Abstract
Striking successes in classical biological control in agriculture and rangelands engender great interest in using this technology for wildlands conservation and environmental purposes. However, well known unintended consequences of several biological control projects have led to concern that possible environmental benefits do not warrant inherent risks. Four risks demand attention: (1) direct attack on non-targets; (2) indirect effects on non-targets; (3) dispersal of a biocontrol agent to a new area, either autonomously or with deliberate or inadvertent human assistance; (4) changed relationships between a control agent and a native species, particularly as generated by global climate change. Procedures for assessing risk of direct attack on non-targets by phytophagous biological control agents have steadily improved and an expanded centrifugal phylogenetic approach appears to provide adequate insight. Direct non-target impacts by entomophages are more difficult to predict. Myriad possible indirect effects, some subtle but nonetheless important, present a far greater challenge, and techniques of assessing such risks are in their earliest infancy and not as closely regulated. Despite prominent examples in both the general invasion literature and that for biological control, the risk that a species, once introduced, will spread beyond its intended range, and the consequences of such spread, are not routinely treated by risk assessors. This phenomenon deserves far more attention. Global changes—especially climate change—can lead to modified ranges and efficacies of introduced biological control agents and their targets. Although many examples show that climatic niches are often not conserved, an important first routine step would be to combine climatic envelopes with general circulation models for predicted future climates. Finally, actions based on a risk assessment are always implemented in a framework of predicted costs and benefits, which are inevitably asymmetric, so it is critically important that all stakeholders, including conservationists, participate in the decision-making process.
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References
Asner GP, Vitousek PM (2005) Remote analysis of biological invasion and biogeochemical change. Proc Nat Acad Sci (USA) 102:4383–4386
Babendreier D, Bigler F, Kuhlmann U (2006) Current status and constraints in the assessment of non-target effects. In: Bigler E, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. Methods and risk assessment. CABI Publishing, Wallingford, pp 1–14
Barratt BIP, Howarth FG, Withers TM, Kean M, Ridley GS (2010) Progress in risk assessment for classical biological control. Biol Control 52:245–254
Bauer LS, Liu H-P (2007) Oobius agrili (Hymenoptera: Encyrtidae), a solitary egg parasitoid of emerald ash borer from China. In: Proceedings of the 2006 Emerald Ash Borer Research and Technology Development Meeting, Cincinnati. U.S.D.A. Forest Service FHTET-2007-04, pp 63–64
Bauer LS, Liu H, Miller D, Gould J (2008) Developing a classical biological control program for Agrilus planipennis (Coleoptera: Buprestidae), an invasive ash pest in North America. Newsl Michigan Entomol Soc 53:38–39
Beaumont LJ, Gallagher RV, Thuiller W, Downey PO, Leishman MR, Hughes L (2009) Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers Distrib 15:409–420
Bezemer TM, Jones TH (1998) Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82:212–222
Bigler F, Kölliker-Ott UM (2006) Balancing environmental risks and benefits: a basic approach. In: Bigler E, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. Methods and risk assessment. CABI Publishing, Wallingford, pp 273–290
Booth RG, Cross AE, Fowler SV, Shaw RH (2001) Case study 5.24. Biological control of an insect to save an endemic tree on St. Helena. In: Wittenberg R, Cock MJW (eds) Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford, p 192
Bradley BA, Wilcove DS, Oppenheimer M (2010) Climate change increases risk of plant invasion in the Eastern United States. Biol Invasions 12:1855–1872
Broennimann O, Guisan A (2008) Predicting current and future biological invasions: both native and invaded ranges matter. Biology Letters 4:584–589
Broennimann O, Treier UA, Müller-Schärer H, Thuiller W, Peterson AT, Guisan A (2007) Evidence of climatic shift during biological invasion. Ecol Lett 10:701–709
