Skip to main content
SpringerLink
Log in

Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control

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

Abstract

A seminal paper by Howarth (Proc Hawaii Entomol Soc 24:239–244, 1983) entitled “Classical biological control: Panacea or Pandora’s Box” ignited a sometimes acrimonious debate over the relative safety of introductions for classical biological control. Extolled for years as environmentally benign, the litany of negative non-target effects profiled by Howarth heightened awareness of this issue. Several factors have muddied this debate including the conflation of frequency of effects with their strength, grouping the effects of disparate biological control agents together, and the lack of quantitative data on either side of the argument. Here, I examine the potential for non-target effects among insect parasitoids, the most common group used for biological control of arthropods. In response to calls for better quantitative studies, I highlight three different techniques, quantitative food webs, life table analysis, and experimental populations, respectively, to quantitatively assess or reassess non-target effects in different systems. I also explore three methodological approaches employed to ascertain the strength of competitive interactions between native and introduced parasitoids, a potential non-target effect that has received little attention in the literature. These types of studies may greatly increase our understanding of the nature of non-target interactions with introduced parasitoids and bring more rigor to a debate often dominated by rhetoric.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

CBC:

Classic biological control

References

  • Angalet GW, Fuester R (1977) The Aphidius parasites of the pea aphid Acyrthosiphon pisum in the eastern half of the United States. Ann Entomol Soc Am 70:87–96

    Google Scholar 

  • Arnaud PH Jr (1978) A host-parasite catalog of North American Tachinidae (Diptera). USDA, Science and Education Administration, Washington, DC (Miscellaneous Publication Number 1319)

    Google Scholar 

  • Bennett FD (1993) Do introduced parasitoids displace native ones? Fla Entomol 76:54–63

    Article  Google Scholar 

  • Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniids moths. Conserv Biol 14:1798–1806

    Article  Google Scholar 

  • Briese DT (2005) Translating host-specificity test results into the real world: the need to harmonize the yin and yang of current testing procedures. Biol Control 35:208–214

    Article  Google Scholar 

  • Coulson JR, Soper RS, Williams DW (eds) (1991) Biological control quarantine: needs and procedures. In: Proceedings of a workshop sponsored by United States Department of Agriculture, Agricultural Research Service, ARS-99, pp 77

  • Culver JJ (1919) A study of Compsilura concinnata, an imported tachinid parasite of the gypsy moth and the brown-tail moth. Bulletin Number 766:1–27. United States Department of Agriculture

    Google Scholar 

  • Danyk TP (1993) Competitive interactions between the pea aphid parasitoids, Aphidius ervi and Praon pequdorum (Hymenoptera: Aphidiidae): influence of guild composition in southern British Columbia. Dissertation, Simon Frazer University, Burnaby, British Columbia, Canada

  • Davis CJ (1964) The introduction, propagation, liberation, establishment of parasites to control Nezara viridula variety smaragdula (Fabricius) in Hawaii (Heteroptera: Pentatomidae). Proc Hawaii Entomol Soc 18:369–375

    Google Scholar 

  • DeLoach CJ (1991) Past successes and current prospects in biological control of weeds in the United States and Canada. Nat Areas J 11:129–142

    Google Scholar 

  • Duan JJ, Purcell MF, Messing H (1996) Parasitoids of non-target tephritid flies in Hawaii: Implications for biological control of fruit fly pests. Entomophaga 41:245–256

    Article  Google Scholar 

  • Elkinton JS, Parry D, Boettner GH (2006) Implicating an introduced generalist parasitoid in the invasive browntail moth’s enigmatic demise. Ecology 87:2664–2672

    Article  PubMed  Google Scholar 

  • Ellis A, Walter AD, Tooker JF, Ginzel MD, Reagel PF, Lacey ES, Bennett AB, Grossman EM, Hanks LM (2005) Conservation biological control in urban landscapes: manipulating parasitoids of bagworm (Lepidoptera: Psychidae) with flowering forbs. Biol Control 34:99–107

