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Coral Reefs DOI 10.1007/s00338-015-1382-z

REPORT

An assessment of shallow and mesophotic reef brachyuran assemblages on the south shore of O‘ahu, Hawai‘i

1 1,2,3 4 Kaleonani K. C. Hurley • Molly A. Timmers • L. Scott Godwin • 1 5 1 Joshua M. Copus • Derek J. Skillings • Robert J. Toonen

Received: 1 February 2015 / Accepted: 27 November 2015 Ó Springer-Verlag Berlin Heidelberg 2015

Abstract Shallow coral reefs are extensively studied but, communities. A total of 663 brachyuran representing although scleractinian corals have been recorded to 165 m, 69 morphospecies (16 families) were found. Community little is known about other mesophotic coral reef ecosystem composition was not significantly different within depths, (MCE) inhabitants. Brachyuran crabs fill many ecological but was highly stratified by depth. Each depth was distinct, and trophic niches on reefs, making them ideal candidates but the 30 and 60 m depths were least dissimilar from one for evaluating species composition among depths to ask another. We show that deeper reefs host significantly dif- whether MCEs host the same communities as shallower ferent brachyuran communities, and at much lower total reef communities that have been well studied. Here we abundance, than shallow reefs in Hawai‘i, with 4–27 deployed autonomous reef monitoring structures for 2 yr on unique morphospecies per depth and only 3 of 69 mor- the south shore of O‘ahu along a depth gradient (12, 30, 60, phospecies (*4 %) occurring across the entire depth range and 90 m) to sample and assess brachyuran crab sampled.

Keywords Biodiversity Depth gradient Cryptic fauna Á Á Á Communicated by Biology Editor Dr. Mark J. A. Vermeij Autonomous reef monitoring structures (ARMS)

Electronic supplementary material The online version of this article (doi:10.1007/s00338-015-1382-z) contains supplementary material, which is available to authorized users. Introduction

& Kaleonani K. C. Hurley Tropical coral reefs are among the most biodiverse and [email protected] productive ecosystems in the world (Moberg and Folke

1 1999; Roberts et al. 2002; Knowlton et al. 2010). A vast The Hawai‘i Institute of Marine Biology, University of Hawai‘i at Ma¯noa, Coconut Island, P.O. Box 1346, Kaneohe, majority of coral reef studies to date have focused on HI 96744, USA shallow habitats of B40 m due to the physiological 2 Joint Institute for Marine and Atmospheric Research, restrictions placed on divers using SCUBA, but coral reefs University of Hawai‘i at Ma¯noa, 1000 Pope Road, MSB 312, extend well beyond SCUBA depth limits (Maragos and Honolulu, HI 96822, USA Jokiel 1986; Kahng et al. 2010). Mesophotic coral reef 3 Ecosystem Sciences Division, Pacific Islands Fisheries ecosystems (MCEs) occur in the deeper parts of the photic Science Center, National Oceanic and Atmospheric zone (30 to [150 m) and are predominantly characterized Administration, 1845 Wasp Boulevard, Building 176, by light-dependent corals and algae (Hinderstein et al. Honolulu, HI 96818, USA 4 2010). Office of National Marine Sanctuaries, Papaha¯naumokua¯kea Studies to date examining MCEs have primarily focused Marine National Monument, National Oceanic and Atmospheric Administration, 1845 Wasp Boulevard, on fish or the dominant sessile taxa, including sponges, Building 176, Honolulu, HI 96818, USA macroalgae, and scleractinian corals (Lesser et al. 2009; 5 Brooklyn College, 2900 Bedford Avenue, Brooklyn, Bongaerts et al. 2010; Kahng et al. 2010, 2014). A range of NY 11210, USA physical and biological mechanisms results in depth

