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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

2019 Annual Report

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.

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 host-specific 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
Initiation of a biological control program requires long-term investment with significant up-front costs. It is necessary to prioritize weed targets for biological control based on the damage they cause to natural resources, and on the difficulty, cost feasibility and degree of efficacy of other control methods. Multiple ice plant species are widespread invaders of coastal habitats in California. Under Sub-objective 1.1, sea fig ice plant was sampled at 16 sites, and was not infested with Pulvinariella soft scales accidentally introduced to the U.S. in the 1950s. In 2019, due to requests from stakeholders, a second species known as crystalline ice plant was added to the study and sampled at five sites. Also under Sub-objective 1.1, a weed biological control prioritization process for the western U.S., developed in collaboration with scientists from Australia, was completed. The first phase harnessed the knowledge of 187 weed scientists and land managers across 10 states to compile a list of 33 key weeds, their impacts and management goals. The second phase used the expertise of biological control scientists and practitioners to assess the feasibility of pursuing a biological control program, and the likelihood of successfully achieving goals. Nine weeds were identified as having low priority for biocontrol, whereas 24 were considered moderate or high. Six weeds were characterized as having both high priority for successful biological control and greatest impact on natural environments. A final report was completed and circulated among stakeholders. Once target weeds have been selected, the host range, biology, and effectiveness of candidate biological control agents must be evaluated. Yellow-starthistle is the most widespread non-grass invasive weed in California rangelands. Under Sub-objective 1.2, a colony of the seedhead weevil, Larinus filiformis, was established in quarantine and life history studies were conducted to develop rearing methods and design parameters for host specificity testing. A field experiment was conducted in Greece to test host plant specificity. Russian thistle is one of the worst invaders of rangelands, roadsides, and agricultural areas in the arid western U.S. Under Sub-objective 1.2, pupae of the stem-boring moth, Gymnancyla canella, were collected in France and Italy and reared for host specificity testing. French broom has invaded pastures and forests in California, Oregon and Washington. Under Sub-objective 1.2, in efficacy tests of the shoot tip-galling weevil Lepidapion argentatum, galling by three females led to production of 48% more galls than did galling by one female. Galling reduced seedling height by 55%, canopy width 29%, and growth rate threefold. Studies were conducted on winter diapause requirements of the weevil, its life history, and host specificity. Cape-ivy smothers native plants and obstructs waterways in California’s sensitive coastal habitats. Under Sub-objective 1.2, evaluations of the leaf and stem-mining moth Digitivalva delaireae on a closely-related native plant, rayless ragwort, indicated that young larvae mined leaves at least 10-fold less frequently than on Cape-ivy. Tests on another close relative, arrowhead ragwort, confirmed prior results that the moth cannot complete immature development. A distantly-related rare plant was tested and did not support feeding. Moth pupae and technology for their rearing were provided to collaborators at the Commonwealth Science, Industry and Research Organization (CSIRO) in Canberra, Australia. In previous years, ARS scientists tracked dispersal of the Scotch broom gall mite, Aceria genistae, into California. Prior results indicated that the mite does not induce gall formation on native or exotic plant relatives. New research under Objective 1 investigated the influence of gall production on Scotch broom growth and reproduction. Plants replaced galled leaves but at a significant cost to reproduction. Medusahead, an annual grass that invades grazing lands and displaces forage species, is a close relative to wheat and other grain crops, and so a high level of host specificity is required for biological control. Recent surveys of Central and Eastern Europe by an ARS collaborator in Reno, Nevada, resulted in the discovery of a small mite (Aculodes altamurgiensis) that feeds on medusahead. Under Objective 1, the mite was reared under lab conditions on medusahead, but the mite was also able to complete development on wheat. The host range of the mite is thus too broad for use in biocontrol. Field surveys of medusahead plants in California revealed a small suite of herbivores attacking the exotic weed, including the medusahead mite. This mite is thus already present in California, but it remains unclear how