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. that has invaded the southern Europe tomato crop However, with advances in the molecular taxonomy from South America. A symbiont from a different of symbiont species and strains, and in the techno- insect species could be transferred to a population of logy to facilitate horizontal transfer between species, T. absoluta that conferred cytoplasmic incompatibility it is possible to envisage future novel combinations when male moths mated with females of the estab- of arthropod species and microbial symbionts that lished European population. In an application to might be exempt from any regulation, subject to one release the ‘new’ symbiont-containing non-native T. or more of the existing EU regulatory frameworks absoluta, the insect would clearly be a plant pest, and e.g. genetically modified organisms (GMOs) or plant therefore subject to a Pest Risk Analysis by the Plant protection products (PPPs), or may require a new Health Panel of the European Food Safety Authority regulatory process, or guidance. The following sec- (EFSA), but it would also function as a non-native tion outlines some current and hypothetical exam- biocontrol agent. ples to highlight some of the regulatory challenges For the purpose of this review, it has been that may lie ahead. assumed that non-native arthropods containing their In Australia, a native strain (wMel) of the bacterial natural symbionts would be subject to the existing endosymbiont Wolbachia pipientis has been transferred regulations for such IBCAs that operate in different under laboratory conditions from one native insect EU countries, although it will be important for the species (Drosophila melanogaster) to a different native arthropod symbiosis community and industrial part- species, the mosquito Aedes aegypti, as part of a con- ners to explore the legislation and regulatory systems trol strategy for mosquito-transmitted dengue fever that will be encountered as the science develops and (http://www.eliminatedengue.com). The transfer of specific arthropod–symbiont combinations become the wMel strain confers cytoplasmic incompatibility potential biocontrol products with market opportuni- when ‘infected’ A. aegypti male mosquitos mate with ties. wild-type females such that there is a progressive An analysis of the status of biocontrol in Europe reduction in vector competence and loss of other fit- with invertebrate agents conducted 10 years ago ness traits over time (O’Neill pers. comm.). In this would have identified a number of issues and prob- example, the donor and recipient insect species and lems that needed to be addressed including: the Wolbachia strain are all native to the same coun- l Fragmented system of regulation across Europe try where the release will be made, and although l Inconsistency in information requirements A. aegypti has not acquired the wMel Wolbachia strain between countries in nature so far, it has a continuing opportunity to l No agreement on format for environmental risk do so. A case can be made that the novel A. aegypti– assessment Wolbachia wMel strain combination is a native organ- l No guidance on methods for environmental risk ism that requires no regulation beyond that already assessment in place for other native biocontrol agents (which l Lack of knowledge on the applicability of envi- may be none). It would be interesting to pose the ronmental risk assessment methods to different taxo- question of how IBCA regulators in EU countries nomic groups (insects, mites and nematodes) would view a similar case in Europe. l No process for updating the EPPO ‘Positive List’ In other situations, it is clear that regulations gov- of safe species (created in 2001) erning GMOs and PPPs would apply. For example, if l Limited expertise in biocontrol in some countries a symbiont was genetically modified and transferred to evaluate environmental risk assessment data on back into the same insect species, or a different spe- the first release in Europe of a non-native species cies, whether native or non-native, the symbiont l No forum for contact between regulators in dif- would be classed as a GMO and regulated under ferent countries

