BioControl

, Volume 56, Issue 4, pp 681–698

Benefits and risks of exotic biological control agents

  • Patrick De Clercq
  • Peter G. Mason
  • Dirk Babendreier
Article

Abstract

The use of exotic (=alien) arthropods in classical and augmentative biological control programs has yielded huge economic and ecological benefits. Exotic species of arthropods have contributed to the suppression of key pests in agriculture and forestry or have aided in restoring natural systems affected by adventive species. However, adverse non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, e.g. 2% parasitization on a non-target insect on a local level, to massive effects on a large scale. Until now, no consensus on how to judge the magnitude of non-target effects and whether these effects can be tolerated or are unacceptable has emerged. In this paper, we briefly review both the benefits of biological control as well as the associated risks including to human and animal health, plant health and particularly the environment. We also make an attempt at identifying the major challenges for assessing risks and for balancing benefits and risks. There is general agreement that sound risk assessment procedures should precede the release of exotic invertebrate biological control agents and a recent shift—especially for arthropod biological control—from introductions done without meaningful risk assessment studies to projects conducting thorough host range testing can be observed. However, overly stringent regulations that would preclude promising agents from being developed must be avoided.

Keywords

Augmentative biological control Augmentation Classical biological control Exotic species Non-target effects Risk assessment Risk-benefit analysis 

References

  1. Adriaens T, San Martin y Gomez G, Maes D (2008) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl 53:69–88CrossRefGoogle Scholar
  2. Aebi A, Brown PMJ, De Clercq P, Hautier L, Howe A, Ingels B, Ravn H-P, Sloggett JJ, Zindel R, Thomas A (2011) Detecting arthropod intraguild predation in the field. BioControl. doi:10.1007/s10526-011-9378-2
  3. Albajes R, Castañé C, Gabarra R, Alomar O (2006) Risks of plant damage caused by natural enemies introduced for arthropod biological control. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford, UK, pp 132–144CrossRefGoogle Scholar
  4. Alomar O, Wiedenmann RN (eds) (1996) Zoophytophagous Heteroptera: Implications for life history and integrated pest management. Proceedings of Thomas Say publications in entomology, Entomological Society of America, Lanham, MDGoogle Scholar
  5. Andreassen LD, Kuhlmann U, Mason PG, Holliday NJ (2009) Host range testing of a prospective classical biological control agent against cabbage maggot in Canada. Biol Control 48:210–220CrossRefGoogle Scholar
  6. Arnó J, Castañé C, Riudavets J, Gabarra R (2010) Risk of damage to tomato crops by the generalist zoophytophagous predator Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae). Bull Entomol Res 100:105–115PubMedCrossRefGoogle Scholar
  7. Babendreier B (2007) Pros and cons of biological control. In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 403–418Google Scholar
  8. Babendreier D, Bigler F (2005) How to assess non-target effects of polyphagous biological control agents: Trichogramma brassicae as a case study. In: Proceedings of the second international symposium on biological control of arthropods, 12–16 September 2005, USDA Forest Service FHTET-2005-08, Davos, Switzerland, pp 603–610Google Scholar
  9. Babendreier D, Kuske S, Bigler F (2003a) Non-target host acceptance and parasitism by Trichogramma brassicae (Hymenoptera: Trichogrammatidae) under laboratory conditions. Biol Control 26:128–138CrossRefGoogle Scholar
  10. Babendreier D, Kuske S, Bigler F (2003b) Overwintering of the egg parasitoid Trichogramma brassicae (Hym.: Trichogrammatidae) in Northern Switzerland. BioControl 48:261–273CrossRefGoogle Scholar
