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

lable at ScienceDirect

Estuarine, Coastal and Shelf Science xxx (2013) 1e12

Contents lists avai

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

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

Pilar Díaz-Tapia a,*, Ignacio Bárbara a, Isabel Díez b

aBioCost Research Group, Universidade da Coruña, Facultade de Ciencias, Campus da Zapateira s/n, 15071 A Coruña, SpainbDepartment of Plant Biology and Ecology, University of the Basque Country UPV/EHU, PO Box 644, 48080 Bilbao, Spain

a r t i c l e i n f o

Article history:Received 19 March 2013Accepted 10 August 2013Available online xxx

Keywords:biodiversitysedimentsspatial variationsintertidal environmentassemblage structurerocky shores

* Corresponding author.E-mail address: [email protected] (P. Díaz-Tapia).

0272-7714/$ e see front matter � 2013 Elsevier Ltd.http://dx.doi.org/10.1016/j.ecss.2013.08.019

Please cite this article in press as: Díaz-Tapsand-free and sand-covered rocky habitats,

a b s t r a c t

The presence of high loads of sediment is often thought to be negatively associated with sessile speciesliving on rocky reefs, leading to assemblages with low alpha diversity (average species richness) and betadiversity (heterogeneity). Here we examine the effects of sand deposition on rocky assemblages bycontrasting the multivariate composition, spatial variation and alpha diversity between sand-free as-semblages and assemblages covered by sand. The assemblage composition differed markedly betweensand-covered and sand-free reefs, supporting the idea of that sedimentation is one of the major physicalfactors influencing the structure of benthic assemblages. More surprisingly, our findings suggest thatsand-covered assemblages have greater spatial variation in terms of multivariate dispersion at smallspatial scales (from metres to 100s of metres) than sand-free assemblages. No differences were detectedbetween the two habitats in average species richness and Shannon diversity, whereas sand-coveredassemblages were found to be taxonomically more diverse. Thus, the effects of sedimentation on thediversity of assemblages from rocky shores remain unclear and further investigation is needed to clarifyits structuring role in combination with other environmental factors.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

The successful management and protection of biological di-versity, the assessment of anthropogenic impacts and the restora-tion of altered ecosystems rely largely on understanding theprocesses and factors that structure assemblages (Chapman, 1999;Anderson et al., 2005; Terlizzi et al., 2007). Causal relationshipsbetween influential factors, ecological processes and subsequentdistribution of species need to be explored by experimentalresearch (Underwood et al., 2000), but quantifying the range ofnatural variation of assemblages may help to identify whichphysical and biological factors are most relevant to be explored firstunder an experimental approach (Underwood and Chapman, 1996;Menconi et al., 1999; Coleman, 2002). Thus, research efforts haveincreased recently to provide a more in-depth knowledge ofassemblage heterogeneity for a broad variety of habitats(Benedetti-Cecchi, 2001; Pérez-Ruzafa et al., 2007; Smale et al.,2010). In particular, marine benthic assemblages have been found

All rights reserved.

ia, P., et al., Multi-scale spatiEstuarine, Coastal and Shelf S

to be highly variable across different scales of time and space(Coleman, 2002; Fraschetti et al., 2005).

With regard to intertidal systems, ecologists have devotedspecial attention to examining patterns of variation along the ver-tical gradient imposed by tidal cycles. The role of biotic interactionsand physical factors in structuring intertidal assemblages along thisgradient of stress has long been studied (Dayton, 1971; Schonbeckand Norton, 1980; Moreno and Jaramillo, 1983; McCook andChapman, 1993; Jenkins et al., 1999). By contrast, along-shorevariation has received far less attention despite the fact that itmight be greater than vertical variation, depending on the spatialscale (Benedetti-Cecchi, 2001; Valdivia et al., 2011). In recent years,studies on horizontal heterogeneity have quantified variabilityacross multiple scales of space, increasing knowledge of the pro-cesses that regulate species distribution from fine (patchiness) tobroad spatial scales (Menconi et al., 1999; Johnson et al., 2001;Coleman, 2003; Denny et al., 2004).

The physical factors traditionally explored as sources of varia-tion in intertidal assemblages include seawater temperature,salinity, wave exposure and intertidal height (Stephenson andStephenson, 1949; Underwood, 1978; Druehl and Green, 1982;McQuaid and Branch, 1984; Josselyn and West, 1985). However,despite the large role that sedimentation plays in modifying coastal

al variability in intertidal benthic assemblages: Differences betweencience (2013), http://dx.doi.org/10.1016/j.ecss.2013.08.019

Delta:1_given name

Delta:1_surname

Delta:1_given name

mailto:[email protected]

www.sciencedirect.com/science/journal/02727714

http://www.elsevier.com/locate/ecss

http://dx.doi.org/10.1016/j.ecss.2013.08.019



Fig. 1. Map of the study area showing the sampling locations on the northwestern coast of the Iberian Peninsula: 1) Picón, 2) Bares, 3) Burela, 4) Peinzás, 5) Llas, 6) Catedrales, 7)Rinlo and 8) Serantes. Unshaded squares and shaded circles correspond to sand-free and sand-covered reefs, respectively.

P. Díaz-Tapia et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e122

environments, its potential influence on the structure of rocky as-semblages has been rarely studied until recently (but see Daly andMathieson, 1977; Littler et al., 1983; Airoldi et al., 1995). In recentyears there have been some studies on the effects of the increase ofanthropogenic sediment loads in rocky coastal assemblages(Airoldi, 2003 and references therein), which has been reported as amajor threat to marine biodiversity on a global scale (UnitedNations Environment Programme, 1995). By contrast, the role ofnatural sedimentation in the structure of benthic assemblages hasreceived little attention (but see e.g. Daly and Mathieson, 1977;Taylor and Littler, 1982; Littler et al., 1983; Airoldi and Hawkins,2007; Anderson et al., 2008b). The two approaches to the studyof sedimentation in regard to benthic assemblages agree in thatsedimentation affects the composition and distribution of rockycoast organisms, but they present contrasting views regarding itseffects on diversity. The prevalent opinion is that high sedimentloads related to anthropogenic activities are detrimental to theoverall diversity of rocky coast organisms (Airoldi, 2003 and ref-erences therein), but some authors support the hypothesis that thenatural presence of sediments promotes species diversity (Littleret al., 1983; McQuaid and Dower, 1990). However, a multiple-scale approach comparing the relevant spatial-scales of variationin diversity between sand-covered and sand-free rocky assem-blages has never been attempted. Indeed, the issue of scale hasrarely been addressed in research into the impacts of sedimenta-tion on rocky coast assemblages (Airoldi, 2003).

Descriptive studies of rocky intertidal assemblages from theAtlantic coast of the Iberian Peninsula have shown differences incomposition between sand-free and sand-covered rocky assem-blages (e.g. Miranda, 1931; Ardré, 1970; Pérez-Cirera, 1976; Pérez-Cirera and Maldonado, 1982; Bárbara, 1994; Bárbara et al., 1995;Díaz-Tapia and Bárbara, 2005). However, quantitative data onspatial patterns of distribution of organisms are scarce (Boaventuraet al., 2002; Cremades et al., 2004; Araújo et al., 2005; Díez et al.,2009). In addition, all these studies are focused on sand-freerocky habitats, while there are no previous quantitative studies ofsand-covered assemblages, even though they are commonlydistributed along the Atlantic coastline of the Iberian Peninsula (seeDíaz Tapia et al., 2011).

