Assessing Risks of Releasing Exotic Biological Control Agents of Arthropod Pests

27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV 10.1146/annurev.ento.51.110104.151129

Annu. Rev. Entomol. 2006. 51:609–34 doi: 10.1146/annurev.ento.51.110104.151129 Copyright c 2006 by Annual Reviews. All rights reserved First published online as a Review in Advance on September 7, 2005

ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL AGENTS OF ARTHROPOD PESTS

J.C. van Lenteren,1 J. Bale,2 F. Bigler, 3 H.M.T. Hokkanen,4 and A.J.M. Loomans5 1Laboratory of Entomology, Wageningen University, 6700 EH, Wageningen, The Netherlands; email: [email protected] 2School of Biosciences, University of Birmingham, Birmingham B15 2TT, United Kingdom; email: [email protected] 3Swiss Federal Research Station for Agroecology and Agriculture, Zurich¨ CH 8046, Switzerland; email: [email protected] 4Department of Applied Biology, University of Helsinki, FIN-00014, Finland; email: [email protected].ﬁ 5Section Entomology, Plant Protection Service, 6700 HC Wageningen, The Netherlands; email: [email protected]

KeyWords environmental risk assessment, host range, establishment, dispersal, nontarget effects ■ Abstract More than 5000 introductions of about 2000 species of exotic arthropod agents for control of arthropod pests in 196 countries or islands during the past 120 years rarely have resulted in negative environmental effects. Yet, risks of environmental effects caused by releases of exotics are of growing concern. Twenty countries by Wageningen UR on 06/07/07. For personal use only. have implemented regulations for release of biological control agents. Soon, the In- ternational Standard for Phytosanitary Measures (ISPM3) will become the standard for all biological control introductions worldwide, but this standard does not provide methods by which to assess environmental risks. This review summarizes documented nontarget effects and discusses the development and application of comprehensive and Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org quick-scan environmental risk assessment methods.

SETTING THE SCENE: NONTARGET EFFECTS CAUSED BY EXOTIC BIOLOGICAL CONTROL AGENTS

Classical biological control (CBC) of insects, in which exotic natural enemies are introduced to control exotic pests, has been applied for more than 120 years, and the release of more than 2000 species of natural enemies has resulted in the permanent reduction of at least 165 pest species worldwide (45, 46). Augmentative biological control (ABC), in which exotic or native natural enemies are periodically

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released, has been used for 90 years, and more than 150 species of natural enemies are available on demand for the control of about 100 pest species (107). Contrary to the thorough environmental risk evaluations applied in the search for natural enemies of weeds (15, 75, 117), potential risks of biological control agents for arthropod control have not been routinely studied in prerelease evaluations (111, 108), with the exception of several CBC programs for which accurate nontarget species testing has been used (10, 83). The reason might be that, until now, very few problems have been reported concerning negative effects of releases of arthropods for control of arthropods (77), despite more than 5000 introductions in at least 196 countries or islands (45, 46, 106, 107). However, discussion of the risks of releases of exotic natural enemies for nontarget species now takes a prominent place in biological control programs. Retrospective analyses of biological control projects have provided quantitative data on nontarget effects and illustrated the need for risk assessments to increase the future safety of biological control (76, 77). A logical way to reduce the risks of releasing exotic species, and particularly in ABC, would be to use native species. Nonetheless, many exotic species have been released without even considering the use of native species (106, 107). In this review, the terminologies relating to biological control and environmental risk assessment (ERA) have been taken from recent publications in this area (23, 32, 38, 62, 85).

Potential Risks of Releasing Exotic Biological Control Agents Potential risks arising from the introduction of exotic biological control agents include those to human health, the economy, and the environment. An overview of potential risks is given in Table S1 (follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org). Health risks to production/application personnel and consumers are not unique to exotic inverte-

by Wageningen UR on 06/07/07. For personal use only. brates, and none are known for any macroorganisms, except some cases of allergy in the mass production of predatory mites or nematodes (31). Sometimes, economic losses may occur if introduced natural enemies attack previously introduced biological control agents (43). By far the most important risks from biological control introductions relate to possible changes in the distribution and abundance of na- Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org tive organisms, i.e., the environmental risks. A distinction should be made between nontarget feeding and nontarget impact: If occasional feeding on a nontarget does not result in changes in the distribution or abundance of the nontarget, it should not be regarded a problem. Another distinction to be made is between native and exotic nontargets: If a biological control agent affects exotics (other than those introduced on purpose), the impact should not be considered negative. The true environmental risks include the possibility of a global or local extinction of a native species (target or nontarget); large reductions in either the distribution or abundance of native organisms; interference in the efﬁcacy of native natural enemies of pests via intraguild interactions or competitive displacement; vectoring of pathogens harmful to native organisms; loss of biodiversity and identity of 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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native species via hybridization between close relatives; and in general, any major shifts in the balance of native species via direct or indirect mechanisms. The most serious threat is that of global extinction of a species—all other possible impacts are relative and may be reversible. We refer to Louda et al. (76) for an extensive discussion of environmental risks related to the release of exotic natural enemies.

Nontarget Effects Caused by Exotic Biological Control Agents To obtain a realistic perspective, it is essential to review the abundance and nontarget impacts of all nonindigenous organisms before considering those caused by exotic natural enemies. An overview of these nontarget impacts is given in Table S2 (follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org). Accidentally introduced organisms greatly outnumber those that have been intentionally introduced practically everywhere, often by a factor of 10 or more. Of the approximately 50,000 accidentally introduced organisms in the United States, 10% to 50% have caused ecological problems (88). Most intentional introductions concern crop and ornamental plants, many of which have become troublesome weeds (2.2% of all introduced plants in the United States) (87). Of all the nonindigenous insects in the continental United States (1554 species), more than 50% are considered pests (92), whereas of the intentionally introduced insects, only about 1.4% have caused problems (87). Interestingly, many of the exotic biological control agents recorded in the United States have arrived there accidentally (92). Looking speciﬁcally at biological control introductions of insects, it becomes obvious that these introductions have been comparatively safe, particularly in light of the general safety patterns of exotic organisms (see above): Less than 1% appears to have caused population-level effects in nontargets, and only 3% to 5% may have caused some smaller effects. However, only a minority of introductions have