  11. Babendreier D, Kuske S, Bigler F (2003c) Parasitism of non-target butterflies by Trichogramma brassicae (Hymenoptera: Trichogrammatidae) under semifield and field conditions. Biol Control 26:139–145CrossRefGoogle Scholar
  12. Babendreier D, Bigler F, Kuhlmann U (2005) Methods used to assess non-target effects of invertebrate biological control agents of arthropod pests. BioControl 50:821–870CrossRefGoogle Scholar
  13. Bale JS (2011a) Harmonisation of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions. J Appl Entomol doi:10.1111/j.1439-0418.2011.01611.x
  14. Bale JS (2011b) Regulation of invertebrate biological control agents in Europe: recommendations for a harmonized approach. In: Ehlers R-U (ed) Regulation of biological control agents in Europe. Springer, Dordrecht, pp 323–373CrossRefGoogle Scholar
  15. Bale JS, van Lenteren JC, Bigler F (2008) Biological control and sustainable food production. Phil Trans R Soc B 363:761–776PubMedCrossRefGoogle Scholar
  16. Barratt BIP, Blossey B, Hokkanen HMT (2006) Post-release evaluation of non-target effects of biological control agents. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford, UK, pp 166–186CrossRefGoogle Scholar
  17. 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
  18. Barron MC, Barlow ND, Wratten SD (2003) Non-target parasitism of the endemic New Zealand red admiral butterfly (Bassaris gonerilla) by the introduced biological control agent Pteromalus puparum. Biol Control 27:329–335CrossRefGoogle Scholar
  19. Beaulieu F (2009) Review of the mite genus Gaeolaelaps Evans & Till (Acari: Laelapidae), and description of a new species from North America, G. gillespiei n. sp. Zootaxa 2158:33–49Google Scholar
  20. Benson J, Pasquale A, van Driesche RG, Elkinton J (2003) Assessment of risk posed by introduced braconid wasps to Pieris virginiensis, a native woodland butterfly in New England. Biol Control 26:83–93CrossRefGoogle Scholar
  21. Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2008) Pollen as an alternative food for Harmonia axyridis. BioControl 53:201–210CrossRefGoogle Scholar
  22. Berkvens N, Landuyt C, Deforce K, Berkvens D, Tirry L, De Clercq P (2010) Alternative foods for the multicoloured Asian lady beetle Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 107:189–195CrossRefGoogle Scholar
  23. 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, Wallingford, UK, pp 273–286CrossRefGoogle Scholar
  24. Bigler F, Babendreier D, Kuhlmann U (eds) (2006) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UKGoogle Scholar
  25. Bjørnson S (2008) Natural enemies of the convergent lady Hippodamia convergens Guérin-Méneville: their inadvertent importation and potential significance for augmentative biological control. Biol Control 44:305–311CrossRefGoogle Scholar
  26. Blossey B, Skinner LC, Taylor J (2001) Impact and management of purple loosestrife (Lythrum salicaria) in North America. Biodivers Conserv 10:1787–1807CrossRefGoogle Scholar
  27. 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
  28. Boivin G, Kölliker-Ott UM, Bale J, Bigler F (2006) Assessing the establishment potential of inundative biological control agents. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford, UK, pp 98–113CrossRefGoogle Scholar
  29. Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE (2011a) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240CrossRefGoogle Scholar
  30. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley L-J (2011b) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl. doi:10.1007/s10526-011-9379-1
  31. Calvo J, Bolckmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. BioControl 54:237–246CrossRefGoogle Scholar
