ORIGINAL ARTICLE

Luis Giménez Æ Ana Inés BorthagarayMarcel Rodrı́guez Æ Alejandro BrazeiroCaterina Dimitriadis

Scale-dependent patterns of macrofaunal distribution in soft-sedimentintertidal habitats along a large-scale estuarine gradient

Received: 3 January 2005 / Revised: 12 April 2005 / Accepted: 14 April 2005 / Published online: 1 June 2005� Springer-Verlag and AWI 2005

Abstract We investigated the pattern of distribution ofintertidal soft-bottom fauna in streams and lagoons ofthe Uruguayan coast at three spatial scales. The Rı́o de laPlata and the Atlantic Ocean produce on this coast alarge-scale gradient in salinity, defining a freshwater(west), an estuarine (central) and a marine (east) region.Within each region, there are several streams and coastallagoons (sites) that define a second scale of variability. Athird scale is given by intertidal gradients within eachsite. Species richness and total abundance was low in thefreshwater west region and high in the central and eastregions. The community in the west region was charac-terized by the clam Curbicula fluminea; in the other re-gions, it was dominated mainly by the polychaeteHeteromastus similis. The polychaete Nephtys fluviatiliswas more abundant in the east region, while anotherpolychaete, Laeonereis acuta, characterized the centralregion. Sediment fractions did not vary significantly atthis scale. At the scale of the sites, species richness andtotal macrofaunal abundance were higher in coastal la-goons than in streams. Coarse sands were more commonin coastal lagoons, while medium and fine sand charac-terized the sediment in streams. Within each site, speciesrichness and total abundance increased towards thelower intertidal level; the macrofauna of the upper levelswere a subsample of the fauna occurring at the lower

levels. There was also a significantly lower proportion offine sand at the upper level. At regional scales, the ob-served patterns may be indirectly or directly related tothe gradient in salinity, through differential physiologicaltolerance to osmotic stress. At the scale of the sites,variability may be explained mainly by geomorphologi-cal and sedimentological differences between lagoonsand streams. Variation among levels may be related togradients in desiccation, colonization and predation.

Keywords Biodiversity Æ Macrobenthos Æ Estuarinefauna Æ Scale dependence

Introduction

Most ecological theories rely on the study of small-scalepatterns of distribution of animals and plants; however,the patterns of distribution change with the temporaland spatial scale of observation (Wiens 1989; Schneider1994). Scale-dependent patterns of distribution havebeen increasingly evidenced in studies of benthic fauna(Thrush et al. 1997, 2003; Giménez and Yannicelli 2000;Ysebaert and Herman 2002). An evaluation of thesepatterns is the first step to understand the set of pro-cesses that structures the communities and thus to for-mulate predictive models (Underwood et al. 2000).

Scale-dependent patterns of distribution may beparticular important in coastal areas since they arecharacterized by a high spatial and temporal variabilityin abiotic conditions. For benthic fauna, the patterns ofdistribution are related to depth, salinity (Remane andSchlieper 1971; Wolff 1983; Holland et al. 1987;Mannino and Montagna 1997; Ysebaert et al. 1998,2003; Atrill 2002; Attrill and Rundle 2002), sedimentcharacteristics (Gray 1981; Day et al. 1989; Teske andWooldridge 2001, 2003; Anderson et al. 2004) amongothers. For instance, low salinity and/or variability insalinity are responsible for a consistently low number ofspecies occurring in estuarine waters as compared with

Communicated by H.-D. Franke

L. Giménez Æ A. I. Borthagaray Æ M. Rodrı́guezC. DimitriadisFacultad de Ciencias, Sección Oceanologı́a, Iguá 4225,Montevideo, Uruguay

L. Giménez (&)Biologische Anstalt Helgoland,Alfred Wegener Institute for Polar and Marine Research,27498 Helgoland, GermanyTel.: +49-4725-819361Fax: +49-4725-819369

A. BrazeiroDepartamento de Ecologı́a, Facultad de Ciencias, Montevideo,Uruguay

Helgol Mar Res (2005) 59: 224–236DOI 10.1007/s10152-005-0223-9

freshwater- or ocean-influenced habitats. However, thepatterns may be more complex due to spatial heteroge-neity in the distribution of substrate types. Apart fromany effect produced by a gradient in intertidal height, ahigher level of complexity may arise in intertidal zones ifthey are located directly on the coast or on streams,rivers, or lagoons that are open to the oceanic coast or toan estuarine zone.

