Abstract
Biological control is a valuable and effective strategy for controlling arthropod pests and has been used extensively against invasive arthropods. As one approach for control of invasives, exotic natural enemies from the native range of a pest are introduced to areas where control is needed. Classical biological control began to be used in the late 1800s and its use increased until, beginning in 1983, scientists began raising significant concerns and questions about nontarget and indirect effects that can be caused by these introductions. In recent years, similar issues have been raised about augmentative use of exotic natural enemies. Subsequently, international guidelines, national regulations and scientific methods being used for exotic natural enemies in biological control have changed to require appropriate specificity testing, risk assessment and regulatory oversight before exotic natural enemies can be released. National and international standards aimed at minimizing risk have increased awareness and promoted more careful consideration of the costs and benefits associated with biological control. The barriers to the implementation of classical and augmentative biological control with exotic natural enemies now are sometimes difficult and, as a consequence, the numbers of classical biological control programs and releases have decreased significantly. Based in part on this new, more careful approach, classical biological control programs more recently undertaken are increasingly aimed at controlling especially damaging invasive arthropod pests that otherwise cannot be controlled. We examine evidence for these revised procedures and regulations aimed at increasing success and minimizing risk. We also discuss limitations linked to the apparent paucity of post-introduction monitoring and inherent unpredictability of indirect effects.
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References
Arnaud PH Jr (1978) A host-parasite catalog of North American Tachinidae (Diptera). USDA Miscellaneous Publication No. 1319
Aukema JE, McCullough DG, Von Holle B, Liebhold AM, Britton K, Frankel SJ (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897
Bale J (2011) Harmonization of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. J Appl Entomol 135:503–513
Barratt BIP, Ferguson CM (2000) Predicting the risk from biological control agent introductions: a New Zealand approach. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer Academic Publishers, Dordrecht, pp 59–75
Barratt BIP, Howarth FG, Withers TM, Kean JM, Ridley GS (2010) Progress in risk assessment for classical biological control. Biol Control 52:245–254
Bauer LS, Duan JJ, Gould JR (2014) Emerald ash borer. In: Van Driesche R, Reardon R (eds) The use of classical biological control to preserve forests in North America. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2013-2, pp 189–209
Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford
Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14:1798–1806
Boyd EA, Hoddle MS (2007) Host specificity testing of Gonatocerus spp. Egg-parasitoids used in a classical biological control program against Homalodisca vitripennis: a retrospective analysis for nontarget impacts in southern California. Biol Control 43:56–70
Cameron PJ, Hill RL, Bain J, Thomas WP (1989) A review of biological control of invertebrate pests and weeds in New Zealand 1874 to 1987. Technical Communication No. 10, CAB International Institute of Biological Control, CAB International, Farnham Royal
Cameron PJ, Hill RL, Teulon DAJ, Stukens MAW, Connolly PG, Walker GP (2013) A retrospective evaluation of the host range of four Aphidius species introduced to New Zealand for the biological control of pest aphids. Biol Control 67:275–283
Clausen CP (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. Agricultural Handbook No. 480. United States Department of Agriculture, Washington DC, USA
Clough Y (2012) A generalized approach to modeling and estimating indirect effects in ecology. Ecology 93:1809–1815
Cock MJW (1985) A review of biological control of pests in the Commonwealth Caribbean and Bermuda up to 1982. Technical Communication No. 9, Commonwealth Institute of Biological Control, Commonwealth Agricultural Bureaux, Farnham Royal, UK
Cock MJW, van Lenteren JD, Brodeur J, Barratt BIP, Bigler F, Bolckmans K, Cônsoli FL, Haas F, Mason PG, Parra JRP (2010) Do new Access and Benefit Sharing procedures under the Convention on Biological Diversity threaten the future of biological control? Biocontrol 55:199–218
