spatial variability in the structure of intertidal crab and gastropod assemblages within the...

Journal of Sea Research 69 (2012) 8–15

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Journal of Sea Research

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Spatial variability in the structure of intertidal crab and gastropod assemblageswithin the Seychelles Archipelago (Indian Ocean)

Dan A. Smale a,⁎, David K.A. Barnes b, Richard S.K. Barnes b,c, David J. Smith b, David J. Suggett b

a Oceans Institute and School of Plant Biology, University of Western Australia, Crawley 6009, WA, Australiab Coral & Coastal Ecology of the Seychelles Research Programme, Coral Reef Research Unit, University of Essex, Colchester, Essex, UKc Department of Zoology, University of Cambridge, Cambridge, UK

⁎ Corresponding author at: Oceans Institute, UniversityWestern Australia 6009, Australia. Tel.: +61 8 64882219

E-mail address: daniel.smale@uwa.edu.au (D.A. Sma

1385-1101/$ – see front matter © 2012 Elsevier B.V. Alldoi:10.1016/j.seares.2012.01.002

a b s t r a c t

Article history:Received 12 July 2011Received in revised form 5 January 2012Accepted 6 January 2012Available online 14 January 2012

Keywords:Intertidal AssemblagesTropical EcologySpatial VariabilityIsland BiogeographyNested Sampling Designs

Tropical nearshore ecosystems represent global hotspots of marine biodiversity and endemism but are oftenpoorly understood and impacted by human activities. The Seychelles Archipelago (Western Indian Ocean)sustains a wealth of marine life, much of which is threatened by rapid development associated with tourismand climate change. Six marine parks exist within the Archipelago, but their biodiversity value and ecologicalhealth are poorly known, especially with regards to non-fish and coral species. Here we investigate spatialpatterns of littoral biodiversity on 6 islands, 5 of which were granitic and within marine parks, includingthe first surveys of Curieuse and Ile Cocos. Our surveys formed a nested sampling design, to facilitate an ex-amination of variability in species richness, faunal abundance, taxonomic distinctness and assemblage com-position at multiple spatial scales, from islands (>100 s km) to quadrats (metres). We identified (mostly tospecies) and enumerated two target taxa, brachyuran decapod crustaceans and gastropod molluscs, andrecorded over 8300 individuals belonging to over 150 species. Crabs and gastropods exhibited different pat-terns of spatial variability, as crab assemblages were generally more distinct between islands, while gastro-pod assemblages were markedly variable at the smallest spatial scales of ‘patch’ and ‘quadrat’. Intertidalbiodiversity was greatest on Curieuse Island and least at Desroches, the latter was being the only coralatoll we surveyed and thereby differing in its geological and ecological context. We discuss likely drivers ofthese biodiversity patterns and highlight urgently-needed research directions. Our assessment of the statusof poorly-known invertebrate assemblages across the Seychelles will complement more extensive surveysof coral and fish assemblages and, in doing so, provide a useful baseline for monitoring the effects of keystressors in the region, such as coastal development and climate change.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Tropical nearshore ecosystems represent global hotspots of ma-rine biodiversity and endemism (Roberts et al., 2002) but are current-ly threatened by rapid environmental change (Hughes et al., 2003).Increased temperature, storminess, acidification, fishing pressure,sedimentation and pollution may interact in non-linear and unpre-dictable ways to influence patterns of biodiversity and the distribu-tion of living marine resources (Hughes et al., 2003; Przeslawskiet al., 2008). Compared to corals and fish, biodiversity patterns ofmobile benthic invertebrates (e.g. gastropods, crabs, amphipods) arepoorly known, and there are few reliable long-term biodiversity data-sets that can be used to determine the magnitude and direction ofecological change (Przeslawski et al., 2008). This, in turn, makesdetecting ecological responses to human activities, such as coastal de-velopment and fishing, challenging and thus poses a problem for

of Western Australia, Crawley,; fax: +61 8 64881108.le).

rights reserved.

management and conservation. Clearly, documenting patterns of ma-rine biodiversity, and understanding the processes that drive them,are necessary to detect (and mitigate for) environmental change intropical coastal ecosystems.

Marine protected areas (e.g. no-take sanctuaries, restricted fishingzones) are widely used management tools intended to conserve liv-ing resources. The size, number, location, function, management andeffectiveness of marine protected areas have been a subject of greatdebate, although they are near universally agreed to be of overall ben-efit in conservation. There is a general scientific consensus that ma-rine national parks have a vital role in maximising the quantity andquality of many ‘ecosystem services’ (Moberg and Folke, 1999) espe-cially in regions where dependence on the coast for economy andfood is very high. The Seychelles Archipelago, central-west IndianOcean, is clearly one such region, with United Nations DevelopmentProgramme reports showing that coastal tourism and food fromExclusive Economic Zone fisheries are key drivers of its economy(see Clifton et al., 2012 for further discussion). Most of the humanpopulation, and thus pressure on resources, centres on the innergroup of granitic islands but the 16 protected areas span these to

Fig. 1. Map 1: Positions of islands sampled within the Seychelles Archipelago. S = Sil-houette, P = Praslin, C = Curieuse, co = Cocos, M=Mahe, D= Descroche. Map 2: TheSeychelles relative to East Africa and Madagascar.

