Research Project: Biological Control for Management of Invasive Pest Management, Emphasizing Brown Marmorated Stink Bug, Spotted Wing Drosophila and other Invasive Insect Pests of Crops

Location: Beneficial Insects Introduction Research Unit

2021 Annual Report

Objectives
Objective 1: Discover, identify, characterize the biology, evaluate the efficacy (using native-range studies and host-range specificity testing in quarantine), and determine the physiological, behavioral, and ecological basis of the host range of exotic predators and parasitoids as classical biological control agents of invasive arthropod pests of agricultural crops, with a focus on BMSB and SWD. [NP304, C1, PS1A; C3, PS3A, 3B and 3C] Sub-objective 1A: Discovery Sub-objective 1B: Characterization and identification Sub-objective 1C: Evaluation and risk assessment Objective 2: Improve understanding of biological and environmental factors and processes that influence the successful establishment of introduced biological control agents, such as climate adaptation, release methodologies, genetic variation in source and founder populations, using natural enemies of current target pests as model systems. [NP304, C1, PS1A; C3, PS3A, 3B and 3C] Sub-objective 2A: Conduct laboratory studies of basic biology and behavior to enable continuous laboratory rearing, including mass production when needed for eventual field releases. Sub-objective 2B: Conduct laboratory and field studies of selected biological traits and ecological requirements that influence the establishment and efficacy of the target biological control agents under field conditions. Objective 3: Prepare (with collaborators when appropriate) petitions to regulatory agencies for field release of candidate agents, conduct field releases for establishment of new agents, and monitor and evaluate the impact of the natural enemies on target populations and on non-target species in the field. Sub-objective 3A: Develop and submit a petition for release that describes the importance of the target pest and the efficacy and safety of the candidate biocontrol agent; and participate in the regulatory decision process as needed. Sub-objective 3B: Conduct field releases for establishment of new biological control agents and monitor and evaluate the impact of these natural enemies on target pest populations and on non-target species in the field. [NP304, C1, PS1A; C3, PS3A 3B and 3C]

Approach
Classical (importation) biological control is a pest management technology that is environmentally safe and sustainable. This project focuses on discovery, evaluation, and establishment of classical biological control agents of selected agricultural pests in the U.S. Previous research continued into this project addresses as targets brown marmorated stink bug and spotted wing drosophila. New targets may be added at any time according to national need. To address objective (1) we will conduct foreign exploration in Asia and other regions as needed to discover, identify and evaluate the biology, ecology, and efficacy of exotic predators and parasitoids as classical biological control agents of the targeted pests. Agents discovered in exploration will be returned to our laboratory and identified using the best available morphological characters in conjunction with molecular sequence data, and evaluated in our quarantine facility for efficacy by measuring attack rates, reproductive output and development rates, and for host specificity by testing both close relatives to target hosts and progressively more distantly related species under choice and no-choice conditions. Objective (2) will address the role of various biological, behavioral and environmental factors such as climate and photoperiod or inherent genetic variability in determining establishment success, using parasitoids of current target pests as the model subjects. Research will be conducted in environmental growth chambers and, when feasible, with in-field experiments. To address objective (3) we will prepare petitions for field release of qualified candidate agents of all target pests determined to be both effective and safe, based on satisfactory results of evaluation studies. These will be submitted to technical advisory panels and APHIS, in collaboration with relevant project partners as necessary. Supplemental research will be conducted to provide additional information if requested by APHIS. Once permits are received we will participate with cooperators as needed in conducting releases and post-release monitoring of the natural enemies. Where possible the releases will be designed to compare different geographic populations or genetic accessions of the agent for differences in climate adaptation, efficacy or other behavioral characteristics.

