Source: AGRICULTURAL RESEARCH SERVICE submitted to
BIOLOGICAL CONTROL OF INVASIVE WOOD-BORING INSECT PESTS SUCH AS EMERALD ASH BORER AND ASIAN LONGHORNED BEETLE
Sponsoring Institution
Agricultural Research Service/USDA
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
0429043
Grant No.
(N/A)
Project No.
8010-22000-028-00D
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Jul 2, 2015
Project End Date
Jul 1, 2020
Grant Year
(N/A)
Project Director
DUAN J J
Recipient Organization
AGRICULTURAL RESEARCH SERVICE
(N/A)
NEWARK,DE 19711
Performing Department
(N/A)
Non Technical Summary
(N/A)
Animal Health Component
(N/A)
Research Effort Categories
Basic
20%
Applied
70%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2150699113050%
2152110113025%
2153110113025%
Goals / 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.
Project Methods
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 07/02/15 to 07/01/20

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. Through the support by U.S. Forest International Program (Interagency Reimbursable Agreement (IRA) 60-1926-2-043 & 60-8010-6-004 and collaborations with Chinese Academy of Forestry (Non-Assistance Cooperative Agreement (NACA) 58-8010-5-001F & 58-8010-7-005F), we collected and described three new species of encyrtid parasitoids of the emerald ash borer from Northeast Asia (the Russian Far East and China) during the life cycle of the project (Objective 1). One of the new egg parasitoids, O. primorskyensis, has been imported to the Newark USDA quarantine facility, tested for host specificity and is now being evaluated for environmental releases against emerald ash borer in the U.S. Working with cooperators from China, South Korea, and Animal and Plant Health Inspection Service (APHIS), we surveyed Asian longhorned beetle parasitoid guilds and their seasonal abundance using field-deployed sentinel host eggs or larvae in China (Beijing City, Shanghai City, and Jilin Province) and South Korea. Our survey in China detected over 12 species of hymenopteran parasitoids (four Pteromalidae, three Braconidae, two Eupelmidae, one Eurytomidae, one Ichneumonidae, and one Bethylidae) attacking sentinel Asian longhorned beetle larvae or eggs deployed in these sites (Li et al. 2020). Among all the parasitoid species recovered, the four most abundant species have been imported to the Beneficial Insects Introduction Research Unit (BIIRU) quarantine for further evaluation of their reproductive biology and host specificity. In South Korea, at least one egg parasitoid and one larval parasitoid were collected, but they have not been identified to species yet. In addition, over 120 permitted consignments were received annually by the Quarantine Facility from 2015 to 2020, consisting of over 10,000 specimens and 20 different beneficial species. A total of 53 outgoing shipments (~700 pest specimens; 150,000 parasitoids in 8 genera) were shipped to different cooperators in four states plus Canada every year. A total of 57 identification requests were submitted to the ARS Systematic Entomology Laboratory for determination. From 2015 to 2020, a total of 15 collaborators from 10 different states and Canada were involved in quarantine services. Through collaborations with the University of Massachusetts (NACA 58- 5010-5-013), University of Maryland (58-8010-5-015), Virginia Tech (58- 8010-5-016), USDA APHIS (IRA 60-8010-9-001), and U.S. Forest Service, we conducted field releases and evaluations of three previously introduced Chinese parasitoids as well as a more recently introduced Russian larval parasitoid in Michigan, Maryland, and Northeastern U.S. (Massachusetts, New York, Connecticut) and Virginia (Objective 2). Based on data collected from our study sites in these States, we constructed life tables of the emerald ash borer populations and quantified the role of both the native North American natural enemies and introduced biocontrol agents in suppressing the pest⿿s population growth rate. Using quantitative life-table analysis, we discovered that native North American natural enemies (a parasitoid wasp and woodpeckers) play a key role in suppressing the outbreak population of the invading emerald ash borer in central Michigan, but one introduced biocontrol agent became the dominant mortality factor of emerald ash borer larvae in small ash trees and ash saplings in the aftermath of emerald ash borer invasion (approximately five years after its releases there). However, the role of that agent in protection of large ash trees will be limited or inactive because of its short ovipositor (1.5 - 2.5 mm). Our recent field study showed that the more recently introduced parasitoid with a much longer ovipositor (4 ⿿ 5 mm) caused nearly 50% beetle mortality (by parasitism) approximately 2 years after major releases in some of our study sites in Northeastern U.S. It is expected that this newly introduced larval parasitoid and an Asian egg parasitoid may provide effective protection of large ash trees against emerald ash borer. Findings from these field studies also showed that the most recently introduced Russian larval parasitoid along with the earlier introduced agent have established increasing populations and spread widely in our study sites in Michigan, Massachusetts, New York, and Connecticut, where it was released between 2015 ⿿ 2017 (Duan et al. 2019). However, findings from the study in Michigan also showed that approximately 18⿿50% of parasitoid larvae were killed by extreme winter weather due to the 2019 polar vortex (Duan et al. 2020), indicating that extreme climates may negatively affect the efficacy of emerald ash borer biocontrol. In addition, our field study in Maryland and Virginia also suggests that the diapause status and release time affect the synchronization of the parasitoids and beetle populations and thus their establishment in the released regions (Abel et al, 2019; George et al. 2020, Ragzzino et al. 2020). For our field work testing the augmentative releases of a North American parasitoid against the invasive Asian Longhorned beetle population in the quarantined area (Worcester, Massachusetts), we have recently gathered and submitted the necessary safety data to USDA APHIS and Massachusetts State Conservation Department for their review and approval of the work permit in Worcester, Massachusetts. Significant progress has been made in developing effective rearing technologies for emerald ash borer and Asian longhorned beetle natural enemies used for biological control of the target pests (Objective 3). This includes the successful development of an evergreen ash-based rearing system for year-around production of various life stages of emerald ash borer for parasitoid production. Using this host-rearing method, we have successfully determined the key life-history parameters and optimal rearing conditions (temperature, host stage, host-to- parasitoid ratio and group structures) for the previously introduced emerald ash borer parasitoids. In addition, we have recently evaluated the potential of a native North American parasitoid as a novel association control agent for Asian longhorned beetle, by charactering various aspects of the parasitoid⿿s reproductive traits, including egg maturation dynamics, host size preference and suitability in association with Asian longhorned beetle. Our results showed that female wasps emerged with a substantial portion of their lifetime complement of mature eggs. Mature egg load reached a peak 4⿿6 d post-eclosion, and mature egg load also increased with female⿿s body size. Oviposition prompted production of more mature eggs in young female wasps. The parasitoid did not show a significant preference for large over small hosts in a choice test. Offspring survival, developmental time and sex ratio were not affected by host size. However, clutch size increased with host size and female wasps that developed from the large host had a larger body and consequently higher mature egg load than those reared from the small host. Neither longevity nor total number of parasitized hosts over a female lifetime were affected by female⿿s body size, but life-time fecundity, in terms of total number of offspring produced, increased with the female⿿s size. These results have important implications for improving rearing and field-release protocols of this parasitoid and have been submitted for publication (Log No: 373071). To further optimize the conditions for mass- rearing the native parasitoid for augmentative field releases, we have Investigated effects of different densities of host and parasitoid on its parasitization efficiency and reproductive outcomes. Results showed that overall parasitism and total numbers of parasitized hosts or progeny produced increased with host and/or parasitoid densities, but the number of parasitized hosts or progeny produced per female parasitoid decreased with parasitoid density at each given host density. Female parasitoids responded to increased parasitoid density with a significant increase in clutch size. Overall, per capita parasitization efficiency or reproductive outcomes were optimized at a low parasitoid-host ratio but with large group size of hosts and parasitoids. An optimal combination of exposing three or four parasitoids to four hosts is proposed for efficient mass-rearing of this parasitoid (Log No: 374591). Accomplishments 01 Biocontrol for emerald ash borer to protect North American ash trees. The emerald ash borer is a serious invasive forest pest that has destroyed natural and urban ash forests and threatens the existence of North American ash species. ARS researchers at Newark, Delaware, introduced a parasitic wasp, Spathius galinae, which has established a self-sustaining population three years after its release. The wasp has now spread to other infested areas and is providing significant biocontrol of the borer in large ash trees in the northeast United States. This natural enemy of emerald ash borers is critical for the protection of large ash trees in the U.S. forest ecosystems. 02 A new parasite that attacks the Asian longhorned beetle discovered. The Asian longhorned beetle is a high-risk, invasive forest pest that has established small populations in several U.S. states and threatens to cause severe damage to American hardwood forests if not successfully controlled or eradicated. ARS scientists at Newark, Delaware, working with researchers at USDA Animal Plant Health and Inspection Service and collaborators in China recently discovered and collected several new wasp parasites from northern China and brought them to Newark for evaluation of their host specificity.

