both.”
“Humphreys had degenerated into perhaps the cleverest financial crook in Eastern Europe,” said Feng. “The way in which he held Audley aloof from his wife while his friends Graydon and Ruthen were at the same time terrorizing him and compelling him to assist in passing their spurious notes, was a most remarkable feature of the case. He acted with such caution and pre-arranged things so cunningly, that I confess I was more than once misled and befogged.
“It was he who sent you those warnings from Hammersmith and North London in an endeavor to frighten you off. He certainly had a sort of superstitious fear of you. My chief fear for Thelma was that she might be secretly poisoned in a similar manner to the attempt upon yourself. Therefore I insisted that she should never take her meals in a restaurant alone.”
“And I was in ignorance,” I exclaimed.
“I deemed it best. I did not wish to alarm either of you, and indeed it is only since the narrow escape you both had at Heathermoor Gardens that I revealed to Thelma the motive of the plot. I did not suspect that terrible death-trap, but as soon as Thelma was missing I naturally felt that she must have fallen into the hands of one or other of the gang. Judge my surprise when I discovered that she surreptitiously, at Audley’s request, rejoined him in hiding at a small private hotel in Gloucester Road, Kensington. Audley was in constant dread of the police, an apprehension kept alive by Ruthen and Graydon, and for that reason he destroyed his clothes and some false notes before escaping from the room at Lancaster Gate. He turned the key from the outside, in order further to mystify those whom he believed to be his pursuers.”
“I was his pursuer,” I remarked.
“True. But he was avoiding you, as well as the police,” Feng said. “He was told that you were making inquiries concerning him on his
wife’s behalf and would, if you gained the truth, reveal it to her Naturally, he had no desire that Thelma should know that the police were wanting him upon grave charges of forgery.”
“But why did he not openly defy those men into whose hands he fell before his marriage?” I asked. “Surely, he could have cleared himself and have given information to the police.”
“Ah! Humphreys, the criminal with the master-mind took very good care that he was so deeply implicated that he dare not utter a word,” my friend pointed out. “Recollect his determination was that Thelma, alone and without friends except her mother, should meet with an untimely end in order that the Sung-tchun fortune should pass to him.
“First, however, she married unexpectedly, and, secondly, you came upon the scene as her protector. It was for that reason an attempt was first made to poison you, and then that clever plot at Stamford whereby you were drugged by that final cigarette given you by the supposed commercial traveler, who afterwards entered your room, forced against your lips a bottle containing a deadly drug, and made it appear as though you had committed suicide. Humphreys believed that you knew too much, so he intended that you should die before the girl over whom you were so carefully watching. He had no idea, however, of the part I was playing—until the police went to arrest him.”
“But could you not have told me the truth long ago—and given me warning?” I asked.
“That was impossible,” he replied. “Remember I warned you repeatedly. You would only have laughed had I told you Humphreys was your enemy: you were already deeply prejudiced against me. Thelma, too, tried to induce you to give the whole thing up, but you refused. Had Humphreys known that you suspected him he would have had you both murdered out of hand and chanced detection. But as things were he elected to wait until he could devise a plot that would be absolutely safe. So long as Stanley Audley was out of the way there was no need for him to do anything rash. And by his patience he nearly won in the end.”
“But he very nearly lost,” I said. “Suppose Thelma and I had been burnt to death. We could never have been identified and Humphreys could not have proved Thelma’s death. That meant he could not have inherited her fortune at any rate until sufficient time had elapsed for the Courts to presume her death.”
“You are a lawyer, Yelverton, and of course that point would occur to you. But it also occurred to Humphreys—another instance of his amazing foresight—and he took steps accordingly. Thelma, show Mr. Yelverton your locket.”
With a smile Thelma took from her pocket a heavy locket attached to a chain and handed it to me. I was astonished at its massiveness and weight, until I saw both locket and chain were of platinum. On the front of the locket was deeply engraved the inscription, “Thelma Audley—from Stanley.”
“Platinum; you see, Yelverton!” said old Feng. I gasped in astonishment at the realization of Humphreys’ cleverness.
“Of course,” I said, “it would resist the fire, the locket would be found in the débris and Thelma’s disappearance would be explained, in part at any rate.”
“Yes,” rejoined Feng, “the locket would account for Thelma and what more natural than the conclusion that the remains of the man found with her were those of her husband?”
“But what has become of Stanley?” I asked, wondering why Thelma was here without him.
“Stanley Audley is dead,” said Feng very gently, and I noticed the slow tears begin to trickle down Thelma’s face. “He died like a hero. It was he who rescued Thelma from the blazing room. By some extraordinary chance the fire seems to have spread mainly in your direction and Thelma escaped with the loss of most of her clothing and her hair which was almost burnt off. But poor Stanley was so terribly burned that he died three days later in the hospital. There is no doubt he loved Thelma deeply and utterly regretted the trouble he had brought upon her.”
