Skip to main content
Log in

An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Invasive alien species can act as ‘evolutionary traps’ for indigenous parasites and predators when the alien species is accepted as prey or a host but is unsuitable for consumption or development. We tested the relationship between acceptance and suitability of eggs of the invasive alien Halyomorpha halys (Hemiptera: Pentatomidae) in North America relative to eggs of the indigenous Podisus maculiventris (Pentatomidae) for the indigenous generalist egg parasitoid Telenomus podisi (Hymenoptera: Scelionidae). T. podisi accepted 0–24 h old H. halys eggs at a rate similar to P. maculiventris eggs (87.5 ± 6.0 and 70.2 ± 9.1 %, respectively). Successful development of T. podisi occurred in 98.3 % of attacked P. maculiventris eggs, but was not observed in H. halys eggs. Oviposition by T. podisi did, however, reduce the developmental success of H. halys embryos relative to unattacked controls by 24.1 % in 0–24 h old eggs and 29.6 % in 24–48 h old eggs. We suggest that as H. halys spreads and increases in abundance in North America, it could operate as an evolutionary trap for indigenous egg parasitoids, thereby indirectly causing an increase in population levels of indigenous pentatomids. This predicted indirect effect would be a result of H. halys eggs acting as an egg sink for T. podisi. We also introduce the concept of a ‘time sink’, which may be particularly relevant for parasitoids such as T. podisi that spend considerable time protecting their reproductive investments.

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

Similar content being viewed by others

References

  • Abdel-Latief M, Hilker M (2008) Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochem Mol Biol 38:136–145

    Article  CAS  PubMed  Google Scholar 

  • Agboka K, Schulthess F, Chabi-Olaye A, Labo I, Gounou S, Smith H (2002) Self-, intra-, and interspecific host discrimination in Telenomus busseolae Gahan and T. isis Polaszek (Hymenoptera: Scelionidae), sympatric egg parasitoids of the African cereal stem borer Sesamia calamistis Hampson (Lepidoptera: Noctuidae). J Insect Behav 15:1–12

    Article  Google Scholar 

  • Bin F, Vinson SB, Strand MR, Colazza S, Jones WA (1993) Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol Entomol 18:7–15

    Article  Google Scholar 

  • Boivin G (2010) Reproduction and immature development of egg parasitoids. In: Consoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, The Netherlands, pp 1–23

    Google Scholar 

  • Bruni R, Sant’Ana J, Aldrich JR, Bin F (2000) Influence of host pheromone on egg parasitism by scelionid wasps: comparison of phoretic and nonphoretic parasitoids. J Insect Behav 13:165–173

    Article  Google Scholar 

  • Colazza S, Rosi MC, Sebastiani P, Ursini M (1996) Host acceptance behavior in the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Acta Oecologica 17:109–125

    Google Scholar 

  • Field SA (1998) Patch Exploitation, patch-leaving and pre-emptive patch defence in the parasitoid wasp Trissolcus basalis (Insecta: Scelionidae). Ethology 104:323–338

    Article  Google Scholar 

  • Firlej A, Lucas É, Coderre D, Boivin G (2010) Impact of host behavioral defenses on parasitization efficacy of a larval and adult parasitoid. Biocontrol 55:339–348

    Article  Google Scholar 

  • Firlej A, Girard P-A, Brehélin M, Coderre D, Boivin G (2012) Immune response of Harmonia axyridis (Coleoptera: Coccinellidae) supports the enemy release hypothesis in North America. Ann Entomol Soc Am 105:328–338

    Article  Google Scholar 

  • Hänninen L, Pastell M (2009) CowLog: open source software for coding behaviors from digital video. Behav Res Methods 41:472–476

    Article  PubMed  Google Scholar 

  • Heimpel GE, Neuhauser C, Hoogendoorn M (2003) Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecol Lett 6:556–566

    Article  Google Scholar 

  • Henter HJ (1995) The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid host. Evolution 49:439–445

