A REVIEW OF NONTARGET EFFECTS OF INSECT BIOLOGICAL CONTROL AGENTS: CONCEPTS AND EXAMPLES Roy Van Driesche1 and Mark Hoddle2 1Department of Environmental Conservation, University of Massachusetts, Amherst 2Department of Entomology, University of California, Riverside For additional copies of this publication, contact: Richard Reardon U.S. Forest Service Forest Health Technology Enterprise Team 180 Canfield Street Morgantown, WV 26505 (304) 285-1566 [email protected] This publication is available online at http://www.fs.fed.us/foresthealth/technology/ and http://bugwoodcloud.org/resource/pdf/nontarget.pdf Contents Introduction . .1 Types of Impacts . .4 Type 1. Direct Attacks on Native Insects . 4 The concept . .4 Examples . .4 (a) Compsilura concinnati . 4 (b) Microctonus aethiopoides . 6 (c) Trichopoda pennipes (pilipes) . .8 Putting direct attack by parasitoids in context . 10 Mitigation of direct attacks . .10 Type 2. Negative Food Web Effects . 11 The concept . 11 (a) Apparent competition . 11 (b) Displacement via competition for prey . .13 (c) Displacement via competition among parasitoids for hosts . 15 (d) Parasitoid host shifts caused by competitive displacement . 16 Putting risk in context . .16 Mitigation . 17 Type 3. Beneficial Food Web Effects . .17 Type 4. Hybridization with Native Congeners . .20 The concept . 20 Examples . 20 (a) Chrysoperla lacewings . .21 (b) Chestnut gall wasp parasitoids . .21 (c) Laricobius adelgid predators . .22 Putting risk in context . .22 Mitigation . 22 Type 5. Attack on Weed Biocontrol Agents . .23 The concept . 23 Examples . 23 (a) The oligophagous weevil parasitoid, Microctonus aethiopoides . .23 (b) Parasitoids of frugivorous tephritid flies . 23 (c) Predatory phytoseiids attacking spider mites . 24 Putting risk in context . .24 Mitigation . 25 Contents How Common Have Population-level Nontarget Effects Been? . .26 (continued) Group 1. No Impact . .27 Bessa remota and levuana moth . 27 Australian mealybug parasitoids in New Zealand . 28 Citrus blackfly parasitoids on the island of Dominica . .28 Neotropical phytoseiid, Typhlodromalus airpo, in Africa . .28 Parasitoids attacking the endemic Hawaiian moth Udea stellata . 28 Peristenus digoneutis Loan (Hymenoptera: Braconidae) . .29 Torymus sinensis Kamijo (Hymenoptera: Torymidae) in Italy . .30 Rodolia cardinalis in the Galápagos . 30 Pteromalus puparum on Bassaris butterflies in New Zealand . 31 Trigonospila brevifacies in New Zealand . 32 Trichopoda giacomellii (Diptera: Tachinidae) . .32 Parasitoids of frugivorous and native gall making tephritids in Hawaii . .33 Group 2. Direct Trophic Impact . 33 Tamarixia (formerly Tetrastichus) dryi in La Réunion . .33 Brachymeria lasus and two native butterflies on Guam . .33 Cotesia glomerata in the Canary Islands . 34 Peristenus relictus Loan (= P. stygicus) and the western tarnished plant bug . 34 Group 3. Displacement or Other Indirect Impacts . 34 Cotesia flavipes Cameron in Trinidad and Brazil . 35 Aphytis holoxanthus DeBach (Hymenoptera: Aphelinidae) . 35 Cales noacki Howard (Hymenoptera: Aphelinidae) . 36 Trigonospila brevifacies (Hardy) (Diptera: Tachinidae) . .36 Diadegma semiclausum (Hymenoptera: Ichneumonidae) . .37 Parasitoids introduced into the United States against tobacco whitefly . .38 Looking Ahead: What Impacts Will New Parasitoid/Predator Introductions Have on Nontarget Species? . .39 Forecasting Likely Host Use . 39 Moving from Host Use to Population-level Effects . .41 From Host Impact to Determination of a Project’s Risks and Benefits . .41 Recent Practice (1985-2016) as Predictor of Future Nontarget Impacts . 42 Contents Concluding Remarks . .45 (continued) Caveats and Clarifications . .45 Guides for Future Thinking . .46 Acknowledgments . .47 References . .48 Appendix 1 . .89 Apendix 2 . .121 INTRODUCTION Whether, when, and how frequently introductions this article opened a conversation on the potential of biological control agents have important environmental effects of classical biological population-level effects on nontarget species control, it did not provide a definitive answer. is a question of continuing importance to both Further discussion of this issue ensued in the biological control scientists and conservation following decades (Follett and Duan, 2000; Follett biologists. This issue was first raised by Howarth et al., 2000; van Lenteren and Loomans, 2000; (1991), who outlined evidence for significant Louda et al., 2003; Hoddle 2004a,b,c; Stewart nontarget impacts from biological control agents. and New, 2007; Parry, 2009; Barratt et al., 2010; While breaking new ground in raising the issue, Suckling and Sforza, 2014). this article was, in our opinion, flawed. First, Here we focus on potential nontarget impacts of rather than assessing