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.     

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。     

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.     

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。     

Evaluating risks of biological control introductions: A probabilistic risk-assessment approach

We address the need to develop improved quantitative procedures for estimating potential non-target impacts of biological control agents in this paper, and propose a probabilistic risk-assessment approach. This approach employs risk-assessment procedures commonly used in many disciplines. The procedure described here uses precision trees to estimate risk based on probabilities that biological control agents will demonstrate predictable behavior under specific conditions, based on their ecological characteristics. We use Trichogramma ostriniae, an egg parasitoid deployed augmentatively against Ostrina nubilalis in the US as case study to conceptually demonstrate the proposed procedure. We propose that this new approach has potential for widespread use in quantifying non-target risk of biological control introductions prior to introductions being made.     

Effect of mechanical damage on emission of volatile organic compounds from plant leaves and implications for evaluation of host plant specificity of prospective biological control agents of weeds

Assessment of host plant specificity is a critical step in the evaluation of classical biological control agents of weeds which is necessary for avoiding possible damage to non-target plants. Volatile organic compounds (VOCs) emitted by plants likely play an important role in determining which plants attract and are accepted by a prospective arthropod agent. However, current methods to evaluate host plant specificity usually rely on empirical choice and no-choice behavioural experiments, with little knowledge about what chemical or physical attributes are stimulating the insect. We conducted experiments to measure the quantitative and qualitative effects on emission of VOCs caused by simple mechanical damage to leaves of plants known to differ in suitability and attractiveness to a prospective agent. More VOCs were detected from damaged than from undamaged leaves for all three species tested. Discriminant analysis was able to correctly distinguish the taxonomic identity of all plants based on their VOC profiles; however, the VOCs that discriminated species among undamaged leaves were completely different from those that discriminated among damaged leaves. Thus, damaged and undamaged plants present different VOC profiles to insects, which should be considered when conducting host plant specificity experiments. An unacceptable non-target plant, Centaurea cineraria, emitted all except one of the VOCs that were emitted by its preferred host plant, Centaurea solstitialis, indicating the importance of compounds that are repellant in host plant specificity. Centaurea cyanus emitted fewer VOCs than C. solstitialis, which suggests that it lacked some VOCs important for host plant recognition.     

Beyond Pandora’s Box: quantitatively evaluating non-target effects of parasitoids in classical biological control

A seminal paper by Howarth (Proc Hawaii Entomol Soc 24:239–244, 1983) entitled “Classical biological control: Panacea or Pandora’s Box” ignited a sometimes acrimonious debate over the relative safety of introductions for classical biological control. Extolled for years as environmentally benign, the litany of negative non-target effects profiled by Howarth heightened awareness of this issue. Several factors have muddied this debate including the conflation of frequency of effects with their strength, grouping the effects of disparate biological control agents together, and the lack of quantitative data on either side of the argument. Here, I examine the potential for non-target effects among insect parasitoids, the most common group used for biological control of arthropods. In response to calls for better quantitative studies, I highlight three different techniques, quantitative food webs, life table analysis, and experimental populations, respectively, to quantitatively assess or reassess non-target effects in different systems. I also explore three methodological approaches employed to ascertain the strength of competitive interactions between native and introduced parasitoids, a potential non-target effect that has received little attention in the literature. These types of studies may greatly increase our understanding of the nature of non-target interactions with introduced parasitoids and bring more rigor to a debate often dominated by rhetoric.     

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.     

Do laboratory studies predict parasitoid interaction outcomes in the field?

Studying competitive interactions among natural enemies is important to elucidate the success and non-target impact of candidate biological control agents. Increased regulation of new introductions requires that studies on non-target species be carried out in confined conditions. Hypotheses about potential impacts of biological control agents in the field are based on data from Petri dish or small cage experiments conducted in the laboratory. This study compared the performance of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), parasitoids Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae) and Microplitis plutellae (Muesebeck) (Hymenoptera: Braconidae) in experiments conducted in small cages in the laboratory and in large cages in the field. Results showed no significant differences between laboratory and field outcomes for D. insulare alone and when D. insulare and M. plutellae were combined. For M. plutellae alone, parasitism in the laboratory cages was significantly less than in the field cages. These results demonstrate that laboratory studies may be useful to develop hypotheses on competitive interactions of candidate parasitoid biological control agents.     

