Hydrobiologia 449: 171–177, 2001.J.P.M. Paula, A.A.V. Flores & C.H.J.M. Fransen (eds), Advances in Decapod Crustacean Research.© 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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Intertidal distribution and species composition of brachyuran crabsat two rocky shores in Central Portugal

Augusto A. V. Flores & Jose PaulaInstituto do Mar - Laboratorio Maritimo da Guia, Faculdade de Ciências da Universidade de Lisboa,Estrada do Guincho, 2750, Cascais, Portugal

Key words: intertidal zonation, rocky shores, species composition, brachyuran crabs

Abstract

The objectives of the present study are to describe and compare the brachyuran community of rocky shores withinthe Central Portuguese coast and to examine the zonation patterns of the most representative species. For this, ran-domly placed transects were surveyed to obtain crab counts according to microhabitat and intertidal level. Repeatedsampling in two different shores during two different seasons provided spatial and temporal replication for zonationanalyses. Seven species were registered: Pachygrapsus marmoratus, Eriphia verrucosa, Xantho incisus, Carcinusmaenas, Necora puber, Pirimela denticulata and Pilumnus hirtellus. Species density rankings are the same at bothlocalities, but the less exposed shore presents higher diversity. While most species are mainly confined to specificmicrohabitats in the lower level, P. marmoratus and E. verrucosa can exploit the whole intertidal range. Regardlessof shore and season, E. verrucosa is more abundant in the lower intertidal levels, while no such zonation patternswere recorded for P. marmoratus. Initial predictions concerning the effect of wave exposure and temperature on thezonation of those species are not validated after analysing the factorial model proposed. Between-shore contrastswere found instead, with higher densities recorded in the more exposed locality for both species. Possible causesof the observed patterns are discussed.

Introduction

In spite of several available studies on the distribu-tion of intertidal brachyuran crabs (e.g. Bacon, 1971;Griffin, 1971; Hartnoll, 1975; Jones, 1976; Wada,1983), there are no conclusive models explaining pop-ulation density as a function of key environmentalfactors related to desiccation potential. Such factorsare known to constrain the intertidal distribution ofsessile invertebrates in which comprehensive descript-ive models have been proposed and reviewed (seeLewis, 1964; Stephenson & Stephenson, 1970; Little& Smith, 1980; Rafaelli & Hawkins, 1996). Mobilefauna, however, may behave so as to minimise harshenvironmental conditions. In addition to the remark-able osmoregulatory capacity of certain crab species(Gross, 1964; Barnes, 1967; Schubart & Diesel,1998), locomotion may also allow the exploitationof different shelter resources (Cannicci et al., 1999),which may obscure eventual zonation patterns of theseorganisms.

As for sessile forms, most discussion has centeredon the nature of limiting factors that set the upperand lower boundaries of a given species distribution.In this sense, it has been argued that tidal exposuretime (McLay & McQueen, 1995) and substrate type(Menendez, 1987) may be the major factors causingzonation in brachyurans. However, there is evidence ofactive shelter exclusion (Navarrete & Castilla, 1990)and predator–prey interactions (Willason, 1980) actingas mechanisms of interspecific segregation.

In this study, we describe the composition of thebrachyuran fauna at two rocky shores in the Cent-ral Portuguese coast and examine their distributionaccording to microhabitat and intertidal level. The ver-tical zonation of the most common species was studiedin further detail by obtaining crab density estimates inreplicate samples at different shores and seasons. Byanalysing the factorial model, results concerning theeffect of temperature and wave exposure on zonationpatterns are presented and discussed.

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Materials and methods

The intertidal occupation patterns of brachyuran spe-cies were assessed by means of vertical transects overthe entire tidal amplitude exposed at diurnal spring lowtides. Within each transect, infra, meso and supra-littoral areas were delimited according to prevailingsessile communities (Hawkins & Jones, 1992), andcounts were recorded separately for each intertidallevel. Nine replicate transects were randomly assignedat each of two rocky shores located within the Lisbonregion, Cabo Raso (38◦ 42′ N; 09◦ 29′ W) and Avencas(38◦ 41′ N; 09◦ 21′ W), respectively, highly and mod-erately exposed to wave action, during two samplingseasons; winter (sampling dates centered on February,1998) and summer (centered on September, 1998).