Impacts
(N/A)

Publications

  • Golec, J.R., Aparicio, E.M., Wang, X., Duan, J.J., Fuester, R.W., Tatman, D.M., Kula, R.R. 2020. Cerambycid communities and their associated hymenopteran parasitoids from major hardwood trees in Delaware, USA: implications for biocontrol of invasive longhorned beetles. Environmental Entomology.
  • Wang, X., Biondi, A., Daane, K.M. 2019. Functional responses of three candidate Asian larval parasitoids evaluated for classical biological control of Drosophila suzukii. Journal of Economic Entomology.
  • Ragozzino, M., Meyer, R., Duan, J.J., Salom, S. 2020. Differences in early season emergence and reproductive activity between Spathius agrili (Hymenoptera: Braconidae) and Spathius galinae, larval parasitoids of the invasive emerald ash borer (Coleoptera: Buprestidae). Environmental Entomology. 49:334-341.
  • Abell, K.J., Duan, J.J., Shrewsbury, P.M. 2019. Determining optimal parasitoid release timing for the biological control of emerald ash borer (Coleoptera: Buprestidae). Florida Entomologist. 102(4):691-694.
  • Dhandapani, R.K., Duan, J.J., Palli, S.R. 2020. Orally delivered dsRNA induces knockdown of target genes and mortality in the Asian Long-horned Beetle, Anoplophora glabripennis. Archives of Insect Biochemistry and Physiology. 2020;e21679.
  • Dhandapani, R.K., Gurusamy, D., Duan, J.J., Palli, S.R. 2020. RNAi for management of Asian long-horned beetle, Anoplophora glabripennis: identification of target genes. Journal of Pest Science. 93:823⿿832.
  • Li, F., Wang, X., Cao, L., Yang, Z., Gould, J.R., Duan, J.J. 2020. Discovery of parasitoids of Anoplophora glabripennis (Coleoptera: Cerambycidae) and their seasonal abundance in China using sentinel host eggs and larvae. Journal of Economic Entomology. 2020: 1⿿10.
  • Duan, J.J., Bauer, L.S., Van Driesche, R., Schmude, J.M., Petrice, T., Chandler, J.L., Elkinton, J. 2020. Effects of extreme low winter temperatures on the overwintering survival of the introduced larval parasitoids Spathius galinae and Tetrastichus planipennisi. Journal of Economic Entomology. 1-7.
  • Shuai, H., Xiao-Yi, W., Zhong-Qi, Y., Duan, J.J. 2019. Effects of photoperiod and light intensity on wing dimorphism and development in the parasitoid Sclerodermus pupariae (Hymenoptera:Bethylidae). Biological Control. 133: 117⿿122.
  • Wang, X., Gülay, K., Kent, D.M. 2019. Temporal dynamics of host use by Drosophila suzukii in California⿿s San Joaquin Valley: Implications for area-wide pest management. Insects. 10: 2016.
  • Wang, X., Aparicio, E.M., Murphy, T.C., Duan, J.J., Elkinton, J.S., Gould, J.R. 2019. Assessing the host range of the North American parasitoid Ontsira mellipes: potential for biological control of Asian longhorned beetle. Biological Control. 137: 104028.
  • George, D., Duan, J.J., Tallamy, D., Slager, B.H. 2020. Effects of parental diapause status and release time on field reproductive biology of the introduced egg parasitoid, Oobius agrili (Hymenoptera: Encyrtidae) in the Mid-Atlantic. Biological Control. 149.
  • Duan, J.J., Van Driesche, R.G., Crandall, R.S., Schmude, J.M., Rutledge, C. E., Slager, B.H., Gould, J.R., Elkinton, J.S. 2019. Establishment and early impact of Spathius galinae (Hymenoptera: Braconidae) on Emerald Ash Borer (Coleoptera: Buprestidae) in the Northeastern U.S. Journal of Economic Entomology. 112: 2121-2130.
  • Hougardy, E.H., Wang, X., Hogg, B.N., Johnson, M.W., Daane, K.M., Pickett, C.H. 2020. Current distribution of the olive psyllid, Euphyllura olivina, in California and initial evaluation of the parasitoid Psyllaephagus euphyllurae as a biological control candidate. Insects. 11(3):146. https:// doi.org/


