Effect of Phase Shift from Corals to Zoantharia on Reef Fish Assemblages

Abstract

Consequences of reef phase shifts on fish communities remain poorly understood. Studies on the causes, effects and consequences of phase shifts on reef fish communities have only been considered for coral-to-macroalgae shifts. Therefore, there is a large information gap regarding the consequences of novel phase shifts and how these kinds of phase shifts impact on fish assemblages. This study aimed to compare the fish assemblages on reefs under normal conditions (relatively high cover of corals) to those which have shifted to a dominance of the zoantharian Palythoa cf. variabilis on coral reefs in Todos os Santos Bay (TSB), Brazilian eastern coast. We examined eight reefs, where we estimated cover of corals and P. cf. variabilis and coral reef fish richness, abundance and body size. Fish richness differed significantly between normal reefs (48 species) and phase-shift reefs (38 species), a 20% reduction in species. However there was no difference in fish abundance between normal and phase shift reefs. One fish species, Chaetodon striatus, was significantly less abundant on normal reefs. The differences in fish assemblages between different reef phases was due to differences in trophic groups of fish; on normal reefs carnivorous fishes were more abundant, while on phase shift reefs mobile invertivores dominated.

About the Authors:

Igor C. S. Cruz

* E-mail: [email protected]

Affiliations Programa de Pós Graduação em Ecologia, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil, Laboratório Recifes de Corais e Mudanças Globais, Instituto de Geociências, Universidade Federal da Bahia, Salvador, BA, Brazil, Laboratório de Ecologia Marinha Bêntica, Departamento de Ecologia, Instituto de Biologia Roberto Alcântara Gomes, Universidade do Estado do Rio de Janeiro—UERJ, PHLC Sala 220, Rio de Janeiro, RJ, Brazil

Miguel Loiola

Affiliations Laboratório Recifes de Corais e Mudanças Globais, Instituto de Geociências, Universidade Federal da Bahia, Salvador, BA, Brazil, Programa de Pós Graduação em Ecologia e Biomonitoramento, Universidade Federal da Bahia, Salvador, BA, Brazil

Tiago Albuquerque

Affiliation: Laboratório Recifes de Corais e Mudanças Globais, Instituto de Geociências, Universidade Federal da Bahia, Salvador, BA, Brazil

Rodrigo Reis

Affiliations Laboratório Recifes de Corais e Mudanças Globais, Instituto de Geociências, Universidade Federal da Bahia, Salvador, BA, Brazil, Programa de Pós Graduação em Ecologia e Biomonitoramento, Universidade Federal da Bahia, Salvador, BA, Brazil

José de Anchieta C. C. Nunes

Affiliations Programa de Pós Graduação em Ecologia e Biomonitoramento, Universidade Federal da Bahia, Salvador, BA, Brazil, Laboratório de Ecologia Bentônica, Instituto de Biologia, Universidade Federal da Bahia, Salvador, Bahia, Brazil

James D. Reimer

Affiliation: Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, Nishihara, Okinawa, Japan

Masaru Mizuyama

Affiliation: Molecular Invertebrate Systematics and Ecology Laboratory, Graduate School of Engineering and Science, University of the Ryukyus, Nishihara, Okinawa, Japan

Ruy K. P. Kikuchi

Affiliation: Laboratório Recifes de Corais e Mudanças Globais, Instituto de Geociências, Universidade Federal da Bahia, Salvador, BA, Brazil

Joel C. Creed

Affiliation: Laboratório de Ecologia Marinha Bêntica, Departamento de Ecologia, Instituto de Biologia Roberto Alcântara Gomes, Universidade do Estado do Rio de Janeiro—UERJ, PHLC Sala 220, Rio de Janeiro, RJ, Brazil

Introduction

Phase shifts are one of the most drastic consequences of coral reef degradation [1–4]. This phenomenon is characterized by an abrupt decrease in coral abundance or cover and concurrent increase to dominance of non-reef-building organisms, such as algae and soft corals [5]. The consequence of this phenomenon is the loss of some ecosystem services, such as fishing and tourism [3], and changes in local biodiversity [1]. It has been estimated that 19% of coral reefs worldwide have been lost and another 35% are threatened [6], which makes this scenario alarming; it has been termed the "Coral Reefs Crisis" [3,4].

Despite the severity of this problem, to date the only mechanism extensively studied is the shift to dominance of macroalgae, leaving a large gap in our knowledge about the processes of phase shifts involving dominance to other types of organisms [7]. The relationship between change in fish assemblages and macroalgal dominance is well known [3,8–10], and although there is no consensus [11–13] the loss of herbivorous fish through overfishing is considered one of the causes of dominance by macroalgae [14–16]. There is also a large information gap regarding the consequences or relationships between these other kinds of benthic phase shifts and fish assemblages.

The effects of composition and structure of benthic assemblages and associated benthic composition, and environmental structural complexity on reef fish assemblages, have been well documented since the beginning of the 1970s [17–24]. A shift in benthic structure can drive a change in abundance and composition of fish species that are directly linked to specific benthic trophic groups. This change can affect those species which were previously abundant and/or those that had key ecological roles in the community, such as herbivores, which control the algae that compete with framework building organisms [3,8,9,16]. The loss of key species implies alterations in the community structure as well as in ecosystem stability [10,15,25]. However, the feedback by which fishes and benthic assemblages influence each other in coral reef ecosystems remains poorly understood. Understanding these ecological interactions is essential in order to prevent and/or manage phase shift situations [26,27].

The present study therefore aims to compare fish assemblages on normal condition reefs, with relatively high coverage of corals, to those shifted to a dominance of the zoantharian Palythoa cf. variabilis (initially identified as Epizoanthus gabrieli [28]) in Todos os Santos Bay (TSB), Brazilian eastern coast. To investigate the differences between these two reef conditions we tested if fish assemblages on phase shift reefs had: (i) less species; (ii) lower abundance; (iii) different trophic structures; and (iv) reduced fitness [29], by perturbing the cleaning service supplied by the Barber (Neon) Goby Elacatinus figaro. We also investigated whether a reduced abundance of a zoantharian predator, the butterfly fish Chaetodon striatus, might be responsible for the zoantharian outbreak (parallel to the loss of herbivores in coral-to-algae reef shifts).

