Genetic Characterization of an Invasive Boa Constrictor Population on the Caribbean Island of Aruba Author(S): Lauretta M
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Genetic Characterization of an Invasive Boa constrictor Population on the Caribbean Island of Aruba Author(s): Lauretta M. Bushar, R. Graham Reynolds, Sharese Tucker, LaCoya C. Pace, William I. Lutterschmidt, R. Andrew Odum, and Howard K. Reinert Source: Journal of Herpetology, 49(4):602-610. Published By: The Society for the Study of Amphibians and Reptiles DOI: http://dx.doi.org/10.1670/14-059 URL: http://www.bioone.org/doi/full/10.1670/14-059 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. Journal of Herpetology, Vol. 49, No. 4, 602–610, 2015 Copyright 2015 Society for the Study of Amphibians and Reptiles Genetic Characterization of an Invasive Boa constrictor Population on the Caribbean Island of Aruba 1,2 3 1 1 4 LAURETTA M. BUSHAR, R. GRAHAM REYNOLDS, SHARESE TUCKER, LACOYA C. PACE, WILLIAM I. LUTTERSCHMIDT, 5 6 R. ANDREW ODUM, AND HOWARD K. REINERT 1Biology Department, Arcadia University, 450 South Easton Road, Glenside, Pennsylvania 19038 USA 3Department of Organismic and Evolutionary Biology & Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138 USA 4Department of Biological Sciences and the Texas Research Institute for Environmental Studies, Sam Houston State University, 1806 Avenue J, Huntsville, Texas 77340 USA 5Department of Herpetology, Toledo Zoological Society, PO Box 140130, Toledo, Ohio 43614 USA 6Department of Biology, The College of New Jersey, 2000 Pennington Road, Ewing, New Jersey 08628 USA ABSTRACT.—Boa constrictor was first documented on the Caribbean island of Aruba in 1999. Despite intensive efforts to eradicate the snake from the island, B. constrictor has established a stable, reproductively successful population on Aruba. We generated mitochondrial sequence and multilocus microsatellite data for individuals from this population to characterize the origins and means of introduction to the island. Phylogenetic analyses and measures of genetic diversity for this population were compared with those for invasive B. constrictor imperator from Cozumel and B. constrictor constrictor from Puerto Rico. Cozumel populations of B. c. imperator had significantly higher numbers of alleles and significantly higher values for FIS than the Puerto Rico and Aruba populations. Observed, expected, and Nei’s unbiased heterozygosities, as well as effective number of alleles, were not significantly different. The effective population sizes from Aruba and Puerto Rico were generally lower than those for either of the Cozumel populations; however, there were broad confidence intervals associated with published estimates. We conclude that the present B. constrictor population on Aruba most likely resulted from the release or escape of a small number of unrelated captive snakes originating from South America (B. c. constrictor) and are phylogenetically distinct from introduced boas on Puerto Rico and Cozumel. This study adds to the growing body of evidence suggesting the ease with which a small number of relatively slow-maturing B. constrictor can quickly invade, become established, and avoid eradication efforts in a new location with suitable habitat. Invasive species can alter habitats, compete with native The release of several related neonate B. constrictor constrictor wildlife for limited resources, reduce biodiversity, and lead to around 1992 is believed to be responsible for the population on extirpation of native species (Pysˇek and Richardson, 2010). Puerto Rico, and B. c. constrictor on Puerto Rico share a Many reptile species have become naturalized and subsequently mitochondrial DNA haplogroup commonly found in breeding invasive outside of their native ranges, occasionally leading to collections and zoo specimens (Reynolds et al., 2013). significant ecological damage to invaded areas (Kraus, 2009). A Aruba is a small continental island approximately 33 km long now classic example, the Brown Treesnake (Boiga irregularia), and 8 km wide (~175 km2). The first five wild B. constrictor were was responsible for the extinction of at least 18 different species documented on the island in 1999, and in 2000 the government of birds, lizards, and bats within 50 yr of its introduction to of Aruba established a program whereby any B. constrictor Guam (Savidge, 