Progress 10/01/18 to 09/30/19

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. No additional progress was made in quantifying recruitment of ALB and EAB stages and associated parasitoids in the pests⿿ native range (Objective 1a ⿿ 48 months milestones) for this fiscal year. With the support from United States Forest Service International Program and USDA APHIS, additional work has been planned this summer through next fiscal year to continue the quantification of impacts of Asiatic natural enemies on the Asian longhorned beetle (ALB) and emerald ash borer (EAB) populations via life-table recruitment studies in South Korea and China, respectively. In addition, we have not been able to select appropriate sites for releasing the North American native parasitoid (Ontsira mellipes) due to low ALB densities in quarantined areas and also permit requirement for deploying sentinel ALB larval logs (Objective 2 ⿿ 48 months milestones). Other than the above not-met milestones, the rest 48 months milestones for Objectives 1, 2 and 3 of both the ALB and the EAB projects were fully or substantially met for this fiscal year. Detailed progress for fiscal year 2019 in accomplishing objectives of both ALB and EAB research is described below: ASIAN LONGHORNED BEETLE RESEARCH: Working with cooperators from the USDA APHIS Otis laboratory, we tested the host specificity of the native North American larval parasitoid (O. mellipes) against two invasive longhorned beetles [ALB Anoplophora glabripennis; Citrus longhorned beetle (CLB)⿿ A. chinensis] and six common North American cerambycid species (Elaphidion mucronatum, Monochamus carolinensis, Monochamus notatus, Neoclytus scutellaris, Xylotrechus colonus, and Xylotrechus sagittatus) (Objective 1C). Results of our host specificity testing showed that the native North American parasitoid (O. mellipes) readily attacked ALB, CLB, and three north American longhorned beetle species (E. mucronatum, M. carolinensis and M. notatus), but did not attack the other three north American longhorned beetle species (Wang et al. 2019, submitted). In addition, our study showed that O. mellipes performed equally well on ALB as on its native North American hosts such as M. carolinensis, indicating that the effect of O. mellipes on ALB could be enhanced in the presence of these alternative and native hosts to support local parasitoid populations in the field. More interestingly, we have found that the performance of O. mellipes on ALB can be significantly improved through continuous rearing on ALB in the laboratory (Golec et al. 2019). To optimize the condition for mass-rearing O. mellipes for augmentative field releases, we investigated some key reproductive traits of the parasitoid, including egg maturation dynamics, host size preference and suitability, as well optimal host to parasitoid ratio in terms of parasitism or offspring production per female. Results showed that female O. mellipes emerged with ca. 15 mature eggs and mature egg load peaked after 4⿿6 days to ~40 mature eggs. Number of mature eggs was also positively related to the female⿿s body size. Female parasitoid preferred to attack middle sized hosts (400-600 mg) and brood size positively increased with host body mass within the host size range (20-800 mg). Above this range brood size no longer increased with the host size. The parasitoid was able to estimate host size most likely based on the host⿿s defense capacity as the clutch size was also positively related to the number of stings (i.e. stinging and releasing venom to paralyze the host prior to oviposition). We tested a range of different ratios of wasps to hosts (1 to 15 wasps and 2 to 4 hosts, n = 1660). These findings suggest the parasitoid is likely most active when it is 4-6 days old, and more productive when using middle sized hosts and a ratio of approximately 3 wasps to 1 host. EMERALD ASH BORER RESEARCH: Considering the current spread of the EAB in the United States to the southern states such as Tennessee, Georgia and Louisiana, it is important to investigate the factors that may have limited the EAB spread to further central and southern parts of its native range China - i.e., no known EAB distribution in the south to Hebei Province (Objective 1b ⿿ 48 milestones). With the financial support by the U.S. Forest Service International Program and cooperators from Chinese Academy of Forestry, we continued our exploration for natural enemies in central and south China by deploying EAB-infested ash logs in the expanded area of central and southwest China, including Changsha in Hunan Province, Xinyang and Xucheng in Henan province, Leshan in Sichuan province, and Fuchou in Fujian province, where no emerald ash borer infestations had been observed. The sentinel ash logs (each about 50 cm long x 12.cm in diameter) were created with artificially infested EAB eggs (15 eggs per log) in July of 2018 and deployed to each of the study sites (10 logs per site) approximately two weeks after the egg infestation. These sentinel logs were then sampled in April of 2019 for EAB parasitoids. We hypothesized that these sentinel emerald ash borer larval logs would attract natural enemies such as parasitoids of wood- boring insects in these native regions, where densities of naturally occurring emerald ash borers (if any) would be too low to allow any detection. Unfortunately, few emerald ash borer larvae infesting the sentinel ash logs survived beyond 3rd instars and no natural enemies (larval parasitoids) were detected in any of these field-deployed logs. Upon dissection, we found that the nearly complete mortality of the EAB larvae inside the sentinel ash logs was due to the desiccation of the cambium tissues of the sentinel ash logs as no evidence of parasitism was observed. We discussed these results with our Chinese cooperators and suggested using girdled-trees (instead of sentinel logs) for future studies (if funds are available). For Objective 1c (48 months milestones), we completed all the physical work on the host specificity testing of the newly described emerald ash borer egg parasitoid, Oobius primorskyensis in the previous fiscal year and published the results of the study in this fiscal year (Duan et al. 2018). Our findings strongly indicate that the host specificity of O. primorskyensis is limited to species in the genus Agrilus, especially those most phylogenetically related to EAB. Results of this study will be used in the future petition for regulatory approval of this newly discovered egg parasitoid for environmental releases against EAB in North America. With university and state cooperators, we continued to collect data on population densities of EAB eggs and larvae and associated natural enemies in our biological control release sites in Maryland, Virginia, Michigan, Massachusetts, New York and Connecticut (Objective 2 ��� 48 milestones) in this fiscal year. The impact of both introduced and North America native natural enemies on the invasive emerald ash borer populations was quantified with life table analysis constructed from these data as well as data collected previously. Findings from the life table analysis showed that the most recently introduced larval parasitoid (Spathius galinae) has established increasing populations in all the release sites in Michigan (6), Massachusetts (2), New York (2) and Connecticut (3), where it was released between 2015 ⿿ 2017 and its density had increased 1.5 to 20-fold (relative to the first post-release sample year), reaching a final density of 2.3 ⿿ 14.3 broods/m2 of phloem area and causing 13.1 ⿿ 49.2% marginal rate of parasitism at some of the release sites (Duan et al. in press). It⿿s hopeful that this newly introduced larval parasitoid (S. galinae), along with earlier introduced agents (T. planipennisi and O. agrili) will provide a whole spectrum of protection of North American ash against EAB (Jennings et al. 2018, 2019). For fiscal year 2019, we continued to optimize the rearing and storage (temperature) conditions for the newly described egg parasitoid O. primorskyensis as well as the previously introduced egg parasitoid O. agrili (Objective 3c- 48 milestones). We exposed diapausing O. primorskyensis and O. agrili larvae to either 1.7°C or 12.8°C for 1 ⿿ 9 months, subsequently evaluated their post-chill development to adults, and assessed the longevity and lifetime fecundity of the emerged adult parasitoids under normal rearing conditions (25°C, 16:8 h L:D). Results of this show that both parasitoid species require periods of chill at either 1.7°C or 12.8°C to resume their development to adults under normal rearing conditions; however, there are clear differences between the two species in their responses to chill regimes. These findings have relevance to laboratory rearing and release strategies of these parasitoids for biocontrol of EAB and have been recently published in a peer reviewed journal (Duan and Larson 2019). QUARANTINE SERVICE: We provided essential quarantine services for two other ARS research projects at the Beneficial Insects Introduction Research Unit as well as several ARS cooperators (Objective 1d ⿿ 48-month milestones). These activities included receipts of a total of 61 permitted consignments of three targeted pests and five species of natural enemies, consisting of incoming shipments of 2472 EAB beetles and 2549 EAB larval and egg parasitoids (219 Spathius agrili, 1530 Spathius galinae, 400 Tetrastichus planipennisi and 800 Oobius agrili), 4 different chalcid parasitoids, 3 separate braconid parasitoids, as well as hand carried shipments of 150 spotted lanternfly (Lycorma delicatula). In addition, we had 5 outgoing shipments of 1440 EAB larval parasitoids (Spathius galinae) and 6 shipments of ALB eggs totaling 600 to support cooperator⿿s research programs at the University of Massachusetts and University of Kentucky, respectively.

