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Annotated bibliography

Biological control safety (general)


Barratt B.I.P. (1996). Biological control: Is it environmentally safe? Forest and Bird 282: 36-41.

Barratt B.I.P. (2002). Risks of Biological Control. Pp. 720-722 In: Encyclopaedia of Pest Management, D. Pimental (Ed.) Marcel Dekker Inc, New York.

Barratt B.I.P., Ferguson C.M. and Evans A.A. (2001). Non-target effects of introduced biological control agents and some implications for New Zealand. Pp. 41-53 In: Balancing Nature: Assessing the Impact of Importing Non-Native Biological Control Agents (An International Perspective), J.A. Lockwood, F.G. Howarth and M.F. Purcell (Ed.) Thomas Say Publications, Maryland.

Bigler F., Babendreier D. and Kuhlmann U. (2006). Environmental impact of arthropod biological control: methods and risk assessment. Pp. 288. CABI Publishing, Delemont, Switzerland.

Carruthers R.I. and D'Antonio C.M. (2005). Science and decision making in biological control of weeds: Benefits and risks of biological control. Biological Control 35: 181-182.

de Clercq, P., Mason, P. and Babendreier, D. (2011). Benefits and risks of exotic biological control agents. Biocontrol 56: 681-698
The use of exotic arthropods in biological control programs has yielded huge economic and ecological benefits. However, non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, to massive effects on a large scale. This paper reviews both the benefits of biological control as well as the associated risks and an attempt is made at identifying the major challenges for assessing risks and for balancing benefits and risks. While sound risk assessment procedures preceding release of biological control agents are advocated, overly stringent regulations that would preclude promising agents from being developed must be avoided.

Drea J.J. (1993). Classical biological control - an endangered discipline? Pp. In: Biological Pollution: The control and impact of invasive exotic species, B.N. McNight (Ed.) Indiana Academy of Science, Indianapolis.

Ehler L.E. (1990). Environmental impact of introduced biological control agents: implications for agricultural biotechnology. Pp. 85-96 In: Risk assessment in agricultural biotechnology, J.J. Marois and G. Breuning (Ed.) California Division of Agriculture and Natural Resources, Oakland.

Ehler L.E. (1999). Critical issues related to nontarget effects in classical biological control of insects. Pp. 3-13 In: Nontarget effects of biological control introductions, P.A. Follett and J.J. Duan (Ed.) Kluwer Academic Publishers, Norwell, Massachusetts, USA.

European and Mediterranean Plant Protection Organization (EPPO) (2010). Import and release of non-indigenous biological control agents. Bulletin OEPP/EPPO Bulletin 40: 335-344

Fowler S.V., Gourlay A.H., Hill R.L. and Withers T. (2003). Safety in New Zealand weed biocontrol: a retrospective analysis of host-specificity testing and the predictability of impacts on non-target plants. Pp. 265�270 in Proceedings of the XI International Symposium on Biological Control of Weeds, Canberra, Australia, 2003, J.M. Cullen, D.T. Briese, D.J. Kriticos, W.M. Lonsdale, L. Morin and J.K. Scott (Ed.).
A retrospective analysis showed that all weed biocontrol agents released in New Zealand were subjected to generally appropriate host-range tests, although there were several examples where significant plant species were not tested. The results have been used to focus field surveys on the most likely non-target plant species to be attacked by biocontrol agents in New Zealand. For example, Tyria jacobaeae (cinnabar moth) did feed on some Senecio species in the original host-range tests, so the occasional field attack on native New Zealand fireweeds such as S. minimus was predictable. To date, this is the only weed biocontrol agent in New Zealand (of the total of 32 established in the field since 1929) that has been recorded attacking a native non-target plant species in the field. There were two cases where test results did not predict potentially substantial non-target impacts: Bruchidius villosus (broom seed beetle) and Cydia succedana (gorse pod moth), attacking seed of nontarget, exotic Fabaceae. Limited replication and duration of tests, were among possible explanations for the failure to predict these impacts.

Frank J.H. (1998). How risky is biological control? Comment. Ecology 79: 1829-1834.

