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.     

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.     

Post-release survey to assess impact and potential host range expansion by Amitus hesperidum and Encarsia perplexa, two parasitoids introduced for the biological control of the citrus blackfly, Aleurocanthus woglumi in Dominica

Four years after the release of two exotic parasitoids, Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae) and Encarsia perplexa Huang and Polaszek (Hymenoptera: Aphelinidae) for the classical biological control of the citrus blackfly (CBF), Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae) in Dominica, a survey was conducted to assess establishment as well as potential nontarget effects especially on Aleyrodidae and other related taxa. CBF populations were low to non-existent in 50 of 51 field sites examined. At the site where CBF was encountered, both E. perplexa and A. hesperidum were present and CBF populations were declining. The two parasitoids were not among the several species collected on nontarget Aleryodidae and Hemiptera. It is concluded that E. perplexa and A. hesperidum have kept CBF populations under effective biological control in Dominica and there is no evidence of any nontarget effects on other Aleyrodidae or their natural enemies. Handling Editor: Dirk Babendreier.     

Impact of Entomopathogenic Nematodes on Non-target Hosts

Biological pest control has been thought to be ecologically safe for many years. More recently, it has been questioned whether entomopathogens and beneficial arthropods or nematodes truly have no impact on non-target species. Only a few studies deal with the action of entomopathogenic nematodes on non-target animals, although a broad spectrum of species has been tested in the laboratory. Entomopathogenic nematodes do not affect vertebrates under natural conditions. Mortality caused by the release of entomopathogenic nematodes among non-target arthropod populations can occur, but will only be temporary, will be spatially restricted and will affect only part of a population. In plots treated with entomopathogenic nematodes, the impact on the non-target fauna proved to be negligible. The possible impact of introduced exotic nematode species is discussed and regulatory measures for the release are proposed.     

Landscape effects of transgenic cotton on non-target ants and beetles

Transgenic crops producing toxins from Bacillus thuringiensis (Bt) can be planted in the same field for many years, and many insects exploiting such crops must disperse to other habitats to persist. Accordingly, effects of transgenic crop farming could accumulate through time and affect insect populations across agricultural landscapes. We monitored the population density of seven ant genera and beetle families and of rare ants and beetles in 84 non-cultivated sites abutting agricultural fields in Central Arizona. We assessed the short-term (during planting year) and long-term (over 5–6 years) landscape effect of farming Cry1Ac cotton on ant and beetle density in non-cultivated sites, in addition to several local and regional variables. Landscape variables (e.g., sequence of crops planted in neighbouring fields, crop diversity, and abundance) were more frequently associated with insect density than local variables (e.g., plant productivity and diversity in non-cultivated sites). In the short-term, use of Bt relative to non-Bt cotton in neighbouring fields was positively associated with density of one ant and two beetle groups in non-cultivated sites. However, acreage of Bt cotton located within 1 km from non-cultivated sites had more negative effects than acreage of non-Bt cotton on density of one ant and one beetle group. In the long-term, the proportion of years that Bt cotton was planted in neighbouring fields was positively associated with ant density but not beetle density. Results suggest that the farming of Bt cotton in neighbouring fields frequently resulted in positive short- and long-term landscape effects on ants and beetles in non-cultivated sites, while Bt cotton planted farther away had less frequent negative short-term impacts.     

After biocontrol: Assessing indirect effects of insect releases

Development of biological control agents for weeds has been motivated by the need to reduce the abundance and distribution of a pest plant where chemical and mechanical control were not cost effective. Primary objectives have been direct reduction in abundance of the target and, secondarily, the increase of desirable species. Recently, wildland weeds have become a focus of biological control projects. Here, desired outcomes include both reduction of the target and indirect effects of increased diversity and abundance of native species and restoration of ecosystem services. However, goals and benefits of biocontrol programs are not always well-articulated and direct and indirect impacts are not easily predicted. We evaluated the extent to which several successful biological control projects for weeds of rangelands and waterways measured indirect impacts on invaded ecosystems. We also examined biocontrol of a wildland pest tree for which the principal objective is restoration of ecosystem services. We found few quantitative assessments of the impacts of pest plant reduction on community composition or ecosystem processes. All examples documented variation in the impacts of agent(s) across the invasive range of the target plant as well as variation in impacts on the invaded ecosystem. However, without appropriate quantitative information, we cannot evaluate site characteristics that may influence vegetation responses. Most successful weed management programs integrated the use of biocontrol agents with other weed management strategies, especially modifications of disturbance and competing vegetation. Discussion and evaluation of responses of nontarget species would improve our understanding of the context-specificity of outcomes.     