Transect demarcation and crab counts

Transects consisted of 15 m wide sections placedrandomly on the shore, each providing three adja-cent sampling units corresponding to the differentintertidal levels. Due to particular characteristics ofeach sampling unit, namely the presence of sandypatches, topography constraints and slope, their actualsampling area varied from 40 to 450 m2. The size ofthe smallest sampling unit was, however, large enoughto minimize the effect of aggregation between con-specifics, thus allowing comparisons of density (cal-culated as individuals m−2) between units of differentsize.

Seven distinct microhabitats within the rockyshores were distinguished: rocky areas (includingcrevices), tide pools, algal canopy, mussel beds,cobbles, Sabellaria reefs and barnacle beds. Transectswere visually surveyed by a single observer. Timeeffort per sampling unit varied from 11 to 95 minaccording to their size. For each crab sight, the cor-responding species and associated microhabitat wererecorded. No methods other than visual inspectionwere used for crab recording.

Quantitative and statistical analyses

Shannon–Wiener Diversity indices were calculated foroverall counts at both shores and a t-test was usedto compare them as described in Poole (1974). Sincenatural logarithms were used in calculations, nits perindividual (Krebs, 1989) is the diversity unit usedhereafter.

The zonation patterns of the most representativespecies were analysed in a fully orthogonal model in

which ‘intertidal level’, ‘season’ and ‘shore’ are allfixed factors. Significance of main factors and theirinteractions were evaluated in a three-way ANOVA,and SNK tests were run for a posteriori comparis-ons. Data were square-root transformed to achievehomoscedasticity, as usually applied in Poisson-likedistributed variables (Underwood, 1997). Null hypo-theses were rejected at probabilities of type I errorlower than 0.05.

Results

Species composition and distribution

Seven species were recorded: Pachygrapsus mar-moratus (Fabricius), Eriphia verrucosa (Forskål),Xantho incisus (Leach), Carcinus maenas (Lin-naeus), Necora puber (Linnaeus), Pirimela denticu-lata (Montagu) and Pilumnus hirtellus (Linnaeus). Atotal of 2518 individuals were recorded, of which78.5% were to the grapsid P. marmoratus. Thexanthoids E. verrucosa and X. incisus made up 14.5and 5.5% of all sampled crabs respectively, while eachof the remaining species accounted for less than 1%.Despite its absence in the samples, the grapsid crabPachygrapsus transversus (Gibbes) was observed ona few occasions at Avencas and once at Cabo Rasoduring nocturnal low tides.

Species density rankings are the same at both loc-alities, but a higher diversity was found at AvencasBeach (H ′

av=0.7479; H ′cr=0.5776; df=1462; t=4.24,

p∼=0.000). This difference is mainly due to the pres-ence of P. denticulata and P. hirtellus and the higherrelative frequency of X. incisus at that site (Fig. 1).While most species are predominantly confined to spe-cific microhabitats in the lower level, namely tidepools and cobble areas (Table 1), P. marmoratus andE. verrucosa can exploit the whole intertidal range,preferably rocky crevices. A much reduced percentageof crab recordings was obtained in other potential shel-ter sources such as mussel and barnacle beds (Table 1)in spite of being these quite common at the study areas.

Zonation patterns of P. marmoratus and E. verrucosa

It was predicted that (1) zonation in these spe-cies would be less pronounced under conditions ofhigher wave exposure and (2) stratification wouldbe more conspicuous during the warmer season dueto physiologically stressful conditions in the upperlevels. Nevertheless, the factorial model analysed in

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Figure 1. Number of individuals recorded for each species at the shores sampled. Pm: Pachygrapsus marmoratus; Ev: Eriphia verrucosa; cm:Carcinus maenas; Xi: Xantho incisus; Np: Necora puber; Pd: Pirimela denticulata; Ph: Pilumnus hirtellus.