Impacts
(N/A)

Publications

  • Duan, J.J., Schmude, J.M., Larson, K.M., Fuester, R.W., Gould, J.R., Ulyshen, M. 2018. Field parasitism and host specificity of Oobius primorskyensis (Hymenoptera: Encyrtidae), an egg parasitoid of the emerald ash borer (Coleoptera: Buprestidae) in the Russian Far East. Biological Control. 130: 44-50.
  • Wang, X., Hogg, B.N., Hougardy, E., Nance, A., Daane, K.M. 2018. Potential competitive outcomes among three solitary larval endoparasitoids as candidate agents for classical biological control of Drosophila suzukii. Biological Control. 130:18-26.
  • Jennings, D.E., Duan, J.J., Shrewsbury, P.M. 2018. Comparing recovery methods for the emerald ash borer (Agrilus planipennis, Coleoptera: Buprestidae) egg parasitoid Oobius agrili (Hymenoptera: Encyrtidae) in Maryland, USA. Forests. 659(9): 1-9.
  • Jennings, D.E., Xiao-Yi, W., Duan, J.J. 0219. Influence of density on interspecific competition between Spathius galinae and Tetrastichus planipennisi, larval parasitoids of the invasive emerald ash borer (Agrilus planipennis). Environmental Entomology. 48(2), 2019, 404⿿409.
  • Golec, J., Duan, J.J., Rim, K.A., Aparicio, E.M., Hough-Goldstein, J. 2019. Laboratory adaptation of a native North American parasitoid to a novel, invasive insect pest. Ecology and Evolution. 92:1179⿿1186.
  • Duan, J.J., Larson, K. 2019. Effects of chilling on diapause development and reproductive fitness of two congeneric species of encyrtid parasitoids (Hymenoptera: Encyrtidae) attacking the invasive emerald ash borer. Biological Control. 134: 163-169.
  • Lee, J.C., Wang, X., Daane, K.M., Hoelmer, K.A., Isaacs, R., Sial, A., Walton, V. 2019. Biological control of spotted-wing drosophila (Diptera: Drosophilidae) - Current and pending tactics. Journal of Integrated Pest Management. 10(1):1-9.