by Wageningen UR on 06/07/07. For personal use only. included a careful evaluation of nontarget effects. On the other hand, if strong nontarget effects had appeared, they would have been observed and reported. Many inundative releases of arthropods appear to have some transient effects on nontargets—particularly polyphagous agents—but none have caused population- level effects, probably because of their transient nature (77). Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org Table 1 gives examples of known cases of suspected nontarget impacts on native insects resulting from biological control introductions. Many of these are subject to controversy because there is no strong evidence for the prime reasons for the observed population declines. All three possible global extinctions that have been linked to biological control introductions are disputed by some experts: Extinctions have not been proven, and other factors may have contributed to them much more than the exotic agents did. However, in several cases successful biological control agents have caused population declines not only in their target hosts, but also in some nontargets, including those that have depended on the target host as their major source of food. Moreover, the exhaustive data search of Lynch et al. (77), in which more than 5000 recorded biological control cases were analyzed and 30 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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TABLE 1 Cases with clearest evidence for nontarget effects on native insects of released exotic biological control agents Suspected effect Introduced natural Affected native (references) enemy species Location, time

Possible global Bessa remota (Aldrich) Levuana iridescens Fiji, 1925 extinction (60, 70, Bethune-Baker 94, 102) (target pest) Possible global Bessa remota (Aldrich) Heteropan dolens Fiji, 1925 extinction (94, 102) Druce (nontarget) Possible global Lespesia archippivora Agrotis crinigera Hawaii, early extinction (41) (Riley) (Butler) 1900s Reduction in Cotesia glomerata (L.) Pieris napi oleraceae Massachusetts distribution range Harris late 1800s (76, 97) Reduction in Tetrastichus dryi Trioza eastopi Orian La Re´union, population levels (3) Waterston 1978 Reduction in Compsilura concinnata Several species of North America, population levels (76) (Meigen) native Lepidoptera 1906 onward (Saturniidae) Partial displacement of Coccinella Coccinella North America, native natural septempunctata (L.) novemnotata Herbst; 1973 onward enemies (33, 119) Coccinella transversoguttata Fald.; Adalia bipunctata (L.) Partial displacement of Cales noacki Howard Native parasitoids of Southern Italy, native natural Aleurotuba jelinekii 1980–1994 enemies (114) (Frauenfeld)

by Wageningen UR on 06/07/07. For personal use only. Interbreeding with Aphelinus varipes Aphelinus varipes North America, native natural Foerster, species Foerster, species 1987 onward enemies (59) complex complex Lowering Cryptolaemus Dactylopius opuntiae Mauritius, late effectiveness of an montrouzieri Mulsant (Cockerell) 1940s Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org introduced natural enemy for weed control (43)

international biological control experts were contacted for additional information, has underlined our ignorance of the degree to which nontarget effects may occur. Therefore, environmental risk analyses need to become standard procedures in each biological control project (24). This does not necessarily result in fewer introductions of exotic agents, as has been shown by an evaluation of the IPPC Code of Conduct (67). However, it does lead to higher costs and delays introductions. 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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Evolution of Environmental Risk Assessment Various international legal frameworks regulate the introduction of exotic species into new environments in addition to several countries that have national regulations (21, 22, 39, 42, 61, 98, 99). For an overview of these regulations we refer to Table S3 (follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org). Countries with extensive experience in CBC (Australia, Canada, New Zealand, South Africa, United Kingdom, and the United States) had legislation and procedures in place relatively early to regulate imports and to analyze risks of exotic biological control agents (98). For those countries that had not, the FAO Code of Conduct served as a guideline (38, 67). The new version of this code of conduct (ISPM3) (62), which will become the international standard, has extended its range from CBC to ABC, native natural enemies, microorganisms, and other beneﬁcial organisms, and also includes evaluation of environmental impacts. Several other organizations have recently developed guidelines for import, evaluation, and release of biological control agents, and evaluation of environmental effects forms a central element of these guidelines (35, 36, 62, 81, 98). Also, a growing number of countries apply ERA procedures prior to the import and/or release of new natural enemies (4, 13, 98). To facilitate decision making on introductions, some organizations recommend working toward a regional species listing system based on higher biogeographic units, con- sistent with international law (42). For natural enemies, such lists are already used in some regions/countries (1, 37), but these are seldom the result of a thorough ERA procedure. Guidelines mentioned above aim to facilitate procedures for a proper risk assessment, but they do not yet provide working instructions for the risk assessment itself. For many other purposes, risk assessments are widely accepted as a tool for decision making and for evaluating economic and environmental costs and beneﬁts (42, 62). Aspects of risk assessments have been developed and applied during the

by Wageningen UR on 06/07/07. For personal use only. past two decades for exotic natural enemies, though often in a preliminary way (108). Methods have generally been derived from existing pest risk analysis protocols developed by regional organizations (34, 81). In others, methods are based on domestic regulative measures, largely as amendments of regulation relating to plant health, pesticide use, and/or biodiversity (28). Most procedures are not yet Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org tailored for the intentional release of biological control agents. Some assessment procedures, like those of Australia, New Zealand, and Hawaii, are so strict that import and release of exotic natural enemies are extremely difﬁcult. By contrast, other countries have no regulations. Currently, there is a trend toward more stringent regulatory requirements (9). Novel strategies are necessary (4), more ecological information should be used to increase the precision of risk assessment (76), and both the risks and the beneﬁts of biological control applications should be considered in the evaluation (98). The Organisation for Economic Cooperation and Development (OECD) developed a harmonized ERA protocol (85), and the IOBC-WPRS (International Organization 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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for Biological Control of Noxious Animals and Plants—West Palearctic Regional Section) has drafted a detailed guideline on information requirements (13). Both documents provide guidelines to the preparation of dossiers in support of applications and assist reviewers in a balanced risk/benefit evaluation of future biological control releases. Today, the major challenge in developing risk assessment methodologies is to produce protocols that will help prevent serious mistakes through release of harmful exotics while promoting safe forms of biological control. The most critical ecological issues are to estimate the probabilities of attack on nontarget organisms and the dispersal and establishment capacities of the biological control agent. Few natural enemies are strictly monophagous (120), but many are oligophagous and thus have a restricted host/prey range. Others are polyphagous and have a wide host/prey choice. We expect that future ERAs will integrate information on the potential of an agent to establish in an environment, its abilities to disperse, its host range, and its direct and indirect effects on nontargets. Contrary to existing risk assessments and in order to be of practical use, future risk assessments should be (a) quantifiable, so that the environmental effects of different biological control agents can be compared and informed decisions made, and (b) consist of a stepwise procedure so that demonstrably safe agents will be identified early in the process, with lowest possible costs involved. The ERAs discussed below form an element of a general risk assessment framework for the regulation of import and release (108) and consist of the following basic elements: (a) characterization and identification of the biological control agent, and determination of (b) health risks for humans, (c)environmental risks, and (d)efficacy.

