Research Project: Biology, Ecology, Genetics, and Genomics of Introduced Species for Biological Control of Invasive and Other Insect Pests

Location: Beneficial Insects Introduction Research Unit

2023 Annual Report

Objectives
Objective 1: Investigate key biotic factors influencing the spatial and temporal dynamics of wood-boring pest (including ALB and EAB) populations in their native range, focusing on exploration and quarantine service for effective, host-specific natural enemies (parasitoids) for biocontrol. Subobjective 1a - Explore for parasitoids of ALB and EAB in the pests’ native range (Asia). Subobjective 1b - Evaluate the role of the key natural enemies in regulating the spatial and temporal dynamics of ALB and EAB in the area of collection in Asia. Subobjective 1c - Evaluate the host specificity of parasitoids discovered for introduction to North America for ALB and EAB control. Subobjective 1d - Quarantine services to support research on exotic insect pests and their natural enemies. Objective 2: Conduct field releases and evaluate impacts of extant (indigenous) and previously introduced parasitoids on populations of wood-boring beetles such as EAB and ALB in the United States, while elucidating factors that influence successful establishment of introduced biological control agents, such as climate adaptation, release methodology, genetic variation in founder populations and risk-spreading (diapause) strategy. Objective 3: For newly discovered parasitoids of ALB, EAB and other invasive pests, and based on studies of life histories and reproductive biology, develop effective rearing technologies for these natural enemies, focusing on optimizing host stage, host substrate complex, temperature, photoperiod and relative humidity. Subobjective 3a - Characterize the reproductive biology, risk-spreading (diapause) strategy and key life history parameters of most promising parasitoid species. Subobjective 3b - Determine the optimal host stage and host-substrate complex in association with host density and host-to-parasitoid ratio. Subobjective 3c - Determine the optimal environmental conditions for adult parasitoid survival, oviposition and progeny development including diapause induction and termination.

Approach
Using the approaches relevant to the knowledge base of the targeted pests and their natural enemies, we will conduct foreign explorations for new natural enemies from the pests’ native home (Northeast Asia) and construct life tables of the target pest populations to evaluate the impact of the natural enemies on the pests’ population dynamics in Northeast Asia. After selecting the most promising (or efficient) natural enemies, we will test the selected natural enemies against non-target wood-boring insects in North America to delineate their host range for biological control introduction against the target pests. Upon regulatory approval for environmental releases of the discovered natural enemies in North America, we will conduct field experiments to assess their establishment, dispersal and impacts on the target pests’ population in the U.S. Laboratory studies will also be conducted to collect information on the parasitoid’s biology, risk-spreading and reproductive strategy and life history and to develop efficient rearing methods for mass-production of the introduced natural enemies for biological control releases. In addition, this project will provide quarantine services, host range data and mass-rearing technologies for natural enemies of high priority plant pests to state and federal agencies.