This study assessed differences in spatial patterns of variabilityin multivariate structure and diversity between sand-free andsand-covered rocky assemblages. We use a hierarchical design toquantify the magnitude of variation attributable to each of severalspatial scales at each of the two habitats. The use of nested hier-archical sampling designs to examine both univariate and

Please cite this article in press as: Díaz-Tapia, P., et al., Multi-scale spatisand-free and sand-covered rocky habitats, Estuarine, Coastal and Shelf

multivariate response variables at multiple spatial scales has led toa greater appreciation of the importance of scale in ecology(Underwood and Chapman, 1996; Fraschetti et al., 2005). Thesedesigns provide unbiased, independent, rigorous quantitativemeasures of variability at predetermined spatial scales with a viewto testing structured hypotheses (Underwood and Chapman, 1996;Terlizzi et al., 2007). Specifically, we address 3 main questions: (1)do sand-free and sand-covered rocky assemblages differ in terms ofmultivariate structure and alpha diversity (species richness, Shan-non and Taxonomic Distinctness measures); (2) are patterns ofvariability in assemblage structure and diversity dependent onspatial scale, and (3) are sand-free rocky assemblages spatiallymore heterogeneous than sand-covered assemblages?

2. Methods

2.1. Study area

The study area extends for approximately 100 km along thenorthern Galician coast in northwestern Spain (43�330 N to 43�470

N and 006�560 W to 007�480 W; Fig. 1). This is an open coastexposed to a large fetch where swell comes mainly from NW (38%)andWNW (29%), with mean significant heights (Hs) of 3 and 2.5 m,respectively (Puertos del Estado, 2013). It consists mostly of rockysubstratum interrupted irregularly by the presence of rias andbeaches. Tides are semidiurnal with a spring tidal range of up to3.8 m, and the sea surface temperature ranges from 11 �C to 18 �C(Bárbara et al., 2005). The flora falls within warm-temperate NEAtlantic subregion 1 (WNE1) according to the phytogeographicalscheme proposed by Hoek and Breeman (1990).

2.2. Collection of data and sampling design

Sampling was conducted from July to August 2010. Twodifferent habitats at the low intertidal level (between 0.4 m and1.2 m above MLWL) were selected for this study: sand-free andsand-covered rocky platforms. The former consists of rocky shoreslocated at least 100 m apart from sandy beaches. The latter are rockoutcrops on sandy beaches constantly covered by a sand layer(>1 cm thick) which is trapped within algal turfs. Sampling loca-tions were randomly selected along a stretch of coastline about100 km long, from a set of locations with comparable environ-mental conditions: N-NE-facing pristine open coastal shoresexposed to strong wave action, with stable substrata (continuousbedrock and large blocks), smooth surfaces and slight to moderate

al variability in intertidal benthic assemblages: Differences betweenScience (2013), http://dx.doi.org/10.1016/j.ecss.2013.08.019

Fig. 2. nMDS ordinations of assemblages based on BrayeCurtis dissimilarity measureson square root transformed cover data (a) and Jaccard coefficients on presence/absencedata (b). Unshaded and shaded symbols correspond to sand-free and sand-coveredreefs, respectively (see Fig. 1).

P. Díaz-Tapia et al. / Estuarine, Coastal and Shelf Science xxx (2013) 1e12 3

slope (0�e45�). Data were collected following a full nested hierar-chical sampling design taking into account four spatial scales:Location (four coastal stretches about 1 km long at least 10 kmapart for each habitat) (Fig. 1), Site (three stretches 100 m long atleast 100 m apart), Patch (three stretches 10 m long at least 10 mapart), and Quadrat (three 20 � 20 cm quadrats at least 1 m apart).The percentage cover of seaweeds and sessile invertebratesexceeding 0.5 cm in length was visually estimated in each quadratas described by Dethier et al. (1993). Representative specimens ofthose taxa that could not be identified in situ were collected foridentification at the laboratory and deposited in the SANT-Algaeherbarium (University of Santiago de Compostela).

2.3. Statistical analyses

Differences in the multivariate structure of assemblages be-tween the two habitats studied were assessed with permutationalmultivariate analysis of variance (PERMANOVA) using the PRIMERV. 6. PERMANOVA package (Clarke and Gorley, 2006; Andersonet al., 2008a). The factors considered were: Habitat (fixed, 2levels), Location (random, 4 levels, nested in habitat), Site (random,3 levels, nested in locations), and Patch (random, 3 levels, nested insites) with n ¼ 3. The resemblance matrices comparing pairs ofsamples were calculated using the BrayeCurtis index on square-root transformed data and the Jaccard coefficient on presence/absence data. The tests used 9999 permutations under a reducedmodel, and significance was accepted at p < 0.05. Given that therewere too few possible permutations (<100) to obtain a meaningfulp-value for the contrast between the two habitats, a p-value wascalculated using 9999 Monte Carlo random draws from theappropriate asymptotic permutation distribution (Anderson andRobinson, 2003). Data were represented graphically using non-metric multidimensional scaling (nMDS) plots. The contributionsof individual taxa to dissimilarities between the two habitats weredetermined using similarity percentage analysis (SIMPER). Therelative contributions of taxa were assessed using k-dominancecurves (Clarke and Warwick, 2001).

Hierarchical PERMANOVA analyses were performed on the basisof Jaccard and BrayeCurtis (square root transformed data) mea-sures for each habitat separately to examine differences in spatialvariability at the four spatial scales considered. Variance compo-nents were estimated for each source of variation in PERMANOVAby setting mean squares equal to their expectations. Occasionally,negative estimates were obtained from the analysis. In these cases,negative values were set to zero, the term was removed from themodel and the data were re-analysed (Fletcher and Underwood,2002).

Differences in the spatial heterogeneity of the multivariatestructure of assemblages between habitats were examined byapplying the permutational test for homogeneity of multivariatedispersions (PERMDISP) (Anderson, 2006). The analysis calculatesan F-statistic to compare the average distance from the observationunits to their group centroid in the multivariate space defined, inthis case, by BrayeCurtis and Jaccard indices. The p-values wereobtained by 9999 random permutations of least-square residuals.

The species richness (SR) and ShannoneWiener index (H0 usingloge) were calculated for each quadrat using the DIVERSE routine ofthe PRIMER statistical package. In addition, average taxonomicdistinctness (D*) was calculated on cover data. Warwick and Clarke(1995) defined this asD*¼ [

PPi<juij xi xj]/[

PPi<j xi xj] whereuij is

the taxonomic distance between species i and j and x denotes theabundance of species in the sample. The measure is independent ofspecies richness or sample size, and it reflects both richness inhigher taxa and the evenness component of taxonomic diversity.Macrophyte species were aggregated into higher taxonomic levels

Please cite this article in press as: Díaz-Tapia, P., et al., Multi-scale spatisand-free and sand-covered rocky habitats, Estuarine, Coastal and Shelf S

following the AlgaeBase classification (Guiry and Guiry, 2013) andinvertebrate species were compiled according to the MarBEF datasystem (MarBEF, 2004). Step lengths from species to phylum wereequally weighted over each taxonomic level and the greatesttaxonomic distance was set to 100.

Univariate PERMANOVA analyses based on Euclidean distancewere performed to test the null hypothesis that there were nodifferences in SR, H0, D*, and the mean percentage cover of the mostabundant species using the same multi-factor experimental designapplied in multivariate analyses. Prior to the analyses, Cochran’s C-test was performed using the GMAV5 package (University of Syd-ney) to check for homogeneity of variance, and data were properlytransformed when necessary. The most stringent criterion ofa < 0.01 was used to reject the null hypothesis when varianceswere heterogeneous and analyses were conducted on untrans-formed data.

