Duration: 10/01/2017 to 09/30/2022

Administrative Advisor(s):

NIFA Reps:

Non-Technical Summary

Statement of Issues and Justification

Broad-spectrum chemical insecticides continue to be the mainstay for control of arthropod pests in most agricultural systems, as well as in natural and urban landscapes. Several chemical pesticides are capable of rapidly killing various pests, but heavy reliance on their use has generated substantial problems including safety risks to humans, negative impacts on beneficial arthropods, outbreaks of secondary pests, which are normally held in check by natural enemies, decreases in biodiversity, and increases the risk of insecticide resistance.  Numerous bacteria, fungi, nematodes, and viruses attack a variety of arthropod pests infesting agricultural and urban landscapes.  There are multiple species of entomopathogens that are commercially available as biopesticides which produce fewer negative consequences in the environment (Lacey, 2017). 

Changes in pest management programs, such as the reduction in organophosphate use dictated by the Food Quality Protection Act (FQPA), and proposed legislation by the EPA regulating the use of neonicotinoids to protect pollinators (Suryanarayanan, 2015) necessitate the development of new management tactics that are environmentally sound and compatible with current production and integrated pest management (IPM) practices. In many agricultural and natural systems, viable alternatives to chemical insecticides are microbial control agents.  In contrast to chemical insecticides, microbial control agents generally are not harmful to the environment, have minimal potential to select for resistant populations, or injure non-target organisms. The focus of this project is to develop and advance entomopathogens for biological pest suppression. 

Development of microbial control tactics using entomopathogens is of great importance to US agriculture. The Experiment Station Committee on Organization and Policy (ESCOP), and Association of Public and Land Grant Universities (NASULGC, APLU) have identified environmental stewardship, including the need to decrease chemical pesticide use, as a primary agricultural challenge in the US. Furthermore, most stakeholder groups developing strategic plans for pest management throughout the U.S. have identified biological control as a major research need, and many have specifically identified use of entomopathogens as a priority. Some commodities that list the development of entomopathogens as a priority include pecan, peaches, apples and grapes (http://www.ipmcenters.org/).

Microbial control research and application has demonstrated major impacts on integrated pest management (IPM) during the past fifty years. The commercialization of Bacillus thuringiensis (Bt) products, including Bt-transgenic plants, is probably the most notable and commercially important event. New discoveries of effective entomopathogens and advances in their production have facilitated the commercialization of numerous products. Although there has been an increase in biopesticide sales and research, microbial control generally is still not considered as a primary strategy for pest management in many crops, especially in conventional production systems (Leng et al., 2011; Sinha, 2012; Lacey, 2016).  However, recent estimates suggest that biopesticides could become the fastest-growing crop protection market sector globally, greatly exceeding the growth of conventional chemical insecticides (Glare et al., 2012).  Biopesticide sales in the US are projected to achieve a compound annual growth rate of 17.4% from 2016 to 2022, with sales reaching $1.25 billion (Markets and Markets, 2016). Thus, there is a need to expand microbial control research and incorporate microbial control options into integrated pest management (IPM) strategies in order to maintain global competitiveness of US agriculture.  Additional research is required to expand and complement the expected increase in demand and use of entomopathogens as vital components of IPM. New scientific tools, including molecular markers, genomics, and in vitro production techniques will allow for novel discovery, identification, and development of entomopathogens for IPM.  For entomopathogens to be incorporated into existing IPM practices, results to support science-based recommendations are necessary.  

The key challenges that limit the implementation of microbial control for arthropod pests will be addressed in this project including: enhancing efficacy through strain discovery and improvement, advancing production and delivery, integration with existing management techniques, conservation of endemic entomopathogens, and gaining greater understanding of fundamental entomopathogen biology and ecology to further improve pest management. The project objectives will address pest issues in large acreage crops, orchards, small fruits and vegetables, urban landscapes, and nurseries.  The consequences of not accomplishing the proposed research may increase use of chemical pesticides in the environment (risking the health of humans and other nontargets) and allow greater crop losses due to endemic and invasive pests. In addition to numerous endemic pests, several invasive pests such as the Asian citrus psyllid (Diaphorina citri), Bagrada bug (Bagrada hilaris), brown marmorated stink bug (Halyomarpha halys), polyphagous shot hole borer (Euwallacea fornicates), and spotted wing drosophila,(Drosophila suzukii) pose a serious threat to several important hosts in agricultural, orchard, urban, and nursery systems.  Entomopathogens are critically important in non-agricultural situations where chemical pesticide use is undesirable and poses a higher human or environmental risk.

Given that these research needs are distributed across numerous US commodities and native environments, a cooperative multi-state approach is justified to provide broad impact solutions that are widely applicable. Entomopathogens and their insect pest hosts are not limited by artificial boundaries. Therefore, entomopathogen efficacy, persistence, safety, resistance management and other parameters must be evaluated under in a range of environments across numerous states. Protocols must be developed and standardized for the diverse types of research being proposed. Multi-state cooperative research among universities, USDA, and industry partners is essential to be successful in fulfilling the objectives of this project proposal.  We acknowledge the wide breadth of opportunities for collaborative research projects, but also recognize that this project will allow communication from numerous participants with expertise with entomopathogens in different agricultural and native environments. Participants in the project will share information and resources, participate in cooperative funding prospects, and evaluate progress of individual and group research projects.   

