W5185: Biological Control in Pest Management Systems of Plants
(Multistate Research Project)
Status: Active
W5185: Biological Control in Pest Management Systems of Plants
Duration: 10/01/2022 to 09/30/2027
Administrative Advisor(s):
NIFA Reps:
Non-Technical Summary
Statement of Issues and Justification
Biological control is the most effective, sustainable, economical, and environmentally-sound, approach to controlling arthropods pests, mites, and weedy plants. Its applications can conserve the biodiversity of millions of acres of natural land, protect our food supply by reducing pesticide use on crops, and mitigate the impact of urban pests. Biological control has traditionally been defined as the "the action of parasites, predators, and pathogens in maintaining another organism's density at a lower level than would occur in the absence of the natural enemies" (DeBach 1964). Applied biological control is typically separated from natural biological control and further defined by three main approaches: importation, augmentation, and conservation. These approaches are via human intervention, which has prompted new definitions to surface. A recently proposed definition of biological control by two collaborating project members is “biological control is the indirect positive effect of a biological control agent on humans that is mediated by direct or indirect negative effects of that agent on populations of one or more target species (Heimpel and Mills 2017).
This regional project shows that all three areas of applied biological control remain relevant in the western U.S. In the importation approach (referred to as classical biological control), exotic natural enemies are imported and released in a new area where the target pest or weed occurs. Research projects that search for effective natural enemies in the pest’s country of origin include years of collaboration with overseas scientists to find a species safe to release; followed by detailed monitoring and evaluation. Augmentation and conservation involve supplementing (or manipulating) natural enemies already in place or modifying the environment, respectively, to improve the effectiveness of biological control. For a given arthropod pest or weed, a pool of natural enemies often exists which consists of vertebrates, invertebrates, and microorganisms. The fundamental problems of applied biological control are to select an appropriate species or combination of species from this pool that will bring about the desired level of pest suppression, while causing minimal impacts on non-target species.
The landscape of the western U.S. is incredibly heterogeneous, consisting of desert, grassland, shrubland, forest, mountains, and urban habitats. Many of these habitats are under the constant threat of invasive species. This region is also home to the most productive agricultural counties in the country (farm gate) and to over 50% of national organic acreage (USDA NASS 2020). Moreover, biological control is a cornerstone of organic farming, and the production of organic commodities in the U.S. continues to increase. Annual global organic retail sales in 2019 were valued at $117 billion, with the U.S. accounting for 42% ($50 billion) of this market (Willer et al. 2020). In the millions of acres of natural areas and rangeland in the western U.S., biological control is often the only choice to suppress invasive species. Biological control is an increasingly important pest management tactic in extensive low-value per acre areas.
Biological control can result in highly significant benefit:cost ratios. Recently, members of this project synthesized data from biological control programs targeting arthropod pests and discovered that for all studies that included economic data, the mean net present value of a classical biological control program was about $37.3M with an average benefit:cost ratio of 61:1 (Naranjo et al. 2019). They found that conservation biological control options also had significant value, averaging $74/ha. High value fruit orchards under biological control saved producers as much as $22,800/ha. over pesticide programs. Another project member documented a ratio of 50:1 for a mole cricket biological control project (Mhina et al. 2016). While these economic benefits are enormous, the true value of biological control is likely even higher due to external benefits such as reductions in pesticide use and exposure. These reductions lead to improved environmental quality and human health, but have not been consistently considered.
Continued project justification: This regional project involves biological control of arthropod pests and weedy plants. The mission of this project is to facilitate all aspects of applied biological control research and implementation among specialists from the participating institutions and organizations. Because biological control of arthropod pests and weeds is based on many of the same ecological principles, researchers from the two fields benefit greatly from information exchange and research collaboration. The methodologies for controlling arthropod pests and weed plants differ, but the scientific issues (e.g., introduction strategies, genetics of colonization, evaluation of natural enemy impact, etc.) overlap extensively. That some individuals involved in this project conduct research in both arthropod pest and weed systems is further evidence of the conceptual similarities between these two fields.
Stakeholder input justifying this project is based on biological control being of great benefit to agriculture, natural ecosystems, the quality of rural life, and the consumer. In 2018, the USDA, EPA, DOI and DOD reaffirmed their commitments to pesticide reduction with their National Road Map for Integrated Pest Management (USDA 2018). One of the goals of this document is to encourage development of low-risk suppression tactics, including biological control. It states that reductions in insecticide and herbicide applications should enable farmers and ranchers to reduce production costs, adopt sustainable pest management practices, and reduce the evolution of pest resistance to pesticides. A relevant example of a W5185 project in this area is the ongoing program to suppress the Asian citrus psyllid in California using an imported parasitoid from Pakistan. Since the start of a biological control program in 2011, psyllid densities in urban citrus have declined by over 70%. This has helped to keep some of the largest citrus producing areas in California psyllid-free for more than 10 years (Milosavljevic, I. et al, 2021).
Regardless of the many biological control advances in recent years, appreciably more research is needed due to an unrelenting introduction of invasive pest species (weeds and arthropods), the impacts of climate change, and how natural enemies are affected by pesticides. Additionally, there has been an increase in federal regulations for imported agent non-target testing and release. Genetically-engineered crops continue to add to the challenges in developing biological control tactics.
The following brief summaries will give compelling reasons for this regional project to continue. Classical biological control release programs continue to be rigorously regulated at the Federal level with much of the focus on non-target impacts. Proactive biological control programs, searching for indigenous vs. exotic natural enemies and the increased use of molecular techniques have all been added to the non-target protocols used to determine if a natural enemy will be safe and effective after release. Further research into the genetics and ecology of colonization is clearly warranted and ongoing. In the future, classical biological control should ideally be able to predict (1) the appropriate species (or biotype) or combination of species (and/or biotypes) to release for control of a target pest in a given situation; and (2) the environmental impact resulting from the introduction of an exotic enemy. Since 2000, regulations on natural enemy importation and introduction have been enforced by the USDA-APHIS, using guidelines from the North American Plant Protection Organization (NAPPO) that require researchers to provide in-depth studies complete with rigorous data on the non-target effects of biological control agents they wish to release (Mason et al. 2005). Currently, non-target testing and regulations involved in releasing biological control agents for both weed and arthropod pests continue to be important topics discussed routinely by this workgroup. We need to develop additional frameworks that evaluate the risks as well as the benefits of potential biological control importations. When considering benefits, we must think broadly and include not only economic benefits but environmental ones, realizing that these can be multi-faceted. USDA-APHIS-PPQ published their 330 Rule in the past five years, with much input from stakeholders, including W4185. Our project has always enjoyed the attendance and participation by Federal representatives from all the agencies that affect the movement and regulation of natural enemies. Our members receive updates routinely via email on many issues that affect biocontrol and when these proposed new regulations debuted they were dispersed via email and thoroughly explained during our annual meeting as a formal presentation. Many project members have import permits for biological control agents, either existing or pending, and the face to face interaction with USDA-APHIS personnel that this project annually provides has always been invaluable.