9D.A. Smale et al. / Journal of Sea Research 69 (2012) 8–15

the outer Archipelago, including the world heritage site of Aldabra(Stoddart, 1984). As with many protected areas worldwide, the un-derlying reason for their size, number, location and function has notbeen clarified nor is their current management underlain by strongscience and thus their effectiveness is largely unknown.

Compared with most island states, there are many organisationsdedicated to Seychelles marine conservation. Such organisations runprojects of diverse size and structure largely to monitor the statusof birds, turtles, fish and corals. Seychelles coral reef associatedwork has shown that, to some extent, the habitats, marine protectedareas and problems are representative of the wider region and indeedthe global tropics. Seychelles coral reefs have been significantly im-pacted by outbreaks of crown-of-thorns starfish (Acanthaster planci,now recognised as several cryptic species), intense bleaching associ-ated with the El Niño Southern Oscillation events and the tsunamiof 2004 (Sheppard and Obura, 2005). In addition, non indigenous spe-cies have become established in nearshore waters, human develop-ment of the coast is considerable, erosion is predicted to increaseand climate change is projected to significantly raise surface temper-atures, ocean acidity and sea level (Sheppard et al., 2005). Loss of livecoral extent and structural complexity has been the most widelyreported result (both in the Seychelles and globally), although patchyrecoveries have also been found (Graham et al., 2007). Despite beingbeyond the generalised indo-west Pacific richness hotspot and beingsmall oceanic islands, the Seychelles support a high diversity of ma-rine invertebrates (Barnes et al., 2009; Mackie et al., 2005; Taylor,1968). More importantly for the various assessment criteria ofSeychellesmarine protected areas,many rare, edge of range and region-al endemics were found in recent baseline surveys at marine parks onthe islands of Mahe, Silhouette and Desroches (Barnes et al., 2009).

Here we evaluate the structure of marine littoral biodiversityacross six major marine parks around the archipelago. In doing sowe undertook the first littoral surveys in both Curieuse Marine Park(both on Curieuse and Praslin shores) and in Ile Cocos Marine Park.These are important both symbolically (the Ile Cocos marine park ismarketed as a tourism highlight and Curieuse is a regional base forthe Seychelles Marine Parks Authority) and because neither Cocosnor Curieuse islands have permanent habitation (other than marinepark rangers on the latter). The lack of development and human hab-itation on Curieuse and Cocos Islands should mean that data provide auseful source of comparison to shores previously surveyed with sim-ilar methodology in other Seychelles localities (Barnes et al., 2009).We used a nested sampling design to investigate biodiversity patternsat multiple spatial scales, from between quadrats to between islands,to empirically examine spatial variability in ecological pattern acrosssix islands of the Archipelago. Our primary aim was to determinehow the structure of littoral biodiversity varied across Seychellesshores at multiple spatial scales. It was not possible to empiricallylink human activities with biodiversity patterns, as reliable data onshoreline activities (e.g. tourist numbers, fishing practices, pollution,hotel developments) were not available for all islands (see Cliftonet al., 2012 for further discussion). As such, our secondary aimswere to provide a baseline of intertidal biodiversity patterns acrosssix marine parks to assist further monitoring efforts, and to initiatediscussion of the key factors that may influence such patterns.

2. Material and methods

2.1. Study area

Sampling was conducted on 6 islands within the Seychelles (Fig. 1,Table 1). Silhouette represents the largest Marine Park in theSeychelles and one of the least known in terms of its coastal ecology.Praslin is the country's second largest island, while the adjacent Cur-ieuse is a small granitic island with a similar geology and ecology(Stoddart, 1984). Study sites on both these islands were situated