Progress 10/01/17 to 09/30/18

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. No additional progress was made in foreign exploration for emerald ash borer (EAB) natural enemies in northeast China, Korea and the Russian Far East for this fiscal year (objective 1a). With the support from U.S. Forest Service International Program and collaboration with Chinese scientists at the Chinese Academy of Forestry, we made substantial progress in evaluating the role of key natural enemies in regulating population dynamics of emerald ash borers and Asian longhorned beetles in their native range (Objective 1b). In addition, most 36-milestones for Objectives 2 and 3 of the emerald ash borer project were substantially met for this fiscal year. Detailed progress for fiscal year 2018 in accomplishing objectives of both emerald ash borer and Asian longhorned beetle research is described below: EMERALD ASH BORER RESEARCH: With support from the U.S. Forest Service International Program and cooperators at the Chinese Academy of Forestry (Objective 1b), a total of 30 ash trees were sampled in the spring of 2018 (April 15 ¿ 29) from three different study sites located in central and southwest China. The sampled ash trees had been artificially infested in the previous (2017) summer with emerald ash borer eggs, including the North American species (Fraxinus velutina) central China (Xucheng city in Henan Province), the Chinese ash species - Fraxinus griffithii in south China (Guilin, Guanxi Province) and F. chinensis in southwest China (Leshan city, Sichuan province). In addition, Lindgren multi-tunnel traps were also deployed at each study site (4 traps per sites) to capture emerald ash borer adults (if they occur at the study sites). Results of our 2018 China study showed that the dominant (perhaps only) ash trees in south or southwest China, are oriental ash species - F. griffithii in Guanxi province and F. chinensis in Sichuan province. These native Chinese ash trees appear to be highly resistant to emerald ash borer larvae. All artificially established emerald ash borer cohorts (N ~ 150) were killed at early instars (1 ¿ 3rd) in these two locations. No adult EAB were captured in the Lindgren traps, nor were wild EAB larvae observed from the ash trees that were previously girdled. Together, these findings indicate that Chinese native host tree resistance may be a key factor to prevent EAB establishment in south and/or southwest China. In central parts of China, however, the North American ash (F. velutina) is widely planted. While no wild EAB larvae were observed in our sampling trees, nor were any adults captured in the Lindgren funnel traps, we found that artificially established EAB cohorts on North American ash (F. velutina) trees successfully developed to adult stages in central China. We observed 100% parasitism by a braconid parasitoid of the artificially established EAB larvae from one of the six infested trees. The adult parasitoids had already exited from the cocoons and could not be collected and identified to species. Based on the characteristic of the cocoon, it was identified as Atanycolus sp. Further work is planned to collect this parasitoid from this location. Results of our field studies in 2018 in Central China raise questions as to why EAB doesn¿t occur in this part of China, where susceptible host plants (F. velutina) appear to be abundant in plantations and urban landscapes and climatic conditions are suitable for EAB larval development to adults. It is possible that natural enemies may have played a key role in preventing EAB from spreading to this part of China or more time is needed for EAB to naturally spread from nearby known EAB-infested regions such as Hebei and Shandong provinces. Considering the current spread of the EAB in the U.S. to the southern states such as Tennessee, Georgia and Louisiana, it is important to investigate the factors that may have limited the EAB spread to further central and southern parts of China - i.e., no known EAB distribution in the south to Hebei Province (including Tianjin and Beijing). For Objective 1c, we completed the host specificity testing of the newly described emerald ash borer egg parasitoid, Oobius primorskyensis, from the Russian Far East against 30 species of nontarget insects, including mostly native North American wood-boring beetles in the families Buprestidae and Cerambycidae plus one unidentified weevil, one predatory coccinellid, one pentatomid and one moth. Results from our host specificity testing showed that O. primorskyensis attacked seven out of nine non-target Agrilus species, but not any of the other non-target species tested. Percentage parasitism of some non-target Agrilus species (A. anxius and A. cephalicus was comparable to parasitism of their corresponding EAB control at 29 - 30%). However, percentage parasitism of most attacked non-target Agrilus species (A. bilineatus, A. egenus, A. fallax, A. macer, and A. oblongus) was significantly less (4 ¿ 17%) than for the EAB control (60 ¿ 90%). These results indicate that the host specificity of O. primorskyensis may be limited to species in the genus Agrilus, especially those most phylogenetically related to EAB, although additional testing is needed to determine whether the eggs of other buprestid genera are utilized by the species as well. In cooperation with the university and state cooperators, we continued to monitor the establishment and impact of previously introduced EAB parasitoids (Oobius agrili, Tetrastichus planipennisi, Spathius agrili and S. galinae) on EAB densities in Maryland, Virginia, Michigan, Massachusetts, New York and Connecticut (Objective 2). All four biocontrol agents have been recovered following their releases in most release sites in these States; however, only T. planipennisi and O. agrili have been consistently recovered more than one year following their releases. Our 2018 data indicates that the introduced biocontrol agent T. planipennisi continues to provide significant biocontrol services in the earliest release sites in southern Michigan, where releases of T. planipennis were conducted between 2007 ¿ 2010. In addition, working with collaborators from University of Maryland, University of Delaware, and U.S. Forest Services, we determined the optimal temperature/photoperiod regimes for induction and termination of emerald ash borer parasitoid O. agrili and Tetrastichus planipennisi and thus improved the current rearing protocols for these parasitoids (Objective 3c). ASIAN LONGHORNED BEETLE RESEARCH: Working with the Cooperator at the Chinese Academy of Forestry, we analyzed field-survey data collected from four Chinese provinces between 2015 and 2017 on mortality factors affecting eggs, immatures (larvae and pupae combined), and adults of the Asian longhorned beetle (ALB) infesting willows and poplar trees (Objective 1b). Our analyses showed that immature ALB density varied by location and tree species; however, overall density was highest in Jilin province. When immature ALB density was compared between host tree species from the same province, nearly four times the immature numbers were found infesting poplar than willow trees. On average, 59.3% of ALB eggs were killed by undetermined factors (likely host tree resistance and microbial pathogens) across all survey sites and years. In contrast, immature ALB stages were least susceptible to mortality factors, where on average 8.3%, 15.6%, and 9.1% of these were killed, respectively, by undetermined factors, woodpeckers, and unidentified predators across all survey sites and years. Parasitoids, Dastarcus helophoroides and Sclerodermus guani, were recovered from immatures in Gansu and Shaanxi provinces and Beijing City, together accounting for around 6.0% mortality of these stages in these sites. Working with cooperators from the USDA- APHIS Otis laboratory, we initiated host specificity testing of D. helophorides against nontarget wood-boring beetles (Objective 1c). Preliminary findings from our host specificity testing indicate that many native North American cerambycids and buprestids would be vulnerable to D. helophoroides and we thus recommend that D. helophoroides should not be considered for release as a biocontrol agent in North America. QUARANTINE SERVICE: We provided essential quarantine services for two other ARS research projects at the Beneficial Insects Introduction Research Unit as well as several ARS cooperators (Objective 1d). These activities included receipts of a total of 104 permitted consignments, consisting of 4652 pest specimens, and 2825 parasitoids, and sending 31 outgoing shipments with 1900 pest specimens, and 2590 parasitoids. In addition, we successfully maintained daily quarantine operation and updated quarantine facility and cultured 18 species of living insect colonies. Accomplishments 01 Two natural enemies of Emerald Ash Borers discovered. Exotic wood- boring insects such as emerald ash borer (EAB) can become serious invasive tree pests when accidentally introduced to new regions or areas. Discovery of new natural enemies in the pests¿ native range can greatly enhance the potential for biological control of these invasive or potentially invasive pests in the U.S. Scientists from the Chinese Academy of Forestry, USDA-ARS and U.S. Forest Service discovered and subsequently described two new species of parasitoids collected from the eggs of a wood-boring beetle (Agrilus fleischeri) infesting poplar trees in northeastern China where EAB also occurs. These new species (Oobius saimaensis and O. fleischeri) also attack EAB eggs in the laboratory and are additional agents for potential introduction to the U.S. for biological control of EAB.