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Coral Reefs zonation of coral reef ecosystems, but such studies are plate, which is affixed to the seafloor (Fig. 2b). Three likewise limited to these same groups (e.g., Wellington ARMS each were deployed at three sites spaced 20 m apart 1982). Despite the overwhelming research focus on these at 12 m in 2009 and retrieved in 2011 (total of 9 units at charismatic taxonomic groups, it is well known that fish 12 m). Six ARMS were deployed at each 30-, 60-, and and reef-building taxa make up only a small portion of the 90-m mesophotic site in 2010 and retrieved in 2012. After total biodiversity; the larger portion of reef organisms is a 2-yr soak period, ARMS were removed from the benthos comprised of cryptic reef dwellers (Small et al. 1998; by encapsulating the unit within a 100-lm mesh-lined crate Fautin et al. 2010; Knowlton et al. 2010). Because so few that prevented motile organisms from escaping (Fig. 2c). studies target cryptic reef fauna, however, it remains Once at the surface, ARMS were transported to shore and unknown how the ecology and diversity of these species placed into a container full of seawater where the mesh- change across reefs, across latitude, or with increasing lined crate was removed and the unit was systematically depth (Fautin et al. 2010; Leray and Knowlton 2015). disassembled plate-by-plate. Seawater from the disassem- The shallow coral reefs of Hawai‘i have been exten- bly container was filtered using 2-mm, 500-lm, and sively studied (reviewed by Jokiel 1987; Kay 1994; Ziegler 100-lm geologic sieves (see Leray and Knowlton 2015 for 2002; Bahr et al. 2015), and although scleractinian corals ARMS processing details), and organisms obtained were have been recorded in mesophotic zones to 150 m (south of preserved in 95 % ethanol for future studies. Adult Hawai‘i Island; Kahng and Maragos 2006), little is known brachyurans (C5 mm) were photographed, identified, about cryptic reef inhabitants that make up the vast assigned a sample number, and preserved in 95 % ethanol majority of marine biodiversity, including dominant taxa (Fig. 2d) and were sent to the Bernice Pauahi Bishop such as brachyuran crabs (Bickford et al. 2007; Fautin et al. Museum for curation (Honolulu, HI, USA). 2010). Brachyurans are ubiquitous members of reef com- munities that fill many trophic niches (Plaisance et al. Data analysis 2011) and are among the most species-rich inhabitants of the benthic community. Because of their abundance and Brachyuran species lists and counts were collated for each ecological importance on tropical coral reefs (Costello ARMS unit and summary statistics on abundance and et al. 2010; Fautin et al. 2010; Knowlton et al. 2010), family distributions were obtained in R v3.1.3 (R Core brachyurans make ideal candidates for the investigation of Team 2015). Although megalopae were present in some cryptic reef infaunal biodiversity. The objective of this ARMS units, they were not included in analyses. Species study was to characterize the abundance and diversity of variability among ARMS at a single depth and among brachyuran crab assemblages across a depth gradient. We depths at a single site was assessed using canonical anal- test the hypothesis that brachyuran crab assemblages are ysis of principal coordinates (CAP), permutational analysis comparable across the depth gradient from 12 to 90 m. of variance (PERMANOVA), and permutational analysis of dispersion (PERMDISP) on Bray–Curtis similarity of square-root-transformed ARMS species abundance data in Materials and methods PRIMER v6 PERMANOVA software (Clarke and Gorley 2006; Anderson et al. 2008). Although this program allows Sample collection for accurate analyses of unbalanced designs, we addition- ally conducted CAP, PERMANOVA, and PERMDISP Standardized collecting and marine biodiversity measuring tests on the abundance data across depths randomly tools called autonomous reef monitoring structures removing three of nine ARMS from 12-m sites to compare (ARMS) were deployed by divers in shallow and meso- with tests on all data from all ARMS (6 units per depth). photic coral reef sites along a depth gradient on the south CAP constrains ordination that is based on distance or shore of the island of O‘ahu, Hawai‘i (Fig. 1). ARMS are dissimilarity measures (Anderson and Robinson 2003; long-term collecting devices designed to mimic the struc- Willis and Anderson 2003). CAP using Bray–Curtis dis- tural complexity of a coral reef and attract colonizing tance and 9999 permutations was used to visualize differ- motile and sedentary marine taxa (Brainard et al. 2009; ences between crab assemblages at each depth. To identify Knowlton et al. 2010; Plaisance et al. 2011; Leray and which crabs characterize differences among groups, vec- Knowlton 2015). They are composed of 10 gray, type 1 tors were imposed based on Spearman rank correlations of PVC plates (23 cm 9 23 cm) stacked in an alternating individual species. PERMANOVA and PERMDISP were series of open and semi-enclosed layers with the topmost also based on Bray–Curtis similarity and 9999 permuta- layer composed of medium-density polypropylene filter tions. CAP, PERMANOVA, and PERMDISP using the media pads (Matala USA, Laguna Hills, CA) (Fig. 2a). Jaccard index were also run for comparison with Bray– This tier of plates is attached to a 35 cm 9 45 cm base Curtis similarity measures. While both Bray–Curtis

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Fig. 1 Map of the south shore of O‘ahu, Hawai‘i, with autonomous reef monitoring structure (ARMS) deployment sites. Three ARMS were deployed at three sites at 12 m, and 6 ARMS were deployed at each of 30, 60, and 90 m depths

Fig. 2 Autonomous reef monitoring structure (ARMS). a Assembled 2-yr submerged period; c retrieval of ARMS; and d brachyuran crabs and ready to be deployed; (b) after various encrusting organisms and collected using ARMS cryptic reef-dwelling organisms colonize the ARMS units during the similarity and Jaccard indexes are commonly used with to test dissimilarity within these a priori groups as com- ecological data, Bray–Curtis similarity was chosen as the pared to between the groups. The a priori groups for this primary index because the analyses were based on abun- study were based on the sampling depths (12, 30, 60, dance data rather than presence/absence data. PERMDISP 90 m). is used to determine whether there are differences in dis- Sample-based rarefaction curves and both Chao I and persions among a priori groups, and PERMANOVA is used abundance-based coverage estimator (ACE) diversity