Progress Report
Asian longhorned Beetle (ALB) Research: Surveys for ALB parasitoids in China and South Korea were continued during 2022 in cooperation with the Chinese Academy of Forestry and Seoul National University, respectively. In China, we surveyed ALB parasitoids using sentinel logs in five geographical regions (Beijing, Gansu, Guizhou, Shanghai, and Yunnan) from 2019 to 2022. In total, 786 sentinel logs were deployed at 28 sites in these five regions and 15,984 ALB larvae were recovered from the exposed logs, including 12,922 alive and 894 parasitized larvae. Seven hymenopteran larval parasitoid species, Bracon planitibiae Yang, Eurytoma chinensis Yang, Heydenia sp., Oxysychus glabripennis Yang, Sclerodermus guani Xiao et Wu, Spathius anoplophorae Yang, and Zolotarewskya anoplophorae Yang, were collected in Beijing. Four, three and two of these species were also found in Shanghai, Guizhou, and Yunnan, respectively. No parasitoid was found in Gansu. Mean parasitism rates by all parasitoid species were 3.6 – 15.8% in Beijing, 1.4 –16.4% in Guizhou, 1.6 – 7.1% in Shanghai, and 5.8% in Yunnan. Spathius anoplophorae and O. glabripennis were the two most dominant parasitoids collected consistently in the four different regions (Log 401429). In South Korea, surveys were conducted in northeastern natural forests in Gangwon and a total of 404 sentinel logs were deployed in the field, and 912 ALB larvae and 2,060 ALB eggs were recovered from these sentinel logs. One larval parasitoid Spathius ibarakius Belokobylskij & Maetô and one unidentified species were collected (Log 401428, submitted). The major parasitoid (S. anoplophorae) found in China has been imported into BIIRU and successfully reared for over 50 generations. Various aspects of the parasitoid’s reproductive biology (egg maturation dynamics, life-time fecundity, host stage preference), developmental time, other life-history traits (clutch size and offspring sex ratio), and host specificity tests have been investigated. Results from these laboratory testing are still being prepared for publication. With the collaboration from APHIS and University of Massachusetts, continued field releases of a North American parasitoid Ontsira mellipes in the quarantine zone in Worcester, MA (with all appropriate federal and state permits and permission to move regulated articles). A total of 90 sentinel host larval logs were deployed and 2500 female wasps were released in the summer and fall of 2022. Although great efforts over the last two years (with 144 logs and 3200 females released in 2021) to rear and release O. mellipes for the control of ALB in MA, its efficiency has not been demonstrated with field-deployed ALB hosts in the release sites. We examined the potential effects of a dsRNA targeting an inhibitor of apoptosis (IAP) of ALB on O. mellipes, directly on adult wasp’s survival via injection, and indirectly on the detectability and suitability of host larvae injected with different does of dsIAP per larva. The results show no direct effect of disIAP on its parasitoid, but the potential indirect effect of dsRNA-affected host on the parasitoid, which may be minimized through optimizing dsRNA dosage to promote compatible applications of both management options for this invasive forest pest (log 395397). Emerald ash borer (EAB) Research: We continued field evaluations of the establishment, persistence, and impact of previously introduced biocontrol agents (egg and larval parasitoids) against emerald ash borer (EAB) in mid-Atlantic (Maryland and Delaware), Midwest (Michigan) and Northeast (Massachusetts, New York, and Connecticut) of the U.S. on the emerald ash borer (Agrilus planipennisi) in FY 2023. Findings from our field studies demonstrated the successful establishment, spread, and persistence of the newly introduced larval parasitoid (Spathius galinae) along with the earlier introduced agent (Tetrastichus planipennisi) and the egg parasitoid (Oobius agrili) (Log 396650; 403099). Further life table analysis also showed that parasitism rates by these introduced biocontrol agents have led to significant suppression of emerald ash borer population growth by these introduced agents in both Midwest and Northeast (Log 403494, in press). In addition, we also completed a long-term field study, demonstrating that selective treatment of ash trees micro-trunk injection of systemic insecticides against EAB in urban forests has no significant effects on the establishment and abundance of introduced EAB larval parasitoids (log 398943). To improve EAB biocontrol release strategy in western U.S. (Oregon), we also cooperated with scientists from Oregon State University and developed an online-operationalized EAB phenology model that accurately predicts the occurrence of various life stages suitable for parasitoid releases (Log 405746, submitted). Through laboratory experiments, we determined the low and upper temperature thresholds (7.8 to 18.3oC) for terminating the diapause of emerald ash borer larvae for effective parasitoid rearing. Data on EAB diapause termination threshold will be written up for publication in next Fiscal year. Spotted Lantern Fly (SLF) Research: With the assistance of cooperators at APHIS and the University of Delaware, we participated in ongoing collections of SLF eggs laid by the 2022 fall generation of SLF adults to monitor for presence of native egg parasitoids and to provide host material for behavioral studies. From some of the egg masses collected in our region (mostly northern Delaware), parasitoid wasps of the genus Anastatus emerged, identified tentatively as Anastatus reduvii, the first records of parasitoids from SLF eggs in Delaware. We continued behavioral assays in quarantine of the response by the Asian egg parasitoid Anastatus orientalis to 5 species of non-target planthoppers, Pselliopus barberi, Oncometopia orbona, Flatormenis proxima, Acanalonia conica, and Poblicia fuliginosa. Preliminary results suggest that A. orientalis does not respond as strongly to cues left by non-target species as it does the target SLF. Bug species Halyomorpha halys, Euschistus tristigmus, and Podisus maculiventris were provided regularly to the OTIS APHIS lab for ongoing no-choice non-target tests of A. orientalis. Greenhouse plantings of tree of heaven were established to support SLF rearing and continued research on this biological control program. SLF egg masses were collected during the late fall, winter, and early spring to maintain a local colony of A. orientalis in the Newark, Delaware, quarantine facility. Through a cooperative agreement with the Chinese Academy of Forestry, native range studies of the natural host range in non-target species in China were continued, although Covid restrictions have restricted the field work component of research in China (8010-22000-033-023S). Foreign travel by ARS was not possible for various administrative reasons, but shipments of a small number of dryinid nymphal parasitoid were sent by Chinese cooperators to APHIS cooperators attempting to establish a lab colony in the U.S. Some of the dryinid wasps reared by APHIS were subsequently sent to Newark to establish a backup colony in the U.S. and provide material for planned biological studies at Newark. Efforts were continued to establish a robust supply of tree-of-heaven as host plant material to support the Dryinus colony. With FY22 Farm Bill funds, we expanded research with South Korean collaborators for surveys of SLF natural enemies that may be present in the invaded South Korean range, where populations of SLF that had been very high are reported to have diminished in the past several years since natural enemies were discovered there. Incoming funds were received through project 8010-22000-033-015R (NIFA/SCRI, Biology, Management and Reducing the Impact of the Spotted Lanternfly on Specialty Crops in the Eastern USA), and Farm Bill award 8010-22000-033-071I, Biological Control of Spotted Lanternfly – FY22) that helped with the lanternfly research discussed above. QUARANTINE SERVICE: We shipped over 110,000 natural enemies state and university cooperators for releases against several invasive species across the United States. These included 100,000 Aphelinus hordei as mummified aphids to Colorado State Universities for field releases against Russian wheat aphids, 100 -200 Spathius galinae, Oobius agrili and Tetrastichus planipennisi to Oregon Department of Agriculture for EAB biocontrol, and 100 Trissolcus japonicus to Plant & Food Research, New Zealand for biocontrol of brown Marmorated stink bugs (BMSB), and 500 Ganaspis brasiliensis to University of Cornell, University of New Hampshire, and New York State University for rearing and releases against spotted wing drosophila. In addition, we also shipped to and received from cooperators the target pest species (EAB, SLF, BMSB, spotted wing drosophila) for research purpose.