Goldson S.L., Barratt B.I.P., Barlow N.D. and Phillips C.B. (1998). What is a safe biological control agent? Pp. 530-538 In: Pest Management - Future Challenges: Proceedings of the 6th Australasian Applied Entomological Research Conference, M. Zalucki, R. Drew and G. White (Ed.) The Cooperative Research Centre for Tropical Pest Management.

Harris P. (1990). Environmental impact of introduced biological control agents. Pp. 289-300 In: Critical issues in biological control, M. Mackauer, L.E. Ehler and J. Roland (Ed.) Intercept, Andover, Hampshire, UK.

Hawkins B.A. and Marino P.C. (1997). The colonization of native phytophagous insects in North America by exotic parasitoids. Oecologia 112: 566.
Classical biological control could have a major environmental cost if introduced natural enemies colonize and disrupt native systems. Impacts were evaluated based on the extent to which exotics have acquired native hosts. The ability of six biological and ecological variables to predict whether or not a parasitoid will move onto natives was evaluated. It was concluded that given the quality of the data available either now or in the foreseeable future, coupled with inherent stochasticity in host shifts by parasitoids, there are no rules of thumb to assist biological control workers in evaluating if an introduced parasitoid will colonize native insect communities.

Hopper K.R. (1998). Assessing and improving the safety of introductions for biological control. Pp. 501-510 In: Pest Management - Future Challenges: Proceedings of the 6th Australasian Applied Entomological Research Conference, M. Zalucki, R. Drew and G. White (Ed.) The Cooperative Research Centre for Tropical Pest Management.

Hopper K.R. (2001). Research needs concerning non-target impacts of biological control introductions. Pp. 39-56 In: Evaluating indirect ecological effects of biological control, E. Wajnberg, J.K. Scott and P.C. Quimby (Ed.) CABI Publishing, Wallingford, Oxon., UK.

Howarth F.G. (1983). Classical biological control: panacea or Pandora's box. Proceedings of the Hawaiian Entomological Society 24: 239-244.

Howarth F.G. (1991). Environmental impacts of classical biological control. Annual Review of Entomology 36: 489-509.

Howarth F.G. (1992). Environmental impact of species purposefully introduced for biological control of pests. Pacific Science 46: 388-389.

Howarth F.G. (2001). Environmental issues concerning the importation of non-indigenous biological control agents. Pp. 70-99 In: Balancing nature: assessing the impact of importing non-native biological control agents (an international perspective), J.A. Lockwood, F.G. Howarth and M. Purcell (Ed.) Entomological Society of America, Lanham, Maryland.

Jacas J.A., Urbaneja A. and Vi�uela E. (2006). History and future of introduction of exotic arthropod biological control agents in Spain: A dilemma? BioControl 51: 1-30.
More success for IBCAs has been achieved with seasonal inoculative releases (50.0% of cases) than for classical biological control programs (17.1% of cases). Concerns about potential non-target effects but post-release evaluation has often been insufficient to draw any conclusions about them. Most of the biological control agents introduced in Spain were parasitoids (n = 53), and the remainder predators (n = 12). Only four parasitoids are considered monophagous. Using information from literature and the internet, the mean number of host species parasitized by parasitoids is 15.2, Therefore, polyphagy appears to be quite common among the IBCAs that have been introduced in Spain.

Lockwood J.A. (1996). The ethics of biological control: Understanding the moral implications of our most powerful ecological technology. Agriculture and Human Values 13: 2-19.
The system of environmental ethics developed by Johnson (1991) is used to analyse the moral implications of biological control. In this formulation of ethical analysis, species and ecosystems are morally relevant because they are not simply aggregates of individuals, so their processes, properties, and well-being interests are not reducible to the sum of their individual members. Following Johnson's thesis, species and ecosystems have morally relevant interests in surviving and maintaining themselves as integrated wholes with particular self-identities. It is evident that not all biological control efforts are ethically defensible. In general terms, natural biological control is most desirable, followed by augmentative strategies, classical approaches, and finally neoclassical biological control.