Buisson L, Thuiller W, Casajus N, Lek S, Grenouillet G (2010) Uncertainty in ensemble forecasting of species distribution. Global Change Biol 16:1145–1157
Callaway RM, DeLuca TH, Belliveau WM (1999) Biological-control herbivores may increase competitive ability of the noxious weed Centaurea maculosa. Ecology 80:1196–1201
Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071
Caltagirone LE, Doutt RL (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Ann Rev Entomol 34:1–16
Carson R (1962) Silent spring. Houghton Mifflin, Boston
Caut S, Casanovas JG, Virgos E, Lozano J, Witmer GW, Courchamp F (2007) Rats dying for mice: modelling the competitor release effect. Austral Ecol 32:858–868
Center TD, Frank JH, Dray FA Jr (1997) Biological control. In: Simberloff D, Schmitz DC, Brown TC (eds) Strangers in paradise. Impact and management of nonindigenous species in Florida. Island Press, Washington, DC, pp 245–263
Cheah CAS-J, McClure MS (2000) Seasonal synchrony of life cycles between the exotic predator, Pseudoscymnus tsugae (Coleoptera: Coccinellidae) and its prey, the hemlock woolly adelgid Adelges tsugae (Homoptera: Adelgidae). Agricult Forest Entomol 2:241–251
Cheah C, Montgomery M, Salem S, Parker B, Skinner M, Costa S (2004) Biological control of hemlock woolly adelgid. FHTET-2004–2004. U.S.D.A. Forest Service, Morgantown
Chew M (2009) The monstering of tamarisk: How scientists made a plant into a problem. J Hist Biol 42:231–266
Civeyrel L, Simberloff D (1996) A tale of two snails: is the cure worse than the disease? Biodiver Conserv 5:1231–1252
Colautti RI, Niimi AJC, van Overdijk DA, Mills EL, Holeck K, MacIsaac HJ (2003) Spatial and temporal analysis of transoceanic shipping vectors to the Great Lakes. In: Ruiz GM, Carlton JT (eds) Invasive species. Vectors and management strategies. Island Press, Washington, D.C, pp 227–246
Courchamps F, Langlais M, Sugihara G (1999) Cats protecting birds: modelling the mesopredator release effect. J Anim Ecol 68:282–292
Cowie RH (2002) Invertebrate invasions on Pacific islands and the replacement of unique native faunas: a synthesis of the land and freshwater snails. Biol Invasions 3:119–136
Cowie RH (2011) Snails and slugs. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 634–643
D’Antonio CM, Mack M (2001) Exotic grasses potentially slow invasion of N-fixing tree into a Hawaiian woodland. Biol Invasions 3:69–73
D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann Rev Ecol Syst 23:63–87
Dark S (2009) Beetles attack! City Weekly (Salt Lake City, Utah), March 11. http://www.cityweekly.net/utah/article-7512-beetles-attack.html, accessed 21 Dec 2010
DeLoach CJ (1990) Prospects for biological control of saltcedar (Tamarix spp.) in riparian habitats of the southwestern United States. In: Delfosse ES (ed) Proceedings of the VII international symposium on biological control of weeds, 6–11 March 1988, Rome, Italy. Istituto Sperimentale per la Patologia Vegetale. Ministero dell’Agricoltura e delle Foreste, Rome, Italy, pp 307–314
DeLoach CJ, Knutson AE, Moran PJ, Michels GDJ, Thompson DC, Carruthers RI, Nibling F, Fain TG (2007) Biological control of saltcedar (Cedro salado) (Tamarix spp.) in the United States, with implications for Mexico. In: Lira-Saldiar RH (ed), Bioplaguicidas y control biológico. Simposia Internacional de Agricultura Sustentable, 23–26 October 2007, Saltillo, Mexico. Centro de Investigación en Química Aplicada, Universidad Autónoma Agraria Antonio Narro, Saltillo, Coahuila, Mexico, pp 142–172
Dhileepan K, Bayliss D, Treviño M (2010) Thermal tolerance and potential distribution of Carvalhotingis visenda (Hemiptera: Tingidae), a biological control agent for cat’s claw creeper, Macfadyena unguis-cati (Bignoniaceae). Bull Entomol Res 100:159–166
DiTomaso JM (1998) Impact, biology, and ecology of saltcedar (Tamarix spp.) in the southwestern United States. Weed Technol 12:326–336
Dodd AP (1940) The biological campaign against prickly pear. Commonwealth Prickly Pear Board Bulletin, Brisbane, Australia
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80
Fitzpatrick MC, Weltzin JF, Sanders NJ, Dunn RR (2007) The biogeography of prediction error: why does the introduced range of the fire ant over-predict its native range? Global Ecol Biogeog 16:24–33
Freinkel S (2007) American chestnut. The life, death, and rebirth of a perfect tree. University of California Press, Berkeley
