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ARS Home Pacific West Area Albany, California Western Regional Research Center Invasive Species and Pollinator Health Research





- Moran, Patrick
- Hogg, Brian
- Pratt, Paul
- Mueller, Rebecca
- Rector, Brian
- 2023
- 2022
- 2021
- Publications
- Crop Protection & Quarantine (304)

Research Project: Biological Control of Invasive Pests in Agroecosystems and Wetland, Forest and Rangeland Ecosystems in the Far Western U.S. **Location:
                            Invasive Species and Pollinator Health** 2022 Annual Report **Objectives**
                                

1) Discover, identify and prioritize the development of new biological control agents for targeted invasive weed and arthropod pests such as medusahead and bagrada bug.
Subobjective 1A: Determine point(s) of origin of ice plant.
Subobjective 1B: Discover, identify, and prioritize candidate agents of cheatgrass, medusahead and ice-plant.
Subobjective 1C: Discover, identify and prioritize candidate agents of bagrada bug.

2) Evaluate the host range, biology, and potential efficacy of prospective biological control agents for weed and arthropod pests such as French broom and bagrada bug.
Subobjective 2A: Deleted.
Subobjective 2B: Evaluate host range, biology and potential efficacy of candidate agents on yellow starthistle, Russian thistle, French broom, cheatgrass, medusahead, ice plant, and arundo.
Subobjective 2C: Evaluate host range, biology and potential efficacy of candidate biocontrol agents of bagrada bug.

3) Release permitted biological control agents targeting terrestrial weed and arthropod pest targets such as yellow starthistle, Cape-ivy, and spotted wing drosophila, and determine their establishment, dispersal, efficacy, influence on pest populations, benefits for native plant communities or crops, and suitability for integration into integrated weed and arthropod pest management plans.
Subobjective 3A: Rear, release and evaluate a new biological control agent of yellow starthistle.
Subobjective 3B: Release and evaluate biological control agents on bagrada bug and spotted-wing drosophila.
Subobjective 3C: Examine ecological impacts of Cape-ivy biocontrol and implications for integrated management. **Approach**
                                

Under Objective 1, we will determine the origin of crystalline ice-plant by sampling the invaded range in California and native ranges in South Africa and Mediterranean Europe. Genetic analyses will involve chloroplast and nuclear DNA. We will isolate soil microbes associated with medusahead and cheatgrass and determine best candidates. Surveys will be conducted in California, Nevada and Oregon and will include determination of symptoms and culturing. We will survey crystalline ice plant in South Africa and the Mediterranean and determine best candidate agents on the basis of host specificity and ability to reduce growth and reproduction. We will identify and prioritize candidate agents of bagrada bug that can attack eggs through surveys in South Africa and Kenya. 

Under Objective 2, we will determine the host specificity and efficacy of one candidate agent each targeting yellow starthistle, Russian thistle and French broom. We hypothesize that these agents will develop and reproduce only on the targeted weed. Biological safety will be examined in no-choice and choice tests. Candidate impact on plant biomass and seed production will be examined in quarantine and in the native range. We will quantify the host range and efficacy of candidate agents of medusahead and cheatgrass. Microbial candidates will be evaluated for inhibition of root development or seed germination. Insects or mites will be evaluated for ability to reduce growth and reproduction. We hypothesize that one host-specific and efficacious agent of crystalline ice plant will be found. We will conduct host range and efficacy tests as for other weeds. We hypothesize that the arundo leafminer can be reared on a California isolate of its fungal associate. We will isolate the leafminer from its native fungal isolate and parasitic nematode. We will assess host specificity of two candidate parasitic wasp species targeting bagrada bug eggs by comparing attack on native plant bugs and the pest, and ability to kill eggs. 

