J. Appl. Entomol. MINI REVIEW Harmonization of regulations for invertebrate biocontrol agents in Europe: progress, problems and solutions J. Bale School of Biosciences, University of Birmingham, Edgbaston, Birmingham, UK Keywords Abstract biological control, environmental risk assessment, Europe, regulation The use of non-native invertebrate biological control agents (IBCAs) in Europe is not covered by a Directive equivalent to that which regulates Correspondence biocontrol with microorganisms or the genetic modification of crop Jeffrey Bale (corresponding author), School of plants. Regulation is at the discretion of individual member states and Biosciences, University of Birmingham, largely derived from national legislation on pesticides, plant health or Edgbaston, Birmingham B15 2TT, UK. environmental protection. There is no EU country with regulation of E-mail: [email protected] IBCAs that requires information on the microbial symbiont content of Received: September 29, 2010; accepted: candidate species, and in the absence of horizontal transfer under natu- December 23, 2010. ral conditions, this policy is unlikely to change. Although there have been few reported negative effects linked to the import and release of doi: 10.1111/j.1439-0418.2011.01611.x IBCAs, a number of countries have introduced or revised their regula- tory frameworks in recent years. This article reviews major develop- ments in the regulation and environmental risk assessment (ERA) of IBCAs in Europe over the last 10 years including: the fragmented pat- tern of regulation between countries, variation in information require- ments for release licences, format and methods of ERA for different taxonomic groups of IBCAs, use and updating of the European Plant Protection Organisation Positive List, sources of expert advice on ERA data, communication between IBCA regulators, and options for the provision of international leadership to coordinate regulatory and ERA-related issues with IBCA-based biocontrol in Europe. home range of introduced pests with the intention Introduction of permanent establishment in the area or country The modern use of biological control with inverte- of release (see Bale et al. 2008 for examples). It is brate agents (insects, mites and nematodes) is widely also a feature of note that attempts at classical bio- regarded as having its first success in the citrus orch- control of insect and mite pests in Europe have been ards of California over 100 years ago with the con- largely unsuccessful, with the recent release of the trol of the introduced scale insect Iceryae purchasi by psyllid Aphalara itadori as a control for the Japanese the predatory ladybird Rodolia cardinalis and the dip- knotweed (Polygonum cuspidatum) in the UK also teran parasitoid Cryptochaetum iceryae, both of which being one of few weed biocontrol schemes in a were collected from the native distribution of the European country (Shaw et al. 2009). pest in Australia. In this respect, it is interesting to Over the last 50 years, systems of biocontrol have note that biological control pre-dates the use of diversified to include ‘open field’ and glasshouse chemical pesticides upon which insect pest manage- crops where there is no expectation or intention of ment came to depend for much of the latter half of long-term establishment (augmentative and inunda- the 20th century. A number of the other ‘early’ suc- tive control), and the manipulation of ecosystems to cesses in biocontrol were also ‘classical’ schemes in attract and increase the local abundance of native which natural enemies were collected from the natural enemies (conservation control). In general, J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH 503 Regulation of invertebrate biocontrol agents in Europe J. Bale classical and conservation control are developed, may be irreversible, it is necessary to take a precau- monitored and maintained by public funding (gov- tionary approach, to include an environmental risk ernment agencies, research institutes and universi- assessment of the candidate organism. ties), whereas augmentative and inundative control At the present time, there are systems of have become commercialized, with a number of regulation in place for the import and release of companies producing large numbers of organisms for non-native biocontrol agents in the USA, Canada, mass release. In effect, there is little or no financial Australia and New Zealand (see Hunt et al. 2007 for return on classical control where there would be no a review). The situation in Europe is more compli- recurrent market for successful agents. cated and is evolving: some countries have regula- Biocontrol often involves the movement of species tion (UK, The Netherlands, Switzerland), others do around the world, from sites of collection, via a pro- not (France, Italy) and some have plans to introduce duction facility, to sites of release. In some schemes, regulation (e.g. in the Flanders region of Belgium). the search for natural enemies is focused on There is therefore nothing to prevent a species