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Published in: BioControl 1/2018

12-09-2017

Shifting paradigms in the history of classical biological control

Authors: George E. Heimpel, Matthew J. W. Cock

Published in: BioControl | Issue 1/2018

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Abstract

Classical biological control using insects has led to the partial or complete control of at least 226 invasive insect and 57 invasive weed species worldwide since 1888. However, at least ten introductions of biological control agents have led to unintended negative consequences and these cases have led to a focus on risk that came to dominate the science and practice of classical biological control by the 1990s. Based upon historical developments in the field we consider that the era of focus on benefits began in 1888 and that it was supplanted by an era in which the focus was on risks during the 1990s. This paradigm shift greatly improved the safety of biological control releases but also led to a decline in the number of introductions, probably resulting in opportunity costs. We note here the development of a third paradigm: one in which the benefits and risks of biological control are clearly and explicitly balanced so that decisions can be made that maximize benefits while minimizing risks.

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Literature
go back to reference Andraca-Gomez G, Ordano M, Boege K, Dominguez CA, Pinero D, Perez-Ishiwara R, Perez-Camacho J, Canizares M, Fornoni J (2015) A potential invasion route of Cactoblastis cactorum within the Caribbean region matches historical hurricane trajectories. Biol Invasions 17:1397–1406CrossRef Andraca-Gomez G, Ordano M, Boege K, Dominguez CA, Pinero D, Perez-Ishiwara R, Perez-Camacho J, Canizares M, Fornoni J (2015) A potential invasion route of Cactoblastis cactorum within the Caribbean region matches historical hurricane trajectories. Biol Invasions 17:1397–1406CrossRef
go back to reference Barratt BIP, Moeed A (2005) Environmental safety of biological control: policy and practice in New Zealand. Biol Control 35:247–252 Barratt BIP, Moeed A (2005) Environmental safety of biological control: policy and practice in New Zealand. Biol Control 35:247–252
go back to reference Beddington JR, Free CA, Lawton JH (1978) Characteristics of successful natural enemies in models of biological control of insect pests. Nature 273:513–519CrossRefPubMed Beddington JR, Free CA, Lawton JH (1978) Characteristics of successful natural enemies in models of biological control of insect pests. Nature 273:513–519CrossRefPubMed
go back to reference Benson J, van Driesche RG, Pasquale A, Elkinton J (2003) Introduced braconid parasitoids and range reduction of a native butterfly in New England. Biol Control 28:197–213CrossRef Benson J, van Driesche RG, Pasquale A, Elkinton J (2003) Introduced braconid parasitoids and range reduction of a native butterfly in New England. Biol Control 28:197–213CrossRef
go back to reference Bigler F, Kölliker-Ott UM (2006) Balancing environmental risks and benefits: a basic approach. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Oxon, pp 273–286CrossRef Bigler F, Kölliker-Ott UM (2006) Balancing environmental risks and benefits: a basic approach. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Oxon, pp 273–286CrossRef
go back to reference Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publising, Oxon Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publising, Oxon
go back to reference Blower SM, Koelle K, Kirschner DE, Mills J (2001) Live attenuated HIV vaccines: predicting the tradeoff between efficacy and safety. Proc Natl Acad Sci USA 98:3618–3623CrossRefPubMedPubMedCentral Blower SM, Koelle K, Kirschner DE, Mills J (2001) Live attenuated HIV vaccines: predicting the tradeoff between efficacy and safety. Proc Natl Acad Sci USA 98:3618–3623CrossRefPubMedPubMedCentral
go back to reference Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14:1798–1806CrossRef Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14:1798–1806CrossRef
go back to reference Caltagirone LE, Doutt RL (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Annu Rev Entomol 34:1–16CrossRef Caltagirone LE, Doutt RL (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Annu Rev Entomol 34:1–16CrossRef
go back to reference Carvalheiro LG, Buckley YM, Ventim R, Fowler SV, Memmott J (2008) Apparent competition can compromise the safety of highly specific biological control agents. Ecol Lett 11:690–700CrossRefPubMed Carvalheiro LG, Buckley YM, Ventim R, Fowler SV, Memmott J (2008) Apparent competition can compromise the safety of highly specific biological control agents. Ecol Lett 11:690–700CrossRefPubMed