Under Objective 3, we will increase production of a newly-permitted rosette-feeding weevil for biological control of yellow starthistle. We will develop an artificial diet to facilitate mass-rearing and refine plant-based rearing. We hypothesize that this weevil will establish on and negatively impact yellow starthistle. Releases will be performed in the coastal hills, Central Valley, and Sierra foothills. We will assess field attack rates by resident enemies on bagrada bug eggs by attracting native natural enemies, and cameras and traps will be used to identify species. Searches will also be made for a non-native natural enemy that may already be present. We will release the first permitted biocontrol agent targeting spotted-wing drosophila in the U.S. and will verify establishment and efficacy. If the new enemy fails to establish, we will study native enemies. We hypothesize that the Cape-ivy shoot tip-galling fly will reduce density and flowering of this weed and increase native plant diversity. Biocontrol will be integrated with physical removal. Where the fly fails to establish, we will release a leaf-mining moth. **Progress Report**
                                

It is necessary to determine the geographic and climatic ranges and invasive origins of weeds and pest insects targeted for biological control, and the identities and distributions of natural enemies as candidate biocontrol agents. Preliminary tests of host range and impact must be done in the target’s native range and in laboratories to prioritize candidates. These studies were carried out under Objective 1. 

Crystalline ice plants smother native plants and alter soil quality along the California coast. In support of Sub-objective 1A, 80 leaf samples of Mesembryanthemum crystallinum and M. nodiflorum were collected from the Channel Islands and mainland coast of California by an ARS scientist in Albany, California. A cooperator in Italy collected samples in the Canary Islands (Spain), Italy, Morocco, and Tunisia. DNA analyses of 111 samples, performed by a cooperator in South Africa where ice plant is native, indicated that samples from the Canary Islands and United States are genetically similar, and are close genetically to samples from western South Africa. Also, under Sub-objective 1A, 89 leaf and 376 seedhead samples of invasive stinkwort were collected in California for studies of genetic origin by ARS in France. 

Cheatgrass and medusahead are major invasive annual grasses covering millions of acres in arid western U.S rangelands, consuming water, degrading forage quality, and fueling wildfires. In support of Sub-objective 1B, a new ARS scientist conducted surveys in California, Nevada, Arizona, Idaho, Utah, and Montana of adjacent populations of cheatgrass and a native perennial bunchgrass, Elymus elymoides. The soil surrounding the roots (“rhizosphere”) of these grasses was collected for analysis to determine if the impact of potential microbial biocontrol agents will be altered by interactions with microbial residents of the rhizosphere. DNA sequencing-based measurements are underway.

In support of Sub-objective 1B, surveys and host range by a cooperator in South Africa to prioritize biological control agents of crystalline ice plant continued. A stem-boring weevil, Lixus carinerostris, was able to develop on ice plant and two closely-related South African plants, but not on three U.S. ornamental plants. A second candidate biocontrol agent, a root-girdling weevil, Calomela prolixus, was identified. 

Since 2008, bagrada bug has invaded California’s $2.3 billion (B)-per-year cole crops industry (cabbage, broccoli, and cauliflower). This stinkbug feeds and spreads on related non-native weeds and native plants. In support of Sub-objective 1C, three sites infested with bagrada bug were located in South Africa by a cooperator, and bagrada bug eggs placed at two sites to collect parasitic wasps. Infested sites for wasp collection were also located on the Mediterranean islands of Malta and Pantelleria (Italy).

Candidate agents of weeds and pest insects must be rigorously evaluated in a quarantine laboratory and, when possible, in the native range, to determine their host range (safety), biological life cycles, and impact. These studies were completed under Objective 2.

Yellow starthistle consumes water, displaces native plants, and hinders cattle and horse grazing in the western United States. In support of Sub-objective 2B, an ARS scientist evaluated the host range of the seedhead weevil Larinus filiformis in quarantine. Plans to examine its host range, and that of a seedhead weevil (Larinus latus) on Scotch thistle, in a field test in Bulgaria were prevented by pandemic travel restrictions. 

Russian thistle and French broom displace native plants in rangelands, forests, and rights-of-way, consume scarce water and fuel wildfires. In support of Sub-objective 2B, a stem-boring and fruit-eating moth, Gymnancyla canella, was reared on Russian thistle in quarantine. Host range tests of the shoot tip-galling and seed-feeding weevil Lepidapion argentatum, a prospective agent of French broom, on six native lupins showed that the weevil was not able to make galls on these relatives.