Progress Report
Populations of the brown marmorated stink bug (H. HALYS) have been significant pests in soybeans, vegetables, nuts, and various tree fruits in the eastern and northwestern U.S. for the past decade. Their impact continues to grow in the southeastern, north north-central. Southwestern U.S. ARS Newark continued to provide technical support to cooperators across the U.S. for sentinel surveys to monitor parasitism of H. HALYS by resident native stinkbug parasitoids in different crop systems, including survey protocols. Annual Workshops are given in each year of this project for U.S. and foreign cooperators (Obj. 1B & 3B; annual Farm Bill awards) had to be postponed in FY21 due to COVID-19. During previous project cycles, field collections of TRISSOLCUS parasitoids of Asian stink bugs and a range of larval and pupal parasitoids of spotted wing drosophila, DROSOPHIA SUZUKII, were obtained from Asia for taxonomic and genetic studies (Obj. 1A,1B) in collaboration with ARS European Biological Control Laboratory (EBCL) and Systematic Entomology Laboratory (SEL) and a Florida state cooperator Non-Assistance Cooperative Agreement (NACA),58-8010-7-012, Taxonomic Studies on Scelionid Parasitoids of Pentatomid Stink Bugs with the Florida Department of Agriculture and Consumer Service and for host range and biological studies (Obj. 2A) in support of host range evaluations by numerous cooperators. Following up on a white paper prepared for the Office of National Programs (ONP) on the subject, exploration in China, Taiwan, South Korea, and Vietnam initiated in 2019 with the Animal and Plant Inspection Service (APHIS) and foreign cooperators was continued by Asian cooperators for natural enemies of roseau cane scale, NIPPONACLERDA BIWAKOENSIS, an invasive insect that has established along the U.S. Gulf Coast and which is killing large areas of roseau cane (PHRAGMITES reed), dense stands of which are important for reducing coastal and shipping channel erosion. U.S. cooperator exploration could not be pursued in 2021 for the second consecutive field season due to COVID-19 restrictions, but Farm Bill-funded NACAs were again put in place for native range research by cooperators. The parasitoid complex in each of the four Asian countries is being documented, and several new species have been found and are being described. Three of these are attentively present in the U.S. Gulf Coast, but others occur thus far only in Asia and could be potential biocontrol agents. Laboratory research on GANASPIS BRASILIENSIS, a larval-pupal parasitoid of the spotted wing drosophila DROSOPHILA SUZUKII, was continued in 2021 (Obj. 2B). Research continued on improving the artificial diet and rearing methods in order to support mass production of the parasitoid for anticipated field release with the expected APHIS approval of a Petition for Field Release later this summer or fall of 2021 (Obj. 3C). As a part of systematic evaluations of other candidate agents, the potential of the Asian parasitic wasp ASOBARA JAPONICA was also assessed (Log No. 374900). This wasp was able to attack and develop in fly larvae infesting cherry, blackberry and strawberry. It was most effective in attacking young fly larvae and on large host species. The host range of three candidate larval parasitoids was evaluated in quarantine host range studies (Log No. 375125 & 380010), identifying G. BRASILIENSIS as the preferred, most specific candidate for field release. Distribution data from our Asian explorations contributed to a new molecular voucher database for identification of DROSOPHILA parasitoids (Log No. 382406). Efforts have been initiated to receive new shipments from cooperators of several other geographic populations of G. BRASILIENSIS to compare with our population from southern China for genetic sequencing at Newark. Our NACA with Yunnan Academy of Agricultural Science (# 58-8010-0-002F) for field surveys and collections in .W.S.W. China has assisted with obtaining specimens for this objective. This information will inform our understanding of the parasitoid's host range and specificity. The potential for biological control of spotted wing drosophila was reviewed in a journal article (Log No. 377753) and book chapter (Log no. 375348). Research following up on an older project (biocontrol of olive fruit fly) examined the regional distributions and dominance of co-evolved parasitoids obtained during exploration for olive fruit fly parasitoids across Africa (Log No. 380529) and