Research Project: Management of Invasive Weeds in Rangeland, Forest and Riparian Ecosystems in the Far Western U.S. Using Biological Control

Location: Invasive Species and Pollinator Health

2021 Annual Report

Objectives
1) Determine the host specificity, life cycle, and efficacy of new candidate biological control agents for invasive weeds of western rangeland, forest and riparian ecosystems, such as yellow starthistle, Russian thistle, Cape-ivy, and French broom. Subobjective 1.1: Determine feasibility of biological control of ice plant and other invasive weeds in the far western U.S. Subobjective 1.2: Determine host specificity, life cycle, and efficacy of new biological control agents of yellow starthistle, Russian thistle, French broom, and Cape-ivy. 2) Release and evaluate new biological control agents of invasive weeds in western rangeland, forest and riparian ecosystems, and evaluate previously released and adventive agents in the context of variation in weed genotype, climatic influences, and land management regimes, including the use of other control methods. Subobjective 2.1: Determine effect of plant genotype on efficacy of extant biocontrol agents of yellow starthistle. Subobjective 2.2: Determine distribution and impact of adventive or recently released insects on Dalmatian toadflax. Subobjective 2.3: Release and evaluate new biological control agents targeting arundo and Cape-ivy.

Approach
We will determine the current status of biological control of ice plant by surveying field sites for extant herbivores, including two soft scale species that feed on the leaves, and several parasitic wasps that were introduced to control these scales,over 40 years ago when ice plant was valued as an ornamental. We will determine the feasibility of biocontrol of ice plant and other candidate invasive weeds using new agents through surveys of land managers and other stakeholders, and by scoring weeds according to invasiveness, damage caused, and the likelihood of finding hostspecific and efficacious biological control agents in their native ranges. These studies will take phylogenies of the weeds and related native plants into account to determine the feasibility of avoiding nontarget plant damage. We will determine the host ranges of new candidate biological control agents of yellow starthistle, Russian thistle, and French broom through overseas collection by collaborators and no-choice and choice tests in our quarantine laboratory. These studies will also evaluate the biology and impact of candidate agents on targeted weeds. We will determine the ability of the Cape-ivy moth to reproduce and feed on closely-related nontarget plants. Information from host range testing and other studies on new candidate agents will be used to submit applications to the USDA for permits for field release. We will determine the ability of previously-released biological control agents of yellow starthistle, including a seedhead-feeding weevil and a seedhead-galling fly, to damage, survive and reproduce on invasive western U.S. genotypes of yellow starthistle in relation to genotypes from the Greek native range where the agents were originally collected, and from western Mediterranean Europe,where yellow starthistle in the western U.S. originated. These studies will be conducted under no-choice and choice conditions in the greenhouse and in field plantings. New accessions of these agents will be collected from western Mediterranean Europe and evaluated for host specificity among close relatives prior to release. At field sites in southern and northern California, we will evaluate the ability of a leaf- and stem-feeding weevil to reduce invasive Dalmatian toadflax plant size and Dalmatian toadflax population size, and determine the degree of recolonization of invaded sites by native plants. We will release and evaluate the impact of a stem-galling wasp and a shoot- and root-feeding armored scale for biological control of the invasive giant grass known as arundo in the Sacramento-San Joaquin Delta and associated river watersheds, where arundo is impacting water resources. These studies will determine the effect of climate on wasp and scale establishment success. We will release and evaluate a shoot tip-galling fly for biological control of Cape-ivy at field sites along the California coast. Studies on arundo and Cape-ivy will include evaluations of agent dispersal within field sites, and of integrated biological-chemical control, in which herbicides will be applied and the ability of biocontrol agents to colonize and have impact on regrowth will be determined.