Gorse is an exotic weed that invades natural areas in California coastal foothills. Under Sub-objective 2B, ARS scientists acquired the gorse thrips from collaborators at the Oregon Department of Agriculture and released them at six sites in northern California. Follow-up surveys in 2022 recovered one adult at each of two sites. It remains unclear if the insect will establish at these locations and what environmental or biological factors limit its success. A laboratory colony is being maintained for additional releases. 

Under Sub-objective 2B, seeds from cheatgrass were collected at sites in the states listed under Objective 1, targeting healthy and diseased plants. Microbial culturing along with DNA analysis were used to characterize microbes on and in the seeds, including those transmitted from the ‘parent’ plant, to characterize diseases of cheatgrass seeds and determine if interactions between cheatgrass and beneficial microbes can be disrupted. Seeds of eighteen species or varieties of native U.S. grasses and important agricultural crops were collected in preparation for host range studies of prospective arthropod (insect or mite) and microbial agents of medusahead and cheatgrass. Select wheat varieties commonly planted in the western United States were shipped to collaborators at the Biotechnology and Biological Control Agency in Rome, Italy, to facilitate future open field host range studies.

To prepare for host range testing of prospective agents of crystalline ice plant, seeds of four U.S. native plants in the genera Sesuvium and Trianthema were collected in Texas by an ARS scientist in support of Sub-objective 2B. Non-native ornamental ice plants were also propagated.

Arundo consumes water in the southwestern United States, incurring over $100 million in control costs. Plans to import and rear the arundo leafminer Lasioptera donacis in quarantine in support of Sub-objective 2B were delayed by pandemic lab access restrictions. Diseased arundo leaf sheaths from California were sampled for culturing and DNA analysis to compare with known fungi in leafminer-infested sheaths in the native European range. 

In support of Sub-objective 2C, an ARS scientist continued testing the host specificity of Gryon aetherium, a parasitic wasp that is a potential biological control agent for bagrada bug. The wasp was tested on eggs of three native stinkbug species (Agonoscelis puberula, Mecidea sp., Pellaea stictica) and was able to attack and lay eggs in two of these, but high proportions of progeny wasps failed to emerge from eggs, indicating that they are suboptimal hosts. Further tests were conducted to assess the preference of the wasp for eggs of two stinkbug species (Thyanta custator, Holcostethus abbreviatus) that it attacked in previous tests. Results showed that the wasp preferred eggs of bagrada bug.

Once permits are received for field release, new biological control agents must be released and evaluated for field establishment, dispersal, and efficacy. These studies were conducted under Objective 3.

In support of Sub-objective 3A, an ARS scientist improved a plant-based rearing method for the yellow starthistle rosette weevil Ceratapion basicorne. Methods to break diapause (hibernation) using hormone treatments and manipulate temperature conditions allowed production of over 200 weevils. A total of 43 weevils were shipped to three rearing facilities in the western United States and a researcher in Idaho. All four recipients reported successful rearing. Efforts to develop an artificial diet were delayed by pandemic lab access restrictions. The weevil was released at one new site in California in March 2022, and measurements of yellow starthistle density and plant diversity were taken at all three California sites. Sampling at release sites in 2022 indicated possible establishment, because up to 2% of roots contained damage likely caused by this weevil.

In support of Sub-objective 3B, an ARS scientist conducted surveys of parasitic wasps attacking bagrada bug eggs at five sites in northern California (one in Solano County and four in Monterey County) using Petri dishes filled with soil placed under infested plants to attract egg-laying bagrada bugs while leaving their eggs exposed to parasites. The adventive (accidentally-introduced in the past by an unknown party) parasitic wasp Gryon aetherium was found at all sites, leading the California Department of Food and Agriculture to classify the wasp as a species of “common occurrence”, exempt from permitting requirements.

