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ORIGINAL PAPER

Reef fish associations with sea urchins in an Atlanticoceanic island

Vinicius J. Giglio1,2 & Maria L. F. Ternes3 & Moyss C. Barbosa2 &Csar A. M. M. Cordeiro2 & Sergio R. Floeter4 & Carlos E. L. Ferreira2

Received: 19 November 2016 /Revised: 27 February 2017 /Accepted: 28 February 2017# Senckenberg Gesellschaft fr Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Abstract Many reef fish are known to be associated withparticular microhabitats that provide food and refuge, suchas branching corals, gorgonians, macroalgal beds and sea ur-chins. We investigate the association of reef fishes with thelong-spined sea urchin Diadema antillarum in shallow reefsof Trindade Island, southeastern Brazil. A total of 1283 fishindividuals from seven families and nine species were associ-ated with 495 sea urchins. Sea urchins provide important shel-ter especially for juveniles of the Noronha wrasse,Thalassoma noronhanum. Larger fishes were found at higherdensities associated to sea urchins with larger spines. At reefslacking structurally complex organisms, such as branchingcorals, sea urchins can be an important refuge for juvenilesor small-bodied reef fish species, influencing their distributionand acting as ecosystem engineers.

Keywords Trindade island .Microhabitat . Habitat use . Fishinteractions . Tropical reefs . Fish behavior . Reef complexity

Introduction

Habitat structure and complexity are known to influence reeffish abundance and diversity at various spatial scales frommicro to mega habitats (Roberts and Ormond 1987; Ferreiraet al. 2001; Rogers et al. 2014). In reef environments, manyfish species are known to be associated with particular habi-tats, mostly due to optimal refuge against predators and avail-ability of food (Dahlgren and Eggleston 2000). Many organ-isms are known to modify the environment or create micro-habitats, being described as ecosystem engineers (Jones et al.1994). Several species of small sized or juvenile reef fish canbe associated with microhabitats provided by complex bio-genic sessile structures such as branching corals (Pereira andMunday 2016), macroalgae (Chaves et al. 2013), gorgonians(Goh et al. 1999) and mobile organisms such as sea urchins,cucumbers and crinoids (Karplus 2014).

The fish-sea urchin association has long been reported, es-pecially for the cardinalfishes (Apogonidae) and clingfishes(Gobiesocidae) families with sea urchins from the familyDiadematidae (Randall et al. 1964; Karplus 2014). The struc-tural complexity generated by sea urchin spines harbors a di-versity of small fish that can be closely associated, favoring thedevelopment of juvenile stages or even a whole life stage as anobligatory association (Randall et al. 1964; Sakashita 1992).For some fish species, sea urchins may influence the densityof their commensals in the reef by providing refuges againstpredators. For instance, Hartney and Grorud (2002) found aclose association among the crowned sea urchin,Centrostephanus coronatus, and the blue-banded gobyLythrypnus dalli. Results showed that the crowned sea urchinhas an influence on the abundance, recruitment, migration ratesand survival of this small fish. However, only a small fractionof associated fish is permanent and obligatory (Karplus 2014).Most of the fish and sea urchin associations are facultative and

Communicated by O. Aksel Bergstad

* Vinicius J. Gigliovj.giglio@gmail.com

1 Programa de Ps-Graduao em Ecologia, Universidade Federal doRio de Janeiro, Rio de Janeiro, Brazil

2 Reef Systems Ecology and Conservation Lab, Departamento deBiologia Marinha, Universidade Federal Fluminense, Rio deJaneiro, Brazil

3 Programa de Ps-Graduao em Zoologia, Universidade Estadual deSanta Cruz, Bahia, Brazil

4 Departamento de Ecologia e Zoologia, Universidade Federal deSanta Catarina, Santa Catarina, Brazil

Mar BiodivDOI 10.1007/s12526-017-0677-4

http://crossmark.crossref.org/dialog/?doi=10.1007/s12526-017-0677-4&domain=pdf

commensal (Moore and Auster 2009). Fish from theGobioesocidae and Gobbidae families are also described asectoparasitic, in which the associated fish feed on the tube feetor pedicelaria of their hosts (Dix 1969; Karplus 2014).

In some reefs, sea urchins occur at higher abundances,providing an increase in the reef complexity and, consequently,microhabitats for themarine biota. Thismay have positive effectsfor reef fish by providing them habitat structure, otherwise atsome tropical reefs, sea urchins can largely increase bioerosion(McClanahan and Kurtis 1991) and erode reef structural com-plexity (Graham and Nash 2012). However, in the southwesternAtlantic reefs, such associations between reef fish and sea urchinsremain poorly described (Dalbern and Floeter 2012).