  32. Cock MJW (2003) Risks of non-target impact versus stakeholder benefits in classical biological control of arthropods: selected case studies from developing countries. In: van Driesche RG (ed) Proceedings of the international symposium on biological control of arthropods, Honolulu, Hawaii, 14–18 January 2002, United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003-05, pp 25–33Google Scholar
  33. Cock MJW, Kuhlmann U, Schaffner U, Bigler F, Babendreier D (2006) The usefulness of the ecoregion concept for safer import of invertebrate biological control agents. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UK, pp 202–221CrossRefGoogle Scholar
  34. Coulson JR (2000a) Chapter I 1883–1933. In: Coulson JR, Vail PV, Dix ME, Nordlund DA, Kauffman WC (eds) 110 years of biological control research in the United States Department of Agriculture 1883–1993. United States Department of Agriculture, Agriculture Research Service, Washington, DC, pp 6–14Google Scholar
  35. Coulson JR (2000b) Chapter IV 1973–1993. In: Coulson JR, Vail PV, Dix ME, Nordlund DA, Kauffman WC (eds) 110 years of biological control research in the United States Department of Agriculture 1883–1993. United States Department of Agriculture, Agriculture Research Service, Washington, DC, pp 44–99Google Scholar
  36. Coulson JR, Day WH (2000) Chapter III 1953–1972. In: Coulson JR, Vail PV, Dix ME, Nordlund DA, Kauffman WC (eds) 110 years of biological control research in the United States Department of Agriculture 1883–1993. United States Department of Agriculture, Agriculture Research Service, Washington, DC, pp 23–43Google Scholar
  37. Coutanceau JP (2006) Harmonia axyridis (Pallas, 1773): une Coccinelle asiatique introduite, acclimatée et en extension en France. Bull Soc Entomol Fr 111:395–401Google Scholar
  38. De Clercq P, Bale JS (2011) Risks of invertebrate biological control agents—Harmonia axyridis as a case study. In: Ehlers R-U (ed) Regulation of biological control agents in Europe. Springer, Dordrecht, pp 243–255CrossRefGoogle Scholar
  39. Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. BioControl 46:387–400CrossRefGoogle Scholar
  40. EPPO (2010) List of biological control agents widely used in the EPPO region. EPPO standards on safe use of biological control PM 6/3—version 2010. http://archives.eppo.org/EPPOStandards/biocontrol_web/bio_list.htm#biolist
  41. Evans EW, Soares AO, Yasuda H (2011) Invasive Coccinellidae and other predatory Coleoptera. BioControl. doi:10.1007/s10526-011-9374-6
  42. Galvan TL, Burkness EC, Hutchison WD (2007) Enumerative and binomial sequential sampling plans for the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in wine grapes. J Econ Entomol 100:1000–1010PubMedCrossRefGoogle Scholar
  43. Gassmann A, Louda SM (2001) Rhinocyllus conicus: initial evaluation and subsequesnt ecological impacts in North America. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishng, Wallingford, pp 147–183Google Scholar
  44. Gerson U, Smiley RL, Ochoa R (2003) Mites (Acari) for pest control. Blackwell Science, Oxford, UKCrossRefGoogle Scholar
  45. Gillespie DR, Shipp JL, Raworth DA, Foottit RG (2002) Aphis gossypii Glover, melon/cotton aphid, Aulacorthum solani (Kaltenbach), foxglove aphid, Macrosiphum euphorbiae (Thomas), potato aphid, and Myzus persicae (Sulzer), green peach aphid (Homoptera: Aphididae). In: Mason PG, Huber JT (eds) Biological control programmes in Canada, 1981–2000. CABI Publishing, Wallingford, UK, pp 44–49Google Scholar
  46. Goettel MS, Inglis GD (2006) Methods for assessment of contaminants of invertebrate biological control agents and associated risks. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UK, pp 145–165CrossRefGoogle Scholar
  47. Goldson SL, McNeill MR, Proffitt JR, Barratt BIP (2005) Host specificity testing and suitability of a European biotype of the braconid parasitoid Microctonus aethiopoides Loan as a biological control agent against Sitona lepidus (Coleoptera: Curculionidae) in New Zealand. Biocontrol Sci Technol 15:791–813CrossRefGoogle Scholar
