CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2011 6, No. 042 Review Assessing safety of biological control introductions Barbara I.P. Barratt* Address: AgResearch Invermay, PB 50034, Mosgiel, New Zealand. *Correspondence: Email: barbara.barratt©agresearch.co.nz Received: 4 September 2011 Accepted: 4 October 2011 doi: 10.1079/PAVSN N R20116042 The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews © CAB International 2011 (Online ISSN 1749-8848) Abstract Biological control is an important component of pest management systems. It was generally considered safe and sustainable until the validity of this consensus was challenged by researchers who pointed out that there was a lack of study, and hence evidence, to support it and provided examples of non-target impacts. Biosafety of biological control subsequently received considerable attention from both biocontrol practitioners and regulators. Many countries now have legislation in place, which is focused on risk assessment for biological control and protecting native and valued biota and the environment from potential adverse impacts. This review summarizes the biosafety debate and characterizes the direct and indirect risks of biological control mainly for weeds and insect pests. During a biological control programme, there are several ways in which aspects of biosafety can be considered and addressed: exploration in the native range of the target species; from literature and knowledge of the biological control agent and host; experience from use of the biological control agent elsewhere; and host-range tests. The value of post-release monitoring and retrospective studies for validation of pre-release predictions is discussed. A poorly studied aspect is analysis of the population impacts of non-target attack by biological control agents. The literature from the last 20-30 years can help define some useful principles by which a risk assessment can be conducted to minimize adverse environmental effects. It has become clear over this period that comprehensive assembly of information and robust quarantine testing to provide a well-structured risk assessment can reduce uncertainty in decision-making in this area. Keywords: Biological control, Biosafety, Risk assessment, Non-target effects, Regulation Review Methodology: Literature was accessed on a regular basis using alerts generated by OvidSP in order to update the bibliography of the BIREA database [1]. The searches include CAB Abstracts and BIOSIS databases and the search terms used were safety, biosafety, non target, nontarget, host-range testing, host specificity, risk assessment, post release, host range, biological control, biocontrol. Journals also scanned on a regular basis include Biological Control, BioControl, Biocontrol News and Information, Environmental Entomology and Entomologia Experimentalis et Applicata. A number of books published on the subject of risks of biological control were consulted [2-6]. The scope of this review is mainly classical biological control of weeds and insect pests, with some reference to control. A recent review of inundative biocontrol reports predators and pathogens as biological control agents. The on the trend away from the use of exotic organisms by literature on biosafety of predator introductions includes commercial producers, partly because of the increase many examples of research on ladybirds (Coleoptera: in regulatory demands [7], and the ERBIC programme Coccinellidae) [9-13] and tachinids (Diptera: Tachinidae) (see below) reported results on biosafety research for [14, 15], and prediction and assessment of non-target inundative biological control [8]. In addition, the emphasis impacts of pathogens used for biological control has been of this contributionis on insects used for biological well reviewed [16-19]. http://www.cabi.org/cabreviews 2 Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources Biological Control Safety: The Debate Regulations and Guidelines Biological control was heralded as one of the safe alter- While biological control biosafety was still being debated, natives to pesticides when public demands to reduce regulatorsin some countries began to review their pesticide use were made in the 1960s and 1970s. This legislation. Australia and New Zealand were allegedly pressure arose partly as a result of concerns about en- the front-runners with their Biological Control Act (1984) vironmental risk, prompted not only by Rachel Carson in (Australia is the only country with specific legislation) her landmark publication 'Silent Spring' [20] but also by and the Hazardous Substances and New Organisms Act the increasing incidence of pesticide resistance, and the (1996) (HSNO), respectively. A global review of risk- promotion of the philosophy of sustainable agricultural cost-benefit analyses for weed biological control agents practices. Several prominent biological control research- introductions globally concluded that only New Zealand ers provided assurances thatbiologicalcontrol was came near to a complete and transparent process [35]. environmentally safe and risk-free [21]. This view was not However,it was pointed out that Australia,unlike shared universally by scientists, but,inparticular, the New Zealand, requires the submission of a test plant list environmental safety of biological control was questioned for approval (by agricultural and conservation agencies) [22-26]. It was pointed out that in comparison with the for host specificity testing of weed biological control application of pesticides, biological control is irreversible, agents, before an application to releaseisaccepted. self-perpetuating and self-dispersing,attributesclearly This 'Nomination of Target Weeds for Biological Control' considered among the benefits of biological control by to the Australian Weeds Committee can result ina some, but factors alerting others to the potential en- requirement for more test species to be added to the list. vironmental implications of such introductions. Views It was later suggested that Europe lagged behind remained highly polarized for several years, especially in Australasia and North America in implementing legislation Hawaii where biological control has been particularly for biological control, partly because Europe has more intensively practised [27]. Proponents of biological con- often been the exporter of biological control agents, trol claimed that the 'conservationists' had no evidence rather than the recipient [36]. An agreed approach to for negative impacts of biological control and that claims regulation of biological control introductions between of adverse impacts were overstated, often using examples countries in Europe appeared to be an obvious require- either from the past before consideration was given to ment since biological control agents are highly likely to risk, or the more visible consequences of vertebrates spread across borders [37] and it was clearly argued that used for biological control[27-30].Inrecent years, for risk assessment, ecoregions would be more relevant however, funding has become available for research in this spatial units than national boundaries [38]. The need for area and it has presented an opportunity to conduct consistent standards in regulation of biological control challenging ecological research [31, 32]. In response, a was recognized [39], and a detailed history of efforts in number of meetings and workshops were held to present Europe to achieve adoption of 'harmonized' regulation for research and establish research priorities in risk assess- biological control was compiled [36, see Table 1]. ment for biological control [2, 5, 33, 34]. Biological control practitioners have generally accepted The European Union funded a 4-year programme that regulation of biological control agent introduction is involving five partner countries, titled'Evaluating en- required in the public interest because of its irreversibility vironmental risks of biological control' or ERBIC. One of and the potential for biological control agents to disperse the main objectives of this programme was to ensure that to habitats other than those where they were released the introduction of biological control agents does not put [40]. In New Zealand, for example, the Hazardous Sub- non-target organisms at risk. With the emphasis mainly stances and New Organisms (HSNO) Act 1996 [41] on either seasonal inoculative or inundative releases requiresthat new organismintroductions,including rather than classical biological control, the ERBIC study biological control agents, must be compatible with safe- set out to determine the negative and positive impacts guarding the life-supporting capacity of air, water and of biological pest control, to develop methods to assess ecosystems, the sustainability of flora and fauna, and the risk, and to design specific European guidelines to ensure intrinsic value of ecosystems (Section 36 of the HSNO environment safety. The finalreport [8]stated that Act, 1996). The Environmental Protection Authority, the research had shown that 'biological control overall formerly the Environmental Risk Management Authority has been extraordinarily safe', but that this can still be New Zealand, has responsibility for implementation of the improvedusingrisk assessment methods developed HSNO Act [42]. during the project. Furthermore, the authors concluded In 1995, the Food and Agriculture Organization