Harmonia axyridis: an environmental risk assessment for Northwest Europe

In this paper, we summarize the international situation with respect to environmental risk assessment for biological control agents. Next, we apply a recently designed, comprehensive risk evaluation method consisting of a stepwise procedure to evaluate the environmental risks of Harmonia axyridis in Northwest Europe. This resulted in the very clear conclusion that H. axyridis is a potentially risky species for Northwest Europe, because it is able to establish, it has a very wide host range including species from other insect orders and even beyond the class of Insecta, it may feed on plant materials, it can cover large distances (>50 km per year), it does move into non-target areas, it may attack many non-target species including beneficial insects and insects of conservation concern, its activities have resulted in the reduction of populations of native predators in North America, it is known as a nuisance in North America and recently also in Northwest Europe, and it may develop as a pest of fruit in North America. Considering the H. axyridis case, current knowledge would lead to the conclusion that, although the predator is capable to effectively control several pest species, its risks are manifold and it should, thus, not have been released in Northwest Europe. At the time of the first releases in Nortwest Europe in 1995, the available scientific literature made clear that H. axyridis is a large sized polyphagous predator and has a great reproductive capacity in comparison with other ladybird beetles, and that there was a need to study non-target effects because of its polyphagous behaviour. In retrospect, this information should have been sufficient to reject import and release of this species, but it was apparently ignored by those who considered release of this predator in Northwest Europe. The case of Harmonia releases in Northwest Europe underlines that there is an urgent need for harmonized, world-wide regulation of biological control agents, including an information system on risky natural enemy species.     

The value of simulating herbivory in selecting effective weed biological control agents

Invasive species have a significant economic and ecological cost and biological control can be a powerful tool in their management. Classical biological control practice involves the re-establishment of trophic links between specialist insect and fungal agents to regulate populations of invasive species. However, the permanent nature of biological control agent introductions raises concerns about the unintended consequences of such introductions on non-target organisms, particularly when such agents are ineffective on their target organisms. In this paper, we explore the current debate in the selection of agents for weed classical biological control. We then propose an alternate approach, based on studying plant response to simulated herbivory, that could minimize the chances of release of ineffective agents. Simulating herbivory could yield insights into the vulnerability of plants to certain types of damage. Selection of agents within guilds that are likely to have a significant influence on the plant can improve the chances of achieving biological control sooner and reduce the likelihood of releasing ineffective agents that may have non-target impacts. We propose a method by which simulated herbivory could be integrated into the agent selection process and discuss its strengths and shortcomings. We present case studies of two Neotropical weeds illustrating how this method could be applied.     

The potential for biological control of invasive alien aquatic weeds in Europe: a review

A retrospective analysis shows that invasive, alien, free-floating and emergent aquatic weeds in Europe are good targets for classical biological control, and that genus-specific chrysomelid and curculionid beetles offer the most potential. Ludwigia spp., Azolla filiculoides, Lemna minuta, Crassula helmsii and Hydrocotyle ranunculoides should be prioritised as targets. Fungal pathogens have been under-utilised as classical agents but, whilst they may have some potential against free-floating weeds, they appear to be poor candidates against submerged species, although the suitability of arthropod agents against these difficult targets still merits investigation. The use of indigenous pathogens as inundative agents (mycoherbicides) shows some promise.     

Ecological studies to assess the efficacy of biological control on populations of alligator weed and lippia

Abstract  The risk of non-target effects from biological control agents can be reduced if we can better identify effective agents prior to release. Introducing only those agents with high potential for effective control will reduce the number of agents released and reduce the probability of both direct and indirect non-target impacts. Identifying effective agents requires understanding the roles that resources, disturbances and herbivory play in regulating plant populations under natural field conditions. Here we propose a series of experiments that will contrast the mechanisms of population regulation of two invasive wetland plants, alligator weed ( Alternanthera philoxeroides ) and lippia ( Phyla canescens ), with native congener species, Alternanthera denticulata and Phyla nodiflora . We hypothesise that the native plants will have greater growth rates when nutrients are low and herbivores are present, whereas the introduced plants will exhibit greater growth rates when nutrients are high and herbivores are absent.     

Evolution of biological control agents following introduction to new environments

The introduction of biological control agents (BCAs) creates the potential for adaptive evolution in translocated organisms. BCAs are confronted with new environments that can promote adaptation to exploit novel resources, even within short ecological time frames. In particular, insect BCAs are amenable to rapid evolution due to their short generation times and relatively large population sizes. These factors hypothetically increase the likelihood that, when exposed to novel habitats, environmental selection could cause BCAs to extend their range to non-target host species. Alternatively, insects may simply extend their range as their generalist or polyphagous habits are fully realized. In this review, we consider recent literature that addresses these topics. Adaptations to environmental conditions have been demonstrated in a number of BCAs. Mechanisms of adaptation include founder effects, hybridization, and endosymbiosis. Yet, there is little evidence of adaptive host range expansions among insect and weed biological control agents to non-target species, albeit existing examples are from limited numbers of studies. Important future directions and current developments in the field incorporate next generation sequencing technology that can promote better resolution of population divergence, possible mechanisms involved in adaptation to novel resources, and insect hybridization. Future studies should also include a careful consideration of the influence of microbes on BCA efficacy and environmental adaptation.     