Through international migration, transport, and commerce, human activities have accidentally or deliberately moved plants and animals to new regions, and these events have contributed greatly to the introduction of many species around the globe (Mack et al., 2000). Invasive species are not only recognized as one of the main drivers of global change (Sala et al., 2000); they often pose an enormous threat to agricultural lands and thus have high economic costs (Pimentel et al. 2005). Because of their negative consequences, many techniques and strategies have been deployed to control and manage invasive arthropod pests and weedy plants. When these methods are successful, they can result in long-term reduction in the distribution and abundance of such pests and weeds. Unfortunately, these efforts are not always successful, and such species proliferate and cause great ecological and economic harm. The United States Department of the Interior estimated that invasive species was causing $143 million in damage annually to the US (United States Department of the Interior, Invasive Species Strategic Plan. 2021-2025). Biological control is often the only tool available to control invasive species, especially weeds, when affected habitats involve enormous acreage (Hinz et al. 2019). Often these areas are home to critical natural habitats and the goal is to preserve biodiversity. Many collaboratives within this project have continued to work on invasive weeds which impact several states and their overseas cooperators in Europe, who help search for natural enemies, attend the annual meetings to discuss results. But, protecting endangered habitat from invasive species need not involve extensive acreage. A parasitoid released in Hawaii to mitigate damage by the erythrina gall wasp has proved successful in saving the beloved, native wiliwili tree (Kaufman et. al 2020). Every approach possible to alleviate the impact of invasive species must be considered and biological control will continue to play an important role.
We continue to increase our understanding of the ecological mechanisms by which a successful natural enemy operates in nature, and why a particular organism is successful in one situation and not in another. Where success has been achieved in classical biological control, the underlying ecological mechanisms are not always clear. Basic research on augmentation and conservation of natural enemies is also needed. In augmentation, we urgently need a coherent theory of inundative/inoculative release as well as basic efficacy data in order to more readily incorporate commercially available predators and parasitoids of arthropod pests into IPM systems. The genetics of mass production must be evaluated experimentally so that quality control procedures can improve the final product (Gebiola et al. 2019). Advances in the nutrition of parasitoids and predators are needed. Continued commitment to conservation of natural enemies is required, including innovative ways of integrating pesticides and cultural controls with natural enemy species. As IPM programs become more environmentally-friendly, they are using more biopesticides (Bordini et al. 2021) and techniques like Sterile Insect Technique (SIT) or mating disruption chemicals. In the past five years, W4185 scientists have examined interactions between transgenic crops and biological control species, and these studies will increase as more such crops are approved (Fleischer et al. 2021).
Global warming has long been accepted as an official threat to our natural and agroecosystems. Climate change and its impact on biological control, predator-prey and host-parasitoid dynamics could impact all three approaches to biological control. NOAA Administrator Rick Spinrad, Ph.D. said “July is typically the world’s warmest month of the year, but July 2021 outdid itself as the hottest July and month ever recorded. This new record adds to the disturbing and disruptive path that climate change has set for the globe.” (NOAA, August 2021). It will be imperative that scientists watch for the effects of climate change on biological control agents and the arthropod and weed pests that have been kept in check by those agents (Nechols 2021). Recommended actions include conducting surveys for non-target species in areas undergoing climate change, determining tolerances to changes in temperature and precipitation for natural enemies and hosts/prey, incorporating climate data into insect population models, and long-term assessments to document the impact of climate change on non-target species and efficacy of biological control programs. Because climate change will impact both target pests and non-target species, the work will be best-accomplished by grant-funded programs involving interdisciplinary teams of scientists.
Regional, Collaborative Character of Project: Invasive pests continue to arrive in the western U.S., and many of these will become permanently established. The use of classical biological control will remain a high priority. At the same time, our IPM programs must be continuously evaluated, refined, and adjusted in response to changes in newer and more specific control technologies and production practices. The most effective way to address these new pests that become quickly established and spread to other states is through regional collaboration of state and federal scientists. Experiment Stations and non-Land Grant institution members to this project accrue timely and relevant benefits to participation. Regionality is essential to implementing biological control-based solutions to our pest problems for the following reasons: 1) numerous target pests occur in three or more western states or territories; for these pests, the research effort must be coordinated and duplication minimized to effectively utilize very limited resources; 2) regional importation/quarantine facilities are critical for a coordinated response to exotic arthropod pests and weeds. These facilities are finite, there are no plans to expand them in the foreseeable future, and they serve the needs of all states and territories in the region; and 3) interstate exchange of information and exotic species/biotypes is facilitated through a regional approach. Sharing the cost of foreign exploration and quarantine is essential, as is sharing of methodological advances and our knowledge base. Without a regional project in biological control, the western states and territories will not be able to rapidly share current information on controlling new and existing pest species, many of which have ranges over multiple states. Additionally, this group discusses emerging pest threats and forms collaborations and networks that anticipate and plan for pest arrival. Besides state to state (Experiment Station) collaborations, active participants often include scientists from USDA-ARS, USDA-APHIS, USFS, and state departments of agriculture, all of which benefit from rapid information transfer and shared projects.
Advances in the development of sound ecological theory concerning pest population dynamics, predator-prey interactions, the role of invasion genetics, methodologies for the evaluation and release of natural enemies, and new regulatory policies are all fundamental needs in biological control, along with coordination and cooperation of research for a given pest. For example, theoretical and experimental studies of the actual ecological mechanisms that underpin pest population regulation are being addressed in several states and among pest systems. In addition, our members and Federal Advisers, serve on key committees that are steering efforts to minimize non-target effects through policy discussions and recommendations
The value of networking that takes place during the 2 day annual meeting of this project cannot be over-emphasized. Without this multistate project, many arthropod and weed pest species will not be targeted for suppression and will cause damage to both agriculture and to natural U.S. ecosystems. Results produced by the members of this regional project have historically had, and will continue to have, a significant domestic and global impact in the field of biological control.
Related, Current and Previous Work
Related, Current and Previous Work
New invasive pest species continue to arrive in the western U.S., and others have gained in importance, so these have been incorporated into a revised species target list [Appendix A].
Since 2016, twenty one additional arthropod pests have been added to the work list, (minimum of 107 total arthropod pests), and 6 new weeds (minimum of 60 weed species). Because “proactive biocontrol” is now seen as a critical tool, species such as the spotted lanternfly have been added to this list. Five years ago, the emerging threat was the Asian citrus psyllid, which had devastated citrus in Florida and spread to California. These are high profile insects due to their urban invasion ranges, but should not eclipse the importance of others, especially many weeds, that impact critical natural areas.
