Multi-scale spatial variability in intertidal benthic assemblages: Differences between sand-free and sand-covered rocky habitats

1 This is an Accepted Manuscript of an article published by Elsevier in Estuarine, 1 Coastal and Shelf Sciencie on 23th August 2013, available at: 2 https://doi.org/10.1016/j.ecss.2013.08.019 3 4 2 Multi-scale spatial variability in intertidal benthic assemblages: differences between 5 sand-free and sand-covered rocky habitats 6 7 Pilar Díaz-Tapiaa, *, Ignacio Bárbaraa, Isabel Díezb 8 9 aBioCost Research Group, Universidade da Coruña, Facultade de Ciencias, Campus da 10 Zapateira s/n. 15071 A Coruña. Spain. 11 bDepartment of Plant Biology and Ecology, University of the Basque Country 12 UPV/EHU, PO Box 644, 48080 Bilbao, Spain. 13 14 15 *Corresponding author: 16 E-mail address: [email protected] (P. Díaz-Tapia) 17 Phone: 0034 981167000 2236 18 19 20 21 22 3 Abstract 23 The presence of high loads of sediment is often thought to be negatively 24 associated with sessile species living on rocky reefs, leading to assemblages with low 25 alpha diversity (average species richness) and beta diversity (heterogeneity). Here we 26 examine the effects of sand deposition on rocky assemblages by contrasting the 27 multivariate composition, spatial variation and alpha diversity between sand-free 28 assemblages and assemblages covered by sand. As expected, assemblage composition 29 differed markedly between sand-covered and sand-free reefs, supporting the idea of that 30 sedimentation is one of the major physical factors influencing the structure of benthic 31 assemblages. More surprisingly, our findings suggest that sand-covered assemblages 32 have greater spatial variation in terms of multivariate dispersion at small spatial scales 33 (from metres to 100s of metres) than sand-free assemblages. No differences were 34 detected between the two habitats in average species richness and Shannon diversity, 35 whereas sand-covered assemblages were found to be taxonomically more diverse. Thus, 36 the effects of sedimentation on the diversity of assemblages from rocky shores remain 37 unclear and further investigation is needed to clarify its structuring role in combination 38 with other environmental factors. 39 40 Keywords: Biodiversity, sediments, spatial variations, intertidal environment, 41 assemblage structure, rocky shores. 42 43 4 1. Introduction 44 The successful management and protection of biological diversity, the assessment 45 of anthropogenic impacts and the restoration of altered ecosystems rely largely on 46 understanding the processes and factors that structure assemblages (Chapman, 1999; 47 Anderson et al., 2005; Terlizzi et al., 2007). Causal relationships between influential 48 factors, ecological processes and subsequent distribution of species need to be explored 49 by means of experimental research (Underwood et al., 2000), but quantifying the range 50 of natural variation of assemblages may help to identify which physical and biological 51 factors are most relevant to be explored first under an experimental approach 52 (Underwood and Chapman, 1996; Menconi et al., 1999; Coleman, 2002). Thus, research 53 efforts have been intensified in the last twenty years to provide a more in-depth 54 knowledge of assemblage heterogeneity for a broad variety of habitats (Benedetti-55 Cecchi, 2001; Pérez-Ruzafa et al., 2007; Smale el al., 2010). In particular, marine 56 benthic assemblages have been found to be highly variable across different scales of 57 time and space (Coleman, 2002; Fraschetti et al., 2005). 58 With regard to intertidal systems, ecologists have devoted special attention to 59 examining patterns of variation along the vertical gradient imposed by tidal cycles. The 60 role of biotic interactions and physical factors in structuring intertidal assemblages 61 along this gradient of stress has long been studied (Dayton, 1971; Schonbeck and 62 Norton, 1980; Moreno and Jaramillo, 1983; McCook and Chapman, 1993; Jenkins et 63 al., 1999). By contrast, along-shore variation has received far less attention despite the 64 fact that it might be greater than vertical variation, depending on the spatial scale 65 (Benedetti-Cecchi, 2001; Valdivia et al., 2011). In recent years, studies on horizontal 66 heterogeneity have quantified variability across multiple scales of space, shedding light 67 5 on the processes that regulate species distribution from fine (patchiness) to broad spatial 68 scales (Menconi et al., 1999; Johnson et al., 2001; Coleman, 2003; Denny et al., 2004). 