ECOLOGICAL FACTORS DETERMINING THE ENVIRONMENTAL IMPACT OF AN INTRODUCED AGENT by Wageningen UR on 06/07/07. For personal use only. In this section, the significance of five risk factors of natural enemies (host range, establishment, dispersal, and direct and indirect effects on nontargets) and the ecological mechanisms involved are identified. Also, guidelines to data requirements and approaches for their quantification are provided. Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org Host Range Assessment The first, most critical, and difficult step in host range assessments is the selection of appropriate nontarget species (69, 105, 109). The centrifugal phylogenetic method based on phylogenetic/taxonomic affinities of nontarget species, which has been used for more than 30 years in weed biological control programs (117), is usually the starting point when evaluating natural enemies of arthropods. However, this phylogenetic approach is insufficient in arthropod biological control for a number of reasons, including poor knowledge of arthropod phylogeny, unreliable host lists, the greater number of taxa that can be attacked by natural enemies, and 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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other parameters such as the same feeding niche or the common habitat of target and nontarget species that may be more meaningful as nontarget indicators (69, 105). In addition, species of conservation concern may need to be included in nontarget testing. As a result, the initial nontarget test lists are often composed of large numbers of species, and testing of all these species would be impossible. Host range testing in weed biological control may include 40 to more than 100 plant species and is feasible because of the ease of storing plant seeds and plant rearing. However, arthropod hosts and natural enemies may not be amenable to laboratory culture, or their rearing is much more complicated. Thus, it has been proposed that nontarget species be selected from the following three categories to design initial test species lists (69): (a) species with phylogenetic/taxonomic affinities, (b) species with ecological similarities (habitat and/or niche overlap), and (c) species of conservation concern (beneficial, or rare/endangered). If this first selection results in an impractically long list, species can be filtered out on the basis of attributes such as nonoverlapping geographical distribution, different climate requirements, phenological asynchronization, or host size outside the range accepted by the candidate biological control agent. Other species might need to be removed from the test list because they are not available in large enough numbers. Furthermore, rare and endangered species might be replaced by congenors as surrogates for testing. The filtering process results in a provisional test list of 10 to 20 species from which species can be removed or added during a reiterative process that evaluates the outcome from the ongoing host range testing program (69). The actual host range tests aim to demonstrate if a natural enemy can feed, develop, or reproduce on a nontarget species. Laboratory testing can become complicated as a result of multitrophic chemical communication, learning, and wide host ranges involving many host plant species. Host preferences are determined not only by the choice of species offered, but also by the physiological condition and experience of the natural enemy under investigation. Hence, before a specific testing scheme is designed, knowledge needs to be obtained about the multitrophic by Wageningen UR on 06/07/07. For personal use only. system in which the natural enemy forages in order to make the tests meaningful (109). Particularly, behavioral variation, including learning, intraspecific variation, and genetic changes occurring during laboratory rearing of natural enemies, may complicate host range testing (73, 84, 105, 113, 118).

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org The literature abounds with speculations on how to perform host range testing, both from a theoretical and practical perspective (10, 12, 15, 108, 109). Here, we summarize a practical approach for host range testing for arthropod natural enemies (116) (Figure 1). The philosophy is that specialist natural enemies (mono- or slightly oligophagous species) are identiﬁed quickly with the relatively simple tests in steps 1 and 2. In these two no-choice tests (which are cautious in that they might overestimate the host range), the key question is whether the biological control agent attacks nontarget organisms in the appropriate stage on the relevant part (e.g., the leaf or a root) of its natural host plant/substrate. Use of positive (target species with the natural enemy) and negative (target and nontarget species without the natural enemy) controls is essential for interpretation of host range 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

616 VA N LENTEREN ET AL. by Wageningen UR on 06/07/07. For personal use only. Figure 1 Flow chart summarizing host range assessment of arthropod biological control agents. NT, nontarget. Modiﬁed after References 108, 109.

