CSIRO PUBLISHING

Marine and Freshwater Research, 2007, 58, 194–203 www.publish.csiro.au/journals/mfr

Changes in distribution and abundance of juvenile fishesin intertidal soft sediment areas dominated by the burrowingcrab Chasmagnathus granulatus

Paulina MartinettoA,B,C, Pablo RibeiroA,B and Oscar IribarneA,B

ALaboratorio de Ecología, Departamento de Biología (FCEyN), Universidad Nacional de Mar del Plata,CC 573 Correo Central (7600), Mar del Plata, Argentina.

BConsejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.CCorresponding author. Email: pmartin@mdp.edu.ar

Abstract. Intertidal estuarine areas located between southern Brazil and the northern Argentinean Patagonia are charac-terised by extended beds of the burrowing crab Chasmagnathus granulatus. Their activity leads to profound changes in thestructure, quality and dynamics of sediments, which affect the entire benthic community and create a patchy distributionof resources for other species. In this study, the differences in habitat use by juvenile fishes above soft sediments inhabitedby C. granulatus were evaluated. Adjacent areas with (‘crab beds’) and without crab burrows in intertidal mudflats of theMar Chiquita Coastal Lagoon (37◦32′S, 57◦19′W) were sampled seasonally from 2000 to 2002. There were more fishspecies in crab-bed areas. Abundances of benthivorous and planktivorous fishes were also higher in crab beds during floodtide; however, during ebb tide, planktivorous fishes were more abundant outside crab-bed areas, whereas benthivores didnot vary between areas. The present study demonstrated that species composition and abundance of juvenile fishes canbe affected by the presence of bioturbator species such as C. granulatus.

Additional keywords: Argentina, bioturbation, burrowing crab, estuaries, fish habitat use, mudflats.

Introduction

Habitat structure plays an important role in habitat use by fishes.Studies in estuaries have shown that the presence of physicalstructures is important as refuge and foraging habitat for juvenilefishes (Rozas and Minello 1998; Rozas and Zimmerman 2000).Such studies have generally compared small-scale habitat use byfishes in vegetated v. non-vegetated shallow estuarine areas, doc-umenting the role of seagrasses and saltmarshes as nursery areas(e.g. Rozas and Minello 1998; Hindell et al. 2000; Rozas andZimmerman 2000; Jackson et al. 2001). However, there is lim-ited information on how fishes use soft sediment estuarine areaslacking structural vegetation in areas where there is strong envi-ronmental heterogeneity, often owing to sediment bioturbation(see Snelgrove et al. 2000; Thompson 2004).

In the South-western Atlantic (from 32◦S in southern Brazilto 42◦S in northern Argentinean Patagonia), estuaries are char-acterised by the presence of the burrowing crab Chasmagnathusgranulatus (e.g. Boschi 1964; Spivak et al. 1994; Iribarneet al. 1997; Bortolus and Iribarne 1999). This bioturbatorinhabits the intertidal zone from the soft bare sediment tothe salt marsh vegetated by cordgrasses (Boschi 1964). Indi-viduals reaches a size of up to 60 mm in carapace width,excavating large semi-permanent open burrows and generat-ing discrete patches of burrowing assemblages that are oftenof many hectares (e.g. Spivak et al. 1994; Iribarne et al. 1997;Iribarne et al. 2003). Density can exceed 60 crabs m−2, andtheir burrows can extend 1 m into the sediment with a surface

opening of up to 30 cm diameter (Iribarne et al. 1997). Theiractivity leads to profound changes in the structure, quality anddynamics of the sediment, generating a patched distribution ofresources with concomitant effects on the entire benthic com-munity (e.g. Botto and Iribarne 1999). The burrowing bedsaffect the habitat use and foraging activity of shorebirds (Bottoet al. 1998, 2000; Palomo et al. 2003; Iribarne et al. 2005),feeding behaviour of polychaetes (Palomo et al. 2004), habitatuse of another grapsid crab (Cyrtograpsus angulatus, Irib-arne et al. 2003; Martinetto 2006) and the fiddler crab Ucauruguayensis (Daleo et al. 2003) and predator–prey interactionbetween juvenile fishes and their benthic prey (Martinetto et al.2005).

Like other estuaries worldwide, the South-western Atlanticestuaries are important nursery and feeding areas for fishes (e.g.Diaz de Astarloa et al. 1999; Cousseau et al. 2001), and the largeburrowing assemblages may affect the habitat use by fishes. It isknown that the distribution of fishes in an estuary is associatedwith how fish respond to physical and chemical characteristics oftheir habitat. Some estuarine fishes feed exclusively on benthicinfauna, and their distributions depend on the distribution ofthe benthos (Little 2000). Moreover, benthic species are moreimportant prey in the diets of fishes collected from mudflatsthan in the diets of fishes from other intertidal habitats (Nortonand Cook 1999). Any effect on the behaviour, availability orabundance of benthic infauna will also affect the diet, and likelythe habitat use by fishes foraging in these areas. Thus, it is likely

© CSIRO 2007 10.1071/MF06079 1323-1650/07/020194

Fish habitat use in intertidal soft sediments Marine and Freshwater Research 195

that the large beds produced by burrowing species such as crabsand shrimps will affect the habitat use by fishes.

In the present study, we evaluated whether the presence andactivity of the burrowing crab C. granulatus affected habitat useby juvenile fishes in an estuarine soft-sediment environment.With this purpose, we compared species composition, abundanceand size of juvenile fishes in paired areas with and without crabburrows, and related these variables to particulate organic matter(POM) concentrations in the water column and availability ofbenthic prey in both areas.

Materials and methodsStudy siteThe study was conducted at Mar Chiquita Coastal Lagoon(Argentina: 37◦32′S, 57◦19′W). This is a body of brackish water(∼46 km2) affected by a microtidal regime (≤1 m) and charac-terised by mudflats surrounded by a large cordgrass (Spartinadensiflora) area (Fasano et al. 1982; Bortolus and Iribarne 1999).Freshwater contribution comes from several creeks that runthrough the Buenos Aires Province, ending in the coastal lagoon

Fig. 1. Photographs showing a (a) Chasmagnathus granulatus crab bed, (b) C. granulatus burrow and (c) nearbyintertidal areas without crab burrows. Photo credits: P. Martinetto (a, b), F. Botto (c).

