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A Vector Analysis of Marine Ornamental Species in California

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A Vector Analysis of Marine Ornamental Species in California Management of Biological Invasions (2015) Volume 6, Issue 1: 13–29 doi: http://dx.doi.org/10.3391/mbi.2015.6.1.02 Open Access © 2015 The Author(s). Journal compilation © 2015 REABIC Research Article A vector analysis of marine ornamental species in California Susan L. Williams1*, R. Eliot Crafton2, Rachel E. Fontana1,2,3, Edwin D. Grosholz4, Grace Ha1,2, Jae R. Pasari1 and Chela J. Zabin4,5 1Bodega Marine Laboratory and Department of Evolution and Ecology, University of California at Davis, PO Box 247, Bodega Bay, CA 94923 USA 2Graduate Group in Ecology, University of California at Davis, Davis, CA 95616 USA 3Present address: Office of Oceanic and Atmospheric Research, National Oceanic and Atmospheric Administration, Silver Spring, MD 20910 USA 4Department of Environmental Science and Policy, University of California at Davis, Davis, CA 95616 USA 5Smithsonian Environmental Research Center, Tiburon, CA 94920 USA E-mail: [email protected] (SLW), [email protected] (REC), [email protected] (REF), [email protected] (EDG), [email protected] (GH), [email protected] (JRP), [email protected] (CJZ) *Corresponding author Received: 9 July 2014 / Accepted: 28 October 2014 / Published online: 10 December 2014 Handling editor: Alisha Davidson Abstract The trade in marine and estuarine ornamental species has resulted in the introductions of some of the world’s worst invasive species, including the seaweed Caulerpa taxifolia and the lionfish Pterois volitans. We conducted an analysis of the historical introductions and establishments of marine and estuarine ornamental species in California using a database (‘NEMESIS’) and the contemporary fluxes (quantities, taxa) based on government records, direct observations of aquarium-bound shipments, and internet commerce. California is the major port of entry of marine ornamental species in the United States, which is the major global importing country. The vector was considered possibly responsible for twelve species introduced between 1853–2011, nine of which successfully established, including Caulerpa taxifolia (Mediterranean invasive strain). The flux of imported ornamental species was over 11 million individual animals in 2009 and included 37 taxa from at least six temperate countries, although the majority originated from the Indo-Pacific region. Almost 4,000 individuals representing at least 149 species were imported into San Francisco on a single day in 2012. Estimates of imported quantities were probably accurate within an order of magnitude but could be improved with data on interstate shipments and internet commerce. Importations of high concern included P. volitans, live rock, Chromis viridis (green chromis), and Cromileptes altivelis (panther or humpback grouper). The low historical establishment rate for ornamental species hypothetically could be explained in part by a low release rate or temperature mismatch, but the flux remains high and is a growing concern that could be addressed by heightened public education. Key words: invasive, marine, ornamental, aquarium, internet commerce, vector countries where specimens are collected (Edwards Introduction and Shepherd 1992; Kay and Hoyle 2001; Bruckner 2005; Wabnitz et al. 2003; Bunting et al. 2008; The trade in ornamental (‘aquarium') species can Secretariat of the Convention on Biological be a potent vector for the introduction of non- Diversity 2010). Most research on the ornamental indigenous species (NIS) (Les and Mehrhoff 1999; species trade has focused on potential impacts to Padilla and Williams 2004; Cohen et al. 2007; biodiversity from destructive collection and Gertzen et al. 2008; Maceda-Veiga et al. 2013). shipping practices in the source regions (Edwards Exotic plants and animals are prized for their and Shepherd 1992; Kolm and Berglund 2003; beauty and novelty, making the ornamental trade Shuman et al. 2005; Smith et al. 2008, 2009; lucrative and resulting in its promotion as a Rhyne et al. 2012b, 2014). Far less attention has means of potentially sustainable development for been devoted to the potential ‘downstream’ 13 S.L. Williams et al. environmental effects of releasing marine NIS at as cited above for Caulerpa taxifolia. We their final destination (Andrews 1990; Semmens conducted a vector analysis of the organisms et al. 2004; Calado and Chapman 2006; Whittington circulating in the trade and estimated vector and Chong 2007). strength, sensu Ruiz and Carlton (2003). As a vector for invasive species, the marine Specifically, we assessed the 1) historical marine and estuarine (hereafter ‘marine’) ornamental NIS introductions and establishments attributed trade generally has received less attention from to the