Materials and Methods

Study area

This study was carried out in Todos os Santos Bay (TSB) (12°50'S and 38°38'W). It is the second largest embayment in Brazil (about 1235 km2), located on the Brazilian eastern coast, and surrounded by Salvador City, the third largest urban area in the country [30] (Fig. 1). The Brazilian eastern coast has the highest coral diversity in the South Atlantic Ocean [31,32]. The TSB is an environmentally protected area (EPA), equivalent to the landscape/seascape IUCN category [33]. Nevertheless, this bay receives numerous environmental stressors such as sewage, industrial runoff, overfishing, dynamite fishing, disorderly occupation of the coastline and has suffered environmental disasters such as contamination by lead, mercury, and oils spills [34]. Faced with these stressors, identifying the probable cause of this Palythoa phase shift is not easy, although Yang et al. [35], performing a study in Okinawa, Japan, pointed out that the dominance of P. tuberculosa in some reef areas may be related to nutrient input from terrestrially derived river run-off. Costa et al. [36], in their review article of the role of nutrient overloading on Brazilian coral reefs, also mention how Palythoa benefits from nitrification enrichment in coastal reefs. Despite heavy impacts some reefs in TSB still have a coral cover considered high for the region (between 8% and 27% c.f. Cruz et al. [36]) relative to other Brazilian inshore reefs (3.6% c.f. Leão et al. and Costa et al. [37,38]). On the other hand some reefs (total area of approximately 10.5 km2) are dominated by the zoantharian Palythoa cf. variabilis and have a coral cover lower than 3.6% [28].

[Figure omitted. See PDF.]

Fig 1. Sampling stations in Todos os Santos Bay.

Reefs under normal conditions are represented by white circles while reefs under phase shift (high zoantharian cover) are signed by black circles.

https://doi.org/10.1371/journal.pone.0116944.g001

Ethics statement

We used a non-destructive methodology to assess fish assemblages. These data were collected using visual census and recorded images. This bay is an Environmentally Protected Area, and according to Brazilian law SNUC (National System of Conservation Areas) [39] this kind of conservation unit does not require a license for studies that use non-destructive methods. Only Palythoa specimens as detailed below were collected under license N° 24958–1 issued by the Brazilian Environment Ministry and sent to Japan for genetic analysis under transport and genetic heritage license N° 14BR013578/DF, also issued by the Brazilian Environment Ministry.

Analyses of Palythoa specimens

In situ images were collected of each Palythoa (Anthozoa: Hexacorallia: Zoantharia: Sphenopidae) specimen before collection. Four Palythoa specimens were collected from the study site on a phase shift reef by hand and preserved in 95% ethanol. Only small fragments consisting of 3 polyps were collected from each sampled Palythoa colony. The specimens were collected from Poste 1 (12°49'20.1"S 38°33'35.4"W) within the study site. From in situ observations and digital images, the Palythoa specimens were believed to belong to a single species, and all specimens were zooxanthellate, with heavily encrusted body walls, and polyps were separated from each other and only joined by a thin coenenchyme.

Molecular analyses were performed on four Palythoa specimens (specimen numbers 418–421). DNA extraction with a DNeasy Blood and Tissue Kit (Qiagen, Tokyo, Japan) followed the manufacturer’s instructions. Sequences of mitochondrial 16S ribosomal DNA (mt 16S rDNA) and the internal transcribed spacer region of ribosomal DNA (ITS-rDNA) were amplified using previously reported methods and primers [40,41]. Amplified PCR products were visualized on 1.0% agarose gel and cleaned up following a shrimp-alkaline phosphatase treatment. Subsequently, mt 16S rDNA and ITS-rDNA products were sequenced at Fasmac Co., Ltd (Kanagawa, Japan).

Newly acquired mt 16S rDNA and ITS-rDNA sequences were deposited in GenBank (GenBank Accession Numbers KP174720-KP174725). Following the methodology of Bo et al. [42], we compared our newly acquired sequences for similarity with previously reported Zoantharia sequences by: 1) National Center for Biotechnology Information’s Basic Local Alignment Search Tool (NCBI BLAST) [43], and 2) by manual visual comparison using alignment software Se-Al v2.0a11 (University of Edinburgh). As in Bo et al. [42], our newly acquired sequences were compared by similarity only with no additional phylogenetic analyses, as previous research has shown that mt 16S rDNA and ITS-rDNA sequences combined are generally accurate in identifying zoantharian specimens to the species level [44,45].

Data collection

In 2011 we sampled eight reefs where we collected data on reef fish assemblages and benthic cover of the corals and P. cf. variabilis. We used a video transect method to assess benthic assemblages [46,47]. We performed six parallel band transects at each sampled station, registered on digital video. We used the video-transect method with a 40 cm long aluminum rod coupled to the filming system to standardized the image area [48]. At this distance the transect width sampled by the camera was 0.2 m. The length of the belt-transects was 20 m, which gave a sampled area of 24 m2 per station. The relative coverage of corals and P. cf. variabilis on each sampled reef was estimated using the software CPCe 3.6 [49]. We divided the belt transects into successive frames, on which 20 randomized points were placed to estimate cover of the benthic organisms. The stations were divided in phase-shift reefs and normal reefs: reefs presenting a zoantharian coverage greater than 30% and coral cover lower of 3.6% were considered to have shifted phase (12°49'45"S 38°32'52"W; 12°49'31"S 38°32'08"W; 12°49'20"S 38°33'36"W; 12°50'00"S 38°31'31"W) while those on which zoantharian coverage did not exceed 10% were considered ‘normal’ (12°48'33"S 38°37'35"W; 12°50'43"S 38°30'47"W; 12°50'13"S 38°32'57"W; 12°47'54"S 38°35'02"W).

We sampled fish assemblages with visual censuses. In each station, we used an adaptation of Atlantic and Gulf Rapid Reef Assessment (AGRRA) Fish Protocol [50] with 10 band transects of 30 meters long by 2 meters wide, covering a total sampled area of 600 m2. In each transect we estimated the abundance of all observed species during 15 minutes. The fish species found were classified into the following trophic groups: carnivores, mobile invertivores, sessile invertivores, piscivorous, planktivores, omnivores, territorial herbivores, roving herbivores and cleaners as according to Ferreira et al. and Medeiros et al. [51–53].