Cock MJW, Biesmeijer JC, Cannon RJC, Gerard PJ, Gillespie D, Jiménez JJ, Lavelle PM, Raina SK (2012) The positive contribution of invertebrates to sustainable agriculture and food security. CAB Rev: Perspec Agric, Vet Sci, Nutr Natl Res 7(43)
Collen B, Bohm M, Kemp R, Baillie JEM (2012) Spineless: status and trends of the world’s invertebrates. Zoological Society of London, London
Coutinot D, Briano J, Parra JRP, De Sá LAN, Cônsoli FL (2013) Exchange of natural enemies for biological control: is it a rocky road? The road in the euro-mediterranean region and the South American common market. Neotrop Entomol 42:1–14
Cowie RH (2001) Can snails ever be effective and safe biocontrol agents? Int J Pest Mgmt 47:23–40
De Clerck-Floate RA, Mason PG, Parker DJ, Gillespie DR, Broadbent AB, Boivin G (2006) Guide for the importation and release of arthropod biological control agents in Canada. Pest Management Centre, Agriculture and Agrifood Canada, Minister of Supply and Service Canada, Ottawa
Delfosse ES (2005) Risk and ethics in biological control. Biol Control 35:319–329
Elkinton JS, Boettner GH (2012) Benefits and harm caused by the introduced generalist tachinid, Compsilura concinnata, in North America. Biocontrol 57:277–288
Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647
Evans EW, England S (1996) Indirect interactions in biological control of insects: pests and natural enemies in alfalfa. Ecol Appl 6:920–930
Fisher TW, Andrés LA (1999) Quarantine: concepts, facilities and procedures. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, San Diego, pp 103–124
Follett PA, Duan JJ (eds) (2000) Nontarget effects of biological control. Kluwer Academic Publishers, Dordrecht
Funasaki GY, Lai PY, Nakahara LM, Beardsley JW, Ota AK (1988) A review of biological control introductions in Hawaii: 1890 to 1985. Proc Hawaiian Entomol Soc 28:105–160
Garnas JR, Hurley BP, Slippers B, Wingfield MJ (2012) Biological control of forest plantation pests in an interconnected world requires greater international focus. Int J Pest Manag 58:211–223
Greathead DJ, Greathead AH (1992) Biological control of insect pests by insect parasitoids and predators: the BIOCAT database. Biocon News Info 13:61N–68N
Hajek AE (2004) Natural enemies: an introduction to biological control. Cambridge University Press, Cambridge
Hajek AE, McManus ML, Delalibera Junior I (2007) A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biol Control 41:1–13
Hansen AK, Jeong G, Paine TD, Stouthamer R (2007) Frequency of secondary symbiont infection in an invasive psyllid relates to parasitism pressure on a geographic scale in California. Appl Environ Microbiol 73:7531–7535
Hawkins BA, Marino PC (1997) The colonization of native polyphagous insects in North America by exotic parasitoids. Oecologia 112:566–571
Henne DC, Johnson SJ, Cronin JT (2007) Population spread of the introduced red imported fire ant parasitoid, Pseudacteon tricuspis Borgmeier (Diptera: Phoridae), in Louisiana. Biol Control 42:97–104
Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316
Hoddle MS (2006) Historical review of control programs for Levuana iridescens (Lepidoptera: Zygaenidae) in Fiji and examination of possible extinction of this moth by Bessa remota (Diptera: Tachinidae). Pacif Sci 60:439–453
Hogendoorn K, Keller MA, Baker G (2013) Preparedness for biological control of high-priority arthropod pests. Grape and Wine Research Development Corporation, University of Adelaide, Adelaide, NSW
Holt RD, Hochberg M (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, Wallingford, pp 13–37
Hopper KR (2001) Research needs concerning nontarget impacts of biological control introductions. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI, Wallingford, pp 39–56
Howarth FG (1983) Classical biocontrol: panacea or Pandora’s box. Proc Hawaiian Entomol Soc 24:239–244
Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509
Huang HT, Yang P (1987) The ancient cultured citrus ant. Bioscience 37:665–671
Hunt EJ, Kuhlmann U, Sheppard A, Qin TK, 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 harmonised European system. J Appl Entomol 132:89–123
IPPC (International Plant Protection Convention) (2006) Guidelines for the export, shipment, import and release of biological control agents and other beneficial organisms (2005) International standards for phytosanitary measures No 3. Food and Agriculture Organisation of the United Nations, Rome
IUCN (International Union for Conservation of Nature) (2015) The IUCN Red List of Threatened Species. Version 2015-3. http://www.iucnredlist.org. Accessed 19 Sept 2015
Karban R, Hougen-Eitzmann D, English-Loeb G (1994) Predator-mediated apparent competition between two herbivores that feed on grapevines. Oecologia 97:508–511
