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

2024 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
This is the final report for the Project 8010-22000-033-000D which ended 6 March 2024. This project was consolidated with project 8010-22000-031-000D entitled “Biology, Ecology, Genetics, and Genomics of Introduced Species for Biological Control of Invasive and Other Insect Pests” to strengthen complementary research efforts in biological control of invasive and other insect pests. This project has fully met the major milestones: (1) a parasitoid from Asia, Trissolcus japonicus, was identified as the most effective natural enemy of the brown marmorated stink bug (BMSB) Halyomorpha halys. The efficacy and host specificity studies of T. japonicus have been completed to develop a petition for release this parasitoid. The wasp has already established itself accidentally, and its impact on BMSB populations is being assessed. (2) An Asian larval parasitoid Ganaspis kimorum has been successfully introduced for biological control of the spotted wing drosophila Drosophila suzukii. The wasp has been reared and distributed for field release in 15 U.S. states. Widespread distribution is expected to help it become established, with monitoring ongoing. (3) Surveys have discovered one major egg parasitoid Anastatus orientalis, and one major nymphal parasitoid Dryinus sinicus of the spotted lanternfly (SLF) Lycorma delicatula in China. Studies are underway to evaluate their effectiveness and host specificity for SLF control. In addition, the parasitoid complex 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 have been surveyed in China, Taiwan, South Korea and Vietnam in cooperation with APHIS and potential control agents are being evaluated. The spotted wing drosophila (SWD), Drosophila suzukii, native to Asia, has become widely established in the U.S., and is now a devastating pest of soft-skinned fruit crops. We have introduced an Asian larval SWD parasitoid Ganaspis kimorum and developed its rearing and field release and sampling protocols. As part of our involvement in an NIFA/SCRI project for SWD Management (8010-22000-031-088R), we reared and provided parental colonies of this parasitoid to 17 labs in 15 states across the U.S. for their rearing and releases since 2022. The number of released wasps during 2023 doubled from 2022, and the release continued in 2024. We also reared and provided wasps for release in three mid-Atlantic states. Research was also conducted to (1) characterize the genetic makeup and mating compatibility of several populations of G. kimorum that confirmed two cryptic species, (2) determine the compatibility of released and adventive populations of G. kimorum in Pacific Northwest and (3) ecological factors (e.g., habitats, host plants) affecting the efficiency and establishment of this parasitoid in the field (on-going). Other collaborative research included assessing native parasitoids attacking SWD in the southeastern US, population dynamics and parasitism of SWD in non-crop hosts, and compatibility of bioinsecticides with G. kimorum for enhanced integrated pest management of SWD. Parts of recent research results have been presented at the Delaware Invasive Species Council Annual Meeting (October 2023), ESA Annual Meeting (November 2023), North American SWD Biocontrol Working Group (November 2023), SWD biological control webinar (December 2023), and 27th International Congress of Entomology (August 2024). Incoming funds were also received through the FY24 USDA-APHIS PPA7721 Program (8010-22000-031-081I). Collaborative research was conducted through cooperative agreements with Yunnan Academy of Agricultural Science, China (8010-22000-031-085S), University of Delaware (8010-22000-031-097A), University of Maryland (8010-22000-031-098A) and Pennsylvania State University (8010-22000-031-099A). The spotted lanternfly (SLF) Lycorma delicatula is an invasive planthopper that is native to China but invaded Pennsylvania in 2014. Since then, SLF has spread rapidly to 20 neighboring states by 2024. It threatens the production of grapes and hops, tree fruits, and plant nurseries. Past surveys for native natural enemies in China have discovered one egg parasitoid Anastatus orientalis, and one nymphal parasitoid Dryinus sinicus. In addition, surveys in the eastern US have found a resident generalist egg parasitoid Anastatus reduvii attacking SLF. During fall 2023, we re-collected D. sinicus from China, and re-imported A. orientalis from APHIS PPQ Forest Pest Methods Laboratory (FPML) and collected A. reduvii in Delaware to re-establish colonies of all three parasitoids. We completed behavioral assays on the responses by A. orientalis to three non-target species: BMSB and Poblicia fuliginosa and Actias luna. A. orientalis showed significant interest towards SLF adult-exposed substrate, but no interest towards other species’ adult substrates. We provided several non-target stink bug species to FPML for host specificity tests on D. sinicus, investigated the foraging behavior of D. sinicus and developed its rearing methods. D. sinicus can attack all three instars of SLF nymphs; attacking the 1st instar is more likely leading to host feeding, attacking the 2nd instar is more likely leading to a successful oviposition, while attacking the 3rd instars resulted in a lower successful rate of oviposition or feeding. While studies are under the way to systematically evaluate the behavior, biology and ecology of these parasitoids, parts of the results were submitted for publication or presented at the 2024 ESA Eastern Branch Meeting, USDA SLF Group Seminars (January 2024) and 27th International Congress of Entomology (August 2024, Japan). Incoming funds were received through project 8010-22000-031-086R (NIFA/SCRI), and USDA-APHIS PPA7721 Program awards (8010-22000-031-073I, FY23; 8010-22000-031-094I, FY24). Collaborative research was conducted through cooperative agreements with Chinese Academy of Forestry (8010-22000-033-023S), University of Delaware (8010-22000-033-068A) and FPML. The brown marmorated stink bug (BMSB) Halyomorpha halys, native to Asia, has been a significant invasive pest of soybeans, vegetables, nut, and various tree fruits in the U.S. for the past decade. During previous years, we identified an Asian egg parasitoid Trissolcus japonicus as a major biological control agent for H. halys. The efficacy and host specificity studies of imported T. japonicus populations have been completed. Although adventive populations of T. japonicus have established in many locations the US, these populations may not be optimized to their locations. We thus continually analyzed host specificity test data to develop a petition to the North American Plant Protection Organization for release of the imported material that may be pre-adapted to BMSB or more suitable than the extant adventive populations. At the meantime, we also collected and analyzed genetic variation among different geographical populations of T. japonicus from China, the US, Canada, and Europe. These studies may inform future introductions (e.g., to increase genetic diversity of adventive populations). We currently maintain five other related stink bug species (Euschistus tristigmus, E. servus, Podisus maculiventris, Nezara viridula and Thyanta custator), many lines of T. japonicus collected from China, Japan, South Korea, and the Eastern US, and T. mitsukurii, T. curbtis, and A. reduvii. Studies are underway to quantify the effects of different host species on T. japonicus and other related egg parasitoids. Other collaborative research included evaluations of a newly discovered Asian Trissolcus species for the control of BMSB, and support of international collaborator programs for augmentative releases of T. japonicus in New Zealand. Some results will be presented at the 27th International Congress of Entomology in August 2024. In addition, other collaborative research included “Preemptive Biological Control of a High-Risk Invasive Longhorn Beetle” funded through a USDA-APHIS PPA7721 Program award (FY23) in cooperation with Seoul National university, South Korea (8010-22000-031-075A) and National Research Council, Italy (8010-22000-031-077A) and biological control of other invasive pests such as tephritid fruit flies and woodboring beetles.

Accomplishments
1. First widespread field releases of an introduced natural enemy against spotted wing drosophila. Spotted wing drosophila is an invasive Asian fly that has become a serious pest of small fruits and berries across the U.S. ARS scientists in Newark, Delaware, and collaborator at University of Caliofnria Berkeley identified a key Asian natural enemy of the fly, the parasitoid wasp Ganaspis kimorum. After extensive host range testing, a field release permit was authorized by USDA-APHIS. ARS scientists scaled up laboratory production of the wasp for distribution and field release by federal, state and university researchers in seventeen states since summer 2022 and continuing in 2023 and 2024. Widespread distribution is expected to facilitate rapid establishment of the wasp in the U.S., which will be monitored in the coming years.

Review Publications
Wang, X., Ramadan, M.M., Hoelmer, K.A. 2024. Biological Control Introductions Against Invasive Tephritid Fruit Flies (Diptera: Tephritidae) in the US: Achievements, Opportunities, and Challenges. Management of fruit flies in the Americas. 461–499. https://doi.org/10.1007/978-3-031-48608-1_17.
Giunti, G., Benelli, G., Campolo, O., Canale, A., Kapranas, A., Liedo, P., Meyer, M., Nestel, D., Ruiu, L., Scolari, F., Wang, X., Papadopoulos, N. 2023. Management of the Mediterranean fruit fly, Ceratitis capitata: past, present and future. Entomologia Generalis. 43:1241-1263. https://doi.org/10.1127/entomologia/2023/2136.