69 The physical factors traditionally explored as sources of variation in intertidal 70 assemblages include seawater temperature, salinity, wave exposure and intertidal height 71 (Stephenson and Stephenson, 1949; Underwood, 1978; Druehl and Green, 1982; 72 McQuaid and Branch, 1984; Josselyn and West, 1985). However, despite the large role 73 that sedimentation plays in modifying coastal environments, its potential influence on 74 the structure of rocky assemblages has been rarely studied until recently ( but see Daly 75 and Mathieson, 1977; Littler et al., 1983; Airoldi et al., 1995). In recent years there have 76 been some studies focused on the effects of the increase of anthropogenic sediment 77 loads in rocky coastal assemblages (Airoldi, 2003 and references therein), which has 78 been reported as a major threat to marine biodiversity on a global scale (United Nations 79 Environment Programme, 1995). By contrast, the role of natural sedimentation in the 80 structure of benthic assemblages has received little attention (but see e.g. Daly and 81 Mathieson, 1977; Taylor and Littler, 1982; Litter et al., 1983; Airoldi and Hawkins, 82 2007; Anderson et al., 2008b). The two approaches to the study of sedimentation in 83 regard to benthic assemblages agree in that sedimentation affects the composition and 84 distribution of rocky coast organisms, but they present contrasting views regarding its 85 effects on diversity. The prevalent opinion is that high sediment loads related to 86 anthropogenic activities are detrimental to the overall diversity of rocky coast organisms 87 (Airoldi, 2003 and references therein), but some authors support the hypothesis that the 88 natural presence of sediments promotes species diversity (Littler et al., 1983; McQuaid 89 and Dower, 1990). However, a multiple-scale approach comparing the relevant spatial-90 scales of variation in diversity between sand-covered and sand-free rocky assemblages 91 6 has never been attempted. Indeed, the issue of scale has rarely been addressed in 92 research into the impacts of sedimentation on rocky coast assemblages (Airoldi, 2003). 93 Descriptive studies of rocky intertidal assemblages from the Atlantic coast of the 94 Iberian Peninsula have pointed out differences in composition between sand-free and 95 sand-covered rocky assemblages (e.g. Miranda, 1931; Ardré, 1970; Pérez-Cirera, 1976; 96 Pérez-Cirera and Maldonado, 1982; Bárbara, 1994; Bárbara et al., 1995; Díaz-Tapia and 97 Bárbara, 2005). However, quantitative data on spatial patterns of distribution of 98 organisms are scarce (Boaventura et al., 2002; Cremades et al., 2004; Araújo et al., 99 2005; Díez et al., 2009). In addition, all these studies are focused on sand-free rocky 100 habitats, while there are no previous quantitative studies of sand-covered assemblages, 101 even though they are commonly distributed along the Atlantic coastline of the Iberian 102 Peninsula (see Díaz Tapia et al., 2011). 103 The aim of this study is to test for differences in spatial patterns of variability in 104 multivariate structure and diversity between sand-free and sand-covered rocky 105 assemblages. We use a hierarchical design to quantify the magnitude of variation 106 attributable to each of several spatial scales at each of the two habitats. The use of 107 nested hierarchical sampling designs to examine both univariate and multivariate 108 response variables at multiple spatial scales has led to a greater appreciation of the 109 importance of scale in ecology (Fraschetti et al., 2005; Underwood and Chapman, 110 1996). These designs provide unbiased, independent, rigorous quantitative measures of 111 variability at predetermined spatial scales with a view to testing structured hypothesis 112 (Underwood and Chapman, 1996; Terlizzi et al., 2007). Specifically, we address 3 main 113 questions: (1) do sand-free and sand-covered rocky assemblages differ in terms of 114 multivariate structure and alpha diversity (species richness, Shannon and Taxonomic 115 Distinctness measures)?; (2) are patterns of variability in assemblage structure and 116 7 diversity dependent on spatial scale?; (3) are sand-free rocky assemblages spatially 117 more heterogeneous than sand-covered assemblages? 118 119 2. Methods 120 2.1. Study area 121 The study area extends for approximately 100 km along the northern Galician 122 coast in northwestern Spain (43º33’ N to 43º47’ N and 006º56’ W to 007º48’ W; Fig. 123 1). This is an open coast exposed to a large fetch where swell comes mainly from NW 124 (38 %) and WNW (29 %), with mean significant heights (Hs) of 3 and 2.5 m, 125 respectively (Puertos del Estado, 2013). It consists mostly of rocky substrate interrupted 126 irregularly by the presence of rias and beaches. Tides are semidiurnal with a spring tidal 127 range of up to 3.8 m, and the sea surface temperature ranges from 11 ºC to 18 ºC 128 (Bárbara et al., 2005). The flora falls within warm-temperate NE Atlantic subregion 1 129 (WNE1) according to the phytogeographical scheme proposed by Hoek and Breeman 130 (1990). 