Table 1. Percentage of crabs recorded in each microhabitat for each species. Speciesabbreviations as indicated in Figure 1

Species Microhabitat

Rocky Tide Algal Mussel Cobble Sabellaria Barnacle

area pools canopy beds reefs beds

Pm 69.0 13.5 1.7 3.3 12.2 0.1 0.2

Ev 90.1 8.8 0.3 0.8 0.0 0.0 0.0

Cm 6.7 93.3 0.0 0.0 0.0 0.0 0.0

Xi 10.1 36.2 0.0 0.0 53.6 0.0 0.0

Np 0.0 87.0 4.3 0.0 8.7 0.0 0.0

Pd 0.0 100.0 0.0 0.0 0.0 0.0 0.0

Ph 0.0 100.0 0.0 0.0 0.0 0.0 0.0

Table 2. Three-way ANOVA describing intertidal density patterns of Pachy-grapsus marmoratus (Fabricius) and Eriphia verrucosa (Forskål). SV: sourceof variation; MS: mean square; L: (intertidal) level; S: season; Sh: shore

SV Pachygrapsus marmoratus Eriphia verrucosa

MS F-ratio p MS F-ratio p

Level 0.0039 0.39 0.6787 0.0029 4.45 0.0142

Season 0.0863 8.59 0.0042 0.0003 0.51 0.4761

Shore 0.0408 4.06 0.0466 0.0062 9.58 0.0026

L×S 0.0034 0.34 0.7156 0.0000 0.01 0.9909

L×Sh 0.0084 0.84 0.4361 0.0006 0.96 0.3879

S×Sh 0.081 8.06 0.0055 0.0004 0.61 0.4354

L×S×Sh 0.0036 0.36 0.6973 0.0002 0.26 0.7726

res. 0.01 0.0006

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Figure 2. Zonation pattern of Eriphia verrucosa (Forskål). Bars in-dicate standard errors. Density between intertidal levels sharing aletter is not significantly different (SNK tests; p>0.05).

Figure 3. Density of Eriphia verrucosa (Forskål) and Pachygrapsusmarmoratus (Fabricius) at the shores studied. Bars indicate stand-ard errors. Results from SNK tests indicated as follows; ns: notsignificant; ∗∗: p<0.01.

this study does not support the above hypotheses since‘level’ vs. ‘shore’ and ‘level’ vs. ‘season’ interactionsare not significant (Table 2). Regardless of shore andseason, the density of E. verrucosa is higher in thelower intertidal levels (Table 2, Fig. 2). This trendwas not observed in P. marmoratus, in which dens-ity among levels did not show significant differences.Between-shore contrasts were also found in both spe-cies, which depend on the season sampled in the caseof P. marmoratus as indicated by a significant ‘season’vs. ‘shore’ interaction (Table 2). While E. verrucosais clearly more abundant at Cabo Raso, this differencewas only significant during winter for P. marmoratus(Fig. 3).

Discussion

The brachyuran taxocenoses found at the study sitesare composed of two dominant warm temperate spe-cies, P. marmoratus and E. verrucosa, and fiveless common typical temperate species, using thebiogeographical classification proposed by d’Udekemd’Acoz (1999). These less abundant species are re-stricted to specific microhabitats within the lowerintertidal, as verified in this study, extending their ba-thymetric distribution to a few meters depth and occa-sionally to considerably deeper grounds (see ZariquieyAlvarez, 1968; Ingle, 1980; d’Udekem d’Acoz,1999). The presence of the subtropical species Pachy-grapsus transversus provides further indications offaunal affinity between the study area and other warm-temperate regions such as the Western Mediterranean.The significant difference found between diversity atboth sites is probably related to shore profile. At Aven-cas Beach, the infralittoral area exposed at spring lowtides may be notably larger because it extends over agently sloped rocky platform. Therefore, the relativedensity of species restricted to that level is greater atAvencas than at Cabo Raso, which explains the higherdiversity at the former shore due to higher speciesevenness. Abele (1974) found that number of sub-strates within a given habitat is the most importantfactor determining diversity of decapod crustaceansin marine habitats. Within a single marine habitat,however, the number of available substrates wouldbe less variable and diversity differences would bethus largely dependent on the area each substrate ac-tually covers. Using the present study as an example,tide pools is the only microhabitat where all recordedspecies were found (Table 1). If other conditions are

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considered to be equivalent, which may seldom be thecase, it could be expected that diversity of brachy-uran crabs in rocky shores enclosing larger pool areaswould be higher.

The values of species density presented hereshould only be considered valid for the specific pur-poses of this study. They are obviously underestim-ations since only visual sights were used for counts.Such bias would be more pronounced in cobble areas,where Xantho incisus is mainly found, and biogenicsubstrates where juvenile individuals of different spe-cies may remain concealed (Spivak et al., 1994;Flores & Negreiros-Fransozo, 1999). More accurateestimates would involve a combination of destruct-ive methods for sorting individuals from mussel beds,Sabellaria reefs and algal associations, and marking-recapture techniques such as those detailed in Begon(1979) to quantify crab abundance in the bedrock pop-ulations. Although beyond the scope of the presentstudy, gathering such information would be very valu-able since such data are still lacking.

