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Eleven Years of Range Expansion of Two Invasive Corals (Tubastraea Coccinea and Tubastraea Tagusensis) Through the Southwest Atlantic (Brazil)

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Eleven Years of Range Expansion of Two Invasive Corals (Tubastraea Coccinea and Tubastraea Tagusensis) Through the Southwest Atlantic (Brazil) Estuarine, Coastal and Shelf Science 141 (2014) 9e16 Contents lists available at ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Eleven years of range expansion of two invasive corals (Tubastraea coccinea and Tubastraea tagusensis) through the southwest Atlantic (Brazil) Amanda Guilherme da Silva a, Alline Figueira de Paula b, Beatriz Grosso Fleury c, Joel Christopher Creed c,* a Programa de Pós Graduação em Ecologia e Evolução, Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, CEP: 20550-900 Maracanã, Rio de Janeiro, Brazil b Petrobras, CEP: 20271-205 Maracanã, Rio de Janeiro, Brazil c Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, CEP: 20550-900 Maracanã, Rio de Janeiro, Brazil article info abstract Article history: We report on the temporal and spatial changes in populations of the invasive corals Tubastraea coccinea Received 4 November 2013 and Tubastraea tagusensis over an eleven year period at the Ilha Grande Bay, tropical southwest Atlantic. Accepted 30 January 2014 A semi-quantitative method was used to investigate the geographical distribution of the two congeners Available online 8 February 2014 on subtidal rocky reefs along 350 km of coastline by applying a relative abundance index (RAI) to quantify change. Data were compared among 2000, 2004, 2010 and 2011. The indices showed a transition Keywords: from rarity to dominance throughout the region as well as range expansion; in contrast at one site, where abundance a pilot management initiative of manual control has been carried out, there was a reduction in abun- coral distribution dance over time. Abundance values were compared to distance from possible points of introduction to range expansion pinpoint where the initial introduction occurred. The observed relationship between the possible points reef of entry and abundance of the two Tubastraea species was highly significant for the achorage and oil Tubastraea spp. terminal whereas somewhat less so for the shipyard and port. The data obtained in this study are being used to plan further urgent management actions to control the biological invasion of the two Tubastraea species throughout the region, as well as being applied in modeling the range expansion into other regions. Ó 2014 Elsevier Ltd. All rights reserved. 1. Introduction species can transform the structure and function of an ecosystem by creating novel interactions, or by changing fluxes of material and The rates and pathways by which species move around the energy through the system. planet have been completely modified by human action (Vitousek Tubastraea coccinea Lesson, 1829 and Tubastraea tagusensis et al., 1987). Shipping contributes to the elimination or reduction Wells, 1982 (Anthozoa; Dendrophyllidae) are considered to be the of the natural barriers that have always delimited marine ecosys- first scleractinian corals to have invaded the southern Atlantic, in tems, increasing homogenization of marine flora and fauna what is an uncommon two-species marine introduction. They are worldwide (Silva and Souza, 2004). The successful establishment of azooxanthellate, not depending directly on sunlight for their marine invasive species is largely due to the transport of ballast development, and can frequently be found in shaded places like water, and fouling on ships, platforms and floating objects (Carlton caves, overhangs and beneath boulders on subtidal tropical rocky and Geller, 1993; Carlton, 1996). Regardless of the pathways and shores and reefs (De Paula and Creed, 2005). T. coccinea is now mechanisms involved in the process of introduction, invasive considered to be a cosmopolitan species (Cairns, 1994). T. tagusensis was first described in the Galapagos Archipelago (Wells, 1982) but has also been recorded from Nicobar Islands (Cairns, 2000), Palau * Corresponding author. Laboratório de Ecologia Marinha Bêntica, Universidade (Cairns, 2000) and Kuwait (Hodgson and Carpenter, 1995). Both are do Estado do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, considered non-indigenous and invasive along the Brazilian coast Departamento de Ecologia, Rua São Francisco Xavier 524, PHLC Sala 220, CEP (De Paula and Creed, 2004), and T. coccinea has also been consid- 20550-900 Rio de Janeiro, RJ, Brazil. E-mail address: [email protected] (J.C. Creed). ered invasive in the Caribbean (since 1943, in Puerto Rico and http://dx.doi.org/10.1016/j.ecss.2014.01.013 0272-7714/Ó 2014 Elsevier Ltd. All rights reserved. 