    Article  Google Scholar 

  • Hirose Y, Ehler LE, Hirose Y (2003) Influence of host age on patch use by a quasi-gregarious egg parasitoid. Environ Entomol 32:789–796

    Article  Google Scholar 

  • Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237

    Google Scholar 

  • Hoelmer KA, Tatman K (2011) Natural enemies of the brown marmorated stink bug: what are the prospects for biological control? In: The plague of the brown marmorated stink bug, Entomological Society of America Eastern Branch 82nd annual meeting, Harrisburg, PA. Retrieved from http://www.northeastipm.org/neipm/assets/File/BMSB%20Resources/ESA-Eastern-Branch-2011/13-Natural-Enemies-of-the-Brown-Marmorated-Stink-Bug.pdf. 15 May 2013

  • Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229

    Article  CAS  PubMed  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 

  • Keeler M, Chew F (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 

  • 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 

  • Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280

    Article  CAS  PubMed  Google Scholar 

  • Lawrence PO (1990) The biochemical and physiological effects of insect hosts on the development and ecology of their insect parasites: An overview. Arch Insect Biochem Physiol 13:217–228

    Article  CAS  Google Scholar 

  • Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer K, Lee D-H, Wright SE (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226

    Article  Google Scholar 

  • McPherson J (1982) The Pentatomoidea (Hemiptera) of northeastern North America with emphasis on the fauna of Illinois. Southern Illinois University press, Carbondale, p 256

    Google Scholar 

  • Moreau SJM, Guillot S (2005) Advances and prospects on biosynthesis, structures and functions of venom proteins from parasitic wasps. Insect Biochem Mol Biol 35:1209–1223

    Article  CAS  PubMed  Google Scholar 

  • Nénon J-P, Boivin G, Allo M (1995) Fine structure of the egg envelopes in Listronotus oregonensis (Leconte) (Coleoptera: Curculionidae) and morphological adaptations to oviposition sites. Int J Insect Morphol Embryol 24:333–342

    Article  Google Scholar 

  • Nielsen AL, Hamilton GC (2009) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140

    Article  PubMed  Google Scholar 

  • Nielsen AL, Hamilton GC, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355

    Article  PubMed  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

    Google Scholar 

  • Orr DB, Russin JS, Boethel DJ, Jones WA (1986) Stink bug (Hemiptera: Pentatomidae) egg parasitism in Louisiana soybeans. Environ Entomol 15:1250–1254

    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 USA 101:17150–17155

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna

    Google Scholar 

  • Rabb RL, Bradley JR (1970) Marking host eggs by Telenomus sphingis. Ann Entomol Soc Am 63:1053–1056

    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 

  • Strand MR, Ratner S, Vinson SB (1983) Maternally induced host regulation by the egg parasitoid Telenomus heliothidis. Physiol Entomol 8:469–475

    Article  Google Scholar 

  • Vinson SB (2010) Nutritional ecology of insect egg parasitoids. In: Consoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, The Netherlands, pp 25–55

    Google Scholar 

  • Wajnberg É, Curty C, Colazza S (2004) Genetic variation in the mechanisms of direct mutual interference in a parasitic wasp: consequences in terms of patch-time allocation. J Anim Ecol 73:1179–1189

    Article  Google Scholar 

  • Weber CA, Smilanick JM, Ehler LE, Zalom FG (1996) Ovipositional behavior and host discrimination in three scelionid egg parasitoids of stink bugs. Biol Control 6:245–252

    Article  Google Scholar 

  • Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen Schweizerische Entomol Gesellschaft 81:1–8

    Google Scholar 

  • Yeargan KV (1979) Parasitism and predation of stink bug eggs in soybean and alfalfa fields. Environ Entomol 8:715–719

    Google Scholar 

  • Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS One 7:e31246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Allison Bruin for technical assistance. This work was supported by a Natural Sciences and Engineering Council of Canada postgraduate scholarship to P. K. Abram.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. K. Abram.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abram, P.K., Gariepy, T.D., Boivin, G. et al. An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions 16, 1387–1395 (2014). https://doi.org/10.1007/s10530-013-0576-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0576-y

Keywords

Navigation