Progress Report
This is the final report for bridging project 2030-22000-031-00D, entitled “Management of Invasive Weeds in Rangeland, Forest and Riparian Ecosystems in the Far Western U.S. Using Biological Control,” which has been replaced by new project 2030-22000-033-00D, entitled, “Biological Control of Invasive Pests in Agroecosystems and Wetland, Forest and Rangeland Ecosystems in the Far Western U.S.” For more information see the fiscal year (FY) 2021 Annual Report for the new project. It is necessary to prioritize which weeds and pest insects to target for biological control (biocontrol), followed by determination of their geographic origins, and the identities and distributions of natural enemies. Once candidate biocontrol agents are identified, tests of their host ranges, biological life cycles and potential efficacy must be conducted. 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 1.1, 100 samples were collected from 12 sites in the native range by a South African cooperator, and from 16 sites in two countries in the Mediterranean Basin by an Italian cooperator. The South African cooperator performed DNA extractions for determination of geographic origin of the invasion. Six insects were collected in South Africa. A promising stem weevil was colonized at the cooperator’s laboratory. Also under Sub-objective 1.1, a weed biological control prioritization process for the western United States was developed in collaboration with scientists from Australia. The first phase included a census of 187 weed scientists and land managers across 10 western states, leading to a list of 33 key weeds. The second phase used the expertise of biological control scientists to assess program feasibility and likelihood of success. Nine weeds were identified as low priority and 24 as moderate or high. Six weeds were characterized as having both high biocontrol feasibility and greatest environmental benefits. A report was shared with stakeholders and a journal article is in preparation. The prioritization results also formed the basis for selecting new weed targets in the new five-year project plan. Yellow starthistle, Russian thistle, and French broom displace native plants and forage grasses in rangelands, forests, and rights-of-way, consume scarce water, and fuel wildfires. In support of Sub-objective 1.2, quarantine laboratory colonies of prospective biological control agents were maintained and multiplied, including: the seed-feeding weevil Larinus filiformis targeting yellow starthistle; the stem-boring moth Gymnancyla canella targeting Russian thistle; and the shoot-galling and seed-feeding weevil Lepidapion argentatum targeting French broom. 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 non-crop plants. In support of Objective 1, the stinkbug species Cosmopepla uhleri, Banasa sordida, Chinavia hilaris, Thyanta custator, Dedrocoris sp. and Euschistus sp. were collected for host specificity testing of the potential biological control agent Gryon aetherium. Twelve no-choice replicates were started on C. uhleri in late April 2021. The foraging efficiency of G. aetherium in soils of different particle sizes was tested, and factors influencing rearing of G. aetherium were examined. Once permits are received for field release, new biological control agents must be released and evaluated for establishment and efficacy. Prior-released and extant (native or accidentally-released) agents must also be studied in the field. These studies were conducted under Objective 2. Under Sub-objective 2.1, data were analyzed to determine if plant region of origin – United States (California), France/Spain, or northern Greece - affect yellow starthistle biocontrol agent reproduction. The three prior-released insects examined were sourced from northern Greece. Plant origin did not affect densities of a bud- and seed-feeding weevil, Eustenopus villosus, or a flower-galling fly, Urophora sinuraseva, in either field plantings or greenhouse tests. In a 2015 field plot, the false peacock fly, Chaetorellia succinea, was 30% more abundant in seedheads from U.S. yellow starthistle than on Greek seedheads. On caged plants, density was 47% higher on U.S. seedheads. However, in later field plantings, the fly was 56% more abundant on Greek seedheads, and 28% more abundant on seedheads from France/Spain, than on U.S. seedheads. The results suggest that the three Greek insects are well-adapted to invasive yellow starthistle in California. Also in support of Sub-objective 2.1, a release permit was obtained for the rosette-feeding weevil, Ceratapion basicorne, which was collected in Greece with the help of foreign collaborators, multiplied in the laboratory and released for the first time in the field in California. Adults were also provided to cooperators in Colorado and Idaho for them to multiply for release. This is the first new released agent targeting yellow starthistle since 2003. If the weevil establishes, it will help reduce populations of this weed. Dalmatian toadflax invades rangelands and reduces desirable vegetation in the western United States. Under Sub-objective 2.2, prior (2014) releases of the stem-boring weevil, Mecinus janthiniformis, were evaluated at a site in southern California, the southernmost release site in North America. The weevil multiplied and reduced the weed by 99% within five years of release, providing self-perpetuating control of the weed without any negative nontarget effects on native plants. Arundo consumes water in the southwestern United States, incurring over $100 million in control costs. In support of Sub-objective 2.3, 2,400 females of the shoot tip-galling wasp, Tetramesa romana, were released at four sites in the Central Valley. Some of the arundo was pre-cut to induce lateral shoot growth. Nine months later, shoot tip exit holes indicative of new wasp emergence were 4.8-fold more abundant in pre-cut plots. Arundo wasps were present at two new sites in the Sacramento-San Joaquin Delta one year after release. In bagged field shoots, arundo wasps from southern California produced two-fold more offspring than wasps sourced from Texas, suggesting superior adaptation to hot, dry conditions. A test of the arundo root-feeding armored scale Rhizaspidiotus donacis found that adults were 27-fold more abundant with reproduction 74-fold higher on arundo than on a related native/invasive plant, common reed. Cape-ivy invades consumes water and displaces native species along the California coast, costing over $1M per year to control. In support of Sub-objective 2.3, plants with a total of 1,778 galls made by the fly, Parafreutreta regalis, were planted and 1,539 adults of this biological control agent were released. Follow-up surveys indicated overwintering and fly establishment at one new site in northern California, for a total of five sites established. Long-term monitoring at four sites showed that fly populations increased 11-fold in summer and 9-fold in the fall of 2020 relative to the previous winter. Fly females made 72% fewer galls on plants subjected to drought. The galls were 39% smaller, and fly pupae inside galls were 35% smaller. Adult production was reduced 78%. The fly can thus survive under drought conditions, but should be released on well-watered plants. Gorse is an exotic weed that invades natural areas, particularly foothills near the California coast. Under Sub-objective 2.3, ARS scientists acquired gorse thrips from collaborators at the Oregon Department of Agriculture and developed a laboratory colony. The thrips were reared and then released for the first time in California at three gorse patches located in Marin and Mendocino Counties. The insects established limited populations at each release site and injury to the target weed was apparent within 30 days following release. It is too early to determine if these insects will persist or control the weed but regular monitoring is planned under the replacement project. In support of Objective 2, samples of bagrada bug eggs collected in fall 2020 were sorted and emerging parasitic wasps were identified. Two were recovered from sentinel card eggs, Ooencyrtus californicus and Gryon aetherium (formerly known as G. gonikopalense). The former is native, while the latter is non-native and may have been released accidentally in California. Testing of G. aetherium has been underway in quarantine for several years, but it has not been recorded in the field in California before. Only G. aetherium emerged from soil collected under infested mustard plants, and tests are underway to determine whether the strain found in California is capable of attacking buried bagrada bug eggs.