1991; Mackessy et al., 2006). The Burmese found was collected, recorded, and euthanized. Despite these Python, Python bivittatus, was first observed in southern Florida efforts to eradicate the snake from the island, a reproductively approximately 30 yr ago and is implicated in the decline of successful population had been established by 2005 (Quick et several species of mammals in Everglades National Park al., 2005). All size classes have been reported, from neonates to (Dorcas et al., 2011). adults approaching 3 m total length, as well as gravid females A particularly interesting situation in invasion biology is (Quick et al., 2005). Ongoing research is determining the when species that are threatened in their native range become ecological impacts of this invasion, and initial dietary data invasive elsewhere. For example, several mainland and insular suggest that B. constrictor snakes on the island are euryphagous populations of Boa constrictor are considered threatened or (Quick et al., 2005). There is concern that B. constrictor could endangered (e.g., Chiaraviglio et al., 2003; Boback, 2005; directly compete with the endemic Aruba Island Rattlesnake Henderson and Powell, 2009), primarily as a result of (Crotalus unicolor), impact populations of native wildlife, and persecution, collection for the pet trade (Dodd, 1986), and prey upon domestic animals (Quick et al., 2005; van Buurt, hunting for their skins. Nevertheless, invasive populations of B. 2011). constrictor have recently become established in southern Florida Four important lines of inquiry can yield meaningful (Snow et al., 2007), on the Mexican island of Cozumel information in forensic invasive species genetics: species or (Martı´nez-Morales and Cuaro´n, 1999), and on the Caribbean lineage identification, geographic origins of the invasive islands of Puerto Rico (Reynolds et al., 2013) and Aruba (Quick individuals, assessment of evidence for propagule pressure or et al., 2005). The Cozumel population of B. constrictor imperator multiple introductions, and possible means by which the species is ecologically damaging (Romero-Na´jera et al., 2007) and is arrived in the invaded range (Fitzpatrick et al., 2012). believed to have become established island wide following the Furthermore, comparison among separately introduced popu- release of between 2 and 30 individuals in 1971 (Martı´nez- lations of invasive species might yield important population Morales and Cuaro´n, 1999; Va´zquez-Domı´nguez et al., 2012). genetic information germane to control efforts and the study of invasion biology. 2Corresponding Author. E-mail: [email protected] Boa constrictor is comprised of multiple highly divergent DOI: 10.1670/14-059 lineages (up to seven million years divergent; Sua´rez-Atilano et INVASIVE BOA CONSTRICTOR ON ARUBA 603 al., 2014), and identifying lineages present in an invasive data from studies on the invasive B. constrictor populations on population might shed light on origins and introduction history the islands of Cozumel and Puerto Rico. (Va´zquez-Domı´nguez et al., 2012; Reynolds et al., 2013). Boas on Cozumel belong to the Central American subspecies B. c. MATERIALS AND METHODS imperator, and established boas in Puerto Rico are South American B. c. constrictor. Some authors (e.g., Henderson and Sample Collection.—The first B. constrictor was documented on Powell, 2009) recognize West Indian populations of B. constrictor Aruba in 1999 (Quick et al., 2005), and the administration of as separate species (Boa nebulosa and Boa orophias), and recent Parke Nacional Arikok in conjunction with the Aruba Veterinaire work has suggested that B. c. constrictor and B. c. imperator Dienst established a program whereby any B. constrictor found should be elevated, with the potential for recognizing a third was collected, recorded, and euthanized. Prior to euthanasia, we species (Boa sigma) in Mexico (Reynolds et al., 2014; Sua´rez- obtained blood from 22 B. constrictor collected in 2007 (Fig. 1). We Atilano et al., 2014). These species are not yet formally excised tissue samples (tail tips) from 24 B. constrictor that were described; hence we continue to refer to the subspecies, but collected and euthanized in 2014 and stored at -208Cuntil we note that there are important ecological, evolutionary, and processing. Blood samples were stored at -20 or -808C, and tail conservation implications for