    Article  Google Scholar 

  • Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647

    Article  Google Scholar 

  • Follett PA, Duan JJ (2000) Nontarget effects of biological control. Kluwer, Dordrecht

    Google Scholar 

  • Follett PA, Johnson MT, Jones VP (2000) Parasitoid drift in Hawaiian pentatomoids. In: Follet PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Dordrecht, pp 77–93

    Google Scholar 

  • Frank JH (1998) How risky is biological control? Comment. Ecology 79:1829–1834

    Google Scholar 

  • Fuester RW, Sandridge PT, Dill NH, McLaughlin JM, PeiVer RA, Taylor PB, Sigmon JOD, Newlon CJ (1997) Parasitism of gypsy moth (Lepidoptera: Lymantriidae pupae on the Delmarva Peninsula with emphasis on Coccygomimus disparis (Hymenoptera: Ichneumonidae). J Econ Entomol 90:1551–1559

    Google Scholar 

  • Funasaki GY, Lai PO, Nakahara LM, Beardsley JW, Ota AK (1988) A review of biological control introductions in Hawaii 1890–1985. Proc Hawaii Entomol Soc 28:105–160

    Google Scholar 

  • Gagne WC, Howarth FG (1985) Conservation status of endemic Hawaiian Lepidoptera. In: Heath J (ed) Proc 3rd Congr Eur Lepidopterol, Cambridge UK, pp 74–84

  • Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Gould JR, Elkinton JS, Wallner WE (1990) Density-dependent suppression of experimentally created gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), populations by natural enemies. J Anim Ecol 59:213–233

    Article  Google Scholar 

  • Hawkins BA (1994) Pattern and process in host–parasitoid interactions. Cambridge University Press, Cambridge

    Google Scholar 

  • Hawkins BA (2000) Species coexistence in parasitoid communities: does competition matter? In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, pp 198–214

    Google Scholar 

  • Hawkins BA, Marino PC (1997) The colonization of native phytophagous insects in North America by exotic parasitoids. Oecologia 112:566–571

    Article  Google Scholar 

  • Hawkins BA, Mills NJ (1996) Variability in parasitoid community structure. J Anim Ecol 65:501–516

    Article  Google Scholar 

  • Headrick DH, Goeden RD (2001) Biological control as a tool for ecosystem management. Biol Control 21:249–257

    Article  Google Scholar 

  • Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biocontrol agents. Science 293:1314–1316

    Article  PubMed  CAS  Google Scholar 

  • Hochberg ME, Hawkins BA (1992) Refuges as a predictor of parasitoid diversity. Science 255:973–976

    Article  PubMed  Google Scholar 

  • Hoddle MS (2004) Restoring balance: using exotic species to control invasive exotic species. Conserv Biol 18:1–12

    Article  Google Scholar 

  • Howarth FG (1983) Biological control: panacea or Pandora’s box? Proc Hawaii Entomol Soc 24:239–244

    Google Scholar 

  • Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509

    Article  Google Scholar 

  • Johnson MT, Follett PA, Taylor AD, Jones VP (2005) Non-target impact of biological control and invasive species on the non-target native Hawaiian koa bug. Oecologia 142:529–540

    Article  PubMed  Google Scholar 

  • Kellogg SK, Fink LS, Brower LP (2003) Parasitism of native luna moths, Actias luna (L) (Lepidoptera: Saturniidae) by the introduced Compsilura concinnata (Meigen) (Diptera: Tachinidae) in central Virginia, their hyperparasitism by trigonalid wasps (Hymenoptera: Trigonalidae). Environ Entomol 32:1019–1027

    Google Scholar 

  • Kuris AM (2003) Did biological control cause extinction of the coconut moth, Levuana iridescens, in Fiji? Biol Invasions 5:131–141

    Article  Google Scholar 

  • Lai PY (1988) Biological control: a positive point of view. Proc Hawaii Entomol Soc 28:179–190