131 132 2.2. Collection of data and sampling design 133 Sampling was conducted from July to August 2010. Two different habitats at the 134 low intertidal level (between 0.4 m and 1.2 m above MLWL) were selected for this 135 study: sand-free and sand-covered rocky platforms. The former consists of rocky shores 136 located at least 100 m apart from sandy beaches. The latter are rock outcrops on sandy 137 beaches constantly covered by a sand layer (> 1 cm thick) which is trapped within algal 138 turfs. Sampling locations were randomly selected along a stretch of coastline about 100 139 km long, from a set of locations with comparable environmental conditions: N-NE-140 facing pristine open coastal shores exposed to strong wave action, with stable substrates 141 8 (continuous bedrock and large blocks), smooth surfaces and slight to moderate slope 142 (0º–45º). Data were collected following a full nested hierarchical sampling design 143 taking into account four spatial scales: Location (four coastal stretches about 1 km long 144 at least 10 km apart for each habitat) (Fig. 1), Site (three stretches 100 m long at least 145 100 m apart), Patch (three stretches 10 m long at least 10 m apart), and Quadrat (three 146 20 × 20 cm quadrats at least 1 m apart). The percentage cover of seaweeds and sessile 147 invertebrate exceeding 0.5 cm in length was visually estimated in each quadrat as 148 described by Dethier et al. (1993). Representative specimens of those taxa that could not 149 be identified in situ were collected for identification at the laboratory and deposited in 150 the SANT-Algae herbarium (University of Santiago de Compostela). 151 152 2.3. Statistical analyses 153 Differences in the multivariate structure of assemblages between the two habitats 154 studied were assessed with permutational multivariate analysis of variance 155 (PERMANOVA) using the PRIMER V. 6. PERMANOVA package (Clarke and 156 Gorley, 2006; Anderson et al., 2008a). The factors considered were: Habitat (fixed, 2 157 levels), Location (random, 4 levels, nested in habitat), Site (random, 3 levels, nested in 158 locations), and Patch (random, 3 levels, nested in sites) with n = 3. The resemblance 159 matrices comparing pairs of samples were calculated using the Bray-Curtis index on 160 square-root transformed data and the Jaccard coefficient on presence/absence data. The 161 tests used 9999 permutations under a reduced model, and significance was accepted at p 162 < 0.05. Given that there were too few possible permutations (< 100) to obtain a 163 meaningful p-value for the contrast between the two habitats, a p-value was calculated 164 using 9999 Monte Carlo random draws from the appropriate asymptotic permutation 165 distribution (Anderson and Robinson, 2003). Data were represented graphically using 166 9 non-metric multidimensional scaling (nMDS) plots. The contributions of individual taxa 167 to dissimilarities between the two habitats were determined using similarity percentage 168 analysis (SIMPER). The relative contributions of taxa were assessed using k-dominance 169 curves (Clarke and Warwick, 2001). 170 Hierarchical PERMANOVA analyses were performed on the basis of Jaccard and 171 Bray-Curtis (square root transformed data) measures for each habitat separately to 172 examine differences in spatial variability at the four spatial scales considered. Variance 173 components were estimated for each source of variation in PERMANOVA by setting 174 mean squares equal to their expectations. Occasionally, negative estimates were 175 obtained from the analysis. In these cases, negative values were set to zero, the term 176 was removed from the model and the data were re-analysed (Fletcher and Underwood, 177 2002). 178 Differences in the spatial heterogeneity of the multivariate structure of 179 assemblages between habitats were examined by applying the permutational test for 180 homogeneity of multivariate dispersions (PERMDISP) (Anderson, 2006). The analysis 181 calculates an F-statistic to compare the average distance from the observation units to 182 their group centroid in the multivariate space defined, in this case, by Bray-Curtis and 183 Jaccard indices. The p-values were obtained by 9999 random permutations of least-184 square residuals. 185 The number of species (SR) and Shannon–Wiener index (H’ using loge) were 186 calculated for each quadrat using the DIVERSE routine of the PRIMER statistical 187 package. In addition, average taxonomic distinctness (Δ*) was calculated on cover data. 188 According to Warwick and Clarke (1995) this is defined as Δ* = [∑∑i<j ω ij xi xj] / [∑∑i<j 189 xi xj] where ω ij is the taxonomic distance between species i and j and x denotes the 190 abundance of species in the sample. The measure is independent of species richness or 191 16 et al., 1995). However, our results show that both sand-free and sand-covered rocky 341 assemblages exhibit similar species richness and tend to be dominated by a few species. 