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

Location: Beneficial Insects Introduction Research Unit

2023 Annual Report

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

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

Progress Report
Populations of the brown marmorated stink bug HALYOMORPHA HALYS have been significant pests in soybeans, vegetables, nut and various tree fruits in the eastern and northwestern U.S. for the past decade, and their impact continues to increase in the southeastern, north central and southwestern U.S. We continued to provide technical support to cooperators across the U.S. for sentinel surveys to monitor parasitism of H. HALYS by resident native stinkbug parasitoids in different crop systems, including survey protocols. During previous project cycles field collections of TRISSOLCUS parasitoids of Asian stink bugs were obtained from Asia for taxonomic and genetic studies (Objective 1A,1B) in collaboration with university cooperators. Research was continued to assess the potential impact of Asian TRISSOLCUS JAPONICUS on target and non-target species in the field in the U.S. and to monitor the regional distribution of an adventive population of T. JAPONICUS. This research addresses Objective 1. Sites of field releases throughout Delaware made during previous summers are being monitored to determine whether establishment occurred and whether any non-target species are being attacked; these are ongoing (Objective 3B). Previous laboratory research on the behavioral response of the parasitoid TRISSOLCUS JAPONICUS to its host and to non-target kairomones (chemical footprints) were extended to the field in 2021 and 2022 with open-field releases at Newark with mass-reared parasitoids released into arrays of potted trees containing H. HALYS or P. MACULIVENTRIS egg masses, or applications of isolated kairomone components. Parasitoid response was examined in field trials to determine if host kairomones would increase the chances that parasitoids will discover host stink bug eggs under actual field conditions. These data were analyzed, and parasitoid species were identified during FY23, in part through the work of an intern. This research was presented at regional and national meetings. Results thus far continue to show that behavioral and ecological responses under field conditions are more moderate than under controlled laboratory conditions, but are still likely to reduce the potential non-target impact of this Asian parasitoid (Objective 1C). Other collaborative research involving Asian TRISSOLCUS species included development of rearing methodology to support large scale field releases, development of a predictive model of the joint impact in the field under varied climatic conditions of T. JAPONICUS and T. MITSUKURII, and support of international collaborator programs for augmentative releases of T. JAPONICUS in New Zealand and Italy. Foreign exploration for the parasitoids of spotted wing drosophila, DROSOPHILA SUZUKII, were conducted in South Korea in the past year to collect fresh materials for these key parasitoid colonies maintained at our quarantine (Objective 1A,1B). Laboratory research on the key parasitoid GANASPIS BRASILIENSIS, was continued in 2023 (Objective 2B) for purposes of parasitoid mass-rearing to supply material to multiple cooperators across the U.S. The rearing at Newark supported large-scale production of the parasitoid for widespread field releases that began in summer 2022 following APHIS approval of a Petition for Field Release in the fall of 2021 (Objective 3C) and which were continued into 2023. Research was also conducted in FY23 to characterize the genetic makeup of several populations of GANASPIS BRASILIENSIS that may include cryptic species, and for host range and biological studies (Objective 2A) in support of host range evaluations by numerous cooperators. This information will inform a more comprehensive understanding of the parasitoid’s host range and specificity. As part of our involvement in an SCRI CAP project for D. SUZUKII management with biocontrol (8010-22000-033-015R) we provided live shipments of GANASPIS BRASILIENSIS to project cooperators in seventeen states along with technical support to enable them to establish their own rearing colonies. Field releases were initiated at numerous locations by the cooperators, including releases by our laboratory at sites in Delaware. These results will be detailed in publications in FY23-24. Building upon a white paper prepared for the Office of National Programs on the subject, previous exploration in China, Taiwan, South Korea and Vietnam initiated with APHIS and foreign cooperators led to continued native-range studies by Asian cooperators with natural enemies of roseau cane scale, NIPPONACLERDA BIWAKOENSIS, an invasive insect that has established along the U.S. Gulf Coast and which is killing large areas of roseau cane (PHRAGMITES reed), dense stands of which are important for reducing coastal and shipping channel erosion. The parasitoid complex in each of the four Asian countries is being documented and their impact on the scale evaluated, and several new species have been found and are being described. Three of these are already present adventively in the U.S. Gulf Coast, but others occur thus far only in Asia and could be potential new biocontrol agents. Rearing studies and evaluations of agents are being conducted by cooperators. Research on another target pest that was originally part of the past 5-year project, LYCORMA DELICATULA (spotted lanternfly), is now described in the annual report for project 8010-22000-031-000D. Incoming funds were received through subordinate projects 8010-22000-030-001R (NIFA/SCRI, Management of Brown Marmorated Stink Bug (BMSB) in U.S. Specialty Crops), 8010-22000-033-024R (NIFA/SCRI, for Management of DROSOPHILA SUZUKII), and annual Farm Bill awards (8010-22000-033-060A and 8010-22000-033-067I for Roseau Cane Scale) that helped with the research discussed above. The overall impact of the research is that producers will have new biological control agents available that will help them manage key insect pests by reducing chemical pest management inputs, thereby maximizing profits and sustaining yield.

