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Marine Ecology. ISSN 0173-9565 ORIGINAL ARTICLE Spatial discordance in fish, coral, and sponge assemblages across a Caribbean atoll reef gradient Charles Acosta1, Robin Barnes2 & Rebecca McClatchey1 1 Department of Biological Sciences, Northern Kentucky University, Highland Heights, KY, USA 2 Florida Department of Environmental Protection, Watershed Monitoring Section, Temple Terrace, FL, USA Keywords Belize; Caribbean; coral reef; fish diversity; Glover’s Reef; spatial gradient; sponge diversity. Correspondence Charles Acosta, Department of Biological Sciences, Northern Kentucky University, Highland Heights, Kentucky 41099, USA. E-mail: [email protected] Accepted: 12 October 2013 doi: 10.1111/maec.12129 Abstract Certain biodiversity patterns on coral reefs are generally consistent but we still lack fundamental insight into how assemblages vary across spatially heterogeneous reef systems. We compared fish, coral, and sponge assemblages across a symmetrical physiographical gradient (windward forereef, lagoon patch reef, leeward forereef) of the Glover’s Reef atoll, Belize. Species richness of fishes and corals was highest in the deep habitat (15 m) on the windward forereef. Sponges were diverse and abundant on both deep windward and leeward forereefs but not on the exposed shallow (5 m) windward forereef. Fish and benthic assemblages were relatively distinct in each reef zone, with the lagoon patch reef communities consisting of a combination of leeward and windward species. Nevertheless, there were no clear patterns in community similarity matrices of fish and benthic assemblages, suggesting that overall coral and sponge assemblages had weak or no direct association with patterns in fish assemblages. A closer examination of fish trophic groups indicated that planktivores and predators were predictably associated with depth, whereas herbivores were associated with shallow protected reefs. None was specifically associated with spatial location along the atoll gradient. These patterns of diversity distribution are important for identifying spatial conservation priorities. A Marine Protected Area (MPA) at Glover’s Reef encompasses substantial windward forereef and patch reef habitats. A much lesser extent of protection is afforded the leeward forereef that supports faunal assemblages that are unique and productive, if not as diverse as the windward forereef. Isolated coral atolls can serve as ideal systems to study spatial heterogeneity and biodiversity patterns, but more experimental studies are needed to reveal the mechanistic processes underlying these patterns. Introduction Coral reef ecosystems support highly diverse and productive faunal communities. Occupying less than 0.1% of ocean surface area, coral reefs may contain up to 40% of all fish species (Moyle & Cech 2003), as well as representatives of most invertebrate metazoan phyla. Much effort in community ecology has focused on identifying and predicting diversity patterns on coral reefs at various scales. It is expected that reef-building corals facilitate Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH high diversity of other taxa by enhancing spatial heterogeneity and other ecological factors (Karlson 1999; Pratchett et al. 2008). Yet, we do not fully understand spatial zonation patterns of diversity and assemblage structure within any taxonomic group and, in particular, correlational patterns between fish and benthic communities. Reef communities vary along certain physical gradients. A well-known pattern is zonation of coral species and morphotypes with wave energy stress (Darwin 1842; 1 Spatial discordance in reef assemblages Odum & Odum 1955; Goreau 1959; Geister 1977). Huston (1985) suggested that factors such as wave energy, light attenuation, and plankton availability associated with depth produce the highest diversity of corals at intermediate depths, consistent with predictions of the intermediate disturbance hypothesis (Connell 1978). Species richness has been shown to increase with depth from near surface to maximum at 10–30 m for both scleractinian corals (Sheppard 1980; Liddell & Ohlhorst 1981; DeVantier et al. 1998) and gorgonians (Lasker & Coffroth 1983; Dahlgren 1989). Depth and spatial location across reef gradients may influence morphological variability in scleractinian corals (Madin & Connolly 2006). This may also apply to sponges, another important functional component of the reef benthos (Diaz & R€ utzler 2001). Bell & Barnes (2002) showed that morphological diversity of sponges was highest at intermediate depths at 10–15 m, but assemblage patterns were not clearly defined. Physical stress gradients have also been linked to diversity patterns and