(Piccolo and Perillo 1999). Chasmagnathus granulatus inhabitboth S. densiflora areas and mudflats, but the present study waslimited to open intertidal mudflats, which is the only habitatregularly flooded daily by tides. In both areas, crabs generatespatially discrete burrowing beds (see Fig. 1 for an example inmudflats) that are easily identifiable and spatially stable overperiods of years (see Iribarne et al. 1997; Botto and Iribarne1999; Escapa et al. 2004; Martinetto et al. 2005). Densitieswithin these beds may vary depending on season, recruitmentor environmental fluctuations, but their location remains stable.Samples were collected in the low intertidal near the mouth ofthe lagoon and in similar paired areas with active bioturbation bycrabs (hereafter ‘crab beds’) and without the presence of crabs(hereafter ‘outside crab beds’; Fig. 1; see also Iribarne et al.1997, 2000). The selected paired areas represent similar tidalheights and general characteristics, and were used in previousstudies that contrasted the effects of crab beds (e.g. Botto andIribarne 1999; Escapa et al. 2004; Martinetto et al. 2005).

Given that the present study focused on variation in fish abun-dances dependent on presence or absence of crab burrows, oursampling design and subsequent statistical analysis was planned

196 Marine and Freshwater Research P. Martinetto et al.

on the basis of a two-habitat comparison. For this purpose, twosimilar paired areas (one crab bed and one outside crab bed) weresampled monthly during three austral summers (2000, 2001 and2002), two springs (2000 and 2001) and two winters (2001 and2002). Given that finding more than two similar paired areaslarge enough to be seined and used as replicates was unfeasi-ble, we took samples during three to five consecutive days eachmonth from the same sites. Pairs of samples from the two typesof habitats were collected on the same day.

Spatial and temporal variability in food for fishesand environmental factorsTo compare food availability for fishes and environmental char-acteristics between habitats, we measured POM, polychaetedensity, water salinity and crab burrow density. In both habitats,we measured POM by filtering 1 L of estuarine water throughpre-combusted GF/C Whatman filters (4.7-cm diameter, 1.2-µmpore). Filters with samples were dried at 60◦C, weighed, incin-erated at 500◦C for 6 h, and weighed again. POM was measuredas ash-free dry weight (Crisp 1971). In all cases, water sampleswere collected at 0.5-m depth and 0.5 m above the sediment dur-ing flooding and ebbing tide, on the same days that fish werecollected.

To evaluate benthic food source, 10 sediment samples fromeach habitat were obtained with a core (10-cm diameter × 10-cmdepth, sieved through a 0.5-mm mesh) concurrently with fishsampling from June 2001 to July 2002. Organisms retained inthe sieve were identified and counted.

Salinity was measured in the different areas and tidal stateson each sampling occasion. Since there were no differences insalinity between areas and tidal state on each sampling occasion,the data were pooled by month.

To evaluate whether burrow density varied over time, burrowabundances were measured each on sampling occasion in crab-bed habitat during low tide by counting the number of burrowsinside ten randomly distributed squares (1 × 1 m).

Spatial and temporal variability in species compositionand abundance of juvenile fishTo evaluate whether species composition and abundance of juve-nile fishes vary over time and between areas with and withoutcrab burrows, fish were collected using a beach seine (1-cmmesh size), towed for 50 m parallel to the shore. The seine wastowed by two people handling a 7-m rope in order to maintaina constant net opening (thus covering 350 m2 each time). Sam-ples were taken during flooding tide (1 h before high tide) andebbing tide (1 h after high tide) to compare the relative abun-dances of each fish species in both areas between tidal states.After each tow the captured individuals were identified, countedand measured (total length, accuracy 0.5 mm). The abundancesof total juvenile fishes and the numerically dominant specieswere compared among habitats and months.

Spatial and temporal variability of fish trophic groupsTo evaluate if the main fish trophic groups have differentresponses to areas and tide, fishes were categorised as eitherplanktivorous (Brevoortia aurea; Giangiobbe and Sanchez 1993;

Ramnogaster arcuata; Cousseau et al. 2001; Odontesthes argen-tinensis <8 cm TL; Martinetto et al. 2005) or benthivorous(Micropogonia furnieri; Hozbor and García de la Rosa 2000;Pimelodella laticeps and O. argentinensis >8 cmTL; Martinettoet al. 2005). Differences in the abundances of planktivorous andbenthivorous fishes between crab beds and outside crab bedsduring flood and ebb tide were tested.

To evaluate whether densities of polychaetes and crab bur-rows, POM concentrations and tidal state (flooding or ebbing)account for the variation in the abundance of both planktiv-orous and benthivorous groups of fishes, linear models wereconstructed following Neter et al. (1991).

Spatial and temporal variability in juvenile fish sizesTo test whether the sizes of the numerically dominant speciesdiffered between habitats, the mean sizes of each species werecontrasted. In the particular case that size distribution presenteda clear bimodal shape showing two class sizes without overlap,the distribution was separated into two and tested independently.

Statistical analysisWe considered days within a month as replicate samples, andall our analyses were performed using repeated-measures one-way (for salinity and burrows density) and two-way (for POM,polychaetes and fish abundances) ANOVAs with time (months)as the repeated measure (Zar 1999). Given weather constrains,the number of samples differed among months, especially inwinter months, and thus data were unbalanced. For this reason,we used repeated-measures ANOVAs Type III for unbalanceddata (see Shaw and Mitchell-Olds 1993). When the interac-tion between factors was significant, planned comparisons wereconducted to identify how factors interacted (Zar 1999). If inter-action effects were not present, main effects were analysed.When ANOVA assumptions were not met, transformation wasapplied as necessary (following Underwood 1997).

To evaluate whether food abundance, density of crab bur-rows, and tidal state accounted for the variation in the abundanceof both planktivorous and benthivorous groups of fishes, linearmodels were constructed following Neter et al. (1991). Densityof polychaetes, density of crab burrows and POM concentrationswere incorporated as continuous variables and tidal state as acategorical variable. The analysis was restricted to the monthsduring which fishes were present in the area (based on theprevious analysis), and different days were considered to be inde-pendent samples. Data were log-transformed to comply with theassumptions of the statistical procedure.

