Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe?

Halyomorpha halys was accidentally introduced into Switzerland around 2004 and has recently spread to several additional areas in Europe, with established populations documented in France, Italy, Greece and Hungary. To test whether generalist egg parasitoids of European Pentatomidae have the potential to control H. halys, and whether these could be as effective as their related Asian species, sentinel egg masses of H. halys and six native European pentatomids were exposed in two regions of Switzerland. Freeze-killed sentinel egg masses of H. halys were attacked by the platygastrid Trissolcus cultratus and the eupelmid Anastatus bifasciatus, whereas fresh egg masses of native Pentatomidae occassionally yielded four Scelionidae species: Trissolcus semistriatus, T. scutellaris, T. cultratus and Telenomus chloropus. In no-choice tests, T. chloropus and T. semistratus produced no offspring from fresh H. halys eggs, whereas T. cultratus and T. scutellaris were sporadically able to complete development. Stopping embryogenesis by freezing egg masses of H. halys at -80 °C enabled T. cultratus and T. semistriatus to produce a high number of offspring without influencing the behaviour of the parasitoids. In contrast to European platygastrids, the Asian parasitoids Trissolcus japonicus and T. cultratus (Chinese strain) caused significantly higher parasitism of fresh H. halys eggs. Differences in developmental success may be related to less efficient venom of European scelionids injected during oviposition. To date, A. bifasciatus is the only potential candidate for augmentaive biological control of H. halys in Europe as it was the only European parasitoid capable of consistent, successful development on fresh H. halys eggs.

[1]  H. Godfray,et al.  Parasitoids: Behavioral and Evolutionary Ecology , 1993 .

[2]  P. Milonas,et al.  First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece , 2014 .

[3]  R. Guidetti,et al.  A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy , 2015, Journal of Pest Science.

[4]  F. J. Simmonds,et al.  A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or prey/Enemy. Volume I. Arachnida to Heteroptera. Volume II. Homoptera. Volume III. Coleoptera to Strepsiptera. , 1971 .

[5]  Lara Maistrello,et al.  Primi rinvenimenti in Italia della cimice esotica Halyomorpha halys, una nuova minaccia per la frutticoltura , 2014 .

[6]  W. Wu,et al.  The bionomics of Anastatus sp. and its utilization for the control of lichee stink bug. Tessaratoma papillosa Drury. , 1974 .

[7]  T. Haye,et al.  Recent range expansion of brown marmorated stink bug in Europe , 2014 .

[8]  M. Bon,et al.  Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America , 2015 .

[9]  S. Toepfer,et al.  Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe , 2004, BioControl.

[10]  Cultivation of teratocytes of the egg parasitoid telenomus heliothidis (hymenoptera: Scelionidae) , 1985, In Vitro Cellular & Developmental Biology.

[11]  S. Graff,et al.  First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. , 2011 .

[12]  A. Clarke.  The control of Nezara viridula L. with introduced egg parasitoids in Australia. A review of a 'landmark' example of classical biological control , 1990 .

[13]  M. Hoddle,et al.  Parasitoid Guilds of Agrilus Woodborers (Coleoptera: Buprestidae): Their Diversity and Potential for Use in Biological Control , 2012 .

[14]  S. A. Field.  Patch Exploitation, Patch‐leaving and Pre‐emptive Patch Defence in the Parasitoid Wasp Trissolcus basalis (Insecta: Scelionidae) , 2010 .

[15]  A. T. Drooz,et al.  North American egg parasite successfully controls a different host genus in South America. , 1977, Science.

[16]  T. Haye,et al.  Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland , 2013, Journal of Pest Science.

[17]  W. R. Thompson.  A catalogue of the parasites and predators of insect pests. Section 2. Host parasite catalogue. Part 1. Hosts of the Coleoptera and Diptera. , 1944 .

[18]  S. Vinson.  How parasitoids deal with the immune system of their host: An overview , 1990 .

[19]  Joanne Whalen,et al.  Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) , 2014 .

[20]  G. Boivin,et al.  Susceptibility of Halyomorpha halys (Hemiptera: Pentatomidae) eggs to different life stages of three generalist predators , 2014, The Canadian Entomologist.