being co-evolved predators or parasitoids of the target spe- ‘prohibited’ for release after an environmental risk cies in its country or region of origin, as is the case assessment in one country, but then released in a for many classical programmes. For augmentative neighbouring country which has no regulation. To and inundative control, candidate agents may be col- some extent, that has been the situation with the lected on the basis of taxonomic and related predatory ladybird Harmonia axyridis. This species behavioural traits – for example, predatory mites was first released in Europe in trials on hops in that attack other acarine prey – rather than a pur- France about 20 years ago – a country with no regu- poseful attempt to ‘reunite’ natural enemies with lation – and then commercially released in The their hosts and prey in a new environment. Netherlands and Belgium from 1996 to 2004; and The scale of the release of non-native natural ene- although it was never subject to a risk assessment at mies has been quantified by van Lenteren et al. that time, a retrospective analysis (van Lenteren (2006): 5000 introductions of approximately 2000 et al. 2008) has shown that because of its winter species into 196 countries or islands over the past cold tolerance, polyphagy, and dispersal potential, 120 years. The fact that is most striking about these licences for release were not likely to have been figures is that many of these releases were made granted (see also De Clercq and Bale 2011). How- prior to the era of legislation, regulation and risk ever, under the currently fragmented landscape of assessment of biocontrol agents, and yet, there have regulation in Europe, there is nothing to prevent a been remarkably few reports of negative environ- recurrence of this type of release. mental effects. At the same time, and particularly Over the last 20–30 years, with an increasing over the last 30 years, the perception that non- emphasis on environmental protection, and the per- native species pose a risk to native flora and fauna ception if not the reality of risks posed by non-native has gained ground, to the extent that organisms that biocontrol agents, various international organizations biocontrol companies describe collectively as ‘benefi- have produced guidance on the risk assessment of cials’, have a status in some countries analogous to such species, including the European Plant Protec- invasive aliens. tion Organisation (EPPO), the Food and Agriculture The debate about the environmental safety of Organisation of the United Nations (FAO) and the non-native biocontrol agents has become polarized Organisation of Economic Cooperation and Develop- into two broadly distinct and opposing schools of ment (OECD) (see Bigler et al. 2005 for details). thought. The first argues that organisms have been Developments in Europe, particularly over the last transported around the world through international decade, have stemmed from the realization that the trade for hundreds of years and that biocontrol is an European Commission had no intention of introduc- extension of this ‘natural’ process; there have been ing a Directive for the regulation of invertebrate bio- very few reports of negative environmental effects control agents – as had been done for microbial over the past 100 years, hence the introduction of organisms and semiochemicals (Directive 91/414) – legislation would be disproportionate to the risks. and that as a consequence, any regulation would The second view is that biocontrol represents a dif- remain at the discretion of individual member states, ferent situation because the movement of organisms and therefore, any agreement between countries through trade is accidental whereas introductions for would have to operate on a voluntary basis. pest management are intentional and can therefore In the context of the focus on arthropod be evaluated prior to release; also, because releases symbionts, it is of interest to note that since the 504 J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH J. Bale Regulation of invertebrate biocontrol agents in Europe introduction of regulation for invertebrate biological Directive 2001/18, and the arthropod containing the control agents (IBCAs) in parts of Europe, no coun- GMO could be viewed as a PPP containing an ‘active try has required information on the symbiont con- substance’ (the GMO) and regulated under Directive tent to be provided as part of the licensing process 91/414 and EC Regulation 1107/2009. for the import and release of non-native insects and A further hypothetical arthropod–symbiont combi- mites, although this is usually included for entomo- nation could emerge in the future that would raise pathogenic nematodes (EPNs). As there is no evi- different regulatory questions. There is a regular dence of horizontal transfer of symbionts between influx of non-native insect and mite pests into Europe arthropod species, at least under natural conditions such as the leaf mining Tomato moth Tuta absoluta (Chiel et al. 2009), this policy is unlikely to change.