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Coral Reefs estimates for species abundance, depth, and site were cre- among families, results are consistent whether Chlorodiella ated using EstimateS v 9.1 (Chao et al. 2009; Colwell spp. specimens are included or excluded from the analyses 2013). For sample-based rarefaction, each ARMS unit (ESM Table S3; ESM Figs. S5, S6, S7, S8). (sample) at a single depth was treated as a replicate. The PERMANOVA and PERMDISP pairwise comparisons rarefaction curve was based on re-sampling abundance data between assemblages at the three 12-m sites (with site as a from all units at each depth, regardless of uneven sampling fixed factor with three levels) revealed similarity among effort. Rarefaction curves at each depth were calculated the three sites (p = 0.1–0.8). Likewise, constrained ordi- using 100 randomizations (reference sample = 9 ARMS at nation (CAP) revealed no significant separation among the 12 m; 6 ARMS at each 30, 60, and 90 m) without three 12-m sites. All 12-m sites were therefore combined as replacement and extrapolated to 18 samples for all depths. a single grouping for further analyses. The 95 % confidence intervals were added based on Col- PERMANOVA and PERMDISP were used to test for well (2013) derivations as implemented in EstimateS. The differences in crab assemblages at each depth (12, 30, 60, classic formula for the Chao I estimator was used to cal- 90 m). Depth was a fixed factor with four levels. Tests culate asymptotic species richness. Following Plaisance based on Bray–Curtis similarities were not significantly et al. (2009), we used Chao I and ACE, as conservative different from tests based on the Jaccard index (ESM nonparametric estimators of species richness, to estimate Table S4). Tests of data with three of the nine ARMS units the lower bound on species richness in the community. at 12 m randomly removed to balance sampling efforts across depths (6 ARMS each at 12, 30, 60, and 90 m) were also not significantly different from analyses of all ARMS Results data including the original 9 ARMS at 12 m (ESM Table S5). PERMANOVA pairwise comparisons revealed A total of 663 brachyuran crabs were collected from the 27 that crab assemblages from all 27 ARMS were significantly ARMS units (Electronic Supplementary Material, ESM different between depths (Table 1). Within-group similar- Tables S2 and S3; Fig. S1). Brachyuran crabs were iden- ities among ARMS at each depth were 53 % for samples tified to 69 morphospecies in 16 families (see ESM from 12 m, 47 % at 30 m, 44 % at 60 m, and 48 % at Table S1). The five families with the most individuals 90 m. PERMDISP pairwise comparisons showed that crab found in the ARMS across the various depths were assemblages were not statistically different between depths Dynomenidae, Epialtidae, Pilumnidae, Portunidae, and (Table 1). CAP demonstrated that depth was a significant (ESM Fig. S2). Xanthidae were the most factor in the differences among assemblages (d2 = 0.99, abundant brachyurans, with 63 % of all crabs belonging to p = 0.0001) and with few exceptions grouped ARMS from this family. Xanthidae also had the highest percentage of each depth most closely to others from the same depth species, representing 44 % of species across all depths (Fig. 4). The canonical axes CAP1 and CAP2 (correlations

(ESM Fig. S3). d1 = 0.99, d2 = 0.88, respectively) effectively separated Over half of the crabs were collected from the nine 12-m most of the 27 ARMS units into their respective depth ARMS units, and 40 % of the species identified were groups, particularly separating 12-m ARMS from all other detected exclusively among these shallow ARMS (ESM depths. Spearman rank correlations (q = 0.8) revealed that Table S1; Fig. S4). The highest percentage of individuals two of the three species found across all four depths— identified as species unique to a single depth was at 12 m, Chlorodiella spp. and Epiactaea nodulosa (Xanthidae)— while the lowest percentage of individuals identified as drove the grouping of ARMS by depth (Fig. 4). Addi- unique species occurred at 30 m (Fig. 3; ESM Table S1). tionally, CAP analyses successfully assigned ARMS The greatest percentage of individual specimens belonging assemblages to the respective depths, except for one 30-m to species found at two to three depths occurred both at ARMS assemblage that was assigned to 60 m. Results 30 m and at 60 m (Fig. 3). Overall, 61 % of the total were similar to Chlorodiella spp. excluded from the CAP species identified across the depths occurred in ARMS at analyses (ESM Fig. S8). 12 m. Only three species (\5 % of species found) occurred With the possible exception of 30 m, sample-based across all four depths, and the remaining 16–19 % of rarefaction curves generated for each depth did not reach species identified were found in ARMS units from two or an asymptote (Fig. 5; ESM Fig. S10), and these curves three different depths. Chlorodiella spp. (Xanthidae) were show that the sampling effort provided insufficient data for the most common crabs, in terms of both numbers and the generalizing about the expected number of brachyuran crab depths across which species were recovered (Fig. 3). The species present across the depth gradient. Using nonpara- highest percentage of Chlorodiella spp. specimens were metric species richness estimators, the depth with the found at 12 m, and the lowest percentage of Chlorodiella highest expected number of brachyuran species (Chao spp. specimens were found at 90 m. Despite the disparity I = 48, ACE = 44) was 12 m (Table 2). The depth with

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Fig. 3 Percentage of crab 100 specimens collected at four depths grouped by species into shared or restricted among depths. Species occurring exclusively in one depth are 80 Species group: colored purple; species found in Single depth only at least two depths are orange; Occurred 2 depths species occurring at three depths Occurred 3 depths are red. Chlorodiella spp., Epiactaea nodulosa, and 60 Occurred all depths: Liomera medipacificus Epiactaea nodulosa (indicated by various shades of Liomera medipacificus blue) were the only three Chlorodiella spp. species (of 69 total species) that occurred in all four depths 40 sampled Percentage of total specimens total of Percentage

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0 12 30 60 90 Depth (m)