Therefore, for the case of large estuarine areas such asthe Rı́o de la Plata in South America, studies on patternsof distribution in relation to physical gradients involveconsideration of various spatial scales of variability. Nostudy about the benthic fauna has covered a spatial scalelarge enough to include the whole environmental gra-dient of the estuary. The Rı́o de la Plata estuary (Fig. 1)is one of the largest estuaries of South America, with ariver funnel of 280 km in extent and 80–230 km in cross-section (Guerrero et al. 1997; Mianzan et al. 2001). Atthe northeast side, the Uruguayan coast, with a tidalrange of less than 0.3 m, is characterized by a large-scalegradient caused by the estuary flowing into the AtlanticOcean. The gradient defines an upper region of highlyturbid waters with salinity

the scale of regions, we investigated the variability ofmacroinfauna in relation to the above-described large-scale salinity gradient. As a potential source of among-site variability, we explored if there were differences be-tween coastal lagoons and streams. We also exploredpotential relationships between sediment characteristicsand macroinfauna at all scales of variability.

Methods

Sampling design

We sampled three sites at random in each of the above-defined regions (Fig. 1) in the spring of 2002, at low tide.Each site consisted of a stream or a coastal lagoon opento coastal waters. The sites were from west to east, LaCaballada, Rosario, Santa Lucı́a (for the west region);Pando, Solı́s Grande, Maldonado (central region);Garzón, Rocha and Valizas (east region). The sitesGarzón and Rocha are coastal lagoons; the other sitesare streams. The most common habitats at these sites arenarrow (

and CAP. For these multivariate analyses, data was log(X+1) transformed; the similarity matrix was built withthe Bray–Curtis index. Then, we performed univariatetwo-way nested ANOVAs with the most importantspecies to test for effects of regions and sites, and plan-ned comparisons to test for differences between lagoonsand streams. We used log (X+1)-transformed datasince, unlike untransformed data, they were homoge-neous and normally distributed. For core samples, wetested if species richness and total abundance variedamong intertidal levels with repeated-measures ANO-VA. In these tests, we excluded Caballada and Rosariosince almost no macroinfauna was found at these sites(see Results).

Relationships between species richness and salinitywere analysed with single and multiple Pearson corre-lation and regression. Relationships between granulo-metric data and fauna were investigated by correlatinggranulometric fractions and the two main axis of prin-cipal coordinate analysis (PCO) done on the speciesmatrix and by multiple Pearson correlation of abun-dance of each species and the proportion of the maingranulometric fractions.

Results

Salinity and granulometric fractions

Salinities were lower than 1 ppt at the freshwater ex-treme (La Caballada, Rosario and Santa Lucı́a); at thesites open to estuarine waters it ranged from 1 ppt(Pando stream) to 15 ppt (Maldonado stream) while atthose open to oceanic waters it ranged from

opseudes schubarti was found only at Solı́s stream. Otherspecies were seldom sampled: the deep burrowing razorclam Tagelus plebeius was found in only one site, but itmay not be well sampled by the corer used here; thepolychaete Neanthes succinea and mussels Brachidontesspp were found very seldom, but they are more commonon rocky shores (Giménez et al. in preparation); thesame occurred with the isopod Excirolana armata, acharacteristic species of sandy beaches (Giménez andYannicelli 1997).