We anticipate that the project will produce substantial benefits for both producer and consumer stakeholder groups. Stakeholders will include farmers, pest control advisors, biopesticide industry, the scientific community, and the general public. Experiments will be conducted in cropping and natural environments. Given the broad nature of the research, we anticipate considerable knowledge transfer to additional crops/settings during the project period. Foremost, the proposed research will facilitate transition from a reliance on chemical insecticide usage by providing effective and environmentally-friendly alternatives. At a minimum, results from the project will be integrated into existing IPM programs as additional tools.  Development of entomopathogens for use in IPM will fill vital gaps caused by the loss of broad spectrum chemical control products. This strategy is of particular importance in specialty crops that have few remaining pest management options. Furthermore, as new pest assemblages arise, novel microbial control tactics will contribute substantially to the development of innovative IPM programs.  Microbial control products already are important tools in several commodity sectors, including organic crops, and for the control of invasive pests. The proposed project will improve quality of life by providing farmers additional tools to manage arthropod pests without negative human and environmental risks, and by providing the public with food containing lower levels of synthetic chemical residues. Economic opportunities will be created by enhancing the commercial aspects of biological products and improving the productivity of various crops.

This project has broad and unique expertise represented by a working group from across the US which will enable us to achieve the proposed objectives. This project strongly addresses several US agricultural and Southern Association of Agricultural Experiment Station Directors (SAAESD) priority areas, particularly priorities 1, 4, and 5 (Developing greater harmony between agriculture and the environment; establishing an agricultural system that is highly competitive in the global economy, and enhanced economic opportunity and quality of life for Americans).

Related, Current and Previous Work

The proposed project is unique. Although there are other entomology and IPM projects that include some of the members or this project, there is no common overlap in research with other multi-state efforts or individual CRIS projects. This is a comprehensive project that focuses on the development of entomopathogens and microbial control across a wide range of arthropod pests involving researchers from many regions of the US.  This project also complements other multi-state projects focusing on environmentally sustainable pest management practices, including S1058: Biological Control of Arthropod Pests and Weeds, https://www.nimss.org/projects/view/mrp/outline/14496  and NCERA224: IPM Strategies for Arthropod Pests and  Diseases in Nurseries and Landscapes https://www.nimss.org/projects/view/mrp/outline/18353.

A CRIS search (using keywords such as microbial control, insect, entomopathogenic, as well as names of individual genera as targets) reveals that the vast majority of research on applied microbial control of arthropod pests in the US is being conducted by our project participants and collaborators.  Although some level of research with entomopathogens is ongoing at several institutions, the specific objectives of these projects do not overlap directly with those of our project. We will continue to encourage all scientists working on microbial control of arthropod pests to participate in this multi-state project including those representing private industry. We will ensure that those scientists working on entomopathogens are aware of our project by advertising through professional societies (Entomological Society of America [ESA], Society of Invertebrate Pathology) and in direct communication with industry colleagues.  We will continue to organize the annual meeting of our working group at ESA annual meetings, the largest global venue for entomologists.

The proposed project builds strongly upon decades of research on invertebrate pathology and microbial control. The breadth of research on insect pathology and microbial control of pests is reviewed in various texts (Tanada and Kaya, 1993; Metz, 2003; Grewal et al., 2005; Ekesi and Maniania, 2007; Vega and Kaya, 2012; Lacey, 2017).  During the previous 5 years of this project, new multi-state collaborations have been established (or continued) that addressed the development of entomopathogens for biological control of selected arthropod pests. These efforts have resulted in contributions to numerous scientific publications. In addition, a formal symposium has served to deliver current information on entomopathogens to peer groups annually at the national ESA conference. This opportunity for outreach has allowed the results of the project to be distributed to a broad segment of the pest management community, further enhancing the potential for adoption of microbial control tactics in existing IPM programs or for invasive pests. 

The following section lists examples of important accomplishments the project has made over the past 5 years. Advancements were made in the discovery, production, formulation and efficacy of microbial control agents used in biological pest suppression. Additionally, noteworthy advances were accomplished in a greater understanding of the basic biology of microbial control agents. Research in this project has supported the initiation of microbial control, or expanded microbial control, for arthropod pests in diverse systems. In the new proposed project, we will expand microbial control efforts against current and new targets. Thus, the past accomplishments for participants in this project are a basis for future research objectives. 

Summary of accomplishments from prior S1052 objectives:

PROJECT 1:  Discovery of entomopathogens and their integration and safety in pest management programs for major acreage crops.

In collaboration with EMBRAPA, Brazil and Ismailia Agricultural Research Station, Egypt, scientists at USDA-ARS, Peoria, IL developed a biopesticide with Bacillus thuringiensis and Beauveria bassiana, which had synergistic insecticidal activity against the cabbage looper, Trichoplusia ni. 

Scientists at USDA-ARS, Sidney, MT developed a prototype loop-mediated isothermal amplification (LAMP) method for identifying Beauveria pseudobassiana and generic Beauveria spp. in plants and other places to simplify molecular characterization.  They also evaluated the efficacy of B. bassiana encapsulated in alginate microbeads against chewing pests and endophytic potential of five B. pseudobassiana isolates from the wheat stem sawfly, Cephus cinctus, in 15 varieties of spring, winter, and durum wheat.  Additional studies included surveys of the seasonal occurrence of Zoophthora phytonomi and Beauveria spp. in the alfalfa weevil, Hypera postica, in alfalfa, and field evaluation of a B. thuringiensis subsp. gallariae-based biopesticide with Cry 8Da protein against larvae of H. postica.

A team of scientists evaluated virulence factors of insect pathogens.  Two cyclooligomer depsipeptides, bassianolide and beauvericin, were biosynthesized during this research (Xu et al., 2008; Xu et al., 2009) and determined to be virulence factors of B. bassiana.

Researchers at Montana State University, Conrad, MT evaluated several strategies for controlling wheat midge, Sitodiplosis mosellana, with entomopathogenic nematodes, entomopathogenic fungi, and other options and the impact on secondary pests.

PROJECT 2: Discovery of entomopathogens and their integration and safety in pest management programs for ornamental, vegetable, fruit and nut crops.