Stanley Audley dead! I held my breath! Then Thelma was free! Such was my involuntary reflection.
Thelma was weeping softly I hardly dared look at her But I put out my hand and clasped hers. She turned her head away and gazed in silence at the golden glow in the west across the sea. But she did not withdraw her hand and a great wave of joy flooded through me.
“But how did we escape?” I asked Feng.
“We were only in the nick of time,” he replied. “When Thelma disappeared from her husband in Gloucester Road I felt certain that she had been decoyed away. She was—by a message purporting to come from her husband asking her to call at Heathermoor Gardens. She did so and fell into the hands of the man who intended she should die. Yet so clever was old Humphreys, that, though I kept him under close observation, I could not discern that he was acting at all suspiciously. I did not know of course, of his plot to burn you alive. But we were watching him very closely. That night Stanley and I tracked him to the house at Hampstead. We saw you arrive later, but we little dreamed that Thelma was held there a drugged and helpless prisoner. She screamed twice, apparently, and you heard her, but some accomplice of Humphreys’ gave her a hypodermic injection—we found the mark afterwards on her arm.
“We watched until the first man-servant came out and later Humphreys himself left the place and walking in some distance away concealed himself in full view of the house. Then I knew you were left in there, and I became seriously alarmed.
“Fortunately a constable was near, and unseen by the old villain I approached him, told him of my suspicions, and we all three approached the house together. To our rings and knocks there was no answer, therefore we forced the door and rushed in. As we opened the door of the room where you were, we saw the air-ball burst and in a second the room was a furnace.
“Then came a desperate fight for life. Audley dashed to Thelma and succeeded in getting her out into the street at the cost of his own life, while I and the constable cut the rope which secured your wrists, and
carried you out terribly burned and insensible. Both the constable and I were also burned, but not very seriously. Before the fire brigade arrived the house had been seriously damaged: but for our early warning it must have been utterly destroyed, as Humphreys intended.
“Meanwhile, Humphreys, who had seen the failure of his plot, made himself scarce and it was not until three days later that Inspector Cayley of Scotland Yard, with two sergeants traced him to a room in Earl’s Court Road, where he was hiding. But the old criminal had locked himself in and before they could break open the door he had put a bullet through his brain. A week ago both Ruthen and Graydon were arrested at the Pavilion Hotel in Boulogne on charges of passing spurious notes in various towns in France. They will, no doubt, go to hard labor for some years.”
“Well, Yelverton,” the old man concluded, “I think you know everything now. You have both had a very narrow escape from a terrible fate. Only a devil in human form could have devised such an atrocity. But now I’ll leave you alone for a bit: you will have plenty to talk about.”
And with a cheery smile and a loving look at Thelma, the sturdy, bearded old man, to whose watchfulness we both owed our lives, turned on his heel and left the room.
The calm Riviera sunset had deepened into twilight, swiftly as it always does, and the night clouds rising over the pine-clad Esterels cast their long grey shadows across the calm sea. Beneath our window twinkling lights shone and from among the orange graves below came voices and merry laughter.
I had been speaking earnestly to Thelma—pleading with her all the fervor of the love I had so long held in restraint but which, now she was free, poured out with violence that overwhelmed me. She heard me without comment or response. But she made no protest, she
allowed me to hold her hand, even when I pressed it tenderly to my lips she did not withdraw it.
The hope that had never quite died rose again in my heart. I felt Thelma trembling; a beautiful warmth that I had never seen before glowed upon her cheeks, her eyes were lustrous with the brilliancy of tears which welled up into them but did not fall. She stood looking out across the broad Mediterranean towards the African coast which the colors of the sunset paled into the faint splendor of the afterglow.
The light was nearly gone, and still she made no sign. But presently words failed me and I simply stood and held out my arms in a last despairing appeal.
Then my darling came to me, slowly and sweetly, her great grey eyes aflame with a light I had never seen before. And our lips met at last.
We were married in October and spent our honeymoon in Seville and Malaga. Christmas found us at the Hotel Regina at Wengen, a little below Mürren, where we both went skiing daily. We visited Mürren, of course, hallowed to us for all time as the place of that strange first meeting from which all our troubles and all our happiness had sprung.
We are rich, of course, Sung-tchun’s fortune was enormous. But we live very quietly in my old home—my father’s quaint, old-world cottage on the Salisbury road a few miles from Andover. Most of our income, apart from our own modest wants, goes to help the slum children of London. Thelma never tires of them and every summer forms a big camp to which hundreds come down for a few days’ glorious holiday. They all seem to worship her and over even the roughest of them she seems to exercise a magical fascination.