3. Results

3.1. Assemblage composition

Overall, 127 taxa were identified in this study. The most widelyrepresented phylum was Rhodophyta with a total of 90 taxa, fol-lowed by Ochrophyta with 18 and Chlorophyta with 14 (Appendix1). Sessile invertebrates were scarcely represented, with just twotaxa belonging to Mollusca and two to Arthropoda. PERMANOVAanalyses on multivariate data detected significant differences be-tween sand-free and sand-covered assemblages, in both species


Fig. 3. K-dominance plot for abundance of species in benthic assemblages from sand-covered reefs (shaded circles) and sand-free platforms (unshaded squares).


composition (pseudoF ¼ 7.19; p(MC) ¼ 0.001) and abundance(pseudoF ¼ 22.96; p(MC) ¼ 0.0001). These differences betweenhabitats are graphically illustrated by the patterns in the non-metric multidimensional scaling (nMDS) (Fig. 2), which show thetwo habitats clearly separated from each other. A K-dominance plot(Fig. 3) also revealed differences in the structure of assemblagesbetween sand-free and sand-covered habitats. The accumulationcurve of rocky assemblages is characterised by few numericallydominant species while sand-covered assemblages are moreequitable in terms of species abundance.

The patterns of variation in the multivariate structure of as-semblages across spatial scales were examined for each habitatseparately. For sand-free rocky assemblages, PERMANOVA analysisdetected significant variation across all the spatial scales consid-ered, in both composition and the relative abundance of species(Table 1). Variance components indicated that the variability at thelargest (km) and at the smallest (m) spatial scales contributed mostto the overall variability (Table 1). By contrast, PERMANOVAdetected no differences between locations within sand-coveredrocky habitat, and revealed the scale of hundreds of metres (sites)as the most variable when considering abundance of species, andmetres (residual) when considering composition (Table 1).

PERMDISP revealed that spatial heterogeneity in multivariatestructure based on the relative abundance of species was

Table 1Results of PERMANOVAs testing for spatial differences in the structure of assemblages at scon BrayeCurtis (square root transformed data) and Jaccard (presence/absence data) d**p < 0.01; ***p < 0.001; ns ¼ not significant.

Source df BrayeCurtis

MS Pseudo F Varianc

Sand-free rocky assemblagesLocation ¼ L 3 11,935 7.22*** 380.8Site ¼ Si(L) 8 1652.6 2.13*** 97.5Patch ¼ P(Si(L)) 24 775.5 3.14*** 176.2Residual 72 246.83 246.8Total 107

Sand-covered rocky assemblagesLocation ¼ L 3 9734.6 0.97ns 0.00Site ¼ Si(L) 8 10073 5.00** 885.4Patch ¼ P(Si(L)) 24 2011.9 3.25** 464.4Residual 72 618.54 618.5Total 107


significantly greater in sand-covered habitats than in sand-freerocky habitats at the scale of metres (quadrat), tens of metres(patch), and hundreds of metres (site), while no differences weredetected at the km scale (location) (Fig. 4A). With respect tocomposition, sand-free rocky assemblages were also more homo-geneous than sand-covered assemblages at the smallest spatialscales (i.e. quadrat & patch), but PERMDISP showed that rocky as-semblages were marginally (p ¼ 0.05) more heterogeneous at thescale of kilometres (Fig. 4B).

SIMPER analysis on BrayeCurtis measures showed that ninetaxa accounted for most of the differentiation between sand-freeand sand-covered rocky assemblages (Table 2). Each taxon ac-counts for more than 2% of the average dissimilarity between thetwo habitats (84.8%), and their cumulative contribution is 51.82%.Their contribution to the average dissimilarity between habitats isconsistent across pairs of samples since the ratio di/SD(di) was>2 inmost cases.

The red calcareous alga Corallina elongata (90.00%� 1.02; overallaverage cover� SD, n¼ 108) was the dominant species at the sand-free rocky reefs followed by the red encrusting species Lithophyllumincrustans (66.68% � 2.43). The main accompanying species(cover > 2%) were the epiphytes Mesophyllum lichenoides, Boerge-seniella thuyoides, Falkenbergia rufolanosa and Ceramium echiono-tum. In addition, the mussel Mytilus galloprovincialis formed smallclumps among turfs of Corallina. Several characterising specieswerefound exclusively in the sand-free rocky habitat: the macrophytesGastroclonium ovatum, Osmundea pinnatifida, Jania rubens, Cys-toseira tamariscifolia and Gelidium corneum, and the invertebratesPollycipes pollycipes, Patella spp. and Semibalanus balanoides.

Assemblages in the sand-covered rocky habitats were domi-nated by the red filamentous species Rhodothamniella floridula(64.06% � 4.19; overall average cover � SE, n ¼ 108) or by Ophi-docladus simpliciusculus (25.35% � 3.31). Occasionally, Plocamiummaggsiae (12.56% � 2.51) overgrew them. Other important specieswith an average cover of >2% were Pterosiphonia pennata, Poly-siphonia caespitosa, P. foetidissima, Hypoglossum hypoglossoides,Hildenbrandia rubra, Lithophyllum incrustans, and Boergeseniellathuyoides. Characterising species only found in this habitat wereP. nigra, P. foetidissima, P. fucoides, Ptilothamnion sphaericum, Gym-nogongrus griffithsiae and Gastroclonium reflexum.

Results from univariate PERMANOVA on the cover of the ninemost important species in differentiating between the two habitatsaccording to the SIMPER procedure are summarised in Table 3.PERMANOVA indicated a significant effect of variability betweenlocations for Corallina elongata only. By contrast, analyses detectedsubstantial spatial heterogeneity at the medium spatial scales: site

ales of location, site and patch in the two rocky habitats studied. Analyses performedissimilarities. Estimates of multivariate variation are given for each spatial scale.

Jaccard

e component MS Pseudo F Variance component

26,512 6.92** 840.13829.8 2.04** 217.01876.5 2.32** 356.1808.36 808.4

14,053 1.48ns 168.59504.1 3.26** 731.72918.5 2.07** 502.51411.1 1411.1


(a)

0

5

10

15

20

25

30

35

40

45

50

Location Site ** Patch ** Quadrat **

Dis

tanc

e to

cen

troid

(b)

0

10

20

30

40

50

60

Location Site Patch ** Quadrat **

Dis

tanc

e to

cen

troid

Fig. 4. Average distance from centroid (þSE), defined by BrayeCurtis (a) and Jaccard (b) dissimilarity measures, of sand-free (grey) and sand-covered rocky assemblages (black) atthe scale of location (n ¼ 4), site (n ¼ 12), patch (n ¼ 36) and quadrats (n ¼ 108). Average distances from the centroid that are significantly different from one habitat to another areindicated by ** (p < 0.01).


(hundreds of metres) and patch (tens of metres) for most of thespecies examined (p < 0.05, Table 3). Variance components, withsome exceptions, tend to increase as the spatial scales decrease. Themean percentage cover of these species for each site and patchwithin sand-free and sand-covered rocky habitats are shown in Figs5 and 6, respectively (Fig. 7).

3.2. Diversity measures

The total number of taxawas similar in the two habitats studied:100 in the sand-free platforms and 96 in the sand-covered rocky

Table 2Summary of SIMPER analyses identifying contributions (di) from themost importanttaxa (individual contribution > 2%) to the average BrayeCurtis dissimilarity (onsquare root transformed data) between habitats. SD(di) standard deviation of indi-vidual species contribution; di% percentage of contribution. Species average cover in% in sand-free (CR) and sand-covered (CS) rocky habitats.

