Distribution of the Invasive Orange Cup Coral Tubastraea Coccinea Lesson, 1829 in an Upwelling Area in the South Atlantic Ocean Fifteen Years After Its First Record

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Distribution of the Invasive Orange Cup Coral Tubastraea Coccinea Lesson, 1829 in an Upwelling Area in the South Atlantic Ocean Fifteen Years After Its First Record Aquatic Invasions (2017) Volume 12, Issue 1: 23–32 DOI: https://doi.org/10.3391/ai.2017.12.1.03 Open Access © 2017 The Author(s). Journal compilation © 2017 REABIC Research Article Distribution of the invasive orange cup coral Tubastraea coccinea Lesson, 1829 in an upwelling area in the South Atlantic Ocean fifteen years after its first record Daniela Batista1,*, Jose Eduardo Arruda Gonçalves1, Héctor Fabian Messano1, Luciana Altvater1, Rogério Candella1, Leandro Machado Calil Elias2, Luciana Vicente Resende De Messano1, Moacir Apolinário3 and Ricardo Coutinho1 1Instituto de Estudos do Mar Almirante Paulo Moreira IEAPM, Arraial do Cabo, RJ, Brazil 2Acquamodel Oceanografia Aplicada, Rio de Janeiro, RJ, Brazil 3Centro de Pesquisas Leopoldo Américo Miguez de Mello CENPES/PDES/AMA, Rio de Janeiro, RJ, Brazil *Corresponding author E-mail: [email protected] Received: 3 May 2016 / Accepted: 14 October 2016 / Published online: 22 November 2016 Handling editor: Elisabeth Cook Abstract A survey of the distribution and abundance of the invasive orange cup coral Tubastraea coccinea Lesson, 1829 was conducted using photoquadrats during 2014/2015, fifteen years after its first documented introduction in a Cabo Frio upwelling area in the western South Atlantic (42º00′W–22º44′S). These data were related to local currents and to a dispersion model of particles and with sea surface temperatures (SST). The objective was to investigate how variations in environmental conditions (local currents and temperatures) influence the dispersion and survival of T. coccinea. Complementary laboratory experiments were performed to investigate the effects of low temperatures on the survival of this species. T. coccinea has expanded its distribution and larval dispersion seems to be driven by the local currents. Furthermore, higher densities of colonies and recruits were observed within areas with higher water temperatures (>20 °C), while no coral was found in the area of direct upwelling influence, suggesting that cold waters limited the distribution of T. coccinea. These findings were corroborated by laboratory experiments that showed a negative effect of cold water (≤ 12.5 °C) on colony survival. The present data contribute to our understanding of the worldwide geographical expansion of T. coccinea and could be particularly important for management decisions to prevent new invasions. Key words: bioinvasion, orange cup coral, temperature, western South Atlantic, Brazil nutrient cycles, disturbance in natural communities Introduction integrity, and sometimes the extinction of native species (Carlton and Geller 1993; Lodge 1993; Grosholz and The globalization of maritime trade plays a key role Ruiz 1996; Lafferty and Kuris 1996; Crooks 1998; in the spread of marine species beyond their native Blackburn et al. 2014). ranges since many of them are dispersed as fouling The orange cup coral Tubastraea coccinea Lesson, on vessels and in ballast water (Seebens et al. 2013; 1829 is native to the Indo-Pacific province—from Williams et al. 2013; Katsanevakis et al. 2014). Non- the Red Sea and Madagascar to the tropical Americas, indigenous marine species (NIMS) generally exhibit occurring mostly in shallow waters (Fofonoff et al. fast growth, high recruitment rates, and elevated 2003). This azooxanthellate coral successfully invaded competition potential (Lodge 1993), being recognized the Western Atlantic Ocean in the 1930s through as one the major drivers of biodiversity changes shipping activities in the eastern Caribbean Sea worldwide (Montefalcone et al. 2015). These attributes (Cairns 2000). Thereafter, T. coccinea expanded its facilitate their establishment in new environments geographical distribution worldwide, especially in and may cause a range of negative effects on the tropical zones (Fenner 2001; Fenner and Banks 2004), health of native ecosystems (Gallardo et al. 2015), but also to higher latitudes (Cairns and Zibrowius such as alterations in species interactions and 1997; Paz-Garcia et al. 2007). T. coccinea was recorded 23 D. Batista et al. in Southwestern Atlantic on artificial substrates off southeastern Brazilian in the late 1990s (Castro and Pires 2001). Subsequently, T. coccinea was observed on natural substrates in two coastal areas located in Rio de Janeiro state (23ºS–43ºW) and about 300 kilometers apart: Ilha Grande Bay (de Paula and Creed 2004) and Arraial do Cabo Bay (Ferreira 2003). While Ilha Grande Bay is located in a typical tropical area, Arraial do Cabo is within the central zone of the Cabo Frio upwelling system (Coelho- Souza et al. 2012), and it is recognized as an unusual region where tropical and subtropical species co- occur (Guimaraens and Coutinho 1996; Ferreira 2003; Granthom-Costa et al. 2016). Both localities have port areas with vessel traffic related to commercial, recreational, offshore, and fisheries activities. After