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Research Project: Development and Implementation of Biological Control Programs for Natural Area Weeds in the Southeastern United States

Location: Invasive Plant Research Laboratory

2021 Annual Report

The objectives of this project plan are to develop environmentally safe, self-sustaining methods for the management of invasive weeds of exotic origin that threaten ecologically sensitive aquatic and terrestrial ecosystems of the United States, with a focus on the southeastern region. The following four objectives are relevant to the NP 304 Action Plan, Component 2 – Weeds; Problem Statement 2B: Biological control and ecosystem research and Problem Statement 2C: Integrated approaches to weed management. Objective 1: Identify and prioritize invasive weeds that negatively affect ecologically sensitive terrestrial and aquatic ecosystems of the southeastern United States. [C2, PS 2C] Objective 2: Survey native habitats of the candidate weeds in their geographical areas of origin for potential biological control agents. Acquire and characterize biological control agents and conduct thorough host-specificity tests informed by molecular phylogeny to determine fundamental host range. [C2, PS 2B] Objective 3: Deploy APHIS-approved biological control agents and evaluate their efficacy by documenting impacts to target weed populations. [C2, PS 2B] Objective 4: Evaluate impact of biological control projects on native plant diversity, invertebrate food webs, and plant disease dynamics at community and landscape levels. Develop integrated methods to improve overall weed management efforts. [C2 PS 2B and 2C]

Biological control research is a dynamic process and thus the proposed research objectives detailed below are often interconnected, flexible, with feedback loops. Although we have presented discrete research objectives in a generalized fashion to accommodate the various weed targets and their natural enemies which are currently under investigation, some may be removed and others added during the life of the proposed 5 yr research project. A Milestone Table has been prepared for each objective which details the hypotheses, scientific assignments, annual goals (milestones), and expected outcomes of the given research activities