Species CR CS di SD(di) di/SD(di) di %P

di %

Corallina elongata 90.0 1.34 11.34 3.68 3.08 13.37 13.37Lithophyllum incrustans 66.68 3.36 9.24 2.34 3.95 10.90 24.27Rhodothamniella floridula 0.00 64.06 9.10 1.52 5.99 10.74 35.00Ophidocladus simpliciusculus 0.07 25.35 4.09 0.97 4.22 4.82 39.82Polysiphonia caespitosa 0.00 6.80 2.40 1.12 2.14 2.83 42.65Plocamium maggsiae 0.49 12.56 2.26 0.79 2.86 2.66 45.32Pterosiphonia pennata 0.21 7.88 1.93 0.77 2.51 2.28 47.60Boergeseniella thuyoides 4.47 2.29 1.87 0.94 1.99 2.20 49.79Mesophyllum lichenoides 5.39 0.00 1.71 0.81 2.11 2.02 51.82


shores. Univariate PERMANOVA showed no habitat effect(pseudoF ¼ 5.0616; p(MC) ¼ 0.065) on species richness (SR). The SRper quadrat ranged from 10 to 38, with an overall mean of 25.06(SD¼6.30;n¼108) in sand-free assemblages, and from3 to36,withan overall mean of 18.32 (SD ¼ 7.80) in sand-covered assemblages.Patterns of spatial variation in SR were dependent on spatial scaleand habitat (Table 3). PERMANOVA analysis detected significantvariability in SR of sand-free rocky assemblages at all spatial scales,with the km scale (location) contributing most to total variation. Bycontrast, PERMANOVA detected no differences between locationswithin the sand-covered rocky habitat, and revealed the site scale(100s m) as the most variable within this habitat.

PERMANOVA detected no differences (pseudoF ¼ 3.261;p(MC) ¼ 0.12) in Shannon diversity (H’) between habitats. Thepatterns of variation in Hʹ across spatial scales were similar to thosedetected in SR (Table 3). H0 per quadrat ranged from 0.92 to 2.25with an overall mean of 1.60 (SD¼ 0.32; n¼ 108) in sand-free rockyassemblages, and from 0.11 to 2.34 with an overall mean of 1.32(SD ¼ 0.56) in sand-covered assemblages.

Average taxonomic distinctness (D*) was significantly greater(pseudoF ¼ 14.66; p(MC) ¼ 0.0094) in sand-covered rocky as-semblages (mean � SD; 70.35 � 11.08; n ¼ 108) than in sand-freeones (63.43 � 4.28). With respect to sand-covered assemblages,no differences were detected between locations, whereas D*varied significantly across small spatial scales (i.e. site, patch).Variance components indicated that the variability at the spatial


Table

3Resultsof

three-way

nestedunivariate

PERMANOVAstestingforsp

atialdifferencesin

mea

npercentage

cove

rof

mostab

undan

ttaxa

anddiversity

mea

sures(SR:sp

eciesrich

ness;

H0 :

Shan

non

diversity;D*:

taxo

nom

icdistinctness)

inthetw

orock

yhab

itatsstudied.*p<

0.05

,**p

<0.01

;ns:

not

sign

ificant.

Sourceof

variation

Location

¼L

Site

(L)¼

Si(L)

Patch(Si(L))¼

P(Si(L))

Residual

Coc

hran’stest

Tran

sf.

MS

Pseu

doF

Variance

compon

ent

MS

Pseu

doF

Variance

compon

ent

MS

Pseu

doF

Variance

compon

ent

Variance

compon

ent

Sand-freehab

itats

Corallina

elon

gata

1640

.15.70

0*50

.089

287.73

05.94

7**

26.595

48.38

0.95

0ns

0.00

050

.289

ns

Lithop

hyllu

mincrustans

4586

.11.63

6ns

66.033

2803

.24.37

8**

240.32

640.29

2.78

3**

136.73

230.1

p<

0.05

e

Boergeseniella

thuy

oide

s7.73

91.47

8ns

0.09

35.23

52.12

3*0.30

82.46

63.24

5**

0.56

90.76

0ns

sqrt(x

þ1)

Mesop

hyllu

mliche

noides

1272

.61.86

9ns

21.910

680.97

01.59

6ns

28.246

426.76

7.14

9**

122.35

59.694

p<

0.01

e

SR69

5.49

06.80

7*21

.975

102.18

04.78

3**

8.97

921

.361

1.85

8*3.28

711

.500

ns

H0

2.11

812

.575

**0.07

20.16

83.17

4*0.01

30.05

32.27

5**

0.01

00.02

3ns

D*

77.239

2.53

55ns

1.73

2430

.463

1.54

3ns

1.19

1119

.743

1.40

68ns

1.90

2914

.034

p<

0.01

Sand-cov

ered

hab

itats

Oph

idocladu

ssimpliciusculus

1881

.10.37

8ns

0.00

049

75.5

2.89

5*36

1.87

1718

.83.12

6**

371.9

603.07

ns

Rho

dotham

niella

floridula

3497

.80.31

5ns

0.00

011

,111

4.60

4**

966.39

2413

.13.80

5**

554.82

748.68

ns

Polysiph

onia

caespitosa

2.0

2.14

6ns

0.03

90.91

33.00

8**

0.06

80.30

34.23

9**

0.07

70.07

2ns

ln(x

þ1)

Plocam

ium

mag

gsiae

1.9

0.58

2ns

0.00

03.27

023

.221

**0.34

80.14

11.01

3ns

0.02

30.21

0ns

ln(x

þ1)

Pterosipho

niape

nnata

0.1

0.49

9ns

0.00

00.22

51.94

9ns

0.01

20.11

54.43

8**

0.02

90.02

9ns

Arcsin

SR27

4.01

00.68

9ns

0.00

039

7.87

07.64

3**

38.424

52.056

2.97

2**

8.09

327

.778

ns

H0

0.54

80.20

9ns

0.00

02.62

212

.253

**0.26

80.21

42.89

5**

0.04

00.09

3ns

D*

275.84

00.39

3ns

0.00

070

2.74

05.48

3**

63.840

128.18

2.46

9**

22.435

60.871

p<

0.01

e



scales of hundreds of metres (site) and metres (quadrat)contributed most to the overall variability (Table 3). By contrast,D* in sand-free rocky assemblages did not present significantspatial variation at any scale, indicating a homogeneousdistribution.

4. Discussion

Along-shore heterogeneity in the multivariate composition ofrocky intertidal assemblages (beta diversity) is shown here to bedependent on spatial scale and habitat (sand-free versus sand-covered rocky platforms). Sand-covered assemblages were foundto have greater spatial variation in terms of multivariate dispersionat small spatial scales (frommetres to 100s of metres). In relation toalpha diversity, no differences were detected between habitats inaverage SR and H0, however, sand-covered assemblages were foundto be taxonomically more diverse than sand-free rockyassemblages.