  48. Griffiths DA (1999) Biological control of mites. In: Albajes R, Gullino ML, van Lenteren JC, Elad Y (eds) Integrated pest management in greenhouse crops. Kluwer Academic, Boston, pp 217–234CrossRefGoogle Scholar
  49. Gullino ML, Albajes R, van Lenteren JC (1999) Setting the stage: characteristics of protected cultivation and tools for sustainable crop protection. In: Albajes R, Gullino ML, van Lenteren JC, Elad Y (eds) Integrated pest management in greenhouse crops. Kluwer Academic, Boston, pp 1–15CrossRefGoogle Scholar
  50. Harlequin Ladybird Survey (2010) http://www.harlequin-survey.org/. Accessed on 1 April 2011
  51. Harmon JP, Stephens E, Losey J (2007) The decline of native ladybirds (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Conserv 11:85–94CrossRefGoogle Scholar
  52. Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316PubMedCrossRefGoogle Scholar
  53. Hoddle MS (2003) Classical biological control of arthropods in the 21st century. In: van Driesche RG (ed) Proceedings of the international symposium on biological control of arthropods, Honolulu, Hawaii, 14–18 January 2002, United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003-05, pp 3–16Google Scholar
  54. Hoddle MS (2004) Restoring balance: using exotic species to control invasive exotic species. Conserv Biol 18:38–49CrossRefGoogle Scholar
  55. 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). Pac Sci 60:439–453CrossRefGoogle Scholar
  56. Hoddle MS, Syrett P (2002) Realizing the potential of classical biological control. In: Hallman GJ, Schwalbe CP (eds) Invasive arthropods in agriculture: problems and solutions. Science Publishers Inc, Enfield, NH, USA, pp 395–424Google Scholar
  57. Hoddle MS, van Driesche RG, Sanderson JP (1998) Biology and use of the whitefly parasitoid Encarsia formosa. Annu Rev Entomol 43:645–669PubMedCrossRefGoogle Scholar
  58. Hopper KR, Britch SC, Wajnberg E (2006) Risks of interbreeding between species used in biological control and native species, and methods for evaluating their occurrence and impact. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UK, pp 78–97CrossRefGoogle Scholar
  59. Howarth FG (1983) Classical biocontrol: panacea or Pandora’s box. Proc Hawaiian Entomol Soc 24:234–244Google Scholar
  60. Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509CrossRefGoogle Scholar
  61. Howarth FG (2001) Environmental issues concerning the importation of nonindigenous biological control agents. In: Lockwood JA, Howarth FG, Purcell MF (eds) Balancing nature: assessing the impact of importing non-native biological control agents (an international perspective). Proceedings of Thomas Say publications in entomology, Entomological Society of America, Lanham, MD, pp 70–99Google Scholar
  62. Hunt EJ, Kuhlmann U, Sheppard A, Qin T-K, Barratt B, Harrison L, Mason PG, Parker D, Goolsby J, Flanders B (2008) Regulation of invertebrate biological control agents in Australia, New Zealand, Canada and the USA: recommendations for Europe in its pursuit of a harmonised regulatory system. J Appl Entomol 132:89–123CrossRefGoogle Scholar
  63. Ingels B, De Clercq P (2011) Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus. BioControl. doi:10.1007/s10526-011-9363-9
  64. Jenner WH (2008) Evaluation of a candidate classical biological control agent and critical assessment of suggested host specificity testing guidelines. PhD Thesis, Carleton University, Ottawa, CanadaGoogle Scholar
  65. Jetter K, Klonsky K, Pickett CH (1997) A cost/benefit analysis of the ash whitefly biological control program in California. J Arboricult 23:65–72Google Scholar
  66. Kaufman LV, Wright MG (2009) The impact of exotic parasitoids on populations of a native Hawaiian moth assessed using life table studies. Oecologia 159:295–304PubMedCrossRefGoogle Scholar
  67. Kenis M, Auger-Rozenberg M-A, 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
  68. Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35CrossRefGoogle Scholar