within the Curieuse marine park. Ile Cocos (‘Cocos’) is the smallest is-land we sampled and is the focus of a surrounding marine park. Thecoastal ecology of Mahe, the largest and most populated island ofthe Seychelles, is relatively well known and the most impacted byhuman activity. We sampled in two marine parks on Mahe, Port Lau-nay and Baie Ternay. Marine parks in the Seychelles are declared ‘no-take’ zones; any damage, disturbance or removal of flora and fauna isstrictly prohibited and legislated under the Nature and ConservancyAct. Desroches is the most isolated study island, forming part of theAmirante Island group over 200 km southwest of the main islandgroup (Fig. 1). Although Desroches is not classified as a marine park,its remoteness and small population (~50 inhabitants) mean thatthe littoral assemblages are relatively unaffected by human activity,such as hotel construction, trampling and extraction. All the studyislands are old, granitic fragments of micro-continental crust, withthe exception of Desroches which is a low-lying coral atoll. Intertidalhabitats on these islands are predominantly sandy, although juttingrocky reefs and large expanses of exposed coral rubble are common.The Seychelles experience small (typical range 1.2–1.5 m), semi-diurnal tides and seawater temperature typically ranges from 25 to29 °C throughout the year (Spencer et al., 2000). Despite minimaltidal ranges, the structure of intertidal assemblages changes consider-ably from the upper to the lower shore, with lower shore zones sup-porting a high richness of molluscs, crustaceans and echinoderms andthe upper shore characterised by few (often highly abundant) speciesof crabs and gastropod molluscs (Barnes et al., 2009).

2.2. Sampling protocol

At each island 1 to 4 sites were selected for sampling. Sites werehundreds of metres apart and selected to comprise similar habitat,profile, exposure and substratum types. Specifically, large patches of

Table 1Island type, size, population and sampling information for each island sampled within the Seychelles Archipelago. * denotes one missing sample from the Silhouette samplingdesign.

Island Island type Approx popn Approx area Sites surveyed Samples Marine parks Date sampled

Silhouette Granitic 135 20 km2 3 44* Silhouette Aug 2007Praslin Granitic 6500 38 km2 1 15 Curieuse Dec 2010Curieuse Granitic 6 5 km2 3 45 Curieuse Aug 2009/Dec 10Cocos Granitic 0 2 km2 1 15 Ile Coco Dec 2010Mahe Granitic 80,000 155 km2 2 30 Port Launay/Baie Ternaie Aug 2006Desroches Atoll 50 3 km2 4 60 – Aug 2006

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semi-stable substrata (i.e. boulders and coral rubble) were targetedfor sampling. At each site, 3 patches of exposed low shore (at least20 m apart) were chosen at random, and 5 haphazardly placed 1 m2

quadrats (at least 3 m apart) were sampled within each patch. Inthis way, a fully nested sampling design was achieved, with quadratnested in patch, patch within site, and site within island (seeUnderwood, 1997 for further discussion on nested designs). At onesite on Silhouette Island, one patch comprised only four quadratsdue to time constraints (Table 1). Fieldwork was conducted aroundspring low tides, so that samples were collected from ~0.1 to 0.3 mabove the extreme low tide mark. Within each quadrat, all substratawere removed to a depth of ~2 cm and all (live) fauna larger than4 mm were examined. Previous surveys and preliminary analysessuggested that decapod crustaceans and gastropod molluscs werekey indicators of ecological structure, due to being the most specioseand abundant components (Barnes et al., 2009). As such, for the cur-rent study only brachyuran decapod crustaceans (hereafter ‘crabs’)and gastropod molluscs (hereafter ‘gastropods’) were identified tothe lowest taxonomic level possible (usually species, see results sec-tion) and enumerated. Individuals were photographed in situ usinghigh-resolution cameras with 1:1 macro lenses and, where necessary,specimens were collected, preserved and later sent to expert taxono-mists for species level identification. Crabs and gastropods were tar-geted because: (1) previous surveys (Barnes et al., 2009) suggestedthat they are the most rich and abundant taxa on these shores;(2) there are relatively well developed taxonomic keys/guides forthese taxa; and (3) they have important (but different) ecologicalroles in these intertidal communities. Sampling was conducted overseveral field expeditions, between 2006 and 2010 (Table 1).

2.3. Statistical analysis

Species accumulation curves were constructed for each island foreach taxon (using 999 randomisations in PRIMER 6 software), to ex-amine the effectiveness of sampling and to compare the rate of spe-cies accumulation between islands. Initially, variability in speciesrichness (SR) and total abundance (TA) for both crabs and gastropodsbetween islands and sites was examined by plotting mean values perpatch (with 5 quadrats pooled). Variability in SR and TA was formallyexamined at the different spatial scales (i.e. islands, sites, patches,quadrats) with univariate PERMANOVA, conducted with Primer 6software and PERMANOVA add-on (Anderson et al., 2007; ClarkeandWarwick, 2001a). A fully nested design was employed and all fac-tors were treated as random. A similarity matrix based on Euclideandistance of untransformed SR and TA was generated for the analyses,which used 4999 permutations under a reduced model. Althoughislands were chosen arbitrarily and treated as a random factor, itwas of interest to conduct a posteriori pairwise comparisons betweenislands where differences were significant, to identify islands of highbiodiversity value.