Goldson SL (2007) Climate change and biological control. In: Paul C, Newton D, Carran RA, Edwards GR, Niklaus PA (eds) Agroecosystems in a changing climate. CRC Press, Boca Raton, pp 329–332
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009
Hawaiian Ecosystems at Risk (2010) http://www.hear.org/species/morella_faya/, accessed 28 Nov 2010
Hays WST, Conant S (2007) Biology and impacts of Pacific island invasive species. 1. A worldwide review of effects of the small Indian mongoose, Herpestes javanicus (Carnivora: Herpestidae). Pacific Sci 61:3–16
Hespenheide HA (1996) Buprestidae. In: Llorente BJ, Garcia AAN, González SE (eds) Biodiversidad, taxonomia y biogeografia de artrópodos de México. Hacia una Síntesis de su Conocimiento. Universidad Nacional de México, Instituto de Biología, Mexico City, pp 411–421
Hill JK, Hodkinson ID (1992) Effects of temperature on phenological synchrony and altitudinal distribution of jumping plant lice (Hemiptera; Psylloidea) on dwarf willow (Salix lapponum) in Norway. Ecol Entomol 20:237–244
Holt RD, Hochberg ME (2001) Indirect interactions, community modules and biological control: a theoretic perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI, Wallingford, pp 13–37
Huffaker CB, Kennett CE (1959) A ten-year study of vegetation changes associated with biological control of Klamath weed. J Range Mgt 12:69–82
Julien MH, Center TD, Tipping PW (2002) Floating fern (Salvinia). In: van Driesche R, Blossey B, Hoddle M, Lyon S, Reardon R (eds) Biological control of invasive plants in the Eastern United States (FHTET-2002–2004). United States Department of Agriculture Forest Service. Forest Health Technology Enterprise Team, Morgantown, Morgantown, pp 17–32
Karban R, Hougen-Eitzmann D, English-Loeb G (1994) Predator-mediated apparent competition between two herbivores that feed on grapevines. Oecologia 97:508–511
Koch RL, Glavan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35
Koch RL, Venette RC, Hutchinson WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: Implications for South America. Neotropical Entomol 35:421–434
Krivánek M, Pyšek P, Jarosik V (2006) Planting history and propagule pressure as predictors of invasion by woody species in a temperate region. Conserv Biol 20:1487–1498
Kuhlmann U, Schaffner U, Mason PG (2006) Selection of non-target species for host specificity testing. In: Bigler E, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. Methods and risk assessment. CABI Publishing, Wallingford, pp 15–37
Liu H-P, Bauer LS (2007) Tetrastichus planipennisi (Hymenoptera: Eulophidae), a gregarious larval endoparasitoid of emerald ash borer from China. In: Proceedings of the 2006 emerald ash borer research and technology development meeting, Cincinnati. U.S.D.A. Forest Service FHTET-2007-04, pp 61–62
Loo SE, MacNally R, Lake PS (2007) Forecasting New Zealand mud snail invasion range: model comparisons using native and invaded ranges. Ecol Applic 17:181–189
Louda SM, O’Brien CW (2002) Unexpected ecological effects of distributing the exotic weevil, Larinus planus (F.), for biological control of Canada thistle. Conserv Biol 16:717–727
Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090
Louda SM, Arnett AE, Rand A, Russell FL (2003) Invasiveness of some biological control insects and adequacy of their ecological risk assessment and regulation. Conserv Biol 17:73–82
Lowe S, Browne M, Boudjelas S (2001) 100 of the world’s worst invasive alien species. A selection from the global invasive species database. IUCN-ISSG, Auckland
Mack MC, D’Antonio CM (2003) The effects of exotic grasses on litter decomposition in a Hawaiian woodland: the importance of indirect effects. Ecosystems 6:723–738
Mack MC, D’Antonio CM, Ley RE (2001) Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C4 grasses in Hawaii. Ecol Applic 11:1323–1335
Marsico TD, Wallace LE, Ervin.N, Brooks CP, McClure JE, Welch ME (2011) Geographic patterns of genetic diversity from the native range of Cactoblastis cactorum (Berg) support the documented history of invasion and multiple introductions for invasive populations. Biol Invasions 13:857–868
Master LL, Stein BA, Kutner LS, Hammerson GA (2000) Vanishing assets. Conservation status of U.S. species. In: Stein BA, Kutner LS, Adams JS (eds) Precious heritage. The status of biodiversity in the United States. Oxford University Press, New York, pp 93–118