  69. Kok LT, Salom SM, Yan S, Herrick NJ, McAvoy TJ (2008) Quarantine evaluation of Eucryptorrhynchus brandti (Harold) (Coleoptera: Curculionidae), a potential biological control agent of tree of heaven, Ailanthus altissima, in Virginia, USA. In: Julien MH, Sforza R, Bon MC, Evans HC, Hatcher, PE, Hinz HL, Rector BG (eds) Proceedings of the XII international symposium on biological control of weeds, La Grande Motte, France, 22–27 April 2007. CABI Publishing, Wallingford, UK, pp 292–300Google Scholar
  70. Kovach J (2004) Impact of multicolored Asian lady beetles as a pest of fruit and people. Am Entomol 50:159–161Google Scholar
  71. Kuhlmann U, Mason PG (2003) Use of field host range surveys for selecting candidate non-target species for physiological host specificity testing of entomophagous biological control agents. In: van Driesche RG (ed) Proceedings of the international symposium on biological control of arthropods, Honolulu, Hawaii, 14–18 January 2002, United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003-05, pp 370–377Google Scholar
  72. Kuhlmann U, Mason PG, Hinz HL, Blossey B, Dosdall LM, Olfert OO, McClay AS, De Clerck-Floate RA, Brodeur J, Wiedenmann RN, Gassmann A, McCaffrey JP, Schwarzlaender M (2006a) Compatibility of classical biological control of insects and weeds: a case study using cabbage seedpod weevil for ecological assessment of potential non-target effects. J Appl Entomol 130:129–141CrossRefGoogle Scholar
  73. Kuhlmann U, Schaffner U, Mason PG (2006b) Selection of non-target species for host specificity testing. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UK, pp 15–37CrossRefGoogle Scholar
  74. Kuris AM (2003) Did biological control cause extinction of the coconut moth, Levuana iridescens, in Fiji? Biol Invasion 11:21–45Google Scholar
  75. Linder Ch, Lorenzini F, Kehrli P (2009) La coccinelle asiatique donne-t-elle un faux goût au Chasselas et au Pinot noir? Revue Suisse Vitic Arboric Hortic 41:61–62Google Scholar
  76. Lockwood JA (1999) Non-target effects of biological control: what are we trying to miss? In: Follett PA, Duan JJ (eds) Non-target effects of biological control. Kluwer, Dordrecht, pp 15–30Google Scholar
  77. Lockwood JA, Howarth FG, Purcell MF (2001) Summary: common ground, great divides, and building bridges. In: Lockwood JA, Howarth FG, Purcell MF (eds) Balancing nature: assessing the impact of importing non-native biological control agents (an international perspective). Proceedings of Thomas Say publications in entomology, Entomological Society of America, Lanham, MD, pp 120–130Google Scholar
  78. Louda SV (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090CrossRefGoogle Scholar
  79. Louda SV (2000) Negative ecological effects of the musk thistle biological control agent, Rhinocyllus conicus. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer Academic Publishers, Dordrecht, pp 215–243CrossRefGoogle Scholar
  80. Louda SV, 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 48:365–396PubMedCrossRefGoogle Scholar
  81. Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Progress in biological control, vol 7. Springer, DordrechtGoogle Scholar
  82. Lynch LD, Hokkanen HMT, Babendreier D, Bigler F, Burgio G, Gao ZH, Kuske S, Loomans A, Menzler-Hokkanen I, Thomas MB, Tommasini G, Waage JK, van Lenteren JC, Zeng QQ (2001) Insect biological control and non-target effects: a European perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, UK, pp 99–125Google Scholar
  83. Majerus M, Kearns P (1989) Ladybirds. Richmond Publishing, SloughGoogle Scholar
  84. Majerus MEN, Strawson V, Roy HE (2006) The potential impacts of the arrival of the Harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215CrossRefGoogle Scholar
  85. Mason PG, Huber JT, Boyetchko SM (2002) Introduction. In: Mason PG, Huber JT (eds) Biological control programmes in Canada, 1981–2000. CABI Publishing, Wallingford, UK, pp xi–xivGoogle Scholar