documented the influence of male behavior on female reproductive performance of a related tephritid parasitoid, DIACHASMIMORPHA TRYONI (Log No. 381279). The research was continued in the field and the laboratory to assess the potential impact of Asian TRISSOLCUS JAPONICUS on target and non-target species in the U.S. and to expand the regional distribution of an adventive population of T. JAPONICUS. This research addresses Objective 1. Sites of field releases throughout Delaware made during the previous two summers are being monitored to determine whether establishment occurred and whether any non-target species are being attacked; these are ongoing (Obj. 3B). Previous laboratory research on the behavioral response of the parasitoid TRISSOLCUS JAPONICUS to its host and to non-target kairomones (chemical footprints) was published (Log no. 370916) and has now been extended to the field with open-field releases at Newark with mass-reared parasitoids released into arrays of potted trees containing H. HALYS or P. MACULIVENTRIS egg masses, or applications of isolated kairomone components. In the earlier lab experiments, T. JAPONICUS remained the most extended amount of time on leaves that were contaminated with host chemical footprints. The results also showed that although T. JAPONICUS can detect the chemical footprints of the adult non-target spined soldier bug, they have a much stronger behavioral response to H. HALYS, and thus are likely to spend more time searching for stink bug eggs on plants contaminated by H. HALYS. Parasitoid response was examined in field trials to determine if host kairomones would increase the chances that parasitoids will discover host stink bug eggs under actual field conditions. In this year's field studies, these lab trends were repeated but with more variability due to the effects of environmental factors. Extracts of the kairomones that were isolated and identified in collaboration with ARS Invasive Insect Biocontrol and Behavior Laboratory (IIBBL) in Beltsville, Maryland, E-2-decenal and tridecane, are the major components of the BMSB kairomone that elicit a TRISSOLCUS response. Preliminary results shows that behavioral and ecological responses were moderate but may still reduce the potential non-target impact of this Asian parasitoid (Obj. 1C). Field surveys to monitor the status of stink bug natural enemies in North America and Europe detected the presence of the Asian hyperparasitoid Acroclisoides sinicus. Because hyperparasitoids attack the natural enemies of pests rather than the pests themselves, the adventive A. sinicus populations could eventually threaten the biological control of invasive and native stink bugs by reducing the impact of their natural enemies. Laboratory colonies of the hyperparasitoid were established by collaborators from specimens collected in Europe and the U.S. to investigate the biology of this species. This information will allow researchers to evaluate the potential spread and impact of the hyperparasitoid (Log no. 382359). Other collaborative research with Asian TRISSOLCUS species included laboratory studies of host range evaluation techniques that provide accurate results with simplified methods, (Log no. 374388) and rearing methodology to support large scale field releases (Log. no. 379410), a risk analysis for potential release of another Asian parasitoid, T. MITSUKURII (Log no. 382465) and a predictive CLIMEX model of the potential distribution of T. JAPONICUS and T. MITSUKURII (Log. no. 382535). Note that research on another target pest that was originally part of the past 5-year project, LYCORMA DELICATULA (spotted lanternfly) is now described in the annual report for project 8010-22000-031-00D. Incoming funds were received through subordinate projects 58-8080-7-002 , National Institute of Food and Agriculture/Specialty Crop Research Initiative (NIFA/SCRI, Management of Brown Marmorated Stink Bug (BMSB) in U.S. Specialty Crops), 60-8010-1-001, (NIFA/SCRI, for Management of DROSOPHILA SUZUKII), 8010-22000-033-25R, 60-8010-1-002, (University of California, for Biocontrol of D. SUZUKII), and several annual Farm Bill awards 60-8010-0-001for H. HALYS), and 60-8010-0-004for Roseau Cane Scale) that helped with the research discussed above. The overall impact of the research is that producers will have new biological control agents available that will help them manage key insect pests by reducing chemical pest management inputs, thereby maximizing profits and sustaining yield.