whether nontarget impacts parasitoids and predacious arthropods introduced had occurred regularly or to what degree on as classical biological control agents. The impacts average, Howarth (1991) advocated strongly of these agents are less understood than those of for the proposition that they had occurred, herbivorous insects and pathogens released against supporting the article’s assertion by selectively invasive plants. Releases of plant biocontrol agents assembling instances of possible impact. are well documented (Winston et al., 2014), and While it alerted society to this unintended risk, population-level impacts of herbivorous biocontrol Howarth (1991) did little to objectively assess agents on native plants have been rare (Suckling the magnitude of the problem posed by natural and Sforza, 2014). Analysis of all 512 species enemy introductions. Second, the author grouped known to have been released for weed biocontrol vertebrate introductions, some made as far back worldwide found no evidence of impact for 99% as the 1700s by farmers, with introductions of of the agents. Of the few known cases of impacts, biological control agents made by government most (>90%) were only of minor importance, scientists after biological control began to develop without long-term harm to nontarget plant as a science (post 1920s). This greatly enhanced populations. Important population-level effects the perceived negative impact of biological are known only in the cases of some thistle and control as most vertebrate introductions for pest cacti-attacking insects, principally Cactoblastis control did cause ecological damage. Third, the cactorum (Bergroth) (Figure 1A,B) on some native article did not adequately differentiate between cacti (Figure 2) (Stiling et al., 2004; Pemberton simple use (feeding or parasitism to any degree) and Liu, 2007) and Rhinocyllus conicus Fröelich and evidence-based, population-level impacts (Figure 3) on some native thistles (Figure 4) on nontarget species. Fourth, Howarth (1991) (Louda, 1998; Louda et al. 2005). In contrast, greatly overstated the risk of extinctions from for parasitoids and predators, whose actions are introductions, by emphasizing the effects of generally invisible to any but specialists, we have vertebrate and mollusk introductions, as opposed less information on population-level impacts. This to arthropods (e.g., herbivores, parasitoids, and has led to speculation that nontarget impacts are predators) that are used most commonly for high, based largely on extrapolation from several biocontrol of pest plants and arthropods. While INTRODUCTION A Figure 2. Opuntia hemifusa, attacked by Cactoblastis cactorum in Florida (photo of Kristen E. Sauby). B Figure 3. An oligophagous thistle feeding weevil, Rhinocyllus conicus (photo of Eric Coombs, Oregon Department of Agriculture, Bugwood.org). Figure 1. Cactoblastis cactorum larvae (A) (photo of Ignacio Baez, USDA Agricultural Research Service, Bugwood.org); feeding damage (B) (photo of Rebekah D. Wallace, University of Georgia, Bugwood.org). Figure 4. A rare native thistle, Cirsium canescens, fed on by Rhinocyllus conicus (photo of Irene Shonle). INTRODUCTION cases of likely or presumed high-level impact, Seventeen cases (17/5,000 = 0.34%), however, especially the coccinellid beetles Harmonia were classified as causing population reductions axyridis (Pallas) and Coccinella septempunctata or other severe impacts. (However, below, we (L.) (Harmon et al., 2007; Losey et al., 2007) and show that some of these cases were in fact of the tachinid flies Compsilura concinnata (Meigen) no ecological concern). No credible cases of (Boettner et al., 2000) and Bessa remota (Aldrich) extinction were found; one such case is claimed (Kuris, 2003; Hoddle, 2006), as discussed below. by Howarth (1991), but see Hoddle (2006). For introduced parasitoids and predators successfully Past summaries of impacts of parasitoids and established in Florida (Frank and McCoy, 2007), predators on nontarget insects and mites include grouping cases by 20-yr intervals (data from a mini-review for the island of Guam (Nafus Table 4 in Frank and McCoy, 2007), found no 1993a); global literature reviews (Lynch and detectable trend in either the average severity of Thomas, 2000; van Lenteren et al., 2006), and impacts (categories 1 through 6) or the frequency a detailed analysis of releases of both weed and of instances in high-impact categories suggestive insect biocontrol agents in Florida (Frank and of population-level effects; there were 2 to 5 such McCoy, 2007). Lynch and Thomas (2000) state events per 20-yr period. No further reviews of that nontarget effects are recorded for 1.7% of the nontarget effects of insect biocontrol have been ca 5000 recorded cases of parasitoid