ResultsSpatial and temporal variability in food for fishesand environmental factorsPOM concentrations in flooding tides showed no dif-ferences between habitats (d.f. = 1, F = 2.926, P = 0.491;interaction: d.f. = 7, F = 0.270, P = 0.924), but there weredifferences among months (d.f. = 7, F = 0.492, P = 0.038;Fig. 2a). Differences were not significant between habitatsduring ebb tides (d.f. = 1, F = 0.001, P = 0.97; interaction:d.f. = 7, F = 0.158, P = 0.975), but they differed among months(d.f. = 7, F = 7.306, P < 0.005; Fig. 2b). Variations among

Fish habitat use in intertidal soft sediments Marine and Freshwater Research 197

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Fig. 2. Particulate organic matter (POM; g L−1) in Mar Chiquita CoastalLagoon in areas disturbed by Chasmagnathus granulatus (crab bed) and inundisturbed areas (outside), with (a) flood and (b) ebb tide. Hereafter, boxplots are constructed with limits of boxes being the 75th and 25th percentile,lines representing the 10th and 90th percentiles, points inside boxes beingmedians and circles outliers. Horizontal lines indicate no significant differ-ences between sampled months (P > 0.05, ANOVA, planned comparisons).Parallel lines (//) in the horizontal axes indicate no sampled time intervals.

months showed the same pattern in flooding and ebb tides: POMconcentrations were lower in July 2001 and March 2002 than inJune and December 2001 or in January, February, June and July2002. In addition, the variances were higher in crab-bed areaswith flooding tide and outside crab-bed areas with ebbing tide(flood tide: d.f. = 21, F = 0.175, P < 0.001; ebb tide: d.f. = 21,F = 1.930, P = 0.047).

The only benthic organism that was abundant enough to per-form statistical analysis was the polychaete Laeonereis acuta.Abundances of L. acuta showed an interaction with month andarea (d.f. = 6, F = 4.417, P = 0.001; Fig. 3). In June 2001,abundance was higher than in other months and was higher incrab beds, whereas abundance was higher outside crab beds inFebruary and March 2002.

Salinity varied over time (d.f. = 14, F = 1.945, P = 0.022;Fig. 4a). In June and July 2001 and March, June and July 2002,salinity was lower than in other months. In addition, in December2001 and January and February 2002, salinities were lower thanin those same months of the previous summer.

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Fig. 3. Abundance of the polychaete Laeonereis acuta in Mar ChiquitaCoastal Lagoon in areas disturbed by Chasmagnathus granulatus (crab bed,grey boxes) and in nearby undisturbed areas (outside, empty boxes). Hori-zontal lines indicate no significant differences (P > 0.05, ANOVA, plannedcomparisons).

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Fig. 4. (a) Chasmagnathus granulatus burrow abundances (boxes) andwater salinity (dotted line; ppt) in Mar Chiquita Coastal Lagoon; the arrowindicates a shift in burrow abundances and salinity. (b) Odontesthes argen-tinensis, (c) Micropogonias furnieri, (d) Brevoortia aurea, (e) Ramnogasterarcuata and ( f ) Pimelodella laticeps abundances in areas disturbed byC. granulatus (crab bed, grey boxes) and outside crab beds (empty boxes) inMar Chiquita Coastal Lagoon.

198 Marine and Freshwater Research P. Martinetto et al.

Table 1. Absolute and relative abundance of fishes collected between January 2000 and July 2002from inside and outside Chasmagnathus granulatus crab beds in Mar Chiquita Coastal Lagoon

Family/ Common name Inside OutsideScientific name n % n %

EngraulidaeLycengraulis grossideus Atlantic sabretooth anchovy 8 0.17 8 0.28

ClupeidaeBrevoortia aurea Brazilian menhaden 1819 39.76 365 12.64Ramnogaster arcuata Jenyns’s sprat 433 9.46 170 5.89

HeptapteridaePimelodella laticeps Catfish 92 2.01 96 3.32

MugilidaeMugil platanus Mullet 6 0.13 677 23.44

AtherinopsidaeOdontesthes argentinensis Silverside 1667 36.44 1404 48.61

AnablepidaeJenynsia multidentata Rio de la Plata onesided 2 0.04 12 0.41

livebearedPomatomidae

Pomatomus saltatrix Bluefish 1 0.02 2 0.07Sciaenidae

Micropogonias furnieri White-mouth croaker 489 10.69 146 5.05Cichlidae

Cichlasoma facetum Chameleon cichlid 4 0.09 0 0Paralichthyidae

Paralichthys orbignyanus Flatfish 54 1.18 0 0Total 4575 2880

Burrow densities varied among months (d.f. = 12; F = 5.48;P < 0.01; Fig. 4a), but the crab beds remained in the sameplace and easily identifiable throughout the study period. DuringFebruary and March 2000, burrow abundances were higher thanother months. In winter 2001, burrows abundances decreasedand remained lower during 2002.

Spatial and temporal variability in species compositionand abundance of juvenile fishHighest species richness of fishes occurred in crab beds. Weidentified 11 species of juveniles fishes (Table 1), 9 of whichwere common to both areas, and 2 (the estuarine-dependentflatfish Paralichthys orbignyanus and the freshwater chameleoncichlid Cichlasoma facetum) were caught only in crab beds. Theabundance of P. orbignyanus was constant over time, but wastoo low to perform a separate analysis, and C. facetum was onlyfound on two sampling dates, March and July 2002, during a lowsalinity period. Juveniles of the mullet Mugil platanus (meantotal length = 26.7 mm, s.d. = 3.54 mm) were caught only out-side crab beds in one tow in March 2000; thus, further analysiswas not performed.

The silverside Odontesthes argentinensis, the menhadenBrevoortia aurea, the sprat Ramnogaster arcuata and the white-mouth croaker Micropogonias furnieri were the more abun-dant and commonly caught species in both areas (Table 1).Odontesthes argentinensis was the most common fish foundthroughout the sampling period. Brevoortia aurea, R. arcuataand M. furnieri showed higher densities during summer but were

almost absent in winter. These species were individually anal-ysed. In addition, the most abundant species in summer 2002was the freshwater catfish Pimelodella laticeps. However, thisfish was not found in other months; thus, analysis was only per-formed for these months. In winter 2002, fishes were almostabsent. Only two silversides were captured in June (one in eacharea) and, in July, only one cichlid in the crab bed.

Highest abundances of all fishes occurred in crab bed. Com-parison of the total number of fishes showed that abundanceswere higher in crab beds (Table 2) and during summer months(mainly February; Table 2, Fig. 5).