Evaluating risks of biological control introductions: A probabilistic risk-assessment approach

We address the need to develop improved quantitative procedures for estimating potential non-target impacts of biological control agents in this paper, and propose a probabilistic risk-assessment approach. This approach employs risk-assessment procedures commonly used in many disciplines. The procedure described here uses precision trees to estimate risk based on probabilities that biological control agents will demonstrate predictable behavior under specific conditions, based on their ecological characteristics. We use Trichogramma ostriniae, an egg parasitoid deployed augmentatively against Ostrina nubilalis in the US as case study to conceptually demonstrate the proposed procedure. We propose that this new approach has potential for widespread use in quantifying non-target risk of biological control introductions prior to introductions being made.     

Host range tests reveal Paectes longiformis is not a suitable biological control agent for the invasive plant Schinus terebinthifolia

The most critical step during a weed biological control program is determination of a candidate agent’s host range. Despite rigorous protocols and extensive testing, there are still concerns over potential non-target effects following field releases. With the objective to improve risk assessment in biological control, no-choice and choice testing followed by a multiple generation study were conducted on the leaf-defoliator, Paectes longiformis Pogue (Lepidoptera: Euteliidae). This moth is being investigated as a biological control agent of Schinus terebinthifolia Raddi (Sapindales: Anacardiaceae), which is one of the worst invasive plant species in Florida, USA. Results from no-choice testing showed higher larval survival on S. terebinthifolia (48 %) and its close relative Schinus molle L. (47 %), whereas lower survival was obtained on six non-target species (<25 %). When given a choice, P. longiformis females preferred to lay eggs on the target weed, but oviposition also occurred on four non-target species. An improved performance on the native Rhus aromatica Aiton was found when insects were reared exclusively on this non-target species for one or two generations. Results from host range testing suggest that this moth is oligophagous, but has a preference for the target weed. Non-target effects found during multiple generation studies indicate that P. longiformis should not be considered as a biological control agent of S. terebinthifolia.     

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.     

Ecological role of control agent,and not just host‐specificity,determine risks of biological control

Biological control agents used to manage alien vegetation are generally viewed as providing an ecosystem service, owing to reduced ecological and economic costs of invasion following their release. In particular, gall‐formers are popular as biological control agents because they are host‐specific and therefore considered low risk. However, galls can also be considered to be ecological engineers, because they provide nutritional resources for native invertebrates. We tested whether native invertebrates had formed associations with the gall‐forming fungus Uromycladium tepperianum, introduced into South Africa to control the Australian invasive alien tree Acacia saligna, by collecting U. tepperianum galls and monitoring emergence. We found that a number of invertebrates had formed associations with the biological control agent, among which was the important citrus pest, Thaumatotibia leucotreta (false codling moth). We used pheromone‐baited traps to ascertain if this supplementary source of T. leucotreta increased their abundance in orchards close to patches of gall host, but did not find this to be the case. We did find, however, that control measures used by farmers explained T. leucotreta abundances in traps, which may have obscured detection of any effects of a nearby host for the pest. Nevertheless, this study illustrates the first case of a host‐specific classical biological control agent providing resources for an economically significant crop pest. We conclude that although biological control agents are strictly vetted to ensure host‐specificity, introduced biological control agents that become abundant and can act as ecological engineers pose risks when native biota form associations with them, resulting in a number of possible cascading ecosystem effects. In addition, there could be economic consequences when these associated species include agricultural pests. We conclude that not just host specificity, but potential ecological effects of biological control agents, should be considered in their selection.     

What Magnitude Are Observed Non-Target Impacts from Weed Biocontrol?

A systematic review focused by plant on non-target impacts from agents deliberately introduced for the biological control of weeds found significant non-target impacts to be rare. The magnitude of direct impact of 43 biocontrol agents on 140 non-target plants was retrospectively categorized using a risk management framework for ecological impacts of invasive species (minimal, minor, moderate, major, massive). The vast majority of agents introduced for classical biological control of weeds (>99% of 512 agents released) have had no known significant adverse effects on non-target plants thus far; major effects suppressing non-target plant populations could be expected to be detectable. Most direct non-target impacts on plants (91.6%) were categorized as minimal or minor in magnitude with no known adverse long-term impact on non-target plant populations, but a few cacti and thistles are affected at moderate (n = 3), major (n = 7) to massive (n = 1) scale. The largest direct impacts are from two agents (Cactoblastis cactorum on native cacti and Rhinocyllus conicus on native thistles), but these introductions would not be permitted today as more balanced attitudes exist to plant biodiversity, driven by both society and the scientific community. Our analysis shows (as far as is known), weed biological control agents have a biosafety track record of >99% of cases avoiding significant non-target impacts on plant populations. Some impacts could have been overlooked, but this seems unlikely to change the basic distribution of very limited adverse effects. Fewer non-target impacts can be expected in future because of improved science and incorporation of wider values. Failure to use biological control represents a significant opportunity cost from the certainty of ongoing adverse impacts from invasive weeds. It is recommended that a simple five-step scale be used to better communicate the risk of consequences from both action (classical biological control) and no action (ongoing impacts from invasive weeds).