Assemblage composition differed markedly between sand-covered and sand-free reefs. Two coralline algae, the articulatealga Corallina elongata and the encrusting species Lithophyllumincrustans, dominated sand-free rocky surfaces, whereas red fila-mentous forms, mainly Rhodothamniella floridula and Ophidocladussimpliciusculus, dominated sand-covered substrata. The only sessileinvertebrate thriving on sand-covered platforms was the musselMytilus galloprovincialis, which seems to be capable of with-standing periodic sand burials and the scouring stress of heavyloads of suspended sand (Zardi et al., 2006). The dominant role ofCorallinaceae along wave exposed shores on the Atlantic coast ofthe Iberian Peninsula (Sierra and Fernández, 1984; Bárbara et al.,1995; Díez et al., 2009) and in other temperate regions (Stewart,1982; Benedetti-Cecchi and Cinelli, 1994; Kelaher et al., 2001) hasbeen previously reported. Similarly, filamentous algal turfs havealso been documented as the dominant type of assemblages inhabitats influenced by sediments (e.g. Airoldi et al., 1995; Gorgulaand Connell, 2004; Díaz Tapia and Bárbara et al., 2005; Mei andSchiel, 2007). Sand inundation strongly influences assemblagecomposition involving effects that are species-specific andmorphology-dependent (Markham, 1973; Daly and Mathieson,1977; Devinny and Volse, 1978; D’Antonio, 1986; Umar et al.,1998; Albrecht, 1998; Eriksson and Johansson, 2003; Airoldi,2003; Airoldi and Hawkins, 2007). Burial, abrasion and modifica-tion of rocky surface features by sandmay directly influence speciesdistribution by interfering with settlement, recruitment, andgrowth processes, but also indirectly by unbalancing biologicalinteractions (Devinny and Volse, 1978; Mathieson, 1982; Kendrick,1991; Airoldi, 2003).

Sediment deposition is often thought to be negatively associatedwith macroalgal species living on rocky reefs (e.g. Mathieson, 1982;Engledow and Bolton, 1994; Irving and Connell, 2002; Airoldi,2003; Balata et al., 2007a,b). There is the prevalent opinion thatsedimentation results in reduced diversity by causingmortality andrecruitment inhibition of less tolerant species (Devinny and Volse,1978; Schiel et al., 2006) and/or enhancing the spatial dominanceof a few tolerant space-monopolising species (Airoldi et al., 1995).However, our results show that both sand-free and sand-coveredrocky assemblages exhibit similar species richness and tend to bedominated by a few species. It is of note that the average taxonomicdistinctness (D*) is significantly higher in the sediment-influencedhabitat. Taxonomic distinctness may be influenced by naturaldisturbance (Bevilacqua et al., 2009) and habitat features(Bevilacqua et al., 2011; Sandulli et al., 2011). Previous studies havesuggested that high taxonomic diversity might be expected underlow environmental stress since such conditions are conducive to


0

30

60

90

2 3 4 72 3 4 7

Corallina elongata

0

30

60

90

2 3 4 72 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)

Fig. 5. Spatial distribution of percentage cover (mean þ SE) of four taxa identified as important in differentiating sand-free rocky assemblages at the scale of site (n ¼ 9) and patch(n ¼ 3). Numbers indicate the sand-free rocky locations (see Fig. 1).


the establishment of macrophyte species with different biologicalrequirements (Mouillot et al., 2005).

It is also of note that most of the response variables examinedvaried considerably at all spatial scales. This emphasises the com-plex nature of these assemblages and the importance of adoptingmulti-scale designs in ecological studies (Benedetti-Cecchi, 2001;Coleman, 2002; Terlizzi et al., 2007; Chapman et al., 2010).


Heterogeneity at a small spatial scale (patchiness) is considered tobe a general property of benthic assemblages in marine coastalhabitats (Fraschetti et al, 2005; Anderson et al., 2005; Terlizzi et al.,2007; Chapman et al., 2010; Smale et al., 2011). Regarding our re-sults, the multivariate structure of assemblages in terms of therelative abundance of species was found to be highly variable at thescale of metres in both habitats. However, the multivariate


0

30

60

90

1 5 6 81 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 81 5 6 8

0

30

60

90

Rhodothamniella floridula

Ophidocladus simpliciusculus

1 5 6 8

Polysiphonia caespitosa

1 5 6 8

Plocamium maggsiae

1 5 6 8

Pterosiphonia pennata

(a)

(b)

(c)

(d)

(e)

Fig. 6. Spatial distribution of percentage cover (mean þ SE) of five taxa identified as important in differentiating sand-covered rocky assemblages at the scale of site (n ¼ 9) andpatch (n ¼ 3). Numbers indicate the sand-covered rocky locations (see Fig. 1).


Please cite this article in press as: Díaz-Tapia, P., et al., Multi-scale spatial variability in intertidal benthic assemblages: Differences betweensand-free and sand-covered rocky habitats, Estuarine, Coastal and Shelf Science (2013), http://dx.doi.org/10.1016/j.ecss.2013.08.019

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 81 5 6 8

2 3 4 72 3 4 7

2

1

0

H’

(c)

2 3 4 7

1 5 6 81 5 6 8

2

1

0

H’

(d)

1 5 6 8

2 3 4 72 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

Fig. 7. Mean (þSE) species number (SR), Shannon diversity (H0) and taxonomic distinctness (D*) of the assemblages from the two habitats studied - sand-free (a, c, e) and sand-covered (b, d, f) rocky platforms e at multiple spatial scales. Numbers under bars indicate the locations (see Fig. 1).


composition of sand-covered assemblages shows most variabilityat the scale of site (100s m). Similarly, in relation to species richnessand diversity, sand-covered assemblages show the largest compo-nent of variation between sites, whereas location (km) is the majorcontributor to overall variability in sand-free rocky assemblages.Therefore, it is not possible to postulate a general pattern regardingspatial variability in the assemblages studied. Similar trendsemerge from previous studies, which found that different spatialscales explain the variability of different community characteristics(Lindegarth et al., 1995; Archambault and Bourget, 1996).

Our results suggest that the processes that determine the spatialvariability in the two habitats studied operate at different spatialscales. Although this study was not specifically designed to inves-tigate the causes of the spatial scales of variability detected, somehypotheses may explain the high contribution to the overall vari-ability observed at the scale of 100s of metres in sand-coveredassemblages and km in sand-free rocky assemblages. Sediments


surrounding sand-covered assemblages are in continuous move-ment in linewith the energy input provided bywaves, currents, andtides (Daly and Mathieson, 1977). The direction and intensity ofthese factors change over time, resulting in sediment depositionfluctuations that may promote differential burial periods of as-semblages at the scale of 100s of metres. The strong effect ofburying on the structure of assemblages has been reported inseveral papers (Daly and Mathieson, 1977; Littler et al., 1983;Anderson et al., 2008b), but its role in generating spatial patternsof variability at different spatial scales remains unstudied. In thecase of sand-free rocky assemblages that are highly variable at thescale of location (km apart), differences in substratum topographyand wave exposure may explain the patterns observed(Archambault and Bourget, 1996; Denny et al., 2004; Tuya andHaroun, 2006). Alternatively, differences in spatial variability be-tween habitats could also be explained by the life history charac-teristics and dispersal potential of the dominant species. The



calcareous red alga Corallina elongata mostly colonises the sub-stratum by recruitment from spores (Benedetti-Cecchi and Cinelli,1994) while filamentous turf-forming algae have been suggestedto benefit from stoloniferous growth of creeping axes under sandburial conditions (Airoldi et al., 1995; Mei and Schiel, 2007). Studiesof intertidal molluscs with different life histories have shown thatthe abundance of species with direct development has a highervariability at scales of 100s of metres, while species with larvaldispersal vary at km scales (Johnson et al., 2001). Analogously, itcould be hypothesised that assemblages dominated by algal speciesthat reproduce via spores or propagules may have larger spatialscales of variability than those that do so by vegetative growth.However, it is of note that the spores of seaweeds are often char-acterized by their short viability and dispersion, while detachedparts of plants increase their dispersal capacity (Santelices, 1990).