go back to reference Civeyrel L, Simberloff D (1996) A tale of two snails: is the cure worse than the disease? Biodivers Conserv 5:1231–1252CrossRef Civeyrel L, Simberloff D (1996) A tale of two snails: is the cure worse than the disease? Biodivers Conserv 5:1231–1252CrossRef
go back to reference Cock MJW, Day RK, Hinz H, Pollard KM, Thomas SE, Williams FE, Witt ABR, Shaw RH (2015) The impacts of some classical biological control successes. CAB Rev 10:1–57 Cock MJW, Day RK, Hinz H, Pollard KM, Thomas SE, Williams FE, Witt ABR, Shaw RH (2015) The impacts of some classical biological control successes. CAB Rev 10:1–57
go back to reference Cock MJW, Murphy ST, Kairo MTK, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. BioControl 61:349–363CrossRef Cock MJW, Murphy ST, Kairo MTK, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. BioControl 61:349–363CrossRef
go back to reference Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–298CrossRefPubMed Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–298CrossRefPubMed
go back to reference Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeen S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260CrossRef Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeen S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260CrossRef
go back to reference Crawley MJ (1989) The successes and failures of weed biocontrol using insects. Biocontrol News Info 10:213–223 Crawley MJ (1989) The successes and failures of weed biocontrol using insects. Biocontrol News Info 10:213–223
go back to reference Culliney TW (2005) Benefits of classical biological control for managing invasive plants. Crit Rev Pl Sci 24:131–150CrossRef Culliney TW (2005) Benefits of classical biological control for managing invasive plants. Crit Rev Pl Sci 24:131–150CrossRef
go back to reference De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698CrossRef De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698CrossRef
go back to reference Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30CrossRef Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30CrossRef
go back to reference Ehlers R-U (2011) Regulation of biological control agents and the EU policy support action REBECA. In: Ehlers R-U (ed) Regulation of biological control agents. Springer, Dordrecht, pp 2–23CrossRef Ehlers R-U (2011) Regulation of biological control agents and the EU policy support action REBECA. In: Ehlers R-U (ed) Regulation of biological control agents. Springer, Dordrecht, pp 2–23CrossRef
go back to reference Esler KJ, van Wilgen BW, te Roller K, Wood AR, van der Merwe JH (2010) A landscape-level assessment of the long-term integrated control of an invasive shrub in South Africa. Biol Invasions 12:211–218CrossRef Esler KJ, van Wilgen BW, te Roller K, Wood AR, van der Merwe JH (2010) A landscape-level assessment of the long-term integrated control of an invasive shrub in South Africa. Biol Invasions 12:211–218CrossRef
go back to reference Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647CrossRef Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647CrossRef
go back to reference Follett PA, Duan JJ (2000) Nontarget effects of biological control. Kluwer Academic Publishers, Norwell Follett PA, Duan JJ (2000) Nontarget effects of biological control. Kluwer Academic Publishers, Norwell
go back to reference Greathead DJ, Greathead AH (1992) Biological control of insects pests by insect parasitoids and predators: the BIOCAT database. Biocontrol News Inf 13:61N–67N Greathead DJ, Greathead AH (1992) Biological control of insects pests by insect parasitoids and predators: the BIOCAT database. Biocontrol News Inf 13:61N–67N
go back to reference Gurr GM, Wratten SD (2000) Biological control: measures of success. Kluwer, Dordrecht Gurr GM, Wratten SD (2000) Biological control: measures of success. Kluwer, Dordrecht
go back to reference Gutierrez AP, Caltagirone LE, Meikle W (1999) Evaluation of results, economics of biological control. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic, San Diego, pp 243–252CrossRef Gutierrez AP, Caltagirone LE, Meikle W (1999) Evaluation of results, economics of biological control. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic, San Diego, pp 243–252CrossRef
