Transgenic Arthropods for Pest Management Programs: Risks and Realities

The ability to genetically engineer arthropods using recombinant DNA meopens new opportunities for improving pest management programs but also creates new responsibilities, including evaluation of the potential risks of releasing transgenic arthropods into the environment. It is now becoming easier to transform diverse species of arthropods by a variety of recombinant DNA methods. Useful genes and genetic regulatory elements are being identified for pest arthropods, but less effort is being expended to identify genes that could improve the efficacy of beneficial arthropods. A transgenic strain of the natural enemy Metaseiulus (= Typhlodromus or Galendromus) occidentalis (Acari: Phytoseiidae) was developed using a method termed maternal microinjection. This transgenic strain was released into an experimental site on the campus of the University of Florida in 1996 after extensive reviews by the University of Florida Biosafety Committee, Florida Department of Agriculture and Consumer Services, United States Department of Agriculture Animal and Plant Health Inspection Service, and the United States Fish and Wildlife Service. The short term releases established a precedent for releasing a transgenic arthropod but, at present, no guidelines are available that would allow transgenic arthropods to be released permanently into the environment. Several scientific, environmental, and policy issues must be resolved before transgenic pests or beneficial arthropods can be deployed in practical pest management programs.     

From researcher to farmer: The use of extension programs to transfer biological control technology in developed countries

Effective use of biological control by the pest manager requires knowledge of the biologies of the pests and natural enemies, and their interactions with their environment and agronomic practices. Manufacturers provide information for products such as microbial pesticides and entomophagous arthropods used in augmentative biological control. However, information about process-oriented methods such as classical (importation) biological control and conservation of natural enemies is not often available to the farmer. Governmental extension programs are one method for providing practical biological control information, but availability in developed countries varies considerably. Examples of transfer of biological control information are provided for New Zealand, Canada, and Australia. In the United States, the Extension Service, a branch of the U.S. Department of Agriculture, provides partial funding and coordination for pest management educational programs conducted at the national, regional, state and local levels. In a twelve-state region of the North Central United States, university extension and research entomologists have developed a coordinated program to educate county extension personnel, farmers, and private consultants about the use of biological controls in pest management. The details of this model program are discussed. The paper concludes with a discussion of the educational constraints that must be overcome to successfully increase the adoption of biological control.     

Fungal and animal associates of Toxicodendron spp. (Anacardiaceae) in North America

Toxicodendron spp. (Anacardiaceae; the poison ivies, oaks, and sumacs) are regarded by some as noxious, tenacious weeds in forests, grasslands, and waste places across the United States, despite playing numerous important ecological roles. Biological control of Toxicodendron spp. is a virtually unexplored option for ecosystem managers. The purpose of this review is twofold: (1) to synthesize and consider what is known about the biological relationships of Toxicodendron spp. from an ecological standpoint; and subsequently (2) to consider these associations from a managerial standpoint. Fungal, arthropodal, mammalian, and avian relationships are detailed, and their potential utility as biological control agents for Toxicodendron spp. are evaluated based on effectiveness, selectivity, practicality, and indirect or side effects. Fungi, and to a lesser extent arthropods, represent the most feasible agents for Toxicodendron spp. biological control.     

Winter mortality of Aceria chondrillae, a biological control agent released to control rush skeletonweed (Chondrilla juncea) in the western United States

Abstract:  Classical biological control of weeds is based on the assumptions that: (1) plant species are in part invasive in their introduced range because of the absence of coevolved specialist herbivore arthropods and plant pathogens; and (2) that these specialist herbivores can regulate host-plant populations. Although the need for quantitative post-release monitoring studies testing these assumptions has been acknowledged repeatedly, the number of assessments is still remarkably small and usually restricted to systems with notable impact of an agent species. However, studying systems where biological control agents cause no observable target weed reductions may be important to identifying factors that limit the population size or impact of biological control agents. Three biological agents were released for the control of the herbaceous perennial rush skeletonweed, Chondrilla juncea in North America between 1975 and 1977. Although all three species are widely established, weed densities are increasing and there is little quantitative information on factors limiting biological control efficacy. We examined the winter biology and survivorship of the rush skeletonweed gall mite Aceria chondrillae at two rush skeletonweed field sites in south-western Idaho over 2 years. Gall mite winter mortality was high (>90%) in both years and for both sites. Gall mites were more abundant on plants that produced rosettes in fall and rush skeletonweed plants growing on southern aspect were 3.4 times more likely to produce rosettes than those growing on northern aspects. Our data suggest that A. chondrillae population densities are limited by its high winter mortality. The gall mites may require fall rosettes to successfully survive the winter, which are commonly absent on north-facing aspects, impairing the efficacy of A. chondrillae to control rush skeletonweed in the intermountain western United States.     