Variability in multivariate assemblage structure between islands,sites, patches and quadrats was also examined with PERMANOVA,for both crabs and gastropods. Species level abundance data wereanalysed with a fully nested design, again with all factors treated asrandom. Permutations were based on a Bray–Curtis similarity matrix

generated from square-root transformed data. This transformationwas chosen to down weight the influence of a few highly abundantspecies, such as the gastropod Nerita albicilla. As PERMANOVA is sen-sitive to within-factor differences in multivariate dispersions, aPERMDISP test was also performed for each factor in the model to ex-amine heterogeneity in multivariate dispersion between groups(using 4999 permutations). MDS plots based on the Bray–Curtis sim-ilarity matrix were generated to visualise multivariate patterns be-tween islands, with centroids representing average assemblagestructure for each patch. Where PERMANOVA detected significantdifferences between islands, a SIMPER analysis was conducted to de-termine which species were driving the observed between-islandvariability.

Finally, in addition to species richness and turnover (i.e. multivariateassemblage structure), the taxonomic breadth of assemblages at eachsite was assessed using average taxonomic distinctness (Av. TD) andvariation in taxonomic distinctness (Var. TD) measures (again usingPrimer 6). This is a useful approach, as the diversity of any given assem-blage is not simply the number of species represented, but also howclosely related the species are in their phylogeny. Av. TD is calculatedby summing the path lengths through a taxonomic tree connectingevery pair of species in an assemblage, and then dividing by the totalnumber of paths (Clarke andWarwick, 1998). Var. TD is simply the var-iance of the pairwise path lengths and reflects the unevenness of thetaxonomic tree (Clarke and Warwick, 2001b). While these metricshave been most frequently used to detect anthropogenic impacts,they are equally suitable for describing diversity patterns along largescale environmental gradients. Moreover, they are advantageous inthat they are independent of sampling effort, and generally do not co-vary with species richness or diversity, thereby depicting a distinctfacet of biodiversity.

3. Results

In total, 59 crab taxa (52 named species and a further 7 distinctgenera), represented by >1800 individuals, and 101 gastropod taxa(97 named species and a further 4 distinct genera), represented by>6500 individuals, were sampled. A list of species recorded in thelow shore quadrats analysed for the present study is provided as elec-tronic Supplementary material (additional species have been sur-veyed by the Coral & Coastal Ecology of the Seychelles ResearchProgramme). Due to the unbalanced sampling design between islands,direct comparisons of species richness (which is strongly influencedby sampling effort) must be made with caution. However, species ac-cumulation curves showed that, for crabs, asymptotic levels of rich-ness were only reached at Mahe (Fig. 2). Furthermore, whensampling effort was standardised at 30 quadrats per island, almosttwice as many crab species were sampled at Curieuse comparedwith Desroches and Mahe. For gastropods, asymptotic levels of rich-ness were only observed at Silhouette, while gastropod richnesswas considerably higher at Curieuse (and perhaps Cocos) comparedwith the other islands (Fig. 2).

Plots of species richness (SR) and total abundance (TA) for eachsite on each island (means of 3 patches, with each patch comprising

Fig. 2. Species accumulation curves constructed for each study island for (a) crabs and(b) gastropods. 999 randomisations of quadrat samples were conducted for each curve.Island codes are: S = Silhouette, P = Praslin, C = Curieuse, co = Cocos, M = Mahe,D = Descroche.

Fig. 3. Species richness (a) and total abundance (b) for crabs and species richness (c) and toBar represent means per patch (5 quadrats pooled); 3 patches were sampled at each site. E

11D.A. Smale et al. / Journal of Sea Research 69 (2012) 8–15

5 pooled quadrats) were constructed to examine variability betweenislands, sites and patches (Fig. 3). For crabs, SR and TA were consis-tently lower at Desroches compared with all other islands, but partic-ularly Silhouette and Curieuse. The plots also suggested that TA (andto some extent SR) was highly variable between sites and patches. Forexample, the total number of crabs sampled per patch at Curieuseranged from 37 to 200. Richness and abundance patterns for gastro-pods were notably more variable between sites and patches, althoughSR and TA were generally lower at Desroches than the other islands.Gastropod abundance was extremely variable at small spatial scalesat Praslin, where TA per patch ranged from 6 to 1010. Similarly, gas-tropod abundance was extremely variable at the scale of site at Mahe,where TA per site ranged from 73 to 2990.

PERMANOVA indicated that both crab SR and TA varied significantlyat all spatial scales examined, although variability at the largest (island)and smallest (quadrat) spatial scales contributed most to total variabil-ity (Table 2). Pairwise tests for the ‘island’ factor showed that SR and TAat Silhouette and Curieuse were significantly greater than at Desroche(SR: Silhouette vs. Desroches, t=4.55, P=0.014; Curieuse vs. Des-roches, t=5.99, P=0.021. TA: Silhouette vs. Desroches, t=3.60,P=0.003; Curieuse vs. Desroches, t=4.17, P=0.028). Conversely, gas-tropod SR did not vary between islands or sites, but was extremely var-iable between transects and quadrats, which contributed to 65% of thetotal observed variability (Table 2). Finally, gastropod TA varied signifi-cantly between islands and patches (but not sites), while greatest rela-tive variability was observed at the scale of quadrat. Pairwise islandtests showed that gastropod TA was greater at Mahe than Desroches(t=1.85, P=0.048).