go back to reference Hajek AE, McManus ML, Junior ID (2005) Catalogue of introductions of pathogens and nematodes for classical biological control of insects and mites. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown Hajek AE, McManus ML, Junior ID (2005) Catalogue of introductions of pathogens and nematodes for classical biological control of insects and mites. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown
go back to reference Hajek AE, McManus DP, Delalibera I Jr (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13CrossRef Hajek AE, McManus DP, Delalibera I Jr (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13CrossRef
go back to reference Hall RW, Ehler LE (1979) Rate of establishment of natural enemies in classical biological control. Bull Entomol Soc Am 25:280–282 Hall RW, Ehler LE (1979) Rate of establishment of natural enemies in classical biological control. Bull Entomol Soc Am 25:280–282
go back to reference Hall RW, Ehler LE, Bisabri-Ershadi B (1980) Rate of success in classical biological control of arthropods. Bull Entomol Soc Am 26:111–114 Hall RW, Ehler LE, Bisabri-Ershadi B (1980) Rate of success in classical biological control of arthropods. Bull Entomol Soc Am 26:111–114
go back to reference Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Ins Cons 11:85–94CrossRef Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Ins Cons 11:85–94CrossRef
go back to reference Harrison L, Moeed A, Sheppard A (2005) Regulation of the release of biological control agents of arthropods in New Zealand and Australia. In: Hoddle M (ed) International symposium on biological control of arthropods. US Forest Service, Davos, pp 715–725 Harrison L, Moeed A, Sheppard A (2005) Regulation of the release of biological control agents of arthropods in New Zealand and Australia. In: Hoddle M (ed) International symposium on biological control of arthropods. US Forest Service, Davos, pp 715–725
go back to reference Hawkins BA, Cornell HV (1994) Maximum parasitism rates and successful biological control. Science 266:1886CrossRefPubMed Hawkins BA, Cornell HV (1994) Maximum parasitism rates and successful biological control. Science 266:1886CrossRefPubMed
go back to reference Heimpel GE, Mills NJ (2017) Biological control: ecology and applications. Cambridge University Press, CambridgeCrossRef Heimpel GE, Mills NJ (2017) Biological control: ecology and applications. Cambridge University Press, CambridgeCrossRef
go back to reference Heimpel GE, Yang Y, Hill J, Ragsdale DW (2013) Environmental consequences of invasive species: greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. PLoS ONE 8(8):e72293CrossRefPubMedPubMedCentral Heimpel GE, Yang Y, Hill J, Ragsdale DW (2013) Environmental consequences of invasive species: greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. PLoS ONE 8(8):e72293CrossRefPubMedPubMedCentral
go back to reference Hennemann ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316CrossRef Hennemann ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316CrossRef
go back to reference Hill R, Campbell D, Hayes L, Corin S, Fowler S (2013) Why the New Zealand regulatory system for introducing new biological control agents works. In: XIII International Symposium on Biological Control of Weeds, vol 2011. Waikoloa, Hawaii, USA, pp 75–83 Hill R, Campbell D, Hayes L, Corin S, Fowler S (2013) Why the New Zealand regulatory system for introducing new biological control agents works. In: XIII International Symposium on Biological Control of Weeds, vol 2011. Waikoloa, Hawaii, USA, pp 75–83
go back to reference Hinz H, Schwartzlander M, Gassmann A, Bourchier RS (2014) Successes we may not have had: a retrospective analysis of selected weed biological control agents in the United States. Inv Plant Sci Manag 7:565–579CrossRef Hinz H, Schwartzlander M, Gassmann A, Bourchier RS (2014) Successes we may not have had: a retrospective analysis of selected weed biological control agents in the United States. Inv Plant Sci Manag 7:565–579CrossRef
go back to reference Hoddle MS, Crespo Ramirez C, Hoddle CD, Loayza J, Lincango PM, van Driesche RG, Causton CE (2013) Post release evaluation of Rodolia cardinalis (Coleoptera: Coccinellidae) for control of Icerya purchasi (Hemiptera: Monophlebidae) in the Galapagos Islands. Biol Control 67:262–274CrossRef Hoddle MS, Crespo Ramirez C, Hoddle CD, Loayza J, Lincango PM, van Driesche RG, Causton CE (2013) Post release evaluation of Rodolia cardinalis (Coleoptera: Coccinellidae) for control of Icerya purchasi (Hemiptera: Monophlebidae) in the Galapagos Islands. Biol Control 67:262–274CrossRef