The silverside O. argentinensis was found throughout thestudy period. There were differences in abundances amongmonths but there were not between areas (Table 2). In Januaryand February 2000, and January, February, June, and Decem-ber 2001 abundances were higher than in any other month(Fig. 4b).

The white-mouth croaker M. furnieri was captured duringsummer only, and there were differences in abundances amongsummer months (Table 2). In March 2000 and February 2002,abundances were higher than in February 2000, February andDecember 2001 and January and March 2002 (Fig. 4c).

The menhaden B. aurea occurred only in summer. Its abun-dance did not differ among summer months, but it was moreabundant inside crab beds (Table 2; Fig. 4d).

The sprat R. arcuata was only found in January and February2000 and January, February and June 2001. The higher abun-dances of this species occurred in February 2000 and 2001.ANOVA analysis revealed a significant interaction between

Fish habitat use in intertidal soft sediments Marine and Freshwater Research 199

Table 2. Results of repeated-measures two-way ANOVAs (Type III SS)testing for the effects of habitat type (inside and outside crab beds),month and the habitat × month interaction of abundances for the four

most abundant fishes and total fishes

Source of variation d.f. MS F P

Total fishesArea 1 1616.27 41.189 0.020*Month 14 2175.81 1.945 0.035*Area × Month 14 951.84 0.851 0.614

Odontesthes argentinensisArea 1 416.29 3.282 0.211Month 13 925.52 2.411 0.027*Area × Month 13 741.15 1.589 0.152

Micropogonias furnieriArea 1 20.22 0.097 0.768Month 6 130.33 7.865 <0.001*Area × Month 6 46.6 0.949 0.475

Brevoortia aureaArea 1 1050 0.273 0.038*Month 7 353.81 0.837 0.564Area × Month 7 311.89 0.890 0.525

Ramnogaster arcuataArea× Month 4 8.86 6.101 0.001*

Pimelodella laticepsArea 1 3.63 0.017 0.898Month 2 122.58 14.238 <0.001*Area × Month 2 29.71 14.238 0.229

*P < 0.05.

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habitat and month (Table 2). In February 2000 and 2001, abun-dances were higher in crab beds; there were no differencesbetween habitats in other months (Fig. 4e).

Pimelodella laticeps was the most abundant species duringsummer 2002, but was not found in other months. In March,abundance was significantly higher than in January and February(Table 2), but there were no differences in abundances betweenhabitats (Fig. 4f).

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Fig. 6. Planktivorous fish abundances with (a) flood and (b) ebb tide, andbenthivorous fish abundances with (c) flood and (d) ebb tide. Planktivoresare Brevoortia aurea, Ramnogaster arcuata and Odontesthes argentinensis(<8 cm total length). Benthivores are Micropogonias furnieri, Pimelodellalaticeps and Odontesthes argentinensis (>8 cm total length). *P < 0.05,differences in abundances between areas (significance level of P < 0.05,ANOVA, planned comparisons).

Spatial and temporal variability of fish trophic groupsTidal state affected the abundance of planktivorous fishes.Abun-dances of planktivorous fishes were higher during flood tide thanduring ebb tide in crab beds (d.f. = 1, F = 24.448, P = 0.016)and outside crab beds (d.f. = 1, F = 14.898, P = 0.061). Theabundance of planktivorous was higher in crab beds during floodtide (Fig. 6a; d.f. = 1, F = 8.722, P = 0.048), whereas the inter-action between habitat and month was significant (d.f. = 10,F = 2.866, P = 0.022) during ebb tide. During ebb tide, theabundance of planktivorous fishes was higher outside than insidecrab beds in most months, but in March 2000 and 2002 theopposite pattern was observed (Fig. 6b). In addition, the abun-dance of planktivorous fishes showed a significant interactionbetween habitat and month (d.f. = 7, F = 2.419, P = 0.039). InJanuary and February 2000, there were no differences betweenhabitats; in contrast, from September 2000 to March 2002,abundances were higher in crab beds (Figs 6a, b).

200 Marine and Freshwater Research P. Martinetto et al.

Table 3. Linear models and standardized parameter estimates evalu-ating the variation in the abundance of benthivorous and planktivorousfishes in relation to POM concentration, density of polychaetes, density

of crab burrows and tidal state (flooding and ebbing)

Fish group SS d.f. MS F P β s.e.

BenthivoresPOM 1.927 1 1.927 1.653 0.206 −0.17 0.14Polychaetes 14.895 1 14.895 12.781 0.001 0.51 0.14Burrows 9.669 1 9.669 8.297 0.006 0.40 0.14Tidal state 1.504 1 1.504 1.290 0.263 0.15 0.13Error 46.616 40 1.165

PlanktivoresPOM 5.365 1 5.365 3.768 0.062 0.35 0.18Polychaetes 2.134 1 2.134 1.499 0.231 −0.23 0.19Burrows 0.073 1 0.073 0.051 0.822 0.04 0.19Tidal state 2.402 1 2.402 1.688 0.204 0.24 0.18Error 39.860 28 1.424

The abundance of benthivorous fishes also showed a sig-nificant interaction between habitat and month (d.f. = 12,F = 3.683, P = 0.001). In September 2000, January 2001 andMarch 2002 abundances were higher outside crab beds, inJanuary, February and December 2000 and July 2001 no dif-ferences were observed, while in February, June and December2001 and January, February and March 2002 abundances werehigher in crab beds (Figs 6c, d). The tide effect differed depend-ing on the habitat. Abundance of benthivores in crab bedwere higher during flood tide than during ebb tide (d.f. = 1,F = 12.413, P = 0.042), while there were no differences outsidecrab bed (d.f. = 1, F = 1.050, P = 0.413). In addition, duringflood tide, abundances of benthivores were higher in crab bedsthan outside crab beds (d.f. = 1, F = 2.416, P = 0.044; Fig. 5c);there was no effect during ebbing tide (d.f. = 1, F = 0.794,P = 0.467; Fig. 6d).

The abundance of benthivores was positively related to thedensity of polychaetes and the density of crab burrows (linearmodel analysis, Table 3), and was not related to POM con-centration or tidal state (total model: r2 = 0.303, F = 4.345,P = 0.005). The abundance of planktivorous fishes was notrelated to any of the four considered variables (total model:r2 = 0.174, F = 1.478, P = 0.235; Table 3).