Progress Report
Melaleuca quinquenervia is an evergreen tree, introduced into southern Florida in 1886, and by 1994 had infested about 800 square miles. Infestations of melaleuca outcompete native plants, eliminate animal habitats, increase fires, disrupt nutrient storage and cycling, and affect human health. Classical biological control programs at the USDA-ARS Invasive Plant Research Lab (IPRL) in Fort Lauderdale, Florida, have transformed this plant into a less invasive form that no longer dominates the landscape and is now much easier to control using conventional methods. The latest prospective biological control agent is the galling fly Lophodiplosis indentata. A completed host range examination was submitted to the Technical Advisory Group (TAG) for evaluation, and in May 2020 was recommended for release. The application to release L. indentata is now undergoing review with USDA. Old World climbing fern, Lygodium microphyllum, is a climbing fern native to tropical Asia that has invaded Florida and is smothering tree islands, cypress domes, pine woodlands, and tropical hammocks in the Everglades and peninsular Florida. To date, IPRL has developed and established a moth and a mite whose ranges continue to increase across Florida. An additional 366,971 brown lygodium moths (Neomusotima conspurcatalis) and 267,047 mites (Floracarus perrepae) were released at remote and key conservation areas throughout central and south Florida. Outbreaks of the moth continue to be observed in multiple locations leading to browning out of lygodium populations. ARS scientists in Fort Lauderdale, Florida, continue to learn more about the biology of F. perrepae to optimize rearing and release methods, and increase establishment of the mite, which can cause a fourfold reduction in growth rates of attacked rachises. Long-term research is quantifying the damage these agents cause to Lygodium in the field both on their own and as part of an integrated weed management strategy. New biological control agents for lygodium continue to be developed including two leaf feeding moths, a sawfly, and four species of stem borers. The moth, Lygomusotima stria, shows high specificity after quarantine testing against 69 non-target plants. IPRL scientists in Fort Lauderdale, Florida, are collaborating with a modeler to project the potential range of this candidate agent compared to the range of the US native plant L. palmatum. Molecular analysis confirmed that a December 2019 collection of the lygodium sawfly, Neostrombocerus albicomus, can be merged with the IPRL quarantine colony to increase colony diversity before completing host range testing. The noctuid moth Callopistria exotica has been tested against 59 non-target species with plant production and acquisition underway for additional species. This insect feeds voraciously and is a lygodium specialist, with a clear preference for the two invasive lygodium species present in the U.S. Chinese tallow, (Triadica sebifera), is an invasive tree that has invaded about 500,000 acres of southern U.S. forests where it reduces timber harvests and wildlife habitat. The TAG, USDA-APHIS, and USFWS approved the release of the biological control agents, the flea beetle (Bikasha collaris) and the moth Gadirtha fusca. Currently we are waiting for USDA-APHIS to issue a release permit. Research to maximize agent production indicated that potting media affect rearing success of the root feeding flea beetle, B. collaris. Rearing conditions for G. fusca, including survival, development rate, pupal weights, and fecundity where greatest at 25 C temperature. Diapause in G. fusca larvae was induced by short photoperiod resulting in greater pupal weights and slower development rates. Brazilian peppertree (BP), Schinus terebinthifolia is one of the worst invasive weed species in southern Florida, occupying over 700,000 acres, more area than melaleuca and lygodium combined. It displaces and degrades Florida’s ecosystems, which include the Florida Everglades Ecosystem and, more specifically, plant communities such as cypress, hammocks, pinelands, and mangroves. Biological control agents may provide land managers and farmers with a cost-effective means of controlling Brazilian pepper by reducing the current and expensive reliance on herbicidal and mechanical control. The newly implemented mass rearing project with the thrips, Pseudophilothrips ichini for the biological control of Brazilian pepper continues to grow. Mass production techniques in large screen cages and field nurseries have been developed and shared with other USDA and State agencies. During the FY 2021, 607,460 adult thrips have been released at 348 locations in nine southern Florida counties and biocontrol impact research sites. Currently, preliminary results indicate that field populations have established at numerous locations with damage to Brazilian peppertree infestation becoming more apparent. Effective sampling methods are being developed to monitor thrips populations. Thrips dispersal is being monitored at several sites and thrips have been found to disperse 35 m from a central release point over the course of 12 months. Food web studies as part of Brazilian pepper tree biocontrol research have been concluded. Two semi-permanent long-term field research sites have been established during FY 2021 and two additional sites will be established during the first quarter of FY 2022 aiming at representing north-south distribution range of BP in Florida. Waterhyacinth, Pontederia crassipes, is often described as the world’s worst floating aquatic weed, damaging ecosystems, economies, and even public health of developing countries. The planthopper Megamelus scutellaris was the first new biological control agent released against waterhyacinth in more than 30 years and is now widely established in southern and northern Florida locations. To accommodate new projects (see section below under Accomplishments) and based on the widespread establishment of M. scutellaris, we scaled back rearing and release efforts. Waterlettuce, Pistia stratiotes, is a serious floating weed of the southeastern U.S. Genetic research comparing worldwide populations of this weed have identified at least 7 distinct clades, 3 of which may possibly be new cryptic species. One of these appears to be native in countries bordering the Caribbean (including Florida), and another may be more broadly native throughout the Americas (including portions of US Gulf Coast). This discovery has postponed efforts to gain approval to release the Argentine planthopper Lepidelphax pistae in the U.S. Air potato (Dioscorea bulbifera) vine is one of the most invasive climbing vines of exotic origin. It has spread throughout public and private forested properties in all 67 Florida counties and in other adjacent states. IPRL has developed two genotypes (Nepalese and Chinese) of a biological control beetle Lilioceris cheni that feed only on air potato leaves and vine-tips. Agents have been mass reared and released during FY 2012-2020 and additional 565 at 10 locations in 2021. Focus of the project has now shifted to another agent, Lilioceris egena, which feeds and develops on this vine’s vegetative propagules (called bulbils). Following APHIS approval in March 2021, beetle colonies have been removed from biocontainment, mass-rearing has begun, and initial releases have been conducted. Earleaf acacia (Acacia auriculiformis) is a fast-growing, evergreen tree that invades agricultural, disturbed, and natural areas of Florida in the wetland/upland ecotone. Extensive field surveys in Australia discovered dozens of potential agents including various seed feeding beetles, leaf feeding beetles (Calomela sp. and Dicranosterna sp.), foliage feeding mites, fruit galling flies, leaf tying caterpillars, two species of mirid bugs, including Riptortus sp., and a galling wasp, Trichilogaster sp. Foreign surveys for additional agents have been scaled back and only include unsurveyed areas in the indigenously-controlled Arnhemlands in Northern Territory. The beetle Calomela intermerata passed initial screening for host specificity in Australia and has been imported into the quarantine facility in Fort Lauderdale where it is currently undergoing host range evaluation, biology studies, and impact assessments. Additionally, rearing protocols for Trichilogaster have been established and host range tests have commenced in Australia at the Australian Biological Control Laboratory (ABCL). A Next Generation GBS population study, displaying the origins of the Florida invasive population as the Northern Territories, Australia, has been published. Additionally, temperature dependent development and reproduction studies are now underway with the Queensland and Northern Territory genotypes of C. intemerata. Casuarina species, or Australian pine, are fast growing evergreen trees that have become serious invasive weeds of agricultural, urban, and coastal areas in the US especially in southern Arizona, California, Florida, Hawaii, and Texas. With their shallow root system, they are extremely dangerous as they are prone to fall during extreme wind events causing economic damage to agriculture, homes, and businesses. Casuarina trees produce thick blankets of leaves that leach toxic substances preventing the germination of other plants. When in flower, people suffer from allergic reactions to the abundant amounts of pollen produced seasonally. Biological control is being examined with the USDA-Australian biological control lab and has discovered and prioritized several agents with potential to be safe and effective. These include the gall inducing wasps Selitrichodes spp, the seed feeders Bootanelleus orientalis and Dasineura sp., the defoliating moths, Cryptophasa irrorata, and Calathusa maritime, and a cecidomyiid tip gall midge Ophelmodiplosis clavate.