Table 1 Permutational analysis Depth (m) comparisons PERMANOVA PERMDISP of variance (PERMANOVA) p values and permutational p value Unique permutations p value analysis of dispersions (PERMDISP) p values, obtained 12, 30 0.0005 4301 0.4382 using 9999 permutations, for 12, 60 0.0003 4329 0.1856 pairwise brachyuran crab 12, 90 0.0003 4328 0.6033 assemblage comparisons between samples from depths of 30, 60 0.0025 462 0.7171 12, 30, 60, and 90 m 30, 90 0.0022 462 0.8913 60, 90 0.0026 462 0.6355 Resemblance matrices created for PERMANOVA and PERMDISP were based on the Bray–Curtis simi- larity index the lowest expected number of species was 30 m, with only across this depth gradient off the south shore of O‘ahu, 28 (Chao I) to 31 (ACE) species expected (Table 2). Hawai‘i, we found that each depth zone (12, 30, 60, and 90 m) hosted significantly different crab assemblages (Table 1). The most striking difference among depths was in Discussion the xanthid genus Chlorodiella, but even when this most abundant group was excluded from the analyses, the There is growing interest in MCEs (e.g., Lesser et al. 2009; brachyuran assemblage at each depth was significantly dif- Bongaerts et al. 2010; Hinderstein et al. 2010; Kahng et al. ferent (ESM Table S3; ESM Figs. S5, S6, S7, S8). The most 2010, 2014). Among the most common reasons cited for the notable trend in these data is the substantially lower abun- study of MCE habitats are that they are dramatically dance of brachyurans from deep than from shallow ARMS understudied and host taxonomic novelty (e.g., Pyle et al. (ESM Fig. S2). It is also noteworthy that the general 2008; Petrescu et al. 2012; reviewed by Bridge et al. 2012; decrease in abundance of crabs from shallow to mesophotic Kahng et al. 2014) or that they have potential to provide a depths was consistent across families, but only when depth refuge in the face of global climate change (e.g., Chlorodiella was included; analyses with Chlorodiella Glynn 1996; Lesser et al. 2009; White et al. 2013; reviewed excluded revealed the reverse pattern in the remaining by Bongaerts et al. 2010). Based on the ARMS deployed Xanthidae (ESM Figs. S3, S4). One important caveat is that

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0.4 Table 2 Observed (Sobs) and estimated species richness (Sest) for the Depth (m) 12 crab assemblage at each depth 30 60 Depth (m) Ref sample Sobs Sest ACE Chao I 90 0.2 12 9 42 42 ± 4 68 ± 8 73 ± 22 30 6 25 25 ± 2 32 ± 4 28 ± 3 60 6 24 24 ± 3 34 ± 3 44 ± 17 90 6 21 21 ± 3 31 ± 3 46 ± 24 0 Chlororidella spp.

CAP2 The Sest, ACE, and Chao I estimators and standard deviations (SD) were calculated using EstimateS (reported as mean ± SD)

-0.2 Epiactaea Thalamita nodulosa coeruleipes change horizontally. Regardless, the majority of the brachyuran diversity sampled in this study was restricted to the shallow water reef habitats, with 27 unique morphos- -0.4 pecies, or roughly *40 % of crab species based on average -0.4 -0.2 0 0.2 0.4 number of crab species by depth, found only within the CAP1 ARMS from the 12-m sites (ESM Table S1; ESM Fig. S2). Fig. 4 Vector overlays of Spearman rank correlations of individual Drawing accurate estimates of species richness from crab species on canonical analysis of principal coordinates (CAP) community samples is an area of considerable research and ordination of brachyuran crab assemblages for autonomous reef debate (Gotelli and Colwell 2001). Following similar pre- monitoring structures (ARMS) at 12 m (green crosses), 30 m (orange triangles), 60 m (blue squares) and 90 m (red diamonds). Resem- vious work (Plaisance et al. 2009) and recent reviews on blance matrix based on Bray–Curtis similarity; Spearman rank the subject (Walther and Moore 2005; Knowlton et al. restricted to q = 0.8 2010), we used Chao I and ACE nonparametric abundance- based estimators of species richness (Hortal et al. 2006). the characteristic assemblages for each depth could also be Expected species richness was close to the Chao I and ACE influenced by the geographic spread or some gradient other estimated values for 12 and 30 m, but fell short of the than depth among the sites (Fig. 1). Further sampling of estimated species richness at 60 and 90 m (Table 2). Thus, reefs around O‘ahu will enhance our understanding of the based on the reference sample sizes, the sampling effort at spatial scale at which shallow and mesophotic communities 60 and 90 m should be expanded to at least nine ARMS for

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0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 Number of ARMS

Fig. 5 Rarefaction curves for crab assemblages of all ARMS units from 12 m (green), 30 m (orange), 60 m (blue), and 90 m (purple). The number of ARMS used at 12 m as reference is 9. For all other depths, reference sample = 6