J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH 505 Regulation of invertebrate biocontrol agents in Europe J. Bale l Absence of coordinated international representa- in licence (permit) application documentation to be tion for IBCA-based biocontrol in development of a major problem; in effect, a new dossier had to be regulatory and related policies prepared for each submission. This variation was Against this backdrop, over the last 10 years, vari- unsurprising given that the legislative basis for regu- ous EU-funded projects such as ERBIC (‘Evaluating lation differed between countries (e.g. pesticides, environmental risks of biological control introduc- phytosanitation, environmental protection), and tions into Europe’) and REBECA (‘Regulation of there was no dialogue between countries when biological control agents’ http://www.rebeca-net.de) establishing the scope of the information require- and international organizations such as the Interna- ments. The REBECA project produced a standardized tional Organisation for Biological Control – West Pal- application form to be used by companies when aearctic Regional Section (IOBC-WPRS) and EPPO applying for a licence to release a non-native inver- have focused attention on some or all of the issues tebrate biocontrol agent (Bale 2011). The form is identified above, with the collective aim of harmo- divided into five sections: (i) ‘Information on the nizing regulatory requirements so that costs to the applicant’ and ‘Purpose of application and use’. (ii) biocontrol industry could be minimized without ‘Taxonomy and origin’ and ‘Product information’. compromising environmental safety. This article pro- (iii) ‘Biology and ecology’ and ‘Assessment of risks vides an overview of developments in each of these and benefits’. (iv) ‘Submission details’ and subject areas, with direction to key references that ‘Agreement’. (v) ‘Appendices’. The merit of this provide more detailed information. standardized form is that it covers all types of appli- cation – native (where required) and non-native, and ‘research only’ as well as release. A guidance Regulation of invertebrate biocontrol agents in Europe document has been produced to accompany the The general situation has not changed greatly over application form which sets out the information that the past 10 years, with no large scale movement is required in each section (Bale 2011). This appli- either toward or away from regulation. Belgium has cation form has been adopted by the UK and the plans to introduce regulation for the first time in the same general format is used in The Netherlands and Flanders region and in some countries such as the Switzerland. It would clearly be helpful if this form UK there has been major revision of the types of became the standard document to be used in all EU information required in environmental risk assess- countries that regulate the import and release of ment; for example, direct measurement of overwin- non-native invertebrate agents. Discussions are tering ability rather than using climate matching underway with EPPO with the idea that these docu- between the countries of origin and release as a ments would become adopted as ‘EPPO Standards’, proxy indicator of establishment potential. The lack and thus recommended for use throughout the of interest of the European Commission in develop- EPPO region. ing a Directive for invertebrate biocontrol agents has had both advantages and disadvantages: based on the Environmental risk assessment experience of the regulation of microorganisms, a Directive would be bureaucratic and likely to The risks posed by the release of a non-native spe- increase ‘registration’ costs for an SME-based indus- cies can be categorized based initially on the purpose try with limited investment in R&D; but the down- of the introduction: for classical biocontrol, establish- side is the continued risk that a species with serious ment is an essential pre-requisite for success, and it non-target impacts could still be released in a country may also be desirable for populations to disperse with no regulation, and without any EU-wide coordi- widely from sites of release – hence good powers of nation, companies have to prepare separate licence establishment and dispersal would be beneficial applications (dossiers) depending on the information traits. The main concern over the release of a non- requirements of individual member states. native species for classical biocontrol would be its host range and the risk of predation or parasitism of non-target species, especially any that were rare or Information requirements for release licences endangered. By contrast, for an augmentative (permits) release into a glasshouse, evidence of a lack of over- During the REBECA project, biocontrol companies wintering ability (and thus likelihood of establish- identified the variation and inconsistencies between ment outdoors) would be a requirement for a different countries in the information requirements licence application in some northern European

506 J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH J. Bale Regulation of invertebrate biocontrol agents in Europe