MDS ordination suggested that multivariate crab assemblagestructure differed between islands, with pronounced partitioning be-tween assemblages at Desroches and those at Silhouette and Curieuse(Fig. 4, but note moderate stress values). Subsequent PERMANOVAindicated that assemblage structure varied significantly at all spatialscales examined (Table 3). Pairwise comparisons between islandgroups showed that assemblages at Silhouette were distinct fromthose at Desroches and Curieuse (Silhouette vs. Desroches: t=2.40,P=0.007; Silhouette vs. Curieuse: t=1.40, P=0.023) and that as-semblage structure at Desroches and Curieuse also differed fromone another (Desroches vs. Curieuse: t=3.00, P=0.028). SIMPER

tal abundance (d) for gastropod molluscs at each study site within each island sampled.rror bars represent standard error. Note differences in scale on y-axis between plots.

Table 2PERMANOVA results based on Euclidian distance measures for untransformed speciesrichness and total abundance data for crab and gastropod assemblages. All tests used4999 permutations under a reduced model. Estimates of (pseudo) variance compo-nents, and their relative contribution to total variance, are also shown.

Source df MS F P Var. comp. (%)

a. Crab species richnessIsland 5 102.9 5.4 0.027 1.6 (34)Site 8 19.0 5.5 0.001 1.0 (21)Patch 28 3.4 1.6 0.033 0.5 (10)Residual 167 2.1 1.5 (33)

b. Crab abundanceIsland 5 1088.2 4.1 0.036 4.9 (25)Site 8 264.4 2.1 0.046 3.0 (16)Patch 28 127.7 2.1 0.004 3.7 (19)Residual 167 59.9 7.7 (40)

c. Gastropod species richnessIsland 5 120.7 2.5 0.123 0.6 (19)Site 8 77.5 1.8 0.116 0.5 (16)Patch 28 148.7 2.8 0.001 0.8 (24)Residual 167 310.3 1.3 (41)

d. Gastropod abundanceIsland 5 183,170 11.6 0.027 71.0 (21)Site 8 15,742 0.2 0.952 0.0 (0)Patch 28 69,119 2.2 0.005 86.3(26)Residual 179.2 (53)

Table 3PERMANOVA results based on Bray–Curtis similarity matrices constructed fromsquare-root transformed abundance data for crab and gastropod assemblages. Alltests used 4999 permutations under a reduced model. Estimates of (pseudo) variancecomponents, and their relative contribution to total variance, are also shown.

Source df MS F P Var. comp. (%)

a. Crab assemblage structureIsland 5 27,028 2.6 0.002 22.4 (23)Site 8 10,306 3.4 0.001 22.1 (22)Patch 28 3052 2.5 0.001 19.3 (20)Residual 167 1204 34.7 (35)

b. Gastropod assemblage structureIsland 5 15,714 1.5 0.143 12.7 (14)Site 8 10,475 3.0 0.001 21.7 (24)Patch 28 3437 2.4 0.001 20.1 (22)Residual 167 1432 37.8 (41)

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analysis indicated which species were primary contributors to the ob-served differences between these islands. Desroches was depauperatein crabs, so that differences between the other islands were

Fig. 4. MDS ordinations of (a) crab and (b) gastropod assemblages based on Bray–Curtissimilarity matrices constructed from square-root transformed abundance data. Centroidsrepresent averages for ‘patch’ (n=5 quadrat samples), while symbols show islandgroupings.

consistently driven by lower abundances of dominant crabs, such asActaeodes tomentosus and Pachygrapsus minutus (Table 4). Further-more, very few hermit crabs were sampled at Desroches, whereashermit crabs (e.g. Calcinus latens, Calcinus laevimanus and Calcinusmorgani) were common at Curieuse, therefore driving differences inoverall assemblage structure between the islands (Table 4). Differ-ences between Silhouette and Curieuse were largely driven by theabundances of A. tomentosus (being greater at Curieuse) and P. minutus(being greater at Silhouette).

In contrast to the crabs, MDS ordination of gastropod assemblagesindicated minimal partitioning between islands, and suggested thatbetween-site variability at Mahe was particularly pronounced (Fig. 4,but note moderate stress values). This was supported by PERMANOVA,as significant differences in gastropod assemblage structure were ob-served between sites and patches, but not islands (Table 3). PERMDISPwas conducted for both crab and gastropod assemblages to examinevariability inmultivariate dispersionwithin island groups, but no differ-ences in multivariate dispersion were observed (crabs: F5,36=1.28,P=0.60; gastropods: F5,36=2.51, P=0.26).