Data analysis

The species richness was estimated and compared by a rarefaction analysis using an accumulated species curve Mao tau (Sobs) and their respective confidence interval at 95% [54,55]. Each transect was used as samples totalled 40 samples on normal reefs and another 40 in phase shift reefs. Each set of 40 samples was distributed 999 times in random order to calculate average species accumulation (Sobs) and its confidence interval [56]. The confidence interval was calculated using Student’s t distribution: if the limits did not overlap the data sets were judged as different [57,58]. In addition, qualitative ACE, Chao 1, Jack 1 and quantitative ICE, Chao 2 and Jack 2 indices of species number were used to estimate the richness of fishes in phase shift reefs compared with species accumulation on normal reefs. We performed these analyses using EstimateS 8.2.0 software [59]. We tested the difference in the abundance of fishes, density of Chaetodon striatus and Elacatinus figaro between normal and phase shift reefs with Student’s t-test [57] using StatSoft STATISTICA, version 8.0 software.

Standard multivariate analyses were performed to explore differences in trophic guilds between normal and phase shift reefs (α = 0.05), a multivariate nonparametric test based on the Bray-Curtis similarity index [60,61]. The similarity percentage (SIMPER) routine was used to identify which trophic guilds were important in the groupings identified by ANOSIM [60–62]. Finally, multi-dimensional scaling (MDS) was applied and the Bray-Curtis similarity index was used to illustrate patterns of similarities and differences [60,61]. Theses multivariate analyses were undertaken using PRIMER 6 (Primer-E) software.

Results

Palythoa specimen identification

Newly acquired sequences of mt 16S rDNA and ITS-rDNA from specimens matched closely with previously reported Palythoa species’ sequences.

For mt 16S rDNA, sequences were obtained from all four examined specimens, and were identical over their entire length (480 base pairs). By BLAST comparison, these sequences were identical to previously reported sequences from Palythoa heliodiscus (GenBank Accession Number AB219224) and Palythoa cf. heliodiscus (HM754466), etc.) from the Indo-Pacific and the aquarium trade, respectively.

For ITS-rDNA, only short sequences were obtained from two examined specimens (418, 419), and these were identical to each over their entire length (178 base pairs). By BLAST comparison, these sequences were most similar (177/178 base pairs) to a previously reported sequence from Palythoa aff. variabilis (JX119123) from Florida.

Recent research has shown that there are closely related sibling species of Palythoa in the Atlantic and Indo-Pacific Oceans. Among these are the species P. heliodiscus (Indo-Pacific) and P. variabilis (Atlantic), which have identical mt 16S rDNA and similar ITS-rDNA sequences [63]. Therefore, for this study, based on mt 16S rDNA and ITS-rDNA sequence similarity, specimen sampling location, and general morphological characteristics, we identified the specimens from TSB as Palythoa cf. variabilis.

Community assessment

In normal reefs the coral coverages were 16.1% ±6.4 (SD), 34.2% ±3.82, 19.1% ±2.4 and 23.7% ±3.8 while in phase shifted reefs coverages were 2.4% ± 2.0, 2.0% ± 0.7, 0.5% ± 0.4 and 0.9% ± 0.6. Palythoa cf. variabilis coverages were 0.1% ± 0.1, 0.1% ± 0.1, 0% ± 0 and 8.4% ± 13.7 on normal reefs and 88.6% ± 6.2, 60.3 ± 10.7%, 33.8% ± 10.2 and 61.5% ± 4.4 on phase shift reefs.

We found a significant difference in the fish richness between phase-shift reefs with 38 species and normal reefs with 48 species (Fig. 2A). In addition, all richness estimators of phase-shift reefs showed a lower number of species than the number of species observed on normal reefs (Fig. 2B). Furthermore, the only richness estimator that still overlapping the confidence interval of normal reefs Sobs was Jack 1. Moreover, the normal reefs had higher diversity than phase shift reefs (H’ = 2.74 ± 0.01(SD), J’ = 8.61 ± 0.01 and H’ = 2.11 ± 0.01; J’ = 5.03 ±0.01, respectively).

[Figure omitted. See PDF.]

Fig 2. Probabilities of numbers of fishes species by number of samples with (a) number of species observed (Sobs) in normal (NR) and phase shift (PS) reefs with their respective confidence intervals (95%), and (b) estimators of species richness of reefs in phase shift (PS) in comparison with the number of species observed in normal reef (NR) and its confidence interval less than 95%.

https://doi.org/10.1371/journal.pone.0116944.g002

The analysis of similarity (ANOSIM) showed a difference in patterns of dominance in fish assemblages, for trophic groups, between reef types (Global R = 0.479; p = 0.029). The percentage of dissimilarity (SIMPER) between these two groups was 41.4%, explained mainly (50%) by a higher number of mobile invertivores in phase shift reefs (Table 1). Moreover the sessile invertivores and carnivores were more abundant on unaffected reefs and together with the mobile invertivores represented 88.2% of the difference between the reef types. The difference between phases shift of reefs in relation to trophic groups was clear on the MDS (Fig. 3), with the total separation of normal and phase shift reef groups along the first axis.

[Figure omitted. See PDF.]

Fig 3. Multidimensional scaling of trophic structure of reef fishes assemblage on normal reefs (represented by dark balls) and phase shift reefs (dominated by the zoantharian Palythoa cf. variabilis), which in figure are represented by asterisks.

https://doi.org/10.1371/journal.pone.0116944.g003

[Figure omitted. See PDF.]

Table 1. Dissimilarity between the trophic structure of reef fish on normal and phase shift (high zoantharian cover) reefs calculated by Similarity Analysis.

https://doi.org/10.1371/journal.pone.0116944.t001

We observed that there was no difference in overall fish abundance between normal and phase shift reefs (Student’s t-Test, t = 1.555; df = 6; p = 0.173, Fig. 4A). In relation to Elacatinus figaro there was no significant difference between densities on the two groups of reefs (t = -0.734, df = 6, p = 0.490; Fig. 4B). Finally, normal reefs had significantly lower density of Chaetodon striatus than zoantharian dominated reefs (t = 2.752; df = 6; p = 0.033; Fig. 4C).