Impacts
(N/A)

Publications

  • Wetherington, M.T., Jennings, D.E., Shrewsbury, P.M., Duan, J.J. 2017. Climate variation alters the synchrony of host¿parasitoid interactions. Ecology and Evolution. 7(20):8578-8587.
  • Duan, J.J., Van Driesche, R.G., Bauer, L.S., Reardon, R., Gould, J., Elkinton, J.S. 2017. The role of biocontrol of Emerald Ash Borer in protecting ash regeneration after invasion. FHAAST-2017-02. Morgantown, WV: U.S. Department of Agriculture, Forest Service, Forest Health Assessment and Applied Sciences Team. 10 p. [brochure]. Available:
  • Rim, K., Golec, J., Duan, J.J. 2018. Host selection and potential non- target risk of Dastarcus helophoroides, a larval parasitoid of the Asian longhorned beetle, Anoplophora glabripennis. Biological Control. 123:120- 126.
  • Yao, Y., Duan, J.J., Mottern, J.L., Wang, X., Yang, Z., Bauer, L.S. 2018. Two new species of Oobius Trjapitzin (Hymenoptera: Encyrtidae) and their phylogenetic relationship with other congeners from Northeastern Asia. The Canadian Entomologist. 150:303-316.
  • Duan, J.J., Schmude, J.M., Watt, T., Wang, X., Bauer, L.S. 2018. Host utilization, reproductive biology and development of the larval parasitoid Tetrastichus planipennisi as influenced by temperature: implications for biological control of the emerald ash borer in North America. Biological Control. 125:50¿56.
  • Golec, J.R., Fei, L., Cao, L., Wang, X., Duan, J.J. 2018. Mortality factors of Anoplophora glabripennis (Coleoptera: Cerambycidae) infesting Salix and Populus in central, northwest, and northeast China. Biological Control. 126: 198-208.
  • Duan, J.J., Bauer, L.S., Van Driesche, R.G., Gould, J.R. 2018. Progress and challenges of protecting North American ash trees from the Emerald Ash Borer using biological control. Forests. 9(3):142.
  • Rodrigues, T.B., Duan, J.J., Rieske, L.K., Palli, S.R. 2018. Identification of highly effective target genes for RNAi-mediated control of emerald ash borer, Agrilus planipennis. Scientific Reports. 8:5020.
  • Kashian, D.M., Bauer, L.S., Spei, B.A., Duan, J.J., Gould, J.R. 2018. Potential impacts of emerald ash borer biocontrol on ash health and recovery in southern Michigan. Forests. 9(6):296.