Spotted-wing drosophila, a fruit fly that lays eggs inside fruit, is a major invasive pest of blueberries, blackberries, raspberries, strawberries, and cherries in California. This insect pest is spreading across the United States, threatening a $3.4B crop industry with up to $1B in projected losses, and causing over $40 million in losses in California. In support of Sub-objective 3B, an ARS scientist released 1,000 Ganaspis brasiliensis parasitic wasps from Asia into an organic raspberry field in Watsonville, the first release in California. The wasp was also released into cages to examine how it tolerates environmental conditions.

Cape-ivy invades forests, stream-side habitats, and scrublands along the California coast, consuming water and displacing native species. In support of Sub-objective 3C, an ARS scientist took measurements of shoot tip density and biomass and plant diversity at three sites at which the shoot tip-galling fly Parafreutreta regalis is established. Studies on the ability of the fly to reduce post-grazing regrowth were initiated by planting at one field site to stimulate regrowth, while protecting some of the ivy plants with insecticide to exclude fly galling. **Accomplishments**
                                

1. Adventive natural enemy for bagrada bug found throughout north-central California. Bagrada bug spread rapidly and became a major pest of cole crops (cabbage, kale, broccoli, etc.) in California after its discovery near Los Angeles in 2008. Current control methods rely on insecticides that can harm human health and the environment. A biological control agent is needed that can attack bagrada bug eggs in the soil, where they are laid. An ARS scientist in Albany, California, in collaboration with researchers at the California Department of Food and Agriculture, found the non-native parasitic wasp Gryon aetherium attacking bagrada bug eggs at locations throughout north-central California. This wasp is from the native range of bagrada bug in Asia, and it could help control bagrada bug throughout the cole crop growing areas of California. These ARS research findings led the California Department of Food and Agriculture to classify the wasp as a species of “common occurrence” that is exempt from permitting requirements. This decision will allow possible mass-rearing and re-distribution of the parasitic wasp from sites where it already occurs. 2. First release of an imported natural enemy for spotted wing drosophila in California. Spotted-wing drosophila is now a major invasive pest of berries and other soft-skinned fruit in Europe, northern Africa, and North America, including California, a leading producer of berry crops such as raspberries and strawberries. Control of spotted wing drosophila currently relies on repeated insecticides, which can harm human health and the environment. No naturally occurring parasites in North America consistently attack spotted wing drosophila larvae in fruit. A specialized natural enemy that attacks larvae, the parasitic wasp Ganaspis brasiliensis, was imported from the Asian native range of the fly and permitted for release by USDA. An ARS scientist in Albany, California, in collaboration with researchers at the University of California, Berkeley, conducted the first release of this wasp in California in June 2022 in an organic raspberry production field in Watsonville, Santa Cruz County. By helping to control spotted wing drosophila, release and dispersal of this wasp is expected to reduce growers’ reliance on insecticides and increase the feasibility of high-value organic berry production. **Review Publications**
                            *Daane, K.M., Cooper, M.L., Mercer, N.H., Hogg, B.N., Yokota, G.Y., Haviland, D.R., Welter, S.C., Cave, F., Sial, A.A., Boyd, E. 2021. Pheromone deployment strategies for mating disruption of a vineyard mealybug. Journal of Economic Entomology. 114(6):2439–2451. https://doi.org/10.1093/jee/toab198.*
                                *Hogg, B.N., Hougardy, E.H., Talamas, E. 2021. Adventive Gryon aetherium Talamas (Hymenoptera, Scelionidae) associated with eggs of Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae) in the USA. Journal of Hymenoptera Research. 87:481-492. https://doi.org/10.3897/jhr.87.73778.*
