Skip to main content
Log in

Exploitation of pentatomids by native egg parasitoids in the native and introduced ranges of Halyomorpha halys: a molecular approach using sentinel egg masses

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Following introduction of Halyomorpha halys in Europe and North America, a concerted effort has been made to characterize host–parasitoid interactions involving H. halys. Yet, it is unclear whether the reported low parasitism in the field is due to the rejection of H. halys by native parasitoids, or the inability of larvae to develop. To determine whether native and exotic pentatomids are equally exploited by native parasitoids in the introduced range of H. halys, sentinel stink bug (native and exotic) egg masses were exposed in different habitats and the incidence of parasitism was determined by rearing and DNA-based approaches. Parasitism estimates were always lower with rearing compared to the molecular method. Egg masses of both native and exotic host species were equally likely to be attacked under natural conditions, supporting the idea that H. halys represents an evolutionary trap for native parasitoids. Lack of parasitoid emergence from H. halys eggs is probably not due to native parasitoids rejecting this host, but rather due to the inability of larvae to complete development. The frequent parasitization of H. halys by native parasitoids highlights the possibility of interspecific interactions with natural enemies considered for introduction as part of biological control programme (e.g. Trissolcus japonicus). Oviposition in eggs of the unsuitable H. halys host by native parasitoid may also have population-level consequences for both parasitoids (e.g. reduced population size, shifts in parasitoid community composition) and pentatomids (e.g. competition with H. halys, deceased population regulation by parasitoids). These effects should be considered when developing biological control strategy for H. halys.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abram PK, Gariepy TD, Boivin G, Brodeur J (2014) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions 16:1387–1395

    Article  Google Scholar 

  • Abram PK, Brodeur J, Burte V, Boivin G (2016) Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biol Control 98:52–60

    Article  Google Scholar 

  • Abram PK, Hoelmer KA, Acebes-Doria A, Andrews H, Beers EH, Bergh JC et al (2017) Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J Pest Sci 90:1009–1020

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Berthon K (2015) How do native species respond to invaders? Mechanistic and trait-based perspectives. Biol Invasions 17:2199–2211

    Article  Google Scholar 

  • Bland JM, Altman DG (2000) Statistics notes. The odds ratio. BMJ 320:1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodeur J, Vet LEM (1995) Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two related parasitoid species. Physiol Entomol 20:7–12

    Article  Google Scholar 

  • Carroll SP, Dingle H, Klassen SP (1997) Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51:1182–1188

    Article  PubMed  Google Scholar 

  • Choi M-Y, Yang Z-Q, Wang X-Y et al (2014) Parasitism rate of egg parasitoid Anastatus orientalis (Hymenoptera : Eupelmidae) on Lycorma delicatula (Hemiptera : Fulgoridae) in China. Korean J Appl Entomol 53:135–139

    Article  Google Scholar 

  • Cornelius ML, Dieckhoff C, Hoelmer KA, Olsen RT, Weber DC, Herlihy MV, Talamas EJ, Vinyard B, Greenstone MH (2016a) Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys (Stål) in Mid-Atlantic USA ornamental landscapes. Biol Control 103:11–20

    Article  Google Scholar 

  • Cornelius ML, Dieckhoff C, Vinyard BT, Hoelmer KA (2016b) Parasitism and predation on sentinel egg masses of the brown marmorated stink bug (Hemiptera: Pentatomidae) in three vegetable crops: importance of dissections for evaluating the impact of native parasitoids on an exotic pest. Environ Entomol 45:1536–1542

    Article  PubMed  Google Scholar 

  • Cusumano A, Peri E, Amodeo V, McNeil JN, Colazza S (2013) Intraguild interactions between egg parasitoids: window of opportunity and fitness costs for a facultative hyperparasitoid. PLoS ONE 8:e64768

    Article  PubMed  PubMed Central  Google Scholar 

  • Cusumano A, Peri E, Colazza S (2016) Interspecific competition/facilitation among insect parasitoids. Curr Opin Insect Sci 14:12–16

    Article  Google Scholar 

  • Dieckhoff C, Tatman KM, Hoelmer KA (2017) Natural biological control of Halyomorpha halys by native egg parasitoids: a multi-year survey in northern Delaware. J Pest Sci 90:1143–1158

    Article  Google Scholar 

  • Elton CS (2000) The ecology of invasions by animals and plants. University of Chicago Press, Chicago

    Google Scholar 

  • Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Gariepy TD, Haye T, Zhang J (2014) A molecular diagnostic tool for the preliminary assessment of host-parasitoid associations in biological control programmes for a new invasive pest. Mol Ecol 23:3912–3924

    Article  CAS  PubMed  Google Scholar 

  • Gariepy TD, Bruin A, Konopka J, Scott-Dupree C, Fraser H, Bon M-C, Talamas E (2018) A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids. Mol Ecol. https://doi.org/10.1111/mec.14868

    Article  PubMed  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Article  Google Scholar 