go back to reference Holt RD, Hochberg ME (2001) Indirect interactions: community modules and biological control: a theoretical perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Press, Oxon, pp 13–38 Holt RD, Hochberg ME (2001) Indirect interactions: community modules and biological control: a theoretical perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Press, Oxon, pp 13–38
go back to reference Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509CrossRef Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509CrossRef
go back to reference Hunt EJ, Kuhlmann U, Sheppard A, Qin T-K, Barratt BIP, Harrison L, Mason PG, Parker D, Flanders RV, Goolsby J (2008) Review of invertebrate biological control agent regulation in Australia, New Zealand, Canada and the USA: recommendations for a harmonized European system. J Appl Entomol 132:89–123CrossRef Hunt EJ, Kuhlmann U, Sheppard A, Qin T-K, Barratt BIP, Harrison L, Mason PG, Parker D, Flanders RV, Goolsby J (2008) Review of invertebrate biological control agent regulation in Australia, New Zealand, Canada and the USA: recommendations for a harmonized European system. J Appl Entomol 132:89–123CrossRef
go back to reference Kaser JM, Heimpel GE (2015) Linking risk and efficacy in biological control host-parasitoid models. Biol Control 90:49–60CrossRef Kaser JM, Heimpel GE (2015) Linking risk and efficacy in biological control host-parasitoid models. Biol Control 90:49–60CrossRef
go back to reference Kaser JM, Ode PJ (2016) Hidden risks and benefits of natural enemy mediated indirect effects. Curr Opin Ins Sci 14:105–111CrossRef Kaser JM, Ode PJ (2016) Hidden risks and benefits of natural enemy mediated indirect effects. Curr Opin Ins Sci 14:105–111CrossRef
go back to reference Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol Invasion 6:301–318CrossRef Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol Invasion 6:301–318CrossRef
go back to reference Lane SD, Mills NJ, Getz WM (1999) The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data. Ecol Ent 24:181–190CrossRef Lane SD, Mills NJ, Getz WM (1999) The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data. Ecol Ent 24:181–190CrossRef
go back to reference Lazo-Langer JA, Rodger MA, Barrowman NJ, Ramsay T, Wells PS, Coyle DA (2012) Comparing multiple competing interventions in the absence of randomized trials using clinical risk-benefit analysis. BMC Med Res Meth 12:3CrossRef Lazo-Langer JA, Rodger MA, Barrowman NJ, Ramsay T, Wells PS, Coyle DA (2012) Comparing multiple competing interventions in the absence of randomized trials using clinical risk-benefit analysis. BMC Med Res Meth 12:3CrossRef
go back to reference Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. BioScience 56:311–323CrossRef Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. BioScience 56:311–323CrossRef
go back to reference Louda SM, O’Brien CW (2002) Unexpected ecological effects of distributing the exotic weevil, Larinus planus (F.), for the biological control of Canada thistle. Cons Biol 16:717–727CrossRef Louda SM, O’Brien CW (2002) Unexpected ecological effects of distributing the exotic weevil, Larinus planus (F.), for the biological control of Canada thistle. Cons Biol 16:717–727CrossRef
go back to reference Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRef Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRef
go back to reference Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects-the Achilles’ heel of biological control? Annu Rev Entomol 48:365–396CrossRefPubMed Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects-the Achilles’ heel of biological control? Annu Rev Entomol 48:365–396CrossRefPubMed
go back to reference Luck RF (1990) Evaluation of natural enemies for biological control: a behavioral approach. Trends Ecol Evol 5:196–199CrossRef Luck RF (1990) Evaluation of natural enemies for biological control: a behavioral approach. Trends Ecol Evol 5:196–199CrossRef
go back to reference Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht
go back to reference Maron M, Cockfield G (2008) Managing trade-offs in landscape restoration and revegetation projects. Ecol Appl 18:2041–2049CrossRefPubMed Maron M, Cockfield G (2008) Managing trade-offs in landscape restoration and revegetation projects. Ecol Appl 18:2041–2049CrossRefPubMed
go back to reference McBride MF, Wilson KA, Burger J, Fang YC, Lulow M, Olson D, O’Connell M, Possingham HP (2010) Mathematical problem definition for ecological restoration planning. Ecol Modell 221:2243–2250CrossRef McBride MF, Wilson KA, Burger J, Fang YC, Lulow M, Olson D, O’Connell M, Possingham HP (2010) Mathematical problem definition for ecological restoration planning. Ecol Modell 221:2243–2250CrossRef