Previous work (2016-2021): Biological control research projects in this regional group made significant impacts on suppression of both arthropod and weed pests through introduction (classical), conservation, and augmentation approaches. Measures of progress for the W4185 group detailed in Appendix B include 512 professional publications produced as a result of research conducted under project objectives. These breakdowns are as follows; 466 peer reviewed journal articles, 21 technical reports, 14 book chapters/contributed sections, 1 book and 10 proceedings papers. Project members were asked to provide a list of only their publications, this number therefore represents a conservative estimate of the research productivity of W4185 members because it does not include PhD dissertations, Masters theses, extension publications, or trade journal articles.
Past research projects that are continuing include not only those seeking rapid control of pests, but also those that focus on fundamental biological discoveries or changes in conceptual frameworks that influence biological control research. The past 5 years has also seen the continued development of new methods that influence how biological control research is conducted. Underlying these many accomplishments were the critical interactions and collaborations that transcended state and institutional boundaries and were made possible through this regional research project. Of the 512 peer-reviewed publications by the group, 105 were co-authored by W4185 members working together from different institutions. Many of the biocontrol programs on weed species covered under this project depend on the collaboration of researchers in several states at any given time, and many of these work hand in hand with overseas W4185 partners, the BBCA, CABI Biosciences, and USDA-ARS EBCL. One example of this is the Tree of Heaven (Ailanthus altissima) biological control program currently being developed using the eriophyid mite Aculus mosoniensis, (Marini et al. 2021).
The detailed research accomplishments by W4185 scientists from 2017-2022 are presented in the annual reports. The group is simply too large, and the accomplishments too diverse, to present these findings in detail below (W4185 participants work on approximately 168 different pest species). Impact Statements summarize findings in Appendix C and cumulative publications in Appendix B provide an excellent overview of the diverse and productive nature of this group. Therefore, selected projects representing the current and ongoing projects of some members are highlighted below.
Applied biological control accomplishments. Many arthropod and weed pests targeted over the past 5 years saw promising declines. Classical and augmentative releases of millions (individuals) of natural enemies were used against at least 25 pest arthropods or weeds in western states. Other programs are still searching for agents in native host ranges, evaluating non-target effects of potential biological control agents and applying for release permits. Some of these ongoing projects are assessing environmental consequences of former releases and documenting ecosystem impacts. Summarized examples from the past 5 years follow.
Surveys conducted for native and the self-introduced parasitoid, Trissolcus japonicus, attacking the eggs of the brown marmorated stink bugs (BMSB) started two years ago. Researchers are looking in southern California using frozen sentinel BMSB egg masses and field exposed eggs are sent to CDFA for rearing of parasitoids. The goal is to collect the self-introduced BMSB egg parasitoid, Trissolcus japonicus, which has been previously collected in the LA Basin (and therefore not be dependent on BMSB programs outside of the western region. CDFA is using these parasitoids to start T. japonicus colonies for mass production and release (Lara et al. 2019). Biological control of the Erythrina gall wasp appears to have successfully prevented the extinction of the native tree, Erythrina sandwicensis, a keystone species in Hawaii’s few remaining threatened lowland forest ecosystems (Kaufman et al. 2020). Surveys were conducted at 30 sites (15 in Montana; 15 in Colorado) of Lepdium draba (hoary cress) for insect herbivores (both native and previously established introduced species) in preparation for evaluating the effects of releasing the recently approved mite biocontrol agent Aceria drabae. Lab trials were conducted to assess the efficacy of a commercially available soil-dwelling predatory mite (Stratiolaelaps scimitus) to suppress bulb mite populations. Results showed the 1:5 predator to prey ratio yielded mortality of 72.5%, which was significantly greater than the other treatments and controls. Future experiments will replicate the laboratory trials in soil in the laboratory with this rate. These trials will also offer options for managing mites in other crops, such as onions and garlic. Greenhouse and field cage studies of the interactions (facilitation and competition) between the two biocontrol agents, Jaapiella ivannikovi and Aulacidea acroptilonica and their impact on Russian knapweed stem densities was conducted. Aphthona flea beetles were redistributed on all significant leafy spurge populations in New Mexico and have reduced densities to non-economic levels throughout the state. Action thresholds based on predator to prey ratios were developed for the management of Bemisia tabaci in cotton. These new thresholds were tested in comparison with conventional, pest-centric thresholds in experimental plots and grower fields in Arizona and Mexico. Thresholds advanced insecticide applications in about 5-35% of cases, suggesting insufficient biocontrol, but deferred or eliminated sprays in >60% of cases compared with conventional thresholds. Biocontrol-based thresholds have the potential to reduce risk and pest control costs to cotton growers (Vandervoet et al. 2018). The egg parasitoid, Anastatus orientalis, native to China and a natural enemy of spotted lantern fly, is being subjected to host range and host specificity testing in quarantine at UC Riverside. Eggs from twelve species (8 hemipterans [this total includes 3 native fulgorid species] and 4 lepidopterans) have been exposed to A. orientalis to assess their suitability as hosts. Preliminary results indicate that eggs of the pestiferous brown marmorated stink bug are suitable for A. orientalis development. This tentative finding confirms observations made by colleagues on the east coast.
Advancing the conceptual framework for biological control research. Projects involving development or tests of theory provided new insights in basic biology, or improved our understanding of evolutionary relationships between groups of pests or natural enemies. Invasion biology is also a rapidly evolving field and many projects are starting to utilize these concepts and management disciplines. A number of projects are looking at genetic diversity of biological control agents, whether in the original host range to determine if the introduction will be successful, or in a post-introduction evaluation (Gaskin et al. 2019; Daane et al. 2018). Projects are asking, once released, how are introduced natural enemies interacting with native biological control species, and how are they evolving in their new environments (Wright et al. 2018). Work continued to understand the impact of RNA viruses on the efficacy of the predatory biocontrol agent Geocoris pallens. This includes work on virus discovery, assessment of which viruses are virulent (causing decreased body condition or fecundity), and assessment of which viruses might be candidates for causing elevated expression of cannibalism by G. pallens. This project is also conducting modeling studies to determine the impact of a cannibalism-amplifying pathogen on the population dynamics of G. pallens (Rosenheim et al. 2019). Studies have now determined that the southward spread of the tamarisk leaf beetle (Diorhabda carinulata) is unlikely to be due to the evolution of increased flight tendencies at the range edge. Common environment experiments show that individual female beetles from edge populations are larger, and have a tendencies towards higher fecundity than individuals from the core of the range, suggesting those populations are evolving in response to high host abundance and weak competition. There is substantial heritable variation for the evolution of cues leading to winter diapause. Populations in the south have evolved to initiate diapause at a shorter day length than northern (core) populations. Host choice evaluations of beetles from populations where hybrids are common between the Diorhabda species indicate they prefer tamarisk (Pratt et al. 2019). An improved invasive species distribution model was developed for the light brown apple moth, Epiphyas postvittana (LBAM), and a positive linear relationship was found between model predictions of environmental suitability and observed relative abundance of LBAM larvae for localities in coastal California (Hogg et al. 2017). Other projects are looking at risk assessment for exotic generalist predators; symbionts in natural enemies and how these impact biological control; how climate change is impacting existing control programs; non-consumptive effects on natural enemies and more. These are just a few examples from a large number of ecological studies.
