Exotic biological control agents: A solution or contribution to arthropod invasions?

Biological control is a valuable and effective strategy for controlling arthropod pests and has been used extensively against invasive arthropods. As one approach for control of invasives, exotic natural enemies  from the native range of a pest are introduced to areas where control is needed. Classical biological control began to be used in the late 1800s and its use increased until, beginning in 1983, scientists began raising significant concerns and questions about nontarget and indirect effects that can be caused by these introductions. In recent years, similar issues have been raised about augmentative use of exotic natural enemies. Subsequently, international guidelines, national regulations and scientific methods being used for exotic natural enemies in biological control have changed to require appropriate specificity testing, risk assessment and regulatory oversight before exotic natural enemies can be released. National and international standards aimed at minimizing risk have increased awareness and promoted more careful consideration of the costs and benefits associated with biological control. The barriers to the implementation of classical and augmentative biological control with exotic natural enemies now are sometimes difficult and, as a consequence, the numbers of classical biological control programs and releases have decreased significantly. Based in part on this new, more careful approach, classical biological control programs more recently undertaken are increasingly aimed at controlling especially damaging invasive arthropod pests that otherwise cannot be controlled. We examine evidence for these revised procedures and regulations aimed at increasing success and minimizing risk. We also discuss limitations linked to the apparent paucity of post-introduction monitoring and inherent unpredictability of indirect effects.     

外来入侵杂草传统生物防治的生态风险及其防范对策

长期大量实践说明,引进天敌防治外来入侵杂草的传统生物防治方法是治理外来入侵杂草的一条切实可行的有效途径,但对其潜在的生态风险——对本土生物的直接或间接不良影响不容忽视。利用传统评价方法预测候选天敌的生态风险存在缺陷,主要表现在：（1）寄主专一性测定过分依赖室内进行的生理寄主范围测定结果,对生态寄主范围（实际寄主范围）问题重视不够,后者指在新环境中的一系列物理和生物条件下的寄主利用预测;（2）在生理寄主范围测定中,过分依赖完成生长发育的可能性,对行为、遗传性状以及系统发育关系重视不够;（3）在风险评估中,过多强调对经济作物的风险,而对自然生态系统的风险重视不够。对此,建议：（1）鼓励对已释放的天敌进行回顾性跟踪研究,从而为杂草生物防治实践提供生态学理论支撑;（2）在运用生物防治手段对付外来入侵杂草实践中,建议采用“有害推论”的预防性原则,以避免在面临入侵生物重大威胁时草率做出释放天敌的决策;（3）在评估候选天敌风险中重视生态效应的风险评估。     

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.     

Assessment of ecological risks in weed biocontrol: Input from retrospective ecological analyses

Prediction of the outcomes of natural enemy introductions remains the most fundamental challenge in biological control. Quantitative retrospective analyses of ongoing biocontrol projects provide a systematic strategy to evaluate and further develop ecological risk assessment. In this review, we highlight a crucial assumption underlying a continued reliance on the host specificity paradigm as a quantitative prediction of ecological risk, summarize the status of our retrospective analyses of nontarget effects of two weevils used against exotic thistles in North America, and discuss our prospective assessment of risk to a federally listed, threatened species (Cirsium pitcheri) based on those studies. Our analyses quantify the fact that host range and preference from host specificity tests are not sufficient to predict ecological impact if the introduced natural enemy is not strictly monophagous. The implicit assumption when such use is made of the host specificity data in risk assessment is that population impacts are proportional to relative preference and performance, the key components of host specificity. However, in concert with shifting awareness in the field, our studies demonstrate that the environment influences and can alter host use and population growth, leading to higher than expected direct impacts on the less preferred native host species at several spatial scales. Further, we have found that straightforward, easily anticipated indirect effects, on intraguild foragers as well as on the less preferred native host plant species, can be both widespread and significant. We conclude that intensive retrospective ecological studies provide some guidance for the quantitative prospective studies needed to assess candidate biological control agent dynamics and impacts and, so, contribute to improved rigor in the evaluation of total ecological risk to native species.     