    Google Scholar 

  • Lockwood JA (1993) Benefits and costs of controlling rangeland grasshoppers (Orthoptera: Acrididae) with exotic organisms: search for a null hypothesis and regulatory compromise. Environ Entomol 22:904–914

    Google Scholar 

  • Louda SM, Stiling P (2004) The double edge sword of biological control in conservation and restoration. Conserv Biol 18:50–53

    Article  Google Scholar 

  • Luck RF, Podoler H (1985) Competitive exclusion of Aphytis lingnanensis by A. melinus: potential role of host size. Ecology 66:904–913

    Article  Google Scholar 

  • Lynch LD, Thomas MB (2000) Nontarget effects in the biocontrol of insects with insects, nematodes and microbial agents: the evidence. Biocontrol News Inf 21:117–130

    Google Scholar 

  • Marino PC, Landis DA, Hawkins BA (2006) Conserving parasitoid assemblages of North American pest Lepidoptera: does biological control by native parasitoids depend on landscape complexity? Biol Control 37:173–185

    Article  Google Scholar 

  • McEvoy PB, Coombs EM (2000) Why things bite back: unintended consequences of biological weed control. In: Follet PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Dordrecht, pp 167–194

    Google Scholar 

  • Memmott J (2000) Food webs as a tool for studying non target effects in biological control. In: Follet PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Dordrecht, pp 147–163

    Google Scholar 

  • Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4(3):132–140

    Article  Google Scholar 

  • Mills NJ (2003) Parasitoid interactions and biological control. In: 1st international symposium on biological control of arthropods. FHTET-03-05, USDA Forest Service

  • Minnesota Department of Natural Resources (1997) Gypsy moth biological control. For Insect Dis Newslett, May 21, 1997

  • Minnesota Department of Natural Resources (1999) Biological control of gypsy moth. For Insect Dis Newslett, June 1, 1999

  • Munro VMV, Henderson IM (2002) Nontarget effect of entomophagous biocontrol: shared parasitism between native lepidopteran parasitoids and the biocontrol agent Trigonospila brevifacies (Diptera: Tachinidae) in forest habitats. Environ Entomol 31:388–396

    Article  Google Scholar 

  • Murdoch VV, Briggs CJ, Nisbet RM (1996) Competitive displacement and biological control in parasitoids: a model. Am Nat 148:806–826

    Article  Google Scholar 

  • Nishida T (1956) An experimental study of the ovipositional behavior of Opius fletcheri. Proc Hawaii Entomol Soc 16:126

    Google Scholar 

  • Onstad DV, McManus ML (1996) Risks of host range expansion by parasites of insects. Bioscience 46:430–435

    Article  Google Scholar 

  • Parry D (2007) Trouvelot’s legacy? The disappearance of North American giant silk moths (Saturniidae). In: Proceedings of the 4th North American forest insect work conference, Asheville, NC, pp 145–149

  • Parry D, Spence JR, Volney VJA (1997) The response of natural enemies to experimentally increased populations of forest tent caterpillar. Ecol Entomol 22:97–108

    Article  Google Scholar 

  • Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258

    Article  PubMed  CAS  Google Scholar 

  • Reitz SR (1996) Development of Eucelatoria bryani and Eucelatoria rubentis (Diptera: Tachinidae) in different instars of Helicoverpa zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 89:81–87

    Google Scholar 

  • Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  PubMed  CAS  Google Scholar 

  • Sands DPA, Van Driesche RG (2004) Using the scientific literature to estimate the host range of a biological control agent. In: Van Driesche RG, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. USDA Forest Health Technology Enterprise Team, Morgantown, pp 15–23

    Google Scholar 

  • Schaefer PV, Fuester RV, Chianese RJ, Rhoads LD, Tichenor RB Jr (1989) Introduction and North American establishment of Coccygomimus disparis (Hymenoptera: Ichneumonidae), a polyphagous pupal parasite of Lepidoptera, including gypsy moth. Environ Entomol 18:1117–1125