Accomplishments
1. Successful establishment, persistence, and impacts of introduced emerald ash borer parasitoids. The emerald ash borer (EAB) is a serious invasive forest pest that has devastated natural and urban ash forests and threatens the existence of North American ash species. Biocontrol program against EAB began with the introduction of four insect parasitoid species from Northeast Asia (EAB’s native range) between 2007 and 2015. Our recent field study in Northeastern and North central parts of the United States demonstrates that three of the four introduced parasitoids (Spathius galinae, Tetrastichus planipennisi, and Oobius agrili) have successfully established persistent populations and significantly reduced EAB’s densities, contributing to North American ash recovery and regeneration Log (396650; 403494; 403099).

Review Publications
Duan, J.J., Gould, J., Quinn, N.F., Petrice, T., Slager, B., Poland, T., Bauer, L.S., Rutledge, C., Elkinton, J., Van Driesche, R. 2023. Protection of North American ash against emerald ash borer with biological control: ecological premises and progress toward success. BioControl. https://doi.org/10.1007/s10526-023-10182-w.
Wang, X., Faucher, J., Dhandapani, R., Duan, J.J., Palli, S. 2022. Potential effects of RNA interference of Asian longhorned beetle on its parasitoid. Pest Management Science. https://doi.org/10.1002/ps.7328.
Li, T., Wang, X., Desneux, N., Song, L., Zang, L. 2022. Performance of Chouioia cunea reared from a coleopteran alternative host as a biocontrol agent against the invasive lepidopteran pest, Hyphantria cunea. Pest Management Science. https://doi.org/10.1002/ps.7318.
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.
Broadley, H.J., Sipolski, S.J., Pitt, D.B., Hoelmer, K.A., Wang, X., Cao, L., Tewksbury, L.A., Hagerty, T.J., Bartlett, C.R., Russell, A.D., Wu, Y., Davis, S.C., Kaser, J.M., Elkinton, J.S., Gould, J.S. 2023. Assessing the host range of Anastatus orientalis, an egg parasitoid of spotted lanternfly (Lycorma delicatula) using Eastern U.S. non-target species. Frontiers in Insect Science. 3:1154697. https://doi.org/10.3389/finsc.2023.1154697.
Van Driesche, R.G., Duan, J.J., Osnas, J. 2023. Effect of tenthredinid leaf miner invasions on growth of Alaska white birch in Anchorage, Alaska, and the interaction with biocontrol of ambermarked birch leaf miner. Florida Entomologist. 106(2):110-116. https://doi.org/10.1653/024.106.0207.
Sherr, A., Quin, N.F., Tallamy, D., Duan, J.J. 2023. Effect of forest microhabitat and larval stage on overwintering survival, development, and phenology of Spathius galinae, classical biological control agent of emerald ash borer. Florida Entomologist. 106(2) : 104-109. https://doi.org/10.1653/024.106.0206.
Petrice, T.R., Poland, T.M., Bauer, L.S., Strazanac, J.S., Schmude, J.M., Duan, J.J., Ravlin, W.F. 2023. Factors affecting the yellow pan captures of the larval parasitoids for biocontrol of emerald ash borer: implications for monitoring parasitoid establishment and seasonal abundance. Biological Control. https://doi.org/10.1016/j.biocontrol.2023.105272.
Quinn, N., Petrice, T., Duan, J.J., Schmude, J.M., Theresa, P., Bauer, L.S., Rutledge, C., Van Driesche, R., Elkinton, J. 2023. Post-release assessment of Oobius agrili establishment and impacts in Michigan and the Northeastern U.S. Journal of Economic Entomology. 1-6. https://doi.org/10.1093/jee/toad120.
Duan, J.J., Crandall, R.S., Grosman, D., Schmude, J.M., Quinn, N., Chandler, J.L., Elkinton, J.S. 2023. Protective effects of emamectin benzoate trunk injection on neighboring ash trees against emerald ash borer (Coleoptera: Buprestidae): potential benefits to classical biological control. Journal of Economic Entomology. 116(3): 848–854. https://doi.org/10.1093/jee/toad074.