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.     

Host and habitat preferences of polypore fungi in Micronesian tropical flooded forests

The distribution and ecological impacts of plant-associated fungi is determined in large part by their degree of specificity for particular host species or environmental conditions. Here we evaluate the host and habitat preferences among the Aphyllophorales, a guild of wood-decay basidiomycete fungi usually considered to be host generalists. We determined the patterns of host association in three well-defined, floristically distinct, tropical wetlands — freshwater forested wetlands, saltwater mangrove forests, and peatlands with scattered trees — on the islands of Kosrae and Pohnpei in the Federated States of Micronesia. Of 33 fungal species, 20 were locally rare. Of the 11 species sufficiently common to evaluate habitat specificity, nine showed significant habitat preferences. Of eight species common enough to evaluate within-habitat host specificity, six showed strong host preferences. All except one of the nine habitat-specialized fungi showed either statistically significant host specificity or strong numerical biases toward single host species. Our results suggest that host preferences may be important in shaping the assemblages of wood-decay fungi, and that the effect of environment on the distribution of susceptible plant species, rather on the fungi themselves, may ultimately drive the apparent habitat specificity of many fungi.     

Regional ecological risk assessment for the introduction of Gambusia affinis (western mosquitofish) into Montana watersheds

Qualitative risk assessment methodologies were used to assess the risk of establishment and consequent impacts on native minnows and species of concern (SOC) associated with the intentional or unintentional introduction of the mosquito biological control agent, Gambusia affinis, to various Montana watersheds. Gambusia affinis introductions for mosquito control have been made throughout the world; some introductions have resulted in deleterious effects on native species. We used average January water temperatures, the presence of dams, and the presence of native minnows and SOC to define endpoints for our assessment. Our results suggest that a section of the Missouri River running between Wolf Creek and Landusky had the highest overall risk score, which corresponds to the highest likelihood of establishment and effects on native minnows and SOC. We also demonstrate how rivers with the highest temperatures are not necessarily at the highest risk of having deleterious effects on minnows and SOC; conversely, these rivers were found to be at highest risk of a population of G. affinis establishing.     

Post-dispersal seed mortality of exotic and native species: Effects of fungal pathogens and seed predators

The invasive behaviour of exotic species is assumed to be due to the reduced impact of enemies on their performance, along with other possible mechanisms. I studied whether the seeds of exotics (6 species) are less impacted by seed predators and seed fungal pathogens than the seeds of their related natives (5 species). I also explored whether the co-occurrence of related natives and the time since introduction increased the percentage of lost seeds in exotics. Seeds were either left unprotected during a period of seven months or treated with fungicide, protected by seed predator exclosures or subjected to both treatments. Both treatments improved seed survival rate. Fungicide treatment had more positive effect on seeds of native than of exotic species but the fungicide-by-origin interaction was insignificant. When exotic species only were considered, fungicide had neutral effect on survival of their seeds, irrespective of the co-occurrence of related natives in the vegetation. Time since introduction was shown not to influence the proportion of seeds lost due to fungi or seed predators. Though the results of this study did not support enemy release as a possible mechanism causing the invasiveness of exotic species, it identified fungal pathogens as an enemy group with possibly differential impacts on native and exotic seeds, which thus deserves attention in future studies.     

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。     

Gallerucida bifasciata (Coleoptera: Chrysomelidae), a potential biological control agent for Japanese knotweed (Fallopia japonica)

Host specificity of foreign natural enemies are becoming more and more critical in classical biological control programs, as concerns about potential risk from introduced biocontrol agents have been increasing recently. Understanding the insect's fundamental and ecological host ranges is the first step in determining the potential for introduction of an insect to control invasive plants. Japanese knotweed, Fallopia japonica (Houttuyn) Ronse Decraene (Polygonaceae) is an invasive weed in the United States and Europe. A leaf beetle, Gallerucida bifasciata (Coleoptera: Chrysomelidae) is an important natural enemy attacking this plant in Asia. However, its host range records were ambiguous. This study examined the beetle's host specificity through a set of choice and no-choice tests in the laboratory and field in its native China. Gallerucida bifasciata larvae were able to complete development on seven of 87 plant species in larval development tests, while adults fed and oviposited on 10 plants in no-choice tests. Multiple choice tests showed adults strongly preferred Fallopia japonica, Persicaria perfoliata (L.) H. Gross and Polygonum multiflorum Thunb over all other plants. Open field tests and field surveys further revealed that these three species were in its ecological host range. The results of this study suggest that G. bifasciata is a potential promising agent for control of Japanese knotweed in the United States and Europe, although additional host specificity tests and risk assessment should be completed.     

Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore

The consequences of invasive species on ecosystem processes and ecological interactions remain poorly understood. Predator–prey interactions are fundamental in shaping species evolution and community structure and can be strongly modified by species introductions. To fully understand the ecological effects of invasive species on trophic linkages it is important to characterize novel interactions between native predators and exotic prey and to identify the impacts of invasive species on the performance of native predators. Although seaweed invasions are a growing global concern, our understanding of invasive algae—herbivore interactions is still very limited. We used a series of feeding experiments between a native herbivore and four invasive algae in the Mediterranean Sea to examine the potential of native sea urchins to consume invasive seaweeds and the impacts of invasive seaweed on herbivore performance. We found that three of the four invasive species examined are avoided by native herbivores, and that feeding behaviour in sea urchins is not driven by plant nutritional quality. On the other hand, Caulerpa racemosa is readily consumed by sea urchins, but may escape enemy control by reducing their performance. Recognizing the negative impacts of C. racemosa on herbivore performance has highlighted an enemy escape mechanism that contributes to explaining how this widespread invasive alga, which is preferred and consumed by herbivores, is not eradicated by grazing in the field. Furthermore, given the ecological and economic importance of sea urchins, negative impacts of invasive seaweeds on their performance could have dramatic effects on ecosystem function and services, and should be accounted for in sea urchin population management strategies.     

Increased chemical resistance explains low herbivore colonization of introduced seaweed

The success of introduced species is often attributed to release from co-evolved enemies in the new range and a subsequent decreased allocation to defense (EICA), but these hypotheses have rarely been evaluated for systems with low host-specificity of enemies. Here, we compare herbivore utilization of the brown seaweed, Fucus evanescens, and its coexisting competitors both in its native and new ranges, to test certain predictions derived from these hypotheses in a system dominated by generalist herbivores. While F. evanescens was shown to be a preferred host in its native range, invading populations supported a less diverse herbivore fauna and it was less preferred in laboratory choice experiments with important herbivores, when compared to co-occurring seaweeds. These results are consistent with the enemy release hypothesis, despite the fact that the herbivore communities in both regions were mainly composed of generalist species. However, in contrast to the prediction of EICA, analysis of anti-grazing compounds indicated a higher allocation to defense in introduced compared to native F. evanescens. The results suggest that the invader is subjected to less intense enemy control in the new range, but that this is due to an increased allocation to defense rather than release from specialized herbivores. This indicates that increased resistance to herbivory might be an important strategy for invasion success in systems dominated by generalist herbivores.     

Assessing the ecological impacts of an introduced seastar: the importance of multiple methods

Introduced species are having major impacts in terrestrial, freshwater, and marine ecosystems worldwide. Given that resources for management are limited and that only a small percentage of invaders are likely to cause large ecological change, management priorities should be based on the severity of immediate and anticipated impacts on native assemblages and commercial species. This paper synthesizes work on the current and predicted impacts of an introduced predatory seastar (Asterias amurensis) on soft sediment assemblages, including native species subject to commercial fishing, in the Derwent Estuary and other areas of southeast Tasmania. Due to the absence of baseline data prior to the arrival of the seastar and the presence of other anthropogenic stressors in the estuary, estimating the impact of the seastar is difficult. To help overcome the weaknesses of any single method, our assessment of impact rests on 'weight of evidence' from multiple approaches. Results from experimental manipulations at small scales, detailed observations of feeding, and field surveys over a range of spatial scales in areas with and without the seastar provide strong evidence that predation by the seastar is likely to be responsible for the decline and subsequent rarity of bivalve species that live just below or on the sediment surface in the Derwent Estuary. The data suggest that should seastar densities in other areas on the Tasmanian coast attain the current levels in the Derwent Estuary, there are likely to be large direct effects on native assemblages, particularly on populations of large surface dwelling bivalves, including several commercial species. Given the seastar's ability to exploit a broad range of food resources other than bivalves, and the functional importance of bivalves in native systems, we predict broader direct and indirect effects on native assemblages. We would be unable to reach these same conclusions from a single approach to assessing impacts. The overall picture from the combination of methods at different scales provides more information than the sum of the results of the separate lines of investigation.     