Technological advances and new methods.
W5185 researchers continue to develop and use cutting edge tools that are making impacts in biological control. New methods include molecular/genetic techniques, novel, low-tech pest management tools, new genomic and phylogenomic approaches to host range and non-target testing for classical programs, and the formal adoption of proactive biological control tactics. Several of these are highlighted below. Proactive biocontrol is a new approach to using the classical method of using natural enemies for suppressing invasive pest populations. Instead of a "reactive" approach to an invasion a forward leaning alternative is to be "proactive" and commence screening of candidate natural enemies for potential release in advance of an anticipated invasion event. A good example for California is the spotted lanternfly (Hoddle et al. 2018). It is a significant pest on the east coast, it is now established in some areas of the Midwest, and it is highly likely to invade and establish in ca where it could become a significant pest of grape and nut crops. A project is getting ahead of this problem now by working on biocontrol options for this pest ahead of its likely invasion into the west. They are using the pest free window to advance the biocontrol program significantly before spotted lanternfly invades and this will save years of time. A reactive "business as usual" approach is to respond after the pest has established and is causing economic or environmental damage. In another project, all five species of the plumeless thistle genus Carduus are invasives and listed as state noxious weeds in the U.S. Multiple populations of an unknown plumeless thistle species were found in remote areas of Oregon and Idaho. The plants were unrecognizable, so ARS researchers in Montana analyzed the plant’s DNA and matched it to specimens from the eastern Mediterranean. Then ARS, working with botanists from Oregon, California and Spain, definitively identified the plants as Carduus cinereus, a species never before found in the Americas. Northwestern states are now taking EDRR (Early Detection, Rapid Response) action on this new invasive threat (Gaskin, et al. 2020). Biological control management techniques often include ant control. A new, and more effective, bait has been developed that is controlling Argentine ant in commercial citrus (McCalla et al. 2020). All systematics projects within the group are utilizing modern molecular, morphological, and bioinformatics approaches. A huge NSF funded project to revise the classification of the entire superfamily Chalcidoidea has been ongoing and will continue. Members of this superfamily are among the most important natural and introduced control agents of other pest insects, and this will form a foundation for all future studies on the group. Investigators have also obtained nexgen sequencing data for over 600 taxa that cover the entire superfamily. The final results are in progress and work continues on an edited book to cover the entire superfamily. This research is taking a bioinformatic approach by developing a new database to house all of the taxonomic and biological information on the superfamily in TaxonWorks. Publications for this project are debuting with each subgroup analyzed and are included in Appendix B. Augmentation biological control is benefiting from work on mass rearing techniques as many of these multistate projects are distributing natural enemies after mass rearing, often at state run insectaries. One collaborative project has improved rearing for parasitoids of olive fly (Chardonnet et al. 2019). And the commercial biological control community continues to need and depend on research that improves the production of the 30 plus species being used for protected culture biological control. This area is booming with the increase in greenhouse agriculture and organic farming. One W4185 project, with some overlap to the southern multistate project, addressed the need to transfer new methodology to this demographic, and others who are involved in insect rearing, by publishing information about the International Insect Rearing Workshops (Schneider et al. 2018).
Areas needing further investigation. Classical biological control programs require a) identifying a country of pest origin, b) locating and successfully importing a natural enemy, c) rearing the natural enemy and testing for non-target impacts, d) applying for release of promising agents and waiting for approval, and finally, e) releasing the agent and evaluating field efficacy. These steps take time and additional work needs to be done on most of the pest groups for which current research is ongoing. This group is instrumental in the development of procedures for host range testing of arthropod natural enemies. Another invaluable function of W5185 to the western region is information exchange on new theoretical concepts impacting biological control and these ideas are applicable to both arthropod and weed programs. Many W5185 participants operate globally, engaged in foreign exploration and collaborating with scientists in other states and countries. This group provides a network of resources with which to anticipate and plan for the inevitable arrival of an arthropod or weed pest that will appear without its natural enemies (proactive vs. reactive). In addition to the yearly meeting, an email list is maintained of the members and many other biological control scientists and regulatory personnel. Timely information on regulations, annual meetings, job vacancies and more are sent whenever appropriate.
The regulatory structure for classical biological control programs continues to be an issue that impacts everything from foreign exploration to the release of natural enemies that have been thoroughly screened for non-target impacts. Lengthy delays before permitting, rules prohibiting hand carrying of biological control organisms, problems with shipping live organisms worldwide, and other regulations mandated by the U. S. Department of Homeland Security, continue to significantly constrain project research. While we support regulations promoting environmentally sustainable and ethical practices in biological control, we also strive to maintain research projects that will control devastating arthropod and weed pests. In the past 5 years we have addressed these concerns at our annual meetings, and worked with our National Program Leaders in biological control in USDA-ARS, USDA-NIFA, and USDA-APHIS-PPQ to resolve these constraints. We intend to continue to be a voice for a regulatory process that provides the needed oversight of biological control research to ensure it is safe and effective, but does not impede progress on what is often the most ecologically benign method of pest suppression.
Objectives
-
Import and Establish Effective Natural Enemies (Classical Biological Control)
Comments: Objective 1a. Survey indigenous natural enemies. Objective 1b. Conduct foreign exploration and ecological studies in native range of pest. Objective 1c. Determine systematics and biogeography of pests and natural enemies. Objective 1d. Determine environmental safety of exotic candidates prior to release. Objective 1e. Release, establish and redistribute natural enemies. Objective 1f. Evaluate natural enemy efficacy and study ecological/physiological basis for interactions. -
Conserve Natural Enemies to Increase Biological Control of Target Pests
Comments: Objective 2a. Characterize and identify pest and natural enemy communities and their interactions. Objective 2b. Identify and assess factors potentially disruptive to biological control. Objective 2c. Implement and evaluate habitat modification, horticultural practices, and pest suppression tactics to conserve natural enemy activity. -
Augment Natural Enemies to Increase Biological Control Efficacy
Comments: Objective 3a. Assess biological characteristics of natural enemies. Objective 3b. Develop procedures for rearing, storing, quality control and release of natural enemies, and conduct experimental releases to assess feasibility. Objective 3c. Implement augmentation programs and evaluate efficacy of natural enemies. -
Evaluate Environmental and Economic Impacts and Raise Public Awareness of Biological Control
Comments: Objective 4a. Evaluate the environmental and economic impacts of biological control agents. Objective 4b. Develop and implement outreach activities for biological control programs.