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。     

Risks of biological control for conservation purposes

Striking successes in classical biological control in agriculture and rangelands engender great interest in using this technology for wildlands conservation and environmental purposes. However, well known unintended consequences of several biological control projects have led to concern that possible environmental benefits do not warrant inherent risks. Four risks demand attention: (1) direct attack on non-targets; (2) indirect effects on non-targets; (3) dispersal of a biocontrol agent to a new area, either autonomously or with deliberate or inadvertent human assistance; (4) changed relationships between a control agent and a native species, particularly as generated by global climate change. Procedures for assessing risk of direct attack on non-targets by phytophagous biological control agents have steadily improved and an expanded centrifugal phylogenetic approach appears to provide adequate insight. Direct non-target impacts by entomophages are more difficult to predict. Myriad possible indirect effects, some subtle but nonetheless important, present a far greater challenge, and techniques of assessing such risks are in their earliest infancy and not as closely regulated. Despite prominent examples in both the general invasion literature and that for biological control, the risk that a species, once introduced, will spread beyond its intended range, and the consequences of such spread, are not routinely treated by risk assessors. This phenomenon deserves far more attention. Global changes—especially climate change—can lead to modified ranges and efficacies of introduced biological control agents and their targets. Although many examples show that climatic niches are often not conserved, an important first routine step would be to combine climatic envelopes with general circulation models for predicted future climates. Finally, actions based on a risk assessment are always implemented in a framework of predicted costs and benefits, which are inevitably asymmetric, so it is critically important that all stakeholders, including conservationists, participate in the decision-making process.     

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.     

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.     

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.     

Assessment of ecological risks in weed biocontrol: Input from retrospective ecological analyses

Prediction of the outcomes of natural enemy introductions remains the most fundamental challenge in biological control. Quantitative retrospective analyses of ongoing biocontrol projects provide a systematic strategy to evaluate and further develop ecological risk assessment. In this review, we highlight a crucial assumption underlying a continued reliance on the host specificity paradigm as a quantitative prediction of ecological risk, summarize the status of our retrospective analyses of nontarget effects of two weevils used against exotic thistles in North America, and discuss our prospective assessment of risk to a federally listed, threatened species (Cirsium pitcheri) based on those studies. Our analyses quantify the fact that host range and preference from host specificity tests are not sufficient to predict ecological impact if the introduced natural enemy is not strictly monophagous. The implicit assumption when such use is made of the host specificity data in risk assessment is that population impacts are proportional to relative preference and performance, the key components of host specificity. However, in concert with shifting awareness in the field, our studies demonstrate that the environment influences and can alter host use and population growth, leading to higher than expected direct impacts on the less preferred native host species at several spatial scales. Further, we have found that straightforward, easily anticipated indirect effects, on intraguild foragers as well as on the less preferred native host plant species, can be both widespread and significant. We conclude that intensive retrospective ecological studies provide some guidance for the quantitative prospective studies needed to assess candidate biological control agent dynamics and impacts and, so, contribute to improved rigor in the evaluation of total ecological risk to native species.     

Can natural enemies of current insect pests provide biotic resistance to future pests?

1. Economic pests jeopardize agricultural production worldwide. Classical biological control, comprising the import of exotic natural enemies to control target pest populations, has a successful history in many countries. However, little is known about how these natural enemies contribute to the suppression of pests that are yet to arrive. Biotic resistance theory, though, posits that communities resist species invasions as a result of natural enemies.
2. We assessed the potential of the resident exotic parasitoid wasp fauna in New Zealand (intentionally‐introduced biological control agents and unintentionally‐introduced species) to provide biotic resistance against possible future pests. A dataset was generated containing resident exotic parasitoid species (Ichneumonoidea: Braconidae; Ichneumonidae) in New Zealand, as well as their known global host ranges and the pest status of host species, to infer the potential for biotic resistance.
3. The known exotic ichneumonoid fauna in New Zealand comprises 65 species. These species associate with 107 host species in New Zealand, of which 54 species are pests. However, the current exotic species could potentially suppress 442 pest species not yet occurring in New Zealand.
4. This approach could be used to inform pest management programmes worldwide. Future research should consider how biotic resistance from the established parasitoid fauna can be used to inform specific decisions with respect to classical biological control.

     

生物防治利用生物多样性保护生物多样性

本文论述了生物防治与保护生物多样性的关系,提出生物多样性是生防作用物的必要来源,生物防治是保护生物多样性的重要措施。文中分析了自然界和农田生态系统中天敌的多样性和寄主专一性,并从外来种的治理、濒危物种和栖境的保护等几个方面探讨了生物防治对于保护生物多样性的作用。作者还强调应加强国际间天敌资源的交换,建立严格的天敌引种释放法规,以便开展更多的安全有效的生物防治项目。     

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.     

Selection of biological control agents for bridal creeper: a retrospective review

Abstract  We reviewed in retrospect the selection process of agents for the biological control of bridal creeper ( Asparagus asparagoides ) in Australia. Selection of agents was facilitated by first investing resources, mostly in South Africa, to clarify identification of the target weed, locate most suitable areas to search for natural enemies, make preliminary observations on phenology, host range and impact of natural enemies and experimentally demonstrate indirect impact of a foliage feeder on below-ground biomass of bridal creeper. Although only limited climate modelling was performed to predict abundance of prioritised agents in Australia, their widespread distribution in South Africa was a good indication that they were likely to establish. No attempts were made to predict possible levels of parasitism that could be encountered in Australia and no formal assessment was undertaken to decide in what order prioritised agents should be released. Three of the four agents prioritised have now been released in Australia. The rust fungus Puccinia myrsiphylli (Thüm.) G. Winter and leafhopper Zygina sp. have widely established and have already demonstrated their capacity to reduce significantly density of bridal creeper populations. It is still too early to determine the contribution that the third agent released, the Crioceris sp. leaf beetle, will make to the program.     