  • Hassell MP, Waage JK (1984) Host-parasitoid population interactions. Annu Rev Entomol 29:89–114

    Article  Google Scholar 

  • Haye T, Fischer S, Zhang J, Gariepy T (2015) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88:693–705

    Article  Google Scholar 

  • Hedstrom C, Lowenstein D, Andrews H, Bai B, Winman N (2017) Pentatomid host suitability and the discovery of introduced populations of Trissolcus japonicus in Oregon. J Pest Sci 90:1169–1179

    Article  Google Scholar 

  • Herlihy MV, Talamas EJ, Weber DC (2016) Attack and success of native and exotic parasitoids on eggs of Halyomorpha halys in three Maryland habitats. PLoS ONE 11:e0150275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoogendoorn M, Heimpel GE (2002) Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol Control 25:224–230

    Article  Google Scholar 

  • Hrček J, Godfray HCJ (2015) What do molecular methods bring to host-parasitoid food webs? Trends Parasitol 31:30–35

    Article  PubMed  Google Scholar 

  • IBM (2016) IBM SPSS statistics for windows, Version 24.0. IBM Corp, Armonk

  • Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385

    Article  CAS  PubMed  Google Scholar 

  • Jones AL, Jennings DE, Hooks CRR, Shrewsbury PM (2014) Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys. Biol Control 78:61–66

    Article  Google Scholar 

  • Kaser JM, Nielsen AL, Abram PK (2018) Biological control effects of non-reproductive host mortality caused by insect parasitoids. Ecol Appl 28:1081–1092

    Article  PubMed  Google Scholar 

  • Keeler MS, Chew FS (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568

    Article  PubMed  Google Scholar 

  • Kivan M, Kilic N (2005) Effects of storage at low-temperature of various heteropteran host eggs on the egg parasitoid, Trissolcus semistriatus. Biocontrol 50:589–600

    Article  Google Scholar 

  • Kokko H, Chaturvedi A, Croll D et al (2017) Can evolution supply what ecology demands? Trends Ecol Evol 32:187–197

    Article  PubMed  Google Scholar 

  • Konopka JK, Haye T, Gariepy T, Mason P, Gillespie D, McNeil JN (2017a) An exotic parasitoid provides an invasional lifeline for native parasitoids. Ecol Evol 7:277–284

    Article  PubMed  Google Scholar 

  • Konopka JK, Haye T, Gariepy TD, McNeil JN (2017b) Possible coexistence of native and exotic parasitoids and their impact on control of Halyomorpha halys. J Pest Sci 90:1119–1125

    Article  Google Scholar 

  • Konopka JK, Poinapen D, Gariepy T, McNeil JN (2018) Understanding the mismatch between behaviour and development in a novel host-parasitoid association. Sci Rep 8(1):15677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koppel AL, Herbert DA, Kuhar TP, Kamminga K (2009) Survey of stink bug (Hemiptera: Pentatomidae) egg parasitoids in wheat, soybean, and vegetable crops in southeast Virginia. Environ Entomol 38:375–379

    Article  CAS  PubMed  Google Scholar 

  • Lau JA (2008) Beyond the ecological: biological invasions alter natural selection on a native plant species. Ecology 89:1023–1031

    Article  PubMed  Google Scholar 

  • Laumann RA, Moraes MCB, Pareja M, Alarcão GC, Botelho AC, Maia AHN, Leonardecz E, Borges M (2008) Comparative biology and functional response of Trissolcus spp. (Hymenoptera: Scelionidae) and implications for stink bugs (Hemiptera: Pentatomidae) biological control. Biol Control 44:32–41

    Article  Google Scholar 

  • Milnes JM, Wiman NG, Talamas EJ, Brunner JF, Hoelmer KA, Buffington ML, Beers EH (2016) Discovery of an exotic egg parasitoid of the brown marmorated stink bug, Halyomorpha halys (Stål) in the Pacific Northwest. Proc Entomol Soc Wash 118:466–470

    Article  Google Scholar 

  • Ogburn EC, Bessin R, Dieckhoff C, Dobson R, Grieshop M, Hoelmer KA, Mathews C, Moore J, Nielsen AL, Poley K, Pote JM, Rogers M, Welty C, Walgenbach JF (2016) Natural enemy impact on eggs of the invasive brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), in organic agroecosystems: a regional assessment. Biol Control 101:39–51

    Article  Google Scholar 

  • Okuda MS, Yeargan KV (1988) Habitat partitioning by Telenomus podisi and Trissolcus euschisti (Hymenoptera: Scelionidae) between herbaceous and woody host plants. Environ Entomol 17:795–798

    Article  Google Scholar 

  • Orr D (1988) Scelionid wasps as biological control agents: a review. Florida Entomol 71:506–528

    Article  Google Scholar 

  • Orr D, Sussin J, Boethel D, Jones W (1986) Stink bug (Hemiptera: Pentatomidae) egg parasitism in Louisiana soybeans. Environ Entomol 15:1250–1254