Drop–trap samples contained mostly crustaceans andmolluscs; nine species comprised more than 95% of the

Fig. 2 Variation of the maingranulometric fractions ofunvegetated sandflats along theUruguayan coast of the Rı́o dela Plata and the Atlantic Ocean(a); biplot of Canonical analysisof principal coordinates to lookfor variation in sedimentfractions among sites (b).Abbreviations of sites areCa Caballada, Ro Rosario;Sa Santa Lucı́a, Pa Pando,So Solı́s Grande, MaMaldonado, Ga Garzónlagoon, Ra Rocha lagoon,Va Valizas

Table 1 Contribution of each granulometric fraction to the for-mation of the two principal factors obtained from a principalcomponent analysis

Factor I (47.23%) Factor II (33.58%)

Gravel 0.235 0.249Coarse sand 0.011 0.066Medium sand 0.698 0.007Fine sand 0.058 0.678Mud

collected individuals (Table 4). The barnacle Balanusimprovisus, the hydrobiid gastropod Heleobia cf australisand the bivalve E. mactroides were the most abundantand widespread species comprising more than 75% ofthe collected organisms and occupying more than 50%of the sampled sites. Abundance of these species varied

significantly among sites but not among regions, withpeaks at the coastal lagoons (Table 5; Fig. 6). The samepattern was found for the isopod Dies fluminensis andthe crab Cyrtograpsus angulatus. The abundance of thetanaid Sinelobus stanfordi was significantly higher in theeast region, and in the coastal lagoons within that

Table 2 Summary of two-wayANOVA to evaluate the effectof intertidal level on the (arcsintransformed) percentage of themain sediment fractions foundat nine sandflats along theUruguayan coast

Gravel Medium sand Fine sand

F P F P F P

Level 6.25

region. All these species contributed to separate thecentral from the east region in CAP analysis (Table 4;Fig. 4). Other species such as Jassa falcata and Pseu-dosphaeroma platensis did not vary significantly amongsites or regions although they tended to increase fromwest to east. The bivalve Corbicula fluminea was onlypresent in the west region, contributing to separate itfrom the other regions in CAP (Table 4; Fig. 4).

The species richness and the total abundance ofmacroinfauna collected from core samples were signifi-cantly lower at the upper level of the sandflats as com-pared with the middle and lower levels (Table 6).Among the polychaetes, H. similis had significantlylower abundance at the upper level, while L. acuta didnot show any significant trend. For N. fluviatilis, the testfor the effect of levels was possible using data from thecoastal lagoons: at these sites, they were significantly lessabundant at the upper level.

Relationships between environmental variablesand macrofauna

Correlations between the recorded salinity and speciesrichness were not significant. Significant correlationswerefound only for the total faunal abundance from coresamples (r = 0.74, P

richness, total abundance (not including barnacles),Erodona mactroides, Heleobia australis, Cyrtograpsusangulatusand Jassa falcata (Table 7). The significantcorrelations were determined mainly by the high per-centage of coarse sand in the coastal lagoons.

Discussion

This is one of only a few studies examining spatial var-iation in estuarine macrofauna at different spatial scales

(see Ysebaert and Herman 2002). We used a nested de-sign to study variation among regions and sites. Thiswas a requisite to examine the patterns of macrofaunaldistribution in streams and coastal lagoons locatedalong the salinity gradient produced by the Rı́o de laPlata and the Atlantic Ocean, since several sources ofvariability occur at different spatial scales.

A low number of species were found in the soft-sed-iment estuarine sites. This is consistent with generaltrends in the estuarine fauna all over the world. Speciescomposition was consistent with earlier studies on theUruguayan coast (Muniz and Venturini 2000; Cardezo1989; Jorcin 1999). Species composition was also similarto that of Patos lagoon (Capitoli et al. 1978; Seeliger2001) and Samborombom bay on the Argentinean coastof the estuary (Ieno and Bastida 1998). Species compo-sition differed from that observed in the sandy andmuddy bottoms of the Rı́o de la Plata (8–40-m deep:Mianzan et al. 2001; Giberto et al. 2004), suggesting adepth-related zonation pattern. Species richness on theUruguayan coast seemed to be higher than the one re-ported by Ieno and Bastida (1998) for Samborombombay. The fact that we used a drop–trap allowed us toestimate the abundance of several mobile epifaunalspecies and infaunal species with low abundancebut buried within the first centimetre of sediment. Thedrop–trap is much better suited to collect mobile epi-benthos than core sampling; this was the first time thistechnique was used in Uruguay.