Spatial and temporal variability in juvenile fish sizesMean sizes of the more abundant fish species were variableamong months in the different habitats. Odontesthes argenti-nensis exhibited differences between habitats in February 2000and in January, June and December 2001. The fishes were largeroutside crab beds except in January 2000, in which the inversewas observed (Fig. 7a). Micropogonias furnieri showed differ-ences in mean size during February 2000 and 2002. In February2000 fishes were larger in crab beds, while in February 2002mean size was larger outside crab beds (Fig. 7b). The mean sizeof Brevoortia aurea was larger in crab beds in January 2000(Fig. 7c), whereas the opposite pattern was recorded in February2001. Ramnogaster arcuata exhibited differences in mean sizeonly in February 2001, during which time they were larger incrab beds (Fig. 7d).

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Fig. 7. Mean size of (a) Odontesthes argentinensis, (b) Micropogoniasfurnieri, (c) Brevoortia aurea and (d) Ramnogaster arcuata, captured in areasdisturbed (crab bed, grey boxes) and undisturbed (outside, empty boxes)by the burrowing crab Chasmagnathus granulatus. *P < 0.05, differencesbetween areas in the mean size (t-test). Two boxes in the same habitat andmonth represent two separate class sizes.

Discussion

Our results show that the presence of the burrowing crabC. granulatus affects the habitat use by juvenile fishes overintertidal flats. The differences in fish species composition,abundances and size between areas with and without crab bedsare evidence of this effect. In the present study, crab-bed areasshowed more species and much higher abundances of juvenilefishes than nearby areas without crab beds.

Higher abundances of juvenile fish and higher densities ofcrab burrows in Mar Chiquita Coastal Lagoon occur in summer.However, fish abundance and crab burrows densities shifted dur-ing the time of this study, declining from December 2001. Thisdecrease in C. granulatus burrow density in mudflat areas hasbeen related to a long rainy period, in which C. granulatus movedfrom mudflats to the salt marsh (Iribarne et al. 2003). Duringthese periods mudflats remained mostly covered by freshwater,affecting the crab burrowing activity (see Iribarne et al. 2003).

Fish habitat use in intertidal soft sediments Marine and Freshwater Research 201

The increase in precipitation was followed by a high dischargeof freshwater from creeks into the lagoon, changing its waterlevel, salinity, temperature and nutrient and suspended materialloads. From August to December 2001 rainfall exceeded theaverage for this region (Argentinean National Weather ForecastService (ANWFS), unpublished data), and salinity was signif-icantly lower in the estuary. Fish composition changed afterthis rainy spring and early summer. Estuarine-dependent speciessuch as B. aurea, R. arcuata and O. argentinensis (Cousseauet al. 2001) were almost absent. Nevertheless, M. furnieri, aspecies with a wide range of salinity tolerance (Cousseau et al.2001), was present at high abundances in summer 2002. Inaddition, freshwater organisms occurred in summer 2002, suchas the catfish P. laticeps (captured only during this summer).Most coastal fishes, such as B. aurea and R. arcuata, spawnin marine waters adjacent to the estuary during late spring andearly summer (Cousseau et al. 2001). Larvae and juveniles aretransported or migrate into the estuary where they find shelterand food (Cousseau et al. 2001). Under conditions of high fresh-water discharge and limited saltwater intrusion into the estuary,few juvenile estuarine-dependent fishes appear to move into theshallow water of estuaries (e.g. see study of similar system byGarcia et al. 2003). Juveniles tolerant to variable salinity oftenremain in the estuary, but new individuals cannot be transportedby saltwater intrusion. This could be the case for M. furnieri,given that only large individuals were captured during December2001. In contrast, with high freshwater discharge and the conse-quent decline of dominant euryhaline fishes, freshwater vagrantspecies such as P. laticeps and Cichlasoma facetum can tem-porarily expand their range throughout the estuary until highersalinity returns. During summer 2000, fish abundances werehigher than during other summers, especially those of B. aurea,R. arcuata, O. argentinensis and some marine vagrants asso-ciated with high salinity (e.g. Pomatomus saltatrix) (Cousseauet al. 2001). Precipitation in 1999 was below average (ANWFS,unpublished data), and it is during such drought periods thatnutrient-rich saltwater enters the estuaries and enhances phyto-plankton production (Dyer 1997). Thus, recycling of nutrients insediments combined with intrusion of nutrient-enhanced marinewater could have stimulated primary production in the estu-ary in the summer of 1999–2000, with concomitant growth andsurvival of estuarine-dependent fishes.

Food availability (Rozas and Zimmerman 2000) and shelteropportunities (Rozas and Minello 1998; Halpin 2000; Hindellet al. 2000; Rozas and Zimmerman 2000) are the most commonfactors proposed to account for differences in habitat use by estu-arine fishes. In the present study, we found that benthivorousfishes more frequently use crab-bed areas. Although variable,sizes of these species were also larger in crab beds. Moreover,the flatfish P. orbignyanus was captured only on crab-bed areas.Previous studies of Mar Chiquita Coastal Lagoon showed thatthese fishes prey mostly on crustaceans (small crabs, shrimpsand amphipods) and polychaetes (Hozbor and García de la Rosa2000; Rivera Prisco et al. 2001; Martinetto et al. 2005). Thesebenthic prey are strongly influenced by C. granulatus. For exam-ple, megalopae of C. granulatus have been found in the interiorof burrows where metamorphosis and growth occurs (Luppiet al. 2002); thus, small crabs can reach higher densities incrab beds. Polychaete densities did not differ between areas,

but the feeding rate of the polychaete L. acuta is higher in crabbeds, consequently resulting in better body condition (Palomoet al. 2004). Also, sediment in crab beds is softer (Escapa et al.2004), with a lower proportion of sand than outside crab beds andhomogeneous across the intertidal, which may facilitate the cap-ture of polychaetes. Preferences of fishes for areas with lowerproportions of sand in intertidal mudflats have been observed(Quammen 1984; Martinetto et al. 2005). Fish abundances andpredation by fishes were higher in such areas, and the floun-der Paralichthys californicus was only found in muddy areas(Quammen 1984). Moreover, an experimental study performedin Mar Chiquita Coastal Lagoon showed that the effect of fishpredation on benthic prey is higher in crab beds than outside crabbeds: O. argentinensis and P. laticeps consume more polychaetesper capita in crab beds, and the percentage of these fish andM. furnieri with empty stomachs is lower in crab beds thanoutside (Martinetto et al. 2005). Although the implications ofsediment type for availability of prey for fish was not determined,sand grains could interfere with benthic prey capture, as shownfor shorebirds (Quammen 1984) and crabs (Seitz et al. 2001).Thus, crab beds could be preferred by benthivorous fishes giventhe higher quantity (e.g. small crabs; Luppi et al. 2002) and qual-ity (e.g. polychaetes with better body condition; Palomo et al.2004) of benthic prey, and also because the cost of prey captureis likely to be lower (Escapa et al. 2004) in softer sediment.

