Allelopathic Effects on the Sun-Coral Invasion: Facilitation, Inhibition And
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Mar Biol (2017) 164:139 DOI 10.1007/s00227-017-3164-3 ORIGINAL PAPER Allelopathic effects on the sun‑coral invasion: facilitation, inhibition and patterns of local biodiversity Damián Mizrahi1 · Suelen F. Pereira2 · Sergio A. Navarrete3,4 · Augusto A. V. Flores1 Received: 22 September 2016 / Accepted: 14 May 2017 © Springer-Verlag Berlin Heidelberg 2017 Abstract In spite of growing concerns about the invasion higher number of native species than anticipated and sug- of the sun-coral Tubastraea coccinea along the tropical gesting that local richness offers little resistance to inva- Southwestern Atlantic, the biological interactions mediating sion. Highest density of T. coccinea recruits observed on the this species’ establishment and spread are largely unknown. least bioactive encrusting corallines suggests this taxonomic Here, we identifed species associations with T. coccinea by group may constitute doorways to the establishment of this comparing community structure between invaded and non- coral. In contrast, feld patterns of sun-coral colonies and invaded areas at Búzios Island, SP, Brazil. We also investi- recruits, as well as laboratory trials, suggest that cnidarian- gated effects of chemical cues from representative benthic dominated habitats represent obstacles to the sun-coral inva- species on sun-coral larval performance in the laboratory sion. Thus, while areas dominated by the snowfake coral and quantifed the density of sun-coral recruits across dif- Carijoa riisei—which showed the greatest negative allelo- ferent microhabitats in the feld. Field surveys showed that pathic effect on T. coccinea—likely provide resistance to the invasion of the sun-coral is more intense at reef areas the invader spreading, areas covered by encrusting coralline of higher species richness and diversity, putting at risk a algae and ‘barren substrates’ probably facilitate its estab- lishment. Because these latter, less-structured microhabitats Responsible Editor: E. Briski. often prevail after disturbance, damage assessment follow- ing human-mediated impacts should include detection and Reviewed by A. B. Bugnot and an undisclosed expert. control of sun-coral populations. Electronic supplementary material The online version of this article (doi:10.1007/s00227-017-3164-3) contains supplementary material, which is available to authorized users. Introduction * Damián Mizrahi Reef habitats are generally inhabited by diverse communi- [email protected] ties of sessile invertebrates and macroalgae, usually cover- 1 Universidade de São Paulo, Centro de Biologia Marinha ing most of the available space (Witman et al. 2004; Linares (CEBIMar/USP), Rod. Manoel Hipólito do Rego, km 131.5, et al. 2012). In these environments, interspecifc interactions São Sebastião, SP 11600‑000, Brazil are expected to be strong and play a signifcant role on the 2 Universidade de São Paulo, Instituto de Biociências structure of benthic assemblages (Cornell and Lawton 1992; (IB/USP), Rua do Matão, Travessa 14, n. 321, Cidade Witman et al. 2004). Under these circumstances, theory pre- Universitária, São Paulo, SP 05508‑090, Brazil dicts that the chances for the successful establishment of 3 Estación Costera de Investigaciones Marinas, Las Cruces, exotic species would be facilitated by positive interactions Center for Marine Conservation, LincGlobal, Pontifcia (e.g. species that facilitate larval settlement) and curtailed by Universidad Católica de Chile, Casilla 114‑D, Santiago, Chile intense local negative interactions, especially when species diversity is high (Elton 1958; Stachowicz et al. 1999; Frid- 4 Departamento de Ecología, Center for Applied Ecology and Sustainability (CAPES), Pontifcia Universidad Católica ley et al. 2007). Therefore, species successfully invading de Chile, Casilla 114‑D, Santiago, Chile diverse shallow reef habitats are expected to be either strong 1 3 139 Page 2 of 15 Mar Biol (2017) 164:139 competitors or good colonizers, making an effcient use of critical processes in the establishment of many coral spe- resources not fully exploited by native assemblages and to cies (Doropoulos et al. 2015). Successful settlement is be resistant (or resilient) to predation and other sources of expected to occur over benthic substrates of comparatively mortality. The sun-coral, Tubastraea coccinea, is likely one low structural complexity, where colonies can grow fast to a of such species, having remarkably colonized and expanded size at which they are less vulnerable to predators and over- over a variety of shallow hard-bottom habitats along most growing. Patches of bare rock, encrusting algae and dead of the tropical coasts (reviewed in De Paula 2007), although coral skeletons