Species richness, total abundance and species com-position varied among regions, among sites within re-gions and among levels within sites. These patternssuggest a scale-dependent set of processes operatingalong the estuarine benthic communities of Uruguay, asfor other estuaries (Ysebaert and Herman 2002; Thrushet al. 2003) and intertidal communities (Thrush et al.1997; Giménez and Yannicelli 2000). The observedpatterns should be related to (1) the salinity gradientproduced by the Rı́o de la Plata and the Atlantic Oceanat a regional scale, (2) morphological and/or sedimen-tological differences among lagoons and streams orrivers at the scale of sites and (3) the gradient in desic-cation and colonization rates of sediments at the scale ofintertidal levels.

Variability among regions

The influence of the Rı́o de la Plata and the AtlanticOcean defines three main regions on the Uruguayancoast: a west region with a salinity of 30 ppt). Salinitywithin the estuarine areas studied by us may be co-determined by the freshwater from the basin of eachstream and lagoon and from the water masses enteringthrough the mouth. Differences in salinity between thewest and central regions recorded by us were consistentwith the regional pattern of salinity explained above. In

Fig. 5 Spatial variation in abundance of the main infaunalpolychaetes collected with core samples. Symbols as in Fig. 2;error bars are standard errors

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the east region, the Valizas River had a low salinity,reflecting the influence of water discharge at the time ofsampling.

The fact that the sites in the west region are open tofreshwater or low-salinity brackish water explains thespecies composition: one of the dominant species atCaballada and Santa Lucı́a was the freshwater clamCorbicula fluminea. Communities may be differentiatedif they have clear habitat boundaries, if they are char-acterized by dominant indicator species, if there is astrong interaction among species or if it is possible toidentify an assemblage (Morin 1999). Following thesecriteria, the species found at La Caballada should con-stitute a community characterized by C. fluminea anddifferentiated from the estuarine community of othersites that are characterized by the polychaete Hetero-mastus similis. The site Santa Lucı́a should be part of theecotone or ecocline (Attrill and Rundle 2002) betweenfreshwater and estuarine communities: at this site, both

freshwater and estuarine species may be near the limit oftolerance to osmotic stress. Also for the salt marshcrab Chasmagnathus granulata, Santa Lucı́a seems tobe the western limit of distribution (Giménez 2003),due to effects of osmotic stress on the survival ofbenthic or pelagic stages. Within the estuarine com-munity, differences between the central and the eastregion involved changes in abundance of the mainmacrofaunal species rather than changes in speciescomposition. While the polychaete Laeonereis acutawas more abundant in the central region, the poly-chaete Nephtys fluviatilis was more abundant in theeast region.

According to the model of Remane and Schlieper(1971), we expected to find the highest number of speciesat the west region especially at the sites permanentlybathed by freshwater (La Caballada and Rosario). Thus,the prediction of higher number of species at the fresh-water extreme does not seem to apply for the sandflats

Table 4 Benthic macrofauna ofunvegetated sandflats atstreams and lagoons along theUruguayan coast collected withcorer and drop–trap

Percentage of occurrence (%),number of sites occupied (N)and contribution (correlation)of main species to the first twocanonical variables (C-1 andC-2) obtained from CAPmaximizing differences amongregions