                                *Talamas, E., Bremer, J.S., Moore, M.R., Bon, M., Lahey, Z., Roberts, C.G., Combee, L.A., McGathey, N., van Noort, S., Timokhov, A.V., Hougardy, E.H., Hogg, B.N. 2021. A maximalist approach to the systematics of a biological control agent: Gryon aetherium Talamas, sp. nov. (Hymenoptera, Scelionidae). Journal of Hymenoptera Research. 87:323–480. https://doi.org/10.3897/jhr.87.72842.*
                                *Hogg, B.N., Lee, J.C., Rogers, M., Worth, L., Nieto, D., Stahl, J.M., Daane, K.M. 2022. Releases of the parasitoid Pachycrepoideus vindemiae for augmentative biological control of spotted wing drosophila, Drosophila suzukii. Biological Control. 168. Article 104865. https://doi.org/10.1016/j.biocontrol.2022.104865.*
                                *Carmody, C., Mueller, R.C., Grodner, B.M., Chlumsky, O., Wilking, J., McCalla, S. 2022. Chickensplash! Exploring the health concerns of washing raw chicken. Physics of Fluids. 34(3). Article 031910. https://doi.org/10.1063/5.0083979.*
                                *Smith, L., Woods, D.M., Wibawa, M.I., Popescu, V., Moran, P.J., Villegas, B., Pitcairn, M.J., Hon, C. 2021. Release and establishment of the weevil Mecinus janthiniformis for biological control of Dalmatian toadflax in southern California. Biological Control. 161. Article 104633. https://doi.org/10.1016/j.biocontrol.2021.104633.*
                                *Stahlke, A.R., Bitume, E., Ozsoy, Z.A., Bean, D.W., Veillet, A., Clark, M., Clark, E., Moran, P.J., Hufbauer, R., Hohenlohe, P.A. 2022. Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control. Evolutionary Applications. 15(1):60-77. https://doi.org/10.1111/eva.13325.*
                                *Smith, M., Pratt, P.D., Rayamajhi, M.B. 2022. Crown area predicts total biomass for Rhodomyrtus tomentosa, an invasive shrub in Florida. Invasive Plant Science and Management. 15(1):61-66. https://doi.org/10.1017/inp.2022.8.*
                                *Moran, P.J., Goolsby, J. 2022. Biological control of arundo, an invasive grass threatening water resources and national security. In: Van Driesche, R.G., Winston, R.L., Perring, T.M., Lopez, V.M., editors. Contributions of Classical Biocontrol to the U.S. Food Security, Forestry, and Biodiversity. FHAAST-2019-05. Morgantown, WV: USDA Forest Service. p. 373-389. https://bugwoodcloud.org/resource/files/23194.*
                                *Wilson, H., Hogg, B.N., Blaisdell, G.K., Andersen, J., Yazdani, A., Billings, A., Ooi, K., Soltani, N., Almeida, R., Cooper, M.L., Rwahnih, M., Daane, K. 2022. Survey of vineyard insects and plants to identify potential insect vectors and noncrop reservoirs of grapevine red blotch virus. Phytofrontiers. 2(1):66-73. https://doi.org/10.1094/PHYTOFR-04-21-0028-R.*
                                *Hogg, B.N., Grettenberger, I.M., Borkent, C.J., Stokes, K., Zalom, F.G., Pickett, C.H. 2022. Natural biological control of Bagrada hilaris by egg predators and parasitoids in north-central California. Biological Control. 171. Article 104942. https://doi.org/10.1016/j.biocontrol.2022.104942.*
                                *Pickett, C.H., Borkent, C.J., Popescu, V., Lightle, D., Hogg, B.N., Grettenberger, I.M. 2021. New insights into predation through imaging. Biocontrol Science and Technology. 32(2):196-222. https://doi.org/10.1080/09583157.2021.1990856.*
                                *Smith, L., Park, I. 2021. Conditions to terminate reproductive diapause of a univoltine insect: Ceratapion basicorne (Coleoptera: Apionidae), a biological control agent of yellow starthistle. Environmental Entomology. 51(1):71-76. https://doi.org/10.1093/ee/nvab110.*
                                *Park, I., Smith, L. 2021. Topical application of synthetic hormones terminated reproductive diapause of a univoltine weed biological control agent. Insects. 12(9). Article 834. https://doi.org/10.3390/insects12090834.*


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