Progress 10/01/16 to 09/30/17

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. Asian Longhorned Beetle (ALB) Research: Working with cooperators from the University of Delaware (8010-22000-028-09S) and Chinese Academy of Forestry (8010-22000-028-11S), we surveyed natural enemies attacking immature stages of ALB populations infesting poplar and willow trees in northwest China (Objective 1A/1B). Data from the survey indicate that the parasitic beetle (Dastarcus helophoroides) is the dominant natural enemy species, but causes only low levels (<5%) of parasitism. A population of this natural enemy collected from ALB in China has been imported to the Beneficial Insects Introduction Research Unit (BIIRU) and its host association with ALB is confirmed. Working with the University of Delaware we determined the optimal ambient temperature and host ALB stages for rearing the North America native braconid parasitoid (Ontsira mellipes), which could be used for a mass-rearing program (Objective 3b/ 3c). Emerald Ash Borer (EAB) Research: With support from the U.S. Forest Service International Program and cooperators at the Chinese Academy of Forestry (8010-22000-028-22S), we girdled ash trees at sites in central and southwest China (Henan, Guanxi and Shichun Provinces), where EAB is rarely observed and is not a major pest, and we artificially infested the damaged trees with beetle eggs to survey for their natural enemies. A trip to China has been planned for next spring to inspect the survey trees and sample immature EAB stages and associated natural enemies in these regions (Objective 1a/1b). In cooperation with cooperators from University of Maryland (8010-22000-028-04S), University of Massachusetts (8010-22000-028-01S), and Michigan State University (8010-22000-028-13S), we continued to release and evaluate the establishment and impact of previously introduced EAB parasitoids (Oobius agrili, Tetrastichus planipennisi, Spathius agrili and S. galinae) on EAB populations in Maryland, Michigan, Massachusetts, New York and Connecticut (Objective 2). All four biocontrol agents have been recovered following their releases at most sites in these states; however, only T. planipennisi and O. agrili have been consistently recovered more than one year following their releases. Our data indicates that the introduced biocontrol agent T. planipennisi is providing significant biocontrol services at the earliest release sites in southern Michigan, where releases of T. planipennis were conducted previously. In addition, we successfully determined the optimal host density and/or host-to-parasitoid ratio for effectively rearing EAB egg parasitoid (O. agrili) under different temperature/photoperiod regimes (Objective 3b/3c). Quarantine Services: Essential quarantine support was provided for three ARS research projects at BIIRU as well as several ARS cooperators (Objective 1d) with the BSL2+ containment facility. These activities included receipts of a total of 76 APHIS-permitted consignments, consisting of 8,575 pest specimens, and 15,484 parasitoids in 5 genera. A total of 47 outgoing shipments were sent, with 3,939 pest specimens, and 443,347 parasitoids in 5 genera. In addition, 14 identification requests were submitted to the ARS Systematic Entomology Laboratory. Accomplishments 01 Significant biocontrol of emerald ash borer in ash saplings. 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. A classical biocontrol program began with the introduction of three insect parasitoid species from Northeast China in 2007, five years after EAB was first detected in Southern Michigan. For the first time, our study in Michigan demonstrated that one of the introduced parasitoids, Tetrastichus planipennisi, established a self-sustaining population several years after its release, has spread to other infested areas, and is providing significant biocontrol of EAB in ash saplings, which are critical for gradual recovery of ash forest ecosystems in North America.

Impacts
(N/A)

Publications

  • Duan, J.J. 2017. Can ash communities and their dependent species be partially protected through biological control of emerald ash borer? In Van Driexche, Roy G. and Reardon, Richard C. Suppressing Over-Abundant Invasive Plants and Insects in Natural Areas by Use of Their Specialized Natural Enemies. United States Department of Agriculture. pp. 41-47.
  • Duan, J.J., Bauer, L.S., Van Driesche, R.G. 2017. Emerald ash borer biocontrol in ash saplings: the potential for early stage recovery of North American ash. Forest Ecology and Management. 394:64�72.
  • Golec, J.R., Duan, J.J., Hough-Goldstein, J. 2017. Influence of temperature on the reproductive and developmental biology of Ontsira mellipes (Hymenoptera: Braconidae): Implications for biological control of the Asian Longhorned Beetle (Coleoptera: Cerambycidae). Environmental Entomology. 46(4):978-987. doi:10.1093/ee/nvx100.
  • Duan, J.J., Schmude, J.M. 2016. Biology and life history of Atanycolus cappaerti (Hymenoptera: Braconidae), a north american larval parasitoid attacking the invasive Emerald Ash Borer (Coleoptera: Buprestidae). Florida Entomologist. 99(4):722-728.
  • Abell, K.J., Bauer, L.S., Duan, J.J., Van Driesche, R.G. 2016. Monitoring the establishment and flight phenology of egg and larval parasitoids of emerald ash borer (Coleoptera: Buprestidae) in Michigan, USA using sentinel eggs and larvae. Florida Entomologist. 99(4):667�672.
  • Zhang, K., Wang, Y., Yang, Z., Wei, K., Duan, J.J. 2016. Biology and natural enemies of Agrilus fleischeri (Coleoptera:Buprestidae), a newly emerging destructive buprestid pest in Northeast China. Journal of Asia- Pacific Entomology. 20:47�52.
  • Jennings, D.E., Duan, J.J., Bean, D., Rice, K., Williams, G., Bell, S., Shurtleff, A., Shrewsbury, P.M. 2017. Effects of the emerald ash borer invasion on the community composition of arthropods associated with ash tree boles. Agricultural and Forest Entomology. 19:122�129.
  • Larson, K.M., Duan, J.J. 2016. Differences in the reproductive biology and diapause of two congeneric species of egg parasitoids (Hymenoptera:Encyrtidae) from northeast Asia: implications for biological control of the invasive emerald ash borer. Biological Control. 103:30-45.


Progress 10/01/15 to 09/30/16

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. Due to the critical vacancy for the Asian longhorned beetle (ALB) project and lack of operational funds for the emerald ash borer (EAB) project, no substantial progress was made in the investigation of ALB and EAB natural enemies in their native ranges including northeast China, Korea and the Russian Far East (Objective 1a � 12 month milestones). However, substantial progresses were made in the following (12-month) milestones. ALB RESEARCH: We determined the reproductive biology and critical life history parameters (longevity, fecundity, and sex ratio) of a North American native braconid parasitoid (Ontsira mellipes) using larvae of laboratory-reared Asian longhorned beetles (Objective 3a). Our study has shown that this North American native parasitoid can successfully attack and reproduce on ALB larvae and mass-rearing procedures for this parasitoid may be developed using the new association host for development of effective biocontrol programs against ALB. EAB RESEARCH: We discovered and described a new species of the emerald ash borer egg parasitoid (Oobius primorskyensis) previously collected from the Russian Far East, and determined the host range of this new egg parasitoid (Objective 1c). This new species is morphologically very similar to the previously introduced EAB egg parasitoid (O. agrili) from Northeast China. The two species together constitute a cryptic species complex of EAB egg parasitoids in northeast Asia. Further laboratory study reveals that there are distinctive differences in the reproductive biology and progeny dormancy pattern between the two species and the two egg parasitoid species may be complementary to each other in reducing EAB egg densities in the U.S. (Objective 3a). Based on these data, we have submitted the petition to USDA APHIS for regulatory approval of environmental releases of this new parasitoid in the U.S. for EAB biocontrol. In cooperation with university and state cooperators, we also selected and established 14 new study sites in Maryland (5), Massachusetts (3), Michigan (4), and Virginia (2), where over several thousands of previously introduced parasitoids (Tetrastichus planipennisi, Spathius galinae, and Oobius agrili) were released at each site for EAB biocontrol. QUARANTINE SERVICE: We provided essential quarantine services for two other ARS research projects at the Beneficial Insects Introduction Research Unit as well as several ARS cooperators (Objective 1d). These activities included receipts of a total of 131 permitted consignments, consisting of 16,607 pest specimens, and 1,298 parasitoids in 10 genera, and sending 31 outgoing shipments with 17,913 pest specimens, and 331,563 parasitoids in five genera. In addition, four identification requests were provided to the ARS Systematic Entomology Laboratory. Accomplishments 01 Discovery of a new emerald ash borer biocontrol agent. The emerald ash borer (EAB) is a serious invasive forest pest that has been detected in 27 U.S. states and killed hundreds of millions of ash trees since it was first detected from Michigan in 2002. Classical biocontrol via introduction of a diverse complex of co-evolved natural enemies from the pest�s native range (Northeast Asia) may be the only viable option for effective long-term management of EAB in North America natural forests. ARS researchers in Newark, Delaware discovered and described a new species of EAB egg parasitoid previously collected from the Russian Far East. This species is new to science and described as Oobius primorskyensis. Further laboratory study reveals that this new species shows distinctive differences in the reproductive biology and progeny dormancy pattern from the previously introduced EAB egg parasitoid (O. agrili) and may be more suitable for introduction against EAB in Northeast U.S. This new egg EAB parasitoid is currently being evaluated by USDA APHIS for environmental releases as a biocontrol agent and may help improve the efficacy of the current EAB biocontrol programs and increase the survival and recovery of North American ash trees.