原产地和入侵地紫茎泽兰对泽兰实蝇的选择性、卵巢蛋白质含量与解毒酶活性的影响

[目的] 紫茎泽兰是我国危害严重的恶性入侵杂草。比较专一性天敌泽兰实蝇对该杂草入侵前后植株的适应性,是揭示外来植物入侵后适应性机制的重要科学问题之一。[方法] 比较泽兰实蝇对原产地和入侵地紫茎泽兰植株的寄主选择性,并测定寄生于2类植株的上泽兰实蝇卵巢蛋白质含量及乙酰胆碱酯酶、羧酸酯酶、谷胱甘肽S-转移酶活性。[结果] 泽兰实蝇对原产地和入侵地紫茎泽兰的选择无显著性差异;寄生在紫茎泽兰入侵地植株上的卵巢蛋白质含量较原产地植株上更高。解毒酶活力比较表明,入侵地紫茎泽兰上泽兰实蝇的羧酸酯酶活性低于原产地上的,但谷胱甘肽S-转移酶（雌虫）活性比较则相反,乙酰胆碱酯酶活性比较均无显著性差异。[结论] 紫茎泽兰入侵后,专一性天敌泽兰实蝇的适应性有所下降,丰富了外来植物入侵机制中天敌逃逸假说的内涵。     

Alcidodes sedi (Col.: Curculionidae), a natural enemy of Bryophyllum delagoense (Crassulaceae) in South Africa and a possible candidate agent for the biological control of this weed in Australia

The Madagascan endemic, Bryophyllum delagoense (Crassulaceae), is a major weed in Queensland, Australia. Despite having first been recorded in Australia in the 1940s, it is far more invasive there than on the African mainland where it was introduced more than 170 years ago. This may be due to a number of factors, one of which could be the occurrence of new natural enemy associations in southern Africa. Among the insects of crassulaceous plants that have extended their host ranges, a stem-boring weevil, Alcidodes sedi, was studied to elucidate its status as a natural enemy of B. delagoense in southern Africa and as a candidate biological control agent for introduction to Australia. Laboratory studies indicated that damage inflicted by adult and larval feeding caused significant reductions in stem length and number of leaves. Preliminary host-range trials revealed that A. sedi can complete its development on other species in the Crassulaceae, including most of the introduced Bryophyllum species and some Kalanchoe species native to South Africa. Despite the oligophagous nature of A. sedi and the fact that it can complete its development on a number of ornamental species in the Crassulaceae, it should be considered a potential biological control agent in Australia. All of the native Crassulaceae in Australia are in the genus Crassula, most of which are very small and therefore unlikely to support the development of a large weevil like A. sedi. However, additional host-range trials will have to be undertaken in Australia to determine whether the weevil can be considered safe for release.     