go back to reference McEvoy PB, Coombs EV (2000) Why things bite back: unintended consequences of biological weed control. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Dordrecht, pp 167–194CrossRef McEvoy PB, Coombs EV (2000) Why things bite back: unintended consequences of biological weed control. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Dordrecht, pp 167–194CrossRef
go back to reference Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4:132–140CrossRef Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4:132–140CrossRef
go back to reference Mills NJ (2006) Accounting for differential success in the biological control of homopteran and lepidopteran pests. N Zeal J Ecol 30:61–72 Mills NJ (2006) Accounting for differential success in the biological control of homopteran and lepidopteran pests. N Zeal J Ecol 30:61–72
go back to reference Minckley WL, Deacon JE (1968) Southwestern fishes and the enigma of ‘endangered species’. Science 159:1424–1432CrossRefPubMed Minckley WL, Deacon JE (1968) Southwestern fishes and the enigma of ‘endangered species’. Science 159:1424–1432CrossRefPubMed
go back to reference Moeed A, Hickson R, Barratt BIP (2006) Principles of environmental risk assessment with emphasis on the New Zealand perspective. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Oxon, pp 241–253 Moeed A, Hickson R, Barratt BIP (2006) Principles of environmental risk assessment with emphasis on the New Zealand perspective. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Oxon, pp 241–253
go back to reference Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125:344–366CrossRef Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125:344–366CrossRef
go back to reference Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645CrossRefPubMed Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645CrossRefPubMed
go back to reference Neuenschwander P (2001) Biological control of the cassava mealybug in Africa: a review. Biol Control 21:214–229CrossRef Neuenschwander P (2001) Biological control of the cassava mealybug in Africa: a review. Biol Control 21:214–229CrossRef
go back to reference Paynter QE, Fowler SV, Gourlay AH, Haines ML, Harman HM, Hona SR, Peterson PG, Smith LA, Wilson-Davey JRA, Winks CJ, Withers TM (2004) Safety in New Zealand weed biocontrol: a nationwide survey for impacts on non-target plants. New Zeal Plant Prot 57:102–197 Paynter QE, Fowler SV, Gourlay AH, Haines ML, Harman HM, Hona SR, Peterson PG, Smith LA, Wilson-Davey JRA, Winks CJ, Withers TM (2004) Safety in New Zealand weed biocontrol: a nationwide survey for impacts on non-target plants. New Zeal Plant Prot 57:102–197
go back to reference Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461CrossRef Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461CrossRef
go back to reference Pearson DE, Callaway RM (2006) Biological control agents elevate hantavirus by subsidizing deer mouse populations. Ecol Lett 9:443–450CrossRefPubMed Pearson DE, Callaway RM (2006) Biological control agents elevate hantavirus by subsidizing deer mouse populations. Ecol Lett 9:443–450CrossRefPubMed
go back to reference Pemberton RW (2000) Predictable risks to native plants in weed biological control. Oecologia 125:489–494CrossRefPubMed Pemberton RW (2000) Predictable risks to native plants in weed biological control. Oecologia 125:489–494CrossRefPubMed
go back to reference Rose KE, Louda SM, Rees M (2005) Demographic and evolutionary impacts of native and invasive insect herbivores on Cirsium canescens. Ecology 86:453–465CrossRef Rose KE, Louda SM, Rees M (2005) Demographic and evolutionary impacts of native and invasive insect herbivores on Cirsium canescens. Ecology 86:453–465CrossRef
go back to reference Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, van Vlaenderen J, Nedved O, Ravn HP, Gregoire J-C, de Biseau J-C, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distr 18:717–725CrossRef Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, van Vlaenderen J, Nedved O, Ravn HP, Gregoire J-C, de Biseau J-C, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distr 18:717–725CrossRef
go back to reference Seaman GA, Randall JE (1962) The mongoose as a predator in the Virgin Islands. J Mammol 43:544–546CrossRef Seaman GA, Randall JE (1962) The mongoose as a predator in the Virgin Islands. J Mammol 43:544–546CrossRef