[Figure omitted. See PDF.]

Fig 4. Density of fish per reef, where a point represents each station-value. The mean value for each group of reef is represented by the dash line and asterisk (*) marks the graph that had a significant difference (p < 0.05) according the Student's t test.

https://doi.org/10.1371/journal.pone.0116944.g004

Discussion

This is the first study to describe differences in fish assemblages associated with reefs under normal conditions (e.g. with satisfactory coral coverage) and reefs that became dominated by a fast-growing zoantharian and are now regime shifted. Despite the fact that fish richness sampled in both reef groups was relatively low (50 fish species of the 405 species registered in Brazilian reef habitats to date [64], the pattern is consistent with the number of species seen on other Brazilian reefs: 54 species reported by Chaves et al in Porto Seguro [65], 66 species reported by Kajewski and Floeter in Fernando de Noronha Archipelago [66] and 26 species reported by Medeiros et al in Picãozinho reef, located at northeaster of Brazilian coast [53]). The small number of individuals with sizes above 20 cm confirmed that the reefs of the TSB are not pristine and that these communities suffer the direct effects of human stressors as described by Dutra and Haworth [34], such as overfishing, destructive fishing, introduction of alien species, domestic and industrial sewage and oil spills. However, even in a community already under stress, the effects of phase shift on fish assemblages were evident. Under this scenario extra conservation attention needs to be given to these disturbed ecosystems in order to avoid a further worsening in reef degradation and consequent further loss of ecosystem goods and services.

We found that richness and diversity of fishes were lower on TSB phase shift reefs. This result may reflect a homogenization of the reefs under the phase shift situation. Palythoa cf. variabilis polyps are up to 4 cm long (Cruz, ICS pers. obs.) and when this species grows over the reef it obstructs and fills in reef shelters, substantially reducing rugosity by blanketing and smoothing the entire surface of the reef substratum. Moreover, the reduction of stony coral cover negatively modifies the balance between bioconstruction and bioerosion, reducing reef structural complexity [67–69]. The rugosity of a consolidated substrate is the ratio of a surface area with its planar projection and is directly proportional to the number of available shelters [24,70]. In coral reefs, the rugosity is directly proportional to the number and size of coral colonies, which in precipitating calcium carbonate, increase the structural complexity of habitats [71]. According to MacArthur and MacArthur and Tews et al. [72,73] this complexity influences the associated biodiversity and, consequently, the ecosystem function. Thus, we believe that the reduction of rugosity (i.e. habitat complexity) from increased P. cf. variabilis coverage is the main mechanism for observed changes in the local fish richness and diversity.

Positive correlation between structural complexity and reef fish diversity has been widely reported [17,18,21,22,24,74–77]. Additionally, Syms and Jones, Almany and Willis et al. [78–80] have confirmed that increasingly complex habitat provides more shelters against predators and facilitates coexistence, even for competitors, providing niche partitioning. Habitat complexity can therefore be an important factor, explaining the richness and diversity of species and potentially changing competitive interactions and survival [78,81].

Another possible explanation for this richness pattern is the decrease of heterogeneity, by the loss of substrate variety caused by the P. cf. variabilis dominance at phase shift reefs, and according to Tews et al. [73], this process is extremely dependent on scale. Heterogeneity loss probably more intensely affects small fishes with limited mobility. On the same scale, this phenomenon probably affects the mobile invertebrate assembly and may increase the abundance of some invertebrate groups to the detriment of others. Further support of this idea is shown by the fact that Palythoa species are considered to host many invertebrate species which find refuge among their soft polyps [82,83]. This could explain the abundance of mobile invertivores on phase shift reefs. Unlike sedentary fishes, mobile invertivore species can migrate to other reefs in order to find food resources.

In contrast with our results on subtropical Brazilian rocky shores Mendonça-Neto et al. [84] found that over patches with a dominance of the zoantharian Palythoa caribaeorum (~70% of benthic cover) the richness and abundance of fishes were higher than over patches with low zoantharian cover (~10%). According to Ferreira et al. [51] P. caribaeorum is found in shallower zones of these environments, which characteristically have crevices and are therefore considered to be areas of greater structural complexity. The fish richness found by Mendonça-Neto et al. [84] may in fact be associated with benthic complexity rather than being directly related with zoantharian coverage.

The two reef conditions investigated in this study did not differ significantly in total fish abundance. Other studies have indicated a weak relationship between fish abundance and complexity, in contrast to the clear negative pattern observed for richness. However, our results are in agreement with those of Risk, Gladfelter and Gladfelter, and Carpenter et al. [17,18,85], who also found no effect of complexity on species’ abundance.

On zoantharian dominated reefs we observed large number of the grunts Haemulon aurolineatum and H. steindachneri (S1 Table). Grunts are very abundant in shallow reef environments, and are nocturnal and mobile invertivores that forage mostly on zooplankton (basically juveniles) and/or macrobenthic invertebrates (adults) associated with soft substrates [51,86–88]. These two haemulids had an average length of 10 cm and were responsible for greater abundance of this size class on phase shift reefs (unpublished data collected following the AGRRA Fish Protocol [50]).

The trophic structure of fishes differed between reef groups and the large number of mobile invertivores explained this difference as they were favored by or at least uninfluenced by zoantharian dominance (S2 Table). Different from grunts, other fish groups show direct relationships with reef benthic communities, where they seek refuge against predators, find food, utilize cleaning stations, or perform reproduction and have spawning sites [9]. Sessile invertivores and carnivores are good models of groups that interact with the reef substratum. On normal reefs with heterogeneous substrate these two groups were more abundant. Roving herbivores were the other group that did not favor zoantharian dominance; Mendonça-Neto et al. [84]’s results further support the idea that roving herbivores tend to be abundant in zones without zoantharian mats. Despite this, other studies have found no relationship between the abundance of herbivorous fishes and algae cover [89,90]; the absence of zoantharians may provide more space for algal growth, which potentially benefits herbivores [84].