Classical biological control: exploiting enemy escape to manage plant invasions

Practitioners of classical biological control of invasive weeds are confronted with a dual expectation: to achieve successful control of plant invaders and to avoid damage to nontarget plants and adverse indirect effects. In this paper we discuss key issues that we consider to be crucial for a safe, efficient, and successful classical biological control project, and that have also caused some recent controversy. These include selection of effective control agents, host specificity of the biological control agents, implications of the genetic population structure of the target populations, and potential impact on native food webs. With regard to improving the success rate of biological control of plant invaders, we first emphasize the importance of a clear a priori definition of success and a more ecosystem-based approach to better document both negative effects of the invasive plant as well as potential positive and negative effects of introducing biological control agents. Secondly, pre-release impact assessment could be improved by better focusing on how to reach high densities of the control agents and by including tolerance to and compensation of herbivory. Thirdly, we advocate a reinforced effort to integrate and combine biological control in combination with existing or potential management options. Finally, we propose various ecological and evolutionary hypotheses in the framework of our topic to document that biological control programmes against plant invaders also offer a great opportunity to gain new insights into basic processes in ecology and evolution.     

Field assessment of host plant specificity and potential effectiveness of a prospective biological control agent, Aceria salsolae, of Russian thistle, Salsola tragus

The eriophyid mite, Aceria salsolae de Lillo and Sobhian, is being evaluated as a prospective classical biological control agent of invasive alien tumbleweeds, including Salsola tragus, S. collina, S. paulsenii and S. australis, in North America. Previous laboratory experiments to determine the host specificity of the mite indicated that it could sometimes persist and multiply on some nontarget plants, including Bassia hyssopifolia and B. scoparia. These are both European plants whose geographic range overlaps that of the mite, but the mite has never been observed on them in the field. A field experiment was conducted in Italy to determine if the mite would infest and damage these plants under natural outdoor conditions. The results indicate that this mite does not attain significant populations on these nontarget plants nor does it significantly damage them. Salsola tragus was heavily infested by A. salsolae, and plant size was negatively correlated to the level of infestation. Although S. kali plants were also infested, their size did not appear to be affected by the mites. The other nontarget plants were not as suitable for the mite in the field as in previous laboratory experiments. We conclude that there would be no significant risk to nontarget plants as a result of using A. salsolae as a biological agent to control Salsola species in North America.     

The effects of Phoma macrostoma on nontarget plant and target weed species

Phoma macrostoma 94-44B was evaluated against 94 plant species in 34 botanical families, of economically important agricultural, horticultural and ornamental species, as well as target and nontarget weeds. Fifty-seven species from 28 families were found to be resistant to P. macrostoma, while 38 species from 12 families, six of which also contained resistant species, were found to be susceptible. Those families comprising both susceptible and resistant species included the Asteraceae, Brassicaceae, Fabaceae, Lamiaceae, Plantaginaceae and Rosaceae with the foremost three containing the largest numbers of susceptible species. P. macrostoma was pathogenic to many dicotyledonous plant species, but nonpathogenic to monocots. Commercial applications for weed management in turfgrass, agriculture, horticulture and forestry seem probable, while domestically management of weeds in lawns, transplanted ornamental and annual flowering species may provide alternative markets.     

Field assessment of the risk posed by Diorhabda elongata, a biocontrol agent for control of saltcedar (Tamarix spp.), to a nontarget plant, Frankenia salina

The biological control program for saltcedar (Tamarix spp.) has led to open releases of a specialist beetle (Chrysomelidae: Diorhabda elongata) in several research locations, but the controversy over potential impacts to native, nontarget plants of the genus Frankenia remains unresolved. To assess the potential for nontarget impacts under field conditions, we installed cultivated Frankenia spp. (primarily two forms of Frankenia salina but also including Frankenia jamesii) at locations in Nevada and Wyoming where D. elongata densities and saltcedar defoliation were expected to be very high, so insects would be near starvation with high probability of attacking nontargets if these were suitable hosts. Subsequent insect abundance was high, and only minor impact (<4% foliar damage) was observed on both forms of F. salina under these ‘worst case’ conditions; there was no impact to F. jamesii. No oviposition nor larval development were observed on any plants, there was no dieback of damaged F. salina stems, and plants continued growing once insect populations subsided. These results under ‘natural’ field conditions contrast with caged host-range tests in which feeding, development and minor oviposition occurred on the nontarget plant. Other ecological factors, such as distance from target plants to natural Frankenia spp. populations, inhospitable conditions for agent survival in such sites, and intrinsic insect behavior that makes colonization and/or genetic adaptation highly unlikely, lead us to conclude that nontarget impacts following program implementation will be insignificant or absent. Host range testing of new agents, while necessary to ensure safety, must put greater attention on assessing the ecological context where agents will be establishing, and on balancing speculated risks against potential benefits of biological control.