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org test results. If none of the nontargets and only the target is attacked, testing can be stopped because no direct effects are expected on the tested nontarget species in the field. If in step 1 nontarget organisms are attacked, but attack rates for nontargets are significantly lower than that for targets, the hazard to nontargets under field conditions is expected to be low. If nontargets are attacked only at the end of the observation period in step 2, then the risk of direct effects on these species is small. However, if nontargets are consistently attacked, and attack rates on target and nontargets are similar, nontarget effects might be considerable and further testing is mandatory. For polyphagous natural enemies, the time-consuming step 3 test and, in some cases, the even more complicated step 4 test need to be carried out before a 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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recommendation to release the species can be put forward. In step 3, attack of nontargets is tested under more realistic conditions with the option to choose between target and nontarget species. When nontargets are readily attacked on their natural substrate, the natural enemy poses a high risk. If nontargets are attacked late in the test and at a much lower attack rate than the target, then the natural enemy displays a strong preference for the target species but may attack the nontarget species under situations in which the target species is absent. Only when nontargets are consistently attacked at a low attack rate is the risk of direct effects on the nontarget species under field conditions expected to be small. Step 4 is a field test that can be performed in rare situations in which the nontarget species occur in the native area of the natural enemy. If a natural enemy readily attacks nontargets on their host plants in their natural habitat, it poses a high risk for nontarget effects. Depending on the multitrophic study under consideration, it is not always necessary to follow the sequence presented in Figure 1. Sometimes steps can be combined, in other situations, steps can be bypassed; a detailed discussion of this scheme, including statistical aspects, can be found elsewhere (109). Interpreting host range data is often difficult and is complicated by a range of factors: (a) overestimating host ranges in which nonhosts are used by agents when deprived of access to their normal hosts for long periods, (b) overestimating host ranges in which nonhosts are used when in close proximity to the normal host due to transference of stimuli, and (c) underestimating host ranges in which valid, but less preferred hosts, are ignored in the presence of a more preferred host. The disruption of insect behavior when organisms are held in confinement, or outdoors in cages, is well known for arthropod biological control agents (93, 96). For mono- or slightly oligophagous and for strongly polyphagous natural enemies, the above host range testing framework usually leads to clear evidence based on recommendations about risks for nontarget species. Host specificity data reported in the literature have been confirmed for a number of natural enemy species exposed to new nontarget species (20), but exceptions do occur (109). The most by Wageningen UR on 06/07/07. For personal use only. difficult group for which to interpret host range data are the more oligophagous and slightly polyphagous biological control agents. These agents might not be the most efficient natural enemies and result in only partial control, and they may also show more severe nontarget effects when compared with polyphagous species (77).

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org Host range test data have been used to reject introductions, for example, when natural enemies attacked at least 20 species of unrelated native nontarget species (97). In other cases, host range data were used to allow the release of parasitoids in some countries but not in others (95).

Establishment Depending on the control program and the environment into which an exotic agent is released, establishment may be the intended outcome or an undesirable event. Establishment is determined by abiotic and biotic factors. In CBC, preliminary studies are normally conducted to assess the similarity of climatic conditions 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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between the countries of collection and release. Similarly, if an exotic species es- capes after release into a greenhouse, establishment will depend on the ability of the organism to survive in a climate that is usually colder than that into which it was released and from where it was collected, and on sources of native hosts.

ABIOTIC FACTORS The main abiotic factor affecting the establishment of exotic species in new environments is temperature. Although humidity may play a role, it alone does not determine establishment. Many successes in CBC have involved introductions into similar climates, and an inability to survive through winter is a common cause of failure (27). Although “climate matching” is a useful guide to the similarities and differences between native and intended release areas, this approach is limited and is not a reliable basis for predicting survival and establishment (50, 51). Temperature has a major inﬂuence on the key processes that determine establishment and subsequent spread of introduced natural enemies. For all arthropods there is a temperature below which there is no development, i.e., the “developmental threshold.” A number of methods can be used to estimate the threshold temperature, which may lead to variation in the threshold (49–51). The thermal budget is the number of day degrees required to complete one gen- eration and, in combination with the threshold temperature, can provide valuable information on the likelihood of establishment at any intended release site. The threshold temperature can be related to temperature records to indicate periods in the year when there will be no development (such as winter), and the organism may have to enter a dormant state (diapause) to survive. Also, the thermal budget can be compared with estimates of the annual number of available day degrees above the developmental threshold to determine the likely voltinism at the intended release site. Knowledge of the cold tolerance and overwintering ability of a species is a

by Wageningen UR on 06/07/07. For personal use only. vital component in assessing establishment potential. Cold tolerance can be assessed by a number of indices that are best considered in combination rather than separately. Recognition of the importance of “cold” rather than freezing has led to more ecologically relevant classifications of insect overwintering strategies (6, 7) that can be applied to novel biological control agents. For species in Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org which “pre-freeze” mortality is extensive, cold tolerance can be assessed by the lethal temperature at which a given proportion of the population are killed in an exposure of fixed duration (LTemp), and the lethal time at which the same proportion are killed in an exposure at a constant temperature (LTime). These data can be analyzed to produce estimates of the temperature or time at which any proportion of the population would be expected to die (10, 50, or 90%), and then compared with survival under fluctuating field temperatures using outdoor quarantine cages, again varying the duration of exposure. Explanations for the failure to establish in a new environment can sometimes be identified by ecophys- iological comparisons between the introduced and a closely related native species (8). 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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BIOTIC FACTORS The availability of target host/prey in space and time, occurrence of alternative host/prey, presence of competitors, and access to food are important biotic factors that influence establishment. Biotic factors are more difficult to assess than abiotic factors and information from both areas of origin and introduction are often lacking. The ability of predators and parasitoids to synchronize their life cycle with their host/prey (target or alternative) is a fundamental prerequisite for establishment. This is critical for specialist natural enemies because they cannot use alternative hosts/prey to sustain populations when the target is not present or not in the right stage. The degree of synchrony often reflects the likelihood of permanence of host- parasitoid relationships and thus the probability of establishment (30). In temperate climates, permanent establishment of parasitoids is possible only if overwintering hosts are available. Native hosts may not be suitable for overwintering of the introduced parasitoid either because they are attacked at a physiological stage that does not allow development of the overwintering natural enemy or because the type of dormancy is unsuitable for the parasitoid (17). The probability of establishment in temperate climates is affected by mortality due to climatic extremes and to the difficulty of adjusting and synchronizing life cycles, especially when hosts enter quiescent or diapause stages during these unfavorable periods (5). Availability of adequate food increases parasitoid efficacy, but it is difficult to demonstrate the influence of food sources on establishment (63). The level of dependence on food is species specific but also a function of availability and quality, influencing life cycle parameters, behavior, competitive interactions, and niche partitioning of parasitoids and predators (64). Parasitoids and predators are carnivorous, but most species also use plant-derived foods, such as pollen, nectar, plant sap, and honeydew. Plant foods can have a strong effect on survival and population dynamics, particularly for obligatory plant-derived food consumers (115, 116). Facultative consumers can use plant foods to bridge periods of low host/prey availability (74). Plant-derived food is important, but we lack a full by Wageningen UR on 06/07/07. For personal use only. understanding of the effects of such factors on establishment.