Benthivorous abundances were higher during flood tide thanduring ebb tide. Fish access to these intertidal mudflat areas iscontrolled by tide. More benthic prey become available when tideis flooding, and prey stocks become depleted when tide is ebbing,in part owing to predation and in part because the flooded inter-tidal area is smaller (Rozas 1995). In addition, benthic organismsperform vertical movement during the tidal cycle (Joint et al.1982; Zwarts andWanink 1991;Alve and Bernhard 1995; Escapaet al. 2004; Palomo et al. 2004). In Mar Chiquita Coastal Lagoon,the most abundant polychaete L. acuta moves to the surface of thesediment during flood tide in response to feeding requirementsand risk of predation by shorebirds (Escapa et al. 2004). The dis-tribution of infauna is homogeneous across the intertidal crabbeds, whereas infauna abundances decrease in the high inter-tidal level near the salt marsh outside crab beds (Escapa et al.2004). Thus, fishes could be selecting crab-bed areas during theflooding tide in response to higher prey availability.

Planktivores also presented higher abundances and largerindividuals inside crab-bed areas during flood tide, but weremore abundant outside crab beds during ebb tide. There were nodifferences in mean POM concentration between areas; however,variances in crab beds were much higher during flooding tide,whereas variances outside crab beds were higher with ebbing tide(Fig. 2). This pattern may result from higher substrate roughnessin crab beds. Substrate microtopography in crab beds promoteschange in fluids dynamics, and burrows work as traps of sus-pended material, thereby increasing the organic matter content ofsediment (Botto and Iribarne 2000). When mudflats are flooded,the irregularities of substrate could increase near-bed turbulence,which may resuspend organic matter and benthic organisms.Higher diversities of planktonic and benthoplanktonic organ-isms have been recorded in crab beds (Martinetto 2001). Thehigh variances in POM and the increment in diversity of plank-tonic organisms in crab beds may be evidence of this process

202 Marine and Freshwater Research P. Martinetto et al.

(Martinetto 2001). Thus, food availability for planktivorousfishes is likely to be higher in crab beds, which may allow forhigher fish abundances.

The role of microhabitat features has been central to ourunderstanding of the mechanisms that contribute to the variationin fish assemblages. In estuaries, most inter-habitat comparisonshave contrasted nekton densities in vegetated v. non-vegetatedareas, showing species-specific associations between spatialheterogeneity and juvenile fishes (i.e. Gray et al. 1998; Rozasand Minello 1998; Rozas and Zimmerman 2000; Snelgrove et al.2000; Jackson et al. 2001). The results of the present study showthat the presences of burrowing crabs can also affect habitat useby fishes. This may be a common phenomenon in other estuarieswith similar characteristics.

Burrowing crustaceans are commonly an important com-ponent of several temperate and tropical marine benthic com-munities (e.g. shrimps of the genus Neotrypaea [Callianassa],Trypaea and Upogebia, Callianassidae; Posey 1986; Dobbs andGuckert 1988; Posey et al. 1991; Kerr and Corfield 1998; Katrakand Bird 2003). For instance, the ghost shrimp Neotrypaea(Callianassa) californiensis dominate estuarine intertidals fromAlaska to Baja California. This shrimp lives in burrows of up to0.5-m depth and may form dense beds of over 500 individualsm−2 (Posey 1986). Shrimp also have strong effects on sedimentcharacteristics and the entire benthic community (Dobbs andGuckert 1988). Given the results of the present study, it is likelythat the effects of these organisms are broader, extending to alsoinfluence organisms living in the water column.

In conclusion, our results present evidence that the activityof burrowing crustaceans can influence the distribution of fishesover intertidal flats. Based on the present study, and what weknow from these and other burrowing species, we believe thatour results may represent a phenomenon that is common to othersystems.

AcknowledgementsWe thank Gabriela Palomo for statistical advice and comments that improvedthe manuscript. We also thank Ivan Valiela, Mirta Teichberg and BrendanAnnett for useful comments on a first draft; Nora Peskin,Verónica García andMauricio Escapa for helping to collect and process samples; and AgustinaMendez Casariego for photo edition assistance. We appreciate the commentsand suggestions of two anonymous reviewers that helped to improve the finalmanuscript. Financial support was provided by the Universidad Nacional deMar del Plata (UNMDP), CONICET, Fundacion Antorchas and ANPCYT(all to O.I.). P.M. and P.R. were supported by fellowships from CONICET(Argentina). This is part of P.M.’s Ph.D. thesis.

ReferencesAlve, E., and Bernhard, J. M. (1995). Vertical migratory response of ben-

thic foraminifera to controlled oxygen concentration in an experimentalmesocosm. Marine Ecology Progress Series 116, 137–151.

Bortolus, A., and Iribarne, O. (1999). Effects of the burrowing crab Chas-magnathus granulata on a Spartina salt marsh. Marine Ecology ProgressSeries 178, 78–88.

Boschi, E. E. (1964). Los crustáceos decápodos Brachyura del litoralbonaerense. Boletín del Instituto de Biología Marina, Argentina 6, 1–99.

Botto, F., and Iribarne, O. (1999). The effect of the burrowing crab Chas-magnathus granulta on the benthic community of a SW Atlantic coastallagoon. Journal of Experimental Marine Biology and Ecology 241,263–284. doi:10.1016/S0022-0981(99)00089-1

Botto, F., and Iribarne, O. (2000). Contrasting effects of two burrowingcrabs (Chasmagnathus granulata and Uca uruguayensis) on sedimentcomposition and transport in estuarine environments. Estuarine, Coastaland Shelf Science 51, 141–151. doi:10.1006/ECSS.2000.0642

Botto, F., Iribarne, O., Martinez, M., Delhey, K., and Carrete, M. (1998). Theeffect of migratory shorebirds on the benthic fauna of three SW Atlanticestuaries. Estuaries 21, 700–709. doi:10.2307/1353274

Botto, F., Palomo, G., Iribarne, O., and Martinez, M. M. (2000). The effectof the Southwestern Atlantic burrowing crab Chasmagnathus granulataon habitat use and foraging activity of migratory shorebirds. Estuaries23, 208–215. doi:10.2307/1352828

Cousseau, M. B., Díaz de Astarloa, J. M., and Figueroa, D. E. (2001).La ictiofauna de la laguna Mar Chiquita. In ‘Reserva de la Bios-fera Mar Chiquita: Características Físicas, Biológicas y Ecológicas’.(Ed. O. Iribarne.) pp. 187–203. (Editorial Martín: Mar del Plata,Argentina.)