community structure of reef fishes. Fish diversity increases with depth, often peaking at 15–20 m (Harborne et al. 2006; Friedlander et al. 2010). Fish assemblage structure can also vary with reef zonation. High diversity and abundance of planktivores often occur at intermediate depths on forereefs, whereas herbivores are dominant on backreef habitat (Friedlander & Parrish 1998). Friedlander et al. (2010) suggested that piscivorous species are expected to be common across most reef zones and dominate deeper forereef habitat, but this distribution pattern is generally absent on reefs under intense fishing pressure. Establishing associations between diversity of fishes and diversity of reef benthos has been a more intractable issue. Heterogeneity of reef benthic habitat, including corals, seagrasses, and algae, has been correlated with fish diversity (e.g. Roberts & Ormond 1987; Grober-Dunsmore et al. 2007). Species richness and abundance of select fish taxa are often correlated with living coral cover (primarily corallivores such as the Chaetodontidae; Bell & Galzin 1984; Chabanet et al. 1997; Jones et al. 2004; Bouchon-Navaro et al. 2005; Graham et al. 2006; Pratchett et al. 2006; Messmer et al. 2011). However, some studies failed to show a relationship between total fish diversity and coral diversity at local scales (i.e. a diversity; Luckhurst & Luckhurst 1978; Roberts & Ormond 1987; Gratwicke & Speight 2005; Bellwood et al. 2006). Studies of fish communities before and after severe disturbances have revealed complex responses to loss of coral cover, ranging from decreased species richness to changes in community composition (see comprehensive meta-analysis by Pratchett et al. 2011). Other studies suggest that fish diversity varies in proportion to coral diversity at larger scales across seascape gradients (b diversity; Wilson 2 Acosta, Barnes & McClatchey et al. 2006; Arias-Gonzalez et al. 2008; Belmaker et al. 2008). Understanding spatial patterns of biodiversity is important for planning effective conservation strategies for coral reefs (Bellwood et al. 2004). There is a need for further corroboration of patterns of diversity and structure of whole communities, as well as important associations between faunal groups. We studied diversity patterns in fish, coral, and sponge assemblages across a spatial gradient on a geomorphologically symmetrical atoll reef. The gradient from the lagoon to the forereef on both windward and leeward fronts allowed us to compare assemblages in reef zones that were superficially similar (depth, slope) but physiographically different (current flow, wave exposure). We tested several specific hypotheses on spatial patterns in different reef physiographic zones. H1: Is species richness of each taxon similar within and among reef zones? H2: Do species assemblages differ across the windward-leeward atoll gradient? H3: Is diversity in assemblages correlated between fishes and benthos (corals and sponges) in any reef zone? H4: Is diversity of fish trophic groups associated with living coral and sponge abundance (percent cover) or with the physical gradient (depth and windwardleeward location)? Elucidating such patterns has immediate implications for reserve design and management strategies to protect high diversity assemblages, productive communities, and vulnerable species in coral reef ecosystems. Methods Study area Surveys were conducted at the Glover’s Reef atoll off the coast of Belize in the Western Caribbean Sea in the summer months of 2003–2005 (Fig. 1). The atoll is 32 9 12 km along a N–S alignment. It is ringed by an emergent reef crest except for three major breaks on the windward side. Both windward and leeward forereefs slope from the surface to 15–20 m depth, where the vertical reef wall begins. Surrounding depths range from 350 to 1000 m within 2 km from the reef crest. The shallow coral reef community is thus isolated except for larval connectivity with the main Belize Barrier Reef and regional reefs and atolls. The central lagoon contains over 700 patch reefs, many of which rise to near the sea surface Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Acosta, Barnes & McClatchey Spatial discordance in reef assemblages 87°45‘0“W 17°0‘0“N Conservation Zones 200m contour 16°45‘0“N Fig. 1. Location of the Glover’s Reef atoll in the Western Caribbean (inset). Surveys were conducted across the windward–leeward (○, 5 and 15 m windward forereef; □, 5 and 15 m leeward forereefs; D, 3 m patch reefs) gradient of the atoll. The geomorphological cross-section (bottom; not drawn to scale) shows the physical similarity of the physiographical zones on the windward and leeward fronts. The windward forereef experiences wind and wave exposure during most of the