Collaborative research at USDA-ARS near Byron, GA addressed multiple biocontrol issues including: impact of host plants on the efficacy of entomopathogenic nematodes; optimization of artificial media components for producing Steinernema feltiae (Leite et al., 2016); first report of antibiosis (e.g., to entomopathogenic fungi) in an insect pupal cell in the pecan weevil, Curculio caryae, and other weevils (Shapiro-Ilan and Mizell, 2015); discovered that the bacterial-based product from Chromobacterium subtsugae can provide equal levels of control for pecan weevil relative to standard chemical (carbaryl or pyrethroids) controls (Shapiro-Ilan et al., 2013); protecting entomopathogenic nematodes from environmental damage (e.g., UV radiation and desiccation) with low concentrations of a specialized fire gel formulation (Barricade) used against selected greenhouse pests and lesser peachtree borer, Synanthedon pictipes (Shapiro-Ilan et al., 2015); and effective control of the peachtree borer, Synanthedon exitiosa through preventative or curative spring-time applications of S. carpocapsae (Shapiro-Ilan et al., 2016).

Scientists at Cornell, Ithaca, NY; the Illinois Natural History Survey, Urbana, IL; and USDA-ARS, Gainesville, FL; continue to work on a microsporidian pathogen that infects the invasive brown marmorated stink bug, Halyomorpha halys, and other stink bugs. Researchers at University of California Cooperative Extension (UCCE) and Driscoll’s Corporation on the California Central Coast implemented multiple studies evaluating the role of entomopathogenic fungi, B. thuringiensis, and Helicoverpa zea nucleopolyhedrovirus in managing arthropod pests of strawberry.  UCCE research also included entomopathogenic, endophytic and mycorrhiza-like interactions of entomopathogenic fungi in strawberry and vegetables in promoting plant growth or protecting against pests and diseases.

PROJECT 3: Discovery of entomopathogens and their integration and safety in pest management programs for urban and natural landscapes.

Cornell University scientists reported that the Sirex woodwasp, Sirex noctilio, has killed pine trees in seven states and is spreading south and west across the US. The nematode Deladenus siricidicola sterilizes woodwasp eggs and has been a successful biocontrol agent in Australia, but strains of S. noctilio introduced to northeastern North America were different from the woodwasp strains in Australia. This observation potentially explained why the Deladenus sp. nematode strain currently in N. America does not sufficiently sterilize these wasps.  A project is underway to determine if a native nematode, D. proximus, can sterilize the N. American S. noctilio.  

Several research papers generated during this project showed that the microsclerotia of Metarhizium brunneum incorporated into a hydromulch formulation (mixture of wheat straw, a xanthan tackifer and water) and sprayed onto the trunks of trees could reduce Asian longhorn beetle, Anoplophora glabripennis, fecundity and produce significant mortality. Success of this mycoinsecticide treatment was directly related to the amount of rainfall and moisture available during the application of the product. Ongoing research is attempting to elucidate other formulations that can obtain better field persistence and ease of application for prophylactic buffer zone treatments of urban street trees infested with Asian longhorn beetles. 

Scientists with the Illinois Natural History Survey worked to identify and manage microsporidian pathogens of beneficial beetles used for classical biological control of hemlock woolly adelgid (HWA) in forests. Six species of microsporidia were isolated from four beetle species in laboratory colonies including two released species and two that remain in quarantine. Three microsporidian species destroyed colonies and aborted release programs (Solter et al., 2011). Information to mitigate microsporidia from mass rearing facilities and future releases of beetles was distributed to collaborating institutions.

Rutgers University researchers reported combinations of entomopathogenic nematodes and the chemical insecticide imidacloprid provided additive control of annual bluegrass weevil (ABW) larvae in pyrethroid-susceptible and -resistant populations on golf course fairways.  Entomopathogenic nematodes were similarly effective against ABW larvae in both pyrethroid-susceptible and -resistant populations.  Against pyrethroid-resistant ABW adults, the entomopathogenic fungus, B. bassiana (GHA) strain and the pyrethroid bifenthrin were ineffective, but combinations of B. bassiana and bifenthrin interacted synergistically, providing 70-84% control.

University of Florida and USDA-ARS Gainesville, FL scientists characterized the replication of the Musca domestica salivary gland hypertrophy virus (MdSGHV) in adult stable flies, Stomoxys calcitrans. This work showed that this virus, although not causing gland hypertrophy, did sterilize female flies. 

Researchers from the University of Maine and USDA-ARS, Ithaca, NY isolated and described a new species of fungal pathogen, Orphiocordyceps (Hirsutella) myrmicarum, from the invasive, stinging European fire ant, Myrmica rubra.  In addition, working with University of Arizona researchers, nematode populations from this invasive ant were identified to be members of the family Diplogasteridae belonging to the genus Pristionchus, specifically the species P. entomophagus, which has previously been found in association with scarab beetles. This represented a new host relationship, and its virulence against an introduced species is noteworthy and warrants further study as a potential management tool.

Nylanderia fulva virus1 (NfV-1), the first virus from the invasive, tawny crazy ant, Nylanderia fulva, was identified and characterized by USDA-ARS Gainesville, FL scientists.  NfV-1was not detected in limited samples of other Nylanderia species or closely related ant species and is a potential biocontrol.

A collaborative biocontrol project between USDA-ARS Gainesville, FL and the Coachella Valley Mosquito and Vector Control District released and established red imported fire ant, Solenopsis invicta, pathogens Kneallhazia solenopsae and Solenopsis invicta virus-3 (SINV-3) in Palm Desert, CA.  K. solenopsae was found to be established in other areas of the Coachella Valley.  SINV-3 is new to the Coachella Valley red imported fire ant populations and is spreading at the release sites.  These introductions are one component of IPM for fire ants in a unique urban desert environment.