countries; and if this can be shown, it would be less 1 Exotic Native important to investigate host range, because any impacts on non-target species would be unlikely, and also transient. However, in southern Europe 2 Augmentative BC Classical BC where the climate would favour year-round survival, establishment would be much more likely, and an 3 Establishment No assessment of host range would be important. In sit- Certain Possible Not uations where a species is mass released into open On request fields, such as with Trichogramma brassicae against 4 Host range, attack of non-targets Related, unrelated Related, and the corn borer Ostrinia nubilalis in central Europe, No and/or valued non-valued Yes even though it can be shown that populations can- On request not persist from 1 year to the next (or only at a very low level, Kuske et al. 2003), given the very large 5 Dispersal No Extensive Moderate Only local numbers released annually, it would be valuable to have information on likely dispersal distances from release sites, as this affects the risk that the parasit- 6 Direct and indirect effects Likely and Unlikely, limited, No Yes oid would encounter non-target hosts. permanent and transient The construction of a comprehensive risk assess- ment system for biocontrol has therefore to consider Fig. 1 Flow chart summarizing a hierarchical environmental risk asses- a range of interacting factors including the origin of sment scheme for arthropod biocontrol agents (from van Lenteren et al. the species (native or non-native), the purpose of 2006). the release (classical or augmentative/inundative), the type of release environment (glasshouse or open Methods for environmental risk assessment field) and the climate – both for ‘open’ release sites, and that which would be experienced by escaping The environmental risk assessment (ERA) summa- organisms from enclosed areas. rized in fig. 1 provides a conceptual framework for In 2003, IOBC-WPRS established the ‘Commission risk assessment, and a basis for determining the key on the harmonization of invertebrate biological con- information requirements that should be included in trol agents’ (CHIBCA) to review the scope of regula- a dossier compiled by a company when seeking a tion of invertebrate biocontrol agents in the WPRS licence to release a non-native species. However, it area, and following its report published as Bigler et al. is in this area that difficulties can arise in terms of (2005) the EU-funded REBECA project continued this the costs that industry may incur in acquiring essen- review process with representation from all the main tial information (especially if there is no relevant biocontrol stakeholders – industry, regulators and peer-reviewed literature on the subject species) by researchers. Both CHIBCA and REBECA recom- having to undertake research or outsource the work mended the environmental risk assessment system to an independent institution. It would be legitimate proposed by van Lenteren et al. (2006) shown in for a company to seek advice from a regulator on fig. 1, which fulfils all of the above-mentioned criteria the recommended methods by which to acquire the (covers all types of biocontrol and release environ- information or data to complete the application form ments). One of the key features of this approach is the to release a non-native species, but there is no flexibility to adapt the testing procedure depending agreed consensus on ERA methodology between on the intended use of the candidate agent (classical European countries with regulatory legislation. This or augmentative) and the nature and climate of the subject area was reviewed by van Lenteren et al. area of release. For example, if a species was being (2006), the main principles of which were included evaluated as a glasshouse agent for use in northern in a summary of ‘recommended methods for ERA’ Europe, it would be logical for the first test to assess produced by the REBECA project to accompany the winter survival and establishment potential. If the standard application form and guidance document species was found to be capable of overwintering (see Bale 2011). outdoors (possibly with a diapause trait), it is highly There are three main areas in an ERA: establish- unlikely that licences would be granted by the regula- ment, host range and dispersal, and these may inter- tory authorities, and industry could then make an act to produce both direct and indirect effects (van informed decision on the economic value of contin- Lenteren et al. 2006). For a glasshouse agent uing to invest in the risk assessment. intended for release in northern Europe a desirable

J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH 507 Regulation of invertebrate biocontrol agents in Europe J. Bale combination of features would be the absence of enables species to be categorized into three main establishment potential, and if assessed, a narrow ‘risk groups: ‘low’, where all individuals die within host range and limited dispersal. By contrast, for a 4–6 weeks in the field (e.g. Nesidiocoris tenuis; Hughes classical control agent, establishment is essential for et al. 2009), ‘medium’, where there is some survival success, and high dispersal ability would be impor- after 2–3 months (e.g. Macrolophus caliginosus; Hart tant in some situations – only the narrow host range et al. 2002), and ‘high’, where some individuals can would be a desirable feature for both classical and survive for the entire winter (e.g. Dicyphus hesperus; augmentative control schemes. Establishment poten- Hatherly et al. 2008). This relationship appears suffi- tial is primarily focused on overwintering ability and ciently robust for future assessment to be based on related aspects of the organism’s thermal biology, laboratory studies alone. although a source of hosts (for parasitoids) and prey All of the species in the ‘medium to high’ risk area (for predators) when the target pest is not available in fig. 2 overwinter either in one stage of develop- is also an essential requirement for long-term sur- ment, or develop slowly between life cycle stages vival (Hatherly et al. 2005, Hatherly et al. 2009). In without reaching the adult stage and needing to mate the context of Europe, the influence of climate on to sustain the population. There are although some establishment is mainly relevant to countries or species with the potential to establish in temperate regions within large countries that have a distinct and similar climates that within individual life cycle winter season (e.g. northern France). stages would not ‘register’ as high risk based on an There are a number of indicators of an ability to assessment of specific life cycle stages. One such establish in a temperate or colder climate, and each example is the aphid parasitoid Lysiphlebus testaceipes. of these can be assessed. Species originating from Parasitoid larvae are able to develop in winter within tropical and similar warm climates often have a high their aphid hosts and emerging adults can parasitize developmental threshold temperature, e.g. 10Cor new hosts (Hughes et al. 2011). In this example, each higher, whereas temperate species can develop at life cycle stage is sufficiently cold hardy to survive in 5C or lower. Linked to this, when tropical species winter, but no stage survives for the whole winter; are placed in an ‘acclimation regime’, e.g. 5 or 10C maintenance of the population from the end of sum- for 7 days, a substantial proportion die, whereas mer to the following spring depends on development other species become more cold hardy over this per- and reproduction across at least two generations. iod of time. The occurrence of a diapause (dormant) trait is also a common feature in insects and mites living in temperate and colder climates, and where 120 = 1.4656 + 12.355 present in a candidate agent, would increase the y x R2 = 0.9292 likelihood of winter survival and permanent estab- ) 100