Accomplishments

Review Publications
Sabbatini Peverieri, G., Dieckhoff, C., Giovannini, L., Marianelli, L., Roversi, P., Hoelmer, K.A. 2020. Rearing Trissolcus japonicus and Trissolcus mitsukurii for biological control of Halyomorpha halys. Insects. 11(11). 787. 2020. https://doi.org/10.3390/insects11110787.
Giovannini, L., Sabbatini-Peverieri, G., Tillman, P.G., Hoelmer, K.A., Roversi, P. 2021. Reproductive and developmental biology of Acroclisoides sinicus, a hyperparasitoid of scelionid parasitoids. BMC Biology. 10(3): 229. https://doi.org/10.1093/ee/nvaa124.
Wang, X., Daane, K.M., Hoelmer, K.A., Lee, J.C. 2021. Biological control of spotted-wing drosophila - an update on promising agents. In: Garcia, F.R.M., editor. Drosophila suzukii Management. Cham, Switzerland: Springer. p. 143-167. https://doi.org/10.1007/978-3-030-62692-1_8.
Caron, V., Yonow, T., Paull, C., Talamas, E.J., Avila, G., Hoelmer, K.A. 2021. Preempting the arrival of the brown marmorated stink bug, Halyomorpha halys: biological control options for Australia. Insects. 12,581. https://doi.org/10.3390/insects12070581.
Yonow, T., Kriticos, D.J., Ota, N., Avila, G., Talamas, E.J., Hoelmer, K.A., Chen, H., Caron, V. 2021. Modelling the biocontrol potential of Trissolcus species for the brown marmorated stink bug, Halyomorpha halys Stål. Insects. 12, 581. https://doi.org/10.3390/insects12060491.
Xin, B., Zhang, Y., Wang, X., Cao, L., Hoelmer, K.A., Broadley, H.J., Gould, J.S. 2020. Exploratory survey of spotted lanternfly (Hemiptera: Fulgoridae) and its natural enemies in China. Environmental Entomology. https://doi.org/10.1093/ee/nvaa137.
Boyle S, Weber D., Hough-Goldstein J, Hoelmer KA. Parental host species affects behavior and parasitism by the pentatomid egg parasitoid Trissolcus japonicus (Hymenoptera: Scelionidae). Biological Control 149: 104324. 2020. https://doi.org/10.1016/j.biocontrol.2020.104324
Conti, E., Avila, G., Barratt, B., Cingolani, F., Colazza, S., Guarino, S., Hoelmer, K.A., Laumann, R., Maistrello, L., Martel, G., Peri, E., Rodriquez-Saona, C., Rondoni, G., Rostas, M., Roversi, P., Sforza, R., Tavella, L., Wajnberg, E. 2020. Biological control of invasive stink bugs: review of global state and future prospects. Entomologia Experimentalis et Applicata. 169: 28-51. 2020. https://doi.org/10.1111/eea.12967.
Sabbatini Peverieri, G., Boncompagni, L., Mazza, G., Paoli, F., Dapporto, L., Giovannini, L., Marianelli, L., Hoelmer, K.A., Roversi, P. 2021. Combining physiological host range, behavior and host characteristics for predictive risk analysis of Trissolcus japonicus. Journal of Pest Science. 94:1003–1016. https://doi.org/10.1007/s10340-020-01311-w.
Broadley, H.J., Gould, J.S., Wang, X., Hoelmer, K.A., Hickin, M., Sullivan, L., Elkinton, J.S. 2020. Life history and rearing of Anastatus orientalis (Hymenoptera: Eupelmidae), an egg parasitoid of the spotted lanternfly (Hemiptera: Fulgoridae). Environmental Entomology. 50(1), 2021, 28–35. https://doi.org/10.1093/ee/nvaa124.
Wang, X., Biondi, A., Nance, A.H., Zappalà, L., Hoelmer, K.A., Daane, K.M. 2020. Assessment of Asobara japonica as a potential biological control agent for the spotted wing drosophila, Drosophila suzukii. Entomologia Generalis. https://doi.org/10.1127/entomologia/2020/1100.
Wang, X., Lee, J.C., Daane, K.M., Buffington, M.L., Hoelmer, K.A. 2020. Biological control of Drosophila suzukii. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources. 15. Article 054. https://doi.org/10.1079/PAVSNNR202015054.
Wang, X., Walton, V.M., Hoelmer, K.A., Pickett, C.H., Blanchet, A., Straser, R.K., Kirk, A.A., Daane, K.M. 2021. Exploration for olive fruit fly parasitoids across Africa reveals regional distributions and dominance of closely associated parasitoids. Scientific Reports. 11: 6182. https://doi.org/10.1038/s41598-021-85253-y.
Lue, C., Buffington, M.L., Scheffer, S.J., Lewis, M.L., Driskell, A., Jandova, A., Kimura, M., Carton, Y., Kula, R.R., Schlenke, T., Mateos, M., Govind, S., Varaldi, J., Guerrieri, E., Giorgini, M., Wang, X., Hoelmer, K.A., Daane, K., Abram, P., Pardikes, N., Brown, J., Thierry, M., Poirie, M., Goldstein, P.Z., Miller, S., Jiggins, F., Tracey, A., Davis, J.S., Wertheim, B., Lewis, O.T., Leips, J., Lindsey, A., Staniczenko, P., Hrcek, J. 2021. DROP: Molecular voucher database for identification of Drosophila parasitoids. Molecular Ecology. 1-18. https://doi.org/10.1111/1755-0998.13435.
Daane, K.M., Wang, X., Hogg, B.N., Biondi, A. 2021. Potential host ranges of three Asian larval parasitoids of Drosophila suzukii. Journal of Pest Science. https://doi.org/10.1007/s10340-021-01368-1.
Ramadan, M.M., Wang, X. 2021. Male impact on female reproductive performance of the larval tephritid parasitoid Diachasmimorpha tryoni (Hymenoptera: Braconidae). Journal of Economic Entomology. https://doi.org/10.1093/jee/toab063.
Biondi, A., Wang, X., Daane, K.M. 2020. Host preference of three Asian larval parasitoids to closely related Drosophila species: implications for biological control of Drosophila suzukii. Journal of Pest Science. https://doi.org/10.1007/s10340-020-01272-0.
Malek, R., Kaser, J.M., Anfora, G., Ciolli, M., Khrimian, A., Weber, D.C., Hoelmer, K.A. 2021. Trissolcus japonicus foraging behavior: Implications for host preference and classical biological control. Biological Control. https://doi.org/10.1016/j.biocontrol.2021.104700 .