it arrived and if it poses a threat to wheat. Collaborators at the Biotechnology and Biological Control Agency in Italy continue to search for insects that attack medusahead and will ship candidates to the ARS quarantine facility in Albany, California. The Australian melaleuca tree was introduced into Florida in the late 1800s, where it aggressively invaded wetlands in the Everglades. Melaleuca stands typically have large trees in the center and smaller individuals on the periphery. Smaller seedlings and saplings can be difficult for managers to treat due to their intermingled growth within a matrix of native species. The weevil Oxyops (O.) vitiosa was previously released in Florida as a biological control agent of the invasive tree but it remained unknown if the insect would locate small melaleuca at the edge of the weed’s invasion. ARS scientists monitored natural dispersal of the weevil into melaleuca stands to determine if the weevil preferentially selects larger trees. Results showed that tree size did not influence the likelihood of attack by O. vitiosa, as smaller individuals did not escape feeding damage. Scotch thistle is a tall spiny thistle native to Eurasia that has invaded rangeland in the Great Basin region. It has been successfully managed by biological control in Australia. Under Objective 1, a field experiment was conducted in Greece to test host plant specificity of the seedhead weevil, Larinus latus, which is considered to be the most effective agent in Australia. Under Objective 2, new biological control agents are being released against targeted weeds, the efficacy of released agents is being verified, and biocontrol is being combined with other control methods. Under Subobjective 2.1, in greenhouse choice tests, a yellow starthistle seed head-galling fly, Urophora sinuraseva, galled 40 percent of seed heads from French/Spanish plants and only 17 percent of seed heads from Greek plants, while a seed-feeding fly, Chaetorellia succinea, fed on 25 percent of seed heads from either region. The biocontrol agents came originally from Greece, while French/Spanish plants are genetically closest to invasive starthistle in the western U.S. The results provide insight into possible limitations on attack of seedheads by these biocontrol agents introduced many years ago. Dalmatian toadflax invades rangelands and natural areas throughout the western U.S. but has been reduced by a stem-mining weevil, Mecinus janthiniformis, that spread into California from neighboring states. Under Sub-objective 2.2, an eighth year of sampling was completed at field sites in southern California. The weevil dispersed 1 kilometer from release points, and abundance of Dalmatian toadflax declined two-fold. Stem height of toadflax plants declined by 50% between 2014 and 2017, but rebounded in 2018. Larvae of a root-feeding native moth, Penstemonia sp., was found on less than 10 percent of roots. In 2019, we continued to monitor changes in the weed population and the biological control agent. Arundo is a giant grass that invades riparian habitats in northern California and throughout the southwestern U.S. Under Sub-objective 2.3, surveys of six release sites in the Sacramento and San Joaquin River watersheds of northern California confirmed establishment of the shoot tip-galling arundo wasp Tetramesa romana at two sites, two years post-release. The arundo wasp did not establish at three sites in the Sacramento-San Joaquin Delta. Establishment of the root- and shoot bud-feeding arundo armored scale Rhizaspidiotus donacis was confirmed at six sites. A study on the effect of enhanced moisture on arundo wasp galling efficiency was continued in greenhouses, as was a field-based comparison of wasps derived from south Texas releases of known Spanish wasps, versus accidentally-released populations of unknown origin from southern California. Wasps from Texas were provided to a collaborator at the University of California (UC), Santa Barbara, for similar comparisons. Also under Sub-objective 2.3, releases and evaluations continued for the shoot tip-galling fly, Parafreutreta regalis, for biocontrol of Cape-ivy along the California coast. Two-year surveys of 2017 release sites indicated no evidence of establishment at most sites. One possible cause was low vigor of fly colonies. Flies collected in 2018 in the native range in South Africa were used to start new colonies, and by 2019 these produced 4.4-fold more galls per plant than before. Between September 2018 and February 2019, a new technique, involving five sequential releases of females into cages, was tested at seven sites. By June 2019, four sites from San Francisco to the Big Sur area had second-generation galls, and one site had abundant third-generation galls. Investigations of fly dispersal and impact were initiated. Technology for rearing, releasing and monitoring the fly was transferred to a collaborator at UC Santa Barbara. A new release technique involving pre-galled plants planted at the site is being tested, to avoid the need for expensive field cages.