Towards a virtual reality for plant-associated fungi in the United States and Canada

At present knowledge of fungal biodiversity in North America is scattered in diverse sources ranging from well-reviewed, comprehensive databases to unedited databases of reports from the literature, information on file cards, and uncomputerized reference collections. Resources available electronically were used to determine their relative importance in evaluating the plant-associated fungi known from the United States and to a lesser extent Canada. The results demonstrate that the literature provides the greatest information but that reference collections in the US National Fungus Collections contribute between 22–31% additional data. Little overlap exists between fungi isolated as endophytes and those reported in the literature or as reference collections. Eighty to 100% of the plant-associated fungi reported from Canada are accounted for in comprehensive resources for the United States. A comprehensive database of plant-associated fungi in Canada, the United States, and eventually Mexico would serve as a valuable resource for those making plant quarantine decisions.     

The importance of cryptic species and subspecific populations in classic biological control of weeds: a North American perspective

Classical biological control of weeds depends on finding agents that are highly host-specific. This requires not only correctly understanding the identity of the target plant, sometimes to subspecific levels, in order to find suitable agents, but also identifying agents that are sufficiently specific to be safe and effective. Behavioral experiments and molecular genetic tools have revealed that some arthropod species previously thought to be polyphagous really consist of multiple cryptic species, host races or biotypes, some of which are more host-specific than others. Whereas true species are reproductively isolated, individuals from subspecific populations may potentially interbreed with those of other populations if they should encounter them. Furthermore, biotypes may consist of individuals sharing a genotype that is not fixed within a monophyletic group, and thus may not be evolutionarily stable. This raises the question of how such populations should be classified, and how to confirm the identity of live arthropods before releasing them as classical biological control agents. The existence of host races or cryptic species may greatly increase the number of prospective biological control agents available. However, it may also create new challenges for governmental regulation. These issues are discussed using pertinent examples, mainly from North America.     

Current capacity,bottlenecks, and future projections for offsetting habitat loss using Mitigation and Conservation banking in the United States

Habitat banking in its many iterations is an established and popular mechanism to deliver environmental offsets. The United States can look back at over 30 years of banking experience with the underlying framework and policies being consistently updated and improved. Given the increased demand in habitat banking, we provide insights into how bank area capacity is distributed across the United States for four different bank targets (wetlands, streams, multiple ecosystems, species) based on information extracted from the Regulatory In-lieu Fee and Bank Information Tracking System, as well as, estimating future capacities and area reserves through a predictive modeling approach based on data from the past 26 years. Future predictions indicate a decrease in available reserves for banks targeting wetlands or multiple ecosystems, with potential bottlenecks relating to large reserves being limited to the southeast and release schedules not catching up to the current and anticipated demand. Banks targeting species or streams are predicted to meet future demand, with species banks (conservation banks) following a different legislative and operational approach based on the listing of endangered species and pro-active approaches with anticipated future demand. Most current reserves for all four bank types are restricted to very few service areas with around one-third of all bank areas still awaiting release, limiting their availability on a broader scale. Strategic planning networks are necessary to meet future demand on a national scale and to identify areas suitable for banking or likely to experience future environmental or developmental stress.     

Biological control of weeds: an analysis of introductions,rates of establishment and estimates of success,worldwide

The foremost document that comprehensively reports on biological control introductions against weeds—‘Biological control of weeds: a world catalogue of agents and their target weeds’—has been updated and now includes all deliberate releases made through 2012. It includes data on 1555 intentional releases of 468 biological control agent species used against 175 species of target weeds in 48 plant families, in 90 countries. For 55 (31.4%) of the target weed species, only one biocontrol agent was introduced. The largest number of agent species (44) was introduced for the biological control of Lantana camara (Verbenaceae). Three insect orders (Coleoptera, Lepidoptera and Diptera) comprised about 80% of all biocontrol agent species released and releases made. Of the 468 biocontrol agent species introduced, 332 (70.9%) established in at least one instance. Of the 313 species, for which impact could be categorized, 172 (55.0%) caused medium, variable or heavy levels of damage (impacts). Of all releases made through 2012, 982 (63.2%) led to establishment. Forty-two releases were judged too early post-release to categorize impact, leaving 940 releases for which impact analyses were conducted. Similar to agent species, approximately half of the established releases (503 or 53.5%) caused medium, variable or heavy levels of damage on the target weeds, and almost a quarter of releases (225 or 23.9%) caused heavy impact. Across all countries and regions, 65.7% of the weeds targeted for biological control experienced some level of control. These data indicate the value of this practice, on its own, or as a supplement to other methods, in the management of invasive plants.     

Biological control of Parkinsonia aculeata: what are we trying to achieve?