year, whereas the leeward forereef is exposed only on occasion mainly during winter months. The lagoon is protected by an emergent reef crest with few breaks. from the lagoon floor at 2–18 m depth (Wallace & Schafersman 1977). Prevailing wind direction is typically from the ENE, except during occasional frontal systems that approach from the NNW during December to March. Therefore, the shallow windward forereef experiences vigorous wave energy most of the year, but the leeward reefs are relatively calm except occasionally during winter. The Western Caribbean gyre flows in a southerly direction in this region. Tidal amplitude is relatively small (<0.5 m). Therefore, the lagoon is not vigorously flushed on a regular basis. The atoll is currently zoned for various usages, including a Marine Protected Area (MPA) where fishing is prohibited (Fig. 1). Established in 1998, the main Conservation Zone of the MPA is triangular in shape and encompasses 24% of the atoll area. It incorporates more than 10 km of the windward reef but less than 2 km of Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH the leeward reef. Commercial fishing activity is primarily focused on benthic invertebrates (spiny lobster Panulirus argus and queen conch Strombus gigas; Acosta 2002), but high value fish species (e.g. lutjanids, serranids) are often targeted by spearfishing or handline fishing. The use of fish traps, trawling, and other destructive fishing practices is prohibited. Many of the shallow patch reefs in the lagoon have undergone a significant phase shift from coral-dominated to algal-dominated (McClanahan & Muthiga 1998). However, the underlying cause for this disturbance is still not well understood. Field surveys Reef communities were surveyed across the windward– leeward gradient of the atoll (Fig. 1). Five reef physiographic zones were sampled: (i) windward forereef 3 Spatial discordance in reef assemblages at 15 m depth near the reef wall (six sites); (ii) windward forereef at 5 m (seven sites); (iii) lagoon patch reefs at 2– 3 m (nine sites); (iv) leeward forereef at 5 m (eight sites); (v) leeward forereef at 15 m (six sites). Depths of sites were determined using a hand-held depth sounder, and locations were mapped using global positioning satellite (GPS) coordinates. Replicate sites within a reef zone were separated by a minimum of 1 km. Pairs of divers using SCUBA surveyed fish and benthic communities along transects parallel to the N–S reef alignment. One diver swam 2–3 m above the reef and used a digital video camera to record all fishes in a 5-m wide belt transect. The second diver simultaneously placed a 10-m transect tape tautly over the benthic substratum. The second diver used the video camera to record the benthos 1 m on both sides along the transect tape (i.e. a 2-m belt transect). The first diver then conducted stationary visual surveys for cryptic or resting nocturnal fishes in large coral heads and other crevice shelters; three 5-min observations were done along each transect. The recorded video and data sheets were later transcribed in the laboratory. Fishes were identified to species level (B€ ohlke & Chaplin 1993), and the abundance of each species was enumerated for each transect. Fishes were also classified into general trophic groups (piscivores, herbivores, omnivores, planktivores, corallivores) based on available life history information. Species known to occasionally feed on sponges (i.e. angelfishes, boxfishes, filefishes; Pawlik 1998) were placed with the omnivores. Corals and sponges were also identified to species level (Humann 1994a,b). Our species data for the benthos is conservative and likely to underestimate true diversity because of phenotypic plasticity, which requires microscopic analysis, especially for the sponges (Diaz & R€ utzler 2001). Data analysis We first examined species richness graphically using rarefaction curves and their 95% confidence intervals (Colwell et al. 2012). The null hypothesis was that species richness of fishes, corals, and sponges was not significantly different in the reef physiographic zones. Abundance data were pooled from transects in each of the five zones, and the expected number of species was estimated from 1000 permutations. Rarefaction curves were also used to assess whether any zone was insufficiently sampled. The number of common species (encountered in all zones) and rare species (encountered in one zone only) was also examined graphically. Estimates of b diversity were calculated as Whittaker’s bW on presence–absence data (Koleff et al. 2003) for the overall windward–leeward gradient and between pairs of adjacent reef zones. 