lishment, e.g. Neoseiulus californicus (Jolly 2000). Dia- ays (d pause can be obligatory (genetically programmed to l 80 va occur at the same stage of development in every i individual) or facultative (can be induced or averted

surv 60 M. caliginosus depending on environmental cues). The most com- ld E. eremicus e A. swirskii fi mon diapause-inducing cue is the decreasing photo- N. californicus period in autumn; there are standard regimes to test 40 T. montdorensis

mum N. tenuis i for diapause ability and these can be included rou- D. catalinae ax D. hesperus tinely as part of the assessment of establishment M 20 potential.

Species with a low developmental threshold tem- 0 perature, an acclimation ability and a diapause trait, 0 10 20 30 40 50 60 70 are likely to be ‘cold hardy’, and this attribute can LT at 5ºC (days) 50 be quantified by various indices (freezing tempera- ture, lethal temperature, lethal time). A series of studies on a range of glasshouse agents has identified Fig. 2 Relationship between the LTime50 at 5C (days) and maximum field survival in winter of eight biocontrol agents non-native to the UK a strong correlation between laboratory survival at (Macrolophus caliginosus, Neoseiulus californicus, Delphastus catali- 5C (lethal time at which 50% of population are nae, Eretmocerus eremicus, Typhlodromips montdorensis, Dicyphus killed) and the duration of survival in the field in Hesperus, Amblyseius swirskii and Nesidiocoris tenuis; from Bale et al. winter (fig. 2; Hughes et al. 2011). This relationship 2009).

508 J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH J. Bale Regulation of invertebrate biocontrol agents in Europe

The area that is most problematic in an ERA is the a glasshouse release with no establishment potential assessment of host range. A sequential experimental outdoors, there would be no need to assess dispersal; approach has been proposed involving choice and and if unexpected establishment did occur, the no-choice tests with target and non-target hosts and species would most likely disperse over time, and in prey carried out on different spatial scales. The main any case, this would not be preventable. The situa- areas of debate concern the interpretation of labora- tion where dispersal information is most valuable is tory data in the context of natural environments with the inundative mass release of large numbers (including agricultural ecosystems), the numbers of of parasitoids or predators that even with an oligo- species to be included in host range tests, and the cri- phagous feeding behaviour, could impact on non- teria for selecting test species (see Kuhlmann et al. target fauna if dispersal from the release site was 2006 and van Lenteren et al. 2003, 2006 for reviews). extensive. This type of study was conducted for the As an example of one of these problems, in a study parasitoid T. brassicae against O. nubilalis in Switzer- on the parasitoid Peristenus digoneutis, a biocontrol land and dispersal from the release sites in maize agent of European origin released against the mirid fields was extremely limited (Kuske et al. 2003). pest Lygus lineolaris in North America, the fundamen- tal host range assessed in the laboratory was greater ERA for entomopathogenic nematodes than the ecological host range observed in the field (in Europe and North America), both in terms of the The ERA process (fig. 1) and methods described above number of species successfully parasitized and the were devised primarily as a system for insects and level of parasitism (Haye et al. 2005) – overestimating mites. There was extensive discussion during the the actual environmental risk of the control agent. REBECA project as to whether any ERA of EPNs was It is difficult to provide definitive advice on the necessary, and if so, whether the principles developed number of species to be included in host range tests for arthropods were applicable to EPNs. The main and as noted by van Lenteren et al. (2006), transfer- arguments against the need for testing were that EPNs ring the system used in the risk assessment of weed did not persist at release sites, had narrow host ranges, biocontrol agents (where 40–100 plant species might and very limited powers of dispersal before dying out be tested) to arthropods would be prohibitively (Bathon 1996; Barbercheck and Millar 2000). In rec- expensive. Recognizing that non-native glasshouse ognition of environmental concerns in some EU biocontrol agents require sources of wild hosts or countries it was recommended that EPNs should be prey as well as overwintering ability to establish out- included in the same ERA system as arthropods, but doors, Hatherly et al. (2009) proposed that tests on as on the basis of the characteristics of species currently few as 3–5 non-target species could give a prelimin- marketed as biocontrol agents, data on establishment, ary indication of feeding behaviour (e.g. oligopha- dispersal, host range would not normally be necessary gous or polyphagous). Using the known polyphagous because of the limited potential of EPNs to disperse or predator M. caliginosus (marketed as a control agent persist at the site of application. against glasshouse whitefly Trialeurodes vaporariorum), Entomopathogenic nematodes used in biocontrol the performance of the mirid (development and carry symbiotic bacteria (Xenorhabdus and Photorhab- reproduction) was assessed with the target glasshouse dus species), but the nematodes do not infect higher prey, a closely related species, the cabbage whitefly vertebrates and the bacteria cannot survive outside of Aleyrodes proletella, and a further species that would the nematode or insect. However, there is one excep- be encountered outdoors throughout the year, the tion to the normal ERA exemption and this concerns aphid Myzus persicae. The predator was able to com- Heterorhabditis indica because of the rare association plete at least three generations with all prey species, with this nematode of the symbiotic bacterium although the level of mortality during development Photorhabdus asymbiotica (a human pathogen) rather to adult depended on the host plant as well as the than the commonly vectored symbiont P. luminescens prey. Inclusion of 1–2 additional species, less closely subsp. akhurstii. For this reason, there should be a related to the target pest, might be sufficient to at precise identification of the symbiotic bacterium least inform decisions on whether further investment when H. indica is used for biocontrol. in host range testing of the subject species would be economically worthwhile. Updating the EPPO positive list Dispersal is the third component of the ERA (fig. 1), but the need for this assessment would be The EPPO ‘List of biological control agents widely limited to specific circumstances. For example, with used in the EPPO region’ that became commonly