Abstract  The rangeland shrub, Parkinsonia aculeata (parkinsonia), is considered to be a serious pastoral and environmental weed in Australia. Existing biological control agents have been ineffective and native-range surveying is currently being undertaken to find potential new agents. In this paper I develop unambiguous performance criteria to assist in prioritising potential biological control agents, and against which the success of our biological control program can be judged. These include a reduction of patch density (to below 30% cover) and size (<0.1 ha), a reduction in rates of spread and in-fill (by reducing seed production and understorey seed bank densities to <100 viable seeds m⁻²), and the explicit targeting of regions most at risk from parkinsonia impacts. The development of explicit, a priori performance criteria for biological control programs should help biological control develop into a more rigorous and predictive science.     

Using molecular gut content analysis to identify key predators in a classical weed biological control system: a study with Neomusotima conspurcatalis (Lepidoptera: Crambidae)

Predators can severely limit or prevent the establishment of newly introduced biological control agents. Identifying key predators and quantifying their impacts, however, has often proved difficult, especially in cases where the biological control agent has low establishment or detectability. We used molecular gut content analysis to identify predators feeding on Neomusotima conspurcatalis Warren (Lepidoptera: Crambidae), a biological control agent for Lygodium microphyllum (Cavanilles) R Brown (Lygodiaceae), an invasive weed in Florida, USA. We developed DNA primers specific to N. conspurcatalis, and conducted laboratory feeding trials to confirm that agent DNA could be detected in predator guts through PCR amplification. We then released N. conspurcatalis at three L. microphyllum infested sites and one week later conducted field surveys for predators. Our experimental field survey indicated that predatory arthropods were attracted to the immediate locations of N. conspurcatalis releases. A total of 351 predatory arthropods were collected from L. microphyllum infested sites, representing a broad taxonomic range. At least 33% of individuals from all 13 taxa analyzed had fed on N. conspurcatalis. Of the four predator functional groups encountered, spiders were the most numerous, and appeared to be the most important group based on predation rate. Our results can inform the N. conspurcatalis release program, providing guidance on avoiding generating predation hotspots, and facilitating predictions about where and when N. conspurcatalis releases are most likely to result in establishment. Additionally, we highlight the potential of molecular gut content analysis to improve our understanding of the effects of predators on newly introduced classical biological control agents.

     

Assisted existence: an ethnography of being in Ecuador

In Ecuador, reproductive assistance, whether from God, extended family, or medical technologies, is emphasized and desirable in a precarious and unequal world with a minimal social safety net and chronic economic insecurity. Assistance is the very grounds of being. In better‐resourced realities like parts of the United States, assisted reproductive technologies can trouble the biological and social autonomy of individual heterosexual couples. Juxtaposing assisted reproduction in these divergent sites demonstrates that resources can make autonomy easier to establish and assistance between people and things difficult to perceive. Through an insistence on the material specificity of assisted reproduction itself, this ethnographic contrast contributes to anthropological approaches to ontological questions of being. In particular, ethnographic observation of the material realities of reproductive treatments in Ecuador demonstrates that medical care is one means to instantiate race. Private assisted reproduction makes whiter babies and patients in the face of a crumbling public health care infrastructure whose patients are by definition poor and Indian. The framework of assistance might serve then as a means to ethnographically trace the constitution of racial being in better‐resourced nations, as well as allow for a more comprehensive recognition of the interdependence of existence.     

Field Release and Establishment of the Decapitating Fly Pseudacteon curvatus on Red Imported Fire Ants in Florida

Decapitating phorid flies in the genus Pseudacteon are being studied as classical biological control agents of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Pseudacteon curvatus Borgmeier (Diptera: Phoridae) is a small decapitating fly that attacks small fire ant workers. We released a biotype of P. curvatus from Formosa, Argentina, at three sites near Gainesville, FL. Field releases were conducted in the spring and summer of 2003 and monitored monthly. Flies were discovered within 5 weeks at the spring site and then monthly thereafter. By late spring 2004, flies released at this site had expanded 1.6 km both north and south and about 0.8 km westward. Initially, we found no flies from the two summer 2003 releases but we were successful at finding them 8 months after release during spring 2004. This paper documents the first successful release(s) of P. curvatus on red imported fire ants in the United States.     

Applying legal sunshine to the hidden regulation of biological control

This article identifies a serious legal gap in current United States Department of Agriculture (USDA) policy concerning decisions about the review and release of biological pest control agents. Currently, most of the critical documents and the quantitative evidence underlying USDA decisions and policy related to the petition, review, and release of biological pest control agents (biocontrols) for weeds are inaccessible. Current practices do not provide sufficient information for biologists or an informed public to understand or evaluate policy decisions and environmental outcomes. The USDA needs to comply with federal law by making all relevant documents and data available on the internet. Federal law and policy requires that the USDA release all relevant information, and make it readily accessible to all interested parties. Public disclosure of all relevant documents, along with the scientific evidence related to the review and release of biocontrols, is required by the Administrative Procedure Act, the Freedom of Information Act, the Federal Advisory Committee Act, the National Environmental Policy Act of 1970, and the Plant Protection Act of 2000. Disclosure of this information will impose at most a trivial financial and administrative burden on the USDA Animal and Plant Health Inspection Service, or the Division of Plant Protection and Quarantine. The importance of full information and open debate in the pursuit of both scientific knowledge and sound environmental management far outweighs any administrative burden.     