Methods
METHODS
Objective 1. Import and Establish Effective Natural Enemies (Classical Biological Control)
Objective 1a. Survey indigenous natural enemies. The scientific literature will be reviewed to determine prior records and geographic distributions of potential natural enemies of arthropod pests and weeds. A survey and collection of natural enemies will be conducted throughout the geographic area of infestation of each target pest. Parasitized pests and natural enemies will be held in the laboratory to allow natural enemy emergence, identification and determination of levels of parasitism and hyperparasitism. For herbivores, specific types of plant injury will be catalogued and plant species closely related to the target weed will be surveyed.
Objective 1b. Conduct foreign exploration and ecological studies in native range of pest. The purpose of foreign exploration is to find, select, and obtain natural enemies from abroad which show promise as biological control agents. Ecological studies conducted on candidate natural enemies in their native range provide information that allows selection of the safest and most effective candidates, and facilitates their establishment and impact on the target pest in the U.S. Natural enemies will be collected and studied abroad in multiple locations throughout the native range of the respective pests. Live materials will be shipped to quarantine facilities listed under Objective 1d and will be shared among scientists/institutions as discussed under Objective 1e. The overseas activities will be conducted by a) U.S.-based federal and state scientists from this project; b) other federal and state scientists based at domestic and foreign laboratories; c) scientists participating in USDA programs for exchange of science and technology with countries such as Japan, China, and Russia; and d) scientists operating under contracts with overseas institutions such as BBCA (Italy), and CABI Biosciences (Switzerland). The network of foreign cooperators that project scientists collaborate with is extensive, and provides critical support in foreign exploration efforts.
Objective 1c: Determine systematics and biogeography of pests and natural enemies. Correct identification of a target pest and associated natural enemies provides a key to obtaining information in the scientific literature on biogeography, ethology, and ecology of a species. Many target pests and natural enemies belong to systematic groups that are in a state of taxonomic confusion, and some groups are only now being modernized. Detailed systematic studies of target pests and natural enemies will involve traditional morphology-based approaches as well as more novel methods including genomic techniques and species-discovery bioinformatics. Initial analysis of the biogeography of target host and natural enemy species will be based on results of geographical surveys and information in the scientific literature. It is noteworthy that this regional project contains scientists with systematic and molecular genetic expertise in many of the natural enemy groups critical to biological control. Expertise essential for natural enemy studies planned for the next five years is represented (but not limited to) the following participating agencies: CA-AES (Phytoseiidae, Coccinellidae, Aphelinidae, Encyrtidae, Eucharitidae, Eulophidae, Braconidae, Aphidiidae, Pteromalidae, Reduviidae, Mymaridae, Trichogrammatidae (technically all families of the Chalcidoidea); ID-AES (Chrysopidae, Hemerobiidae, Coccinellidae); HI-AES (Encyrtidae, Eucoilidae); KS-AES (Encyrtidae, Aphelinidae); NMSU-AES (Pentatomidae); OR-AES (Coleoptera, Mites, Heteroptera, Lepidoptera, Diptera, Gastropoda); Guam-AES (Formicidae, Aphidae); and WA-AES (Coccinelidae; Aphididae; Scelionidae; Carabidae; Vespidae Chamaemyiidae, Syrphidae). Additional assistance is available through an extensive network of collaborators for taxonomic determinations among the Agricultural Experiment Stations, USDA, and other institutions (e.g., Bishop Museum, Honolulu; USNM; British Museum). Other ARS resources include the Systematic Entomology Laboratory (associated with the Smithsonian Institution, Washington DC), ARS Sidney, MT (weedy Brassicaceae, Tamaricaceae, Euphorbiaceae, Asteraceae, Convolvulaceae and native pollinators associated with weedy plant species).The USDA-ARS, EBCL (European Biological Control Lab) has a molecular laboratory involved in taxonomic and systematics research at various levels ranging from species to higher-level studies.
Objective 1d: Determine environmental safety of exotic candidates prior to release. The environmental safety of classical biological control has been questioned by conservation biologists concerned about direct and indirect non-target impacts of exotic natural enemies. This has resulted in a need for more in-depth study of the environmental safety of candidate agents. Much of this work will be done in U.S. quarantine facilities (as well as overseas). Traditionally, work in U.S. quarantines focused on exclusion of undesirable pathogens, parasitoids, hyperparasitoids, and predators from natural enemy shipments. Also, much host specificity testing of weed agents has been conducted in U.S. quarantines. With enhanced emphasis on assessing the environmental safety of candidate agents prior to release, U.S. quarantines will become an increasingly important resource and of vital importance to serving many of this projects objectives. Exotic biological control agents will be received, processed, and studied in quarantine facilities at CA-B-AES, CA-R-AES, FL-UF/IFAS (Indian River Research and Education Center, FL), HI-HDOA, HI-USDA-FS (Volcano, HI), WA-AES, WA-ARS, Guam-AES, MT-ARS, EBCL-ARS (France) for the management of arthropod pests. Biological control agents of weeds will be handled through quarantine facilities at CA-ARS, FL-USDA-ARS (Invasive Plant Research Laboratory, Ft. Lauderdale, FL), HI-USDA-FS (Volcano, HI), NMSU-AES (New Mexico State University), MT-AES, MT-ARS (NPARL), WA-AES, and EBCL-ARS (France). A few projects will utilize quarantine facilities in other regions (TX-AES, USDA-APHIS-PPQ-CPHST /), DE-ARS, MD-ARS (Fort Detrick), VA-SDA). Quarantine and enhanced pre-release studies of environmental safety will be conducted for exotic natural enemies attacking pests in 11 target pest groups by 12 participating agencies.
Objective 1e: Release, establish, and redistribute natural enemies. Key steps in the implementation of classical biological control are the initial release, establishment, and redistribution of approved natural enemies. The initial numbers of natural enemies available for field release or redistribution are often limiting, requiring laboratory or field propagation. Facilities for mass production exist at CA-DFA, CO-DOA, FL-Department of Agriculture and Consumer Services, Division of Plant Industry, Gainesville, FL and Dundee, FL, MT-FS, MT-ARS, WA-AES, and WA-ARS. There are also limited rearing facilities on Guam, CA-ARS, and WSU-Research and Extension Center, Puyallup, WA. USDA-ARS labs in Newark, DE and the USDA-ARS, EBCL in France also have the capacity to assist this group with mass rearing and mass field collections. Many weed biological programs initiate field insectaries that ultimately produce large numbers of individuals for redistribution. However, even with enough for release, establishment does not always occur. Consequently, studies are being conducted by project members that examine various factors that might influence colonization. A noteworthy feature of this regional project is the high degree of natural enemy sharing among participants for initial release in new habitats and for redistribution.