4 Acosta, Barnes & McClatchey To further compare assemblages of faunal groups within and among reef zones, we used non-metric multidimensional scaling (nMDS) on Bray–Curtis matrices using raw abundance data (Quinn & Keough 2002). Separate tests were conducted on fish, coral, and sponge communities. Analysis of similarities (ANOSIM; Clarke 1993) was then used to corroborate significant differences in assemblage structure between pairs of reef zones. Similarity percentages (SIMPER; Clarke 1993) were used to identify the species with the most influential abundance patterns between reef zones. We then assessed whether any particular fish and benthic assemblages were correlated in a reef zone. We used partial Mantel tests on Bray–Curtis matrices to test the null hypothesis that fish assemblages are not correlated to coral assemblages, controlling for sponge assemblage in each reef zone. P-values were calculated from Monte Carlo permutation tests on correlations between two matrices (Manly 2006). Only those species present in at least one sample in a zone (i.e. non-zero abundances) were included in the matrix. To determine whether the distribution of fish species diversity by trophic group was predictable across the atoll gradient, we compared trophic groups with percent cover of living corals and sponges, reef depth, and location on the windward–leeward gradient. Canonical correspondence analysis (CCA) was conducted on Shannon H’ diversity indices for fish trophic groups scaled with the three environmental variables at each zone. Permutation tests on trace statistics were non-significant for all tests. We started with the neutral assumption that all observed fish species in a zone were part of the community, regardless of whether a species could be regarded as a transient or a habitat specialist. The life histories (including home ranges, habitat specificity, and other factors) are not well known for a substantial number of reef fish species, so we considered all observed species part of the zonal assemblage. Trophic groups were broadly categorized as piscivores, herbivores, omnivores, and planktivores. Due to low non-zero abundances of three species of known corallivores, this group was not included in the final analysis; a strong positive relationship between corallivore diversity and live coral cover is well established in previous studies (see Introduction). Results Patterns in species richness A diverse fish and benthic fauna inhabited shallow reef habitats of the Glover’s Reef atoll. We documented 108 species of fish and, at least 49 species of corals and 33 species of sponges in less than 1 ha of reef surface area Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Acosta, Barnes & McClatchey Spatial discordance in reef assemblages (Table 1). We identified 36% (26 species) of 72 scleractinian corals listed by Humann (1994a) for the tropical Western Atlantic. By comparison, we sampled 61% of sponge species and 24% of reef fish species (excluding pelagics like sharks) listed by Humann (1994b,c). The deep windward forereef at 15 m had more rare species (encountered in one zone only) of fishes and corals than other zones, but there were more rare species of sponges on the deep leeward forereef (Fig. 2). Rarefaction curves indicated that sampling was adequate for corals and sponges at most sites, but the slopes of some rarefaction curves for fishes were still increasing, indicating some underestimation (Fig. 3). Fishes 80 Table 1. Summary of fish, coral, and sponge fauna sampled at the Glover’s Reef atoll, Belize. Corals include both scleractinians and gorgonians. Sponges are listed as ‘Individuals’ but existed in complex forms including encrusting, boring, and multi-branched/tube. The Total column shows absolute values for all sites across the atoll; the number of species/families does not match because of common taxa found in more than one zone. Zone designations are windward forereef at 15 m (WFR15), windward forereef at 5 m (WFR5), lagoon patch reefs at 3 m (PR3), leeward forereef at 5 m (LFR5), and leeward forereef at 15 m (LFR15). 60 40 WFR5 WFR15 LFR5 LFR15 PR3 20 0 0 number of WFR15 WFR5 PR3 LFR3 LFR15 total Individuals Species Families Colonies Species Families Individuals Species Families 935 73 26 1301 43 15 318 20 6 699 59 21 793 49 15 60 5 5 948 58 19 1220 30 13 451 22 2 953 56 15 1826 36 14 228 18 4 583 45 15 1121 34 14 268 23 3 4118 108 34 6261 49 16 1325 33 12 sponges 60 600 800 1000 40 30 20 10 0 0 Fish Coral Sponge 50 Number of species Expected species richness corals 400 Corals 50 fishes 200 400 600 800 1000 1200 1400 1600 1800 Sponges 25 40 200 20 30 15 20 10 10 5 0 Common WFR5 WFR15 LFR5 LFR15 PR Rare Species distribution 0 0 100 200 300 400 Abundance Fig. 2. Comparison of the ubiquity of species of fishes, corals, and sponges at the Glover’s Reef atoll. Graph shows the number of common species encountered in all zones versus rare species found in only one reef zone. Zone designations are windward forereef at 5 m (WFR5), windward forereef at 15 m (WFR15), leeward forereef at 5 m (LFR5), leeward forereef (LFR15) and lagoon patch reefs at 3 m (PR3). Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Fig. 3. Rarefaction curves for expected species richness (1000 permutations) for fishes, corals, and sponges at the Glover’s Reef atoll. To maintain clarity, 95% confidence limits are not shown, but limits were significantly different only for fishes and for corals at site WFR15. There was a paucity of sponges on the shallow windward forereef at 5 m. Zone designations are as listed in Fig. 2. 5 Spatial discordance in reef assemblages Patterns in community assemblages Taken as whole assemblages, there were distinct distributional patterns within faunal assemblages across the atoll gradient (H2). Although there was some overlap in similarity of fish assemblages, the nMDS plot shows clus6 1.0 Fishes 0.71 Corals 0.37 Sponges 0.74 0.8 0.6 bW Expected fish species richness was highest on the deep windward forereef at 15 m, with about 3.6 species encountered for every 25 individuals sampled (Fig. 3). This was significantly different (at the 95% confidence limit) from species richness on the deep leeward reef at 15 m (2.6 species per 25 individuals). Confidence limits overlapped for all zones except for the deep windward reef. Species richness for corals was also higher with marginal significance on the deep windward forereef, with one new species expected for every 46 colonies encountered (Fig. 3). At the local scale, this reef zone was very heterogeneous in species composition, ranging from dense thickets of branching corals (Acropora cervicornis, Acropora palmata), diverse gorgonian stands, and a variety of small mound corals. In contrast, the leeward forereef was dominated by a few species of very large mound corals (Montastraea annularis, Montastraea cavernosa, Diploria labyrinthiformes). The leeward forereef also had higher average percent cover per transect (35%) relative to the windward forereef (29%). Sponge species richness was also highest on the deep forereefs, with the highest species richness and abundance on the deep leeward forereef (Fig. 3). The patch reef environment also had a relatively diverse sponge community consisting of species found on both shallow and deep forereefs. Estimates of species turnover based on presence– absence data indicated that the sponge fauna on the windward forereef differed from that on the other reef zones (Fig. 4). This was due primarily to the low number of species in the wave-exposed shallow windward forereef at 5 m. This species-poor site is primarily characterized by coral spur-and-groove formations and experiences the highest wave energy from prevailing winds, tropical storms, and backflow. When the shallow windward forereef zone is removed and species turnover is recalculated, bW ranges from 0.28 to 0.35 between the deep windward forereef and the other reef zones. This is well within the b diversity range for the coral and fish fauna among all zones. The species turnover patterns then becomes similar among all three faunal groups, suggesting more dynamic assemblages on the windward forereef, with the lagoon patch reefs as a transition zone. On the basis of these results, the species richness (H1) of fishes and corals was significantly higher on the deep windward forereef but sponges were consistently diverse and abundant on the deep leeward forereef. Acosta, Barnes & McClatchey 0.4 0.2 0.0 WFR15 ----- WFR5 ------ PR3 ------ LFR5 ------ LFR15 Reef zone Fig. 4. Comparison of species turnover (b diversity) across the windward–leeward gradient at the Glover’s Reef atoll. Whittaker’s b (bW) is calculated using presence–absence data for pairs of adjacent reef zones, 0 = no difference in species assemblages to 1 = 100% difference in assemblages. Sponge species turnover was impacted by the low diversity on the shallow windward forereef (WFR5); with this outlier removed, bW estimates between WFR15 and other zones were reduced to 0.28–0.35. Global bW for the windward–leeward gradient are shown next to each plot. Zone designations are as listed in Fig. 2. tering of windward reefs with some separation from the cluster of leeward and patch reefs (Fig. 5). ANOSIM tests support this general pattern (overall R = 0.30; P < 0.001) with significant differences in assemblages on windward versus leeward/patch reefs, as well as between windward shallow and windward deep reefs (Table 2). SIMPER comparisons indicate that this pattern is due to numerical dominance of a relatively few species, namely bluehead wrasse Thalassoma bifasciatum