Biol Invasions DOI 10.1007/s10530-008-9319-x ORIGINAL PAPER Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control Dylan Parry Received: 6 June 2007 / Accepted: 9 November 2007 Ó Springer Science+Business Media B.V. 2008 Abstract A seminal paper by Howarth (Proc literature. These types of studies may greatly increase Hawaii Entomol Soc 24:239–244, 1983) entitled our understanding of the nature of non-target inter- ‘‘Classical biological control: Panacea or Pandora’s actions with introduced parasitoids and bring more Box’’ ignited a sometimes acrimonious debate over rigor to a debate often dominated by rhetoric. the relative safety of introductions for classical biological control. Extolled for years as environmen- Keywords Parasitoid drift Á Non-target Á tally benign, the litany of negative non-target effects Competition Á Biological control Á Invasive Á profiled by Howarth heightened awareness of this Native Á Lepidoptera issue. Several factors have muddied this debate including the conflation of frequency of effects with Abbreviation their strength, grouping the effects of disparate CBC Classic biological control 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 Introduction insect parasitoids, the most common group used for biological control of arthropods. In response to calls Classic biological control (hereafter CBC), the for better quantitative studies, I highlight three deliberate introduction of the natural enemies of a different techniques, quantitative food webs, life non-indigenous species, was long considered the table analysis, and experimental populations, respec- most environmentally desirable method for control- tively, to quantitatively assess or reassess non-target ling the proliferation of exotic organisms (McEvoy effects in different systems. I also explore three and Coombs 2000). Francis Howarth (1983) pub- methodological approaches employed to ascertain the lished Panacea or Pandora’s Box, a paper that strength of competitive interactions between native provocatively challenged the long-standing paradigm and introduced parasitoids, a potential non-target of biological control as a safe alternative to chemical effect that has received little attention in the pesticides. His article documented a litany of non- target effects and unintended consequences of organ- isms released in CBC programs. The paper launched D. Parry (&) a heated and sometimes acrimonious debate often College of Environmental Science & Forestry, dominated by rhetoric rather than science. Despite State University of New York, 246 Illick Hall, 1 Forestry Drive, Syracuse, NY 13082, USA bold pronouncements extolling the safety of CBC e-mail: [email protected] (e.g., Funasaki et al. 1988; Lai 1988; DeLoach 1991; 123 D. Parry Frank 1998; Headrick and Goeden 2001), or its 2006), whereas the majority of dipteran parasitoids catastrophic consequences (Lockwood 1993; Ho- are in the family Tachinidae (Stireman et al. 2006), warth 1991) quantitative studies validating either although this life-history strategy does occur in viewpoint are few (Thomas and Willis 1998). numerous other dipteran families. There is little debate that some species introduced for CBC have had or are having detrimental impacts Parasitoid biology on non-target native species (Simberloff and Stiling 1996; Follett and Duan 2000; Strong and Pemberton Parasitoids can be broadly divided into idiobionts and 2000). Certainly, some early CBC programs, espe- koinobionts based on life-history (Hawkins 1994). cially those where vertebrate predators were Idiobiont parasitoids kill their host at or shortly after introduced to islands, had devastating consequences parasitism, then feed externally on the host, a life for non-target organisms (Smith and Remington history strategy that precludes interaction with the 1996; Simberloff and Stiling 1996). Modern practi- intact immune system of the host. Koinobionts on the tioners of CBC point out that none of these other hand, complete most or all of their larval introductions would be considered today, while development in a living host, necessitating evasion or critics rejoin that some organisms introduced within manipulation of host defenses in order to survive and the last 30 years have also had undesirable effects on complete development. This dichotomy has led to non-target species despite extensive screening speculation that idiobionts should have larger host (Strong and Pemberton 2000; Louda and Stiling ranges than koinobionts although the evidence is 2004). While less polarized in recent years, the equivocal (Hawkins and Marino 1997). debate about the risk posed by CBC continues (see Hoddle 2004 and Louda and Stiling 2004). Parasitoid drift The