Objective 1f: Evaluate natural enemy efficacy and study ecological/physiological basis for interactions. The establishment of a natural enemy species does not always result in effective control of the target pest, as many ecological and environmental factors may influence the degree of control achieved. Ecological studies must accompany the release of biocontrol agents to evaluate natural enemy impact, improve efficacy, and determine the ecological/physiological basis for natural enemy-host interactions. Experimental techniques used to quantify natural enemy efficacy include natural enemy inclusion, exclusion and interference. These consist of adding, excluding or interfering with natural enemies in experimental settings and comparing these to un-manipulated controls. Standard techniques will be used to study the influence of environmental variables (e.g., temperature and humidity) on life-history characteristics of the natural enemies and on predator-prey and parasite-host interactions. A key aspect of this regional project is that valuable comparative data from the wide range of habitats found in the Western Region is often obtained through collaboration among participants.
Objective 2: Conserve Natural Enemies to Increase Biological Control of Target Pests.
Objective 2a: Characterize and identify pest and natural enemy communities and their interactions. Two critical first steps in the conservation of natural enemies are determination of the identity of the species involved and characterization of the ecological communities in which they reside. This information is fundamental to developing an understanding of how practices such as pesticide applications will influence pest and natural enemy densities. Much of the methodology needed to address this objective is the same as for Objective 1.
Objective 2b: Identify and assess factors potentially disruptive to biological control. Conservation biological control involves the alteration or modification of the environment to favor natural enemies, either by reducing adverse factors or by providing missing requisites. Specific factors that impede or reduce the efficacy of biological control agents must be identified and quantified as to their impact. For many of the target pest species, this involves the identification of agricultural practices (mainly broad spectrum pesticide applications) that impact biological control agents, including the impact of herbicides on weed biological control agents. Many studies have focused on laboratory surveys and bioassays of various pesticides and subsequent large-scale field tests involving these "softer" compounds. However, factors such as climatic change, interactions with indigenous natural enemies, use of transgenic plants, and cultural management practices, etc., can also be disruptive to the natural enemies.
Objective 2c: Implement and evaluate habitat modification, horticultural practices, and pest suppression tactics to conserve natural enemy activity. As mentioned above, the conservation approach to biological control seeks to enhance the effectiveness of natural enemies, but may also target the pest as well. Examples of the conservation approach include maintaining weedy borders around fields or intercropping with nectar and pollen producing species to increase longevity and reproduction in the natural enemies; providing nesting boxes or shelters to improve reproduction or create refugia from environmental extremes; and using various agronomic approaches to increase the effectiveness of the natural enemies (e.g., plant spacing, cover crops, polycultures, strip crops, strip-cutting, crop rotation, trap crops, early/late planting and harvesting, etc.). These approaches may help conserve natural enemies while still controlling the target pest. The utilization of softer pesticides (biopesticides), including their selective use (e.g., reduced dosages and frequency of application, and selective timing of pesticide application) may help conserve natural enemies while still controlling the target pest. Research studies will focus on the implementation of these approaches and especially field-scale evaluation of the impact on host/prey diversity, natural enemy activity, and pest suppression.
Objective 3: Augment Natural Enemies to Increase Biological Control Efficacy.
Objective 3a: Assess biological characteristics of natural enemies. Natural enemy species and biotypes may show differences with regard to their biological characteristics (e.g., developmental thresholds and rates, fecundity, behavior, host specificity, cold tolerance, etc.) and these differences may influence their effectiveness as biological control agents. Research will be conducted to develop criteria for selecting biotypes, species, and combinations of beneficial species for use against a specific pest to ensure the most suitable natural enemy species are selected for each specific augmentative release program,
Objective 3b: Develop procedures for rearing, storing, quality control and release of natural enemies, and conduct experimental releases to assess feasibility. The success of mass-rearing programs for experimental and commercial augmentation is dependent on the procedures used for rearing, storing, distribution, and release of natural enemies. Large-scale rearing of arthropod natural enemies usually requires production of host plants, the arthropod or weed host, and the natural enemy. Changes in colonies can occur due to genetic or environmental influences that can reduce the effectiveness of the natural enemy after release. Prior to release, it is desirable to increase shelf-life of natural enemies for subsequent distribution. During storage, natural enemy quality such as viability and fecundity may be significantly reduced resulting in decreased efficacy of the agent. Determination of the best natural enemy stage(s) for release and effective release methods are prerequisite for the timely suppression of the target pest. Research will be conducted to develop rearing, storage, and shipping techniques for a variety of natural enemies for both inundative and inoculative release programs. Work will also focus on genetic improvement of natural enemies and assessing their value for pest control in agricultural systems. An understanding of the relationship between the numbers of natural enemies released, the impact on the pest population, and the level of protection to the commodity is required. The development of management and economic models based on an understanding of such population processes will help characterize the benefits of augmentation.
Objective 3c: Implement augmentation programs and evaluate efficacy of natural enemies. The successful suppression of pest populations through augmentative releases of natural enemies is often dependent on a clear understanding of appropriate times and numbers for natural enemy release, and mitigating problems associated with pesticide disruption or cultural management approaches that might be harmful to the natural enemies involved in the augmentation. Augmentation programs must be evaluated to determine the impact of the natural enemies on the target pest using different release strategies, or under varying environmental conditions. The economic feasibility of such programs also needs to be determined. Augmentative releases will be compared in small and large field trials with conventional control methods (e.g., pesticide applications) and untreated controls to assess natural enemy efficacy and the economic feasibility of such releases. Natural enemy exclusion or inclusion approaches may be needed to ensure that observed impacts are due to the inoculative or inundative releases, and not to indigenous natural enemies responding to more suitable conditions following the modification of agricultural practices (e.g., limited pesticide applications).
Objective 4. Evaluate environmental and economic impacts and raise public awareness of biological control.