10 A.G.da Silva et al. / Estuarine, Coastal and Shelf Science 141 (2014) 9e16 Curacao, Cairns, 1994, 2000, Sammarco et al., 2010). T. coccinea subsequently dispersed throughout the Caribbean, and is found on oil rigs in the Gulf of Mexico and on hard grounds in Florida (Fenner and Banks, 2004). T. tagusensis is considered exotic to the Brazilian coast (De Paula and Creed, 2004). Another species of the genus, Tubastraea micranthus, was recently found on a single platform in the northern Gulf of Mexico (Sammarco et al., 2010), but has not yet been reported in Brazil. In Brazil, these invaders are widely distributed, with records of expansion into new areas including several Marine Protected Areas (Silva et al., 2011). The first record of the species on the Brazilian coast occurred in the 1980s, on oil and gas platforms belonging to Petrobras in the Campos Basin, north of the state of Rio de Janeiro (Castro and Pires, 2001). In the 1990s the genus was reported on the rocky shores of the Ilha Grande Bay (De Paula and Creed, 2004). Today, records have extended the occurrence to São Fig. 1. Map of the region of Ilha Grande Bay, Rio de Janeiro, Brazil, with the possible Paulo (Mantelatto et al., 2011), Espírito Santo, Santa Catarina points of entry of Tubastraea spp.: a) Port of Angra dos Reis, b) BrasFels Shipyard c) (Silva and Barros, 2011) and Bahia States (Sampaio et al., 2012), Petrobras Ilha Grande Bay Oil Terminal (TEBIG), d) Bananal Anchorage. along 2000 km of coastline as well as at least 20 oil platforms, drilling ships and floating, storage and offloading ships and mono buoys. 2.2. Monitoring As they are ecosystem engineers, once established Tubastraea fi spp. alter community structure and function (De Paula 2007). Ac- The eld studies were carried out in winter 2000, autumn- cording to Creed and De Paula (2007), Tubastraea spp. did not show winter 2004, winter 2010 and spring 2011. We used a fast, easily significant selection for specific substrate types, which may repeatable semi-quantitative method to carry out extensive contribute to their success in invading new areas. These corals also mapping of the distribution of Tubastraea coccinea and Tubastraea have reproductive characteristics typical of opportunistic species, tagusensis (De Paula and Creed, 2005) at 144 locations. Fieldwork such as high oocyte production, precocious reproduction age, short study locations were distributed approximately equidistantly embryo incubation time and hermaphroditism (De Paula, 2007). along the coastline and islands of the region to generate a ho- The secondary metabolites produced by these species provide an mogenous sampling effort but the exact study sites were chosen additional strategy which may facilitate their colonization and haphazardly from nautical charts with coordinates then fed into a fi expansion. Recent studies have shown that Tubastraea spp. produce GPS for location in the eld. At each site two snorkelers swam substances with anti-fouling and anti-predation properties (Lages parallel to the shore, estimating the density of each species of fi et al., 2010), besides releasing allelopathic substances capable of Tubastraea independently. Each diver conducted ve transects, causing tissue necrosis in the endemic coral Mussismilia hispida (De spending about 1 min recording per 25 m transect. Data recorded “ ” Paula, 2007; Lages et al., 2012). These characteristics ensure that were relative abundances using the DAFOR scale proposed by once established Tubastraea spp. can become the dominant benthic Sutherland (2006): Dominant, when populations Tubastraea spp. > 2 organisms (De Paula 2007), overwhelming native species and are extremely apparent, frequently occupying areas 1m; altering the dynamics of ecosystems that have been invaded (Lages Abundant, when Tubastraea spp. occurred frequently forming e et al., 2011). High cover of these species of Tubastraea changes patches of 10 50 cm diameter; Frequent, numerous isolated col- ecosystem functions compared to the more usual communities of onies or small patches of up to 50 cm in diameter; Occasional, e macroalgae and zooxanthellate cnidarians typical of these shores; when 5 10 colonies or small groups were counted per 1 min dive; fi the community becomes heterotrophic rather than autotrophic Rare, when one-to- ve colonies were counted in 1 min; Absent, (Lages et al., 2011). not seen during the 1 min dive (Sutherland, 2006; Silva et al., In order to best employ management strategies that can be used 2011). These observations were transformed to a quantitative to ameliorate marine biological invasions it is first necessary to relative abundance index (RAI) by assigning a scale from 10 quantify change in the abundance of the populations over time and (dominant), 8, 6, 4, 2 to zero (absent); a mean of the total of ten space in order to determine the rate of increase in abundance and transects was calculated. predict the rate and possible consequences of range expansion. Here we report eleven years of monitoring the distribution and 2.3. Data analysis abundance of the corals Tubastraea tagusensis and Tubastraea coc- cinea at the ground zero of the biological invasion of these species As initially we did not know that two different species co- in the Southwest Atlantic. occurred, in 2000 we quantified abundance only at the genus level (De Paula, 2002). The 2004 data were a compilation of data 2. Materials and methods collected in a separate study using identical methods during a Rapid Assessment of Marine Biodiversity e Marine RAP (Creed 2.1. Study area et al., 2007) supplemented by personal unpublished observations of A.F.
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