arguments about the safety of CBC and its non-target effects may be confounded by sweeping The acquisition of novel non-target hosts by intro- generalizations across diverse groups of organisms. duced parasitoids or ‘drift’ incorporates several For example, while the introduction of mammalian processes, including host shifts, host range expansion, predators and freshwater fish often results in severe and host switching (Follett et al. 2000). Studies non-target consequences (Simberloff and Stiling suggest that parasitoid drift may be extensive. For 1996), fewer non-target effects have been docu- example, of 313 exotic parasitoids released in North mented for the biological control of plants and even America for CBC of holometabolous insects prior to fewer for efforts aimed at arthropods. However, non- 1990, 51 were recorded from native non-target target effects from CBC programs against arthropods insects (Hawkins and Marino 1997). While the may be greater than has been recognized because acquisition of non-target species by so many intro- only a few systems have been extensively studied duced parasitoids is alarming, it is not particularly (e.g., Lynch and Thomas 2000). To move beyond surprising. Few parasitoids are truly monophagous polarization, we need finer scale analyses that (Shaw 1994; Sheehan and Hawkins 1991) and drift scrutinize specific groups of biological control organ- has long been recognized (e.g., Webber and Schaff- isms. Secondly, we must evaluate the effects on non- ner 1926; Nishida 1956; Davis 1964; Duan et al. target species in a more quantitative manner using 1996; Follett et al. 2000). In fact, the expansion of realistic in situ field studies. host range by introduced parasitoids through the acquisition of native species was historically viewed as beneficial (e.g., Culver 1919; Webber and Schaff- Parasitoids in classical biological control ner 1926). Until recently, parasitoids introduced for CBC were thought to have little or no effect on Insect parasitoids, primarily from the orders Diptera populations of most native species (Coulson et al. and Hymenoptera, are the most common organisms 1991; Godfray 1994; Onstad and McManus 1996). used for the CBC of other arthropods. In the The debate over non-target utilization by parasit- Hymenoptera, several large super-families are exclu- oids has been significantly hampered by the sively parasitic or nearly so (Pennacchio and Strand conflation of frequency of occurrence with the 123 Non-target effects of parasitoids strength of their effects. Most reviews have concen- methodologies used in these studies to assess the trated on the former, which is relatively easy to non-target effects of exotic parasitoids and resolve assess. However, estimating the frequency of non- longstanding issues about the nature and conse- target utilization without assessing impact on their quences of parasitoid drift. population density may lead to exaggerated claims of risk or, conversely, underestimate their importance. Quantitative food webs While dramatic effects on non-target species and even extinctions have been proposed (e.g., Gagne and As early as 1958, the loss of lepidopteran biodiversity Howarth 1985), these claims have often not with- in Hawaii had been attributed to parasitism by exotic stood scrutiny (Lynch and Thomas 2000). Despite biological control agents (Gagne and Howarth 1985; increased attention to this issue, the greatest imped- Howarth 1983). While some have argued that iment to understanding non-target issues is the evidence for this outcome is scant (Lynch and absence of quantitative data on the actual impact or Thomas 2000), there is no doubt that Hawaii has strength of the effect. With few exceptions, non- been the recipient of a large number of CBC target species were not routinely surveyed, and we introductions (Funasaki et al. 1988; Messing and often have no knowledge about their population Wright 2006) and that a significant number of these dynamics prior to introductions of biological control attack Lepidoptera. agents. Thus, implicating an introduced parasitoid in To quantitatively assess the effects of introduced the decline of a native insect will always be difficult parasitoids on native Hawaiian Lepidoptera, Henn- and has been shown with confidence in only a few eman and Memmott (2001) focused on community cases. interactions among plants, lepidopteran herbivores, and their parasitoids. The study was conducted in the remote Alakai swamp, a relatively pristine Hawaiian Quantitatively evaluating non-target effects forest. In the study, 58 species of Lepidoptera were systematically collected and reared from 60 plant As the debate over the relative safety of parasitoids