Objectives

1. To study and improve microbial control options in IPM strategies for: a. large acreage crops (alfalfa, corn, dry beans, potatoes, and small grains) b. orchard systems (fruits and nuts) c. small fruits and vegetables (blackberries, blueberries, raspberries, strawberries, and vegetables) d. urban and natural landscapes, rangelands, and nurseries.
   Comments: This single objective encompasses four distinct projects based upon agricultural system and environment
2. To promote information transfer and microbial control options to IPM practitioners through an annual symposium event during the annual meetings of the Entomological Society of America (ESA), addition of the microbial control section to the topics presented at the ESA meetings, conduct extension events specific to microbial control, and offer opportunities for new collaborations and multi-state project evaluation.
   Comments: This objective includes a formal outreach and evaluation process to refine and improve the direction of the research projects and expand the outcomes of the work.

Methods

General Approach Across Projects (Objectives)

Building upon the research accomplishments from the previous project, research will elucidate basic biology and ecology of entomopathogens and their multipurpose use in crop production and protection. The proposed research and outreach will enhance implementation of microbial control in IPM systems.

Following general scientific research procedures, laboratory, greenhouse, and field research will evaluate the potential of entomopathogens as effective alternatives to chemical pesticides, important options in IPM programs, and enhancers of plant growth and health.  There is a need for operational scale field evaluation of entomopathogens to determine how they can be integrated into IPM programs that are acceptable to growers.  Studies to evaluate the efficacy of entomopathogens individually and in combination with each other or with botanical and chemical pesticides will be conducted against endemic and invasive pests.

Enhanced implementation of microbial control in diverse systems will be achieved in a multi-faceted approach. Entomopathogen strain improvement techniques will be implemented to enhance efficacy. Efficacy will also be improved by developing novel application techniques and optimizing parameters such as application rates and timing. Efforts will include conservation, classical introduction, and inoculative or inundative approaches to biocontrol.

Research will be directed toward understanding fundamental entomopathogen biology and ecology and avenues to improve their efficacy by modifying agricultural practices.  For example, recent studies suggest that entomopathogenic fungi antagonize plant pathogens, impact arthropod pests through endophytic colonization, and promote plant growth by forming a mycorrhiza-like relationship with plant roots (Parsa et al., 2013).  Entomopathogen-based metabolites also appear to have potential as biopesticides (Orozco et al., 2016; Sbaraini et al., 2016).  Among the subprojects, the role of entomopathogens will be evaluated as pathogens of arthropods, antagonists of plant pathogens, plant growth promoters, endophytes, or producers of toxic metabolites.

The following specific projects will identify key pests and develop strategies to improve microbial control integration in IPM programs for field crops, orchards, as well as, horticultural, urban, and natural environments.   

Objective 1a. Large acreage crops

Research on microbial control of insect pests infesting major acreage crops has culminated in the development of novel pest management technologies.  For this proposal, we define major acreage crops to generally include commodity grain crops and forage crops along with many common food crops under commercial agricultural production, such as potatoes and dry beans.  Two of the most noteworthy historical technologies were the development of transgenic Bt-crops for pest control and discovery of new pesticides from microbial fermentation. Both technologies have been successful in providing control of arthropod pests in several cropping systems.  Successful implementation of microbial control for major acreage commodities offers substantial reward resulting in the reduction of chemical pesticide applications.  Unfortunately, large scale agricultural production imposes economic restrictions on costs for pest control, often precluding applications of relatively expensive biological pesticides.  Successful implementation of microbial control against large acreage crops continues to require innovative and specialized technology advancement and application.

Discoveries of new entomopathogens, developing more efficacious strains of microbial agents, more efficient production techniques, and improving application methodologies within existing IPM continue to provide opportunities for adoption of microbial-based biological control for large acreage crops. New technologies include: fermentation techniques that produce novel fungal structures (microsclerotia [Jaronski and Jackson, 2008] or blastospores [Mascarin et al., 2016]) for application to soil; formulations such as alginate beads or hydro-mulch containing natural products to protect microbes from environmental degradation; new pathogens and isolates of known pathogens with better virulence to native and exotic insect pests; and integration protocols of entomopathogens into cropping systems. 

Specific research projects that will be continued focus on several weevil  pests as targets for microbial control.  Weevils are a large and diverse group of insects, which includes a number of economically important pest species.  For example, the alfalfa weevil, Hypera postica,  causes damage to alfalfa early in the growing season.  A variety of biorational pesticides are active against the damage-causing larval stage when evaluated under laboratory conditions (Reddy et al., 2016).  This life stage also may be susceptible to traditional foliar spray applications in the field if the treatments are timely.  By contrast, the sweet potato weevil, Cylas formicarius, is a global pest that damages the sweet potato (roots) in the soil environment.  Although susceptible to a variety of bacterial, fungal, and nematode agents, specialized applications may be required to control this pest and prevent crop damage.  The cowpea weevil, Callosobruchus maculatus, is another unique pest causing plant damage in the field followed by the potential to cause additional damage to post-harvested seeds while in storage.  Controlling field populations of this pest reduces damage to seeds during storage.  Potential management strategies for cowpea weevil will focus on in-field applications of entomopathogenic fungi and nematodes; combinations of microbial and chemical pesticides will also be explored.  Diapausing larvae of the wheat stem sawfly, Cephus cinctus, are susceptible to infection by endophytic strains of entomopathogenic Metarhizium and Beauveria fungi.  Basic and applied research are expected to elucidate plant/microbe/insect interactions for the development of these endophytes to provide plant protection. 

Another coleopteran pest, the wireworm complex continues to damage small grains and potatoes in the western high plains.  Planting time applications of entomopathogens as granules or seed coatings will be evaluated for efficacy and economics of pest management under field conditions. 

Diapausing larvae of the wheat stem sawfly, Cephus cinctus, a major hymenopteran pest of spring and winter wheat, are susceptible to infection by endophytic strains of entomopathogenic Metarhizium and Beauveria fungi.  Basic and applied research is expected to elucidate critical plant/microbe/insect interactions for the development of these endophytes to provide plant protection for the wheat farmer.