外来红树植物无瓣海桑引种及其生态影响

无瓣海桑是我国首个从国外引进并大面积推广种植的红树植物,生长快,适应性强,已成为华南沿海红树林恢复造林的主要树种。但近年来无瓣海桑引种已引起较大争论,焦点是无瓣海桑是否会对乡土红树植物生长产生不利影响,是否会造成生态入侵,是否应限制推广种植。根据引种以来的研究成果,对无瓣海桑的生态适应性、种植技术、生产力与物质循环、生态影响等四个方面的引种研究进行综述;分析无瓣海桑引种对乡土红树植物生长的影响和生态入侵可能性,对无瓣海桑引种造林提出建议。指出今后无瓣海桑引种的的研究重点为:无瓣海桑引种的生态监测与入侵评估;对滩涂水生生物的影响;与乡土红树植物优化配置的混交种植技术;无瓣海桑的资源化利用。     

Physical and ant-mediated refuges from parasitism: Implications for non-target effects in biological control

A promising natural enemy for release against the Asian soybean aphid, Aphis glycines Matsumura, in North America is the aphidiine braconid wasp Binodoxys communis (Gahan). The aphid Aphis monardae Oestlund, a native of North America’s tall-grass prairies, is a non-target species that may be at risk from releases of B. communis. This paper describes ecological facets of A. monardae populations in their native habitat that could protect them from attack by this exotic biological control agent. In prairie habitats, A. monardae populations aggregate in flower heads of their host plant, Monarda fistulosa L. On this host plant, aphids are also commonly tended by four ant species, and ant-tended colonies are larger than un-attended colonies. Laboratory studies showed that parasitism rates of A. monardae by B. communis are significantly higher on vegetative M. fistulosa than on M. fistulosa flower heads. In addition, attendance of A. monardae by the ant Lasius neoniger Emery significantly decreased parasitism by B. communis. Ants attacked and killed host-seeking adult parasitoids, and preyed upon B. communis mummies. No evidence was found that B. communis reared from A. monardae are less susceptible to attack by ants than parasitoids reared from A. glycines. M. fistulosa flower heads and attendance by L. neoniger may act as refuges for A. monardae against B. communis. Our work describes spatial refuges as ecological filters that separate non-target organisms from exotic natural enemies. Implications for classical biological control of A. glycines are discussed.     

Experimental infections with the tropical monogenean,Gyrodactylus bullatarudis: Potential invader or experimental fluke?

Introduced exotic species have the potential to spread their associated parasites to native species which can be catastrophic if these hosts are immunologically naïve to the novel parasite. The guppy (Poecilia reticulata) has been disseminated worldwide outside of its native habitat and therefore could be an important source of infection to native fish species. Its parasite fauna is dominated by the ectoparasitic monogeneans, Gyrodactylus turnbulli and Gyrodactylus bullatarudis. The current study tested the host specificity of G. bullatarudis by experimentally infecting a range of isolated fish hosts, including temperate species. Surprisingly, the parasite was capable of establishing and reproducing, for several days, on the three-spined stickleback when transferred directly to this host. We also established that G. bullatarudis could be transmitted under aquarium conditions at both 25 °C and 15 °C. At the higher temperature, the parasite was even capable of reproducing on this atypical host. The implications of these findings are discussed in terms of host specificity, host switching and climate change.     

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.     

Causal mechanisms underlying host specificity in bat ectoparasites

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.     

Response of host plants to periodical cicada oviposition damage

Insect oviposition on plants is widespread across many systems, but studies on the response of host plants to oviposition damage are lacking. Although patterns of oviposition vary spatially and temporally, ovipositing insects that exhibit outbreak characteristics may have strong effects on host plants during peak abundance. Periodical cicadas (Magicicada spp.), in particular, may reduce the performance of host plants when they synchronously emerge in massive numbers to mate and oviposit on host plants. Here we provide the first experimental manipulation of host plant use by periodical cicadas to evaluate the impact of cicada oviposition on plant performance across a diversity of host species within an ecologically relevant setting. Using a randomized block design, we established a plantation of three native and three exotic host plant species common to the successional forests in which cicadas occur. During the emergence of Brood X in 2004, we employed a highly effective cicada exclusion treatment by netting half of the host plants within each block. We assessed multiple measures of host plant performance, including overall plant growth and the growth and reproduction of individual branches, across three growing seasons. Despite our thorough assessment of potential host plant responses to oviposition damage, cicada oviposition did not generally inhibit host plant performance. Oviposition densities on unnetted host plants were comparable to levels documented in other studies, reinforcing the ecological relevance of our results, which indicate that cicada oviposition damage did not generally reduce the performance of native or exotic host plants.     