Accomplishments
1. Release of a new biological control agent targeting yellow starthistle. Yellow starthistle is a spiny rangeland weed that is toxic to horses and has invaded about 20 million acres in the western United States. ARS researchers in Albany, California, obtained approval to release the rosette-feeding weevil, Ceratapion basicorne, the first new agent released against this weed in almost 20 years, and the first that feeds on roots and rosettes of immature plants. Weevils obtained from Greece with the help of foreign collaborators were multiplied in the laboratory and released in the field in California. Weevils were provided to state cooperators in Colorado and Idaho for them to multiply for release. This weevil is expected to increase and spread on its own, which will help to reduce populations of yellow starthistle. Successful biological control will increase forage production and desirable native vegetation, and will reduce application of herbicides.

2. First discovery of an introduced biological control agent on Bagrada bug in California. Bagrada bug is a major recent (since 2008) non-native pest of cole crops like broccoli, cauliflower and cabbage in California, the national leader in production, where these crops are worth over $2.3B per year. Control is difficult because bagrada bug, unlike most plant bugs, lays its eggs in the soil. ARS researchers in Albany, California, discovered a tiny parasitic wasp, Gryon aetherium, in north-central California in 2020 and identified it in 2021. The wasp had emerged from bagrada bug eggs collected from the soil under infested host plants. Laboratory breeding experiments confirmed that it is the same species as a candidate biological control agent being tested in quarantine, although genetically a different strain. This is the first discovery of this parasitic wasp as being already present in the field in California. Its ability to attack bagrada bug eggs in soil is currently being verified. If found to be safe and effective, future rearing and release of large numbers of this parasite could significantly reduce economic losses caused by bagrada bug.