Collaborating Institutions: USDA-ARS, Sidney, MT, Byron, GA, and Peoria, IL; Montana State University, Conrad, MT; University of Georgia, Athens, GA.

Objective 1b. Orchard systems

A number of key orchard pests have been identified as targets for microbial control. Varying levels of farm-scale adoption with biocontrol strategies have been accomplished against these pests. Future work will included advanced studies for improving microbial control against these important pests.

In stone fruits, the peachtree borer is a highly attractive target for entomopathogenic nematodes, particularly due to the pending removal of chlorpyrifos (the standard chemical used against this pest).  The pest attacks trees at the base and bores into the roots. Current research indicates a nematode, S. carpocapsae, can control peachtree borer curatively or preventatively in an economically feasible approach (e.g., approximately $20.00 per acre).  New research will be implemented to optimize nematode application rates and timing for peachtree borer control and also to determine other simultaneous benefits of nematode application such as suppression of root-feeding weevils residing in stone fruit orchards.

Another key pest in stone fruits is the lesser peachtree borer, which attacks the tree aboveground.  The use of entomopathogenic nematodes on plant parts aboveground is generally not feasible due to environmental sensitivity of the nematodes; yet use of a fire-gel (Barricade®) formulation allows for effective application of the nematodes for lesser peachtree borer control (equivalent levels of control compared with chlorpyrifos). Additional research will focus on optimizing Barricade or other similar products / formulations for economical control of lesser peachtree borer. This method also will be evaluated against other borer insects of economic importance such as dogwood borer, shot hole borers, and the roundheaded appletree borer.

Polyphagous shot hole borer (PSHB), Euwallacea sp., is a new beetle pest in Southern California, which tunnels into plant material and transports fungi, Fusarium euwallaceae and Graphium sp., in a variety of landscape and horticultural trees that include avocado, California sycamore, coast live oak, and Japanese maple.  Fungal infection causes Fusarium dieback.  PSHB was found susceptible to B. bassiana in preliminary studies and additional research using a fire-gel to improve the environmental persistence of the fungus would be useful in managing PSHB.

Plum curculio, Conotrachelus nenuphar, is a key pest of stone and pome fruits. The insects attacks fruit directly.  Entomopathogenic nematodes have been shown to be highly effective in killing ground-dwelling stages of the pest (before adults emerge). An integrated trap-tree system has been developed to attract weevils to several trees (intentional targets) per hectare.  An adulticide is sprayed on the canopy for initial control and nematodes are used to kill remaining plum curculio below ground and prevent further movement to the interior of the orchard.  Research will be implemented to optimize application parameters in the novel sentinel tree approach and expand the method to other crops (so far it has only been tested in apples yet it has potential in other crops such as peaches, plums, pears, etc.).

Research will be expanded to develop microbial control programs for pecan weevil (a key pecan pest).  Grandevo® (C. subtsugae) application rates and timing will be optimized and integrated use of entomopathogenic nematodes and fungi for weevil hotspots will be incorporated. This research has been supported by funding from a USDA-NIFA Organic Transitions grant.

The citrus weevil, Diaprepes abbreviatus, is a major pest of Florida citrus; the insect feeds on roots and can kill trees. Florida citrus is threatened due to greening disease and D. abbreviatus exacerbates the situation. The pest has also spread to citrus in Texas and California. Entomopathogenic nematodes can provide high levels of control against D. abbreviatus. Research will be implemented to optimize nematode species effects and efficacy while integrating into new management plans that have been initiated to counter the spread of greening disease.  Research will also be conducted to develop the use of entomopathogenic nematodes for D. abbreviatus control in new crops that are expanding in Florida due to the loss of citrus (e.g., peaches).

In addition, a Bacillus thuringiensis galleriae SDS-502, possessing a new Cry protein with activity against Scarabeidae, Chrysomelidae, and Curculionidae, has been recently commercialized.  Commercial emphasis is being placed by the registrant on beetle pests of managed turf (see below). Efficacy against foliar-feeding weevils, such as alfalfa weevil, has been poorly documented, however, nor have IPM approaches using this microorganism been developed. In Northern Plains alfalfa effort will be made to integrate this agent with weevil parasitoids and cultural practices.

The spread of Asian Citrus Psvillid, Diaphorina citri, the vector of Candidatus Liberobacter, causing citrus greening, to new citrus orchard areas outside Florida, has generated research efforts to identify entomopathogenic fungi more efficacious than the current commercial products. An ARS-APHIS cooperative screening program has been established in Mission, TX to evaluate foreign commercial fungi as well as identify novel domestic and non-indigenous fungus strains in laboratory bioassays, as a prelude to field evaluation of the best candidates in the Rio Grande Valley. 

Collaborating Institutions: USDA-ARS, Byron, GA, Kearneysville, WV; University of California Cooperative Extension, Southern and Coastal California counties; University of California, Riverside, CA; University of Georgia, Athens, GA; University of Florida, Gainesville, FL; Montana State University Extension Service, Conrad MT; USDA-ARS, Sidney MT; USDA APHIS CPHST, Mission TX

Objective 1c. Small fruits and vegetables

A variety of small fruits and vegetables are important commercial crops in California with a crop value of several billion dollars.  Several arthropod pests attack these crops causing economic yield losses.  In only limited situations where biological control is possible by the release of commercially available natural enemies, producers typically rely on chemical pesticides.  Substantial quantities of several insecticides and acaricides are applied annually to California crops (CDPR, 2016).  Some important pests of blueberry include masked chafer white grubs, Cyclocephala hirta and C. longula; spotted wing drosophila, Drosophila suzukii; and citrus thrips, Scirtothrips citri. Spotted wing drosophila, twospotted spider mite, Tetranychus urticae; western flower thrips, Frankliniella occidentalis; lygus bugs, Lygus hesperus and L. lineolaris; red berry mite, Acalitus essigi; and broad mite, Polyphagotarsonemus latus; are important pests in caneberries.  The western tarnished plant bug, L. Hesperus; greenhouse whitefly, Trialeurodes vaporariorum; twospotted spider mite; and multiple species of Lepidopteran larvae are pests of strawberry.  The invasive Bagrada bug, Bagrada hilaris; green peach aphid, Myzus persicae; cabbage aphid, Brevicoryne brassicae; cabbage maggot, Delia radicum; are primary pests on cole crops.  Western flower thrips are important pests on lettuce.  Similar pest problems exist across the US on small fruits and vegetable crops.