The corals Montastraea cavernosa, Mussismilia hispida and Siderastrea spp. are the most abundant reef builders on TSB coral reefs [36] and it is known that in the Caribbean the cleaner fish Elacatinus pallens and E. pilepis prefer microhabitats provided by Montastraea and Siderastrea [91]. The coverages on normal reef were 18.88% ±7.12 (SD), 0.98% ±0.80 and 1.88% ±0.80 respectively, while on phase shift reef they were 1.28% ±0.84, 0.01% ±0.01 and 0.02% ±0.02 and the density on normal reef were 3.26 /m2 ±0.99, 0.41 /m2 ±0.41 and 1.12 /m2 ±0.41 while on phase shift reef they were 0.39 /m2 ±0.27, 0.02 /m2 ±00.01 and 0.03 /m2 ±00.02. We therefore expected a greater abundance of the endemic (Brazil) Barber goby E. figaro on normal reefs of the TSB. However we did not observe higher abundance of this cleaner on normal reefs. On Brazilian reefs E. figaro is the main cleaner, being the only species that has an obligate cleaning behavior [92], and is strongly associated to the benthos through the corals that are used to demarcate its cleaning station [92]. The lack of a significant difference between the normal and phase shift reefs indicates the behavioral plasticity of this species, and demonstrates that it can also use other organisms such as crustose coralline algae, echinoderms or even zoantharians to mark its cleaning stations [92]. Another reason for the absence of difference in E. figaro abundance between the two sets of reefs may be the fishing pressure suffered by this species in the TSB. Due to its disruptive coloration E. figaro is a preferred target for the ornamental fish trade [93] and this activity, extensively practiced in the studied reefs, may reduce their natural stocks resulting in similar abundances.

We found a higher abundance of the butterfly fish Chaetodon striatus on phase shift reefs in TSB, a result contrary to what we expected. We can therefore reject the hypothesis that C. striatus is capable of exerting top-down control on P. cf. variabilis. According to Mendonça-Neto et al. [84] Palythoa patches provide optimal conditions for sessile invertebrate feeders (mainly chaetodontids) which may forage on polyps. Chaetodontids are highly associated with corals, especially Pacific species [18,20,94,95]. However, according to Bonaldo et al. [96], C. striatus forages on zoantharian colonies so the availability of food on phase shift reefs probably supported the higher density of butterfly fishes found on phase shift reefs. Studies evaluating what are the potential predators for P. cf. variabilis on Brazilian coral reefs are needed in order to understand underlying interactions.

In summary, we found that phase shift to P. cf. variabilis dominance had a negative effect on the diversity of fish fauna in TSB coral reefs. The impacted reefs showed (i) a lower number of fish species, and (ii) an altered trophic structure of fish assemblages, (iii) but without differences in fishes abundace. We rule out the possibility of (iv) top-down control of P. cf. variabilis from predation by C. striatus (yet also demonstrated that this fish species is favoured by the phase shift), and (v) did not see any effect of this phase shift on the ecosystem services provided by the cleaner E. figaro due to reduced coral cover. Further studies are needed to understand both how this phase shift alters the trophic structure of fish assemblages and the underlying ecological processes involved.

Supporting Information

[Figure omitted. See PDF.]

S1 Table. Reef fishes species recorded in each station.

https://doi.org/10.1371/journal.pone.0116944.s001

(XLSX)

S2 Table. Trophic guilds recorded in each station.

https://doi.org/10.1371/journal.pone.0116944.s002

(XLSX)

Acknowledgments

The authors thank Ricardo J. Miranda and Amanada E.N. de Carvalho for field support and anonymous reviewers for suggestions which improved the manuscript.

Author Contributions

Conceived and designed the experiments: ICSC ML TA RR JACCN RKPK JCC. Performed the experiments: ICSC ML TA RR JACCN. Analyzed the data: ICSC ML TA RR JACCN JDR MM. Contributed reagents/materials/analysis tools: ICSC ML TA RR JACCN JDR MM. Wrote the paper: ICSC ML JACCN JDR MM RKPK JCC.

Citation: Cruz ICS, Loiola M, Albuquerque T, Reis R, de Anchieta C. C. Nunes J, Reimer JD, et al. (2015) Effect of Phase Shift from Corals to Zoantharia on Reef Fish Assemblages. PLoS ONE 10(1): e0116944. https://doi.org/10.1371/journal.pone.0116944

References

1. Done TJ (1999) Coral Community Adaptability to Environmental Change at the Scales of Regions, Reefs and Reef Zones. Am Zool 39: 66–79. Available: http://icb.oxfordjournals.org/cgi/doi/10.1093/icb/39.1.66.

2. McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs : scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18: 357–367.

3. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429: 827–833. Available: http://www.ncbi.nlm.nih.gov/pubmed/15215854. pmid:15215854

4. Hughes TP, Graham NJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25: 633–642. Available: http://www.ncbi.nlm.nih.gov/pubmed/20800316. Accessed 15 July 2011. pmid:20800316

5. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247: 121–132. Available: http://www.springerlink.com/index/10.1007/BF00008211.

6. Wilkinson C (2008) Status of Coral Reefs of the World: 2008. Wilkinson C, editor Townsville, Australia: Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre. Available: http://www.gcrmn.org/status2008.aspx. pmid:25556087

7. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Mar Ecol Prog Ser 376: 295–306. Available: http://www.int-res.com/abstracts/meps/v376/p295-306/. Accessed: 2011 Jun 10.

8. Lirman D (2001) Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19: 392–399. Available: http://www.springerlink.com/openurl.asp?genre=article&id=doi:10.1007/s003380000125. Accessed: 2011 Jul 16.

9. Hoegh-Guldberg O (2006) Complexities of Coral Reef Recovery. Science (80-) 311: 42–43.

10. Mumby PJ (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28: 761–773. Available: http://www.springerlink.com/index/10.1007/s00338-009-0506-8. Accessed: 2011 Jun 13.

11. Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413: 201–216. Available: http://www.int-res.com/abstracts/meps/v413/p201-216/. Accessed: 2011 Jul 16.

12. Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163: 497–507. pmid:20058024

13. Vermeij MJA, Dailer ML, Walsh SM, Donovan MK, Smith CM (2010) The effects of trophic interactions and spatial competition on algal community composition on Hawaiian coral reefs. Mar Ecol 31: 291–299. Available: http://doi.wiley.com/10.1111/j.1439-0485.2009.00343.x. Accessed: 2013 Feb 27.

14. Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16: 747–769. Available: http://www.ncbi.nlm.nih.gov/pubmed/16711060. pmid:16711060

15. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, et al. (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science (80-) 311: 98–101. Available: http://www.ncbi.nlm.nih.gov/pubmed/16400152. Accessed: 2013 Feb 11.

16. Bonaldo RM, Hay ME (2014) Seaweed-Coral Interactions: Variance in Seaweed Allelopathy, Coral Susceptibility, and Potential Effects on Coral Resilience. PLoS One 9: e85786. Available: http://dx.plos.org/10.1371/journal.pone.0085786. Accessed: 2014 Jan 26. pmid:24465707

17. Risk MJ (1972) Fish diversity on a coral reef in the Virgln Islands. Atoll Res Bull 153: 1–4.

18. Carpenter KE, Miclat RI, Albaladejo VD, Corpuz VT (1981) The influence of substrate structure on the local abundance and diversity of Philippine reef fishes. Proceedings of 4th International Coral Reef Symposium. Manila. pp. 497–402.

19. Bell JD, Galzin R (1984) Influence of live coral cover on coral reef fish communities. Mar Ecol Prog Ser 15: 265–274.

20. Roberts CM, Ormond RF (1987) Habitat complexity and coral reef fish diversity and abundance on Red Sea fringing reefs. Mar Ecol Prog Ser 41: 1–8.

21. Gratwicke B, Speight M (2005) Effects of habitat complexity on Caribbean marine fish assemblages. Mar Ecol Prog Ser 292: 301–310. Available: http://www.int-res.com/abstracts/meps/v292/p301-310/.

22. Harborne AR, Mumby PJ, Ferrari R (2011) The effectiveness of different meso-scale rugosity metrics for predicting intra-habitat variation in coral-reef fish assemblages. Environ Biol Fishes. Available: http://www.springerlink.com/index/10.1007/s10641-011-9956-2. Accessed: 2012 Apr 2.

23. Vergés A, Vanderklift MA, Doropoulos C, Hyndes GA (2011) Spatial patterns in herbivory on a coral reef are influenced by structural complexity but not by algal traits. PLoS One 6: e17115. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3037963&tool=pmcentrez&rendertype=abstract. Accessed: 2012 Mar 10. pmid:21347254

24. Luckhurst BE, Luckhurst K (1978) Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol 49: 317–323. Available: http://link.springer.com/10.1007/BF00455026.

25. Graham NAJ, Nash KT, Kool JT (2011) Coral reef recovery dynamics in a changing world. Coral Reefs 30: 283–294. .

26. Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, et al. (2004) Regime Shifts, Resilience, and Biodiversity in Ecosystem Management. Annu Rev Ecol Evol Syst 35: 557–581. Available: http://www.annualreviews.org/doi/abs/10.1146/annurev.ecolsys.35.021103.105711. Accessed: 2012 Feb 29.

27. Work TM, Aeby GS, Maragos JE (2008) Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra atoll. PLoS One 3: e2989. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 2500175&tool = pmcentrez&rendertype=abstract. Accessed: 2013 Oct 9. pmid:18714355

28. Cruz ICS, de Kikuchi RKP, Longo LL, Creed JC (2014) Evidence of a phase shift to Epizoanthus gabrieli Carlgreen, 1951 (Order Zoanthidea) and loss of coral cover on reefs in the Southwest Atlantic. Mar Ecol: n/a–n/a. Available: http://doi.wiley.com/10.1111/maec.12141. Accessed: 2014 May 23.

29. Grutter AS, Murphy JM, Choat JH (2003) Cleaner Fish Drives Local Fish Diversity on Coral Reefs. Curr Biol 13: 64–67. pmid:12526747

30. Cirano M, Lessa GC (2007) Oceanographic characteristics of Baía de Todos os Santos, Brazil. Rev Bras Geofísica 25: 363–387. pmid:11636832

31. Laborel JL (1970) Madreporaires et hydrocoralliaires recifaux des cotes bresiliennes. Systematique, ecologie, repartition verticale et geographie. Paris.

32. Leao ZMAN, Kikuchi RKP, Testa V (2003) Corals and coral reefs of Brazil. In: Cortés J, editor. Latino American Coral Reefs. Amsterdam: Elsevier Science. pp. 9–52.

33. Silva M (2005) The Brazilian Protected Areas Program. Conserv Biol 19: 608–611.

34. Dutra LXC, Haworth RJ (2008) Human Disturbance, Natural Resilience and Management Futures: The Coral Reefs of Todos Os Santos Bay, Bahia, Brazil. J Sustain Dev 1: 13–30.

35. Yang S-Y, Bourgeois C, Ashworth C, Reimer J (2013) Palythoa zoanthid “barrens” in Okinawa: examination of possible environmental causes. Zool Stud 52: 39. Available: http://www.zoologicalstudies.com/content/52/1/39. Accessed: 2014 Jul 12.

36. Cruz ICS, Kikuchi RKP, Leão ZMAN (2009) Caracterização dos Recifes de Corais da Área de Preservação Ambiental da Baía de Todos os Santos para Fins de Manejo, Bahia, Brasil. Rev Gestão Costeira Integr 9: 3–23. Available: http://www.aprh.pt/rgci/rgci150.html. Accessed: 2014 Jun 18. pmid:8977975

37. Leão ZMAN, Kikuchi RKP, Oliveira MDM, Vasconcellos V (2010) Status of Eastern Brazilian coral reefs in time of climate changes. Panam J Aquat Sci 5: 224–235.

38. Costa OS, Nimmo M, Attrill MJ (2008) Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. J South Am Earth Sci 25: 257–270. Available: http://linkinghub.elsevier.com/retrieve/pii/S0895981107001174. Accessed: 2014 May 28.

39. Brasil (2004) Sistema Nacional de Unidades de Conservação da Natureza—SNUC, lei no 9.985, de 18 de julho de 2000; decreto no 4.340, de 22 de agosto de 2002. … PROTEÇÃO DO MEIO Ambient E DO …: 56. Available: http://www.ibap.org/teses2004/teses2004d15.doc.