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
Kelly J (2012) A review of biological control policy: Northern Ireland and Ireland. Prepared as part of Invasive Species Ireland. The Northern Ireland Environmental Agency and the National Parks and Wildlife Service
Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45
Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35
Kuhlmann U, Mason PG (2003) Use of field host range surveys for selecting candidate nontarget species for physiological host specificity testing of entomophagous biological control agents. In: Van Driesche RG (ed) Proceedings of the 1st international symposium on biological control of arthropods, January 14-18, 2002. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003-05, pp 370–377
Kuris AM (2003) Did biological control cause extinction of the coconut moth, Levuana iridescens, in Fiji? Biol Invasions 5:133–141
Lockwood JA (2000) Nontarget effects of biological control: what are we trying to miss? In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer Acad Publ, Dordrecht, pp 15–30
Lockwood JA, Howarth FG, Purcell MF (eds) (2001) Balancing nature: assessing the impact of importing non-native biological control agents (an International Perspective). Thomas Say Publications in Entomology, Entomol Soc Amer, Lanham, Maryland, USA
Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology, 2nd edn. Wiley-Blackwell, Oxford
Lombaert E, Guillemaud T, Thomas CE, Handley LJL, Li J, Wang S, Pang H, Goryacheva I, Zakharov IA, Jousselin E, Poland RL, Migeon A, van Lenteren J, De Clercq P, Berkvens N, Jones W, Estoup A (2011) Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis. Molec Ecol 20:4654–4670
Loomans AJM (2007) Regulation of invertebrate biological control agents in Europe: review and recommendations in its pursuit of a harmonised regulatory system. Report EU project REBECA (Regulation of Biological Control Agents). The Netherlands
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, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects—The Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396
Lynch LD, Thomas MB (2000) Nontarget effects in the biocontrol of insects with insects, nematodes and microbial agents: the evidence. Biocontr News Info 21:117N–130N
Mason PG, Gillespie DR (eds) (2013) Biological Control Programmes in Canada, 2001–2012. CABI, Wallingford
McCoy E, Frank J (2010) How should the risk associated with the introduction of biological control agents be estimated? Agric For Entomol 12:1–8
McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393
Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4:132–140
Neuenschwander P, Borgemeister C, Langewald J (2003) Biological control in IPM systems in Africa. CABI Publishing, Wallingford
Parry D (2008) Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biol Invasions 11:47–58
Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461
Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298
Price P, Bouton C, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65
Roques A, Rabitsch W, Rasplus J-Y, Lopez-Vaamonde C, Nentwig W, Kenis M (2009) Alien terrestrial invertebrates of Europe. In: Hulme PE, Nentwig W, Pyšek P, Vilà M (eds) DAISIE: handbook of alien species in Europe. Springer, Dordrecht, pp 63–79
Roy HE, Wajnberg E (eds) (2007) From biological control to invasion: the ladybird Harmonia axyridis as a model species. Springer, Dordrecht
Roy HE, Roy DB, Roques A (2011) Inventory of terrestrial alien arthropod predators and parasites established in Europe. Biocontrol 56:477–504
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, Nedvěd O, Ravn HP, Grégoire JC, de Biseau JC, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725
Samways MJ (1988) Classical biological control and conservation: are they compatible? Environ Conserv 15:349–354
Samways MJ (1997) Classical biological control and biodiversity conservation: What risks are we prepared to accept? Biodivers Conserv 6:1309–1316
Sands D, Van Driesche RG (2003) Host range testing techniques for parasitoids and predators. In: Van Driesche RG (ed) Proceedings of the first international symposium on biological control of arthropods: January 14–18, 2002. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003–2005, pp 41–53
Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291
Simberloff D (2012) Risks of biological control for conservation purposes. Biocontrol 57:263–276
Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974
Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122
Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9:e84847