1. Arundo wasp and armored scale established in northern California. The giant grass known as arundo invades shorelines along rivers, canals, and lakes in the arid southwestern U.S., including the Central Valley and Sacramento-San Joaquin River Delta of northern California. Arundo consumes water, hinders flood control, and fuels wildfires. ARS researchers at Albany, California, released the shoot tip-galling arundo wasp and root-feeding arundo armored scale, which are both proven biocontrol agents based on past releases in the Lower Rio Grande Basin of Texas and Mexico. After two years, the arundo wasp has established populations at two of six northern California release sites, and the armored scale is established at all sites. These insects, and technology for their release and monitoring, represent a promising new tool for integrated management of invasive arundo in critical watersheds in California.

2. Dalmatian toadflax weevil established in southern California. Dalmatian toadflax, a widespread invader throughout rangelands in the western U.S., has invaded natural grasslands with rare plant species in southern California. ARS researchers in Albany, California, working with collaborators from the California Department of Food and Agriculture, released a stem-mining weevil in 2014 in a state park, after a wildfire allowed Dalmatian toadflax to re-invade a prior release site. This site is the southernmost biocontrol site for this weevil in North America. After five years, the weevil has dispersed throughout the site, and Dalmatian toadflax abundance declined over two-fold, due to both the weevils and climatic factors. Native plants are abundant at the site and stand to benefit from reduction of Dalmatian toadflax. This weevil is a promising tool for biological and integrated control of Dalmatian toadflax at other sites at the southern edge of its invasive range.

Review Publications
Pratt, P.D., Grodowitz, M.J., Center, T.D., Rayamajhi, M.B. 2018. The reproductive biology of Oxyops vitiosa Pascoe, 1870 (Colepotera: Curculionidae), a biological control agent of the invasive tree Melaleuca quinquenervia (Myrtaceae). Pan Pacific Entomology. 94(3):117-129.
Tofangazi, N., Pratt, P.D., Rayamajhi, M.B., Tipping, P.W. 2019. The influence of plant size on attack rates of Oxyops vitiosa, an introduced herbivore of Melaleuca quinquenervia. Biocontrol Science and Technology. 29(6):610-613.
Bitume, E.V., Moran, P.J., Sforza, R. 2019. Impact in quarantine of the galling weevil Lepidapion argentatum on shoot growth of French broom (Genista monspessulana), an invasive weed in the western U.S. Biocontrol Science and Technology. 29(7):615-625.
Tang, Q., Yu, P., Tillman, M., Cohen, J., Slovin, J.P. 2018. Indole-3-acetyl-aspartate and indole-3-acetyl-glutamate, the IAA-amide conjugates in the diploid strawberry achene, are hydrolyzed in growing seedlings. Planta. 249(4):1073-1085.
Wang, R., Chen, H., Luo, Y., Yen, H., Arnold, J.G., Bubenheim, D., Moran, P.J., Zhang, M. 2019. Modeling pesticide fate and transport at watershed scale using the soil & water assessment tool: general applications and mitigation strategies. In: Goh, K.S., Gan, J., Young, D.F., Luo, Y., editors. Pesticides in Surface Water: Monitoring, Modeling, Risk Assessment, and Management. Washington, DC: ACS Publications. p. 391-419.
Pratt, P.D., Pitcairn, M.J., Oneto, S., Beaulieu, F., Sodergren, C., Michael, K.B., Knee, W., Andreas, J. 2019. Invasion of the gall mite Aceria genistae (Acari: Eriophyidae), a natural enemy of the invasive weed Cytisus scoparius, into California, U.S.A. and predictions for climate suitability in other regions. Biocontrol Science and Technology. 29(5):494-513.
Hopper, J.V., McCue, K.F., Pratt, P.D., Duchesne, P., Grosholz, E.D., Hufbauer, R. 2019. Into the weeds: matching importation history to genetic consequences and pathways in two widely used biological control agents. Evolutionary Applications. 12(4):773-790.
Martel, G., Auge, M., Talamas, E., Roche, M., Smith, L., Sforza, R. 2019. First laboratory evaluation of Gryon gonikopalense (Hymenoptera: Scelionidae) as potential biological control agent of Bagrada hilaris (Hemiptera: Pentatomidae). Biological Control. 135:48-56.