    Article  Google Scholar 

  • Pacheco HM, Vanlaerhoven SL, García MAM, Hunt DW (2018) Food web associations and effect of trophic resources and environmental factors on parasitoids expanding their host range into non-native hosts. Entomol Exp Appl 166:277–288

    Article  Google Scholar 

  • Phillips BL, Shine R (2004) Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci 101:17150–17155

    Article  CAS  PubMed  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman & Hall, New York

    Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • Roversi P, Binazzi F, Marianelli L, Costi E, Maistrello L, Sabbatini Peverieri G (2016) Searching for native egg-parasitoids of the invasive alien species Halyomorpha halys Stål (Heteroptera Pentatomidae) in Southern Europe. Redia 99:63–70

    Google Scholar 

  • Roversi PF, Maltese M, Simoni S, Cascone P, Binazzi F, Strangi A (2017) Graphosoma lineatum (Hemiptera: Pentatomidae): a suitable host for mass rearing Ooencyrtus telenomicida (Hymenoptera: Encyrtidae). Int J Pest Manag 64(4):294–302

    Article  Google Scholar 

  • Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480

    Article  Google Scholar 

  • Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246

    Article  Google Scholar 

  • Schmitz DC, Simberloff D (1997) Biological invasions: a growing threat. Issues Sci Technol 13:33–40

    Google Scholar 

  • Skillman VP, Lee JC (2017) Nutrient content of brown marmorated stink bug eggs and comparisons between experimental uses. J Insect Sci 17:120

    Article  CAS  PubMed Central  Google Scholar 

  • Strand MR, Meola SM, Vinson SB (1986) Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis. J Insect Physiol 32:389–402

    Article  Google Scholar 

  • Strand MR, Vinson SB, Nettles WC, Xie ZN (1988) In vitro culture of the egg parasitoid Telenomus heliothidis: the role of teratocytes and medium consumption in development. Entomol Exp Appl 46:71–78

    Article  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374

    Article  Google Scholar 

  • Talamas EJ, Herlihy MV, Dieckhoff C et al (2015) Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae) emerges in North America. J Hymenopt Res 43:119–128

    Article  Google Scholar 

  • Talamas EJ, Buffington ML, Dieckhoff C, Hoelmer K, Buffington M, Bon M-C, Weber DC (2017) Revision of palearctic trissolcus ashmead (Hymenoptera, Scelionidae). J Hymenopt Res 56:79–261

    Article  Google Scholar 

  • Thomsen PF, Willerslev E (2015) Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18

    Article  Google Scholar 

  • Tillman PG (2016) Diversity of stink bug (Hemiptera: Pentatomidae) egg parasitoids in woodland and crop habitats in southwest Georgia, USA. Florida Entomol 99:286–291

    Article  Google Scholar 

  • Turcotte MM, Levine JM (2016) Phenotypic plasticity and species coexistence. Trends Ecol Evol 31:803–813

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S, IV edn. Springer, New York

    Book  Google Scholar 

  • Vidal MC, Murphy SM (2018) Bottom-up vs. top-down effects on terrestrial insect herbivores: a meta-analysis. Ecol Lett 21:138–150

    Article  PubMed  Google Scholar 

  • Vinson SB (1976) Host selection by insect parasitoids. Annu Rev Entomol 21:109–133

    Article  Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Wajnberg E, Roitberg BD, Boivin G (2016) Using optimality models to improve the efficacy of parasitoids in biological control programmes. Entomol Exp Appl 158:2–16

    Article  CAS  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  Google Scholar 

  • Yang Z-Q, Yao Y-X, Qiu L-F, 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. Ann Entomol Soc Am 102:39–47

    Article  Google Scholar 

  • Zhang J, Zhang F, Gariepy T, Mason P, Gillespie D, Talamas E, Haye T (2017) Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. J Pest Sci 90:1127–1141

    Article  Google Scholar 

Download references

Acknowledgements

This work was funded by NSERC PGS Scholarship and ESC Research Travel Scholarship to JKK, and Agriculture and Agri-Food Canada A-base funds to TDG. We would like to thank A. Bruin for technical assistance, and W. Burbridge, H. Deacon, D. Drapeau, as well as S. Deluca, R. Hagedorn and A. Haley for assistance with the field work in Canada and Switzerland, respectively, and T. Cao for assistance in China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. K. Konopka.

Ethics declarations

Conflict of interest

The authors have declared that no conflict of interest exists.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

Data availability

In addition to information in this article [and its supplementary information files], the datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.

Additional information

Communicated by M. Traugott.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 54 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Konopka, J.K., Gariepy, T.D., Haye, T. et al. Exploitation of pentatomids by native egg parasitoids in the native and introduced ranges of Halyomorpha halys: a molecular approach using sentinel egg masses. J Pest Sci 92, 609–619 (2019). https://doi.org/10.1007/s10340-018-01071-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-018-01071-8

Keywords

Navigation