Old Doctor Feng, to whom we owe so much, is our chief friend. He comes and goes as he pleases. There is a room reserved for him and always ready. Devoted to Thelma, he spends much of his time
with us. He never tires of talking of the Crystal Claw, the magic talisman that saved us for each other. And every now and again, with his inimitable chuckle, he croaks out, “Yelverton, I told you the arm of the Thu-tseng was long!”
It was long indeed. It stretched half across the world to give us—two tiny units caught in a cruel trap—a helping hand in our dire distress. We owe our wealth, our radiant happiness, our very lives to the magical influence of the Crystal Claw.
THE END
TRANSCRIBER’S NOTES:
Obvious typographical errors have been corrected. Inconsistencies in hyphenation have been standardized.
Archaic or variant spelling has been retained.
***
END
OF THE PROJECT GUTENBERG EBOOK THE CRYSTAL CLAW
***
Updated editions will replace the previous one—the old editions will be renamed.
Creating the works from print editions not protected by U.S. copyright law means that no one owns a United States copyright in these works, so the Foundation (and you!) can copy and distribute it in the United States without permission and without paying copyright royalties. Special rules, set forth in the General Terms of Use part of this license, apply to copying and distributing Project Gutenberg™ electronic works to protect the PROJECT GUTENBERG™ concept and trademark. Project Gutenberg is a registered trademark, and may not be used if you charge for an eBook, except by following the terms of the trademark license, including paying royalties for use of the Project Gutenberg trademark. If you do not charge anything for copies of this eBook, complying with the trademark license is very easy. You may use this eBook for nearly any purpose such as creation of derivative works, reports, performances and research. Project Gutenberg eBooks may be modified and printed and given away—you may do practically ANYTHING in the United States with eBooks not protected by U.S. copyright law. Redistribution is subject to the trademark license, especially commercial redistribution.
START: FULL LICENSE
THE FULL PROJECT GUTENBERG LICENSE
PLEASE READ THIS BEFORE YOU DISTRIBUTE OR USE THIS WORK
To protect the Project Gutenberg™ mission of promoting the free distribution of electronic works, by using or distributing this work (or any other work associated in any way with the phrase “Project Gutenberg”), you agree to comply with all the terms of the Full Project Gutenberg™ License available with this file or online at www.gutenberg.org/license.
Section 1. General Terms of Use and Redistributing Project Gutenberg™ electronic works
1.A. By reading or using any part of this Project Gutenberg™ electronic work, you indicate that you have read, understand, agree to and accept all the terms of this license and intellectual property (trademark/copyright) agreement. If you do not agree to abide by all the terms of this agreement, you must cease using and return or destroy all copies of Project Gutenberg™ electronic works in your possession. If you paid a fee for obtaining a copy of or access to a Project Gutenberg™ electronic work and you do not agree to be bound by the terms of this agreement, you may obtain a refund from the person or entity to whom you paid the fee as set forth in paragraph 1.E.8.
1.B. “Project Gutenberg” is a registered trademark. It may only be used on or associated in any way with an electronic work by people who agree to be bound by the terms of this agreement. There are a few things that you can do with most Project Gutenberg™ electronic works even without complying with the full terms of this agreement. See paragraph 1.C below. There are a lot of things you can do with Project Gutenberg™ electronic works if you follow the terms of this agreement and help preserve free future access to Project Gutenberg™ electronic works. See paragraph 1.E below.
1.C. The Project Gutenberg Literary Archive Foundation (“the Foundation” or PGLAF), owns a compilation copyright in the collection of Project Gutenberg™ electronic works. Nearly all the individual works in the collection are in the public domain in the United States. If an individual work is unprotected by copyright law in the United States and you are located in the United States, we do not claim a right to prevent you from copying, distributing, performing, displaying or creating derivative works based on the work as long as all references to Project Gutenberg are removed. Of course, we hope that you will support the Project Gutenberg™ mission of promoting free access to electronic works by freely sharing Project Gutenberg™ works in compliance with the terms of this agreement for keeping the Project Gutenberg™ name associated with the work. You can easily comply with the terms of this agreement by keeping this work in the same format with its attached full Project Gutenberg™ License when you share it without charge with others.
1.D. The copyright laws of the place where you are located also govern what you can do with this work. Copyright laws in most countries are in a constant state of change. If you are outside the United States, check the laws of your country in addition to the terms of this agreement before downloading, copying, displaying, performing, distributing or creating derivative works based on this work or any other Project Gutenberg™ work. The Foundation makes no representations concerning the copyright status of any work in any country other than the United States.
1.E. Unless you have removed all references to Project Gutenberg:
1.E.1. The following sentence, with active links to, or other immediate access to, the full Project Gutenberg™ License must appear prominently whenever any copy of a Project Gutenberg™ work (any work on which the phrase “Project Gutenberg” appears, or with which the phrase “Project Gutenberg” is associated) is accessed, displayed, performed, viewed, copied or distributed:
