Assessing Risks of Releasing Exotic

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

Annu. Rev. Entomol. 2006.51:609-634. Downloaded from arjournals.annualreviews.org
and A.J.M. Loomans5

1
Laboratory of Entomology, Wageningen University, 6700 EH, Wageningen,
The Netherlands; email: joop.vanlenteren@wur.nl
by University of Kentucky on 05/28/09. For personal use only.
2
School of Biosciences, University of Birmingham, Birmingham B15 2TT,
United Kingdom; email: j.s.bale@bham.ac.uk
3
Swiss Federal Research Station for Agroecology and Agriculture, Zürich CH 8046,
Switzerland; email: franz.bigler@fal.admin.ch
4
Department of Applied Biology, University of Helsinki, FIN-00014, Finland;
email: hehokkan@mappi.helsinki.fi
5
Section Entomology, Plant Protection Service, 6700 HC Wageningen, The Netherlands;
email: a.j.m.loomans@minlnv.nl
Key Words environmental risk assessment, host range, establishment, dispersal,

nontarget effects
■ Abstract More than 5000 introductions of about 2000 species of exotic arthro-
pod 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 environ-
mental effects caused by releases of exotics are of growing concern. Twenty countries
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
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
0066-4170/06/0107-0609$20.00 609
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610 VAN LENTEREN ET AL.
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-
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 bio-
logical control agents (43). By far the most important risks from biological control
introductions relate to possible changes in the distribution and abundance of na-
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 extinc-
tion of a native species (target or nontarget); large reductions in either the distribu-
tion or abundance of native organisms; interference in the efficacy of native natural
enemies of pests via intraguild interactions or competitive displacement; vector-
ing of pathogens harmful to native organisms; loss of biodiversity and identity of
ASSESSING RISKS OF BIOCONTROL 611
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 non-
target 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 intro-
duced 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 in-
troduced 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
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).
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
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 Reúnion,
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)
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
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.
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 regula-
tions (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 experi-
ence 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 nat-
ural enemies, microorganisms, and other beneficial organisms, and also includes
evaluation of environmental impacts. Several other organizations have recently de-

veloped 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 facili-
tate 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
past two decades for exotic natural enemies, though often in a preliminary way
(108). Methods have generally been derived from existing pest risk analysis pro-
tocols 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
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
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 applica-
tions 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
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 eco-
logical mechanisms involved are identified. Also, guidelines to data requirements
and approaches for their quantification are provided.
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
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 com-
plicated 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
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).
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

Figure 1 Flow chart summarizing host range assessment of arthropod bi-

ological control agents. NT, nontarget. Modified after References 108, 109.
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
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 be-
tween 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 nontar-
gets 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 nec-
essary 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 en-
emies, 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
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).
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, prelimi-
nary studies are normally conducted to assess the similarity of climatic conditions
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 ap-
proach 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 estab-
lishment and subsequent spread of introduced natural enemies. For all arthropods
there is a temperature below which there is no development, i.e., the “develop-
mental 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
vital component in assessing establishment potential. Cold tolerance can be as-
sessed 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 strate-
gies (6, 7) that can be applied to novel biological control agents. For species in
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).
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
understanding of the effects of such factors on establishment.
EXAMPLE OF ASSESSING THE RISK OF ESTABLISHMENT Successful biological con-

trol schemes have been implemented in greenhouses, namely the management of
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 ex-
ample, 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

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
(104), and Typhlodromips montdorensis (52, 53) assessed the effects of tem-
perature 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. montdoren-
sis died out quickly in winter, and survival was largely unaffected by variations
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 establish-
ment 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) or high-
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.
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 abil-
ities 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 (num-
bers 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,
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).
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 po-
tential 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
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 biolog-

ical control agent may affect the abundance of native nontarget species. These
species are not usually the preferred hosts of the agent, and therefore their abun-
dance 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 gen-
erally 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-

PARENT COMPETITION, AND VECTORING When the exotic agent is able to also
attack natural enemies of the target herbivores [intraguild predation (91) or facul-
tative hyperparasitism (101)] it might interfere with the regulation of these herbi-
vores. An example is a study on the trophic and guild interactions of five species
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
a facultative hyperparasitoid, threatening the establishment and survival of other
parasitoid species. Intraguild predators or hyperparasitoids may lead to relaxed pre-
dation (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 (enrich-
ment), increasing these populations, but possibly influencing indirectly popula-
tions 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
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 relation-
ship between a specialist braconid wasp, Cotesia melitaearum, and its generalist
hyperparasitoid, Gelis agilis, was influenced by the introduction of a second bra-
conid 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, to the extent that some of the original
populations went extinct (112).
Sometimes the natural enemy vectors pathogens or hyperparasitoids (14, 44).