Taxon/species Core samples Drop–trap samples

Polychaeta % N C-1 C-2 % N C-1 C-2

Heteromastus similis 28.44 7 0.38 0.56 0.81 4Laeonereis acuta 22.01 7 0.69 0.12 0.17 4Nephtys fluviatilis 16.48 7 �0.39 0.74 3.32 5CrustaceaBalanus improvisus 6.23 1 �0.18 0.58 50.61 5 0.43 �0.44Pseudosphaeroma platensis 10.15 5 �0.08 0.37 6.43 4 0.55 �0.20Dies fluminensis 1.11 2 �0.14 0.60 7.99 3 0.43 �0.44Kalliopseudes schubarti 4.92 1 0.45 �0.11 0.01 1Sinelobus stanfordii 0.70 4 �0.33 0.37 1.51 2 0.42 �0.40Jassa falcata 0.50 4 0.28 0.10 0.83 6 0.43 �0.11Cyrtograpsus angulatus 0.10 1 1.38 6 0.25 �0.07Neomysis americana 0.20 1 1.03 2 0.04 0.52Prawn indet 0.26 2 �0.53 �0.13Ostracoda indet 0.10 2 0.18 �0.19MolluscaHeleobia cf australis 1.21 5 �0.38 0.04 14.54 6 0.35 �0.56Erodona mactroides 5.43 5 �0.30 0.59 9.70 5 0.43 �0.36Corbicula fluminea 0.10 1 0.17 2 �0.70 �0.28Planorbis sp. 0.07 2 0.13 0.14Hirudinea indet 0.20 2 0.03 1 0.20 �0.16LophophorataMembranipora sp. 0.17 1 0.25 �0.18InsectaInsect indet 0.24 2 0.16 �0.03

Table 5 Univariate two-way ANOVAs to evaluate the effect of region and site (nested on region) on the three most common macro-benthic species sampled with corers and drop–trap. Data for were log (X+1) transformed before analyses

Factor df MS F P MS F p MS F p

Corers H. similis Nephtys fluviatilis Laeonereis acutaRegion 2 16.7 10.2 0.01 14.9 6.61 0.03 13.01 23.9

located in streams and rivers along the coast ofUruguay. That model was developed for subtidal mud-dominated sediments, and it may not apply for sandyintertidal environments or for a series of small rivers andlagoons, that are subjected to their own salinity gradi-ents. We did not find any significant variation in sedi-ment fractions among regions.

Variability among sites

Considerable variability in macrofaunal abundance,diversity and composition occurred among sites, andwas related to the differences between coastal lagoonsand streams. Most epibenthic species were more abun-dant at Rocha and Garzón lagoon than at streams. Thepatterns of species composition and abundance ofestuaries in South Africa were associated with differ-ences in estuarine morphology and their open/closedregime (Teske and Woodridge 2001, 2003): permanentriver-dominated open estuaries had lower densities andspecies richness than open/closed estuaries. On theUruguayan coast, Jorcı́n (1999) found a considerablereduction in the number of species at the Valizas streamas compared with Castillos lagoon, located upriver.Coastal lagoons differ from streams and rivers in twoimportant aspects: (1) their intermittent connection withthe sea, and (2) their morphology. In addition, we founda third difference, the sediment composition: while mostof the streams were dominated by fine to medium sand,coastal lagoons were dominated by coarse sand togravel.

The present data do not allow for an evaluation ofwhich factor determined the observed differences be-tween the lagoons and streams: they may be influencedby a large number of community and biological pro-cesses. For instance, both the intermittent connection tothe sea and the morphology should affect the rate ofdisturbance of bottom habitats: in streams and rivers,the channel-like morphology and the permanent contactwith open waters should lead to bottom water erodingthe intertidal habitat more frequently. In the lagoons,the morphology ensures that an extensive portion ofsandflats are located in protected bays, while the inter-mittent connection with the sea ensures a reduction inthe frequency of disturbance and export of organismstowards the sea. The intermittent nature of the lagoonsmay also reduce biological disturbance by marine-fishpredators if it restricts their frequency of invasion. Theeffect of both physical and biological disturbance shoulddepend on life history and other adaptations. The effectof disturbance should be higher on epibenthic crusta-ceans and gastropod molluscs, explaining their reducednumber in streams as compared to lagoons. Erosion orpredation should affect also the shallow burrower Ero-dona mactroides (Capitoli et al. 1978) explaining itshigher abundance in coastal lagoons. The predatorpolychaete Nepthys fluviatilis, supposed to reduce theabundance of small macroinfauna from the upper cen-timetres of the sediment layers (Bemvenuti 1988, 1994),should be affected in the same way. However, theinfaunal worms such as L. acuta and H. similis, commonin streams and lagoons bury deeper in the sediment: theyshould not be affected as much by erosion as the before-mentioned species. Deep burying in H. similis may ex-plain the lack of relationship between its abundance andthat of N. fluviatilis in laboratory and field experiments(Bemvenuti 1988). Limited erosion and higher abun-