  86. McMurtry JA, Oatman ER, Phillips PA, Wood CW (1978) Establishment of Phytoseiulus persimilis (Acari: Phytoseiidae) in Southern California. Entomophaga 23:175–179CrossRefGoogle Scholar
  87. Mills N, Babendreier D, Loomans A (2006) Significance of dispersal and assessment in environmental risk evaluations. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford, UK, pp 114–131CrossRefGoogle Scholar
  88. 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, Wallingford, UK, pp 241–253Google Scholar
  89. Neuenschwander P (1996) Evaluating the efficacy of biological control of three exotic homopteran pests in tropical Africa. Entomophaga 41:403–424CrossRefGoogle Scholar
  90. Neuenschwander P (2001) Biological control of the cassava mealybug in Africa: a review. Biol Control 21:214–229CrossRefGoogle Scholar
  91. Neuenschwander P, Markham R (2001) Biological control in Africa and its possible effects on biodiversity. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, UK, pp 127–146Google Scholar
  92. Orr D (2009) Biological control and integrated pest management. In: Peshin R, Dhawan AK (eds) Integrated pest management: innovation-development. Springer Science+Business Media BV, Dordrecht, pp 207–239Google Scholar
  93. Parry D (2008) Beyond Pandora’s box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biol Invasions 11:47–58CrossRefGoogle Scholar
  94. Pearson DE, Callaway RM (2008) Weed-biocontrol insects reduce native-plant recruitment through second-order apparent competition. Ecol Appl 18:1489–1500PubMedCrossRefGoogle Scholar
  95. Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168CrossRefGoogle Scholar
  96. Perdikis D, Fantinou A, Garantonakis N, Kitsis P, Maselou D (2009) Studies on the damage potential of the predator Nesidiocoris tenuis on tomato plants. Bull Insectol 62:41–46Google Scholar
  97. Sampson C, Jacobson RJ (1999) Macrolophus caliginosus Wagner (Heteroptera: Miridae): a predator causing damage to UK tomatoes. IOBC/WPRS Bull 22:213–216Google Scholar
  98. Sanchez JA (2008) Zoophytophagy in the plantbug Nesidiocoris tenuis. Agric For Entomol 10:75–80CrossRefGoogle Scholar
  99. Sanchez JA (2009) Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol Control 51:493–498CrossRefGoogle Scholar
  100. Sands DPA (1997) The ‘safety’ of biological control agents: assessing their impact on beneficial and other non-target hosts. Mem Mus Vic 56:611–615Google Scholar
  101. Sands DPA (1998) Guidelines for testing host specificity of agents for biological control of arthropod pests. In: Sixth Australian applied entomological research conference, vol I. The University of Queensland, Brisbane, Australia. The University of Queensland, Australia, pp 556–560Google Scholar
  102. Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974CrossRefGoogle Scholar
  103. Smith L, Cristofaro M, Tronci C, Hayat R (2008) Refining methods to improve pre-release risk assessment of prospective agents: the case of Ceratapion basicorne. In: Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, Hinz HL, Rector BG (eds) Proceedings of the XII international symposium on biological control of weeds, La Grande Motte, France, 22–27 April 2007. CABI Publishing, Wallingford, UK, pp 321–327Google Scholar
  104. Svihla A (1952) Two-spotted lady beetles biting man. J Econ Entomol 45:134CrossRefGoogle Scholar
  105. van Driesche RG (1994) Classical biological control of environmental pests. Fla Entomol 77:20–33CrossRefGoogle Scholar
  106. van Driesche RG, Bellows TS (1996) Biological control. Kluwer Academic Press, Dordrecht, The NetherlandsCrossRefGoogle Scholar
  107. 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, Prat, PD, Rayamajhi M, Salom S, Sands D, Schooler S, Sheppard A, Shaw R, Schwarzländer M, Tipping PW, van Klinken RD (2010) Classical biological control for the protection of natural ecosystems: past achievements and current efforts. Biol Control 54:S2–S33CrossRefGoogle Scholar