While these pests are susceptible to a variety of entomopathogens, microbial control is not widely considered as a tool in an IPM strategy, especially in conventional agriculture.  Several studies have shown the potential of microbial control in small fruits and vegetables (Klick and Seagraves, 2015; 2016; Dara, 2016).  Follow up surveys conducted after extension meetings and responses from producers for publications related to microbial control indicate considerable interest.  Preference of consumers for organic products in sustainable systems for fruits and vegetables. 

Studies conducted in California indicate a positive impact of entomopathogenic fungi in promoting plant growth and health as well as antagonizing plant pathogens (Dara, 2013; Dara et al. 2016 a & b).  More studies are needed to understand the non-traditional role of entomopathogens, which can enhance their use in agriculture.  Multiple studies will be conducted in the previously mentioned crops.  The work plan will include: 1) evaluating the efficacy of entomopathogens alone and in combination with other control options against different arthropod pests to identify avenues to incorporate microbial control in small fruit and vegetable IPM in organic and conventional agriculture in California;  2) exploring the endophytic and mycorrhiza-like potential of entomopathogens in promoting plant health, growth, yield, and quality, and their ability to antagonize plant pathogens; and 3) extending training and guidance in microbial control to facilitate grower adoption.

Collaborating Institutions: University of California Cooperative Extension, Coastal California Counties; Driscoll’s, Coastal and Central California Counties.

Objective 1d. Urban and natural landscapes, rangelands, and nurseries

Invasive ants are a growing concern throughout the world, because of the broad diversity of habitats in which they can establish, thrive, and eventually dominate.  Often, they have cryptic, smoldering populations that slowly increase, until their populations explode. By this time, the invaders are too widespread to eradicate, and too expensive or logistically impossible to regionally suppress in natural or conservation lands, and even in urban landscapes.  Release from natural enemies is hypothesized to be a major factor in dominance of invasive ant species (Porter et al., 1997).   Biological control with entomopathogens is considered to be one of the few, if not the only, sustainable strategy for regional suppression of invasive ants.  Advances in metagenomics and sequencing have facilitated the discovery of pathogens in invasive ants such as the red imported fire ant, Solenopsis invicta, the tawny crazy ant, Nylanderia fulva, and the Argentine ant, Linepithema humile, (Valles et al., 2004; 2012; Sébastien et al., 2015). While new pathogens have been discovered, their biology and their impact on invasive ant colonies and populations need to be determined.  New fire ant viruses (e.g. SINV-4) have been recently found and will be further characterized. The host specificity of Nylanderia fulva virus-1 as well as it effect on queens will be assessed. The latter is of particular interest due to the ongoing spread of tawny crazy ants and limited control measures.

Turfgrass areas cover about 20 million ha in the USA and the size of the turfgrass industry is estimated at $40 billion per year.  Home owner lawns represent the largest part of the total turf area (66%). Golf courses only represent about 2% of the total area covered by turfgrasses in the USA, but, due to their much higher maintenance and use intensity, contribute about 20% to the total economic impact.  Many different types of insect pests can cause damage to different turfgrass areas including white grubs , mole crickets, lepidopteran larvae (cutworms, armyworms, sod webworms), weevils (billbugs, annual bluegrass weevil), crane flies, and many others.  Various entomopathogens have provided satisfactory control of several of these pests (Koppenhöfer et al., 2015; Koppenhöfer and Wu, 2017), but to increase the use of entomopathogens their efficacy and ease of use needs to be further improved and their potential for long-term pest suppression further exploited.  Changing attitudes in consumers (e.g., increasing demand for organic lawn care) and local or statewide legislation (school IPM programs) will also increase the need for effective entomopathogen-based products.  The wide-spread resistance to multiple types of insecticides in the annual bluegrass weevil for example (McGraw and Koppenhöfer, 2017), should increase the demand for alternatives to synthetic insecticides on golf courses.  New pathogen species/strains will be evaluated against white grubs, lepidopteran larvae, and annual bluegrass weevil adults and larvae in split applications, species combinations, and potentially synergistic combinations of nematodes with other control agents to improve control of these pests. Promising combinations will be tested for long-term pest suppression.  Of immediate interest are newer strains of Bt (i.e. Bt galleriae SDS-502) and microsclerotia-based formulations of M. brunneum F52 strain, as well as combinations with hydrogels for annual bluegrass weevil management (adults and larvae).  These pathogens and newly developed or isolated pathogens also will be explored for the management of other turfgrass pests including white grubs and lepidopteran larvae.

Rangelands are a uniquely diverse habitat that can benefit greatly through increased productivity from targeted applications of microbial control agents.  Novel formulations that provide UV  protection for fungal spores show promise for improving the microbial control of rangeland grasshoppers, using these agents.  Research will continue from the previous project to field test candidate fungi, identified in a past ARS-APHIS-Utah State project, in combination with the novel formulations against grasshopper populations on rangelend, . A novel locust-active Bt has been recently identified by Chinese researchers. Effort will be made to obtain this Bt for field evaluation, as well as to discover native Bt with similar activity, using published genetic information from the Chinese patent.