EXAMPLE OF ASSESSING THE RISK OF ESTABLISHMENT Successful biological control schemes have been implemented in greenhouses, namely the management of Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org Trialeurodes vaporariorum by Encarsia formosa and Tetranychus urticae by Phy- toseiulus persimilis (111). These two programs have operated effectively over decades without any establishment outside of greenhouses in the cool climates of Western Europe or any deleterious effects on native fauna. In the search for “all-season control” in greenhouses, companies have sought new natural enemy species. Companies wishing to release new species are required to compile an ERA dossier, but critical information is often unavailable. For example, in the absence of studies on cold tolerance, it has been assumed on the basis of climate matching that winter would be an effective barrier to the establishment of species originating from warmer climatic zones in the United Kingdom. This is incorrect, as evidenced by the outdoor establishment of Neoseiulus californicus 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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◦ Figure 2 Relationship between maximum ﬁeld survival (days) and LTime50 at 5 C (days) for ﬁve nonnative biological control agents (data refer to unfed adults of all species except E. eremicus that were exposed as unfed larvae).

after ﬁrst release in 1991 and the occurrence outside of greenhouses in winter of Macrolophus caliginosus following release in 1995 (50, 51). Studies on the thermal biology of N. californicus (50), M. caliginosus (51), Delphastus catalinae (A.G. Tullett, unpublished data), Eretmocerus eremicus

by Wageningen UR on 06/07/07. For personal use only. (104), and Typhlodromips montdorensis (52, 53) assessed the effects of temperature on development, voltinism, and survival in the laboratory and field. A strong correlation was observed between survival in the laboratory at 5◦C and in the field in winter (Figure 2). D. catalinae, E. eremicus, and T. montdorensis died out quickly in winter, and survival was largely unaffected by variations Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org in temperature or access to prey. In contrast, some nymphs of M. caliginosus with whitefly prey survived in the field for more than 200 days. The establishment of N. californicus is attributable to the unintentional release of a diapausing strain, which can tolerate low temperatures and starvation (65), and the ability of the nondiapausing strain to survive for two to three months if prey are available and to reproduce prior to death. A risk assessment protocol of this type allows candidate species to be tested prior to release and placed into appropriate low- (D. catalinae, E. eremicus, T. montdorensis), medium- (M. caliginosus)orhigh- risk (N. californicus) categories in terms of the likelihood of establishment. Further tests on host range, nontarget effects, and dispersal would then be carried out as appropriate. 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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Dispersal The probability that a biological control agent will ﬁnd a potential nontarget host depends strongly on the dispersal capacity of the agent. Below we summarize dispersal characteristics and methods to measure dispersal.

MODES OF DISPERSAL AND ASSOCIATED RISKS Good searching and dispersal abilities are considered valuable indicators of successful biological control agents (111). Knowledge of dispersal characteristics is also essential for researchers to assess to what extent the agent could disperse into nontarget habitats. Dispersal is affected by trivial movements, host foraging, or migratory behaviors and can be separated into short-distance and long-distance movements. The scale (numbers and distance) of dispersal may vary considerably between taxa, populations, and regions (82). Natural enemies disperse actively by ﬂight or locomotion, and distance is positively correlated with body size (103). Dispersal by small-bodied agents such as entomopathogens (56), parasitoids (11, 71), and predatory mites (66) is limited in distance and time. However, such agents can become part of the aerial plankton and thus become widely dispersed. More rarely, adult parasitoids are actively vectored by their hosts (40). Migration, on the other hand, typically involves a mass movement to a distant location and is unidirectional, persistent, and undistracted (29). The encounter probability between the agent and its host or prey depends on the mechanism of dispersal, its life span, the local climate, and habitat conditions in the area of release (71, 76, 103). In ABC, in which natural enemies are released in large numbers for immediate control of the target pest, direct dispersal (overﬂow, drift) from the release area into the surrounding environment is of main concern for direct nontarget effects whether or not the natural enemy species is exotic. Moderate dispersal ability may greatly reduce the risks of nontarget effects (68). Habitat connectivity, in combination with the use of nontarget hosts, however, by Wageningen UR on 06/07/07. For personal use only. may enable an agent to spread rapidly through a landscape (90). Case histories of CBC, in which establishment is intended, indicate that introduced agents are able to disperse and reproduce on nontarget hosts at large distances from their target habitats (54, 76). Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org

METHODS, MARKERS, AND MODELS Knowledge of the dispersal characteristics of a natural enemy is crucial for understanding the probability of temporal and spa- tial encounters between the agent and nontarget species (108). The radius of potential nontarget impacts is determined by the dispersal ability and the potential population-level impacts by the density of the dispersers (80). A wide variety of materials and techniques exist for estimating short- and long-distance dispersal (29, 47, 72, 82, 100), but mark-release-recapture experiments are most suitable to study local dispersal of mass-released agents (80). To distinguish dispersing agents from the wild population, molecular markers are increasingly used (71). Abiotic factors (weather, wind) and biotic features of the agent (longevity, body size, wing 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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forms, sex, mating status, egg-load) and the environment (availability of resources, density of native hosts, landscape elements) largely modify the density-distance curve obtained. For mass-released agents empirical or diffusion-based models give the best estimates of mean and quantile dispersal distance, direction, and density (71, 80). More importantly, analysis of dispersal data can provide qualitative and quantitative scales for environmental impact assessment (108).