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Coral Reefs future studies to obtain a more accurate estimate of total our study are restricted in depthdistribution,itispossible brachyuran species richness at mesophotic depths. that the two cryptic Chlorodiella species may segregate The pairwise comparisons of PERMANOVA (Table 1) by depth, but if not they could be the most promising indicated that the variability between depths was greater species with which future studies might investigate ver- than the variability within a single depth. The lack of tical connectivity. significance of PERMDISP pairwise tests also revealed that these differences were not due to dispersion. Additionally, Hawaiian brachyuran diversity the CAP ordination revealed that the assemblage in an ARMS unit could be reliably reassigned into its coordi- The initial knowledge of brachyuran fauna from meso- nating depth. Although some species overlap was observed photic depths in Hawai‘i came from dredge sampling across depths, this was over a limited depth range, with conducted throughout the archipelago during a research only three species of crabs found at every depth, and only expedition by the United States Fish Commission in 1902 Chlorodiella spp. in abundance across depths (Fig. 3). It is aboard the research vessel Albatross. The Albatross dredge also noteworthy that all three of these depth generalists operations sampled 397 stations that included littoral, (Chlorodiella spp., E. nodulosa, and Liomera medipacifi- mesophotic, and bathyal depths, which provided decapod cus) are members of Xanthidae, which is the largest and samples used to create the first formal inventory one of the least taxonomically resolved brachyuran crab of brachyuran fauna for Hawai‘i (Rathbun 1906). The families (Ng et al. 2008; Lai et al. 2011), and no other crab extensive taxonomic work done on Hawaiian brachyuran families were found across all four depths. Xanthidae are fauna from nearshore reef habitat (Edmondson 1954, 1959, considered omnivore/herbivores, based on cheliped mor- 1962) showed that with the exception of some families, phologies and the structure of their gastric mills (Knudsen there was faunal overlap with the Albatross samples. Our 1960). Monteforte (1987) showed that the zonation and study revealed not only that the greatest percentage of trophic structure of reef-associated brachyurans were based species were found in the shallow 12-m samples, but also on the bioecological characteristics of the species present. that the highest percentage of unique species were found The study also showed that the omnivore/herbivores (rep- there. Further work is required to investigate whether any resented by xanthids) had the highest relative abundance of the species found in our studies are novel. Exploration of across a high-island reef biotope (Monteforte 1987). A MCEs is expected to reveal increasing species richness, but basic premise of crustacean ecology states that the these original studies in combination with our results numerically dominant species within a biotope are gener- suggest that further sampling will reveal greater abun- ally those that are best adapted to efficiently exploit food dances of known species in addition to new species dis- and habitat resources (Abele 1972). coveries, which will help to better characterize overall The crab that occurs most commonly across all sam- biodiversity across the depth gradient. ples on the depth gradient was the xanthid, Chlorodiella There are 284 brachyuran species recorded for the spp., which cannot be reliably identified to species. Hawaiian Archipelago; the most speciose coral reef-asso- Despite being a common member of Indo-Pacific reefs ciated families are the Xanthidae, Pilumnidae, Portunidae, and rocky shores, Chlorodiella taxonomy remains prob- Parthenopidae, Grapsidae, Epialtidae, and Trapeziidae lematic (Rathbun 1906;Lasleyetal.2014), and DNA (Castro 2011). The most common brachyurans found in barcodes exist for fewer thanhalfofthenamedspecies. coral reef habitats in Hawai‘i are from the family Xanthi- Of the six species found in the Pacific, the two found in dae (Castro 2011). This has also been shown to be true in Hawai‘i (Chlorodiella cytherea and C. laevissima; Castro French Polynesia (Poupin 1996), the Marshall Islands 2011)arealmostimpossibletodistinguishmorphologi- (Garth et al. 1987), and the Marianas Islands (Paulay et al. cally except through microscopic examination of the 2003). Particularly successful exploitation of cavity habitat male gonopods (Lasley et al. 2014). Because these spe- associated with coral reefs is another trait that might help cies cannot easily be identified morphologically and DNA to explain the success of the Xanthidae. It has been shown barcodes available in NCBI and BOLD are more diver- that in the absence of cavity substrate and rubble, there is gent within species than between them, we remain higher fish predation pressure on brachyuran populations uncertain about the identity of these crabs and whether or that are adapted to such habitat (Engstrom 1984). Suc- not they represent a single species. Future investigation cessful utilization of coral reef habitat from littoral to into potential vertical connectivity of Chlorodiella spp. is mesophotic depths in all brachyuran families is important possible with genetic samplingfromthepreservedindi- since the particular fish species (Wainwright and Bellwood viduals, but taxonomic resolution seems a necessary first 2002) and octopus (Yarnall 1969) that prey upon them are step. Given that over 95 % of the other crabs sampled in also present.

