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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** 2021 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**
                                

This report documents initial progress on project 2030-22000-033-00D, “Biological Control of Invasive Pests in Agroecosystems and Wetland, Forest and Rangeland Ecosystems in the Far Western U.S.,” which started in May 2021 and continues research from expired project 2030-22000-031-00D, “Management of Invasive Weeds in Rangeland, Forest and Riparian Ecosystems in the Far Western U.S. Using Biological Control.” For more information see the fiscal year (FY) 2021 final report for the expired project.  

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 biological control agents. Preliminary tests of host range and impact must be done in the target’s native range and in laboratories to prioritize candidates for further study. These studies were carried out under Objective 1.  

Crystalline ice plant smothers native plants and alters soil quality along the California coast. In support of Sub-objective 1A, over 100 leaf samples were collected from over 10 sites in California and the Baja Peninsula of Mexico for future genetic analysis by a cooperator in South Africa, who began to develop molecular methods to determine area(s) of origin of invasive populations in the United States. Severe drought limited plant germination and collections from additional sites. 

In support of Sub-objective 1B, a stem-mining weevil, Lixus carinerostris was studied at a South African cooperator’s laboratory as a candidate biological control agent targeting crystalline ice plant, and the insect’s life cycle was observed. Host range tests on two plant species in the same genus as crystalline ice plant that occur in South Africa, but not in the United States, indicated that feeding and development occurred, but to a lesser extent than on ice plant. 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. Recruitment and hiring of a research microbiologist to isolate and identify potential microbial biological control agents that are already present in western United States against cheatgrass and medusahead was completed. 

Since 2008, bagrada bug has invaded California’s $2.3 billion-per-year cole crops industry (for example cabbage, broccoli, and cauliflower). This stink bug feeds and spreads on related non-native weeds and wild native plants. In support of Sub-objective 1C, explorations and collections were conducted in South Africa to collect tiny parasitic wasps as potential candidate biological control agents targeting bagrada bug, in cooperation with the USDA-ARS European Biological Control Laboratory (EBCL) in Montpellier, France, and Stellenbosch University, South Africa. Plans were also finalized with a cooperating researcher at EBCL to sample parasitic wasps of bagrada bug on the island of Pantelleria, Italy, which is the only location in Europe where bagrada bug occurs.

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 efficacy/impact. These studies were completed under Objective 2. 

Yellow starthistle consumes water, displaces native plants, hinders cattle grazing and can poison horses in the western United States. In support of Sub-objective 2B, a laboratory colony of the seed-feeding weevil Larinus filiformis, a prospective biological control agent, was maintained and multiplied. Laboratory colonies of the moth Gymnancyla canella, a prospective agent of Russian thistle, and of the weevil Lepidapion argentatum, a prospective agent of French broom, were maintained and multiplied. Collaborators conducted surveys for natural enemies of cheatgrass and medusahead in Italy, Greece, Armenia and neighboring countries. Candidate insects were catalogued and identified. 

Also under Sub-objective 2B, a preliminary host plant test list with 40 species was constructed for host range testing of candidate agents targeting crystalline ice plant. This weed has no close relatives (same sub-family) in North America. The list includes all nine species in a different sub-family that are native to North America, as well as 14 non-native, ornamental species that are somewhat more closely related, and are present in the wild in California. Ten close relatives of ice plant found in South Africa but not in the United States were also included.

In support of Sub-objective 2C, three previously untested stinkbug species were collected for host specificity (safety) testing of Gryon aetherium, a parasitic wasp that is a potential biological control agent targeting bagrada bug: Cosmopepla conspicillaris; Cosmopepla uhleri; and Chinavia hilaris. These tests are needed to verify that the tiny parasitic wasp, which was discovered under the expired project as being already present in the field in California, but that is being tested as a separate known population in the ARS quarantine laboratory in Albany, California, does not reproduce on ‘non-target’ native stinkbugs to the same extent as it does on bagrada bug. The stinkbug species, Thyanta custator and Holcostethus sp., were also collected for further testing. Twelve ‘no-choice’ tests on Cosmopepla uhleri were started in April 2021 and completed in late May 2021. Testing of C. conspicillaris, C. hilaris and also the brown marmorated stink bug, Halyomorpha halys, will be completed in the summer or early fall of 2021. 

Once permits are received for field release, new biological control agents must be released, and they must be evaluated for field establishment, dispersal and efficacy. Prior-released and extant (native or accidentally-released) agents must also be studied in the field. These studies were conducted under Objective 3. 

In support of Sub-objective 3A, we expanded studies initiated under the expired project on the root- and rosette-feeding weevil, Ceratapion basicorne, which was first released in 2020 as the first new biocontrol agent targeting yellow starthistle in almost 20 years, and the first agent that feeds primarily on roots and immature rosettes. Experiments to evaluate the suitability of an artificial diet to rear larvae of this weevil were started. This work is especially innovative because artificial diets are rarely developed to mass-rear biological control agents of weds. Releases of C. basicorne on yellow starthistle continued at a field site in California. 