Mead C, Kaldor J, Canton M, Gamer G, Crerar S, Thomas S (1996) Rabbit calicivirus and human health. Department of Primary Industries and Energy, Australian Government, Canberra
Medley KA (2010) Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Global Ecol Biogeogr 19:122–133
Messing RH (2001) Centrifugal phylogeny as a basis for non-target host testing in biological control: is it relevant for parasitoids? Phytoparasitica 29:187–189
Messing R, Roitberg B, Brodeur J (2006) Measuring and predicting indirect impacts of biological control: competition, displacement and secondary interactions. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, pp 64–77
Mulvaney M (2001) The effect of introduction pressure on the naturalization of ornamental woody plants in south-eastern Australia. In: Panetta FD, Virtue JG, Groves RH (eds) Weed risk assessment. CSIRO Publishing, Collingwood, pp 186–193
Murphy ST, Evans HC (2009) Biological control of invasive species. In: Clout MN, Williams PA (eds) Invasive species management. A handbook of principles and techniques. Oxford University Press, Oxford, pp 77–92
NatureServe (2010) http://www.natureserve.org. Accessed 5 Nov 2010
New Zealand Parliamentary Commissioner for the Environment (1998) The rabbit calicivirus (RCD) saga: a biosecurity/bio-control fiasco. Parliamentary Commissioner for the Environment, Wellington
Orrell TM, Weigt L (2005) The northern snakehead Channa argus (Anabantomorpha: Channidae), a non-indigenous fish species in the Potomac River. USA Proc Biol Soc Washington 118:407–415
Ortega Y, Pearson DE, McKelvey KS (2004) Effects of biological control agents and exotic plant invasion on deer mouse populations. Ecol Applic 14:241–253
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
Pearson DE, Callaway RM (2003) Indirect effects of host-specifc biological control agents. Trends Ecol Evol 18:456–461
Pemberton RW (1984) Native plant considerations in the biological control of leafy spurge. In: Delfosse ES (ed) Proceedings of the VI international symposium for the biological control, August 19–25. Agriculture Canada, Vancouver, pp 365–390
Pemberton RW (1995) Cactoblastis cactorum (Lepidoptera: Pyralidae) in the United States: an immigrant biological control agent or an introduction of the nursery industry? Amer Entomol 41:230–232
Pemberton RW (2000) Predictable risk to native plants in weed biological control. Oecologia 125:489–494
Peterson AT, Soberón J, Sánchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267
Rafter MA, Wilson AJ, Wilmot Senaratne KAD, Dhileepan K (2008) Climatic-requirements models of cat’s claw creeper Macfadyena unguis-cati (Bignoniaceae) to prioritise areas for exploration and release of biological control agents. Biol Control 44:169–179
Rödder D, Lötters S (2009) Niche shift versus niche conservatism? Climatic characteristics of the native and invasive ranges of Mediterranean house gecko. Global Ecol Biogeogr 18:674–687
Room PM, Forno IW, Taylor MFJ (1984) Establishment in Australia of two insects for biological control of the floating weed Salvinia molesta. Bull Entomol Res 74:505–516
Roy H, Wajnberg E (2008) From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl 53:1–4
Schneider DW, Ellis CD, Cummings KS (1998) A transportation model assessment of risk to native mussel communities of zebra mussel spread. Conserv Biol 12:788–800
Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens C (2004) A hotspot of non-native aquarium fishes: evidence for the aquarium trade as an invasion pathway. Mar Ecol Progr Ser 266:239–244
Simberloff D (1992) Conservation of pristine habitats and unintended effects of biological control. In: Kauffman WC, Nechols JE (eds) Selection criteria and biological consequences of importing natural enemies. Entomological Society of America, Baltimore, pp 103–114
Simberloff D (2005) The politics of assessing risk for biological invasions: the USA as a case study. Trends Ecol Evol 20:216–222
Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268
Simberloff D, Stiling P (1996) Risks of species introduced for biological control. Biol Conserv 78:185–192
Simmonds FJ, Bennett FP (1966) Biological control of Opuntia spp. by Cactoblastis cactorum in the Leeward Islands (West Indies). Entomophaga 11:183–189