go back to reference Sheppard AW, Hill R, DeClerck-Floate RA, McClay A, Olckers T, Quimby PCJ, Zimmermann HG (2003) A global review of risk-benefit-cost analysis for the introduction of classical biological control agents against weeds: a crisis in the making? Biocontrol News Info 24:91N–108N Sheppard AW, Hill R, DeClerck-Floate RA, McClay A, Olckers T, Quimby PCJ, Zimmermann HG (2003) A global review of risk-benefit-cost analysis for the introduction of classical biological control agents against weeds: a crisis in the making? Biocontrol News Info 24:91N–108N
go back to reference Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974CrossRef Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974CrossRef
go back to reference Stephens AE, Srivastava DS, Myers JH (2013) Strength in numbers? Effects of multiple natural enemy species on plant performance. Proc R Soc London B 280:20122756CrossRef Stephens AE, Srivastava DS, Myers JH (2013) Strength in numbers? Effects of multiple natural enemy species on plant performance. Proc R Soc London B 280:20122756CrossRef
go back to reference Stiling P (1990) Calculating the establishment rates of parasitoids in classical biological control. Am Entomol 1990(Fall):225–230CrossRef Stiling P (1990) Calculating the establishment rates of parasitoids in classical biological control. Am Entomol 1990(Fall):225–230CrossRef
go back to reference Stiling P (1993) Why do natural enemies fail in classical biological control programs? Am Entomol 39:31–37CrossRef Stiling P (1993) Why do natural enemies fail in classical biological control programs? Am Entomol 39:31–37CrossRef
go back to reference Stiling P, Moon D, Gordon D (2004) Endangered cactus restoration: mitigating the non-target effects of a biological control agent (Cactoblastis cactorum) in Florida. Restor Ecol 12:605–610CrossRef Stiling P, Moon D, Gordon D (2004) Endangered cactus restoration: mitigating the non-target effects of a biological control agent (Cactoblastis cactorum) in Florida. Restor Ecol 12:605–610CrossRef
go back to reference Story JM, Smith L, Corn JG, White LJ (2008) Influence of seed head-attacking biological control agents on spotted knapweed reproductive potential in western Montana over a 30-year period. Environ Entomol 37:510–519CrossRefPubMed Story JM, Smith L, Corn JG, White LJ (2008) Influence of seed head-attacking biological control agents on spotted knapweed reproductive potential in western Montana over a 30-year period. Environ Entomol 37:510–519CrossRefPubMed
go back to reference Suckling DM (2013) Benefits from biological control of weeds in New Zealand range from negligible to massive: a retrospective analysis. Biol Control 66:27–32CrossRef Suckling DM (2013) Benefits from biological control of weeds in New Zealand range from negligible to massive: a retrospective analysis. Biol Control 66:27–32CrossRef
go back to reference Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biological control agents? Annu Rev Entomol 47:561–594CrossRefPubMed Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biological control agents? Annu Rev Entomol 47:561–594CrossRefPubMed
go back to reference Tipping PW, Martin MR, Nimmo KR, Pierce RM, Smart MD, White EB, Madeira PT (2009) Invasion of a West Everglades wetland by Melaleuca quinquenervia countered by classical biological control. Biol Control 48:73–78CrossRef Tipping PW, Martin MR, Nimmo KR, Pierce RM, Smart MD, White EB, Madeira PT (2009) Invasion of a West Everglades wetland by Melaleuca quinquenervia countered by classical biological control. Biol Control 48:73–78CrossRef
go back to reference Urban MC, Phillips BL, Skelly DK, Shine R (2007) The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc R Soc London B 274:1413–1419CrossRef Urban MC, Phillips BL, Skelly DK, Shine R (2007) The cane toad’s (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proc R Soc London B 274:1413–1419CrossRef
go back to reference van Driesche RG, Hoddle M (1997) Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents? Agric Hum Val 14:211–226CrossRef van Driesche RG, Hoddle M (1997) Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents? Agric Hum Val 14:211–226CrossRef
go back to reference van Driesche R, Reardon R (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. FHTET, USDA Forest Service, Morgantown van Driesche R, Reardon R (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. FHTET, USDA Forest Service, Morgantown