The sea urchin Diadema antillarum was once abundant inAtlantic tropical reefs and referred to as a keystone species upuntil the 1980s, when an event of mass mortality led to sig-nificant depletion (Lessios et al. 2001). Here, we describe theassociation among the long-spined sea urchin Diademaantillarum and reef fishes at Trindade Island, an oceanic islandlocated in the southwestern Atlantic. At Trindade Island, in theshallow reefs, this is the most abundant sea urchin, and is usu-ally found forming densely packed groups of dozens of indi-viduals (Cordeiro et al. unpubl.). Individuals of D. antillarumare commonly found in caves, overhangs, and crevices thatprovide protection against predators and are more abundant inzones protected from strong waves (Alvarado 2008). The aimof this study was to describe which fish species are associatedwithD. antillarum and verify whether density and body size ofassociated fish vary according to the size of sea urchin spines.In addition, we determined if density of fishes associated withsea urchins was correlated to those not associated with urchins,for instance, fish moving across the reef or fish associated withother structures.

Methods

Study area

Trindade Island, along with the Martin Vaz Archipelago, com-prises the most isolated island complex of the Brazilian coast,and is located 1160 km off the coast with a terrestrial area of 9.2km2 (Gasparini and Floeter 2001). Compared to the Braziliancoast, the remote location makes Trindade Island home toimpoverished fish (Floeter et al. 2008; Pinheiro et al. 2011)and benthos assemblages (Pereira-Filho et al. 2011).

Along the Brazilian coast, D. antillarum is more abundantin the tropical northeastern region (Attrill and Kelmo 2007),and rare in the subtropical reefs along the south and southeast-ern coastline (Cordeiro et al. 2014). In the shallow reefs (5-12m depth) of Trindade Island, D. antillarum is the dominantspecies among the five sea urchin species found locally [38%of total abundance of sea urchins and 0.011.5. ind.m2 at five

sites around the island (Cordeiro et al. unpubl.)], and is theonly species with long spines that hosts different fish species.

Data collection

Data were collected from August to September 2014 at threeshallow sites (310 m depth) in the north of Trindade Island:Cabritas, Calheta and Ponta Norte. Observations were con-ducted in rocky reefs through 26 roving scuba diving counts,in which two observers searched for the specimens.To avoid sampling the same sea urchin twice, observers rovedparallel to the reef in the same direction. When a sea urchinwas found, the observer slowly approached to verify the pres-ence of any associated fish, and when found, the abundanceand body size of the fish species was described (total length TL). Fish were identified using checklists from TrindadeIsland (Gasparini and Floeter 2001; Pinheiro et al. 2015).The size of the sea urchin spines was visually estimated basedon the length of the largest primary spines and grouped intothree categories: short (5 cm), medium (615 cm) and long(>15 cm). Additionally, observers described the behavior ofthe fish associated with sea urchins and recorded their spatialdistribution among the urchins spines.

In order to assess reef fish abundance, an underwater visualcensus were performed using belt transects (20x2m) at all thesampled sites (Cabritas, n= 11, Orelhas, n = 10, and Ponta Norte,n = 15). Sampling units were distributed randomly along rockyreef areas, and all fish observed within transects were countedand measured.

Data analysis

Differences between body size and density of the most abun-dant fish species (species of which >15 individuals were re-corded) associated with sea urchins were compared using anon-parametric ANOVA (Kruskal-Wallis test), since the re-sponse distribution was non-normal and data was nonpara-metric. A post-hoc analysis using the Dunns test was per-formed to verify differences among categories of sea urchinspine size. Composition of fish assemblages and mean fishdensity amongst sites were tested using a PERMANOVA(9999 permutations, package vegan, function adonis) andANOVA, respectively. A Pearson correlation was used to ver-ify whether overall abundance of the non-associated fish withsea urchins was correlated with abundance of fish associatedwith the urchinD. antillarum. Analyses were conducted usingthe R software (R Core Team 2016).

Results

A total of 1283 fish from seven families and nine species wererecorded in association with 495 individuals of D. antillarum

Mar Biodiv

with short (n = 98), medium (n = 196) and long (n = 201)spine sizes. Individuals of D. antillarum with long and medi-um spines have higher densities of commensal fishes thanshort-spined sea urchins (Kruskal-Wallis test, H = 117.1,p < 0.001; Dunns test: long = medium > short). Seventy-three percent of sea urchins with short spines hosted no com-mensal fishes, while 83% of sea urchins with medium spinesand 89% with lon