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Comparison of brachyuran diversity with previous revealed that coral communities occurring in shallow mesophotic surveys waters extended down to *60 m (Bridge et al. 2012). Likewise, Luck et al. (2013) found the lower depth limit of Although mesophotic reefs are not as well described as some shallow Leptoseris spp. to be 60–80 m. In this study, their shallow reef counterparts, there is evidence from the we found that three morphospecies of crabs had a species Western Atlantic (e.g., Goreau and Goreau 1973; Liddell range from 12 to 90 m and the CAP ordination (Fig. 4) and Avery 2000) and Indo-Pacific (e.g., Rooney et al. showed that the 30- and 60-m ARMS crab assemblages 2010; Bridge et al. 2012; Wagner et al. 2014) that suggests were more similar to each other than they were to either of a general decrease in species diversity across reef-building the other two depths sampled. Further sampling of similar taxa as depth increases (Liddell and Avery 2000; Kahng depth gradients for other species could support the possi- and Kelley 2007; Bridge et al. 2012). Multiple studies on bility that either this intermediate depth range (30–60 m) dominant mesophotic benthic organisms show that while serves as a transition zone from shallow to mesophotic or some species of coral, sponge, and algae have higher per- that it represents a distinct intermediate depth community. cent coverage below *50 m, the total number of species is Additionally, further research on the cryptic reef-dwelling significantly less than in shallow waters of \30 m (Rezak fauna is needed to reveal how coral reef communities are et al. 1985; Liddell et al. 1997; Kahng and Kelley 2007). segregated by depth, and will help to identify areas of Patterns of decreased diversity are not exclusive to unique biodiversity, as well as boundaries between depth- benthic nonmotile organisms. Decreases in overall species stratified reef ecosystems. richness, number of species per unit area, and individual abundance with decreasing depth are also reported for Acknowledgments This work was funded through a combination of fishes (Kahng et al. 2010; Bryan et al. 2013; Kane et al. grants including NSF OCE 12-60169, NSF GRFP DGE-1329626, the Jessie D. Kay Fellowship, the Seaver Institute, a UH Ma¯noa Arts and 2014), although the proportion of endemics among them Humanities Grant, and the Carol Ann & Myron K. Hayashida can be exceptionally high (Kane et al. 2014). Our study Scholarship. We thank NOAA Coral Reef Ecosystem Division and K. matches these patterns, in which both abundance of crabs Reardon for generous assistance with the shallow ARMS sites and found and total number of species decreased with depth crab identifications and the UH Ma¯noa Dive Safety Office, D. Pence, K. Stender, J. Jones, and C.J. Bradley for installation and retrieval of from 30 to 90 m (the depths at which sampling effort was the mesophotic ARMS. We thank the ToBo laboratory members, equal to 6 units per depth). Despite these trends, more particularly M. Iacchei, C. Ka‘apu-Lyons, and Z. Hee, for discussion, involved studies of mesophotic reef dwellers could show support, and their efforts in the disassembly and sorting of ARMS that overall diversity for reef infauna may be underesti- samples on retrieval. We also thank M. Donahue, R. Coleman, and I. Knapp for their assistance with the analyses and writing. Special mated. New species are regularly recovered across differ- thanks are due to B. Bowen & M. Donahue for their service as ent groups after intense sampling (e.g., Pyle 2000; Pyle committee members and their valuable feedback on the manuscript. et al. 2008; Petrescu et al. 2012, 2013; Copus et al. 2015a, This is HIMB Contribution #1640 and SOEST #9545. b). A calculation of new species discovered in closed-cir- cuit rebreather diver surveys showed that an average of 5.6 new species of fishes are discovered per hour of bottom time on mesophotic reefs in the Pacific Ocean (Pyle 2000). References In addition to new species discoveries, genetic analyses of cryptic species may also contribute to diversity estimates Abele LG (1972) Comparative habitat diversity and faunal relation- and discovery of new species (Bongaerts et al. 2015). ships between the Pacific and Caribbean Panamanian decapod Crustacea: a preliminary report with remarks on the crustacean fauna of Panama. Bull Biol Soc Wash 2:125–138 Anderson MJ, Robinson J (2003) Generalized discriminant analysis Significance of mesophotic reef biodiversity based on distances. Aust N Z J Stat 45:301–318 Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA? for PRIMER: Guide to software and statistical methods. PRIMER- Despite increasing interest, MCEs remain dramatically E, Plymouth, UK understudied (Kahng et al. 2014), and even the identities of Bahr KD, Jokiel PL, Toonen RJ (2015) The unnatural history of the dominant reef-building coral species at depth remain Ka¯ne‘ohe Bay: coral reef resilience in the face of centuries of uncertain (e.g., Luck et al. 2013; Pochon et al. 2015). anthropogenic impacts. PeerJ 3:e950 Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Recent works on coral diversity have argued that the cur- Ingram KK, Das I (2007) Cryptic species as a window on rent designation of 30–40 m as the upper limit of MCEs, diversity and conservation. Trends Ecol Evol 22:148–155 originally defined by the physiological limits of SCUBA, Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) should be based instead on the stratification and composi- Assessing the ‘‘deep reef refugia’’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327 tion of the benthos (e.g., Kahng et al. 2014). For example, a Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh- study on scleractinian corals in the Great Barrier Reef Guldberg O (2015) Prevalent endosymbiont zonation shapes the