go back to reference van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith L, Wagner DL, Blossey B, Brancatini V, Casagrande R, Causton CE, Coetzee JA, Cuda J, Ding J, Fowler SV, Frank JH, Fuester R, Goolsby J, Grodowitz M, Heard TA, Hill MP, Hoffmann JH, Huber J, Julien M, Kairo MTK, Kenis M, Mason P, Medal J, Messing R, Miller R, Moore A, Neuenschwander P, Newman R, Norambuena H, Palmer WA, Pemberton R, Panduro AP, Pratt PD, Rayamajhi M, Salom S, Sands D, Schooler S, Schwarzlander M, Sheppard A, Shaw R, Tipping PW, van Klinken RD (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:S2–S33CrossRef van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith L, Wagner DL, Blossey B, Brancatini V, Casagrande R, Causton CE, Coetzee JA, Cuda J, Ding J, Fowler SV, Frank JH, Fuester R, Goolsby J, Grodowitz M, Heard TA, Hill MP, Hoffmann JH, Huber J, Julien M, Kairo MTK, Kenis M, Mason P, Medal J, Messing R, Miller R, Moore A, Neuenschwander P, Newman R, Norambuena H, Palmer WA, Pemberton R, Panduro AP, Pratt PD, Rayamajhi M, Salom S, Sands D, Schooler S, Schwarzlander M, Sheppard A, Shaw R, Tipping PW, van Klinken RD (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:S2–S33CrossRef
go back to reference van Driesche R, Simberloff D, Blossey B, Causton C, Hoddle M, Marks C, Heinz K, Wagner D, Warner K (2016) Integrating biological control into conservation practice. Wiley, Oxford van Driesche R, Simberloff D, Blossey B, Causton C, Hoddle M, Marks C, Heinz K, Wagner D, Warner K (2016) Integrating biological control into conservation practice. Wiley, Oxford
go back to reference van Klinken RD, Edwards OR (2002) Is host-specificity of weed biological control agents likely to evolve rapidly following establishment? Ecol Lett 5:590–596CrossRef van Klinken RD, Edwards OR (2002) Is host-specificity of weed biological control agents likely to evolve rapidly following establishment? Ecol Lett 5:590–596CrossRef
go back to reference 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 QQ (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38CrossRef 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 QQ (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38CrossRef
go back to reference van Lenteren JC, Bale J, Bigler F, Hokkanen HMT (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634CrossRefPubMed van Lenteren JC, Bale J, Bigler F, Hokkanen HMT (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634CrossRefPubMed
go back to reference van Wilgen BW, Moran VC, Hoffmann JH (2013) Some perspectives on the risks and benefits of biological control of invasive alien plants in the management of natural ecosystems. Environ Manag 52:531–540CrossRef van Wilgen BW, Moran VC, Hoffmann JH (2013) Some perspectives on the risks and benefits of biological control of invasive alien plants in the management of natural ecosystems. Environ Manag 52:531–540CrossRef
go back to reference Wajnberg E, Scott JK, Quimby PC (2001) Evaluating indirect ecological effects of biological control. CABI Press, Wallingford Wajnberg E, Scott JK, Quimby PC (2001) Evaluating indirect ecological effects of biological control. CABI Press, Wallingford
go back to reference Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201–211CrossRef Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201–211CrossRef
go back to reference Wiggering H, Dalchow C, Glemnitz M, Helming K, Muller K, Schultz A, Stachow U, Zander P (2006) Indicators for multifunctional land use—Linking socio-economic requirements with landscape potentials. Ecolog Indicat 6:238–249CrossRef Wiggering H, Dalchow C, Glemnitz M, Helming K, Muller K, Schultz A, Stachow U, Zander P (2006) Indicators for multifunctional land use—Linking socio-economic requirements with landscape potentials. Ecolog Indicat 6:238–249CrossRef
go back to reference Winston RL, Schwartzlander M, Hinz H, Day MD, Cock MJW, Julien MH (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. USDA Forest Service, Forest Heath Technology Enterprise Team, Morgantown Winston RL, Schwartzlander M, Hinz H, Day MD, Cock MJW, Julien MH (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. USDA Forest Service, Forest Heath Technology Enterprise Team, Morgantown
go back to reference Wright MG, Hoffmann MP, Kuhar TP, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347CrossRef Wright MG, Hoffmann MP, Kuhar TP, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347CrossRef
Metadata
Title
Shifting paradigms in the history of classical biological control
Authors
George E. Heimpel
Matthew J. W. Cock
Publication date
12-09-2017
Publisher
Springer Netherlands
Published in
BioControl / Issue 1/2018
Print ISSN: 1386-6141
Electronic ISSN: 1573-8248
DOI
https://doi.org/10.1007/s10526-017-9841-9

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