40. Sinniger F, Montoya-Burgos JI, Chevaldonné P, Pawlowski J (2005) Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on the mitochondrial ribosomal genes. Mar Biol 147: 1121–1128. Available: http://www.springerlink.com/index/10.1007/s00227-005-0016-3. Accessed: 2011 Aug 9.

41. Swain TD (2010) Evolutionary transitions in symbioses: Dramatic reductions in bathymetric and geographic ranges of Zoanthidea coincide with loss of symbioses with invertebrates. Mol Ecol 19: 2587–2598. pmid:20497327

42. Bo M, Lavorato A, Di Camillo CG, Poliseno A, Baquero A, et al. (2012) Black Coral Assemblages from Machalilla National Park (Ecuador). Pacific Sci 66: 63–81. Available: http://www.bioone.org/doi/abs/10.2984/66.1.4. Accessed: 2014 Jul 29. pmid:22307663

43. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. pmid:2231712

44. Reimer JD, Takishita K, Ono S, Maruyama T (2007) Diversity and evolution in the zoanthid genus Palythoa (Cnidaria: Hexacorallia) based on nuclear ITS-rDNA. Coral Reefs 26: 399–410.

45. Sinniger F, Reimer JD, Pawlowski J (2008) Potential of DNA sequences to identify zoanthids (Cnidaria: Zoantharia). Zoolog Sci 25: 1253–1260. pmid:19267653

46. Page C, Coleman G, Ninio R, Osborne K (2001) Surverys of benthic reef communities using underwater video: Long-term monitoring of the Great Barrier Reef. Australian. Townsville: Australian Institute of Marine Science. pmid:25506954

47. Carleton CB, Done TJ (1995) Quantitative video sampling of coral reef benthos: Large-scale application. Coral Reefs 14: 35–46.

48. Cruz ICS, Kikuchi RKP, Leão ZMAN (2008) Use of the video trasnsect method for characterizing the Itacolomis reefs, Eastern Brazil. Brazilian J Oceanogr 56: 271–280.

49. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32: 1259–1269.

50. Lang JC, Marks KW, Kramer PA, Kramer PR, Ginsburg RN (2010) Agrra protocols version 5.4. ReVision: 1–31. Available: www.agrra.org.

51. Ferreira CEL, Floeter SR, Gasparini JL, Ferreira BP, Joyeux JC (2004) Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J Biogeogr 31: 1093–1106. Available: <Go to ISI>://000221906700006.

52. Medeiros PR, Grempel RG, Souza AT, Ilarri MI, Sampaio CLS (2007) Effects of recreational activities on the fish assemblage structure in a northeastern Brazilian reef. Panam J Aquat Sci 2: 288–300.

53. Medeiros PR, Grempel RG, Souza AT, Ilarri MI, Rosa RS (2010) Non-random reef use by fishes at two dominant zones in a tropical, algal-dominated coastal reef. Environ Biol Fishes 87: 237–246. Available: http://www.springerlink.com/index/10.1007/s10641-010-9593-1. Accessed: 2012 Mar 23.

54. Holt BG, Rioja-Nieto R, Aaron MacNeil M, Lupton J, Rahbek C (2013) Comparing diversity data collected using a protocol designed for volunteers with results from a professional alternative. Methods Ecol Evol 4: 383–392. Available: http://doi.wiley.com/10.1111/2041-210X.12031. Accessed: 2014 Jul 12.

55. Acosta C, Barnes R, McClatchey R (2014) Spatial discordance in fish, coral, and sponge assemblages across a Caribbean atoll reef gradient. Mar Ecol: n/a–n/a. Available: http://doi.wiley.com/10.1111/maec.12129. Accessed: 2014 Jul 12.

56. Colwell RK, Chao a., Gotelli NJ, Lin S-Y, Mao CX, et al. (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5: 3–21. Available: http://jpe.oxfordjournals.org/cgi/doi/10.1093/jpe/rtr044. Accessed: 2013 Mar 2.

57. Zar JH (2010) Biostatistical analysis. Fifth edition. New Jersey: Prentice Hall. pmid:25555789

58. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer , editor Sinauer Associates, Inc. Available: http://www.amazon.com/dp/0878932690. pmid:25057686

59. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717–2727.

60. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. 2nd ed. PRIMER-E Plymouth. Available: http://www.primer-e.com/Primary_papers.htm. pmid:25506954

61. Khalaf MA, Kochzius M (2002) Changes in trophic community structure os shore fishes at an industrial site in the Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239: 287–299.

62. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117–143. Available: http://doi.wiley.com/10.1111/j.1442-9993.1993.tb00438.x.

63. Reimer JD, Foord C, Irei Y (2012) Species Diversity of Shallow Water Zoanthids (Cnidaria: Anthozoa: Hexacorallia) in Florida. J Mar Biol 2012: 1–14. Available: http://www.hindawi.com/journals/jmb/2012/856079/. Accessed: 2014 Jul 23.

64. Vila-Nova DA, Ferreira CEL, Barbosa FG, Floeter SR (2014) Reef fish hotspots as surrogates for marine conservation in the Brazilian coast. Ocean Coast Manag 102: 88–93. Available: http://linkinghub.elsevier.com/retrieve/pii/S0964569114002865. Accessed: 2014 Oct 8.

65. Chaves L de CT, Nunes J de ACC, Sampaio CLS (2010) Shallow reef fish communities of south Bahia coast, Brazil. Brazilian J Oceanogr 58: 33–46.

66. Krajewski JP, Floeter SR (2011) Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition. Environ Biol Fishes. Available: http://www.springerlink.com/index/10.1007/s10641-011-9813-3. Accessed: 2011 Aug 3.

67. Knowlton N, Jackson JBC (2001) The ecology of coral reefs. In: Bertness M, Gaines S, Hay M, editors. Marine Community Ecology. Sunderland: Sinauer Associates, Inc. pp. 395–422.