1. Release of the air potato beetle, Lilioceris egena. Air potato (Dioscorea bulbifera) is a subtropical Old World vine that has become invasive along the Gulf Coast, especially Florida. ARS researchers at Fort Lauderdale, Florida, received a permit to release the beetle Lilioceris egena in the U.S., having shown that this beetle is a specialist on the reproductive bulbils (‘potatoes’) associated with air potato. Despite slowed growth and bulbil production caused by a previously released Asian beetle (Lilioceris cheni), stakeholders face significant infestations resulting from germination of those bulbils still being produced. By attacking these bulbils, L. egena will significantly impede population regrowth allowing native species to reclaim stakeholder lands currently covered by air potato.

2. New Areawide Project on Integrated Pest Management of Water Hyacinth. ARS researchers at Fort Lauderdale, Florida received funding for this project which will elucidate potential new management practices utilizing the full suite of available biological control insects, integrated with other control measures. Initial studies continue to mount strong evidence for the efficacy of integrated management of waterhyacinth: reduced herbicide rates and increased time intervals yield the same results as higher inputs when insects are present. Resources from this new award will also explore the viability of Thrypticus spp. for use as biological control agents. Flies in this genus are closely related and often cryptic, confusing initial workers. Excellent research from the Fundacíon para el Estudio de Especies Invasivas (FuEDEI) teased apart these species and now have pure lines of a species of Thrypticus believed to specialize on P. crassipes.

3. New Biological Control Agent for Chinese Tallow. Host range testing indicated the flea beetle, Bikasha collaris and the moth Gadirtha fusca will be safe for release. This release was recommended by Technical Advisory Group and U.S. Fish & Wildlife Service (USFWS). ARS scientists in Fort Lauderdale, Florida, are waiting for the issuance of a release permit from USDA-APHIS. When the release is approved, these biological control agents may provide land managers and farmers with a cost-effective means of controlling Chinese tallow by reducing the current reliance on herbicidal control.