342 Interestingly, we find that the average taxonomic distinctness (Δ*) is significantly 343 higher in the sediment-influenced habitat. Taxonomic distinctness may be influenced by 344 natural disturbance (Bevilacqua et al., 2009) and habitat features (Bevilacqua et al., 345 2011; Sandulli et al., 2011). Previous studies have suggested that high taxonomic 346 diversity might be expected under low environmental stress since such conditions are 347 conducive to the establishment of macrophyte species with different biological 348 requirements (Mouillot et al., 2005). 349 Another relevant result of our study is that most of the response variables 350 examined vary considerably at all spatial scales. This emphasises the complex nature of 351 these assemblages and the importance of adopting multi-scale designs in ecological 352 studies (Benedetti-Cecchi, 2001; Coleman, 2002; Terlizzi et al., 2007; Chapman et al., 353 2010). Heterogeneity at a small spatial scale (patchiness) is considered to be a general 354 property of benthic assemblages in marine coastal habitats (Fraschetti et al., 2005; 355 Anderson et al., 2005; Terlizzi et al., 2007; Chapman et al., 2010; Smale et al., 2011). 356 Regarding our results, the multivariate structure of assemblages in terms of the relative 357 abundance of species was found to be highly variable at the scale of metres in both 358 habitats. However, the multivariate composition of sand-covered assemblages shows 359 most variability at the scale of site (100s m). Likewise, in relation to species richness 360 and diversity, sand-covered assemblages show the largest component of variation 361 between sites, whereas location (km) is the major contributor to overall variability in 362 sand-free rocky assemblages. Therefore, it is not possible to postulate a general pattern 363 regarding spatial variability in the assemblages studied. Similar trends emerge from 364 previous studied, which have found that different spatial scales explain the variability of 365 17 different community characteristics (Lindegarth et al., 1995; Archambault and Bourget, 366 1996). 367 Our results suggest that the processes that determine the spatial variability in the 368 two habitats studied operate at different spatial scales. Although this study was not 369 specifically designed to investigate the causes of the spatial scales of variability 370 detected, some hypotheses may explain the high contribution to the overall variability 371 observed at the scale of 100s of meters in sand-covered assemblages and kilometres in 372 sand-free rocky assemblages. Sediments surrounding sand-covered assemblages are in 373 continuous movement in line with the energy input provided by waves, currents, and 374 tides (Daly and Mathieson, 1977). The direction and intensity of these factors change 375 over time, resulting in sediment deposition fluctuations that may promote differential 376 burial periods of assemblages at the scale of 100s of meters. The strong effect of 377 burying on the structure of assemblages has been reported in several papers (Daly and 378 Mathieson, 1977; Littler et al., 1983; Anderson et al., 2008b), but its role in generating 379 spatial patterns of variability at different spatial scales remains unstudied. In the case of 380 sand-free rocky assemblages that are highly variable at the scale of location (kilometres 381 apart), differences in substrate topography and wave exposure may explain the patterns 382 observed (Archambault and Bourget, 1996; Denny et al., 2004; Tuya and Haroun, 383 2006). Alternatively, differences in spatial variability between habitats could also be 384 explained by the life history characteristics and dispersal potential of the dominant 385 species. The calcareous red alga Corallina elongata mostly colonises the substrate by 386 recruitment from spores (Benedetti-Cecchi and Cinelli, 1994) while filamentous turf-387 forming algae have been suggested to benefit from stoloniferous growth of creeping 388 axes under sand burial conditions (Airoldi et al., 1995; Mei and Schiel, 2007). Studies 389 of intertidal molluscs with different life histories have shown that the abundance of 390 18 species with direct development have a higher variability at scales of 100s of meters, 391 while species with larval dispersal vary at scales of kilometres (Johnson et al., 2001). 392 Analogously, it could be hypothesised that assemblages dominated by algal species that 393 reproduce via spores or propagules may have larger spatial scales of variability than 394 those that do so by vegetative growth. However, it is necessary worth noting that the 395 spores of seaweeds are often characterized by their short viability and dispersion, while 396 detached parts of plants increase their dispersal capacity (Santelices, 1990). 