[21]  E. Talamas,et al.  Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae) , 2015 .

[22]  H. Cornell,et al.  Accumulation of Native Parasitoid Species on Introduced Herbivores: A Comparison of Hosts as Natives and Hosts as Invaders , 1993, The American Naturalist.

[23]  M. Abdel-latief,et al.  Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. , 2008, Insect biochemistry and molecular biology.

[24]  D. Orr.  SCELIONID WASPS AS BIOLOGICAL CONTROL AGENTS: A REVIEW , 1988 .

[25]  D. A. Reed,et al.  Host defensive response against an egg parasitoid involves cellular encapsulation and melanization , 2007 .

[26]  M. Strand,et al.  Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis , 1986 .

[27]  G. Vétek,et al.  First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. , 2014, Zootaxa.

[28]  W. R. Thompson.  A Catalogue of the Parasites and Predators of Insect Pests. Section 1. Parasite Host Catalogue. Part 2. Parasites of the Dermaptera and Diptera. , 1943 .

[29]  A. Khrimian,et al.  Development of Behaviorally-Based Monitoring Tools for the Brown Marmorated Stink Bug (Heteroptera: Pentatomidae) in Commercial Tree Fruit Orchards , 2012 .

[30]  P. Shearer,et al.  Brown marmorated stink bug [Halyomorpha halys (Stål, 1855)] (Heteroptera: Pentatomidae) in Hungary. , 2014 .

[31]  B. Short,et al.  Impact of Insecticides on the Invasive Halyomorpha halys (Hemiptera: Pentatomidae): Analysis of Insecticide Lethality , 2012, Journal of economic entomology.

[32]  P. Abram,et al.  An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid , 2014, Biological Invasions.

[33]  R. Holt.  Predation, apparent competition, and the structure of prey communities. , 1977, Theoretical population biology.

[34]  G. Hamilton,et al.  PEST STATUS OF THE BROWN MARMORATED STINK BUG, HALyOMORPHA HALyS IN THE USA , 2012 .

[35]  K. Hoelmer,et al.  New synonymy of Trissolcus halyomorphae Yang , 2013 .

[36]  L. Tavella,et al.  First discovery of Halyomorpha halys in peach orchards in Piedmont. , 2013 .

[37]  R. Ims,et al.  How rapidly do invasive birch forest geometrids recruit larval parasitoids? Insights from comparison with a sympatric native geometrid , 2013, Biological Invasions.

[38]  W. Jones.  World review of the parasitoids of the southern green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomidae). , 1988 .

[39]  U. T. Lim,et al.  Evaluation of cold-stored eggs of Dolycoris baccarum (Hemiptera: Pentatomidae) for parasitization by Trissolcus nigripedius (Hymenoptera: Scelionidae) , 2007 .

[40]  Á. Callejón-Ferre,et al.  Raising Trissolcus basalis for the biological control of Nezara viridula in greenhouses of Almería (Spain) , 2010 .

[41]  M. Carter,et al.  Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. , 2003 .

[42]  Marc Kenis,et al.  Ecological effects of invasive alien insects , 2008, Biological Invasions.

[43]  S. V. Joseph,et al.  Review of the Biology, Ecology, and Management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea , 2013, Environmental entomology.

[44]  M. Kivan,et al.  Effects of storage at low-temperature of various heteropteran host eggs on the egg parasitoid, Trissolcus semistriatus , 2005, BioControl.

[45]  Zhong-qi Yang,et al.  A New Species of Trissolcus (Hymenoptera: Scelionidae) Parasitizing Eggs of Halyomorpha Halys (Heteroptera: Pentatomidae) in China with Comments on its Biology , 2009 .

[46]  T. Haye,et al.  Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe , 2014, Journal of Pest Science.

[47]  J. Waage,et al.  Parasitoids in classical biological control. , 1986 .

[48]  J. Bale,et al.  Assessing risks of releasing exotic biological control agents of arthropod pests. , 2006, Annual review of entomology.

[49]  B. Short,et al.  Impact of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Stål), in Mid-Atlantic Tree Fruit Orchards in the United States: Case Studies of Commercial Management , 2012 .

[50]  D. Jennings,et al.  Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys , 2014 .