Crisp, D. J. (1971). Energy flow measurements. In ‘Methods for Study ofMarine Benthos’. (Eds N. A. Holme and A. D. McIntyre.) pp. 197–279.(Blackwell Scientific Publications: Oxford.)

Daleo, P., Ribeiro, P., and Iribarne, O. (2003). The SW Atlantic bur-rowing crab Chasmagnathus granulatus Dana affects the distributionand survival of the fiddler crab Uca uruguayensis Nobili. Journal ofExperimental Marine Biology and Ecology 291, 255–267.

Diaz de Astarloa, J. M., Aubone, A., and Cousseau, M. B. (1999). Fishassemblages on the coastal continental shelf of Uruguay and northernArgentina in relation to environmental patterns. Physis (Rio de Janeiro,Brazil) 57, 29–45.

Dobbs, F. C., and Guckert, J. B. (1988). Callianassa trilobata (Crustacea:Thalassinidea) influences abundance of meiofauna and biomass, compo-sition and physiologic state of microbial communities within its burrow.Marine Ecology Progress Series 45, 69–79.

Dyer, K. R. (1997). ‘Estuaries: a Physical Introduction.’ 2nd edn. (Wiley &Sons: London.)

Escapa, M., Iribarne, O., and Navarro, D. (2004). Indirect effect of intertidalburrowing crabs on infaunal zonation patterns, tidal behavior and risk ofmortality. Estuaries 27, 120–131.

Fasano, J. L., Hernández, M.A., Isla, F. I., and Schnack, E. J. (1982).Aspectosevolutivos y ambientales de la laguna Mar Chiquita (provincia de BuenosAires, Argentina). Oceanologica Acta SP, 285–292.

Garcia, A. M., Vieira, J. P., and Winemiller, K. O. (2003). Effects of 1997–1998 El Niño on the dynamics of the shallow-water fish assemblages ofthe Patos Lagoon Estuary (Brazil). Estuarine, Coastal and Shelf Science57, 489–500. doi:10.1016/S0272-7714(02)00382-7

Giangiobbe, A., and Sanchez, F. (1993). Alimentación de la saraca (Brevoor-tia aurea). Frente Marítimo 14, 71–80.

Gray, C. A., Chick, R. C., and McElligot, D. J. (1998). Diel changesin assemblages of fishes associated with shallow seagrass and baresand. Estuarine, Coastal and Shelf Science 46, 849–859. doi:10.1006/ECSS.1997.0321

Halpin, P. M. (2000). Habitat use by an intertidal salt-marsh fish: trade-offbetween predation and growth. Marine Ecology Progress Series 198,203–214.

Hindell, J. S., Jenkins, G. P., and Keough, M. J. (2000). Variability inabundances of fishes associated with seagrass habitats in relation todiets of predatory fishes. Marine Biology 136, 725–737. doi:10.1007/S002270050732

Hozbor, N. M., and García de la Rosa, S. B. (2000).Alimentación de juvenilesde corvina rubia (Micropogonias furnieri) en la Laguna de Mar Chiquita.Frente Marítimo 18, 59–70.

Iribarne, O., Bortolus, A., and Botto, F. (1997). Between habitats differencesin burrows characteristics and trophic modes in the south westernAtlanticburrowing crab Chasmagnathus granulata. Marine Ecology ProgressSeries 155, 132–145.

Iribarne, O., Botto, F., Martinetto, P., and Gutierrez, J. L. (2000). Therole of burrows of the SW Atlantic intertidal crab Chasmagnathus

Fish habitat use in intertidal soft sediments Marine and Freshwater Research 203

granulata in trapping debris. Marine Pollution Bulletin 40, 1057–1062.doi:10.1016/S0025-326X(00)00058-8

Iribarne, O., Martinetto, P., Schwindt, E., Botto, F., Bortolus, A., andGarcia Borboroglu, P. A. (2003). Geographic and local evidence of habi-tat displacement between two common SW Atlantic intertidal crabs.Journal of Experimental Marine Biology and Ecology 296, 167–182.doi:10.1016/S0022-0981(03)00318-6

Iribarne, O., Bruschetti, M., Escapa, M., Bava, J., Botto, F., Gutiérrez, J.,Palomo, G., Delhey, K., Petracci, P., and Gagliardini, A. (2005).Small and large-scale effect of the SW Atlantic burrowing crabChasmagnathus granulatus on habitat use by migratory shorebirds.Journal of Experimental Marine Biology and Ecology 315, 87–101.doi:10.1016/J.JEMBE.2004.09.006

Jackson, E. L., Rowden, A. A., Atrill, M. J., Bossey, S. J., and Jones, M. B.(2001). The importance of seagrass beds as a habitat for fishery species.Oceanography and Marine Biology: An Annual Review 39, 269–303.

Joint, I. R., Gee, J. M., and Warwick, R. M. (1982). Determination of fine-scale vertical distribution of microbes and meiofauna in an intertidalsediment. Marine Biology 72, 157–164. doi:10.1007/BF00396916

Katrak, G., and Bird, F. L. (2003). Comparative effects of the large biotur-bators, Trypaea australiensis and Heloecius cordiformis, on intertidalsediments of Western Port, Victoria, Australia. Marine and FreshwaterResearch 54, 701–708. doi:10.1071/MF03015

Kerr, G., and Corfield, J. (1998). Association between the ghost shrimpTrypaea australiensis Dana 1852 (Crustacea: Decapoda) and a smalldeposit-feeding bivalve Mysella vitrea Laserson 1956 (Mollusca: Lep-tonidae). Marine and Freshwater Research 49, 801–806. doi:10.1071/MF97093

Little, C. (2000). ‘The Biology of Soft Shores and Estuaries.’ (OxfordUniversity Press: New York.)