J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH 509 Regulation of invertebrate biocontrol agents in Europe J. Bale known as the ‘EPPO Positive List’ was first published aged or directed down one of two routes: either the in 2001 and updated in 2002. The central idea of the status quo would continue, in which case any har- Positive List was to provide a reference document of monization would be on a voluntary basis and ‘safe species’ to which regulators and other stake- apply only to those EU countries with regulation holders could refer as part of the evaluation of the (but other countries could ‘opt in’ over time); or an safety of release of a non-native species into a new EU-wide system of regulation could be introduced country in the EPPO region. The original list was via a new legislative Directive of the European divided into two main sections (Appendix I and II) Commission. Once the relevant environmental and comprising ‘commercially produced’ agents and agricultural authorities of the Commission (Director- those introduced for classical biocontrol respectively. ate General Environment – DG Environment and When the list was first compiled there was no coor- Health and Consumer Protection Directorate Gen- dinated history of environmental risk assessment in eral – DG SANCO) made clear that there was no the EPPO region and few peer-reviewed post-release desire to introduce legislation for invertebrate bio- studies on even the most commonly used species. control agents, it was evident that any harmoniza- The first list was therefore prepared on the basis of tion would have to be on a voluntary basis. The ‘expert judgment’ with the main criterion for inclu- aforementioned standardized licence application sion being a record of use in ‘at least five countries form, accompanying guidance document, and rec- for 5 years with no reported negative environmental ommendations on methods for ERA were all devel- effects’. oped in support of the aim of a more consistent From 2002 onwards there was no further re-evalu- approach to regulation among different EU coun- ation or updating of the list until discussions were tries, if not complete harmonization. However, held in 2007 between EPPO and IOBC-WPRS with there was a perception that in some EU member view to establishing a new joint panel to review and states there was limited expertise in biological con- maintain the Positive list – a course of action that was trol that might prevent an appropriate scientific endorsed in the final report of the REBECA project. analysis of dossiers containing ERA data, especially Meetings of the reactivated panel have been held in for species that had never been previously released 2008, 2009 and 2010. Whilst there have been some in a European country. This would not have been a deletions from the original list (see http://archives. problem if a Directive had been in place because a eppo.org/EPPOStandards/biocontrol_web/bio_list.htm panel of experts could have been created to support for updated version) and some recent additions (using the regulation, equivalent to the EFSA panels on broadly the same criteria as above), the judgements GMOs and plant pest species. The REBECA project on safety that were made by the first expert panel recommended that even if it was on a voluntary have been confirmed for the great majority of species. basis, it would be desirable for a reputable interna- The joint EPPO-IOBC panel has also added an tional organization to take on the role of an ‘expert additional appendix which gives details of species that group’ to evaluate the ERA on a first release of a have been removed from the list and the supporting non-native biocontrol agent in Europe as a service evidence for such a decision. Such changes are made to member states, acknowledging that the advice on the basis of published literature rather than anec- given would be non-binding. The EPPO-IOBC panel dotal reports. The future frequency of panel meetings established to update the Positive List was envisaged will depend on the number of proposals for new addi- to have the necessary expertise to fulfil this func- tions to the list, or concerns about the environmental tion; however, it is not within the remit of EPPO to safety of species currently on the list. provide advice to individual countries, hence such an activity for biocontrol would create a precedent, and the resource implications prevented IOBC- First releases in a European country WPRS from taking on this responsibility alone. The earlier activities of the FAO and OECD and The necessity for such an expert group depends more recently, IOBC-CHIBCA and REBECA, shared on the frequency with which new licence applica- a common purpose: to develop guidance on the tions are received in different countries, and the environmental risk assessment of non-native bio- expertise in biological control available within each control agents. In the case of REBECA, this aim national licensing authority. There are successful was intended to lead to a wider objective – the har- models operating in some countries in which a ‘con- monization of regulatory systems across Europe. sultative group’ of experts in biocontrol and environ- Progress toward this goal could have been encour- mental protection provide advice on ‘first releases’ to