Impacts
(N/A)

Publications

  • Duan, J.J., Bauer, L., Abell, K.J., Ulyshen, M.D., Van Driesch, R. 2015. Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: implications for biological control. Journal of Applied Ecology. DOI: 10.1111/1365-2664.12485.
  • Duan, J.J., Aparicio, E.M., Tatman, D.M., Smith, M.T., Luster, D.G. 2016. Potential new associations of North American parasitoids with the invasive Asian longhorned beetle (Coleoptera: Cerambycidae) for biological control. Journal of Economic Entomology. 109(2):699�704.
  • Hoban, J., Duan, J.J., Hough-Goldstein, J. 2016. Effects of temperature and photoperiod on the reproductive biology and diapause of oobius agrili (Hymenoptera: Encyrtidae), an egg parasitoid of emerald ash borer (Coleoptera: Buprestidae). Environmental Entomology. 45(3):726-731. doi: 10.1093/ee/nvw034.
  • Golec, J.R., Duan, J.J., Hough-Goldstein, J., Aparicio, E.M. 2016. Life history, reproductive biology, and larval development of Ontsira mellipes (Hymenoptera: Braconidae), a newly associated parasitoid of the invasive Asian longhorned beetle (Coleoptera: Cerambycidae. Journal of Economic Entomology. 109(4):1545-1554. doi: 10.1093/jee/tow122.
  • Peterson, D.L., Duan, J.J., Yaninek, S.J., Ginzel, M.D., Sadof, C.S. 2015. Growth of larval agrilus planipennis (Coleoptera: Buprestidae) and fitness of tetrastichus planipennisi (Hymenoptera: Eulophidae) in blue ash (Fraxinus quadrangulata) and green ash (F. pennsylvanica). Environmental Entomology. doi: 10.1093/ee/nvv122.
  • Jennings, D.E., Duan, J.J., Bauer, L.S., Schmude, J.M., Wetherington, M.T., Shrewsbury, P.M. 2016. Temporal dynamics of woodpecker predation on the invasive emerald ash borer (Agrilus planipennis) in North America. Agricultural and Forest Entomology. 18:174�181.
  • Jennings, D.E., Duan, J.J., Bean, D., Gould, J., Rice, K.A., Shrewsbury, P. M. 2016. Monitoring the establishment and abundance of introduced parasitoids of emerald ash borer larvae in Maryland, U.S.A. Biological Control. 101:138�144.
  • Wang, X., Jennings, D.E., Duan, J.J. 2015. Trade-offs in parasitism efficiency and brood size mediate parasitoid coexistence, with implications for biological control of the invasive emerald ash borer. Journal of Applied Ecology. 52(5):1365-2664 doi: 10.1111/1365-2664.12487.
  • Wang, X., Liang-Ming, C., Yang, Z., Duan, J.J., Gould, J.R., Bauer, L.S. 2015. Natural enemies and their impacts on emerald ash borer populations in its native range, with new records of parasitism by two species of beetles. The Canadian Entomologist. 148(3):329�342.
  • Wang, X., Wei, K., Qi-Yang, Z., Jennings, D.E., Duan, J.J. 2016. Biotic and abiotic drivers of phenotypic plasticity of wing Effects of biotic and abiotic factors on phenotypic partitioning of wing morphology and development in Sclerodermus pupariae (hymenoptera: bethylidae). Scientific Reports. doi: 10.1038/srep26408.
  • Watt, T.J., Duan, J.J., Tallamy, D.W., Hough-Goldstein, J., Ilvento , T.W., Yue, X., Ren, H. 2016. Reproductive and developmental biology of the emerald ash borer parasitoid Spathius galinae (Hymenoptera: Braconidae) as affected by temperature. Biological Control. 96:1�7.
  • Yao, Y., Duan, J.J., Hopper, K.R., Moltern, J.L., Gates, M.W. 2016. A new species of oobius trjapitzin (hymenoptera:encyrtidae) from the russian far east that parasitizes eggs of emerald ash borer (coleoptera:buprestidae). Annals of the Entomological Society of America. 109(4):629-638. doi: 10. 1093/aesa/saw022.


Progress 10/01/14 to 09/30/15

Outputs
Progress Report Objectives (from AD-416): 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 (from AD-416): 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. No progress made; see annual/final report for 8010-22000-023-00D.

Impacts
(N/A)

Publications