Consequences of exotic host use: impacts on Lepidoptera and a test of the ecological trap hypothesis

Investigating the effects of invasive species on native biodiversity is one of the most pressing challenges in ecology. Our goal in this study was to quantify the effects of invasive plants on butterfly and moth communities. In addition, we sought to elucidate the fitness consequences of non-native hosts on lepidopterans. We conducted a meta-analysis on a total of 76 studies which provided data on larval performance, survival, oviposition preference, abundance, and species richness of Lepidoptera on native and exotic plants. Overwhelmingly, we found that performance and survival were reduced for larvae developing on exotic hosts, relative to native hosts. At the community level, alien plant invasion was associated with a reduction in the overall abundance and richness of lepidopteran communities. We found that lepidopterans did not show strong oviposition preference for native hosts. This result suggests that many invasive plant species may decrease lepidopteran abundance by providing a target for oviposition where larvae have a relatively poor chance of survival. Among studies that tested both survival and preference on exotic hosts, 37.5 % found evidence for novel hosts that could function as ecological traps (the figure was 18 % when considering studies that only assayed larval performance). Thus, although the majority of novel hosts included in our analyses are not likely to act as ecological traps, the potential clearly exists for this effect, and the role of ecological traps should be considered along with other aspects of global change impacting natural communities.     

Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity

The range of hosts a pathogen infects (host specificity) is a key element of disease risk that may be influenced by both shared phylogenetic history and shared ecological attributes of prospective hosts. Phylospecificity indices quantify host specificity in terms of host relatedness, but can fail to capture ecological attributes that increase susceptibility. For instance, similarity in habitat niche may expose phylogenetically unrelated host species to similar pathogen assemblages. Using a recently proposed method that integrates multiple distances, we assess the relative contributions of host phylogenetic and functional distances to pathogen host specificity (functional–phylogenetic host specificity). We apply this index to a data set of avian malaria parasite (Plasmodium and Haemoproteus spp.) infections from Melanesian birds to show that multihost parasites generally use hosts that are closely related, not hosts with similar habitat niches. We also show that host community phylogenetic ß‐diversity (Pßd) predicts parasite Pßd and that individual host species carry phylogenetically clustered Haemoproteus parasite assemblages. Our findings were robust to phylogenetic uncertainty, and suggest that phylogenetic ancestry of both hosts and parasites plays important roles in driving avian malaria host specificity and community assembly. However, restricting host specificity analyses to either recent or historical timescales identified notable exceptions, including a ‘habitat specialist’ parasite that infects a diversity of unrelated host species with similar habitat niches. This work highlights that integrating ecological and phylogenetic distances provides a powerful approach to better understand drivers of pathogen host specificity and community assembly.     

外来养殖鱼类的入侵风险评估及防控对策——以尼罗罗非鱼为例

[目的]筛选合适的指标建立一套外来养殖鱼类的生物入侵风险评估体系,并对外来养殖鱼类的生物入侵防控提出对策建议。[方法]通过文献资料的收集和整理,对外来养殖鱼类中典型入侵物种的入侵过程、影响危害和入侵生物学特性进行分析和归纳,从适应能力、繁殖能力、扩散能力3方面指示其入侵性;从对生物的影响和对环境的影响2方面指示其生态影响;从自然因素和人为因素2方面指示环境可入侵性,以上述3方面为框架进行评估体系构建。[结果]筛选20个指标构建了外来养殖鱼类的生物入侵风险评估体系,并举例说明该评估体系的应用。从法规政策、科学研究、治理技术和公众参与等4个方面针对性地提出外来养殖鱼类生物入侵风险防控对策。[结论]防范和治理入侵生物是一个系统工程。对于外来养殖鱼类的管理,既不能只考虑经济效益而置生态风险于不顾,也不能片面放大外来养殖良种的入侵风险。科学管控的关键在于完善制度建设、加强风险评估、发展防治手段、促进公众参与,使外来鱼类养殖业在严格受控的前提下发挥其经济效益,将其潜在的生态危害效应降到最低。