Our findings also suggest that spatial variation, in terms of ho-mogeneity of multivariate dispersion, is greater in sand-coveredassemblages than in sand-free rocky assemblages at small spatialscales (quadrat, patch, site). Differences in the disturbance regimebetween the two habitats may possibly explain the mechanismsunderlying these differences in beta diversity. Local disturbance haslong been shown to be a major driver of spatial heterogeneity inintertidal assemblages (Sousa, 1979, 1984; Gouhier and Guichard,2007). Therefore, it seems plausible to hypothesise that sand dis-placements may create a disturbance regime that is spatially morevariable than that imposed by factors operating on sand-free rockyassemblages. In this sense, studies on sediment-influenced habitatshave highlighted that the presence of sediments promotes spatialheterogeneity on rocky coasts (Littler et al., 1983; McQuaid andDower, 1990). Conversely, other work supports the argument thatsedimentation reduces the heterogeneity of assemblages (Balataet al., 2007a). These two contrasting views of the effects of sedi-mentation on assemblage heterogeneity may result from differ-ences in the sedimentation regime and its interactions with otherenvironmental variables and biological factors (Airoldi, 2003). Thus,the studies that support the detrimental effect of sedimentation onspatial heterogeneity have been carried out in subtidal habitats andhave focused on the impact of human related sediments on rockyassemblages (Balata et al., 2007a). In contrast, the studies that findthat spatial heterogeneity is increased by the presence of sedimentshave been carried out in the intertidal zone of rocky shores naturallyimpacted by sediments (Littler et al., 1983; McQuaid and Dower,1990). Therefore, the higher energy conditions of intertidal areasmay result in an increased regime of perturbations and in a moredynamic landscape than that found in subtidal areas.

In conclusion, assemblages living on sand-free and sand-covered rocky platforms differ substantially in terms of structureand spatial variability, supporting the idea that sedimentation isone of the major physical factors influencing the structure ofbenthic assemblages. In contrast with previous studies that haveinvestigated the effects of enhanced loads of sediments onassemblage diversity (Balata et al., 2007a, b), our results show thatSR and H0 are similar in both habitats, while taxonomic diversityand spatial variation are higher in the habitat influenced by sand.Thus, although there are numerous papers which agree that sedi-mentation promotes changes in benthic assemblage structure, itseffects on diversity remain unclear. However, it is essential to clarifythis issue in a global scenario in which turf-forming algae arereplacing canopy species supposedly by anthropogenicallyenhanced sediment loads (Airoldi, 2003; Gorgula and Connell,2004). This emphasises the need to study the effects of sedimen-tation on benthic diversity in combination with other environ-mental factors such as wave action, bathymetric level, topographyand sediment characteristics through manipulative experimentsthat enable cause-effect relationships to be established.


Acknowledgements

This study was funded by the project CGL2009-09495/BOS(Ministerio de Ciencia e Innovación, partially funded by the ERDF).

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.ecss.2013.08.019.

References

Airoldi, L., 2003. The effect of sedimentation on rocky coast assemblages. Ocean-ography and Marine Biology, Annual Review 41, 161e236.

Airoldi, L., Hawkins, S.J., 2007. Negative effects of sediment deposition on grazingactivity and survival of the limpet Patella vulgata. Marine Ecology ProgressSeries 332, 235e240.

Airoldi, L., Rindi, F., Cinelli, F., 1995. Structure, seasonal dynamics and reproductivephenology of a filamentous turf assemblage on a sediment influenced, rockysubtidal shore. Botanica Marina 38, 227e238.

Albrecht, A.S., 1998. Soft bottom versus hard rock: community ecology of macro-algae on intertidal mussel beds in the Wadden Sea. Journal of ExperimentalMarine Biology and Ecology 229, 85e109.

Anderson, M.J., 2006. Distance based tests for homogeneity of multivariate dis-persions. Biometrics 62, 245e253.

Anderson, M.J., Robinson, J., 2003. Generalised discriminant analysis based ondistances. Australian and New Zealand Journal of Statistics 45, 301e318.

Anderson, M.J., Diebel, C.E., Blom, W.M., Landers, T.J., 2005. Consistency and vari-ation in kelp holdfast assemblages: spatial patterns of biodiversity for the majorphyla at different taxonomic resolutions. Journal of Experimental MarineBiology and Ecology 320, 35e56.

Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008a. PERMANOVAþ for PRIMER: Guideto Software and Statistical Methods. PRIMER-E, Plymouth, UK, p. 214.

Anderson, R.J., Anderson, D.R., Anderson, J.S., 2008b. Survival of sand-burial byseaweeds with crustose bases or life-history stages structures the biotic com-munity on an intertidal rocky shore. Botanica Marina 51, 10e20.

Araújo, R., Bárbara, I., Sousa-Pinto, I., Quintino, V., 2005. Spatial variability ofintertidal rocky shore assemblages in the northwest coast of Portugal. Estua-rine, Coastal and Shelf Science 64, 658e670.

Archambault, P., Bourget, E., 1996. Scales of coastal heterogeneity and benthicintertidal species richness, diversity and abundance. Marine Ecology ProgressSeries 136, 111e121.

Ardré, F., 1970. Contribution à l’étude des algues marines du Portugal. I. La Flore.Portugaliae Acta Bioogica., Série B. 10, 137e555.

Balata, D., Piazzi, L., Benedetti-Cecchi, L., 2007a. Sediment disturbance and loss ofbeta diversity on subtidal rocky reefs. Ecology 88, 2455e2461.

Balata, D., Piazzi, L., Cinelli, F., 2007b. Increase of sedimentation in a subtidal sys-tem: effects on the structure and diversity of macroalgal assemblages. Journalof Experimental Marine Biology and Ecology 351, 73e82.

Bárbara, I., 1994. Las comunidades de algas bentónicas marinas en al bahía de LaCoruña y ría del Burgo. Microfichas del Servicio de Publicaciones e IntercambioCientífico de la Universidad de Santiago de Compostela, Santiago de Compos-tela, p. 411.

Bárbara, I., Cremades, J., Pérez-Cirera, J.L., 1995. Zonación de la vegetación bentónicamarina en la Ría de A Coruña (N.O. de España). Nova Acta Científica Compos-telana (Bioloxía) 5, 5e23.

Bárbara, I., Cremades, J., Calvo, S., López-RodrÃguez, M.C., Dosil, J., 2005. Checklist ofthe benthic marine and brackish Galician algae (NW Spain). Anales del JardÃnBotánico de Madrid 62, 69e100.

Benedetti-Cecchi, L., 2001. Variability in abundance of algae and invertebrates atdifferent spatial scales on rocky sea shores. Marine Ecology Progress Series 215,79e92.

Benedetti-Cecchi, L., Cinelli, F., 1994. Recovery of patches in an assemblage ofgeniculate coralline algae: variability at different successional stages. MarineEcology Progress Series 110, 9e18.

Bevilacqua, S., Fraschetti, S., Musco, L., Terlizzi, A., 2009. Taxonomic sufficiency inthe detection of natural and human-induced changes in marine assemblages:habitats and taxonomic groups compared. Marine Pollution Bulletin 58, 1850e1859.

Bevilacqua, S., Fraschetti, S., Musco, L., Guarneri, G., Terlizzi, A., 2011. Low sensi-tiveness of taxonomic distinctness indices to human impacts: evidences acrossmarine benthic organisms and habitat types. Ecological Indicators 11, 448e455.