and bicolor damselfish Stegastes partitus on windward reefs. Blue chromis Chromis cyanea were ubiquitous on deeper forereef habitats. Large schools of blue tang Acanthurus coeruleus were frequently encountered on shallow windward forereefs but were rare on leeward forereef or lagoon patch reefs. Coral assemblages showed an even stronger distribution pattern between windward and leeward reefs (Fig. 5). Patch reef assemblages again appeared to have some similarity with leeward reef assemblages (AnoSim overall R = 0.71; P < 0.0001; Table 2). Gorgonian diversity (Pseudopterogorgia spp., Gorgonia spp.) was particularly high on windward reefs relative to other sites, whereas calcareous hydrozoa Millepora, sea rods Eunicea, and mound corals were abundant on leeward and patch reefs. Sponge assemblages on lagoon patch reefs were relatively distinct from any particular forereef assemblage, but this may be an artifact of patch reefs having many species in common with both windward and leeward reefs (Fig. 5). The abundance of erect rope Amphimedon compressa, brown variable Anthosigmella varians, and scattered pore Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Acosta, Barnes & McClatchey Spatial discordance in reef assemblages Table 2. Results of ANOSIM tests on Bray–Curtis distance matrices of fish, coral, and sponge assemblages at the Glover’s Reef atoll. Overall R coefficients indicate strong separation (>0.75), some overlap (0.75– 0.25) or no separation (<0.25). Shown are Bonferroni-corrected P-values for significant correlations between pair of zones across the windward–leeward gradient. Zone designations are as described in Table 1. 0.3 Fishes 0.2 0.1 0.0 WFR5 WFR15 LFR5 LFR15 PR3 –0.1 –0.2 Stress = 0.23 –0.3 –0.3 –0.2 –0.1 0.0 0.1 0.2 0.3 0.4 0.4 Corals 0.3 Axis 2 0.2 0.1 0.0 –0.1 –0.2 Stress = 0.19 –0.3 –0.3 –0.2 fisha WFR15 WFR5 PR LFR15 LFR5 coralb WFR15 WFR5 PR LFR15 LFR5 spongec WFR15 WFR5 PR LFR15 LFR5 WFR15 WFR5 PR LFR15 0.0188 0.0008 0.0051 0.0004 0.0001 0.0024 0.0015 0.1665 0.0762 0.243 0.085 0.006 0.03 0.007 0.008 0.027 0.012 0.016 0.003 0.007 0.139 0.011 0.066 0.585 0.008 0.07 1 0.042 0.14 1 LFR5 Overall R = 0.30; P < 0.001. Overall R = 0.71; P = 0.0001. c Overall R = 0.38; P = 0.0001. a –0.1 0.0 0.1 0.2 0.3 0.3 Sponges b 0.2 0.1 0.0 –0.1 –0.2 Stress = 0.14 –0.3 –0.3 –0.2 –0.1 0.0 0.1 0.2 0.3 Axis 1 Fig. 5. Non-metric multidimensional scaling (nMDS) plots are shown for fishes, corals, and sponges at the Glover’s Reef atoll across reef physiographical zones. Log and square-root transformation of the data did not improve stress, so raw data were used in all simulations. Follow-up ANOSIM tests largely corroborated these patterns (see Table 2). Zone designations are as listed in Fig. 2. sponge Aplysina fulva mainly contributed to the distinctiveness of the sponge assemblage in patch reef habitat (overall ANOSIM R = 0.38; P < 0.001). We found no direct association patterns between fish and benthic assemblages in any reef physiographic zone (H3). Partial Mantel correlations between fish and coral Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Bray–Curtis matrices (controlling for sponge assemblages) were non-significant for all reef zones (Table 3). This was supported by our examination of the distribution of fish trophic groups across the environmental gradients of live coral/sponge cover, depth, and windward–leeward site location (H4). With corallivores removed, only omnivorous fishes showed a strong relationship with percent cover of live corals and sponges (Fig. 6). Planktivores, and to a lesser extent piscivores, were associated with increasing depth, whereas herbivorous species were associated with shallow reef habitats. No fish trophic groups were specifically associated with spatial location on the leeward–windward reef gradient. Discussion Coral reefs are highly heterogeneous ecosystems with complex physical structure and biotic interactions. Even so, the atoll configuration at Glover’s Reef was amenable to a comparison of species richness and assemblage patterns in diverse reef habitats across a windward–leeward physiographical zonation. Exposure to such physical stress gradients may influence corals and associated communities in predictable ways (Huston 1985). The diversity of 7 Spatial discordance in reef assemblages Acosta, Barnes & McClatchey Table 3. Partial Mantel tests on Bray–Curtis distance matrices for correlations between fish and coral assemblages, controlling for sponge assemblages. Only species present on at least one transect in a zone were used in the matrix. Partial R correlations are calculated from 5000 permutations. P-value represents the probability that the matrices are not correlated. Zone designations are as defined in Table 1. LFR15 partial