Biological Invasions

, Volume 18, Issue 4, pp 953–969 | Cite as

Exotic biological control agents: A solution or contribution to arthropod invasions?

  • Ann E. Hajek
  • Brett P. Hurley
  • Marc Kenis
  • Jeffrey R. Garnas
  • Samantha J. Bush
  • Michael J. Wingfield
  • Joop C. van Lenteren
  • Matthew J. W. Cock
Insect Invasions

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.

Keywords

Exotic biological control agents Nontarget effects Environmental safety Classical biological control Augmentative biological control Host range 

References

  1. Arnaud PH Jr (1978) A host-parasite catalog of North American Tachinidae (Diptera). USDA Miscellaneous Publication No. 1319Google Scholar
  2. 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 60:886–897CrossRefGoogle Scholar
  3. Bale J (2011) Harmonization of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. J Appl Entomol 135:503–513CrossRefGoogle Scholar
  4. 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 59–75CrossRefGoogle Scholar
  5. Barratt BIP, Howarth FG, Withers TM, Kean JM, Ridley GS (2010) Progress in risk assessment for classical biological control. Biol Control 52:245–254CrossRefGoogle Scholar
  6. 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 189–209Google Scholar
  7. Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, WallingfordCrossRefGoogle Scholar
  8. Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14:1798–1806CrossRefGoogle Scholar
  9. 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 43:56–70CrossRefGoogle Scholar
  10. 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 RoyalGoogle Scholar
  11. 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 67:275–283CrossRefGoogle Scholar
  12. 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, USAGoogle Scholar
  13. Clough Y (2012) A generalized approach to modeling and estimating indirect effects in ecology. Ecology 93:1809–1815CrossRefPubMedGoogle Scholar
  14. 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, UKGoogle Scholar
  15. 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 55:199–218CrossRefGoogle Scholar
  16. 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)Google Scholar
  17. Collen B, Bohm M, Kemp R, Baillie JEM (2012) Spineless: status and trends of the world’s invertebrates. Zoological Society of London, LondonGoogle Scholar
  18. 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 42:1–14CrossRefPubMedGoogle Scholar
  19. Cowie RH (2001) Can snails ever be effective and safe biocontrol agents? Int J Pest Mgmt 47:23–40CrossRefGoogle Scholar
  20. 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, OttawaGoogle Scholar
  21. Delfosse ES (2005) Risk and ethics in biological control. Biol Control 35:319–329CrossRefGoogle Scholar
  22. Elkinton JS, Boettner GH (2012) Benefits and harm caused by the introduced generalist tachinid, Compsilura concinnata, in North America. Biocontrol 57:277–288CrossRefGoogle Scholar
  23. Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647CrossRefGoogle Scholar
  24. Evans EW, England S (1996) Indirect interactions in biological control of insects: pests and natural enemies in alfalfa. Ecol Appl 6:920–930CrossRefGoogle Scholar
  25. 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 103–124CrossRefGoogle Scholar
  26. Follett PA, Duan JJ (eds) (2000) Nontarget effects of biological control. Kluwer Academic Publishers, DordrechtGoogle Scholar
  27. 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 28:105–160Google Scholar
  28. 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 58:211–223CrossRefGoogle Scholar
  29. Greathead DJ, Greathead AH (1992) Biological control of insect pests by insect parasitoids and predators: the BIOCAT database. Biocon News Info 13:61N–68NGoogle Scholar
  30. Hajek AE (2004) Natural enemies: an introduction to biological control. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  31. 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 41:1–13CrossRefGoogle Scholar
  32. 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 73:7531–7535CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hawkins BA, Marino PC (1997) The colonization of native polyphagous insects in North America by exotic parasitoids. Oecologia 112:566–571CrossRefGoogle Scholar
  34. 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 42:97–104CrossRefGoogle Scholar
  35. Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316CrossRefPubMedGoogle Scholar
  36. 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 60:439–453CrossRefGoogle Scholar
  37. 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, NSWGoogle Scholar
  38. 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 13–37Google Scholar
  39. 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 39–56Google Scholar
  40. Howarth FG (1983) Classical biocontrol: panacea or Pandora’s box. Proc Hawaiian Entomol Soc 24:239–244Google Scholar
  41. Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509CrossRefGoogle Scholar
  42. Huang HT, Yang P (1987) The ancient cultured citrus ant. Bioscience 37:665–671CrossRefGoogle Scholar
  43. 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 132:89–123CrossRefGoogle Scholar
  44. 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, RomeGoogle Scholar
  45. 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
  46. Karban R, Hougen-Eitzmann D, English-Loeb G (1994) Predator-mediated apparent competition between two herbivores that feed on grapevines. Oecologia 97:508–511CrossRefGoogle Scholar
  47. 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 32:1019–1027CrossRefGoogle Scholar
  48. 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 ServiceGoogle Scholar
  49. 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 11:21–45CrossRefGoogle Scholar
  50. Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35CrossRefGoogle Scholar
  51. 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 370–377Google Scholar
  52. Kuris AM (2003) Did biological control cause extinction of the coconut moth, Levuana iridescens, in Fiji? Biol Invasions 5:133–141CrossRefGoogle Scholar
  53. 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 15–30CrossRefGoogle Scholar
  54. 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, USAGoogle Scholar
  55. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology, 2nd edn. Wiley-Blackwell, OxfordGoogle Scholar
