Non-target effects of an introduced biological control agent on deer mouse ecology

Release of exotic insects as biological control agents is a common approach to controlling exotic plants. Though controversy has ensued regarding the deleterious direct effects of biological control agents to non-target species, few have examined the indirect effects of a ”well-behaved” biological control agent on native fauna. We studied a grassland in west-central Montana infested with spotted knapweed (Centaurea maculosa) to examine the effects of knapweed invasion and two gall flybiological control agents (Urophora affinis and U. quadrifasciata) on the native deer mouse (Peromyscus maniculatus). Stomach-content analysis revealed that Urophora were the primary food item in Peromyscus diets for most of the year and made up 84–86% of the winter diet. Stomach contents indicated that wild-caught mice consumed on average up to 247 Urophora larvae mouse^–1 day^–1, while feeding trials revealed that deer mice could depredate nearly 5 times as many larvae under laboratory conditions. In feeding trials, deer mice selected knapweed seedheads with greater numbers of galls while avoiding uninfested seedheads. When Urophora larvae were present in knapweed seedheads, deer mice selected microhabitats with moderately high (31–45% cover) and high knapweed infestation (≥46% cover). After Urophora emerged and larvae were unavailable to Peromyscus, mice reversed habitat selection to favor sites dominated by native-prairie with low knapweed infestation (0–15%). Establishment of the biological control agent, Urophora spp., has altered deer mouse diets and habitat selection by effecting changes in foraging strategies. Deer mice and other predators may reduce Urophora populations below a threshold necessary to effectively control spotted knapweed. Received: 04 May 1999 / Accepted: 14 August 1999     

杂草生防作用物对本土生物群落的影响

传统生物防治是治理外来入侵杂草危害切实可行的有效策略和途径,近来对传统生物防治的批评主要集注于,引进的生防作用物攻击威胁本土非靶标生物。引进的生防作用物可能对本土非靶标生物产生直接和间接影响,这类影响通过不同营养级生物之间的取食关系,以及通过同一营养级内生物间的竞争关系,而影响本土非靶标生物群落。列举若干杂草生物防治案例对以上影响方式及其发生途径进行了评述。就防范杂草生防作用物对非靶标生物的负面影响,提出了以下对策:(i)把引进天敌防治外来入侵生物作为最后的有效手段;(ii)适当增加对非靶标生物潜在影响的生态学评估;(iii)选择寄主专一性强而且能有效控制靶标杂草的天敌;(iv)加强对杂草传统生物防治的生态学研究。     

Predictability of pathogen host range in classical biological control of weeds: an update

Before an exotic pathogen can be released as a classical biological control agent the likely positive and negative outcomes of that introduction must be predicted. Host range testing is used to assess potential damage to non-target plants. To-date 28 species of fungi have been released as classical biological control agents against weeds world-wide. These pathogens have been reported infecting only six non-target plant species outdoors and all of these incidents were predicted. Many more non-target plant species developed disease symptoms in glasshouse tests than in the field. Consequently, data from other sources are needed to ensure potential agents are not prematurely rejected. Predictions of pathogen host range to date have been sufficiently accurate to prevent unpleasant surprises. Exotic pathogens are a safe and useful tool for weed control, especially in natural areas rich in valued non-target species.     

Biological Control not on Target

Non-target effects of exotic biological control agents, parasitoids and predators, released worldwide to control insect pests, are becoming more apparent. This paper summarizes previously recorded information on the diet breadth of natural enemies released to control insect pests worldwide. It also summarizes the diet breadth of native parasitic hymenoptera in North America to determine whether the diet breadths of native and exotic parasitoids differ. Of released biocontrol agents, 48% were recorded as generalists (attacking more than one genus of host) and another 29.2% attacked more than one species in a genus. Only 22.5% were recorded as specialists on the target pests. This suggests that many natural enemies released in biocontrol programs against insect pests have broad diets and that non-target effects are likely. Data from native hymenoptera in North America also show that many species attack multiple host genera and species, with an average of 5.8 genera and 7.3 species attacked, indicating broad agreement with data from biological control releases.     

