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Brazilian Peppertree): a Review of the Project with an Update on the Proposed Agents Author(S): Gregory S

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Brazilian Peppertree): a Review of the Project with an Update on the Proposed Agents Author(S): Gregory S Biological Control of the Invasive Weed Schinus terebinthifolia (Brazilian Peppertree): A Review of the Project with an Update on the Proposed Agents Author(s): Gregory S. Wheeler, Fernando Mc Kay, Marcelo D. Vitorino, Veronica Manrique , Rodrigo Diaz , and William A. Overholt Source: Southeastern Naturalist, 15(sp8):15-34. Published By: Eagle Hill Institute https://doi.org/10.1656/058.015.sp802 URL: http://www.bioone.org/doi/full/10.1656/058.015.sp802 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Everglades Invasive Species 2016 Southeastern Naturalist 15(Special Issue 8):15–34 Biological Control of the Invasive Weed Schinus terebinthifolia (Brazilian Peppertree): A Review of the Project with an Update on the Proposed Agents Gregory S. Wheeler1,*, Fernando Mc Kay2, Marcelo D. Vitorino3, Veronica Manrique4, 5, Rodrigo Diaz4, 5, and William A. Overholt4 Abstract - Schinus terebinthifolia (Brazilian Peppertree) is a South American plant that has become invasive in many countries around the world. It was introduced into the US about 100 years ago as an ornamental. Escaping cultivation, it now occurs in Alabama, Florida, Georgia, Texas, California, and Hawai’i. This species is one of the most invasive weeds threatening agriculture and natural areas in the Southeast. Efforts to manage Brazilian Pep- pertree populations with biological controls began in Hawai’i in the 1950s and resulted in the release of 3 insect species. However, the control agents have had minimal impact, and the weed continues to be a difficult problem. More recently, our international team of col- laborators has discovered and tested numerous new species of potential biological control agents. These species attack different plant tissues and include defoliators, sap-suckers, stem borers, and leaf- and stem-gall formers. Despite difficulty finding an agent sufficiently specific for field release in Florida, we have narrowed the field to 2 promising species, the thrips Pseudophilothrips ichini (Hood) and the foliage-gall former Calophya latiforceps Burckhardt. Results of no-choice and choice trials conducted overseas and in quarantine indicate that both species will safely contribute to the control of this invasive weed. Her- bivorous feeding by immature and adult individuals of both herbivore species stunt growth, distort leaves, and should reduce reproductive output of Brazilian Peppertree. Introduction Schinus terebinthifolia Raddi (Brazilian Peppertree) (Anacardiaceae), native to South America, is one of the most aggressive and widespread invasive species in Florida and Hawai’i (Ewel 1986, Rodgers et al. 2014). Also known as Christmas Berry in Hawai’i, this species constitutes a threat to natural areas, agriculture, and cattle production (Ewel 1986, Morton 1978, Yoshioka and Markin 1991). Brazil- ian Peppertree has successfully colonized most of the Florida peninsula, covering more than 280,000 ha (700,000 acres) with thick monospecific stands that eliminate understory-plant growth (Schmitz et al. 1997). In the Florida Everglades ecosys- tem, Brazilian Peppertree is the most widely distributed and abundant invasive 1Invasive Plant Research Laboratory, USDA-ARS, 3225 College Avenue, Ft. Lauderdale, FL 33314. 2FuEDEI, formerly USDA/ARS/SABCL, Buenos Aires, Argentina. 3Programa de Pós-graduação, em Engenharia Florestal PPGEF, Universidade Regional de 10 Blumenau, Blumenau, SC, Brazil 89012-900. 4Biological Control Research and Containment Labora- tory, University of Florida, 2199 South Rock Road, Ft. Pierce, FL 34945. 