Boaventura, D., Ré, P., Cancela da Fonseca, L., Hawkins, A.J.S., 2002. Intertidal rockyshore communities of the continental Portuguese coast: analysis of distributionpatterns. Marine Ecology 23, 69e90.

Chapman, M.G., 1999. Improving sampling designs for measuring restoration inaquatic habitats. Journal of Aquatic Ecosystem Stress and Recovery 6, 235e251.

Chapman, M.G., Tolhurst, T.J., Murphy, R.J., Underwood, A.J., 2010. Complex andinconsistent patterns of variation in benthos, micro-algae and sediment overmultiple spatial scales. Marine Ecology Progress Series 398, 33e47.

Clarke, K.R., Gorley, R.N., 2006. PRIMER V6: Manual/Tutorial. PRIMER-E, Plymouth.




http://refhub.elsevier.com/S0272-7714(13)00360-0/sref1




























































































Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities, second ed.PRIMER-E, Plymouth.

Coleman, M.A., 2002. Small-scale spatial variability in intertidal and subtidal turfingalgal assemblages and the temporal generality of these patterns. Journal ofExperimental Marine Biology and Ecology 267, 53e74.

Coleman, M.A., 2003. The role of recruitment in structuring patterns of small-scalespatial variability in intertidal and subtidal algal turfs. Journal of ExperimentalMarine Biology and Ecology 291, 131e145.

Cremades, J., Bárbara, I., Veiga, A.J., 2004. Intertidal vegetation and its commercialpotential on shores of Galicia (NW Iberian Peninsula). Thalassas 20, 69e80.

D’Antonio, C.M., 1986. Role of sand in the domination of hard substrata the inter-tidal alga Rhodomela larix. Marine Ecology Progress Series 27, 263e275.

Daly, M., Mathieson, A.C., 1977. The effects of sand movement on intertidal sea-weeds and selected invertebrates at Bound Rock, New Hampshire, U.S.A. MarineBiology 43, 45e55.

Dayton, P.K., 1971. Competition, disturbance and community organization: theprovision and subsequent utilization of space in a rocky intertidal community.Ecological Monographs 41, 351e389.

Denny, M.W., Helmuth, B., Leonard, G.H., Harley, C.D.G., Hunt, L.J.H., Nelson, E.K.,2004. Quantifying scale in ecology: lessons from awave-swept shore. EcologicalMonographs 74, 513e532.

Dethier, M.N., Graham, E.S., Cohen, S., Tear, L.M., 1993. Visual versus random-pointpercent cover estimations: "objective" is not always better. Marine EcologyProgress Series 96, 93e100.

Devinny, J.S., Volse, L.A., 1978. Effects of sediments on the development of Macro-cystis pyrifera gametophytes. Marine Biology 48, 343e348.

Díaz-Tapia, P., Bárbara, I., 2005. Vegetación bentónica marina de la playa de Bar-rañán (A Coruña, Galicia). Nova Acta Científica Compostelana (Bioloxía) 14, 13e42.

Díaz-Tapia, P., Bárbara, I., Barreiro, R., 2011. Iberian intertidal turf assemblagesdominated by Erythroglossum lusitanicum (Ceramiales, Rhodophyta): structure,temporal dynamics, and phenology. Botanica Marina 54, 507e521.

Díez, I., Secilla, A., Santolaria, A., Gorostiaga, J.M., 2009. Ecological monitoring ofintertidal phytobenthic communities of the Basque Coast (N. Spain) followingthe Prestige oil spill. Environmental Monitoring and Assessment 159, 555e575.

Druehl, L.D., Green, J.M., 1982. Vertical distribution of intertidal seaweeds as relatedto patterns of submersion and emersion. Marine Ecology Progress Series 9,163e170.

Engledow, H.R., Bolton, J.J., 1994. Seaweed a-diversity within the lower eulittoralzone in Namibia: the effects of wave action, sand inundation, mussels andlimpets. Botanica Marina 37, 267e276.

Eriksson, B.K., Johansson, G., 2003. Sedimentation reduces success of Fucus ves-iculosus (Phaeophyceae) in the Baltic Sea. European Journal of Phycology 38,217e222.

Puertos del Estado, 2013. http://www.puertos.es/oceanografia_y_meteorologia/redes_de_medida/index.html. Consulted on 2013-01-05.

Fletcher, D.J., Underwood, A.J., 2002. How to cope with negative estimates ofcomponents of variance in ecological field studies. Journal of ExperimentalMarine Biology and Ecology 273, 89e95.

Fraschetti, S., Terlizzi, A., Benedetti-Cecchi, L., 2005. Patterns of distribution ofmarine assemblages from rocky shores: evidence of relevant scales of variation.Marine Ecology Progress Series 296, 13e29.

Gorgula, S.K., Connell, S.D., 2004. Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads.Marine Biology 145, 613e619.

Gouhier, T.C., Guichard, F., 2007. Local disturbance cycles and the maintenance ofheterogeneity across scales in marine metapopulations. Ecology 88, 647e657.

Guiry, M.D., Guiry, G.M., 2013. AlgaeBase. World-wide Electronic Publication, Na-tional University of Ireland, Galway. http://www.algaebase.org. Consulted on2013-01-05.

Hoek, C. van den, Breeman, A.M., 1990. Seaweed biogeography of the NorthAtlantic: where are we now? In: Garbary, D.J., South, G.R. (Eds.), EvolutionaryBiogeography of the Marine Algae of the North Atlantic. Springer-Verlag, Berlin,pp. 55e86.

Irving, A.D., Connell, S.D., 2002. Interactive effects of sedimentation and micro-topography on the abundance of subtidal turf-forming algae. Phycologia 41,517e522.

Jenkins, S.R., Hawkins, S.J., Norton, T.A., 1999. Direct and indirect effects of a mac-roalgal canopy and limpet grazing in structuring a sheltered inter-tidal com-munity. Journal of Experimental Marine Biology and Ecology 188, 81e92.

Johnson, M.P., Allcock, A.L., Pye, S.E., Chambers, S.J., Fitton, D.M., 2001. The effects ofdispersal mode on the spatial distribution patterns of intertidal molluscs.Journal of Animal Ecology 70, 641e649.

Josselyn, M.N., West, J.A., 1985. The distribution and temporal dynamics of the estu-arine macroalgal community of San Francisco Bay. Hydrobiologia 129, 139e152.

Kelaher, B.P., Chapman, M.G., Underwood, A.J., 2001. Spatial patterns of diversemacrofaunal assemblages in coralline turf and their associations with envi-ronmental variables. Journal of the Marine Biological Association of the UnitedKingdom 81, 917e930.

Kendrick, G.A., 1991. Recruitment of coralline crusts and filamentous turf algae inthe Galapagos archipelago: effect of simulated scour, erosion and accretion.Journal of Experimental Marine Biology and Ecology 147, 47e63.

Lindegarth, M., André, C., Jonsson, P.R., 1995. Analysis of the spatial variability inabundance and age structure of two infaunal bivalves, Cerastoderma edule and


C. lamarcki, using hierarchical sampling programs. Marine Ecology ProgressSeries 116, 85e97.

Littler, M.M., Martz, D.R., Littler, D.S., 1983. Effects of recurrent sand deposition onrocky intertidal organisms: importance of substrate heterogeneity in a fluctu-ating environment. Marine Ecology Progress Series 11, 129e139.

MarBEF, 2004. European Marine Biodiversity Datasets. Available online at: http://www.marbef.org/data/imis.php?module¼dataset. Consulted on 2013-01-05.

Markham, J.W., 1973. Observations on the ecology of Laminaria sinclairii on thethree northern Oregon beaches. Journal of Phycology 9, 336e341.