Thrips are among the most ubiquitous insect pests infesting ornamental and vegetable plants in the southern United States (Parker et al., 2013). In addition to direct damage, several thrips vector plants viruses, which cumulatively cost millions of dollars annually in lost production and pest control costs. For example, annual losses from thrips outbreaks in peanut were estimated at over $100 million in Georgia alone (Pearce, 2005). Work at Texas A&M University starting in 2017 will focus on integrated thrips management in ornamental and vegetable plants, with a major focus on the use of entomopathogens and other biopesticides. Several candidate agents have already been identified, including parasitic nematodes, and fungi (Arthurs and Heinz, 2002; 2003; Arthurs et al., 2013; Aristizábal et al., 2016). It will be important to screen commercial biopesticides for activity against these thrips pests. Species such as Frankliniella occidentalis [a vector of plant viruses known to track global trade routes of ornamental plants and other crops (Gilbertson et al., 2015)] are known to rapidly develop resistance against a limited number of effective chemical insecticides.

Ongoing and future projects toward the microbial control of pests in urban environments, natural landscapes, and plant nurseries include: 1) Characterizing the effects of recently discovered entomopathogens of invasive pests at the individual and population levels; 2) Determining host specificity of recently discovered entomopathogens of invasive pests; 3) Evaluating novel formulations and/or application techniques of microbial insecticides; and 4) Incorporating microbial biocontrol agents or microbial insecticide into IPM programs.

Collaborating Institutions: Cornell University, Ithaca, NY; University of Maine, Orono, ME; USDA-ARS, Gainesville, FL; Rutgers University, New Brunswick, NJ; Texas A&M, College Station, TX; USDA-ARS Sidney MT; USDA APHIS CPHST, Phoenix AZ.

Objective 2. Microbial control outreach

The workgroup will continue to hold the annual meeting in conjunction with the ESA national meetings and encourage participation from microbial control researchers from all universities, federal agencies, and private industry.  Grant development opportunities from USDA - NIFA and other funding agencies will be presented at the meeting encouraging members to develop collaborative projects.  Participants in the annaul meeting and formal symposium will be surveyed to evaluate the progress of the projects in this multi-state effort, make necessary changes to the approaches in achieving objectives, and forge new collaborations.  The microbial control symposia at the ESA meetings have been very successful with relatively broad attendance.  The workgroup solicits, discusses, and selects relevant current topics relative to the multi-state project.   Chairs invite experts from US and other countries to present on these topics and discuss the results of the current proejct.   The Entomological Socitey of America (ESA) has been supportive of the workgroup by offering a venue for the annual meeting and providing travel assistance to one or more of the invited symposium speakers.  These efforts have caused ESA to consider offering a microbial control category to the the list of topics presented at the annual meetings, which would give more visibility to the project.   To improve the outreach of the multi-state project, extension events specific to microbial control will also be conducted in one or more key areas fo the US each year.  Workgroup members and other experts will present new developments in applied microbial control aspects at these events with the objective of educating growers, pest control advisors, and IPM practitioners.

Collaborating Institutions: USDA-ARS, Sidney, MT, Byron, GA, and Peoria, IL; Montana State University, Conrad, MT; University of Georgia, Athens, GA; Cornell University, Ithaca, NY; University of Maine, Orono, ME; USDA-ARS, Gainesville, FL; Rutgers University, New Brunswick, NJ; Texas A&M, College Station, TX; USDA-ARS Sidney MT; USDA APHIS CPHST, Phoenix AZ; University of California Cooperative Extension, Coastal California Counties; Driscoll’s, Coastal and Central California Counties; USDA-ARS, Byron, GA, Kearneysville, WV; University of California Cooperative Extension, Southern and Coastal California counties; University of California, Riverside, CA; University of Georgia, Athens, GA; University of Florida, Gainesville, FL; Montana State University Extension Service, Conrad MT; USDA-ARS, Sidney MT; USDA APHIS CPHST, Mission TX.

 

Measurement of Progress and Results

Outputs

• Improved regional collaboration leading to new and enhanced microbial control tools, application strategies, and delivery mechanisms in the respective individual projects
• Scientific publications including peer-reviewed journal articles, books, or book chapters.
• Extension outreach and stakeholder-friendly publications to improve the knowledge and implementation of microbial control.
• Annual meeting of the workgroup members in conjunction with the Entomological Society of America (ESA) annual meetings.
• Microbial information exchange symposia at ESA annual meetings organized by the workgroup members.
• Annual reporting that includes the summary of research achievements, publication lists, tabulation of extension related activities related to this project.
• Development of a website to publish specific recommendations from workshops.

Outcomes or Projected Impacts

• Improved use of microbial control options in conventional agriculture.
• Reduced impact on non-target organisms and the environment, and protection of human health due to decreased use of chemical pesticides.
• Improvements in food security due to the development of alternative pest management for safer foods and added protection against new agricultural threats (e.g., invasive pests). iv. Increased market for biopesticides based on microbial control agents.
• Sustaining and increasing market opportunities for biopesticides based on microbial control agents.

Milestones

(0):Project 1a: 1) Evaluate commercial and experimental applications of microbial agents as conventional sprays for control of emerging or invasive insect pests of crops (Yrs 1-5 Field studies ongoing; Yr 5 milestone achieved). 2) Demonstrate control efficacy of planting time application (as granules or seed coating) for control of early season soil borne insect pests (Yrs 2-4 Field studies ongoing; Yr 5 milestone achieved.). 3) Optimize fermentation production of novel fungal propagules (microsclerotia or blastospores) and develop formulations to provide storage stability and easy application to control target insect pests. (Yrs 1-3 Lab studies ongoing; Yrs 4-5 Field studies ongoing;Yr 5 milestone achieved).