Benefits and risks of exotic biological control agents

The use of exotic (=alien) arthropods in classical and augmentative biological control programs has yielded huge economic and ecological benefits. Exotic species of arthropods have contributed to the suppression of key pests in agriculture and forestry or have aided in restoring natural systems affected by adventive species. However, adverse non-target effects of exotic biological control agents have been observed in a number of projects. Non-target effects range from very small effects, e.g. 2% parasitization on a non-target insect on a local level, to massive effects on a large scale. Until now, no consensus on how to judge the magnitude of non-target effects and whether these effects can be tolerated or are unacceptable has emerged. In this paper, we briefly review both the benefits of biological control as well as the associated risks including to human and animal health, plant health and particularly the environment. We also make an attempt at identifying the major challenges for assessing risks and for balancing benefits and risks. There is general agreement that sound risk assessment procedures should precede the release of exotic invertebrate biological control agents and a recent shift??especially for arthropod biological control??from introductions done without meaningful risk assessment studies to projects conducting thorough host range testing can be observed. However, overly stringent regulations that would preclude promising agents from being developed must be avoided.     

Avoiding conflicts between insect and weed biological control: selection of non-target species to assess host specificity of cabbage seedpod weevil parasitoids

Abstract:  Classical biological control of insect pests and weeds may lead to potential conflicts, where insect pests are closely related to weed biological control agents. Such a conflict may occur in the classical biological control of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) in North America, which belongs to the same subfamily, Ceutorhynchinae, as a number of agents introduced or proposed for introduction against non-indigenous invasive weed species. We propose a step-by-step procedure to select non-target species and thereby to develop a non-target species test list for screening candidate entomophagous biological control agents of a herbivore pest insect in a way that would simultaneously evaluate non-target potential on weed biological control agents and other non-target species. Using these recommendations, we developed a non-target test list for host specificity evaluations in the area of origin (Europe) and the area of introduction (North America) for cabbage seedpod weevil parasitoids. Scientifically based predictions on expected host–parasitoid interactions and ecological information about the ecological host range in the area of origin can help avoid conflicts, while still allowing the introduction of safe and effective agents against both insect pests and weeds.     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Utilization of the Exotic Weed Pluchea odorata (Asteraceae) and Related Plants by the Introduced Biological Control Agent Acinia picturata (Diptera: Tephritidae) in Hawaii

The flower-head feeding fly Acinia picturata (Diptera: Tephritidae) was deliberately introduced from Mexico into Hawaii in 1959 for biological control of the exotic weed Pluchea odorata (Snow) (Asteraceae). Neither field efficacy nor possible non-target effects of the fly have been evaluated in the 40 years since the introduction. We assessed the impact of the fly on both its target host and on seven non-target plant species. The impact on the target weed was limited, with only 5-13% of the developing seeds in P. odorata flowerheads being destroyed by larval feeding. We did not detect any host range expansion of A. picturata onto flowerheads of two exotic or 5 endemic non-target plant species in the family Asteraceae.     

The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach

The safety of biological control is a contentious issue. We suggest that constructing and analyzing food webs may be a valuable addition to standard biological control research techniques, as they offer a means of assessing the post-release safety of control agents. Using preliminary data to demonstrate the value of food webs in biocontrol programs, we quantified the extent to which a key agent has infiltrated natural communities in Australia and, potentially, impacted on non-target species. Using these data, we also demonstrate how food webs can be used to generate testable hypotheses regarding indirect interactions between introduced agents and non-target species. We developed food webs in communities invaded to varying degrees by an exotic weed, bitou bush, Chrysanthemoides monilifera ssp. rotundata, and a key biocontrol agent for this weed in Australia, the tephritid fly, Mesoclanis polana. Three food webs were constructed during springtime showing the interactions between plants, seed-feeding insects and their parasitoids. One food web was constructed in a plot of native Australian vegetation that was free of bitou bush (‘bitou-free’), another in a plot of Australian vegetation surrounded by an invasion of bitou bush (‘bitou-threatened’) and a third from a plot infested with a monoculture of bitou bush (‘bitou-infested’). The bitou-free web contained 36 species, the bitou-threatened plot 9 species and the bitou-infested web contained 6 species. One native Australian herbivore attacked the seeds of bitou bush. M. polana, a seed-feeding fly, was heavily attacked by native parasitoids, these being more abundant than the parasitoids feeding on the native seed feeders. A surprising result is that none of the three species of native parasitoids reared from M. polana were reared from any of the native herbivores. The food webs revealed how a highly host-specific biocontrol agent, such as M. polana has the potential to change community structure by increasing the abundance of native parasitoids. The webs also suggest that indirect interactions between M. polana and native non-target species are possible, these been mediated by shared parasitoids. The experiments necessary to determine the presence of these interactions are outlined.     

History and Future of Introduction of Exotic Arthropod Biological Control Agents in Spain: A Dilemma?