For example, insects always carry various eubacteria. Some of these are oppor-
tunistic, whereas others are highly evolved pathogens such as Wolbachia, an intra-
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 popula-

tion, 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 re-
quirements (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-
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).
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 materi-
als used as well as screening and destruction of contaminants after arrival in the
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 non-
target 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
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 indi-
rect effects. The minimum score therefore is 5 (5 × 1 × 1) and the maximum is
125 (5 × 5 × 5).
In a first application of this methodology, 31 cases of natural enemy introduc-
tions 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 sev-
eral 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
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 A new

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).
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.
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.
For exotic 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 de-
sires, 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
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
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 fol-
lowing 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
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 eco-
logical risk index in the first quantitative assessment (108). When we re-evaluated
these exotic agents with the new stepwise approach, they were considered unsuit-
able 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).
A QUICK 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
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 con-
sidered safe for use, 55% were exotic and 45% were native. Problematic species
(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 introduc-
tions 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 grow-
ing concern. Soon, the revised International Standard for Phytosanitary Measures
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 methodol-
ogy 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 biolog-
ical 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 con-
cerning 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
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
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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P1: JRX
November 2, 2005 13:47 Annual Reviews AR263-FM
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
STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN,
Susan E. Fahrbach 209
EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC
HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233
DOPA DECARBOXYLASE: A MODEL 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, Núria Bonada,
Narcı́s 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
PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC
MICROORGANISMS AND HERBIVOROUS ARTHROPODS,
Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663
INDEXES
Subject Index 691
Cumulative Index of Contributing Authors, Volumes 42–51 717
Cumulative Index of Chapter Titles, Volumes 42–51 722
ERRATA
An online log of corrections to Annual Review of Entomology
chapters may be found at http://ento.annualreviews.org/errata.shtml

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Annu. Rev. Entomol. 2006. 51:609–34

ASSESSING RISKS OF RELEASING EXOTIC

J.C. van Lenteren,1 J. Bale,2 F. Bigler,3 H.M.T. Hokkanen,4

and A.J.M. Loomans5

Key Words environmental risk assessment, host range, establishment, dispersal,

SETTING THE SCENE: NONTARGET EFFECTS CAUSED

610 VAN LENTEREN ET AL.

Potential Risks of Releasing Exotic Biological Control Agents

ASSESSING RISKS OF BIOCONTROL 611

Nontarget Effects Caused by Exotic Biological Control Agents

by exotic natural enemies. An overview of these nontarget impacts is given in

outnumber those that have been intentionally introduced practically everywhere,

612 VAN LENTEREN ET AL.

Possible global Bessa remota (Aldrich) Levuana iridescens Fiji, 1925

extinction (41) (Riley) (Butler) 1900s

international biological control experts were contacted for additional information,

ASSESSING RISKS OF BIOCONTROL 613

Evolution of Environmental Risk Assessment

evaluation of environmental impacts. Several other organizations have recently de-

614 VAN LENTEREN ET AL.

for Biological Control of Noxious Animals and Plants—West Palearctic Regional

ECOLOGICAL FACTORS DETERMINING THE

Host Range Assessment

ASSESSING RISKS OF BIOCONTROL 615

the basis of attributes such as nonoverlapping geographical distribution, different

616 VAN LENTEREN ET AL.

Figure 1 Flow chart summarizing host range assessment of arthropod bi-

ASSESSING RISKS OF BIOCONTROL 617

recommendation to release the species can be put forward. In step 3, attack of

combined, in other situations, steps can be bypassed; a detailed discussion of this

618 VAN LENTEREN ET AL.

ASSESSING RISKS OF BIOCONTROL 619

parasitoid relationships and thus the probability of establishment (30). In temperate

EXAMPLE OF ASSESSING THE RISK OF ESTABLISHMENT Successful biological con-

620 VAN LENTEREN ET AL.

Figure 2 Relationship between maximum field survival (days) and LTime50 at 5◦ C

ASSESSING RISKS OF BIOCONTROL 621

is affected by trivial movements, host foraging, or migratory behaviors and can

distance is positively correlated with body size (103). Dispersal by small-bodied

METHODS, MARKERS, AND MODELS Knowledge of the dispersal characteristics of

622 VAN LENTEREN ET AL.

Direct and Indirect Effects of Released Organisms on

EFFECTS ON NONTARGET HERBIVORES Sometimes the established exotic biolog-

EFFECTS ON OTHER TROPHIC LEVELS: INTRAGUILD PREDATION, ENRICHMENT, AP-

ASSESSING RISKS OF BIOCONTROL 623

response (58). On a longer timescale, the natural enemy population is expected to

Sometimes the natural enemy vectors pathogens or hyperparasitoids (14, 44).

of biological control agents (44).

COMPETITION When an introduced agent attacks and reduces a herbivore popula-

RISK ASSESSMENT METHODOLOGY

624 VAN LENTEREN ET AL.

Risk Identification and Evaluation

RISK IDENTIFICATION AND QUANTITATIVE RISK EVALUATION METHOD Normally,

ASSESSING RISKS OF BIOCONTROL 625

numerical values obtained do not allow an unequivocal separation between risk

IMPROVED, COMPREHENSIVE ENVIRONMENTAL RISK EVALUATION METHOD A new