R P-value 0.373 0.8056 LFR5 WFR15 0.3529 0.1014 0.3173 0.0788 WFR5 PR3 0.2268 0.7656 0.2226 0.1968 0.06 Substratum percent cover Depth 0.04 Omnivores 0.02 Planktivores Axis 2 0.00 Piscivores –0.02 Herbivores –0.04 –0.06 –0.08 –0.10 –0.3 Windward-Leeward gradient –0.2 –0.1 0.0 0.1 0.2 0.3 Axis 1 Fig. 6. Canonical correspondence analysis (CCA) biplot is shown for diversity of fish trophic groups (Shannon Hʹ) against environmental variables at the Glover’s Reef atoll. Environmental variables were substratum percent cover of live corals and sponges, depth (3, 5, and 15 m), and spatial position on the windward–leeward gradient (shallow and deep windward forereef, lagoon patch reef, shallow and deep leeward forereef). Omnivores include occasional spongivores. Corallivores were removed from the analysis due to low abundances. Planktivores were associated with the depth gradient, whereas the greatest diversity of herbivores was found in shallow habitat. Omnivorous species were distributed with increasing live coral– sponge percent cover. Zone designations are as listed in Fig. 2. corals is expected to be low near the surface with high wave energy and ultraviolet exposure, and in deep habitats where light becomes limiting. At Glover’s Reef, the windward forereef at 15 m had the highest species richness of corals compared with other reef zones. This is consistent with patterns of coral diversity peaking at depths of less than 20 m in studies of various forereef ecosystems (Geister 1977; Sheppard 1980; Liddell & Ohlhorst 1981; Huston 1985; DeVantier et al. 1998). However, this pattern was not repeated on the leeward forereef, which is structurally similar to the windward forereef but less exposed to wave and storm stresses. Instead, older massive colonies of important reef-builders such as Montastraea and Diploria were dominant on both shallow and deep leeward reefs. These 8 types of species are important for providing structural habitat for other taxa and for coral recruit production (DeVantier et al. 1998). As such, reliance on species richness alone as a conservation metric would likely result in undervaluing this productive leeward coral community. Sponges were also highly diverse and abundant on the leeward forereef, as well as the deep windward forereef. Sponges with larger robust morphologies, such as barrel sponge Xestospongia and vase sponge Callyspongia, were abundant in the deeper habitats. These large sponges may provide important structural habitat, similar to the role of massive mound corals. Indeed, Arias-Gonzalez et al. (2008) also found that a high diversity of fishes was associated with high sponge diversity in deeper forereef habitat. The patch reefs at 3 m depth in the Glover’s Reef lagoon harbored diverse assemblages of sponges, having many species in common with the forereef. Only a few species, dominated by encrusting and boring sponges, occupied the shallow windward forereef where wave stress was maximum. The literature on coral reef fish diversity has grown extensively in recent years. The diversity of reef-associated fishes is predictably higher on larger three-dimensional reef structure than on low-relief reefs (e.g. Chabanet et al. 1997; Friedlander & Parrish 1998; Acosta & Robertson 2002; Gratwicke & Speight 2005; Arias-Gonzalez et al. 2008) or reefs undergoing degradation due to loss of reefbuilding corals (Jennings et al. 1996; Findley & Findley 2001; Jones et al. 2004; Graham et al. 2006). Similarly, the diversity of reef-dwelling invertebrates has also been shown to increase with the complexity of reef habitat (Idjadi & Edmunds 2006). Physical factors such as wave energy exposure may also structure some fish assemblages, such as small cryptic species (Depczynski & Bellwood 2005). Fish species richness and abundance commonly peak at intermediate depths of 10–20 m, increasing from backreef to deep forereef (Friedlander & Parrish 1998; Arias-Gonzalez et al. 2008; Friedlander et al. 2010). In our study, the windward forereef at 15 m had the highest diversity of fishes, whereas the leeward forereef had lower diversity. Friedlander et al. (2010) noted that windward and leeward forereefs of the Kingman Reef atoll in the Pacific had similar fish species richness and abundance, but the configuration and exposure gradient appear to be different from those at the Glover’s Reef atoll. Our data also did not reveal any clear patterns of increasing diversity from lagoon patch reefs to the deep forereef. In fact, the fish fauna was relatively diverse and abundant on lagoon patch reefs (see also Acosta & Robertson 2002; Karnauskas et al. 2012). Similarity metrics for fishes and corals within any zone were not correlated, suggesting that overall patterns in assemblage structures