3. Success of Cape-ivy biocontrol is affected by simulated drought. Cape-ivy is a vine-like plant that has invaded streamside, forest, and scrub/bluff habitats in coastal California ecosystems, consuming water and displacing rare native species. ARS researchers in Albany, California, released a fly that makes tumors (galls) in shoot tips, but found that fly populations did not establish at warmer sites at which Cape-ivy undergoes wilting in the dry summer and fall Mediterranean climate of California. On greenhouse plants subjected to simulated drought, fly females laid 72% fewer eggs. Fifty percent fewer galls were produced, they were 39% smaller, and the developing flies inside were 35% lighter. Adult reproduction was 78% lower under drought than on well-watered plants, and time to complete development was one week longer. The results provide researchers and natural resource agencies implementing biological control of Cape-ivy with important information on when to release the fly in natural areas that are under increasing drought stress due to climate change.

Review Publications
Marini, F., Vidovic, B., Lonis, S., Wibawa, M.I., De Lillo, E., Kashefi, J., Cristofaro, M., Smith, L. 2020. Comparison of the performance of an eriophyid mite, Aceria salsolae, on nontarget plants in the laboratory and in the field. Biological Control. 152. Article 104455. https://doi.org/10.1016/j.biocontrol.2020.104455.
Portman, S.L., Santacruz, K., Moran, P.J. 2021. Host plant water deficit stress impairs reproduction and development of the galling fly (Parafreutreta regalis), a biological control agent of Cape-ivy (Delairea odorata). Biological Control. 156. Article 104555. https://doi.org/10.1016/j.biocontrol.2021.104555.
Wineriter-Wright, S., Smith, M., Metz, M., Makinson, J., Bradley, B., Purcell, M., Pratt, P.D. 2020. The biology of Casmara subagronoma (Lepidoptera: Oecophoridae), a stem boring moth of Rhodomyrtus tomentosa (Myrtaceae): descriptions of the previously unknown adult female and immature stages, and its potential as a biologic. Insects. 11(10):653. https://doi.org/10.3390/insects11100653.
Smith, M., Wright, S., Clark, P.T., Pratt, P.D., Purcell, M., Brown, B. 2020. Fundamental host range of Lophodiplosis indentata (Diptera: Cecidomyiidae), the last proposed biological control agent for Melaleuca quinquenervia (Myrtaceae) in Florida. Biocontrol Science and Technology. 30(10):1073-1082. https://doi.org/10.1080/09583157.2020.1787345.
Solis, M.A., Pratt, P.D., Makinson, J., Purcell, M.F., Rayamajhi, M.B., Mattison, E.D., Mally, R. 2020. Archernis humilis (Swinhoe) (Lepidoptera: Crambidae) rediscovered feeding on skunk vine (Paederia foetida L.) in southeast Asia. Proceedings of the Entomological Society of Washington. 122(3):732-749. https://doi.org/10.4289/0013-8797.122.3.732.
Rayamajhi, M.B., Rohrig, E., Tipping, P.W., Pratt, P.D., Leidi, J.G. 2020. Allometric equations for the invasive vine air potato (Dioscorea bulbifera) in its exotic range in Florida. Invasive Plant Science and Management. 13(2):76-83. https://doi.org/10.1017/inp.2020.15.
Rayamajhi, M.B., Rohrig, E., Lake, E.C., Smith, M., Pratt, P.D., Dray Jr, F.A., Halbritter, D.A., Leidi, J.G. 2021. Phenological synchrony between a weed (Dioscorea bulbifera) and a biocontrol agent (Lilioceris cheni) in the introduced range, Florida: implication in biological control. Biocontrol Science and Technology. 31(8):797–816. https://doi.org/10.1080/09583157.2021.1885627.
Tofangsazi, N., Hogg, B.N., Hougardy, E.H., Stokes, K., Pratt, P.D. 2020. Host searching behavior of Gryon gonikopalense and Trissolcus hyalinipennis (Hymenoptera: Scelionidae), two potential biological control agents for Bagrada hilaris (Hemiptera: Pentatomidae). Biological Control. 151. https://doi.org/10.1016/j.biocontrol.2020.104397.
Hopper, J.V., Pratt, P.D., Reddy, A.M., McCue, K.F., Rivas, S.O., Grosholz, E.D. 2020. Abiotic and biotic influences on the performance of two biological control agents, Neochetina bruchi and N. eichhorniae, in the Sacramento-San Joaquin River Delta, California (USA). Biological Control. 153. Article 104495. https://doi.org/10.1016/j.biocontrol.2020.104495.