ornamental vector, 2) contemporary flux scientists and policy makers than other maritime as the number or biomass of taxa and individuals and freshwater vectors such as ballast water circulating in the vector including key species in (Ruiz et al. 2000; Weigle et al. 2005). However, internet commerce, and 3) literature on the NIS introduction via the ornamental trade is ecological and economic impacts reported for the different from other aquatic vectors in at least marine ornamental species established in California. two important ways. First, few if any ornamental species arrive in direct contact with the environ- Methods ment, unlike organisms fouling vessel hulls or entrained in ballast water. Second, although their Historical introductions: vector analysis and release rate might be low, ornamental species are strength often hardy and large or fully-grown (Duggan et To conduct a historical vector analysis of the al. 2006), increasing the likelihood of survival number of introductions attributed to the vector and establishment if released (Keller and Lodge (‘vector strength’), we extracted a list of the 2007). introduced and established non-native marine This study describes and broadly assesses the and estuarine species in California attributed to ornamental trade as a vector for marine and the ornamental trade from the National Exotic estuarine (hereafter ‘marine’) ornamental species Marine and Estuarine Species Information System in California. The annual global flux of marine database (‘NEMESIS’, Fofonoff et al. 2013). ornamental species is enormous and the majority NEMESIS includes non-native species that have is exported to the United States (US) and landed been introduced, thought to have established, in California (Balboa 2003; Wabnitz et al. 2003; failed to establish, or have gone extinct or were Tissot et al. 2010). The number of fishes alone eradicated since establishment. NEMESIS records imported into the entire US between 1997–2005 were compiled from the peer-reviewed scientific was estimated at millions of individuals and the gray literature from 1853 through 2011. (Wabnitz et al. 2003; Rhyne et al. 2012a). To estimate vector strength, we used the NEMESIS Examples of invasive ornamental species include assignment of vectors to species, which was based lionfishes (Pterois volitans (Linnaeus 1758)/P. on evidence linking introductions to vectors, miles (Bennett 1828) (Albins and Hixon 2008; species’ life history characteristics, and the Schofield 2010) and the seaweed Caulerpa history of vector operation in specific locations taxifolia (invasive Mediterranean strain) (Meinesz (Fofonoff et al. 2013; Williams et al. 2013). et al. 2001; Meusnier et al. 2002). Caulerpa Additional information on dates of first and taxifolia has been a costly invasive species; its subsequent records on a bay-by-bay basis was successful eradication in California incurred at included (P. Fofonoff and B. Steves, pers. com). least $6 million over the four years required to NEMESIS records through 2006 have been treat two infestations (Jousson et al. 2000; comprehensively reviewed; species added from Withgott 2002; Anderson 2005). 2007 to present are still under review. Crypto- The specific objectives of this study were to genic (i.e., of uncertain origin, Carlton 1996) and characterize the marine ornamental vector and strictly freshwater were excluded from our evaluate the sources and quality of data relevant analysis. We used the year of the first report in for assessing the risk of NIS introductions to California as a proxy for year of introduction. California. In addition to being a major port of entry for marine ornamental species, California Contemporary fluxes is also a major introduction point for NIS to the west coast of North America (Ruiz et al. 2011). To assess the flux of taxa and quantities of The large marine economy of California (Kildow ornamental species currently circulating in the and Colgan 2005) is potentially at risk, and vector operating in California, we obtained significant resources have already been directed importation inspection records from the US Fish to managing invasive marine ornamental species, and Wildlife Service (USFWS)’s Law Enforcement 14 Marine ornamental vector in California Management Information System (LEMIS) unlikely to survive, alive, active/responsive), through a Freedom of Information Act (FOIA). taxonomic identification errors, and discrepancies We requested records for 2009 (the most recent between shipment contents and invoices year for which records were complete) for the (importer information redacted by USFWS). state’s major ports of Los Angeles (LA) and San We also reviewed California Department of Francisco (SF), the only Californian ports inspected Fish and Wildlife (CDFW, previously California by USFWS (any importations into other ports are Department
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