Direct and Indirect Effects of Released Organisms on Other Organisms in Ecosystems

EFFECTS ON NONTARGET HERBIVORES Sometimes the established exotic biological control agent may affect the abundance of native nontarget species. These species are not usually the preferred hosts of the agent, and therefore their abundance is seldom affected. When an agent does affect the abundance of a nontarget, it is highly unlikely that it will, on its own, lead to extinction. Natural enemies generally leave a host patch before they have found all hosts. Hosts also escape their enemies in space and time, reducing the chances of extinction. Furthermore, asyn- chrony between local dynamics allow for large-scale persistence even when local extinctions occur (48). As a result, pests have seldom if ever been exterminated in the more than 100 years of insect biological control. However, effective lowering of population densities in small habitat patches or tropical islands will increase the likelihood that other factors, including chance events, will destroy a population completely, in contrast to patterns observed on large islands or continents (78). Therefore, it can be expected that some species utilized by biological control agents will become part of the natural extinction/ colonization dynamics. It is unlikely that the extinction rates of these species differ signiﬁcantly from that of other species in the same ecosystems.

EFFECTS ON OTHER TROPHIC LEVELS: INTRAGUILD PREDATION, ENRICHMENT, AP- by Wageningen UR on 06/07/07. For personal use only. PARENT COMPETITION, AND VECTORING When the exotic agent is able to also attack natural enemies of the target herbivores [intraguild predation (91) or facultative hyperparasitism (101)] it might interfere with the regulation of these herbivores. An example is a study on the trophic and guild interactions of ﬁve species

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org of indigenous and introduced bethylid wasps used to control the coffee berry borer and lepidopteran pests of coconuts and almonds (86). One of the parasitoids not only killed conspecific and allospecific eggs and larvae, but could also develop as afacultative hyperparasitoid, threatening the establishment and survival of other parasitoid species. Intraguild predators or hyperparasitoids may lead to relaxed predation (19, 91), possibly resulting in temporal outbreaks of the prey. Ultimately, it may increase populations of natural enemies that have been released from their competitors (89). An exotic control agent itself may serve as food for other organisms (enrichment), increasing these populations, but possibly influencing indirectly populations of the target. Introduction of such an exotic may temporarily release or increase the predation pressure on the carnivore’s prey, depending on the behavioral 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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response (58). On a longer timescale, the natural enemy population is expected to increase. Ultimately, this may result in a decrease of its prey (apparent competition between the agent and the other prey) (57, 79). Apparent competition mediated by a generalist hyperparasitoid has been investigated by studying how the relationship between a specialist braconid wasp, Cotesia melitaearum, and its generalist hyperparasitoid, Gelis agilis,was influenced by the introduction of a second braconid host of G. agilis, Cotesia glomerata, into the field (112). The addition of the new primary parasitoid increased populations of the hyperparasitoid, which then reduced populations of C. melitaearum,tothe extent that some of the original populations went extinct (112). Sometimes the natural enemy vectors pathogens or hyperparasitoids (14, 44). Forexample, insects always carry various eubacteria. Some of these are oppor- tunistic, whereas others are highly evolved pathogens such as Wolbachia,anintra- cellular parasite that can have profound negative effects on the reproductive fitness of biological control agents (44).

COMPETITION When an introduced agent attacks and reduces a herbivore population, it may negatively affect other natural enemies that exploit the same resource. Ultimately, only one of them may survive. For example, successive introductions of braconid parasitoids of fruit ﬂies into Hawaii led to the complete displacement and local extinction of the African species Psyttalia humilis by the Australian wasp Diachasmimorpha tryoni and, subsequently, the substantial displacement of D. tryoni in turn by the later arriving Southeast Asian species Fopius arisanus (79).

OTHER INDIRECT EFFECTS AND HYBRIDIZATION Any of the described effects may result in further changes in the ecosystem, for example, by affecting nonfood requirements (e.g., protection, pollination, and seed dispersal) of other species. Besides ecological changes, an exotic biological control agent may also cause genetic changes in other populations in the ecosystem. One possibility is hy- by Wageningen UR on 06/07/07. For personal use only. bridization between the agent and indigenous biotypes of the same or closely related species. An example is the Aphelinus varipes species complex, in which biotypes from various parts of the world hybridize, resulting in changed ecological preferences (59). Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org

RISK ASSESSMENT METHODOLOGY FOR BIOLOGICAL CONTROL AGENTS

Evaluation of risks related to the releases of natural enemies requires integration of many aspects of their biology, as well as information on the ecological interactions identiﬁed above. Risk assessments involve three phases. Phase 1 is the risk identi- ﬁcation and evaluation procedure concerning release of the agent and is reviewed below. Phase 2 consists of the risk management plan and includes risk mitigation and risk reduction (4, 26). It consists of instructions for shipment and materials used as well as screening and destruction of contaminants after arrival in the 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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country of release (108). Phase 3 involves the risk/benefit analysis of the proposed release. An appropriate risk analysis for a new biological control agent should contain risk/benefit analyses of other pest management methods to compare the risks and benefits with any other control method under consideration and make a well-informed decision (11, 98, 110). Phase 2 and 3 are reviewed elsewhere (108).

Risk Identification and Evaluation The ERA is the most difficult part of the overall risk assessment in biological control. A general framework developed for such an assessment (108) identified five risk factors: host range, establishment, dispersal, and direct and indirect nontarget effects, which consider different aspects of natural enemy biology and the environment of the system into which the natural enemy will be introduced.

RISK IDENTIFICATION AND QUANTITATIVE RISK EVALUATION METHOD Normally, for a risk evaluation, hazards are identified and the probabilities of such hazards materializing are assessed (55, 108). The hazard of a biological control agent can be defined as any imaginable adverse effect, which can be named and measured, such as direct and indirect adverse effects on nontarget organisms and adverse effects on the environment. The risk of adverse effects arising from the release of a biological control agent is the product of the impact of likelihood (probability) and the impact of magnitude (consequence). The likelihood (L) and magnitude (M) of the five groups of risk factors (host range, establishment, dispersal, and direct and indirect nontarget effects) are first considered. Then, a numerical value is assigned to each criterion to quantify risk: likelihood, from very unlikely (1) to very likely (5), and magnitude, from minimal (1) to massive (5). The criteria for determining in which likelihood and magnitude category a natural enemy will fall for the five groups of risk factors are specified by van Lenteren et al. (108). The