510 J. Appl. Entomol. 135 (2011) 503–513 ª 2011 Blackwell Verlag, GmbH J. Bale Regulation of invertebrate biocontrol agents in Europe the relevant ministry (e.g. UK and Switzerland), and support for the regulator community that would in in the absence of an international panel, this turn be of considerable benefit to biocontrol in Eur- approach could be adopted more widely. ope and the EPPO region.

Forum for regulators Discussion and Conclusions The absence of a unified system of regulation across A comparison of the scientific and political backdrop Europe has been cited as one of the reasons why to biocontrol in Europe in 2000 set out in the Intro- biocontrol with ‘exotic’ invertebrate agents has been duction to this article and that which pertains in 2010 successful, including the freedom to import and would indicate that progress has been made on a release in some countries without any constraints. number of fronts. There was continuity from IOBC- However, this fragmented backdrop to regulation CHIBCA to the REBECA project and the opportunity has also been unhelpful to the European biocontrol for the industry and regulator perspectives to be industry – the need to prepare a new dossier for discussed openly has been valuable, underpinning each regulating country and the lack of any ‘mutual some significant achievements. At the present time, recognition’ of ERA data between neighbouring although there is no ‘mutual recognition’ of safe countries, even those with similar climates, being releases between neighbouring countries with similar two examples of such problems. But without any climates – which would be valuable for the biocontrol Europe-wide common agreement on regulation, industry – there is the potential for this to happen whether compulsory or voluntary, there has been now that comprehensive licence application docu- no mechanism or forum for regulators to meet mentation is available, and there is an emerging together, or with representatives of the European consensus on reliable ERA methods for the assess- biocontrol industry e.g. International Biocontrol ment of establishment potential and host range of Manufacturers’ Association (IBMA). IBCAs. However, cooperation on biocontrol policy Both the IOBC-CHIBCA and the REBECA project and regulation between countries is more of a politi- ensured that there were representatives of the indus- cal than a scientific issue, requiring encouragement try, regulator and research communities at all discus- and support from national and international agencies. sions, and the need to establish a process for Collaboration between EPPO and IOBC has regulators to meet at regular intervals was identified enabled an updating of the ‘Positive List’, and it will as an ongoing desirable practice. Without the oppor- be important for this activity to continue. The avail- tunity for such meetings, the frequent turnover of ability of expertise on biocontrol in government personnel, the enlargement of the European Com- departments that make decisions on licence applica- mission, and the lack of expertise in some countries tions remains a concern, although some countries all mitigate against beneficial developments such as have introduced national ‘consultative groups’ to adoption of the standardized documentation for provide expert advice. On this basis there would licence applications, sharing of information, and the seem to be scope for a ‘European level Expert possibility of inter-country regulatory collaboration as Group’, but at the present time it is not clear a forerunner to more formalized licensing agree- whether there is an international organization that ments. Since the end of the REBECA project there could take on this role or coordinate the activity, has been no proposal by which to facilitate the what the demand would be from member states, exchange of information between regulators of inver- and how such a venture could be resourced. tebrate agents in different EU member states. A fur- Looking ahead, there are a number of develop- ther consequence of this inertia is that it has not been ments that might lead to a change in the current possible to communicate to regulators the recent situation whereby legislation on non-native IBCAs is developments with the EPPO-IOBC Positive List, or determined by national governments. The Harlequin to gauge the likely demand for an ‘expert group’ to ladybird H. axyridis would have failed the ERA provide advice on first releases, and whether member tests on establishment, host range and dispersal if states would be prepared to pay for such a service. these had been conducted prior to its release in Eur- For these reasons, a meeting of all EPPO region regu- ope 20 years ago (van Lenteren et al. 2008), and is lators with responsibility for invertebrate agents will an example of the type of problem that can arise be included as part of the 2011 EPPO-IOBC Positive when some European countries do not have any List panel meeting. Looking ahead, EPPO-IOBC could restriction on non-native releases for biocontrol. provide the necessary coordinating and logistical Current negative reports on Harmonia include