Plant-mediated interactions: Considerations for agent selection in weed biological control programs

Plant-mediated indirect interactions among herbivores (arthropods and pathogens) are common and extensively reported in the ecological literature. However, they are not well-documented with respect to weed biological control. Such interactions between biological control agents can have net positive or negative impacts on total weed suppression depending on the strength of the interaction(s), the relative importance of the agent indirectly impacted, and the combined weed suppression that results. A better understanding of plant-mediated interactions may improve decision-making about which agents to introduce in classical biological control programs for greatest impact on invasive weeds. This paper reviews the subject, including examples from the biological control literature; outlines the need for research on indirect effects of herbivores on other herbivores; discusses how such knowledge may strengthen classical biological control programs for invasive weeds; and provides recommendations for the kind of studies that should be done and how information about plant-mediated interactions could be integrated into agent evaluation protocols, to assist in decision-making about agents for importation and release.     

Constraints to the implementation of biological control in Sri Lanka

Sri Lanka is a tropical island with a rich diversity of arthropods, with many species of indigenous natural enemies of economic pests. However, no extensive island wide surveys have been carried out for natural enemies of major crop ecosystems and only a few of the indigenous natural enemies are reported useful for augmentation biological pest control by massive field releases of laboratory-produced insects. Most successful biological control programs on the island are importation (i.e. classical) biological control programs, where established exotic natural enemies control certain pest populations in valuable crops. There is growing interest in the use of native natural enemies in pest management, thus creating a need for intensive research on the ecology of indigenous natural enemies and development of infrastructure and technology to produce natural enemies for augmentation. This paper examines constraints and opportunities for implementation of biological control in Sri Lanka.     

Applying legal sunshine to the hidden regulation of biological control

This article identifies a serious legal gap in current United States Department of Agriculture (USDA) policy concerning decisions about the review and release of biological pest control agents. Currently, most of the critical documents and the quantitative evidence underlying USDA decisions and policy related to the petition, review, and release of biological pest control agents (biocontrols) for weeds are inaccessible. Current practices do not provide sufficient information for biologists or an informed public to understand or evaluate policy decisions and environmental outcomes. The USDA needs to comply with federal law by making all relevant documents and data available on the internet. Federal law and policy requires that the USDA release all relevant information, and make it readily accessible to all interested parties. Public disclosure of all relevant documents, along with the scientific evidence related to the review and release of biocontrols, is required by the Administrative Procedure Act, the Freedom of Information Act, the Federal Advisory Committee Act, the National Environmental Policy Act of 1970, and the Plant Protection Act of 2000. Disclosure of this information will impose at most a trivial financial and administrative burden on the USDA Animal and Plant Health Inspection Service, or the Division of Plant Protection and Quarantine. The importance of full information and open debate in the pursuit of both scientific knowledge and sound environmental management far outweighs any administrative burden.     

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.     

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

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

Containment of arthropod disease vectors

Effective containment of arthropod vectors of infectious diseases is necessary to prevent transmission of pathogens by released, infected vectors and to prevent vectors that escape from establishing populations that subsequently contribute to increased disease. Although rare, past releases illustrate what can go wrong and justify the need for guidelines that minimize risks. An overview of recommendations for insectary facilities, practices, and equipment is provided, and features of four recently published and increasingly rigorous arthropod containment levels (ACLs 1-4) are summarized. ACL-1 is appropriate for research that constitutes the lowest risk level, including uninfected arthropods or vectors that are infected with micro-organisms that do not cause disease in humans, domestic animals, or wildlife. ACL-2 is appropriate for indigenous and exotic arthropods that represent a moderate risk, including vectors infected or suspected of being infected with biosafety level (BSL)-2 infectious agents and arthropods that have been genetically modified in ways that do not significantly affect their fecundity, survival, host preference, or vector competence. ACL-3 is recommended for arthropods that are or may be infected with BSL-3 infectious agents. ACL-3 places greater emphasis on pathogen containment and more restricted access to the insectary than ACL-2. ACL-4 is intended for arthropods that are infected with the most dangerous BSL-4 infectious agents, which can cause life-threatening illness by aerosol or arthropod bite. Adherence to these guidelines will result in laboratory-based arthropod vector research that minimizes risks and results in important new contributions to applied and basic science.