Truly intertidal species, P. marmoratus and E.verrucosa are both capable of exploiting the wholeintertidal range at the shores studied. The present ac-count does not demonstrate an effect of temperatureor wave exposure on the zonation patterns of thosespecies. Yet, it should be pointed out that not allthe possible range of wave exposure conditions wascovered by the study design. A more comprehens-ive model should add one level to the ‘shore’ factor,namely by taking samples at a typical sheltered site,and include replication at all that levels for propercomparisons. If this still not demonstrate a ‘level’ vs.‘shore’ interaction it would more adequately indicatethat exposure probably does not influence the zonationof shore crabs at the study region. Further researchaddressing the effect of biotic variables on the distribu-tion patterns of these species would be equally usefulat present, namely the availability of suitable foragingareas. Shelter displacing experiments would also helpto verify whether competition for crevices between P.marmoratus and E. verrucosa exists under conditionsof shelter shortage.

Unlike P. marmoratus, which does not show anyzonation pattern at the study sites, E. verrucosa is sig-nificantly more abundant in the infra and mesolittoralzones than in the supralittoral. This contrast is hardlysurprising since the means by which grapsid andxanthoid crabs had been able to exploit the rocky shoreenvironment are quite distinct. Grapsids are knownto be active, fast-moving animals exploiting a wide

variety of food resources while intertidal xanthoidsare less active, slow-moving crabs often specialized toprey on a very restricted number of food items. WhilePachygrapsus may cope with high salinity variations(Alves, 1974) and osmoregulate under extreme con-ditions (Jones, 1941), low desiccation tolerance hadbeen recorded in the xanthoid Eurypanopeus depres-sus (Smith), which survive in the intertidal zone bybenefiting from the relatively moist shelter providedby oyster reefs (Grant & McDonald, 1979). Eriphiaalso shelters in very specific rock crevices (Vannini& Gherardi, 1979), usually only large enough to holdits occupant (AAVF, pers. obs.). Remaining in thesespecific refuges probably decreases the desiccationrates in those organisms, allowing them to reach thehigher intertidal. However, as observed in this study,xanthoids are mainly found in the lower reaches of theintertidal zone (e.g. Snelling, 1959; Pellegrino, 1984),while grapsids are frequently dominant in the supra-littoral (e.g. Hiatt, 1948; Little, 1990; Omori et al.,1997).

Between-shore density contrasts found in P. mar-moratus and E. verrucosa are clear. In the case of E.verrucosa, this difference is not seasonal, but a con-sistent trend. This species would depend on a suitablesupply of large rock crevices, since this may be alimiting resource in natural conditions (Beck, 1995),and relatively large areas per individual, as agressiveinteractions prevent conspecifics from sharing a com-mon shelter (Warburg & Schwartz, 1989). Althoughfar from its carrying capacity, it was apparent thatthe proportion of potential crevices actually occupiedby crabs was higher at Cabo Raso than at Aven-cas, resulting in the differences found. Causes of thisdensity contrast are still unclear, but anthropogenicimpact may account for at least part of such differ-ence, considering that Avencas Beach is closer to sitesof pollutant discharge along the Tagus estuary andis more exposed to human collecting activities. Lackof between-shore differences in summer for P. marm-oratus is very probably related to seasonal processesoccurring in this species’ populations. Recruitment ofyoung crabs during late autumn – early winter (Flores& Paula, unpublished) seems to be the main factorcontributing to the population increase in this season.Mortality in very young crabs would probably renderits effect by summer, when abundance might be farbelow the species potential at both sites. This possib-ility would indicate that recruitment rates are higher atCabo Raso, a question that needs to be addressed byspecific research.

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Acknowledgements

The authors would like to thank R. G. Hartnoll, C.d’Udekem d’Acoz and S. Cannicci for their helpfulcomments on the manuscript and C. Micheletti Floresfor her valuable assistance during field work. We arealso grateful to the “Fundação para a Ciência e Tecno-logia”, which conceded a PhD fellowship to AAVF.This study was developed within the Task A of EUMAST 3 project “Eurorock – Interactions of Physicaland Biological Factors in the Surf and Swash Zone ofEuropean Rocky Shores”.

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