Comparative Diversity of Anemone-Associated Fishes and Decapod Crustaceans in a Belizean Coral Reef and Seagrass System
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Marine Biodiversity (2019) 49:2609–2620 https://doi.org/10.1007/s12526-019-00993-5 ORIGINAL PAPER Comparative diversity of anemone-associated fishes and decapod crustaceans in a Belizean coral reef and seagrass system Rohan M. Brooker1,2 & William E. Feeney3,4 & Tiffany L. Sih5,6 & Maud. C. O. Ferrari7 & Douglas P. Chivers2 Received: 16 April 2019 /Revised: 5 July 2019 /Accepted: 12 July 2019/Published online: 19 August 2019 # Senckenberg Gesellschaft für Naturforschung 2019 Abstract Within tropical coastal habitats such as coral reefs and seagrass meadows, sea anemones (Actiniaria) provide microhabitats for a diverse range of fauna. However, the mechanisms that enable these interactions, and how actiniarian diversity and abundance mediates associate assemblages, remains poorly understood. Here, we compared sea anemone species richness and abundance with that of their associated decapod crustaceans and teleost fishes across adjacent coral reef and seagrass habitats at Carrie Bow Cay, Belize. At least 16 decapod and seven fish species were associated with anemones across both habitats, including several previously undocumented associations. While overall anemone-associate richness did not differ between habitats, seagrass anemones had the greatest mean abundance and diversity of both decapod and fish associates. This suggests that the importance of anemones as microhabitat reflected broader benthic complexity and shelter availability, with species aggregating on sea anemones when access to alternative shelter, such as corals, was limited. Patterns of associate distributions on anemones were also highly structured, in terms of both associate and anemone species, with these patterns likely reflecting a combination of associate specialization, intraspecific competition, and anemone morphology and toxicity. The diverse multi-species associate complexes observed suggest that sea anemones provide an important refuge for both specialized and generalist species and so have the potential to increase faunal diversity and abundance within tropical coastal habitats. Keywords Actiniaria . Sea anemone . Caribbean . Habitat complexity . Predation risk Introduction Marine sessile invertebrates are common ecosystem engi- Communicated by B. W. Hoeksema neers, providing microhabitat for complex assemblages of as- sociated species (Jones et al. 1994; Gutiérrez et al. 2003; Bell * Rohan M. Brooker 2008; Bos and Hoeksema 2015). With most marine ecosys- [email protected] tems now threatened by climate change and overexploitation, the global contribution of sessile invertebrates to broader hab- 1 Centre for Integrative Ecology, School of Life and Environmental itat quality has received increasing recognition, with substan- Sciences, Deakin University, Geelong, Victoria, Australia tial effort devoted to determining their ecosystem role, 2 Department of Biology, University of Saskatchewan, preventing their decline, and facilitating regeneration and re- Saskatoon, Saskatchewan, Canada silience (Beck et al. 2011; Gillies et al. 2018). Sessile inverte- 3 Environmental Futures Research Institute, Griffith University, brates can create habitat heterogeneity and structural complex- Brisbane, Australia ity that may otherwise be limited (Tews et al. 2004); for ex- 4 School of Biological Sciences, University of Queensland, ample, the occurrence of bivalves on soft sediment can affect Brisbane, Queensland, Australia surrounding biodiversity (McLeod et al. 2014). Therefore, the 5 College of Science and Engineering, James Cook University, relative availability of microhabitat-forming invertebrates can Townsville, Queensland, Australia facilitate overall community composition and biodiversity, as 6 ARC Centre of Excellence for Coral Reef Studies, James Cook well as the distribution, abundance, and population structure University, Townsville, Queensland, Australia of associated fauna (Jones et al. 1994). For associated and 7 Department of Biomedical Sciences, WCVM, University of symbiotic species, sessile invertebrates can influence key Saskatchewan, Saskatoon, Saskatchewan, Canada 2610 Mar Biodiv (2019) 49:2609–2620 factors such as trophic dynamics, mediating predator-prey in- 2018). However, individuals or colonies are generally stable teractions by providing shelter, limiting sensory acuity or enough to support the reproductive cycle of associates, which movement, or reducing the likelihood of attack (Lima and are usually also short-lived (O’Reilly et al. 2018). Associative Dill 1990). Invertebrate hosts can also increase associate fit- relationships range from facultative to obligate, often varying ness, providing food resources and protection from abiotic with