  108. van Lenteren JC (1997) Benefits and risks of introducing exotic macro-biological control agents into Europe. EPPO Bull 27:15–27CrossRefGoogle Scholar
  109. van Lenteren JC (2001) Harvesting safely from biodiversity: natural enemies as sustainable and environmentally friendly solutions for pest control. In: Lockwood JA, Howarth FG, Purcell MF (eds) Balancing nature: assessing the impact of importing non-native biological control agents (an international perspective). Proceedings of Thomas Say publications in entomology, Entomological Society of America, Lanham, MD, pp 15–30Google Scholar
  110. van Lenteren JC (2003) Commercial availability of biological control agents. In: van Lenteren JC (ed) Quality control and production of biological control agents—theory and testing procedures. CABI Publishing, Wallingford, UK, pp 167–179CrossRefGoogle Scholar
  111. van Lenteren JC (ed) (2008) IOBC Internet book of biological control. http://www.iobc-global.org/downlaod/IOBC%20InternetBookBiCoVersion5January2008.pdf
  112. van Lenteren JC, Loomans AJM (2006) Environmental risk assessment: methods for comprehensive evaluation and quick scan. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods. CABI Publishing, Wallingford, UK, pp 254–272CrossRefGoogle Scholar
  113. van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, van Rijn PCJ, Thomas MB, Tomassini MC, Zeng QQ (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38CrossRefGoogle Scholar
  114. 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 51:609–634PubMedCrossRefGoogle Scholar
  115. 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. CABI Publishing, Wallingford, UK, pp 38–63CrossRefGoogle Scholar
  116. van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2008) Harmonia axyridis: an environmental risk assessment for Northwest Europe. BioControl 53:37–54CrossRefGoogle Scholar
  117. van Schelt J, Klapwijk J, Letard M, Aucouturier C (1995) The use of Macrolophus caliginosus as a whitefly predator in protected crops. In: Gerling D, Mayer RT (eds) Bemisia 1995. Taxonomy, biology, damage, control and management. Intercept, Andover, pp 515–522Google Scholar
  118. Walter DE, Campbell NJH (2003) Exotic vs endemic biocontrol agents: would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), please stand up? Biol Control 26:253–269CrossRefGoogle Scholar
  119. Walter DE, Azam GN, Waite G, Hargreaves J (1998) Risk assessment of an exotic biocontrol agent: Phytoseiulus persimilis (Acari: Phytoseiidae) does not establish in rainforest in southeast Queensland. Austr J Ecol 23:587–592CrossRefGoogle Scholar
  120. Warner KD, McNeil JN, Getz C (2009) What every biocontrol researcher should know about the public. In: Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, Hinz HL, Rector BG (eds) Proceedings of the XII international symposium on biological control of weeds. La Grande Motte, France, 22–27 April 2007. CABI Publishing, Wallingford, UK, pp 390–394Google Scholar
  121. Wells PM, Baverstock J, Majerus MEN, Jiggins FM, Roy HE, Pell JK (2011) The effect of the coccinellid Harmonia axyridis (Coleoptera: Coccinellidae) on transmission of the fungal pathogen Pandora neoaphidis (Entomophthorales: Entomophthoraceae). Eur J Entomol 108:87–90CrossRefGoogle Scholar
  122. Zeddies J, Schaab RP, Neuenschwander P, Herren HR (2001) Economics of biological control of cassava mealybug in Africa. Agric Econ 24:209–219CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2011

Authors and Affiliations

  • Patrick De Clercq
    • 1
  • Peter G. Mason
    • 2
  • Dirk Babendreier
    • 3
  1. 1.Department of Crop ProtectionGhent UniversityGhentBelgium
  2. 2.Agriculture and Agri-Food Canada, Research CentreOttawaCanada
  3. 3.CABI Europe-SwitzerlandDelemontSwitzerland

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