by Wageningen UR on 06/07/07. For personal use only. overall risk index for each natural enemy is then obtained by first multiplying the figures obtained for likelihood and magnitude, followed by adding the resulting figures obtained for dispersal, establishment, host specificity, and direct and indirect effects. The minimum score therefore is 5 (5 × 1 × 1) and the maximum is 125 (5 × 5 × 5). Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org In a first application of this methodology, 31 cases of natural enemy introductions were evaluated (108). This risk assessment methodology shows that different values can be obtained for the same organisms when evaluated for different release areas. For example, the whitefly parasitoid Encarsia pergandiella moved from the intermediate risk category (risk index 49) when applied in greenhouses in northern Europe to the highest risk category (risk index 73) when used in the field in the Mediterranean. However, this first quantitative risk assessment methodology also revealed several flaws: (a) Information about likelihood and magnitude of all five risk groups need to be available before an evaluation can be made, even for seemingly unac- ceptable exotic agents, and this results in unnecessary costly assessments. (b) The 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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numerical values obtained do not allow an unequivocal separation between risk categories, resulting in decision making that can be easily manipulated. (c) The overall risk index is obtained by summing ﬁve different categories that are not completely independent and should not be rated equally.

IMPROVED, COMPREHENSIVE ENVIRONMENTAL RISK EVALUATION METHOD Anew methodology that consists of a stepwise procedure has been developed and can be applied to all types of invertebrate natural enemies that are candidates for release in ABC and CBC, for species or biotypes, whether they are native, established exotics, or not yet established exotics (110) (Figure 3). by Wageningen UR on 06/07/07. For personal use only. Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org

Figure 3 Environmental risk assessment (ERA) scheme for arthropod biological control agents. NO: release is not recommended; YES: release is recommended. On request: when the applicant desires, information about following issue(s) in the risk assessment scheme can be provided to allow reconsideration of the decision not to release the species. BC, biological control. Modiﬁed after Reference 110. 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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At the ﬁrst step, exotic and native natural enemies are distinguished. For native natural enemies only one more step (step 6) in the procedure needs to be followed. Forexotic natural enemies, whether already present or absent in the target area, more steps need to be considered. At step 2, natural enemies that are produced for ABC programs, in which establishment of the organism in the area of release is not intended, are separated from natural enemies aimed for CBC, for which establishment is the aim. For ABC natural enemies one then needs to demonstrate that they cannot establish (step 3). If they cannot establish, only one more step of the procedure (step 6) needs to be followed. However, if they can establish, the environmental risk index (ERI = Likelihood × Magnitude) should be calculated for establishment, and if the risk threshold is exceeded, the natural enemy should not be released (details are given in Reference 110). Problematic natural enemies are thus eliminated early in the evaluation process. However, if the applicant desires, data can be provided from studies on host range (step 4), dispersal (step 5), and direct and indirect nontarget effects (step 6) to enable a reconsideration of the decision not to release the species. If the risk threshold is not exceeded, the same procedure needs to be followed as for CBC natural enemies from step 4. At step 4, the host range issue is addressed. If the ABC or CBC agent is either monophagous or oligophagous/polyphagous and attacks only related and nonval- ued nontargets, it should be considered for release. On the other hand, if the agent is oligophagous/polyphagous and does attack related and unrelated nontargets and/or valued nontargets, the agent should not be considered for release. However, if the applicant desires, data can be provided from studies on dispersal (step 5) and direct and indirect nontarget effects (step 6) to allow reconsideration of the decision not to release the species. In this case, the process continues with step 5. At step 5, questions about dispersal of ABC and CBC agents are addressed. If dispersal is local and mainly in the area of release and numbers that disperse out of the target area are very low, the assessment should move to step 6. If dispersal outside the target area is likely and extensive, and if the environmental risk index exceeds by Wageningen UR on 06/07/07. For personal use only. the risk threshold, the agent should not be released. At step 6, issues related to direct and indirect nontarget effects are considered. If direct and indirect effects inside the dispersal area are unlikely and at most transient and limited, the agent can be released. However, if direct and indirect effects inside the dispersal area

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org are likely and permanent, the agent should not be released. To calculate risk levels for establishment, dispersal, and direct and indirect nontarget effects, the earlier published criteria are applied (108), but weighting factors are added (110). This stepwise risk assessment has been applied to natural enemies that are used in Europe (37), with the assumption that they were evaluated for release in The Netherlands. The exercise, which is fully reported elsewhere (110), led to the following conclusions: (a) All native species that were evaluated are considered safe for release. (b) Exotic species intended for use in ABC that are likely to establish and exceed the risk threshold are not recommended for release and are detected early in the evaluation process without the need to study host range, dispersal, and direct and indirect nontarget effects. (c) Exotic species that are monophagous, or oligophagous/polyphagous and attack nontargets related to the target, but do 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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not attack any valued nontargets, are also detected early in the evaluation without the need to study dispersal and direct and indirect nontarget effects; these can be recommended for release. (d) Exotic species that are oligophagous/polyphagous and attack related and unrelated nontargets and/or valued nontargets are excluded from release without the need to study dispersal and direct and indirect nontarget effects. Some exotic biological control agents that have been released in Europe (e.g., Harmonia axyridis, Hippodamia convergens, and Orius insidiosus) had a high ecological risk index in the first quantitative assessment (108). When we re-evaluated these exotic agents with the new stepwise approach, they were considered unsuitable for release at steps 3 and 4. On the other hand, a species such as Trichogramma brassicae, also with a high risk index in the first quantitative assessment, was not eliminated early in the new procedure and could be recommended for release. The early elimination of obviously risky species, but the acceptance of other species that scored, erroneously, a high index in the first quantitative assessment, shows the improvements of the stepwise assessment (110).