    Google Scholar 

  • Schaffner JV, Griswold CL (1934) Macrolepidoptera and their parasites reared from field collections in the northeastern part of the United States. US Department of Agriculture, 160 pp (Miscellaneous Publications Number 188)

  • Schellhorn NA, Kuhman TR, Olson AC, Ives AR (2002) Competition between native and introduced parasitoids of aphids: nontarget effects and biological control. Ecology 83:2745–2757

    Article  Google Scholar 

  • Schweitzer DF (1988) Status of Saturniidae in the Northeastern USA: a quick review. News Lepid Soc 1988:4–5

    Google Scholar 

  • Selfridge JA, Parry D, Boettner GH (2007) Parasitism of barrens buck moth Hemileuca maia Drury in early and late successional pine barrens habitats. J Lepid Soc 61:213–221

    Google Scholar 

  • Shaw MR (1994) Parasitoid host ranges. In: Hawkins BA, Sheehan V (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 111–144

    Google Scholar 

  • Sheehan V, Hawkins BA (1991) Attack strategy as an indicator of host range in metopiinae and pimplinae Ichneumonidae (Hymenoptera). Ecol Entomol 16:129–131

    Article  Google Scholar 

  • Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974

    Article  Google Scholar 

  • Smith HR, Remington CL (1996) Food specificity in interspecies competition: comparisons between terrestrial vertebrates and arthropods. Bioscience 46:436–447

    Article  Google Scholar 

  • Stamp NE, Bowers MD (1990) Parasitism of buckmoth caterpillars (Hemileuca lucina: Saturniidae) by tachinid flies. J Lepid Soc 44:199–200

    Google Scholar 

  • Stireman JO, O’Hara JE, Wood DM (2006) Tachinidae: evolution, behavior, ecology. Annu Rev Entomol 51:525–555

    Article  PubMed  CAS  Google Scholar 

  • Strong DR, Pemberton RV (2000) Biological control of invading species-risk and reform. Science 288:1969–1970

    Article  PubMed  CAS  Google Scholar 

  • Thomas MB, Willis AJ (1998) Biocontrol: risky but necessary? Trends Ecol Evol 13:325–329

    Article  Google Scholar 

  • Tuskes PM, Tuttle JP, Collins MM (1996) The wild silk moths of North America. Cornell University, Ithaca

    Google Scholar 

  • Webber RT, Schaffner JV Jr (1926) Host relations of Compsilura concinnata Meigen, an important tachinid parasite of the gipsy moth and the brown-tail moth. Bull 1363, United States Department of Agriculture, 31 pp

Download references

Acknowledgments

I thank D. Langor and J. Sweeney for organizing the conference and coordinating the ensuing manuscripts. The saturniid research would not have been possible without the efforts and data of G. Boettner, J. Selfridge, B. Hoven, and G. Tuttle. Special thanks are due G. Boettner for much critical discussion of non-target issues and saturniid silk moths as well as constructive comments that improved the manuscript. N. Finley (Cape Cod National Seashore) and N. Gifford (The Nature Conservancy and Albany Pine Bush Preserve) provided accommodation, labor, and necessary permission to conduct various studies in Massachusetts and New York, respectively. The projects were funded by National Science Foundation grant DEB-089699, The Edna Bailey Sussman Foundation, SUNY—College of Environmental Science & Forestry, and the Biological Research Institute (New York State Museum) grant.

Author information

Authors and Affiliations

  1. College of Environmental Science & Forestry, State University of New York, 246 Illick Hall, 1 Forestry Drive, Syracuse, NY, 13082, USA

    Dylan Parry

Authors
  1. Dylan Parry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dylan Parry.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parry, D. Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biol Invasions 11, 47–58 (2009). https://doi.org/10.1007/s10530-008-9319-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-008-9319-x

Keywords

Search

Navigation