68. Sorokin YI (1993) Coral Reef Ecology. Berlin, Heidelberg: Springer Berlin Heidelberg. Available: http://linkinghub.elsevier.com/retrieve/pii/0022098195900535. Accessed: 2014 Oct 11. pmid:25577943

69. Ladd HS (1961) Reef Building: The growth of living breakwaters has kept pace with subsidence and wave erosion for fifty million years. Science 134: 703–715. Available: http://www.ncbi.nlm.nih.gov/pubmed/17795280. Accessed: 2014 Oct 7. pmid:17795280

70. Dustan P, Doherty O, Pardede S (2013) Digital reef rugosity estimates coral reef habitat complexity. PLoS One 8: e57386. Available: http://www.ncbi.nlm.nih.gov/pubmed/23437380. Accessed: 2013 Feb 27. pmid:23437380

71. Feary DA, Almany GR, McCormick MI, Jones GP (2007) Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153: 727–737. Available: http://www.ncbi.nlm.nih.gov/pubmed/17566781. Accessed: 2013 Feb 9. pmid:17566781

72. MacArthur RH., MacArthur JW (1961) On Bird Species Diversity Author. Ecology 42: 594–598. Available: http://www.jstor.org/stable/1932254.

73. Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, et al. (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31: 79–92. Available: http://doi.wiley.com/10.1046/j.0305-0270.2003.00994.x.

74. Caley MJ, StJohn J (1996) Refuge availability structures assemblages of tropical reef fishes. J Anim Ecol 65: 414–428. Available: http://www.jstor.org/stable/5777.

75. Graham NAJ (2014) Habitat complexity: coral structural loss leads to fisheries declines. Curr Biol 24: R359–61. Available: http://www.ncbi.nlm.nih.gov/pubmed/24801184. Accessed: 2014 Jul 12. pmid:24801184

76. Graham NAJ, Nash KL (2012) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32: 315–326. Available: http://link.springer.com/10.1007/s00338-012-0984-y. Accessed: 2014 Jul 12.

77. Rogers A, Blanchard JL, Mumby PJ (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24: 1000–1005. Available: http://www.ncbi.nlm.nih.gov/pubmed/24746794. Accessed: 2014 Jul 12. pmid:24746794

78. Syms C, Jones GP (2000) Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81: 2714–2729.

79. Almany GR (2004) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106: 275–284. Available: http://doi.wiley.com/10.1111/j.0030-1299.2004.13193.x. Accessed: 2014 Jan 17.

80. Willis SC, Winemiller KO, Lopez-Fernandez H (2005) Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia 142: 284–295. Available: http://www.ncbi.nlm.nih.gov/pubmed/15655689. pmid:15655689

81. Jones GP (1988) Experimental evaluation of the effects of habitat structure and competitive interactions on the juveniles of two coral reef fishes. J Exp Mar Bio Ecol 123: 115–126.

82. Den Hartog J, Türkay T (1991) Platypodiella georgei spec. nov. (Brachyura: Xanthidae), a new crab from the island of St. Helena, South Atlantic Ocean, with notes on the genus Platypodiella Guinot, 1967. Zool Meded Leiden 65: 209–220.

83. Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiologia 548: 207–215. Available: http://www.springerlink.com/index/10.1007/s10750-005-5441-2. Accessed: 2014 Oct 12.

84. Mendonça-Neto JP, Ferreira CEL, Chaves LCT, Pereira RC (2008) Influence of Palythoa caribaeorum (Anthozoa, Cnidaria) zonation on site-attached reef fishes. An Acad Bras Cienc 80: 495–513. Available: http://www.ncbi.nlm.nih.gov/pubmed/18797801. pmid:18797801

85. Gladfelter WB, Gladfelter EH (1978) Fish community structure as a function of habitat structure on West Indian patch reefs. Rev Biol Trop 26: 65–84.

86. Ferreira CEL, Gonçalves JEA (2006) Community structure and diet of roving herbivorous reef fishes in the Abrolhos Archipelago, south-western Atlantic. J Fish Biol 69: 1533–1551. Available: http://doi.wiley.com/10.1111/j.1095-8649.2006.01220.x. Accessed: 2014 Oct 12.

87. Pereira PHC, Ferreira BP (2013) Effects of life phase and schooling patterns on the foraging behaviour of coral-reef fishes from the genus Haemulon. J Fish Biol 82: 1226–1238. Available: . Accessed: 2014 Oct 12. pmid:23557301

88. Rocha LA, Lindeman KC, Rocha CR, Lessios HA (2008) Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae). Mol Phylogenet Evol 48: 918–928. Available: http://www.ncbi.nlm.nih.gov/pubmed/18599320. pmid:18599320

89. Wellington GM, Victor BC (1985) El Nino mass coral mortality: a test of resource limitation in a coral reef damselfish population. Oecologia (Berlin) 68: 15–19.

90. Chabanet P, Ralambondrainy H, Amanieu M, Faure G, Galzin R (1997) Relationships between coral reef substrata and fishes. Coral Reefs 16: 93–102.

91. Taylor MS, Van Tassell JL (2002) Observations on Microhabitat Utilization by Three Widely Distributed Neotropical Gobies of the Genus Elacatinus. Copeia 4: 1134–1136. Available: http://www.bioone.org/doi/abs/10.1643/0045-8511(2002)002[1134:OOMUBT]2.0.CO;2.

92. Sazima I, Sazima C, Francini-Filho RB, Moura RL (2000) Daily cleaning activity and diversity of clients of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil. Environ Biol Fishes.

93. Sampaio CLS, Notthinham MMC (2008) Guia para identificação de peixes ornamentais. Ibama, Brasília. pp. 205. pmid:20023804

94. Fowler AJ (1990) Spatial and temporal patterns of distribution and abundance of chaetodontid fishes at One Tree Reef, southern GBR. Mar Ecol Prog Ser 64: 39–53.

95. Cox EF (1994) Resource use by corallivorous butterflyfishes (family Chaetodontidae) in Hawaii. Bull Mar Sci 54: 535–545.

96. Bonaldo RM, Krajewski JP, Sazima I (2005) Meals for two: foraging activity of the butterflyfish Chaetodon striatus (Perciformes) in southeast Brazil. Braz J Biol 65: 211–215. Available: http://www.ncbi.nlm.nih.gov/pubmed/16097723. pmid:16097723