Objective 4a: Evaluate the environmental and economic impacts of biological control agents. Economic and environmental impacts are often not thoroughly evaluated. Research will be conducted to determine patterns of non-target host utilization by natural enemies of weeds and arthropod pests, and the population-level consequences of non-target attack. Studies will evaluate the genetic potential for natural enemies to expand their host ranges and this will be accomplished by surveying closely related species that share similar ecological niches to target species. Field plots will be established in areas where natural enemies are active or have been released, and non-target hosts will be sampled based on the life cycles of the organisms involved. If transfers are detected, the impact of the agents on the non-targets will be measured by determining frequency, geographical, and taxonomic extent of attacks. Loss of growth and viable seed production, mortality rates, or changes in abundance of non-target populations will be determined using replicated check and treatment plots coupled with exclusion or other appropriate techniques. The economic return on research dollars spent on biocontrol is well known to scientists but not widely appreciated by the public. Declining resources and state/federal initiatives towards more accountability make it imperative that benefit/cost ratios of biological control be determined. Benefit/cost ratios of biocontrol programs for pests will be calculated. Using treatment thresholds, the cost of chemical treatment or other control tactics will be determined by querying pest control operators, growers, or by determining the cost of materials, labor, and operation of the application equipment. Using production values associated with the current land use, the economic and environmental benefits of biological control will be determined. The economic value of conservation and/or augmentation of natural enemies will be assessed along with the long- term costs of using the natural enemies. These costs will be compared with the economic inputs of alternative conventional control methods, or total absence of controls.
Objective 4b: Develop and implement outreach activities for biological control programs. This objective encourages greater development of outreach programs, especially efforts that have not been easy to report under our current set of objectives. Well-documented, and highly visible outreach activities include publication of research findings in international journals, which are increasingly more available to clientele. Veritable explosions of websites from land grant and Federal laboratories have made project results much more accessible to other researchers, growers. ranchers, forest managers, and Master Gardener groups, and has included the development of educational materials about biological control programs for the public. Webinars are now a part of routine information dissemination and are frequently free to all “attendees”. A number of national (commercial) conferences and expos have debuted in the past 5 years that have educational tracks with sections devoted to applied biocontrol. Land grant researcher and extension scientists are frequent invited speakers in these sessions and are effective at presenting real-world biological control advice. Compared to five years ago, the ability to broadcast information is limitless.
Measurement of Progress and Results
Outputs
- Outputs: The results of the proposed research activities will consist of finding new or improved natural enemy species or biotypes for biological control of major arthropod and weed pests in the western U.S.; improved methodologies for incorporating biological control into IPM programs for key agricultural resources in the western U.S.; data addressing the ecological basis of success and failure of biological control; and data addressing the environmental and economic impacts of biological control. The publications, presentations and websites will continue to provide state and federal agencies, and grower industry clientele with both technical and practical information on a timely basis.
Outcomes or Projected Impacts
- Projected Impacts: The availability of new or improved biological control options for major pest species in the western U.S. will result in reduced pesticide usage, increased sustainability of agricultural production systems, and economic benefits to both agricultural producers (in the form of reduced pest management costs) and consumers (in the form of reduced food costs). Additional benefits will be the reduction of pesticide usage and include reduced food, soil and water contamination, reduced impacts on non-target species including wildlife and pollinators, and reduced human exposure to potentially harmful chemicals. Enhanced knowledge of the ecological mechanisms underlying biological control will increase success rates. Enhanced knowledge of the environmental and economic impacts of biological control will improve the environmental safety of biological control and promote its adoption in current and new pest management programs.
Milestones
(0):Milestones: The sequence of Objectives 1-3 defines a typical progression for classical, augmentative and conservation biological control programs, respectively. The many specific biological control programs that comprise this proposal are at different points along these spectra. In general, Objectives 1-3 need to be completed before Objective 4.Projected Participation
View Appendix E: ParticipationOutreach Plan
Traditional outlets for disseminating project results, including peer-reviewed articles, progress reports, presentations at scientific meetings, websites, and extension publications and presentations, will continue to be heavily utilized. However, the addition of webinars for both scientists and grower clientele will continue to increase. The publishing effort of this group is both prolific and of very high quality [Appendix B]. As a measure of multidisciplinary research, many of the peer-reviewed papers published in the last 5 years have appeared in non-entomological control journals such as, but not limited to, Ecology and Evolution, Ecology Letters, Ecological Applications, Ecosphere, Global Change Biology, Molecular Ecology, Oecologia, PeerJ, PLoS ONE, PNAS, and Scientific Reports. Our members do not list submitted and invited talks that do not include proceedings papers, however, these would number in the hundreds, over the past 5 years. The annual meeting is well-attended and includes formal presentations on current research. For example, approximately 60 people attended the 2019 meeting in Ft. Collins, Colorado, the last in-person meeting before the coronavirus pandemic. Presentation files are frequently sent to members via email after the meeting. While some participants have extension appointments, most also participate in extension and other outreach activities. A feature of biocontrol research is that many of the activities are conducted in close cooperation with end users. Researchers working on conservation and augmentative biological control also work hand-in-hand with commercial producers and other beneficiaries.
Organization/Governance
The Technical Committee will be comprised of representatives designated by the directors of participating state agricultural experiment stations, state departments of agriculture, and federal agencies. This project is considered a Western Regional Research Project administratively, but because this regional project embraces research topics and biological control tactics of national scope, participation by scientists from other regions of the U.S. is encouraged. The administrative advisor will be selected by the Western Association of Agricultural Experiment Station Directors and will serve the committee without vote. The officers will consist of a Chair, Secretary, and Member at Large elected from the regional project membership. These officials, plus the administrative advisor, comprise the Executive Committee. The Chair will prepare technical and executive meeting agenda, preside at meetings, and prepare an annual report on the research activities of the regional project. The Secretary will record minutes of technical and executive committee meetings and perform other duties as necessary. The Member at Large, will succeed the Secretary, who will, in turn, succeed the Chair. The Technical Committee will meet annually at a place and date designated by majority vote of the Technical Committee members.
Literature Cited
Bordini, I.C., Naranjo, S.E., Fournier, A., Ellsworth, P.C. 2021. Novel insecticides and generalist predators support conservation biological control in cotton. Biological Control 154: 104502 (https://doi.org/10.1016/j.biocontrol.2020.104502)
Chardonnet, F., A. Blanchet, B. Hurtel, F. Marini, L. Smith. 2019. Mass-rearing optimization of the parasitoid Psyttalia lounsburyi for biological control of the olive fruit fly. J. Appl. Entomol. 143, 277–288. doi: 10.1111/jen.12573
Crowder, D. W., & Harwood, J. D. 2014. Promoting biological control in a rapidly changing world. Biological Control 75: 1-7.
Daane KM, Middleton MC, Sforza RFH, Kamps-Hughes N, Watson GW, Almeida RPP, et al. 2018. Determining the geographic origin of invasive populations of the mealybug Planococcus ficus based on molecular genetic analysis. PLoS ONE 13(3): e0193852
DeBach, P. 1964. Biological control of insect pests and weeds, ed. P. DeBach. London: Chapman & Hall. 844 pp.
Fleischer, S.J., Hutchison, W.D., Naranjo, S.E. 2021. Sustainable management of insect-resistant crops. pp. 112-125 in Plant Biotechnology - Experience and Future Prospects, 2nd Ed., A. Ricroch, S. Chopra, M. Kuntz (eds.), Springer, Dordrecht-Heidelberg-London-New York.