397 Our findings also suggest that spatial variation, in terms of homogeneity of 398 multivariate dispersion, is greater in sand-covered assemblages than in sand-free rocky 399 assemblages at small spatial scales (quadrat, patch, site). Differences in the disturbance 400 regime between the two habitats may possibly explain the mechanisms underlying these 401 differences in beta diversity. Local disturbance has long been shown to be a major 402 driver of spatial heterogeneity in intertidal assemblages (Sousa, 1979, 1984; Gouhier 403 and Guichard, 2007). Therefore, it seems plausible to hypothesise that sand 404 displacements may create a disturbance regime that is spatially more variable than that 405 imposed by factors operating on sand-free rocky assemblages. In this sense, some 406 papers on sediment-influenced habitats have highlighted that the presence of sediments 407 promotes spatial heterogeneity on rocky coasts (Littler et al., 1983; McQuaid and 408 Dower, 1990). Conversely, other papers support the argument that sedimentation 409 reduces the heterogeneity of assemblages (Balata et al., 2007a). These two contrasting 410 views of the effects of sedimentation on assemblage heterogeneity may stem from 411 differences in the sedimentation regime and its interactions with other environmental 412 variables and biological factors (Airoldi, 2003). Thus, the studies that support the 413 detrimental effect of sedimentation on spatial heterogeneity have been carried out in 414 subtidal habitats and have focused on the impact of human related sediments on rocky 415 19 assemblages (Balata et al., 2007a). By contrast, the studies that find that spatial 416 heterogeneity is increased by the presence of sediments have been carried out in the 417 intertidal zone of rocky shores naturally impacted by sediments (Littler et al., 1983; 418 McQuaid and Dower, 1990). Therefore, the higher energy conditions of intertidal areas 419 may result in an increased regime of perturbations and in a more dynamic landscape 420 than that which is found in subtidal areas. 421 In conclusion, assemblages living on sand-free and sand-covered rocky platforms 422 differ substantially in terms of structure and spatial variability, supporting the idea that 423 sedimentation is one of the major physical factors influencing the structure of benthic 424 assemblages. By contrast with previous studies that have investigated the effects of 425 enhanced loads of sediments on assemblage diversity (Balata et al., 2007a, b), our 426 results show that SR and H’ are similar in both habitats, while taxonomic diversity and 427 spatial variation are higher in the habitat influenced by sand. Thus, although there are 428 numerous papers which agree that sedimentation promotes changes in benthic 429 assemblage structure, its effects on diversity remain unclear. However, it is essential to 430 clarify this issue in a global scenario in which turf-forming algae are replacing canopy 431 species supposedly by anthropically enhanced sediment loads (Airoldi, 2003; Gorgula 432 and Connell, 2004). 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The 581 effects of dispersal mode on the spatial distribution patterns of intertidal molluscs. 582 Journal of Animal Ecology 70, 641-649. 583 32 Fig. 6. Spatial distribution of percentage cover (mean + SE) of five taxa identified 726 as important in differentiating sand-covered rocky assemblages at the scale of site (n = 727 9) and patch (n = 3). Numbers indicate the sand-covered rocky locations (see Fig. 1). 728 729 Fig. 7. Mean (+SE) species number (SR), Shannon diversity (H’) and taxonomic 730 distinctness (Δ*) of the assemblages from the two habitats studied - sand-free (a) and 731 sand-covered (b) rocky platforms - at multiple spatial scales. Numbers under bars 732 indicate the locations (see Fig. 1). 733 734 12 3 45678 7º W 8º W 43º40’N N 0 30 60 90 2 3 4 7 0 30 60 90 2 3 4 7 Corallina elongata 0 30 60 90 2 3 4 7 0 30 60 90 2 3 4 7 Lithophyllum incrustans 0 30 60 90 2 3 4 7 Boergeseniella thuyoides 0 30 60 90 2 3 4 7 0 30 60 90 2 3 4 7 Mesophyllum lichenoides 0 30 60 90 2 3 4 7 (a) (b) (c) (d) 0 30 60 90 1 5 6 8 0 30 60 90 1 5 6 8 0 30 60 90 1 5 6 8 0 30 60 90 1 5 6 8 0 30 60 90 1 5 6 8 0 30 60 90 1 5 6 8 1 5 6 8 0 30 60 90 Rhodothamniella floridula Ophidocladus simpliciusculus 0 30 60 90 1 5 68 Polysiphonia caespitosa 0 30 60 90 1 5 6 8 Plocamium maggsiae 0 30 60 90 1 5 6 8 Pterosiphonia pennata (a) (b) (c) (d) (e) SR (a) 30 15 02 3 4 7 2 3 4 7 2 3 4 7 30 15 0 SR (b) 1 5 6 8 1 5 6 8 1 5 6 8 2 3 4 7 2 3 4 7 2 1 0 H’ (c) 2 3 4 7 1 5 6 8 1 5 6 8 2 1 0 H’ (d) 1 5 6 8 2 3 4 7 2 3 4 7 100 (e) Δ* 90 60 70 80 2 3 4 7 1 5 6 8 (f) Δ* 90 60 70 80 100 1 5 6 8 1 5 6 8