ontogeny (Baeza and Stotz 2001;Feeneyetal.2019)and extremes and mediating exploitative or interference competi- reflecting the degree of reliance on anemones for food or shelter. tion (Almany 2004; McKeon and O’Donnell 2015). However, The most specialized symbionts, such as the Amphiprion and while they can play a critical role, these invertebrates are usu- Premnas anemonefishes, normally associate with specific anem- ally themselves specialized to specific habitats or abiotic pa- one species and have evolved a suite of innate and acclimation rameters. As such, many are at risk from environmental mechanisms that make them impervious to their host’s feeding change, habitat loss, and exploitation, compromising their and defensive responses (Fautin 1991;Crawford1992;Mebs ecological function and ability to support associated species 2009; Feeney and Brooker 2016). While facultative species usu- (Duke et al. 2007; Hughes et al. 2017). It is therefore essential ally lack these specializations, they could theoretically remain that we quantify the relationship between microhabitat- capable of associating with anemones by avoiding the stinging forming invertebrates and their associated fauna, to identify tentacles or associating with less aggressive or toxic hosts. their ecosystem role, how these interactions are mediated, and Patterns of microhabitat use, host specificity, and distribution the potential impacts of their decline on future biodiversity. on the anemone may be indicative of niche partitioning by as- On tropical reefs, the most ubiquitous ecosystem engineers sociates, reducing competition and increasing diversity are scleractinian corals, with colonial and solitary species (Robertson and Polunin 1981;ElliotandMariscal2001;Khan supporting complex micro- and macrofaunal assemblages et al. 2003;Campetal.2016). Irrespective of the degree of (Stella et al. 2011;Hoeksemaetal.2012; Coker et al. 2014) reliance, relationships between anemones and associates appear and declines associated with decreased biodiversity, habitat to primarily evolve in response to predation risk, with anemones complexity, and resilience (Hughes et al. 2018). However, a providing a protective refuge to small-bodied species or individ- range of other invertebrates, such as sponges, bivalves, and uals within species (Huebner et al. 2012; Feeney et al. 2019). soft corals, also produce microhabitat that can support distinc- However, these interactions are mostly mutualistic, with various tive species assemblages, both on reefs and in adjacent sys- fish and invertebrate associates known to defend their host from tems such as seagrass meadows (Goh et al. 1999;Wulff2006; potential predators or increase aeration and nutrient availability, Neo et al. 2015). While the ecological role of non- leading to greater anemone growth, survival, and reproductive scleractinian invertebrates is often overlooked, their role as rates (Spotte 1996; Holbrook and Schmitt 2005; Porat and microhabitat may become increasingly important if global Chadwick-Furman 2004; Roopen and Chadwick 2009; coral cover continues to decline (Bell et al. 2013). Szczebak et al. 2013; McCammon and Brooks 2014). While In shallow tropical seas worldwide, sea anemones the underlying ecology of most actiniarian-associate relation- (Actiniaria) (herein, anemones) are common, often conspicuous ships is poorly understood, especially with regard to facultative components of benthic communities (Fautin et al. 2013). interactions, it is clear that anemones provide an important mi- Generally consisting of a solitary polyp, the individuals of most crohabitat, and so variations in anemone abundance or diversity species of anemone are highly site attached, affixing themselves could have strong effects on community structure. to the substrate via their pedal disc and extending into the water While tropical anemones can support complex faunal as- column. From this position, the anemone uses its tentacles to semblages, increasing biodiversity and facilitating ecosystem feed, either autotrophically via Symbiodiniaceae and/or hetero- processes such as cleaning interactions (Huebner and trophically using specialized nematocyst cells to capture passing Chadwick 2012; Titus et al. 2015; Colombara et al. 2017), organic material. Anemones range from under 1 mm to over 1 m few studies have examined how broader habitat characteristics in diameter, with some species forming dense aggregations and and anemone morphology affect associate richness and abun- patterns of high local abundance (Colombara et al. 2017;Dixon dance, particularly with regard to facultative associates et al. 2017; Titus et al. 2017a). As such, they can represent an (Huebner et al. 2012). With this in mind, we quantified the important driver of habitat complexity. diversity and abundance of two major groups of anemone- Despite