Gaskin, J.F., Coombs, E., Kelch, D.G., Keil, D.J., Porter, M. and Susanna, A., 2020. Carduus cinereus (asteraceae)–new to North America. Madroño, 66(4), pp.142-147.
Gaskin, JF, SM Bogdanowicz, KR Guilbault, RA Hufbauer, JA Andrés, U Schaffner, P Weyl, L Williams III. 2019. Finding the extremes of genetic diversity in an invasion to assist biological control management. Invasive Plant Science and Management DOI: 10.1017/inp.2019.16
Gebiola M, Streicher JW, Rugman‐Jones PF, Morse JG, Stouthamer R. 2019. Genome‐wide analyses of single nucleotide polymorphisms reveal the consequences of traditional mass‐rearing on genetic variation in Aphytis melinus (Hymenoptera: Aphelinidae): The danger of putting all eggs in one basket. Pest Management Science 74: 3102-3112.
Heimpel, G. E., and Mills, N. J. 2017. Biological Control: Ecology and Applications. Cambridge University Press, Cambridge, UK.
Hinz, H.L., Winston, R.L. and Schwarzländer, M. 2019. A global review of the effectiveness and environmental safety of classical weed biological control. Current Opinion in Insect Science. DOI 10.1016/j.cois.2019.11.006. OPEN ACCESS
Hoddle, M.S. K. Mace, J. Steggall. 2018. Proactive biological control: a cost-effective management option for invasive species. California Agriculture 72: 48-50.
Hogg, B. N., Mills, N. J., and Daane, K. M. 2017. Temporal patterns in the abundance and species composition of spiders on host plants of the invasive moth Epiphyas postvittana (Lepidoptera: Tortricidae). Environmental Entomology 46(3): 502–510. doi: 10.1093/ee/nvx065
https://www.doi.gov/sites/doi.gov/files/doi-invasive-species-strategic-plan-2021-2025-508.pdf
Kaufman, L.V., Yalemar, J., & Wright, M.G. 2020. Classical biological control of the erythrina gall wasp, Quadrastichus erythrinae, in Hawaii: conserving an endangered habitat. Biological Control 142: 104161.
Kimberling, D. N. 2004. Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biological Invasions 6: 301-318.
Lara, J.R., C. Pickett, and M.S. Hoddle. 2019. Physiological host range of Trissolcus japonicus in relation to Halyomorpha halys and other pentatomids in California. BioControl 64: 513-528.
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Marini F, Profeta E, Vidović B, Petanović R, de Lillo E, Weyl P, Hinz HL, Moffat CE, Bon M-C, Cvrković T, Kashefi J, Sforza RFH, Cristofaro M. 2021. Field Assessment of the Host Range of Aculus mosoniensis (Acari: Eriophyidae), a Biological Control Agent of the Tree of Heaven (Ailanthus altissima). Insects. 2021; 12(7):637.
Mason, P. G., Flanders, R. G. & Arrendondo-Bernal, H. A. 2005. How can legislation facilitate the use of biological control of arthropods in North America? Proceedings, 2nd International Symposium of Biological Control of Arthropods, Davos, Switzerland. Sept. 2005. U.S.D.A. Forest Service Publication FHTET-2005-08, vol. 1. pp. 701-714.
McCalla, K.A., J-W Tay, A. Mulchandani, D-H Choe, and M.S. Hoddle. 2020. Biodegradable alginate hydrogel bait delivery system effectively controls high density populations of Argentine ant in commercial citrus. J. Pest. Sci. https://doi.org/10.1007/s10340-019-01175-9
Mhina, G. J., N. C. Leppla, M. H. Thomas and D. Solís. 2016. Cost effectiveness of biological control of invasive mole crickets in Florida pastures. Biological Control 100:108-115.
Naranjo, S.E., Frisvold, G.B., Ellsworth, P.C. 2019. Economic value of arthropod biological control. Pp. 49-85, in The Economics of Integrated Pest Management for Insects, D. Onstad, P. Crain (eds.). CAB International.
Nechols, J. R. 2021. The potential impact of climate change on non-target risks from imported generalist natural enemies and on biological control. BioControl 66: 37–44
NOAA. 2021. https://www.noaa.gov/news/its-official-july-2021-was-earths-hottest-month-on-record
Pimentel, D., Zuniga, R. & Morrison, D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273-288.
Pratt, P. D., J. C. Herr, R. I. Carruthers, M. J. Pitcairn, B. Villegas, and M. Brent Kelley. 2019. Release, establishment and realized geographic distribution of Diorhabda carinulata and D. elongata (Coleoptera: Chrysomelidae) in California, U.S.A. Biocontrol Science and Technology 29(7): 686-705.
Romeis, J., Naranjo, S.E., Meissle, M., Shelton, A.M. 2019. Genetically engineered crops help support conservation biological control. Biological Control 130: 136-154.
Rosenheim, J. A., N. Booster, M. Culshaw-Maurer, T. Mueller, R. Kuffel, Y.-H. Law, P. B. Goodell, T. Pierce, L. D. Godfrey, W. B. Hunter, and A. Sadeh. 2019. Disease, elevated cannibalism expression, and associated population crash in an omnivorous bug, Geocoris pallens. Oecologia 190:69-83.
Sala O, Chapin III FS, Armesto JJ, and others (2000). Global biodiversity scenarios for the year 2100. Science 287:1770-1774
Schneider, J. C., N. C. Leppla, M. F. Chaudhury, L. A. Castrillo, S. Ng, W. R. Fisher, P. M. Ebling, M. A. Caprio, and T. Riddell. 2018. Educating the Next Generation of Insect Rearing Professionals: Lessons from the International Insect Rearing Workshop, Mississippi State University, 2000-2017. American Entomologist. 64: 102-111.
The National Road Map for Integrated Pest Management. 2018. https://www.usda.gov/media/press-releases/2018/10/24/usda-announces-update-national-road-map-integrated-pest-management
United States Department of the Interior, Invasive Species Strategic Plan. 2021-2025).
USDA NASS. 2020. 2019 Organic Survey. 2017 Census of Agriculture. Vol. 3, Part 4.
Vandervoet, T., Ellsworth, P.C., Carriere, Y., Naranjo, S.E. 2018. Quantifying conservation biological control for management of Bemisia tabaci (Hemiptera: Aleyrodidae) in cotton. Journal of Economic Entomology 111: 1056-1068.
Willer, E. H., Schlatter, B., Trávní, J., Kemper, L., & Lernoud, J. (2020). The World of Organic Agriculture Statistics and Emerging Trends 2020. 337.
Wright, M.G. & Bennett, G.B. 2018. Evolution of biological control agents following introduction to new environments. BioControl 63: 105-116. First online July 2017: DOI 10.1007/s10526-017-9830-z