Lockwood J.A. (1997). Competing values and moral imperatives: an overview of ethical issues in biological control. Agriculture and Human Values 14: 205-210.
The perception and resolution of ethical issues relating to biological control appear to emerge from a set of factors that includes one's ethical viewpoint (anthropocentric or biocentric), agricultural system (industrial or sustainable), economic context (rich or poor), and power structure (expert or public). From this set of parameters at least five major ethical questions can be formulated: (1) How we should regulate and apply biological control given uncertainty regarding environmental impacts; (2) How we balance benefits of biological control to human and ecosystem well-being against the known and anticipated risks; (3) Who should be empowered to develop policies and make decisions; (4) How we can assure a more just distribution of benefits and costs associated with biological control technologies and (5) Whether biological control can be justified as a resource substitution for pesticides or is its ethical application only possible as part of a reconceptualization of agricultural production. These central questions and possible answers are presented in a varied set of provocative analyses by some of the leading thinkers and authorities in their fields.

Lockwood J.A., Howarth F.G. and Purcell M. (2001). Balancing nature: Assessing the impact of importing non-target biological control agents (An international perspective). Thomas Say Publications, Lanham, Maryland, USA. 130 pp.

Messing R.H. (1992). Biological control in island ecosystems: cornerstone of sustainable agriculture or threat to biological diversity. Pacific Science 46: 387-388.

Onstad D.W. and McManus M.L. (1996). Risks of host range expansion by parasites of insects. BioScience 46: 430-435.
The authors discuss the estimation of risks that biological control agents pose to nontarget species. There has been no demonstration that biological control agents have threatened, endangered or extirpated any native insect or arachnid species in the USA.

Parry D. (2009). Beyond Pandora's Box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biological Invasions 11: 47-58
Howarth's paper (Proc Hawaii Entomol Soc 24:239-244, 1983) "Classical biological control: Panacea or Pandora's Box" raised awareness of the relative safety of introductions for classical biological control. Here, the author examines the potential for non-target effects among insect parasitoids. In response to the need for quantitative studies, three different techniques, quantitative food webs, life table analysis, and experimental populations are explored along with three approaches to ascertaining the strength of competitive interactions between native and introduced parasitoids.

Pemberton R.W. (2004). Biological control safety within temporal and cultural contexts. Proceedings of the XI International Symposium on Biological Control of Weeds: 245-246
An analysis of non-target plant use resulting from natural enemy introductions in continental USA, Hawaii and the Caribbean between 1902 and 1994 was carried out. Fourteen of the 117 agents introduced have adopted 45 native plants as developmental hosts. All but one of these plants are closely related to the target weeds. The non-target use was predictable, based on known host ranges of the insects in their native areas and host-specificity testing. The single case in which a plant unrelated to the target weed was adopted involves the lantana lacebug (Teleonemia scrupulosa introduced to Hawaii in 1902), which was thought to be a lantana specialist but apparently is not. Almost all insects adopting native plants were introduced between 1902 and 1972 when 20% (13/63) of the agents introduced have adopted native plants compared with only 1.8% (1/54) of the agents introduced between 1973 and 2002. None of the 117 introduced natural enemies have adopted agricultural plants.

Pimentel D. (1980). Environmental risks associated with biological control. Ecological Bulletin 31: 11-24.
A review of the environmental effects of classical biological control programmes against pests and weeds under the headings: beneficial aspects of biological control; negative impacts of classical biological control; solutions; and future directions. Deals mainly with insects and other arthropods used as biological control agents, but microorganisms, molluscs and vertebrates are also included.

Pimentel D. (1995). Biotechnology: environmental impacts of introducing crops and biocontrol agents in North American agriculture. Pp. 13-29 In: Biological Control: Benefits and Risks, H.M.T. Hokkanen and J.M. Lynch (Ed.) Cambridge University Press, Cambridge, UK.

Pimentel D., Glenister C., Fast S. and Gallahan D. (1984). Environmental risks of biological pest controls. Oikos 42: 283-290.

Roberts L.I.N. (1986). The practice of biological control - implications for conservation, science and the community. The Weta, Entomological Society of NZ 9: 76-84.

Samways M.J. (1997). Classical biological control and biodiversity conservation: what risks are we prepared to accept? Biodiversity and Conservation 6: 1309-1316.

Secord D. and Kareiva P. (1996). Perils and pitfalls in the host specificity paradigm. BioScience 46: 448-453.
The importance of host specificity in biological control agents is discussed in relation to unexpected host shifts; specificity assessment, evolution and indirect effects; and host specificity and cost/benefit analysis for biological control.