The colonization of native phytophagous insects in North America by exotic parasitoids

Classical biological control could have a major environmental cost if introduced natural enemies colonize and disrupt native systems. Although quantifying these impacts is difficult for systems already colonized by natural enemies, the a priori condition for such impacts can be evaluated based on the extent to which exotics have acquired native hosts. We use native host records for exotic parasitoids introduced into North America for biological control to document the number of exotic species that have been recorded from at least one native insect species. We also evaluate the ability of six biological and ecological variables to predict whether or not a parasitoid will move onto natives. Sixteen percent of 313 parasitoid species introduced against holometabolous pests are known from natives. Further, the likelihood that a parasitoid had colonized native hosts was largely unpredictable with respect to the independent variables. We conclude that given the quality of the data available either now or in the foreseeable future, coupled with inherent stochasticity in host shifts by parasitoids, there are no rules of thumb to assist biological control workers in evaluating if an introduced parasitoid will colonize native insect communities. Received: 2 July 1997 / Accepted: 3 August 1997     

Are exotic natural enemies an effective way of controlling invasive plants?

Classical biological control (the introduction of exotic natural enemies) is often advocated as a tool for managing invasive species. Here, we review the effectiveness of biocontrol and explore the factors that determine whether it is an appropriate response to the invasive species problem. Although there have been some successes, biocontrol is generally poorly evaluated and, in many cases, its impact is unknown. In particular, there is limited understanding of the nature of the invasive species problem and no clear targets against which 'success' can be gauged. In addition, exotic natural enemies could act as invasive species in their own right. To improve the role of biocontrol in invasive species management, we need a better ecological understanding of the impacts of both the biocontrol agents and the target invasive species.     

Apparent competition can compromise the safety of highly specific biocontrol agents

Despite current concern about the safety of biological control of weeds, assessing the indirect impacts of introduced agents is not common practice. Using 17 replicate food webs, we demonstrate that the use of a highly host-plant specific weed biocontrol agent, recently introduced into Australia, is associated with declines of local insect communities. The agent shares natural enemies (predators and parasitoids) with seed herbivore species from native plants, so apparent competition is the most likely cause for these losses. Both species richness and abundance in insect communities (seed herbivores and their parasitoids) were negatively correlated with the abundance of the biocontrol agent. Local losses of up to 11 species (dipteran seed herbivores and parasitoids) took place as the biocontrol agent abundance increased. Ineffective biocontrol agents that remain highly abundant in the community are most likely to have persistent, indirect negative effects. Our findings suggest that more investment is required in pre-release studies on the effectiveness of biocontrol agents, as well as in post-release studies assessing indirect impacts, to avoid or minimize the release of potentially damaging species.     

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.     

Prospective Biological Control Agents of Varroa destructor n. sp., an Important Pest of the European Honeybee, Apis mellifera

This paper reviews prospective biological control agents of the varroa mite, Varroa destructor n. sp. (Acari, Mesostigmata). This ectoparasite has caused severe damage to populations of the European honeybee, Apis mellifera , world-wide in recent years. To date, no promising natural enemies of varroa species have been identified on A. mellifera or its original host, Apis cerana . Therefore, biological control will probably require natural enemies from other hosts. The following groups of organisms were reviewed as potential biological control agents: predatory mites, parasitoids and entomopathogens (nematodes, protozoa, viruses, Bacillus thuringiensis , rickettsiae, and fungi). The candidate groups were ranked according to their lethality to Acari, likely ability to operate under the physical conditions of honeybee colonies, ease of targeting, and ease of mass-production. Preferential consideration was given to the natural enemies of Acari that occupy taxonomic groups close to varroa. Entomopathogenic fungi, which kill a wide range of acarine species, were identified as prime candidates for screening against varroa. Bacillus thuringiensi s also requires study, particularly strains producing novel toxins active against non-insect hosts. Entomopathogenic protozoa and nematodes show less potential for varroa control, but nonetheless warrant preliminary investigation. We consider predators, parasitoids, viruses and rickettsiae to have little potential to control varroa. Because the physical conditions within honeybee colonies are similar everywhere, it is very likely that a biological control agent of varroa could be used successfully throughout the world.