123 Author's personal copy

Coral Reefs

depth distributions of scleractinian coral species. R Soc Open Sci Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, 2:140297 Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on Brainard R, Moffitt R, Timmers M, Paulay G, Plaisance L, Knowlton ‘‘Mesophotic coral ecosystems: characterization, ecology, and N, Caley J, Rohrer F, Charette A, Meyer C, Toonen RJ, Godwin management’’. Coral Reefs 29:247–251 S, Martin J, Harris L, Geller J, Moews M (2009) Autonomous Hortal J, Borges PAV, Gaspar C (2006) Evaluating the performance reef monitoring structures (ARMS): a tool for monitoring indices of species richness estimators: sensitivity to sample grain size. of biodiversity in the Pacific Islands. 11th Pacific Science Inter- J Anim Ecol 75:274–287 Congress, Papeete, Tahiti http://webistem.com/psi2009/output_ Jokiel PL (1987) Ecology, biogeography and evolution of corals in directory/cd1/Data/articles/000442.pdf Hawaii. Trends Ecol Evol 2:179–182 Bridge TCL, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done Kahng SE, Maragos JE (2006) The deepest, zooxanthellate sclerac- TJ, Webster JM (2012) Diversity of Scleractinia and Octocoral- tinian corals in the world? Coral Reefs 25:254–254 lia in the mesophotic zone of the Great Barrier Reef, Australia. Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa Coral Reefs 31:179–189 on a deep photosynthetic reef (50–140 m) in the Au’au Channel, Bryan DR, Kilfoyle K, Gilmore RG, Spieler RE (2013) Character- Hawaii. Coral Reefs 26:679–687 ization of the mesophotic reef fish community in south Florida, Kahng SE, Copus JM, Wagner D (2014) Recent advances in the USA. J Appl Ichthyol 29:108–117 ecology of mesophotic coral ecosystems. Curr Opin Environ Castro P (2011) Catalog of the anomuran and brachyuran crabs Sustain 7:72–81 (Crustacea: : Anomura, Brachyura) of the Hawaiian Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Islands. Zootaxa 2947:1–154 Weil E, Hinderstein LM, Toonen RJ (2010) Community ecology Chao A, Colwell RK, Lin CW, Gotelli NJ (2009) Sufficient sampling of mesophotic coral reef ecosystems. Coral Reefs 29:255–275 for asymptotic minimum species richness estimators. Ecology Kane C, Kosaki RK, Wagner D (2014) High levels of mesophotic reef 90:1125–1133 fish endemism in the northwestern Hawaiian Islands. Bull Mar Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. Sci 90:693–703 PRIMER-E, Plymouth, UK Kay EA (ed) (1994) A natural history of the Hawaiian Islands: Colwell RK (2013) EstimateS: Statistical estimation of species selected readings II. University of Hawai‘i Press, Ma¯noa, HI richness and shared species from samples. Version 9. User’s Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley guide and application available at http://purl.oclc.org/estimates MJ (2010) Coral reef biodiversity. In: McIntyre AD (ed) Life in Copus JM, Pyle RL, Earle JL (2015a) Neoniphon pencei, a new the world’s oceans. Wiley-Blackwell Publishing Ltd, Chichester, species of holocentrid (Teleostei: Beryciformes) from Raro- UK, pp 65–77 tonga, Cook Islands. Biodivers Data J 3:e4180 Knudsen JW (1960) Aspects of the ecology of the California xanthid Copus JM, Ka‘apu-Lyons C, Pyle RL (2015b) Luzonichthys seaver,a crabs. Ecol Monogr 30:165–185 new species of Anthiinae (Perciformes, Serranidae) from Pohn- Lai JCY, Mendoza JCE, Guinot D, Clark PF, Ng PKL (2011) pei, Micronesia. Biodivers Data J 3:e4902 Xanthidae MacLeay, 1838 (Decapoda: Brachyura: Xanthoidea) Costello MJ, Marta Coll, Danovaro R, Halpin P, Ojaveer H, systematics: A multi-gene approach with support from adult and Miloslavich P (2010) A census of marine biodiversity knowl- zoeal morphology. Zool Anz 250:407–448 edge, resources, and future challenges. PLoS One 5:e12110 Lasley RM Jr, Klaus S, Ng PKL (2014) Phylogenetic relationships of Edmondson CH (1954) Hawaiian Portunidae. Occasional Papers of the ubiquitous coral reef crab subfamily Chlorodiellinae (De- Bernice P. Bishop Museum, Honolulu, Hawai‘i 21:217–274 capoda, Brachyura, Xanthidae). Zoo Scr 44:165–178 Edmondson CH (1959) Hawaiian Grapsidae. Occasional Papers of Leray M, Knowlton N (2015) DNA barcoding and metabarcoding of Bernice P. Bishop Museum, Honolulu, Hawai‘i 22:153–202 standardized samples reveal patterns of marine benthic diversity. Edmondson CH (1962) Xanthidae of Hawaii. Occasional Papers of Proc Natl Acad Sci U S A 112:2076–2081 Bernice P. Bishop Museum, Honolulu, Hawai‘i 22:1–309 Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic Engstrom NA (1984) Depth limitation of a tropical intertidal xanthid coral reefs. J Exp Mar Bio Ecol 375:1–8 crab, Cataleptodius floridanus, and a shallow-water majid, Pitho Liddell WD, Avery WE (2000) Temporal change in hard substrate aculeate: results of a caging experiment. J Crustacean Biol communities 10–250 m, the Bahamas. Proc 10th Int Coral Reef 4:55–62 Symp 1:437–442 Fautin D, Dalton P, Incze LS, Leong JAC, Pautzke C, Rosenberg A, Liddell WD, Avery WE, Ohlhorst SL (1997) Patterns of benthic Sandifer P, Sedberry G, Tunnell JW Jr, Abbott I, Brainard RE, community structure, 10–250 m, the Bahamas. Proc 8th Int Coral Brodeur M, Eldredge LG, Feldman M, Moretzsohn F, Vroom Reef Symp 1:437–442 PS, Wainstein M, Wolff N (2010) An overview of marine Luck DG, Forsman ZH, Toonen RJ, Leicht SJ, Kahng SE (2013) biodiversity in United States waters. PLoS One 5:e11914 Polyphyly and hidden species among Hawai‘i’s dominant Garth JS, Haig J, Knudsen JW (1987) Crustacea Decapoda mesophotic coral genera, Leptoseris and Pavona (Scleractinia: (Brachyura and Anomura) of Enewetak Atoll. In: Devaney Agariciidae). PeerJ 1:e132 DM, Reese ES, Burch BL, Helfrich P (eds) The natural history of Maragos JE, Jokiel PL (1986) Reef corals of Johnston Atoll: one of Enewetak Atoll. Volume II, Biogeography and systematics. US the world’s most isolated reefs. Coral Reefs 4:141–150 Department of Energy Office of Scientific and Technical Moberg F, Folke C (1999) Ecological goods and services of coral reef Information, Oak Ridge, TN, pp 235–261 ecosystems. Ecol Econ 29:215–233 Glynn PW (1996) Coral reef bleaching: facts, hypotheses and Monteforte M (1987) The decapod reptantia and stomatopod implications. Glob Chang Biol 2:495–509 of a typical high island coral reef complex in French Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs II. Polynesia (Tiahura, Moorea Island): zonation, community com- Geomorphology, zonation and sedimentary phases. Bull Mar Sci position and trophic structure. Atoll Res Bull 309:1–37 23:299–464 Ng PKL, Guinot D, Davie PJF (2008) Systema Brachyororum: Part I. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures An annotated checklist of extant brachyuran crabs of the world. and pitfalls in the measurement and comparison of species Raffles Bull Zool 17:1–286 richness. Ecol Lett 4:379–391