5Department of Entomology, Louisiana State University, Baton Rouge, LA 70803. *Corresponding author - [email protected]. Manuscript Editor: Brett Serviss 15 2016 Southeastern Naturalist Vol. 15, Special Issue 8 G.S. Wheeler, F. Mc Kay, M.D. Vitorino, V. Manrique, R. Diaz, and W.A. Overholt weed, occupying 30,379 ha—an area greater than the combined infestations of the next 3 most-problematic plant species (Rodgers et al. 2014). In Hawai’i, surveys conducted in the early 1990s estimated that 50,000 ha were moderately to heavily infested, with another 200,000 ha infested with occasional to scattered plants (Yo- shioka and Markin 1991). In its naturalized range, Brazilian Peppertree decreases biodiversity in coastal and upland habitats (Gann et al. 2015, Mytinger and Wil- liamson 1987). The South Florida Water Mangement District spent an estimated $1.7 million to control Brazilian Peppertree in 2011, and the Florida Department of Environmental Protection spent over $10.5 million for herbicide treatment between 1998 and 2006 (G. Jubinsky, Florida Fish and Wildlife Conservation Commission, Tallahassee, FL, pers. comm.; Rodgers et al. 2012). The US Fish and Wildlife Service (1998) identified Brazilian Peppertree as one of the most significant non- indigenous species currently impacting federally listed threatened and endangered native plants throughout the Hawaiian Islands. Brazilian Peppertree also disrupts traditional Hawaiian archeological settlements because its roots erode protected historic features, especially unfortified rock walls (Leary and Gross 2013). Brazil- ian Peppertree produces allelopathic compounds that suppress the growth of other plant species (Gogue et al. 1974, Morgan and Overholt 2005). Volatiles released by the leaves, flowers, and fruits of this species cause allergic reactions and respiratory illness in sensitive people (Morton 1978, Stahl et al. 1983), and ingestion of the leaves and fruits can have narcotic and toxic effects in grazing animals and birds (Campello and Marsaioli 1974, Morton 1978). Chemical- and mechanical-control measures have been used with some short-term success; however, permanent cost- effective maintenance programs are required to prevent regrowth, particularly in remote wildlands where other control measures are logistically difficult (Doren and Jones 1997). Classical biological control may provide an ecologically sound, cost-effective, and sustainable component of management strategies to protect na- tive plants in these habitats. Our purpose here is to briefly summarize the history of biological control of Brazilian Peppertree and the current status of our project. Surveys of Native Range One of the initial steps in a biological control project is to delimit the native range of the target weed in order to search for agents in a diverse assemblage of habitats. Brazilian Peppertree is a species that covers a latitudinally broad native range, extending from Natal, Brazil (5.8°S) to near Maldonado, Uruguay (34.8°S; Mukherjee et al. 2012, JBRJ 2015, Tropicos.org 2015, G.S. Wheeler, unpubl. data). The northern portion of this distribution remains within about 100 km of the Atlan- tic coast until Minas Gerais and Sao Paulo states, Brazil where it extends west into eastern Paraguay and adjacent northeastern Argentina (Fig. 1). Initial surveys to search for potential biological control agents for Brazilian Peppertree were conducted in northern Argentina and Brazil in the 1950s and early 1960s (Davis and Krauss 1962; Krauss 1962, 1963). The early surveys explored mostly the Brazilian states Minas Gerais, Rio de Janeiro, Sao Paulo, and Paraná, where numerous species of defoliating Lepidoptera, Coleoptera, and Hymenoptera 16 2016 Southeastern Naturalist Vol. 15, Special Issue 8 G.S. Wheeler, F. Mc Kay, M.D. Vitorino, V. Manrique, R. Diaz, and W.A. Overholt were found (Krauss 1962). Gall-forming Lepidoptera, Diptera, and seed-feeding Bruchidae were also reported (Krauss 1962). Bennett et al. (1990) and Bennett and Habeck (1991) conducted literature reviews and field surveys in the late 1980s. From surveys near Curitiba in Paraná state and review of Brazilian catalogs (Silva Figure 1. Map of area that encompasses the distribution of Brazilian Peppertree in its native range in South America. Black dots designate Brazilian Peppertree sites surveyed by the authors during biological control surveys (2005–2014). 17 2016 Southeastern Naturalist Vol. 15, Special Issue 8 G.S. Wheeler, F. Mc Kay, M.D. Vitorino, V. Manrique, R. Diaz, and W.A. Overholt et al. 1968), these authors estimated that 150 herbivore species may be associated with Brazilian Peppertree in Brazil. Beginning in 2005, we conducted South American surveys; the most recent of these occurred during August 2014. We intensively studied Brazilian Peppertree in the northeastern provinces of Argentina and details regarding surveys conducted there are provided in Mc Kay et al. (2009). We undertook 20 surveys during this 9-y period to describe the geographic range of Brazilian Peppertree in Brazil, cata- log the herbivores associated with the plant, and import under
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