Fig. 6 Spatial variation in abundance of the main species collectedwith drop–trap samples. Symbols as in Fig. 2. Error bars arestandard errors

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dance of E. mactroides in coastal lagoons may explainwhy shells of E. mactroides are more commonly depos-ited on lagoonal sandflats, while in streams, they arefrequently transported to open waters. This deposition

seems to favour the establishment of the estuarine bar-nacle Balanus improvisus.

It is well known that macrobenthic fauna respond tosediment composition, but most of the responses arerelated to the proportion of the mud fraction (Gray1981; Thrush et al. 2003). In our sites, that proportionwas rather low, and most of the macroinfaunal changeswere associated with the proportion of coarse sand andgravel found in the coastal lagoons. Coarse sands aremore penetrable than fine sands allowing perhaps epi-faunal species or errant polychates to bury and movemore easily in the sediments.

Variability among intertidal levels

In our study, we did not find any pattern of zonation,but an increase of species richness and total abundancefrom the upper to the lower stations. The only exceptionmay be the barnacle Balanus improvisus that occurs in avery well-defined belt as a consequence of the patterns ofdeposition of Erodona mactroides shells. In somestreams, Chasmagnathus granulata and the fiddler crabUca uruguayensis occupy part of the upper level of thesandflats (LG, personal observation), but this does notoccur at all places. Chasmagnathus granulata occurs

Fig. 7 Animal-sedimentrelationships shown bysemipartial correlationsbetween the first two axes of theprincipal coordinate analysis ofspecies data and the maingranulometric fractions

Table 6 Univariate two-way ANOVA to evaluate the effect of level and site on total abundance and the distribution of the mainmacroinfaunal species collected with core samples. Data of total abundance and of Heteromastus similis and Laeonereis acuta were log(X+1) transformed

df MS F p MS F P

Factor Species richness Total abundanceSite 6 12.58 3.43 0.016 6.56 3.11 0.024Error 21 3.67 2.11Level 2 10.37 3.57 0.037 6.99 6.45 0.003Level·Site 12 2.22 0.76 0.683 0.97 0.89 0.560Error 42 2.90 1.08

Heteromastus similis Laeonereis acutaSite 5 2.62 1.75 0.17 1.56 1.33 0.294Error 18 1.50 1.17Level 2 10.77 18.72

mostly in the salt marshes located beyond the upperlevels of the sandflats. This is in contrast to the patternsof community structure of Uruguayan and other ex-posed oceanic microtidal sandy beaches (Defeo et al.1992; McLachlan and Jaramillo 1995; Brazeiro andDefeo 1996; Giménez and Yannicelli 1997). Macrofaunaof several tidal flats also follow a zonation pattern (Reise1991; Dittman and Vargas 2001), but these have a widertidal range (>1–9 m) and extension as compared withthe sandflats studied here. Our results may be the con-sequence of the resolution of our sampling design, whichwas too low to detect small-scale patterns of distributionacross the sandflats. Ongoing research on Rocha lagoonusing a sampling design with higher resolution did notfind a consistent pattern of zonation across the sandflats(L. Giménez unpublished data; Dimitriadis et al. 2002);future publications will focus on this topic.

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