123 Author's personal copy

Coral Reefs

Paulay G, Kropp R, Ng PKL, Eldredge LG (2003) The crustaceans Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, and pycnogonids of the Mariana Islands. Micronesica McAllister DE, Mittermeier CG, Schueler FW, Spalding M, 35–36:456–513 Wells F, Vynne C, Werner TB (2002) Marine biodiversity Petrescu I, Chatterjee T, Schizas NV (2012) New genus and new hotspots and conservation priorities for tropical reefs. Science species of Cumacea (Crustacea: Peracarida) from the mesophotic 295:1280–1284 coral ecosystem of SW Puerto Rico, Caribbean Sea. Zootaxa Rooney J, Donham E, Montgomery A, Spalding H, Parrish F, Boland 3476:55–61 R, Fenner D, Gove J, Vetter O (2010) Mesophotic coral Petrescu I, Chatterjee T, Schizas NV (2013) Two new species of the ecosystems in the Hawaiian Archipelago. Coral Reefs genus Cumella (Crustacea: Cumacea: Nannastacidae) associated 29:361–367 with mesophotic reefs of Puerto Rico and St. Croix, Caribbean Small A, Adey A, Spoon D (1998) Are current estimates of coral reef Sea. Cah Biol Mar 54:257–262 biodiversity too low? The view through the window of a Plaisance L, Knowlton N, Paulay G, Meyer C (2009) Reef-associated microcosm. Atoll Res Bull 458:1–20 crustacean fauna: biodiversity estimates using semi-quantitative Wagner D, Kosaki RK, Spalding HL, Whitton RK, Pyle RL, sampling and DNA barcoding. Coral Reefs 28:977–986 Sherwood AR, Tsuda RT, Calcinai B (2014) Mesophotic surveys Plaisance L, Caley MJ, Brainard RE, Knowlton N (2011) The of the flora and fauna at Johnston Atoll, Central Pacific Ocean. diversity of coral reefs: what are we missing? PLoS One Mar Biodivers Rec 7:e68 6:e25026 Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in Pochon X, Forsman ZH, Spalding HL, Padilla-Gamin˜o JL, Smith CM, coral reef fishes. In: Sale PF (ed) coral reef fishes. Dynamics and Gates RD (2015) Depth specialization in mesophotic corals diversity in a complex ecosystem. Academic Press, San Diego, (Leptoseris spp.) and associated algal symbionts in Hawai’i. pp 33–55 R Soc Open Sci 2:140351 Walther BA, Moore JL (2005) The concepts of bias, precision and Poupin J (1996) Crustacea Decapoda of French Polynesia (Astacidea, accuracy, and their use in testing the performance of species Palinuridea, Anomura, Brachyura). Atoll Res Bull 442:1–114 richness estimators, with a literature review of estimator Pyle RL (2000) Assessing undiscovered fish biodiversity on deep performance. Ecography 28:815–829 coral reefs using advanced self-contained diving technology. Wellington GM (1982) Depth zonation of corals in the Gulf of Mar Technol Soc J 34:82–91 Panama: control and facilitation by resident reef fishes. Ecol Pyle RL, Earle JL, Greene BD (2008) Five new species of the Monogr 3:224–241 damselfish genus Chromis (Perciformes: Labroidei: Pomacentri- White KN, Ohara T, Fujii T, Kawamura I, Mizuyama M, Montenegro dae) from deep coral reefs in the tropical western Pacific. J, Shikiba H, Naruse T, McClelland T, Denis V, Reimer JD Zootaxa 1671:3–31 (2013) Typhoon damage on a shallow mesophotic reef in R Core Team (2015) R: A language and environment for statistical Okinawa, Japan. PeerJ 1:e151 computing. R Foundation for Statistical Computing, Vienna, Willis TJ, Anderson MJ (2003) Structure of cryptic reef fish Austria. https://www.R-project.org/ assemblages: relationships with habitat characteristics and Rezak R, Bright TJ, McGrail DW (1985) Reefs and banks of the predator density. Mar Ecol Prog Ser 257:209–221 Northwestern Gulf of Mexico: their geological, biological, and Yarnall JL (1969) Aspects of the behavior of Octopus cyanea Gray, physical dynamics. Wiley, New York 1849. Anim Behav 17:747–754 Rathbun MJ (1906) The brachyura and macrura of the Hawaiian Ziegler AC (2002) Hawaiian natural history, ecology, and evolution. Islands. Bulletin of the United States Fish Commission University of Hawai‘i Press, Ma¯noa 23:827–930

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