are usually important settlement substrates its original distribution range was restricted to the Pacifc (Heyward and Negri 1999; Edmunds 2000), probably and Indian Oceans (Cairns 2000). Along the Brazilian coast, because bioflm coating on these otherwise inert substrates this invasive species has been recorded on natural substrates provide strong settlement cues for planula larvae (Morse from Santa Catarina to Bahia (Castro and Pires 2001; Man- and Morse 1984; Hadfeld and Paul 2001). Bioflm settle- telatto et al. 2011; Sampaio et al. 2012). The possibility of ment-inducing substances are composed mostly of small occasional long-distance dispersal through polyp clustering peptides, soluble proteins and carbohydrates, which are (Mizrahi et al. 2014a) and the transportation by sea of sun- highly soluble in seawater and can be detected at distance coral fouled man-made structures (Creed et al. 2017) have by competent larvae of many invertebrate groups (Zimmer- probably enhanced connectivity among invaded areas, while Faust and Tamburri 1994). Substrate searching behaviors the apparent unpalatability to local predators (Moreira and are typically triggered upon detection of these substances Creed 2012) may have favored the persistence of sun-coral (Whittaker and Feeny 1971), ultimately facilitating settle- in colonized areas. Compared to processes that help spread ment and the establishment of developing coral colonies. the sun corals, the local mechanisms that may enhance suc- In contrast, other reef biogenic habitats are predictably cessful colonization or otherwise restrain the establishment unfavorable. For instance, turf or erect macroalgal patches and development of sun-coral colonies at recently invaded are generally inadequate for settlement because they may sites have received much less attention. Interspecifc compe- not provide stable substrates and often retain large quan- tition can be important, to some extent, since recent studies tities of sediments that might clog coral polyps (Hodgson have shown that sun-coral colonies may be overgrown by 1990; Babcock and Davies 1991). Similarly, small polyps sponges (Meurer et al. 2010; Lages et al. 2012) and possibly recruiting near rapidly growing algae, ascidians, bryozoans removed by nesting pomacentrid fsh (Mizrahi et al. 2016). and sponges face a high risk of dislodgment or overgrowth During early ontogenesis, from settling larvae to small (Bruno and Witman 1996; Lapointe et al. 2007). Coral few-polyp colonies, exposure to metabolites released by planulae may be able to detect chemical cues signaling a wide array of benthic organisms may play a particularly the presence of such adverse substrates and actively avoid important role, but the relevance of this sort of interactions them, therefore inhibiting settlement. Moreover, several remains largely unknown. sessile invertebrates and macroalgae can produce bioactive Mizrahi et al. (2014b) undertook laboratory experi- substances that might impair approaching larvae in many ments showing that positive buoyancy combined to active ways (Whittaker and Feeny 1971; Dworjanyn 2001). These habitat selection promotes higher sun-coral settlement rates are usually non-polar compounds of varying toxicity, such on undersurface habitat (i.e. negatively oriented). These as furanones and terpenoids, located over the surface of the laboratory results were consistent with sun-coral distribu- organisms producing them (De Nys et al. 1995; Dworjanyn tion patterns at shallow reefs in Búzios Island, SP, Brazil. 2001). These substances are candidate inhibitors of sun- Given this pattern, the impact of T. coccinea is expected to coral larval settlement. more directly affect assemblages of sessile invertebrates In this study we combined feld and laboratory obser- and macroalgae developing on reef walls and overhang sur- vations and experiments to improve our understanding of faces. Bare space in those substrate orientations is scant at interspecifc interactions mediating the sun-coral inva- Búzios Island and at most shallow rocky reefs in the region. sion at Búzios Island, SP, Brazil. In this island, Tubast- Thus, the establishment and expansion of sun-coral colo- raea coccinea was frst observed in 2008 (Mantelatto nies should largely depend on the occurrence of biogenic et al. 2011) and colonization is still an ongoing process, substrates that either inhibit or facilitate larval settlement with both the scale of invaded areas and overall density and subsequent growth of colonies. Identifying these ben- of coral colonies still much lower than what is presently thic organisms may allow more accurate risk assessments verifed at other places, such as Ilha Grande, RJ, where at areas still not invaded and assist conservation efforts to the frst records of this species date back to the late 80s protect