Accomplishments
1. Spotted wing drosophila. Spotted wing drosophila is an invasive Asian fly that has become a serious pest of small fruits and berries across the U.S. Foreign exploration by ARS and partners identified a key Asian natural enemy of the fly, the parasitoid wasp GANASPIS BRASILIENSIS. After extensive host range testing, APHIS issued a permit for field release, and the Newark laboratory has developed a protocol for rearing this parasitoid and provided parental colonies to 17 laboratories across the U.S. for their rearing and releases of this parasitoid since 2022. The Newark lab also coordinated the rearing and release of this parasitoid in mid-Atlantic states beginning the summer of 2022. Widespread distribution is expected to facilitate its rapid establishment in the U.S., which will be monitored in the coming years. Initial surveys show preliminary evidence of successful overwintering at some release sites.

Review Publications
Suárez, L., Biancheri, M.J., Murúa, F., Ordano, M., Ramadan, M.M., Wang, X., Cancino, J., Garcia, F., Sánchez, G., Beltrachini, S., Kulichevsky, L.E., Ovruski, S.M. 2023. Medfly population suppression through augmentative release of an introduced parasitoid in an irrigated multi-fruit orchard of central-western Argentina. Insects. 14(4). https://doi.org/10.3390/insects14040387.
Mason, P.G., Barratt, B.I., Mckay, F., Klapwijk, J., Silvestri, L.C., Hill, M., Hinz, H.L., Sheppard, A., Brodeur, J., Vitorino, M., Weyl, P., Hoelmer, K.A. 2023. Impact of access and benefit-sharing implementation on biological control genetic resources. BioControl. https://doi.org/10.1007/s10526-023-10176-8.
Abram, P.K., Guerra-Grenier, E., Brodeur, J., Capko, Clarissa, C., Beers, E., Blassioli, C., Borges, M., Cingolani, F.M., Cusumano, A., De Clercq, P., Fernandez, C.A., Gariepy, T.D., Haye, T., Hoelmer, K.A., Laumann, R., Lietti, M., McPherson, J., Punscke, E., Saunders, T., Zhang, J., Hardy, I. 2023. Geometry for the selfish clutch? Protective geometry and reproductive anatomy as candidate determinants of clutch size variation in pentatomid bugs. The American Naturalist. https://doi.org/10.1086/725917.
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.
Gutierrez, A.P., Sabbatini Peverieri, G., Ponti, L., Giovannini, L., Roversi, P., Mele, A., Pozzebon, A., Scaccini, D., Hoelmer, K.A. 2023. Tri-trophic invasive species systems: prospective analysis of the biological control of the brown marmorated stinkbug (Halyomorpha halys (Stål) under extant and climate change weather. Global Change Biology. 96:921–942. https://doi.org/10.1007/s10340-023-01610-y.
Hoelmer, K.A., Sforza, R., Cristofaro, M. 2023. Accessing biological control genetic resources: the United States perspective. BioControl. 68: 269–280. https://doi.org/10.1007/s10526-023-10179-5.
Giovannini, L., Sabbatini-Peverieri, G., Simoni, S., Cervo, R., Hoelmer, K.A., Roversi, P. 2022. Interspecific competition between Trissolcus japonicus and Trissolcus mitsukurii, the two most promising candidates for biocontrol of Halyomorpha halys. Biological Control. 176(2022), 105068. https://doi.org/10.1016/j.biocontrol.2022.105068.
Hougardy, E.H., Hogg, B.N., Wang, X., Daane, K.M. 2022. Discrimination abilities and parasitism success of pupal parasitoids towards spotted-wing drosophila pupae previously parasitized by the larval parasitoid Ganaspis brasiliensis (Hymenoptera: Figitidae). Environmental Entomology. 51(6):1106-1112. https://doi.org/10.1093/ee/nvac083.