Taxonomic distinctness values, both Av. TD and Var. TD, are super-imposed on funnel plots in Fig. 5. In this case, funnels represent 95%probability estimates for Av. TD and Var. TD from 1000 independent

Table 4Percentage contributions of individual species to observed differences in crab assem-blages between islands as determined by SIMPER analysis. Only the top 5 contributorsto dissimilarities are shown. Average dissimilarities between islands are parenthesised.‘Mean Ab.’ relate to each island (in order) in the comparison, ‘Diss/SD’ is average dis-similarity divided by standard deviation, ‘Contr.%’ refers to the contribution of eachspecies to differences between islands, and ‘Cum.%’ is a running total of the contribu-tion to the observed dissimilarity.

Mean Ab.1 Mean Ab. 2 Diss/SD Contri.% Cum.%

Silhouette and Desroches (88%)Pachygrapsus minutus 1.09 0.34 1.08 15.20 15.20Actaeodes tomentosus 1.02 0.30 1.18 13.02 28.22Menaethius monoceros 0.88 0.00 0.82 11.86 40.09Petrolisthes ornatus 0.70 0.00 0.82 8.61 48.70Diogenes sp. 1 0.22 0.41 0.69 7.17 55.86

Silhouette and Curieuse (81%)Actaeodes tomentosus 1.02 1.35 1.19 9.77 9.77Pachygrapsus minutus 1.09 0.13 1.16 9.60 19.37Menaethius monoceros 0.88 0.34 0.98 7.75 27.12Calcinus latens 0.29 0.88 1.01 7.75 34.87Calcinus laevimanus 0.20 0.59 0.81 5.82 40.69

Desroches and Curieuse (94%)Actaeodes tormentosus 0.30 1.35 1.24 12.32 12.32Calcinus latens 0.00 0.88 0.94 10.30 22.62Thalamita sp. 1 0.03 0.83 0.77 8.65 31.26Calcinus laevimanus 0.00 0.59 0.58 7.88 39.14Calcinus morgani 0.00 0.71 0.81 6.51 45.65

Fig. 5. Average taxonomic distinctness (a) and variation in taxonomic distinctness (b) for crabs, and average taxonomic distinctness (c) and variation in taxonomic distinctness (d)for gastropod assemblages for each site within each island. Funnels represent 95% probability for both indices, estimated from 1000 simulations drawn randomly from the completespecies lists for crabs and gastropods.

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simulations, drawn randomly from the master taxonomy list of 67(crabs) and 134 (gastropods) species. For crabs, the plots showedthat Av. TD for one site at Desroches fell below the 95% confidencelimit, while Var. TD was generally high at all Curieuse sites and oneof the Mahe sites (Fig. 5). For gastropods, Av. TD was very variablebetween sites within islands, as one site for each of Silhouette,Desroches, Curieuse and Cocos fell below the 95% confidence limit.Var. TD, however, was notably high at two sites on Silhouette (Fig. 5).

4. Discussion

The islands and marine parks of the Seychelles support a rich andabundant intertidal fauna. The abundance and richness of marine in-vertebrates varied greatly across the marine parks and islands of theSeychelles Archipelago, as did the presence of species of perceivedhigher conservation value (e.g. those that are rare, endemic or edgeof range etc.). Spatial patterns of biodiversity varied considerably be-tween our two chosen taxonomic groups, crabs and gastropods. Forcrabs, we observed significant differences in species richness, totalabundance and multivariate assemblage structure (i.e. species turn-over) at all spatial scales within the nested model (islands, sites andpatches), while the largest spatial scale, ‘island’, and the smallest,‘quadrat’, consistently contributed most to total observed variability.This pattern was somewhat predictable, as islands were separatedby up to 200 km and differed in size and geological history, andemerged as the strongest scale of variance in our previous more re-stricted study (albeit using a different model for analysis, see Barneset al., 2009). Pronounced variability in richness and assemblage struc-ture at small spatial scales is a common pattern for a range of marinebenthic communities (Fraschetti et al., 2005; Smale et al., 2010;Underwood and Chapman, 1996), although this did not emergestrongly in previous analyses of Seychelles littoral data (Barnes etal., 2009).