Luppi, T. A., Spivak, E. D., Anger, K., and Valero, J. L. (2002). Pat-terns and processes of Chasmagnathus granulata and Cyrtograpsusangulatus (Brachyura: Grapsidae) recruitment in Mar Chiquita coastallagoon, Argentina. Estuarine, Coastal and Shelf Science 55, 287–297.doi:10.1006/ECSS.2001.0904

Martinetto, P. (2001). Efecto de los ‘cangrejales’ de Chasmagnathus granu-lata en el uso de habitat de cangrejos, peces y zooplancton. In ‘Reserva dela Biosfera Mar Chiquita: Características Físicas, Biológicas y Ecológ-icas’. (Ed. O. Iribarne.) pp. 165–171. (Editorial Martín: Mar del Plata,Argentina.)

Martinetto, P. (2006). Efecto del cangrejo cavador Chasmagnathus granu-latus en las interacciones biológicas y el uso de hábitat de cangrejos ypeces juveniles. Ph.D. Thesis, Universidad Nacional de Mar del Plata.

Martinetto, P., Iribarne, O., and Palomo, G. (2005). Effect of fish pre-dation on intertidal benthic fauna is modified by crab bioturbation.Journal of Experimental Marine Biology and Ecology 318, 71–84.doi:10.1016/J.JEMBE.2004.12.009

Neter, J., Wasserman, W., and Kutner, M. H. (1991). ‘Applied Linear Sta-tistical Models. Regression, Analysis of Variance, and ExperimentalDesigns.’ (Irwin, Homewood, IL, USA.)

Norton, S. F., and Cook, A. E. (1999). Predation by fishes in intertidal. In‘Intertidal Fishes: Life inTwo Worlds’. (Eds M. H. Horn, K. L. M. Martinand M.A. Chotkowski.) pp. 223–263. (Academic Press: San Diego, CA.)

Palomo, G., Botto, F., Navarro, D., Escapa, M., and Iribarne, O. (2003).The predator-prey interaction between migratory shorebirds and thepolychaete Laeonereis acuta is modified by burrowing crabs. Jour-nal of Experimental Marine Biology and Ecology 290, 211–228.doi:10.1016/S0022-0981(03)00074-1

http://www.publish.csiro.au/journals/mfr

Palomo, G., Martinetto, P., and Iribarne, O. (2004). Changes in the feed-ing behavior of the deposit feeder polychaete Laeonereis acuta onsoft-sediments inhabited by burrowing crabs. Marine Biology 145,657–667.

Piccolo, M. C., and Perillo, G. M. E. (1999). The Argentina estuaries:a review. In ‘Estuaries of South America: their Geomorphology andDynamics’. (Eds G. M. E. Perillo, M. C. Piccolo and M. Pino Quivira.)pp. 101–132. (Springer Verlag: Berlin, Germany.)

Posey, M. H. (1986). Changes in a benthic community associated with densebeds of a burrowing deposit-feeder, Callianassa californiensis. MarineEcology Progress Series 31, 15–22.

Posey, M. H., Dumbauld, B. R., and Armstrong, D. A. (1991). Effects of aburrowing mud shrimp Upogebia pugettensis (Dana), on abundance ofmacro-infauna. Journal of Experimental Marine Biology and Ecology148, 283–294. doi:10.1016/0022-0981(91)90088-E

Quammen, M. L. (1984). Predation by shorebirds, fish, and crabs on inverte-brates in intertidal mudflats: an experimental test. Ecology 65, 529–537.doi:10.2307/1941415

Rivera Prisco,A., García de la Rosa, S. B., and Díaz deAstarloa, J. M. (2001).Feeding ecology of flatfish juveniles (Pleuronectiformes) in Mar Chiq-uita Coastal Lagoon (Buenos Aires, Argentina). Estuaries 24, 917–925.

Rozas, L. P. (1995). Hydroperiod and its influence on nekton use of thesalt marsh: a pulsing ecosystem. Estuaries 18, 579–590. doi:10.2307/1352378

Rozas, L. P., and Minello, T. J. (1998). Nekton use of salt marsh, seagrass,and nonvegetated habitats in a south Texas (USA) estuary. Bulletin ofMarine Science 63, 481–501.

Rozas, L. P., and Zimmerman, R. J. (2000). Small-scale patterns of nektonuse among marsh and adjacent shallow nonvegetated areas of the Galve-ston Bay Estuary, Texas (USA). Marine Ecology Progress Series 193,217–239.

Seitz, R. D., Lipcius, R. N., Hines, A. H., and Eggleston, D. V. (2001).Density-dependent predation, habitat variation, and the persistence ofmarine bivalve prey. Ecology 82, 2435–2451. doi:10.2307/2679927

Shaw, R. G., and Mitchell-Olds, T. (1993). ANOVA for unbalanced data: anoverview. Ecology 74, 1638–1645. doi:10.2307/1939922

Snelgrove, P. V. R., Austen, M. C., Boucher, G., Heip, C., Hutchings, P. A.,King, G. M., Koike, I., Lambdshead, P. J., and Smith, C. R. (2000).Linking biodiversity above and below the marine sediment-waterinterface. Bioscience 50, 1076–1088. doi:10.1641/0006-3568(2000)050[1076:LBAABT]2.0.CO;2

Spivak, E. D., Anger, K., Luppi, T., Bas, C., and Ismael, D. (1994). Dis-tribution and habitat preferences of two grapsid crab species in MarChiquita Lagoon (Province of Buenos Aires, Argentina). HelgolanderMeeresuntersuchungen 48, 59–78. doi:10.1007/BF02366202

Thompson, A. R. (2004). Habitat and mutualism affect the distributionand abundance of a shrimp-associated goby. Marine and FreshwaterResearch 55, 105–113. doi:10.1071/MF03099

Underwood, A. J. (1997). ‘Experiments in Ecology.’ (Cambridge UniversityPress: London.)

Zar, J. H. (1999). ‘Biostatistical Analysis.’ (Prentice-Hall: EnglewoodCliff, NJ.)

Zwarts, L., and Wanink, J. H. (1991). The macrobenthos fraction acces-sible to waders may represent marginal prey. Oecologia 87, 581–587.doi:10.1007/BF00320424

Manuscript received 10 May 2006, accepted 2 November 2006