Mathieson, A.C., 1982. Field ecology of the brown alga Phaeostrophion irregulareSetchell et Gardner. Botanica Marina 25, 87e92.

McCook, L.J., Chapman, A.R.O., 1993. Community succession following massive ice-scour on a rocky intertidal shore: recruitment, competition and predationduring early, primary succession. Marine Biology 115, 565e575.

McQuaid, C.D., Branch, G.M., 1984. Influence of sea temperature, substratum andwave exposure on rocky intertidal communities: an analysis of faunal and floralbiomass. Marine Ecology Progress Series 19, 145e151.

McQuaid, C.D., Dower, K.M., 1990. Enhancement of habitat heterogeneity and spe-cies richness on rocky shores inundated by sand. Oecologia 84, 142e144.

Mei, J., Schiel, D.R., 2007. Survival strategies in Polysiphonia adamsiae andP. strictissima (Rhodophyta, Rhodomelaceae) subjected to sediment depositionand grazing pressure. New Zealand Journal of Marine and Freshwater Research41, 325e334.

Menconi, M., Benedetti-Cecchi, L., Cinelli, F., 1999. Spatial and temporal vari-ability in the distribution of algae and invertebrates on rocky shores in thenorthwest Mediterranean. Journal of Experimental Marine Biology andEcology 233, 1e23.

Miranda, F., 1931. Sobre las algas y Cianofíceas del Cantábrico especialmente deGijón. Trabajos del Museo Nacional de Ciencias Naturales de Madrid. SerieBotánica 25, 7e106.

Moreno, C.A., Jaramillo, E., 1983. The role of grazers in the zonation of intertidalmacroalgae of the Chilean coast near Valdivia. Oikos 41, 73e76.

Mouillot, D., Gaillard, S., Aliaume, C., Verlaque, M., Belsher, T., Troussellier, M., DoChi, T., 2005. Ability of taxonomic diversity indices to discriminate coastallagoon environments based on macrophyte communities. Ecological In-dicators 5, 1e17.

Pérez-Cirera, J.L., 1976. Tipos de vegetación bentónica cormofítica litoral del Nor-oeste de España (Ría de Corme y Lage). Documents Phytosociologiques 15e18,87e122.

Pérez-Cirera, J.L., Maldonado, J.L., 1982. Principales tipos de vegetación bentónica ysu zonación en el litoral comprendido entre las Rías de Camariñas y de Corme yLage (Costa de Camelle, La Coruña). Collectanea Botanica 13, 893e910.

Pérez-Ruzafa, A., Marcos, C., Pérez-Ruzafa, I.M., Barcala, E., Hegazi, M.I., Quispe, J.,2007. Detecting changes resulting from human pressure in a naturally quick-changing and heterogeneous environment: spatial and temporal scales ofvariability in coastal lagoons. Estuarine, Coastal and Shelf Science 75, 175e188.

Sandulli, R., De Leonardis, C., Vincx, M., Vanaverbeke, J., 2011. Geographical anddepth-related patterns in nematode communities from some Italian marineprotected areas. Italian Journal of Zoology 78, 505e516.

Santelices, B., 1990. Patterns of reproduction, dispersal and recruitment in sea-weeds. Oceanography and Marine Biology, Annual Review 28, 177e276.

Schiel, D.R., Wood, S.A., Dunmore, R.A., Taylor, D.I., 2006. Sediment on rockyintertidal reefs: effects on early post-settlement stages of habitat-formingseaweeds. Journal of Experimental Marine Biology and Ecology 331, 158e172.

Schonbeck, M.W., Norton, T.A., 1980. The effects on intertidal fucoid algae ofexposure to air under various conditions. Botanica Marina 23, 141e148.

Sierra, F., Fernández, C., 1984. El horizonte de Corallina elongata Ellis et Soland en lacosta central de Asturias (N.de España). II. Dinámica de un ciclo anual. Revistade Biología de la Universidad de Oviedo 2, 131e143.

Smale, D.A., Kendrick, G.A., Wernberg, T., 2010. Assemblage turnover and taxonomicsufficiency of subtidal macroalgae at multiple spatial scales. Journal of Exper-imental Marine Biology and Ecology 384, 76e86.

Smale, D.A., Kendrick, G.A., Wernberg, T., 2011. Subtidal macroalgal richness, di-versity and turnover, at multiple spatial scales, along the southwesternAustralian coastline. Estuarine, Coastal and Shelf Science 91, 224e231.

Sousa, W.P., 1979. Experimental investigations of disturbance and ecological suc-cession in a rocky intertidal algal community. Ecological Monographs 49, 227e254.

Sousa, W.P., 1984. The role of disturbance in natural communities. Annual Review ofEcology and Systematics 15, 353e391.

Stephenson, T.A., Stephenson, A., 1949. The universal features of zonation betweentide-marks on rocky coasts. Journal of Ecology 37, 289e305.

Stewart, J., 1982. Anchor species and epiphytes in intertidal algal turf. Pacific Science36, 45e59.

Taylor, P.R., Littler, M.M., 1982. The roles or compensatory mortality, physicaldisturbance and substrate retention in the development and organisation of asand influenced, rocky intertidal community. Ecology 63, 135e146.

Terlizzi, A., Anderson, M.J., Fraschetti, S., Benedetti-Cecchi, L., 2007. Scales of spatialvariation in Mediterranean subtidal sessile assemblages at different depths.Marine Ecology Progress Series 332, 25e39.

Tuya, F., Haroun, R., 2006. Spatial patterns and response to wave exposure ofshallow water algal assemblages across the Canarian Archipelago: a multi-scaled approach. Marine Ecology Progress Series 311, 15e28.

Umar, M.J., McCook, L.J., Price, I.R., 1998. Effects of sediment deposition on theseaweed Sargassum on a fringing coral reef. Coral Reefs 17, 169e177.




























































http://www.puertos.es/oceanografia_y_meteorologia/redes_de_medida/index.html

http://www.puertos.es/oceanografia_y_meteorologia/redes_de_medida/index.html
















http://www.algaebase.org







































http://www.marbef.org/data/imis.php?module=dataset














































































































Underwood, A.J., 1978. A refutation of critical tidal levels as determinants of thestructure of intertidal communities on British shores. Journal of ExperimentalMarine Biology and Ecology 33, 261e276.

Underwood, A.J., Chapman, M.G., 1996. Scales of spatial patterns of distribution ofintertidal invertebrates. Oecologia 107, 212e224.

Underwood, A.J., Chapman, M.G., Connell, S.D., 2000. Observations in ecology: youcan’t make progress on processes without understanding the patterns. Journalof Experimental Marine Biology and Ecology 250, 97e115.

United Nations Environmental Programme, 1995. Global Biodiversity Assessment.Cambridge University Press, Cambridge, p. 56.


Valdivia, N., Scrosati, R., Molis, M., Knox, A.S., 2011. Variation in community struc-ture across vertical intertidal stress gradients: how does it compare with hor-izontal variation at different scales? Plos One 6, e24062.

Warwick, R.M., Clarke, K.R., 1995. New ‘biodiversity’ measures reveal a decrease intaxonomic distinctness with increasing stress. Marine Ecology Progress Series129, 301e305.

Zardi, G.I., Nicastro, K.R., Porri, F., McQuaid, C.D., 2006. Sand stress as a non-determinant of habitat segregation of indigenous (Perna perna) and invasive(Mytilus galloprovincialis) mussels in South Africa. Marine Biology 148, 1031e1038.


























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

Top Related