In support of Sub-objective 3B, weekly sampling began in mid-June 2021 at a site in Solano County, California, that is infested with bagrada bug, where two parasitic wasps were collected from bagrada bug eggs in the fall of 2020. On each sample date, 10 to 16 cards containing 10 bagrada bug eggs each were deployed on weedy bagrada bug host plants, in foliage and on the soil underneath plants, where most bagrada bug eggs are laid. Eggs were re-collected weekly and held for emergence of potential egg parasites.

Spotted-wing drosophila, a fruit fly that lays eggs inside fruit, is a major invasive pest of blueberries, blackberries, raspberries, strawberries and cherries, beginning in California and now spreading across the United States, threatening a $3.4 billion U.S. crop industry with up to $1 billion in projected losses, and causing over $40 million in losses in California. In support of Sub-objective 3B, in late May 2021 baseline sampling began at two large sites in Watsonville, California, in anticipation of the release of what will be the first biological control agent in the United States, a tiny parasitic wasp (Ganaspis brasiliensis). Sites were over 200 acres and contained a mixture of cane berry fields and semi-natural habitat. Sampling occurred on a weekly basis. Traps containing a 50% mixture of white wine and apple cider vinegar were deployed on a weekly basis to sample the fruit fly, and traps containing fly larvae and pupae as bait to attract resident natural enemies were deployed monthly to monitor pre-release ‘background’ parasitism rates. Fruit was collected twice per month to monitor fruit fly numbers and parasitism rates.

Cape-ivy invades forests, stream-side habitats and scrublands along the California coast, consuming water, displacing native species and costing over $1 million per year to control. In support of Sub-objective 3C, in May 2021 surveys, the Cape-ivy fly was verified as established at six sites between Mendocino County and San Luis Obispo (SLO) along the California coast. Ten 2 x 2 m biocontrol exclusion plots were set up in a goat-grazed area undergoing Cape-ivy regrowth at one site near SLO. All 10 plots were caged with mesh, and flies were released in five plots. Cages were then removed after four weeks for future evaluation of the impact of galling by the fly on Cape-ivy regrowth. The results of quarantine laboratory host range testing results of the leaf- and stem-mining Cape-ivy moth, Digitivalva delaireae, on six close relatives of Cape-ivy that occur in the United States were summarized. The moth can feed on three California native members of the plant genus Senecio, but can develop to the pupal or adult stage on only one species (arrowleaf ragwort). Insect reproduction is 50-fold or less on that plant than on Cape-ivy, and this non-target plant rarely co-occurs with Cape-ivy. **Accomplishments** **Review Publications**
                            *Wang, X., Ramualde, N., Aparicio, E.M., Maspero, M., Duan, J.J., Smith, L. 2021. Optimal conditions for diapause survival of Aprostocetus fukutai, an egg parasitoid for biological control of Anoplophora chinensis. Insects. 12(6). https://doi.org/10.3390/insects12060535.*
                                *Braman, C.A., Lambert, A.M., Ozsoy, Z.A., Hollstein, E., Sheehy, K., McKinnon, T., Moran, P.J., Gaskin, J.F., Goolsby, J., Dudley, T.L. 2021. Biology of an adventive population of the armored scale Rhizaspidiotus donacis, a biological control agent of Arundo donax in California. Insects. 12(7):588. https://doi.org/10.3390/insects12070588.*
                                *Daane, K.M., Wang, X., Hogg, B.N., Biondi, A. 2021. Potential host ranges of three Asian larval parasitoids of Drosophila suzukii. Journal of Pest Science. https://doi.org/10.1007/s10340-021-01368-1.*
                                *Marini, F., Weyl, P., Vidovic, B., Petanovic, R., Littlefield, J., Simoni, S., De Lillo, E., Cristofaro, M., Smith, L. 2021. Eriophyid mites in biological control of weeds: how to deal with them. Insects. 12(6):513. https://doi.org/10.3390/insects12060513.*
                                *Harms, N.E., Knight, I.A., Pratt, P.D., Reddy, A.M., Mukherjee, A., Gong, P., Coetzee, J., Raghu, S., Diaz, R. 2021. Climate mismatch between introduced biological control agents and their invasive host plants: improving biological control of tropical weeds in temperate regions. Insects. 12(6):549. https://doi.org/10.3390/insects12060549.*
                                *Hougardy, E.H., Hogg, B.N. 2021. Host patch use and potential competitive interactions between two egg parasitoids from the family Scelionidae, candidate biological control agents of Bagrada hilaris (Hemiptera: Pentatomidae). Journal of Economic Entomology. 114(2):611-619. https://doi.org/10.1093/jee/toab014.*
                                *Hogg, B.N., Cooper, M.L., Daane, K.M. 2021. Areawide mating disruption for vine mealybug in California vineyards. Crop Protection. 148: Article 105735. https://doi.org/10.1016/j.cropro.2021.105735.*


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