Simberloff D. (1991). Keystone species and community effects of biological control introductions. Pp. 1-19 In: Assessing ecological risks of biotechnology, L.R. Ginzburg (Ed.) Butterworth-Heinemann, Boston, Massachusetts, USA.

Simberloff D. (1992). Conservation of pristine habitats and unintended effects of biological control. Pp. 103-117 In: Selection Criteria and Ecological Consequences of Importing Natural Enemies, W.C. Kaufmann and J.E. Nechols (Ed.) Entomological Society of America, Lanham, Maryland, USA.
The effect of deliberate introductions of arthropods for biological control purposes on species in pristine habitats is examined. This paper was developed from a symposium held during the 1990 Annual Meeting of the Entomological Society of America in New Orleans, Louisiana.

Simberloff D. (2012). Risks of biological control for conservation purposes. Biocontrol 57: 263-276.

Simberloff D. and Stiling P. (1996). How risky is biological control? Ecology 77: 1965-1974.
Literature review of non-target effects of introduced biological control agents. There are few documented instances of damage to non-target organisms or the environment, however, this is not evidence that biological control is safe, because monitoring of non-target species is minimal. Predicting indirect effects is difficult, plus the fact that introduced species can disperse and evolve. Current regulation of introduced biological-control agents is considered insufficient. It is recommended that the likely impact of both the pest and its natural enemy on natural ecosystems and their species should be considered, not only on potential economic benefits.

Simberloff D. and Stiling P. (1996). Risks of species introduced for biological control. Biological Conservation 78: 185-192.
Biological control introductions have adversely affected nontarget native species, including some recent cases, and little monitoring of impacts is done, so known problems may be the tip of an iceberg. Regulations for officially releases for biological control are insufficient, and there are also freelance unregulated releases undertaken by private citizens. Cost-benefit analyses for conservation issues are difficult because it is hard to assign values to the loss of species or ecosystem functions. Cost-benefit analyses and risk assessments for biological control introductions would enforce consideration of many factors that now often receive cursory attention, and broaden public understanding of the issues.

Simberloff D. and Stiling P. (1998). How risky is biological control? Reply. Ecology 79: 1834-1836.

Stiling P. (2004). Biological control not on target. Biological Invasions 6: 151-159.
Summary of previously recorded information on the diet breadth of natural enemies released to control insect pests worldwide. Of released biocontrol agents in North America, 48% were recorded as generalists, 29% attacked more than one species in a genus, 23% were specialists on the target pests. So many natural enemies released in biocontrol programs against insect pests have broad diets and non-target effects are likely. In North America many parasitoids attack multiple host genera and species, with an average of 5.8 genera and 7.3 species attacked, indicating broad agreement with data from biological control releases.

Stiling P. and Simberloff D. (1999). The frequency and strength of nontarget effects of invertebrate biological control agents of plant pests and weeds. Pp. 31-43 In: Nontarget effects of biological control introductions, P.A. Follett and J.J. Duan (Ed.) Kluwer Academic Publishers, Norwell, Massachusetts, USA.

Strong D.R. and Pemberton R.W. (2001). Food webs, risks of alien enemies and reform of biological control. Pp. 57-79 In: Evaluating indirect ecological effects of biological control, E. Wajnberg, J.K. Scott and P.C. Quimby (Ed.) CABI Publishing, Wallingford, Oxon., UK.

Thomas M.B. and Willis A.J. (1998). Biocontrol - risky but necessary? Trends in Evolution and Ecology 13: 325-329.
Biocontrol advocates appear reluctant to accept the possibility that there could be side-effects associated with biocontrol, often refuting evidence of harmful effects. The biocontrol critics, although eager to provide evidence to the contrary, appear reluctant to propose any detailed, constructive criticisms or workable solutions. Suggestions for directions for future research that might help to resolve some of the problems.

Waage J.K. (2001). Indirect ecological effects of biological control: the challenge and the opportunity. Pp. 1-12 In: Evaluating indirect ecological effects of biological control, E. Wajnberg, J.K. Scott and P.C. Quimby (Ed.) CABI Publishing, Wallingford, Oxon., UK.