(0):Project 1b: 1) Improved methods for control of peachtree borer (Yrs 1-3 Lab/Field/Greenhouse studies ongoing; Yrs. 4-5 Field studies ongoing). 2) Investigation of improved formulations for nematodes (Yrs 1-2 Lab/Field/Greenhouse studies ongoing; Yrs. 3-5 Field studies ongoing). 3) Advanced methods for pecan weevil microbial control (Yrs 1-2 Lab/Field/Greenhouse studies ongoing; Yrs. 3-5 Field studies ongoing). 4) Implementation of sentinel tree approach for plum curculio (Yrs 1-2 Lab/Field/Greenhouse studies ongoing; Yrs. 3-5 Field studies ongoing). 5) Optimization of citrus weevil control using microbials (Yrs 1-2 Lab/Field/Greenhouse studies ongoing; Yrs. 3-5 Field studies ongoing). 6) Evaluation of microbial control for polyphagous shot hole borer (Yrs 1-2 Lab/Field studies ongoing; Yr 3 Milestone achieved).

(0):Project 1c: 1) Exploring the endophytic and mycorrhiza-like impact of entomopathogenic fungi on crop growth, pests, and diseases (Yrs 1-3 Lab/Field/Greenhouse studies ongoing; Yr 4 Milestone achieved). 2) Evaluation of microbial control tools and developing IPM strategies (Yrs 1-3 Field studies ongoing; Yr 4 Milestone achieved). 3)Outreach through meetings and publications (Yrs 1-5 Milestone achieved with annual meetings).

(0):Project 1d: 1)Characterizing the effects of recently discovered entomopathogens of invasive pests (Yrs 1-2 Lab studies ongoing; Yr 3-4 Lab/Field studies ongoing; Yr 5 Milestone achieved). 2) Determine host specificity of recently discovered entomopathogens of invasive pests. (Yrs 2-3 Lab studies ongoing; Yr 4 Milestone achieved). 3) Evaluate novel formulations and/or application techniques of microbial insecticides. (Yrs 1-4 Lab/Field/Greenhouse studies ongoing; Yr 5 Milestone achieved). 4) Incorporate microbial biocontrol agents or microbial insecticide into IPM programs. (Yrs 1-4 Field studies ongoing; Yr 5 Milestone achieved).

(0):Objective 2: 1) Organizing microbial control symposium at the Entomological Society of America annual meetings (Yrs 1-5). 2) Explore opportunities to conduct microbial control workshops or outreach events in different regions (Yrs 2-4).

Projected Participation

View Appendix E: Participation

Outreach Plan

This project will provide educational material for: 1) Entomology colleagues via symposia at national meetings, and refereed research publications, books and book chapters; and 2) Extension personnel and growers via participation in annual project meetings, trade shows, field days, presentations, trade journal articles and factsheets, and production of published and web-based resources on the use of entomopathogens in pest management. Products from this project have applications for both conventional and organic producers, resource managers (e.g. forests), and urban clientele.

Organic growers in particular have typically been under-served by research and extension activities, which have tended to focus on development of chemically-based pest management programs. Additionally, outreach will also extend to numerous institutions some of the project participants have ties to these colleges (e.g., through adjunct professorships) and populations sectors they serve. Today, research and outreach efforts emphasize increasing the implementation of IPM strategies on farms, forests and urban landscapes, with biological controls forming the first line of defense against pests. This project enhances our ability to achieve this goal on a broad range of agricultural commodities and other managed ecosystems.

Organization/Governance

Organization:

Project administration structure includes the following positions: Chair, Vice-Chair, Member-at-Large, and Secretary. Each position is filled for a two-year term, at which time a new Member-at-Large and a new Secretary are elected at the annual meeting. The retiring Member-at-Large replaces the Vice-Chair, and the retiring Vice-Chair replaces the Chair. The Chair is coordinates selected aspects of project, the Vice-Chair and Member-at-Large assist the Chair and serve in his/her place when the Chair is unavailable. The Chair can appoint other ad-hoc officers as needed. The Secretary’s primary responsibility is to compile annual reports and meeting minutes.

Current Officers:

Chair: Surendra K. Dara, University of California Cooperative Extension, San Luis Obispo, CA.

Vice-Chair: Robert Behle, USDA-ARS, Peoria, IL.

Member-at-Large: Jimmy Klick, Driscoll’s, Oxnard, CA

Secretary: Tarryn Goble, BioForest, Sault Sainte Marie, Canada

Project Chairs:  

      1. Robert Behle, USDA-ARS-Peoria, IL                                      

      2. David Shapiro-Ilan, USDA-ARS, Byron, GA

      3. Surendra Dara, UCCE, San Luis Obispo, CA and Jimmy Klick, Driscoll’s, Oxnard, CA

      4. David Oi (USDA-ARS, Gainesville, FL) and Steve Arthurs (Texas A&M, TX)

Projected Participation:

Appendix E of March 1, 2016 shows 27 researcher participants from 17 states AL, AR, AZ, CA, CT, FL, IL, ME, MT, NJ, ND, NJ, NY, OH, PA, TN VT, and WA along with three  USDA researchers from GA, IL, and MT. Additionally, in the previous project, we enjoyed the collaboration and occasional attendance at meetings of non-official participants from various state and USDA institutions, and we project that such outside participation will be similar in the new project. This current project has strong support from the industry partners including participation from a Canadian biopesticide company.  We will continue to organize microbial control symposia at ESA annual meetings and invite participation/collaboration from members of the Biopesticide Industry Alliance and the Society for Invertebrate Pathology.

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Attachments

Land Grant Participating States/Institutions

AZ, CA, FL, MA, ME, MI, MT, NJ, NY, OR, TX, VT

Non Land Grant Participating States/Institutions

Brigham Young University, USDA ARS, USDA-ARS, USDA-ARS/Florida, USDA-ARS/MT