Giunti, G., Benelli, G., Campolo, O., Canale, A., Kapranas, A., Liedo, P., Meyer, M., Nestel, D., Ruiu, L., Scolari, F., Wang, X., Papadopoulos, N. 2023. Biology, ecology and invasiveness of the Mediterranean fruit fly, Ceratitis capitata: a review. Entomologia Generalis. 43:1221-1239. https://doi.org/10.1127/entomologia/2023/2135.
Lisi, F., Cavallaro, C., Pitruzzello, M.F., Arnò, J., Desneux, N., Han, P., Wang, X., Zappalà, L., Biondi, A., Gugliuzzo, A. 2024. Compatibility of bioinsecticides with parasitoids for enhanced integrated pest management of Drosophila suzukii and Tuta absoluta. Insects. 15(7). https://doi.org/10.3390/insects15070467.
Gariepy, T.D., Abram, P.K., Adams, C., Beal, D., Beers, E., Beetle, J., Biddinger, D., Brind’Amour, G., Bruin, A., Buffington, M.L., Burrack, H., Daane, K., Demchak, K., Fanning, P., Gillett, A., Hamby, K., Hoelmer, K., Hogg, B.N., Isaacs, R., Johnson, B., Lee, J.C., Levensen, H., Loeb, G., Lovero, A., Milnes, J., Park, K., Prade, P., Regan, K., Renkema, J., Rodriguez-Saon, C., Neupane, S., Jones, C., Sial, A., Smythman, P., Stout, A.R., Van Timmeren, S., Walton, V.M., Wilson, J., Wang, X. 2024. Widespread establishment of adventive populations of Leptopilina japonica (Hymenoptera, Figitidae) in North America and development of a multiplex PCR assay to identify key parasitoids of Drosophila suzukii (Diptera, Drosophilidae). NeoBiota. 93:63–90. https://doi.org/10.3897/neobiota.93.121219.
Cao, L., Xie, J., Wang, X., Wang, X., Poland, T.M., Petrice, T.R., Yang, Z. 2024. Description of a new species of the genus Atanycolus Foerster (Hymenoptera: Braconidae) parasitizing Lamprodila nobilissima bellula (Lewis) (Coleoptera: Buprestidae) in China. Zootaxa. 5448(2):248–260. https://doi.org/10.11646/zootaxa.5448.2.5.
Lee, S., Park, D., Wang, X., Duan, J.J., Gould, J.R., Kim, I., Lee, S. 2023. Exploration for Asian longhorned beetle parasitoids in Korea using an improved sentinel log trap. Parasite. 30(57):10. https://doi.org/10.1051/parasite/2023062.
Wei, K., Li, F., Tang, Y., Cao, L., Yang, Z., Gould, J.R., Wang, X., Wang, X. 2023. Exploration for native parasitoids of Asian longhorned beetle in China as prospective biological control agents. Agricultural and Forest Entomology. https://doi.org/10.1111/afe.12583.
Mu, M., Chen, Y., Wang, X., Desneux, N., Zang, L. 2023. Comparative demographics, population projections and egg maturation patterns of four eupelmid egg parasitoids on the factitious host Antherae pernyi. Pest Management Science. https://doi.org/10.1002/ps.7537.
Ramadan, M.M., Hoelmer, K.A., Wang, X. 2023. Host immunity, non-reproductive effects and kelptoparasitism from novel interactions: a case study with the fruit fly parasitoid Psyttalia fletcheri (Hymenoptera: Braconidae). Biological Control. https://doi.org/10.1016/j.biocontrol.2023.105307.
Hopper, K.R., Wang, X., Kenis, M., Seehausen, L., Abram, P., Daane, K.M., Buffington, M.L., Hoelmer, K.A. 2024. Genome divergence and reproductive incompatibility among populations of Ganaspis near brasiliensis. G3, Genes/Genomes/Genetics. jkae090:1-13. https://doi.org/10.1093/g3journal/jkae090.
Biancheri, M.J., Wang, X., Núñez-Campero, S.R., Suárez, L., Schliserman, P., Ponssa, M.D., Kirschbaum, D.S., Garcia, F.R., Ovruski, S.M. 2024. The Population Dynamics and Parasitism Rates of Ceratitis capitata, Anastrepha fraterculus, and Drosophila suzukii in Non-Crop Hosts: Implications for the Management of Pest Fruit Flies. Insects. https://doi.org/10.3390/insects15010061.