the initial records of T. coccinea, the situation in the two invaded areas is very distinct. At Ilha Grande Bay, T. coccinea and its congener Tubastraea tagusensis Wells, 1982 are nowadays considered pest corals and occur in high abundances (>700 colonies m-2) on several rocky shores at varying depths, spreading over a substantial distance (25 km) in less than five years (De Paula and Creed 2005; Mantellato et al. 2011; Silva et al. 2014). In contrast, the spread of T. coccinea has been slower at Arraial do Cabo than in Ilha Grande Bay. One year after the detection of six colonies 3 to 5cm in diameter, Ferreira (2003) observed that coral colonies had Figure 1. Map of the study area and the sites examined around tripled in number and size in Arraial do Cabo. After Arraial do Cabo Bay (AC Bay; sites 1, 2, 3, 4, 5, 6, 7, 8, 9, 13, 14, ten years, Mizrahi (2008) reported the presence of 15, 16, 17, 18 and 19) and outside of Cabo Frio Island (sites 10, small colonies on seven rocky shores, only on the 11 and 12). The site 6 corresponds to breakwater. underside of boulders. In addition, T. tagusensis has recently colonized natural substrates in Arraial do Cabo but, until now, its abundance was not Material and methods comparable to that of T. coccinea. It is also important to note that secondary dispersals of both species has Study area recently occurred to four localities along the Brazilian Arraial do Cabo is located 160 km east of Rio de coast, northward (12ºS; 20ºS) and southward Janeiro City, southeastern Brazil (42º00′W–22º44′S) (23.5ºS; 26ºS) in Rio de Janeiro State (Mantellato et (Figure 1). This region experiences the strong al. 2011; Sampaio et al. 2012; Miranda et al. 2012; influence of coastal upwelling of the South Atlantic Capel 2012; Costa et al. 2014; Miranda et al. 2016). Central Water (SACW) due to the local wind Here we tested the hypothesis that the distribution regimes and coastal geomorphology (Valentin 1994; of T. coccinea in Arraial do Cabo region (22º57′ to Cirano et al. 2006). 23º00′S, 41º59′ to 42º01′W) is controlled by low Two general weather conditions dominate the area. seawater upwelling temperatures. We described the Under good weather conditions, the atmospheric distribution and abundance of T. coccinea at Arraial circulation is driven by South Atlantic anticyclone do Cabo Bay fifteen years after its first record, and with northeastern winds. In opposition, poor weather these data were related to local currents, to a situations are related to the passage of cyclonic low dispersion model of particles, and to sea surface pressure systems and winds from southwest/south temperatures (SST). In addition, laboratory experiments direction. Generally, NE wind events are longer in were performed to confirm the effects of low duration than SW/S wind events (Coelho-Souza et al. temperature on the survival of this species and 2012). The coastal water mass typically has a tempe- compared to the field observations. rature range from 20 to 23 °C. In contrast, SACW 24 Orange cup coral Tubastraea coccinea in an upwelling area temperature varies from 6 to 18 °C (Candella 1999). of three years at a depth of 4 meters; totaling 25,920 Based on temperatures recorded from Arraial do Cabo temperature records per site. In addition, the fre- Bay, the coldest daily temperature was 9.8 °C (8 August quency of occurrence of low temperatures (<12.5 °C) 1998) and the warmest was 28.7 °C (28 March 1975) persisting for 48 hours was calculated. (Calil 2009). Northeastern winds are prevalent in the region and are essential to upwelling occurrence, Local circulation and dispersion although they are not the only condition. In general, upwelling season starts in September and extends to The local circulation patterns were estimated with March, but with great interannual variability (Calil the Princeton Ocean Model—POM (Blumberg and 2009). Mellor 1983). We used its 2-d configuration forced Arraial do Cabo has two distinct features concerning by external currents at each open border, local winds, morphological and bathymetric characteristics (Figure and tides. Conditions were maintained constant until 1). The outside southern portion of Cabo Frio Island the kinetic energy of the domain reached stability. A is deep (> 20 m) with rocky shores exposed periodi- simple Lagrangian model was used to evaluate cally to cold water (< 18 °C), especially during the particle dispersion, whose position in space and time upwelling season, and exhibit subtropical fauna and is given by: flora (Ferreira 2003). The inner portion, Arraial do 22 dPn t Pd n Cabo Bay, consists in a sheltered, shallow (15 m n1n tPP 2 maximum depth), bottle-shaped bay that is bounded dt !2 dt by the mainland, Cabo Frio Island and Porcos Island where Pn is the position at time n. The model can (Candella 2009). Coastal water is predominant inside account for advective and diffusive transport. The Arraial do Cabo Bay with water temperatures predo- initial point of particle dispersion was between minantly > 20 °C (Guimaraens and Coutinho 1996) Porcos and Cabo Frio Island (the NE area of the and rocky shores are characterized by tropical reef bay); this position corresponded to the anchoring area.
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