Crab assemblages at Desroches were lower in richness and abun-dance, and different in structure, to those at Curieuse and Silhouette.Factors such as the relatively higher isolation and disturbance fromwave exposure, coupled with the island being a young atoll, werelikely to make assemblages at Desroches appear as outliers in ourdata. The remaining study locations were all old, granitic islands butdiffered in factors such as exposure, profile, substratum geology (i.e.granitic fragments vs. coral rubble) and relative degrees of anthropo-genic impact. The continental shelves between the granitic islands arecontiguous and the islands are thought to be well connected by equa-torial currents (Visram et al., 2010), so that isolation and evolutionaryhistory is unlikely to be important in explaining inter-island differ-ences. Hermit crabs were major contributors to the observed differ-ences in assemblage structure between islands, as many morehermit crab species and individuals were sampled at Curieuse thaneither Desroches or Silhouette. It is known that Hermit crab assem-blage structure varies across tropical shores in response to a wide va-riety of environmental variables and anthropogenic pressures(Barnes, 2001). Direct human presence (locals or tourists visits) atCurieuse was lower than at all other islands during the study period,but elsewhere increased human presence has been linked only withchanges in hermit crab behaviour and not richness and abundance(Barnes, 2001). Thus, the reasons underlying variability in hermitcrab richness and abundance remain obscure but may be as simpleas variability in human activity or habitat availability. More generally,variability in species richness, total abundance and assemblage struc-ture at small spatial scales was most likely driven by variation in mi-crohabitat structure (i.e. complexity and abundance of coral rubble orboulders), which has well-known implications for predation pres-sure, desiccation rates, and the availability of space and food(Meager et al., 2011; Raffaelli and Hawkins, 1999).

In contrast, gastropod species richness and assemblage structuredid not vary significantly between islands, but varied considerablyat the smaller spatial scales of patch and quadrat — contrasting with

14 D.A. Smale et al. / Journal of Sea Research 69 (2012) 8–15

previous findings involving fewer islands (Barnes et al., 2009). Mobil-ity does not explain why gastropod assemblages should be more ho-mogenous and cosmopolitan between islands as crabs are generallymuch more mobile (than gastropods) as adults and similarly mobileas larvae. It is clear that micro-structure massively influences abun-dance; presence of a semi-porous boulder in a quadrat could increasethe number of gastropods by an order of magnitude (authors' person-al observations). Nerita species (e.g. N. albicilla) often formed denseaggregations in some quadrats and remained absent in others, seem-ingly linked to the availability of crevices in boulders or interstitialspace in the coral rubble matrix. Indeed, the relative importance ofvariability in species richness, abundance and structure at the scaleof patch and quadrat was consistently greater than variabilityrecorded at the spatial scale of island, highlighting the importanceof processes acting at small spatial scales in determining biodiversitypatterns. Studies of the structure of gastropod-dominated assem-blages in sea-grass habitats have indicated that at small spatial scalesrandom structuring predominated, becoming non-random (deter-ministic) at scales of 50 m or larger (Barnes and Ellwood, 2011). Ingeneral, it might be expected that deterministic controls will selectthe local pool of species capable of successfully colonising the avail-able habitats, while stochastic effects are more likely to operate inthe actual colonisation, as well as on a wide range of in situ biologicalinteractions including predation. Human harvesting of littoral assem-blages is widespread in the Indian Ocean but simple trampling of‘take nothing but pictures and leave nothing but footprints’ touristshas long been known to have detectable impact (Beauchamp andGowing, 1982). Even low levels of human trampling in marine re-serves have been found to significantly influence rocky shore assem-blage structure and abundance levels (Casu et al., 2006; Pinn andRodgers, 2005) and we suggest testing this as a key hypothesis shouldbe a priority in Seychelles marine parks.

We also assessed littoral diversity patterns with two taxonomicdistinctness metrics, av. TD and var. TD. Distinctness measures aremost commonly applied to environmental impact studies, as ecologi-cal theory predicts that av. TD will decrease and var. TD will increasealong a disturbance gradient (Clarke and Warwick, 1998, 2001b).However, where anthropogenic impacts or pollution stress is relative-ly low, these metrics may be influenced by ecological artefacts, suchas habitat heterogeneity/availability (e.g. Smale et al., 2011). In thiscase, we observed no consistent signal of local disturbance at any is-land, but recorded considerable variability in av. TD and var. TD be-tween sites, which may suggest that very localised processes, suchas hotel development, have influenced species composition. Thiswas most evident for gastropods at Silhouette, where low av. TDand high var. TD values at some sites suggested that species wereclosely related and that certain taxa were over-represented. For ex-ample, our Silhouette study site with the greatest var. TD value (‘LaPasse’) was adjacent to the construction site of a large hotel complex.As construction had commenced immediately prior to sampling a tax-onomically impoverished gastropod assemblage could be an indicatorof low-level disturbance, such as increased sediment loading. TheSeychelles government aims to double annual tourist arrivals to360,000 by 2012 and, as such, new hotels are being built on theshores of many islands and significant construction work is scheduledto occur at many others. Coastal development clearly increases short-term sediment loading and mechanical destruction, which can havedetrimental effects on nearshore biodiversity. For example, increasedcoral mortality associated with sedimentation may occur up to 3 kmfrom hotel construction sites (Clifton et al., 2012). The longer-termissue, however, is likely to be increased visitor numbers (thus tram-pling and pollution) to shore sites. Understanding the effects oflocal disturbances on biodiversity and developing indicators to cost-effectively monitor ecological impacts, should be a priority. However,we note that while some of the techniques we have used are effectiveat visualising and analysing community structure (e.g. TD) they are

not always the most sensitive or reliable at detecting human impactson rocky shores (Costa et al., 2010).