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‘nuisance damage’ in properties, and infestation of similar to regulatory policies in place in Australia and grapes harvested for the wine industry but Harmonia New Zealand, and in line with a commitment given has spread rapidly through Europe over the last dec- by the Council of European Ministers in 2009. ade (Brown et al. 2008) and its full environmental Invasive alien species is a general term that covers impact on non-target species may be still to emerge ornamental plants (e.g. Japanese knotweed P. cuspida- – although there are some ‘early warning’ signs of tum), birds (e.g. Ruddy duck Oxyura jamaicensis), and potential problems in the years ahead (De Clercq aquatic species (e.g. Signal crayfish Pacifastacus lenius- and Bale 2011). A CABI survey of the coccinellid culus), many of which were intentional introductions fauna on broad-leaved trees in North-west Switzer- to Europe but subsequently caused widespread land has found an increasing proportion of Harmo- environmental damage. Unless a distinction is made nia, from around 6% in 2006 to 55% in 2008 (Kenis between ‘beneficial’ organisms and alien species more et al. 2010) and this has reached 90% in 2010 generally, non-native biocontrol agents could become (Kenis pers. comm.). A similar pattern has been included in the proposed new legislation. observed with field monitoring in Belgium where The Plant Health Panel of the European Food Harmonia has extended its distribution and increased Standards Authority (EFSA) carries out ‘Pest Risk in abundance between 2002 and 2008 with a corre- Analysis’ (PRAs) of potential novel pests to Europe sponding decrease in abundance over the same time (or those established only parts of Europe) based on period of native coccinellids such as Adalia bipunctata similar principles to the ERA of non-native biocon- that occupy an overlapping niche with H. axyridis trol agents. There is therefore an ‘expert group’ (Adriaens et al. 2008). Harmonia is therefore a already in place at a European level that could in ‘touchstone’ that may yet drive a change in Euro- theory consider a request from a member state for pean policy, drawing a sharp focus between those an evaluation of a dossier on a non-native biocontrol countries with regulation and evidenced-based safe agent, or provide a model on how this could be releases of non-native species, and those without delivered via a new panel. regulation that can lead to widescale problems When viewed in the round, there does seem to be beyond the country of release. The wider conse- a direction of travel toward greater regulation of quence is that the perception of biocontrol as a safe non-native biocontrol agents in Europe, either as a and reliable component of an integrated strategy to result of an unforeseen environmentally damaging combat insect pests – which justifies the collective release, the inclusion of such species in broader description of predators and parasitoids as ‘benefi- ‘environmental protection’ legislation’, or by an cials’ – may change to a more negative view, with a extension of the remit of an existing European Com- focus on the deleterious impacts on native fauna. It mission funded body. In light of these possible future has to be acknowledged that even if the concerns options it would seem wise for all European member about Harmonia prove to be unfounded, similar states to adopt a voluntary code of risk assessment releases could still occur, and this would stimulate a without delay, or run the risk of having a more further debate about the need for an EU-wide policy expensive, bureaucratic and compulsory system on regulation. introduced, which could seriously undermine the In the same way that national regulation of non- contribution of biocontrol to pest management as native biocontrol agents is founded on existing legisla- well as the viability of the industry in Europe. tion relating to different areas of activity, e.g. plant health or environmental protection, there is the References possibility that in future such species may become regarded as potential invasive alien species rather Adriaens T, Gomez GSMy, Maes D, 2008. 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