Review Publications
David, A.S., Carmona Cortes, A., Lake, E.C. 2021. Bottom-up factors determine local, but not regional, distribution of a biological control agent against invasive Lygodium microphyllum. Biological Control. 159.
Tipping, P.W., Martin, M., Foley, J., Pierce, R., Gettys, L. 2021. The influence of two wildfires and biological control agents on the population dynamics of Melaleuca quinquenervia in a seasonally inundated wetland. Invasive Plant Science and Management. 14(1):3-8.
David, A.S., Glueckert, J.S., Enloe, S.F., Carmona Cortes, A., Abdel-Kader, A.A., Lake, E.C. 2021. Eriophyid mite Floracarus perrepae readily colonizes recovering invasive vine Lygodium microphyllum following herbicide treatment. Biocontrol. 66:573-584.
Wheeler, G.S., David, A.S., Lake, E.C. 2021. Volatile chemistry, not phylogeny, predicts host range of a biological control agent of Old-World climbing fern. Biological Control. 159.
Goode, A.B., Tipping, P.W., Minteer, C.R., Pokorny, E.N., Knowles, B.K., Foley, J.R., Valmonte, R. 2021. Megamelus scutellaris (Berg) (Hemiptera: Delphacidae) biology and population dynamics in the highly variable landscape of southern Florida. Biological Control. 160(2021).
David, A.S., Carmona Cortes, A., Wheeler, G.S., Lake, E.C. 2021. Localized induced defenses limit gall formation by eriophyid mite against invasive Lygodium microphyllum. Environmental Entomology. 50(4):814:820.
Mcculloch, G., Madeira, P.T., Makinson, J., Dutoit, L., Blair, Z., Walter, G., Nawaz, M., Purcell, M. 2020. Phylogenomics resolves the invasion history of Acacia auriculiformis in Florida. Journal of Biogeography. 48(2):453-464.
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.
Kazanski, C., Cowles, J., Dymond, S., Clark, A., David, A.S., Jungers, J., Kendig, A., Riggs, C., Trost, J., Wei, X. 2021. Water availability modifies effects of biodiversity and nitrogen addition on plant productivity in long-term experiments in a mesic grassland. Ecological Applications. 31(6).
French, S.S., Virgin, E.E., Ki, K.C., Maryon, D.F., Goode, A.B., Pasachnik, S.A. 2021. Reproductive stage and clutch size incur energetic and oxidative costs in an endangered iguana, Ctenosaura oedirhina. Herpetologica. 55(2):192–200.
Goode, A.B., Tipping, P.W., Pokorny, E.N., Knowles, B.K., Salinas, L.S., Gettys, L.A. 2020. Proximity to host plant of a congener determines parasitism of a waterhyacinth biological control agent by a native parasitoid. Biological Control. 153.
Halbritter, D.A., Wheeler, G.S. 2021. Life history trade-offs of thrips reared on fertilized and unfertilized Brazilian peppertree with respect to changes in plant terpenoid profiles. Biological Control. 156 (2021) 104553.
Lake, E.C., David, A.S., Spencer, T., Wilhelm, V., Barnett, T., Abdel-Kader, A., Carmona Cortes, A., Acuna, A., Mattison, E.D., Minteer, C. 2020. First drone releases of the biological control agent Neomusotima conspurcatalis on Old World climbing fern. Biocontrol Science and Technology. 31(1):97-106.
Goode, A.B., Knowles, B.K., Tipping, P.W., Foley, J., Gettys, L. 2020. Interactions among biological control agents on waterhyacinth: impacts of herbivory on the oviposition and development of Megamelus scutellaris. Biocontrol Science and Technology. 30(11):1244-1249.
Hernandez, D., David, A.S., Menges, E., Searcy, C., Afkhami, M. 2021. Environmental stress destabilizes microbial networks. The ISME Journal: Multidisciplinary Journal of Microbial Ecology. 15:1722–1734.
Minteer, C., Smith, M., Madeira, P.T., Goosem, C., Zonnevald, R., Makinson, J., Wheeler, G.S., Purcell, M. 2020. Is biological control for earleaf acacia (Acacia auriculiformis) Feasible in the United States? Biocontrol Science and Technology. 30(12):1275-1299.
Tipping, P.W., Martin, M., Rayamajhi, M.B., Pratt, P.D., Gettys, L. 2021. Comparing the Invertebrate Communities and the Decomposition Dynamics Between Dead Native and Non-Native Trees in a Seasonal Everglades Wetland. Ecology and Evolution.