The first documented introduction of an exotic invertebrate biological control agent (IBCA) in Spain occurred in 1908. Sixty-four additional species have been introduced since then. Information, both previously recorded and original data, on the species introduced for pest control is summarized. Most of the introduced IBCAs focused on citrus pests and homopterans clearly predominate among target phytophagous species. Success has been more frequent for IBCAs used in seasonal inoculative strategies (50.0% of cases) than in classical biological control programs (17.1% of cases). Concerns about potential non-target effects of such species are increasing, but post-release evaluation has often been insufficient to draw any conclusions about them. Most of the beneficial species introduced in Spain were parasitoids (n = 53), and the remaining species were predators (n = 12). Only four parasitoids are considered specialized monophagous natural enemies. The mean number of host species parasitized by parasitoids is 15.2, whereas the mean number of prey species attacked by predators is 21.2. Therefore, polyphagy appears to be quite common among the IBCAs that have been introduced in Spain. The rationale guiding many of these introductions in the past would not be acceptable nowadays. Since classical biological control is such a valuable strategy for pest control, straightforward protocols to evaluate exotic candidate species are urgently needed.     

Methods Used to Assess Non-target Effects of Invertebrate Biological Control Agents of Arthropod Pests

The number of concerns regarding potential non-target effects of invertebrate biological control agents of arthropods has risen over the last decade and an increasing number of studies have since dealt with this topic. Despite some recent international initiatives aimed at providing guidance for risk assessment of biological control agents, detailed methods on how tests should be designed and conducted to assess for potential non-target effects still need to be provided. It is believed that this review comes at an ideal time, giving an overview of methods currently applied in the study of non-target effects in biological control of arthropod pests. It provides the first step towards the ultimate goal of devising guidelines for the appropriate methods that should be universally applied for the assessment and minimisation of potential non-target effects. The main topics that are reviewed here include host specificity (including field surveys, selection of non-target test species and testing protocols), post-release studies, competition, overwintering and dispersal. Finally, a number of conclusions that have emerged from this comprehensive compilation of studies are drawn, addressing potential non-target effects in arthropod biological control.     

Habitat Interference by Axis Deer on White-Tailed Deer

Abstract: Many studies of interactions between exotic and native ungulates have not had temporal and spatial controls nor have they considered the types of competitive interactions that would allow coexistence. For exotic axis deer (Axis axis) and native white-tailed deer (Odocoileus virginianus) to coexist one species should be superior at interference competition and the other species should be superior at exploitative competition. We generated and tested predictions, based on body size and diet breadth, about habitat selection by white-tailed deer in the presence and absence of axis deer, dominance relationships, and time at sites provisioned with high quality forage. We conducted our study in treatment (axis and white-tailed deer) and control (white-tailed deer only) areas when both species were present and after axis deer were removed. We conducted vehicle surveys to determine habitat use of both species. At provisioned feeding sites we recorded aggressive behaviors and amount of time species spent at feeding sites alone and together. In the treatment area white-tailed deer selection for wooded habitat increased 2.1 times after axis deer were removed, whereas habitat selection by white-tailed deer was constant in the control area over the same time. At feeding sites axis deer were dominant to white-tailed deer; both species spent a significantly greater amount of time alone than at feeders together, but amount of time that individuals of each species spent at feeders did not differ. Axis deer were superior at interference competition, but white-tailed deer were not superior at exploitative competition; thus, species coexistence is unlikely. Whether white-tailed deer are negatively impacted by axis deer at spatial scales larger than our experiment probably depends on abundance of axis deer at larger spatial scales. Experiments of species interactions with temporal and spatial controls that consider types of competitive interactions increase a manager's understanding of when and how native ungulates may be negatively impacted by exotic ungulates.     

Risk analysis and management decisions for weed biological control agents: Ecological theory and modeling results

Biologically based control methods offer many advantages for the control of invasive plant species; however, these methods are not without risks to native species. Thus, there is a need for more effective and efficient methods of risk analysis for biological control agents. We show how the process of ecological risk assessment established by the United States’ Environmental Protection Agency may be adapted to improve assessment of the risks of proposed biological control agents. We discuss the risks posed by weed biological control agents, and present a simple individual-based model of herbivorous insect movement and oviposition on two species of host plant, a target invasive plant species and a non-target native species, in simulated landscapes. The model shows that risks of non-target impacts may be influenced by the details of the movement behavior of biological control agents in heterogeneous landscapes. The specific details of insect movement that appear to be relevant are readily measured in field trials and the general modeling approach is readily adapted to real landscapes. Current biological control risk assessments typically emphasize effects analysis at the expense of exposure analysis; the modeling approach presented here provides a simple and feasible way to incorporate exposure analyses. We conclude that models such as ours should be given serious consideration as part of a comprehensive strategy of risk assessment for proposed weed biological control agents.     