were not directly Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Acosta, Barnes & McClatchey associated with each other. This does not necessarily contradict evidence that fish communities respond negatively to a decline in coral cover, as this is often a lagged response to disturbances (Wilson et al. 2006). Among fish assemblages, our observations agreed with previous studies that show plankivorous reef fishes and predators are associated with the depth gradient, and herbivorous fishes are associated with shallower reef habitat (Gladfelter et al. 1980; Friedlander et al. 2010). However, there were no clear relationships between fish trophic groups and spatial location across the atoll windward–leeward gradient. This might simply reflect selective pressure for feeding strategies being dictated at the local habitat level rather than along this particular spatial gradient. The lagoonal patch reefs at Glover’s Reef had diverse communities of fishes and sponges but depauperate coral communities. Hundreds of the shallowest patch reefs have undergone a drastic ecological phase shift in which turf algae have replaced corals over the last three decades (McClanahan & Muthiga 1998). We specifically chose patch reefs sites at a deeper depth to survey the remaining coral and sponge communities in the lagoon. Corals occupying the lagoon patch reefs consisted of more gorgonians than scleractinians. Overall coral diversity was lower than in other reef zones and qualitatively much lower than in early reports (Wallace & Schafersman 1977; McClanahan & Muthiga 1998). It is likely that the fish and sponge communities will also deteriorate with loss of scleractinian corals as reef erosion exceeds reef building. It is widely accepted that coral reef MPAs often have positive impacts on fish diversity and biomass which, in turn, have positive influences on benthic community structure (e.g. Newman et al. 2006). Fishing impacts in and around the MPA at Glover’s Reef have not been quantified, and so the impacts on diversity and abundance of various fish trophic levels are unknown. While macroalgal dominance on shallow patch reefs in the lagoon is problematic, our work shows that the deeper patch reefs still contain vital and dynamic communities of fishes, sponges, and some corals such as gorgonians. Additionally, the relatively diverse and productive deeper forereef communities likely function as sources of recruitment to all habitats of the atoll. Both windward and leeward environments contain unique faunal assemblages with high conservation value. With proper management and areal coverage of protection, these reefs provide insurance for continued resilience and rehabilitation of stressed reefs in the regional ecosystem. Conclusions Assemblages of fishes, corals, and sponges were relatively distinct on similar reef physiographic zones across a Marine Ecology (2014) 1–11 ª 2014 Blackwell Verlag GmbH Spatial discordance in reef assemblages windward–leeward spatial gradient. The high diversity of branching, encrusting, and other coral morphotypes on the windward forereef was replaced by fewer species, dominated by older massive mound and boulder corals on the leeward reef. Fish species richness also peaked on the deeper windward forereef but overall zone-specific diversity patterns did not correlate well with diversity of corals and sponges. Sponge assemblages were highly diverse on more sheltered reefs, especially on the leeward exposure. Coral species richness patterns are consistent with predictions of the intermediate disturbance hypothesis (Connell 1978; Huston 1985) but where depth is less important than exposure between the dynamic windward forereef and the sheltered leeward forereef. However, patterns in fish and benthic assemblages are not in general agreement. Coral and fish diversity is high on deeper windward forereefs, but this does not diminish the importance of the deeper leeward habitat, where sponge diversity is very high. We need to move beyond simplifying assumptions (e.g. fish–coral correlations) to a more wholistic and encompassing perspective of reef ecosystems. Acknowledgements This research was funded by grants to C.A. from the Global Conservation Program of the Wildlife Conservation Society. R.M. and R.B. were funded by Northern Kentucky University Greaves Research Fellowships. We thank Janet Gibson and the staff of the Glover’s Reef Research Station at Middle Cay for excellent logistical support. Danny Westby and Andrew Branson provided invaluable field assistance. We thank two anonymous reviewers whose suggestions greatly improved the manuscript. The authors declare that there are no conflicts of interest associated with this paper. 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