AQUICK SCAN FOR ENVIRONMENTAL RISK ASSESSMENT OF NATURAL ENEMIES AL- READY IN USE More than 150 species of natural enemies are used in ABC (1, 2, 25, 37, 107). These species are proposed to be exempted from a comprehensive ERA but to be evaluated with a quick scan on the basis of available information only. The results of a quick scan could help to establish lists of species (white lists) for use in certain speciﬁed regions of the world. This would result in greatly reduced costs for regulation of these agents that are in use, and the continuation of current biological control programs. A quick-scan method applied to 150 species of natural enemies commercially available in Northwest Europe showed that 5% of these species were considered too risky for further release, and release of 80% of species could be continued (110). For the remaining 15%, information was insufﬁcient to complete a quick-scan by Wageningen UR on 06/07/07. For personal use only. assessment, but provision of limited extra information for most species resulted in advice to continue release. All species considered too risky for release were exotic. Of the species considered safe for use, 55% were exotic and 45% were native. Problematic species

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org (polyphagous predators and parasitoids) could be categorized more clearly by host range than by taxonomy.

FUTURE OF RISK ASSESSMENT

The most important risks from biological control introductions are threats to the environment, including global extinction of species. Biological control introductions of arthropods have been remarkably safe. Exotic natural enemies seem to have rarely caused permanent and strong population declines in nontarget organisms. Risks of nontarget effects caused by exotic natural enemies are of recent but growing concern. Soon, the revised International Standard for Phytosanitary Measures 27 Oct 2005 14:14 AR ANRV263-EN51-25.tex XMLPublishSM(2004/02/24) P1: KUV

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No. 3 will become the standard for all biological control introductions (62). Guide- lines to prepare dossiers (13, 85) and methods for risk assessment are now available (12, 108 110). We expect that these guidelines and methods will rapidly evolve within the next ﬁve years. Ecological factors determining the environmental impact of an exotic agent are increasingly included in current evaluations. Host range data are now used to reject or accept introductions (109), and determination of the potential establishment of exotics based on their thermal biology could provide a relatively simple methodology of determining whether exotics can establish in the target area (18). Methods for assessment of dispersal and of direct and indirect effects on nontargets have not been used to a great extent in arthropod biological control but are currently being developed (12, 80). Regulation of exotic natural enemies is a subject keenly debated by the biological control industry, scientists, and regulators (16, 108). Industry fears lengthy, cumbersome procedures leading to high costs and thus, in some cases, the inability to market a safe natural enemy. On the other hand, regulators within ministries of environment and agriculture have a responsibility to prevent unnecessary and risky releases of exotic organisms. When ecological data are used in quantitative, stepwise risk assessment procedures (110), decisions whether to release can be taken in a tiered system approach and lengthy procedures can be avoided. To allow continued use of safe biological control agents, a quick-scan method can be applied to agents already in use. Such scans may result in white lists of supposedly safe species for speciﬁed (eco)regions. Availability of such lists might stimulate the wider application of biological control. The present activities concerning ERA will hopefully result in a light and harmonized regulation procedure that is not prohibitive to the biological control industry and in the selection of safe natural enemies.

ACKNOWLEDGMENTS by Wageningen UR on 06/07/07. For personal use only. We thank the following persons for contributions to this review: Ferdinando Bin, Matthew Cock, Eric Conti, David Gillespie, Thomas Hoffmeister, Peter Mason, Don Sands, and the participants of the 2004 Engelberg Environmental Impact Meeting. The Entomology Section of the University of Perugia, Italy, is thanked Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org for providing the perfect atmosphere for writing this review.

The Annual Review of Entomology is online at http://ento.annualreviews.org

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Annual Review of Entomology Volume 51, 2006

CONTENTS

SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS, Qi Wu and Mark R. Brown 1 PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS:BIOLOGICAL SIGNIFICANCE, David Stanley 25 BOTANICAL INSECTICIDES,DETERRENTS, AND REPELLENTS IN MODERN AGRICULTURE AND AN INCREASINGLY REGULATED WORLD, Murray B. Isman 45 INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67 INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintraub and LeAnn Beanland 91 INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, Anupama Dahanukar, and John R. Carlson 113 INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzer and Hugh V. Danks 137 PLANT CHEMISTRY AND NATURAL ENEMY FITNESS:EFFECTS ON HERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163 APPARENT COMPETITION,QUANTITATIVE FOOD WEBS, AND THE STRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES, F. J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187 by Wageningen UR on 06/07/07. For personal use only. STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN, Susan E. Fahrbach 209 EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233 DOPA DECARBOXYLASE:AMODEL GENE-ENZYME SYSTEM FOR STUDYING DEVELOPMENT,BEHAVIOR, AND SYSTEMATICS, Ross B. Hodgetts and Sandra L. O’Keefe 259 CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PEST MANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285 HOST PLANT SELECTION BY APHIDS:BEHAVIORAL,EVOLUTIONARY, AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh, and Jim Hardie 309

vii P1: JRX November 2, 2005 13:47 Annual Reviews AR263-FM

viii CONTENTS

BIZARRE INTERACTIONS AND ENDGAMES:ENTOMOPATHOGENIC FUNGI AND THEIR ARTHROPOD HOSTS, H.E. Roy, D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331 CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follett and Lisa G. Neven 359 THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIE ARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387 MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413 CANNIBALISM,FOOD LIMITATION,INTRASPECIFIC COMPETITION, AND THE REGULATION OF SPIDER POPULATIONS, David H. Wise 441 BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICA AND THE CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC AND CLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467 DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING:A COMPARATIVE ANALYSIS OF RECENT APPROACHES, Nuria« Bonada, Narc«õs Prat, Vincent H. Resh, and Bernhard Statzner 495 TACHINIDAE:EVOLUTION,BEHAVIOR, AND ECOLOGY, John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525 TICK PHEROMONES AND THEIR USE IN TICK CONTROL, Daniel E. Sonenshine 557 CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks, Kevin R. Foster, and Tom Wenseleers 581 ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL AGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler, H.M.T. Hokkanen, and A.J.M. Loomans 609 DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635 by Wageningen UR on 06/07/07. For personal use only. PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC MICROORGANISMS AND HERBIVOROUS ARTHROPODS, Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org INDEXES Subject Index 691 Cumulative Index of Contributing Authors, Volumes 42Ð51 717 Cumulative Index of Chapter Titles, Volumes 42Ð51 722

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