Risk analysis and management decisions for weed biological control agents: Ecological theory and modeling results

Biologically based control methods offer many advantages for the control of invasive plant species; however, these methods are not without risks to native species. Thus, there is a need for more effective and efficient methods of risk analysis for biological control agents. We show how the process of ecological risk assessment established by the United States’ Environmental Protection Agency may be adapted to improve assessment of the risks of proposed biological control agents. We discuss the risks posed by weed biological control agents, and present a simple individual-based model of herbivorous insect movement and oviposition on two species of host plant, a target invasive plant species and a non-target native species, in simulated landscapes. The model shows that risks of non-target impacts may be influenced by the details of the movement behavior of biological control agents in heterogeneous landscapes. The specific details of insect movement that appear to be relevant are readily measured in field trials and the general modeling approach is readily adapted to real landscapes. Current biological control risk assessments typically emphasize effects analysis at the expense of exposure analysis; the modeling approach presented here provides a simple and feasible way to incorporate exposure analyses. We conclude that models such as ours should be given serious consideration as part of a comprehensive strategy of risk assessment for proposed weed biological control agents.     

Potential Role of Masting by Introduced Bamboos in Deer Mice (Peromyscus maniculatus) Population Irruptions Holds Public Health Consequences

We hypothesized that the ongoing naturalization of frost/shade tolerant Asian bamboos in North America could cause environmental consequences involving introduced bamboos, native rodents and ultimately humans. More specifically, we asked whether the eventual masting by an abundant leptomorphic (“running”) bamboo within Pacific Northwest coniferous forests could produce a temporary surfeit of food capable of driving a population irruption of a common native seed predator, the deer mouse (Peromyscus maniculatus), a hantavirus carrier. Single-choice and cafeteria-style feeding trials were conducted for deer mice with seeds of two bamboo species (Bambusa distegia and Yushania brevipaniculata), wheat, Pinus ponderosa, and native mixed diets compared to rodent laboratory feed. Adult deer mice consumed bamboo seeds as readily as they consumed native seeds. In the cafeteria-style feeding trials, Y. brevipaniculata seeds were consumed at the same rate as native seeds but more frequently than wheat seeds or rodent laboratory feed. Females produced a median litter of 4 pups on a bamboo diet. Given the ability of deer mice to reproduce frequently whenever food is abundant, we employed our feeding trial results in a modified Rosenzweig-MacArthur consumer-resource model to project the population-level response of deer mice to a suddenly available/rapidly depleted supply of bamboo seeds. The simulations predict rodent population irruptions and declines similar to reported cycles involving Asian and South American rodents but unprecedented in deer mice. Following depletion of a mast seed supply, the incidence of Sin Nombre Virus (SNV) transmission to humans could subsequently rise with dispersal of the peridomestic deer mice into nearby human settlements seeking food.     

What makes a successful biocontrol agent? A meta-analysis of biological control agent performance

We qualitatively reviewed the biocontrol literature in two major journals, Biological Control and Environmental Entomology, over the past 10 years by scoring 878 studies into 11 biocontrol-oriented questions. Quantitative meta-analyses were then used on data from 145 studies to examine the effects of different types of biocontrol agents (parasitoids, predators, and pathogens) on several attributes of weed and pest populations. Results for our qualitative review showed that most biocontrol studies were focused on lepidopteran pests, and that parasitoids were the most common biocontrol agents used. Our quantitative review showed that, for weeds, biocontrol agents significantly reduced weed biomass (−82.0%), flower (−98.9%), and seed production (−89.4%). For pests, our quantitative review showed that biocontrol agents significantly reduced pest abundance by 130% compared to control groups, increased parasitism (+139.0%) and increased overall pest mortality (+159.0%) compared to targets not exposed to biocontrol agents. Effects on pest mortality tended to be stronger for parasitoids than predators, although reductions caused in pest abundance were much stronger when predators were used as biocontrol agents. Addition of two or more biocontrol agents increased mortality by 12.97% and decreased pest abundance by 27.17% compared to single releases. Separate sets of meta-analyses demonstrated that the negative impacts of biocontrol on non-target species were much smaller than those for target species, although adverse effects of biocontrol on non-target organisms are based on small sample sizes and should be interpreted with caution. Our results also showed that biocontrol efficacy tended to be higher when agents were generalists than when they were specialists. Large fail–safe numbers found for most of the estimated effects indicate the robustness of the results found for the efficacy of biological control programs.     