Two important limitations to the current study that should be con-sidered when interpreting the data outputs are evident. The first relatesto the inconsistency in the number of sites sampled at each island,which was a consequence of time constraints, safety of access or (inthe case of Ile Cocos) the island's small size negating multiple sites.While permutational methods can deal with unbalanced designs(Anderson, 2001; Anderson et al., 2007) there was considerably morepower to detect differences between islands with multiple sites thanthose with just one, and also less degrees of freedom available at the‘site’ level within the nested design. As such, if assemblages on Praslinor Ile Cocos were distinct, there was less statistical power to detectthis dissimilarity (although the plots suggested that, apart from a highabundance of gastropods at Praslin, biodiversity patterns on theseislands were not divergent). Even so, the unbalanced nested design fa-cilitated a useful test of variability atmultiple spatial scales and elucidat-ed key biodiversity patterns. The second caveat relates to possibletemporal variability in biodiversity patterns that confounded our spatialcomparisons. Due to logistical constraints, islands were not surveyed inthe samemonth or year, which leads to the possibility that observed dif-ferences between islands were an artefact of short-term variability inassemblage structure caused by seasonal or annual environmental var-iability. While this was unavoidable, analysis of multiple years/seasonsof sampling of fish, coral and intertidal invertebrates at Curieuse has in-dicated that short-term temporal variability isminimal when comparedwith spatial variability across islands and sites (authors' unpublisheddata).Moreover, as nomajor, regional-scale physical disturbance events(e.g. ENSO events, tsunamis, anomalous storms) occurred during thesurvey period, ecological structure was unlikely to have been ‘reset’during this time. Even so, biodiversity patterns on these islands arestill poorly understood, and long-term monitoring of intertidal assem-blages will provide useful information on temporal variability in, andenvironmental drivers of, patterns of coastal biodiversity.

A key outcome of this study has been the collection of quantitative,high-resolution baseline data on littoral assemblages across theSeychelles, which can be used to assessmanagement actions and detectfuture change in ecosystem health, driven by (for example) climate orcoastal development for tourism. Overall, littoral biodiversity (in vari-ous forms) on the island of Curieuse was notably high, with a numberof rare species and some being the only record from the Seychelles.For example, surveys on Curieuse have sampled the crab Meractaeabrucei, which represents the only record of the species anywheresince its original description in Kenya, and the holothuroid Stichopuscf rubermaculosus otherwise only known from Malaysia (Y. Samyn,pers. comm). Curieuse Island, with an in situ marine parks ranger sta-tion and no other permanent human settlement, has unusually strongpotential to monitor and police a national park in a region of high andincreasing anthropogenic pressure. Measurement of visitor numbersand trampling effects to construct management plans to protect theseshores from disturbance and development should be a priority if localand regional biodiversity is to be conserved. Ile Cocos, which is alsouninhabited and represents a major tourist attraction, supported a dis-tinct and diverse gastropod assemblage but a fairly typical crab assem-blage. Of the islands previously surveyed, only crab assemblages atSilhouette Island were comparable in diversity and distinctness to Cur-ieuse, while gastropod assemblages were, to some extent, taxonomical-ly impoverished — perhaps as a result of localised disturbance fromnearby hotel construction. Finally, Desroches, which differs from theother islands in terms of its geology, evolutionary context and habitatstructure, supported relatively depaurate, but distinct, littoral assem-blages. Our assessment of the status of poorly-known invertebrate as-semblages across the Seychelles will complement more extensivesurveys of coral and fish assemblages and, in doing so, provide a usefulbaseline for monitoring the effects of key threats in the region, such asclimate change and coastal development.

15D.A. Smale et al. / Journal of Sea Research 69 (2012) 8–15

Supplementary materials related to this article can be found on-line at doi:10.1016/j.seares.2012.01.002.

Acknowledgements

We thank theMitsubishi Corporation and to the Earthwatch Institute(Europe) forfinancial and, in the case of Earthwatch, administrative sup-port. We thank the Seychelles Islands Development Company, NatureProtection Trust of Seychelles and especially the Seychelles NationalParks Authority for logistical support.We are grateful to EduardHeiman,Manuel Malaquias, David Reid, Bill Rudman and John Taylor for aid inidentification of molluscs, to Paul Clark, Peter Davie and Peter Ng foraid in identifying crabs, and Peter Hogarth for examining unfamiliar her-mit crabs and Yves Samyn for identifying Stichopus cf rubermaculosus. Fi-nally we thank the African Capacity Building Fellows of 2009 and 2010for help in the field data collection.

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