Thomas MB, Casula P, Wilby A (2004) Biological control and indirect effects. Trends Ecol Evol 19:61
Tothill JD, Taylor THC, Paine RW (1930) The Coconut Moth in Fiji—a history of its control by means of its parasites. Imperial Bureaux of Entomology, London
Van Driesche RG, Hoddle M (1997) Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents? Agric Human Val 14:211–226
Van Driesche RG, Reardon R (eds) (2014) The use of classical biological control to preserve forests in North America. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2013-2
Van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies. Blackwell Publishing Limited, Malden
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, Perez Panduro A, Pratt PD, Rayamajhi M, Salom S, Sands D, Schooler S, Schwarzländer M, Sheppard A, Shaw R, Tipping PW, van Klinken RD (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54(Suppl)1:S2–S33
van Klinken RD (2000) Host specficity testing: why do we do it and how can we do it better. In: Van Driesche RG, Heard TA, McClay A, Reardon R (eds) Proceedings of session: host-specificity testing of exotic arthropod biological control agents—the biological basis for improvement in safety. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-99-1, pp 54–68
van Lenteren JC (ed) (2003) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford
van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20
van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006a) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634
van Lenteren JC, Cock MJW, Hoffmeister TS, Sands DPA (2006b) Host specificity in arthropod biological control, methods for testing and interpretation of the data. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford, pp 38–63
van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2008) Harmonia axyridis: an environmental risk assessment for Northwest Europe. Biocontrol 53:37–54
van Lenteren J, Cock MJW, Brodeur J, Barratt BIP, Bigler F, Bolckmans K, Haas F, Mason PG, Parra JRP (2011) Will the convention on biological diversity put an end to biological control? Rev Bras Entomol 55:1–5
van Nouhuys S, Hanski I (2000) Apparent competition between parasitoids mediated by a shared hyperparasitoid. Ecol Lett 3:82–84
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 Mgmt 52:531–540
Wajnberg E, Scott JK, Quimby PC (eds) (2001) Evaluating indirect ecological effects of biological control. CABI, Wallingford
Warner K, Kinslow F (2013) Manipulating risk communication: value predispositions shape public understandings of invasive species science in Hawaii. Public Understand Sci 22:203–218
Waterhouse DF, Sands DPA (2001) Classical biological control of arthropods in Australia. ACIAR Monograph No. 77. Australian Centre for International Agricultural Research, Canberra, Australia
White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455
Wingfield MJ, Brockerhoff EG, Wingfield BD, Slippers B (2015) Planted forest health: the need for a global strategy. Science 349:832–836
Winston RL, Schwarzländer M, Hinz HL, Day MD, Cock MJW, Julien MH (eds) (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2014-04
Wright M, Hoffmann M, Kuhar T, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347
Yara K (2006) Identification of Torymus sinensis and T. beneficus (Hymenoptera: Torymidae), introduced and indigenous parasitoids of the chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae), using the ribosomal ITS2 region. Biol Control 36:15–21
Yara K, Sasawaki T, Kunimi Y (2007) Displacement of Torymus beneficus (Hymenoptera: Torymidae) by T. sinensis, an indigenous and introduced parasitoid of the chestnut gall wasp, Dryocosmus uriphilus (Hymenoptera: Cynipidae), in Japanese chestnut fields: possible involvement in hybridization. Biol Control 42:148–154
Acknowledgments
This paper had its origin at a workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” hosted by the DST-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, in November 2014. We thank Drs. M. J. Samways, J. Gould and R. Van Driesche and two anonymous reviewers for valuable suggestions on an early version of this manuscript.
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Guest editors: Matthew P. Hill, Susana Clusella-Trullas, John S. Terblanche & David M. Richardson / Insect Invasions
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Hajek, A.E., Hurley, B.P., Kenis, M. et al. Exotic biological control agents: A solution or contribution to arthropod invasions?. Biol Invasions 18, 953–969 (2016). https://doi.org/10.1007/s10530-016-1075-8
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DOI: https://doi.org/10.1007/s10530-016-1075-8