Indirect nontarget effects of host-specific biological control agents: Implications for biological control

Classical biological control of weeds currently operates under the assumption that biological control agents are safe (i.e., low risk) if they do not directly attack nontarget species. However, recent studies indicate that even highly host-specific biological control agents can impact nontarget species through indirect effects. This finding has profound implications for biological control. To better understand the causes of these interactions and their implications, we evaluate recent case studies of indirect nontarget effects of biological control agents in the context of theoretical work in community ecology. We find that although particular indirect nontarget effects are extremely difficult to predict, all indirect nontarget effects of host specific biological control agents derive from the nature and strength of the interaction between the biological control agent and the pest. Additionally, recent theoretical work suggests that the degree of impact of a biological control agent on nontarget species is proportional to the agent’s abundance, which will be highest for moderately successful control agents. Therefore, the key to safeguarding against indirect nontarget effects of host-specific biological control agents is to ensure the biological control agents are not only host specific, but also efficacious. Biological control agents that greatly reduce their target species while remaining host-specific will reduce their own populations through density-dependent feedbacks that minimize risks to nontarget species.     

Environmental risk assessment of exotic natural enemies used in inundative biological control

In the past 100 years many exotic naturalenemies have been imported, mass reared andreleased as biological control agents. Negativeenvironmental effects of these releases haverarely been reported. The current popularity ofinundative biological control may, however,result in problems, as an increasing number ofactivities will be executed by persons nottrained in identification, evaluation andrelease of biological control agents.Therefore, a methodology for risk assessmenthas been developed within the EU-financedproject `Evaluating Environmental Risks ofBiological Control Introductions into Europe[ERBIC]' as a basis for regulation of importand release of exotic natural enemies used ininundative forms of biological control (i.e.not in `classical biological control' thoughsome of the same principles and approachesapply). This paper proposes a general frameworkof a risk assessment methodology for biologicalcontrol agents, integrating information on thepotential of an agent to establish, itsabilities to disperse, its host range, and itsdirect and indirect effects on non-targets. Ofthese parameters, estimating indirect effectson non-targets will be most difficult, asmyriads of indirect effects may occur whengeneralist natural enemies are introduced. Theparameter `host range' forms a central elementin the whole risk evaluation process, becauselack of host specificity might lead tounacceptable risk if the agent establishes anddisperses widely, whereas, in contrast, amonophagous biological control agent is notexpected to create serious risk even when itestablishes and disperses well. Drawing onpublished information and expert opinion, theproposed risk assessment methodology is appliedto a number of biological control agentscurrently in use. These illustrative casehistories indicate that the risk assessmentmethodology can discriminate between agents,with some species attaining low `risk indices'and others scoring moderate or high. Riskindices should, however, not be seen asabsolute values, but as indicators to which ajudgement can be connected by biologicalcontrol experts for granting permission torelease or not.     

A retrospective analysis of known and potential risks associated with exotic toadflax-feeding insects

To date, eight exotic toadflax-feeding insect species have been accidentally or intentionally introduced to North America. Reports on their establishment and impact have been recorded for more than 60 years. Environmental risks linked to biological control of toadflax were identified in terms of host resources and undesirable impacts on the target species through the critical review of this record. Data gaps revealed during this retrospective analysis are addressed through suggestions for future research and associated experimental methodologies. Known and potential impacts of toadflax-feeding insects on both invasive toadflax and non-target species are examined. Recent programmatic demands for demonstrated agent efficacy and stringent host selectivity during the prerelease screening process clearly illustrate that classical biological control of invasive toadflax in North America is progressing beyond the so-called lottery approach.     

Is host‐specificity of weed biological control agents likely to evolve rapidly following establishment?

Over 352 herbivore species have now been intentionally introduced into new regions as weed biological control agents. Recent evidence shows that rapid and significant evolution in host-specificity can occur. The risk of non-target use by biological control agents increasing to unacceptable levels through rapid evolution therefore needs to be considered. In addition, weed biological control offers many as yet largely unexploited opportunities for improving our basic understanding of host-specificity and its evolution. We therefore evaluate the evidence that rapid evolution (1) alters the use of existing hosts, and (2) alters the fundamental host-range. Most cited examples of so-called host shifts from weed biological control were not the result of genetic change. There was only limited evidence of genetically altered performance on a non-target host and no evidence of altered fundamental host-range. We conclude, from both theory and the available data, that only altered use of existing hosts (through quantitative genetic changes) needs be considered when evaluating the risk of rapid evolution. Host-specificity testing methodologies can be improved and adapted to better assess the risk of occurrence of post-release evolution.