Smith CW (2002) Forest pest biological control program in Hawaii. In: Smith CW, Denslow J, Hight S (eds), Proceedings of workshop on biological control of native ecosystems in Hawaii. Pacific Cooperative Studies Unit (University of Hawaii at Manoa, Department of Botany) Technical Report 129. University of Hawaii at Manoa, Manoa, pp 91–98
Strauss SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6:206–210
Sutherst RW, Maywald GF, Bourne AS (2004) CLIMEX Version 2. User’s guide. Hearne Scientific Software Inc, Melbourne
Thomson LJ, Macfadyen S, Hoffmann AA (2010) Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 54:296–306
Thorpe AS, Archer V, DeLuca TH (2006) The invasive forb, Centaurea maculosa, increases phosphorus availability in Montana grasslands. Appl Soil Ecol 23:118–122
Tuduri JCG, Martorell LF, Gaud SM (1971) Geographical distribution and host plants of the cactus moth, Cactoblastis cactorum (Berg) in Puerto Rico and the United States Virgin Islands. J Agric Univ Puerto Rico 55:130–134
U.S. Department of Agriculture (2010) Memorandum: USDA APHIS PPQ Moratorium for biological control of saltcedar (Tamarix species) using the biological control agent Diorhabda species (Coleoptera: Chrysomelidae). June 10, Riverdale, Maryland
U.S. Department of the Interior (Fish and Wildlife Service) (1997) Endangered and threatened wildlife and plants; Determination of Endangered status for two tidal marsh plants—Cirsium hydrophilum var. hydrophilum (Suisun Thistle) and Cordylanthus mollis ssp. mollis (Soft Bird’s-Beak) from the San Francisco Bay area of California. 50 CFR Part 17, Federal Register 62(224):61916–61921
van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies. An introduction to biological control. Blackwell, Malden
van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, Van Rijn PCJ, Thomas MB, Tommasini MG, Zeng Q-Q (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38
van Nouhuys S, Lei G (2004) Parasitoid–host metapopulation dynamics: the causes and consequences of phenological asynchrony. J Anim Ecol 73:526–535
Vitousek PM (1986) Biological invasions and ecosystem properties: can species make a difference? In: Mooney HA, Drake JA (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 163–176
Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawai’i: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265
Vitousek PM, Walker LR, Whittaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804
Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201–211
Whitfield JB, Wagner DL (1988) Patterns in host ranges within the Nearctic species of the parasitoid genus Pholetesor Mason (Hymenoptera: Braconidae). Environm Entomol 17:608–615
Wootton JT (1994) Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–165
Yang Z-Q, Wang X-Y, Gould JR, Wu H (2008) Host specificity of Spathius agrili Yang (Hymenoptera: Braconidae), an important parasitoid of the emerald ash borer. Biol Control 47:216–221
Zavaleta ES (2002) It’s often better to eradicate, but can we eradicate better? In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN Species Survival Commission, Gland, Switzerland, pp 393–403
Zilahi-Balogh GMG, Kok LT, Salom SM (2002) Host specificity of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a potential biological control agent of the hemlock woolly adelgid, Adelges tsugae Annand (Homoptera: Adelgidae). Biol Control 24:192–198
Zimmermann HG, Moran VC, Hoffmann JH (2000) The renowned cactus moth, Cactoblastis cactorum: its natural history and threat to native Opuntia in Mexico and the United States of America. Diversity Distrib 6:259–269
Zwölfer H, Harris P (1971) Host specificity determination of insects for biological control of weeds. Annu Rev Entomol 16:159–178
Zwölfer H, Harris P (1984) Biology and host specificity of Rhinocyllus conicus (Froel.)(Col., Curculionidae), a successful agent for biocontrol of the thistle, Carduus nutans. Zeitschr Angewandte Entomol 97:36–62
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Roy van Driesche encouraged me to write this paper, while Lucy Jordan, Tom Dudley, and Henry Hespenheide provided important information on particular cases. Two anonymous referees provided useful comments on an early draft.
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Simberloff, D. Risks of biological control for conservation purposes. BioControl 57, 263–276 (2012). https://doi.org/10.1007/s10526-011-9392-4
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DOI: https://doi.org/10.1007/s10526-011-9392-4