  56. 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 20:4654–4670CrossRefGoogle Scholar
  57. 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 NetherlandsGoogle Scholar
  58. Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRefGoogle Scholar
  59. 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 48:365–396CrossRefPubMedGoogle Scholar
  60. 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–130NGoogle Scholar
  61. Mason PG, Gillespie DR (eds) (2013) Biological Control Programmes in Canada, 2001–2012. CABI, WallingfordGoogle Scholar
  62. McCoy E, Frank J (2010) How should the risk associated with the introduction of biological control agents be estimated? Agric For Entomol 12:1–8CrossRefGoogle Scholar
  63. McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393CrossRefPubMedGoogle Scholar
  64. Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4:132–140CrossRefGoogle Scholar
  65. Neuenschwander P, Borgemeister C, Langewald J (2003) Biological control in IPM systems in Africa. CABI Publishing, WallingfordGoogle Scholar
  66. Parry D (2008) Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biol Invasions 11:47–58CrossRefGoogle Scholar
  67. Pearson DE, Callaway RM (2003) Indirect effects of host-specific biological control agents. Trends Ecol Evol 18:456–461CrossRefGoogle Scholar
  68. Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298CrossRefGoogle Scholar
  69. 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 11:41–65CrossRefGoogle Scholar
  70. 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 63–79CrossRefGoogle Scholar
  71. Roy HE, Wajnberg E (eds) (2007) From biological control to invasion: the ladybird Harmonia axyridis as a model species. Springer, DordrechtGoogle Scholar
  72. Roy HE, Roy DB, Roques A (2011) Inventory of terrestrial alien arthropod predators and parasites established in Europe. Biocontrol 56:477–504CrossRefGoogle Scholar
  73. 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 18:717–725CrossRefGoogle Scholar
  74. Samways MJ (1988) Classical biological control and conservation: are they compatible? Environ Conserv 15:349–354CrossRefGoogle Scholar
  75. Samways MJ (1997) Classical biological control and biodiversity conservation: What risks are we prepared to accept? Biodivers Conserv 6:1309–1316CrossRefGoogle Scholar
  76. 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 41–53Google Scholar
  77. Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291CrossRefPubMedGoogle Scholar
  78. Simberloff D (2012) Risks of biological control for conservation purposes. Biocontrol 57:263–276CrossRefGoogle Scholar
  79. Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974CrossRefGoogle Scholar
  80. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122CrossRefGoogle Scholar
  81. Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9:e84847CrossRefPubMedPubMedCentralGoogle Scholar
  82. Thomas MB, Casula P, Wilby A (2004) Biological control and indirect effects. Trends Ecol Evol 19:61CrossRefPubMedGoogle Scholar
  83. 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, LondonGoogle Scholar
  84. 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 14:211–226CrossRefGoogle Scholar
  85. 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-2013-2Google Scholar
  86. Van Driesche R, Hoddle M, Center T (2008) Control of pests and weeds by natural enemies. Blackwell Publishing Limited, MaldenGoogle Scholar
  87. 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–S33Google Scholar
  88. 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 54–68Google Scholar
  89. van Lenteren JC (ed) (2003) Quality control and production of biological control agents: theory and testing procedures. CABI, WallingfordGoogle Scholar
  90. van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20CrossRefGoogle Scholar
  91. 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 51:609–634CrossRefPubMedGoogle Scholar
  92. 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 38–63CrossRefGoogle Scholar
  93. van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2008) Harmonia axyridis: an environmental risk assessment for Northwest Europe. Biocontrol 53:37–54CrossRefGoogle Scholar
  94. 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 55:1–5Google Scholar
  95. van Nouhuys S, Hanski I (2000) Apparent competition between parasitoids mediated by a shared hyperparasitoid. Ecol Lett 3:82–84CrossRefGoogle Scholar
  96. 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 52:531–540CrossRefGoogle Scholar
  97. Wajnberg E, Scott JK, Quimby PC (eds) (2001) Evaluating indirect ecological effects of biological control. CABI, WallingfordGoogle Scholar
  98. Warner K, Kinslow F (2013) Manipulating risk communication: value predispositions shape public understandings of invasive species science in Hawaii. Public Understand Sci 22:203–218CrossRefGoogle Scholar
  99. Waterhouse DF, Sands DPA (2001) Classical biological control of arthropods in Australia. ACIAR Monograph No. 77. Australian Centre for International Agricultural Research, Canberra, AustraliaGoogle Scholar
  100. White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455CrossRefGoogle Scholar
  101. Wingfield MJ, Brockerhoff EG, Wingfield BD, Slippers B (2015) Planted forest health: the need for a global strategy. Science 349:832–836CrossRefPubMedGoogle Scholar
  102. 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-2014-04Google Scholar
  103. Wright M, Hoffmann M, Kuhar T, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347CrossRefGoogle Scholar
  104. 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 36:15–21CrossRefGoogle Scholar
  105. 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 42:148–154CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Ann E. Hajek
    • 1
  • Brett P. Hurley
    • 2
  • Marc Kenis
    • 3
  • Jeffrey R. Garnas
    • 2
  • Samantha J. Bush
    • 2
  • Michael J. Wingfield
    • 4
  • Joop C. van Lenteren
    • 5
  • Matthew J. W. Cock
    • 6
  1. 1.Department of EntomologyCornell UniversityIthacaUSA
  2. 2.Department of Zoology and Entomology, Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  3. 3.CABIDelémontSwitzerland
  4. 4.Department of Microbiology and Pathology, Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  5. 5.Laboratory of EntomologyWageningen UniversityWageningenThe Netherlands
  6. 6.CABIEghamUK

Personalised recommendations