Journal of Experimental Marine Biology and Ecology, 241

LJournal of Experimental Marine Biology and Ecology,241 (1999) 263–284

Effect of the burrowing crab Chasmagnathus granulata(Dana) on the benthic community of a SW Atlantic coastal

lagoon

*Florencia Botto , Oscar Iribarne´Departamento de Biologıa (FCEyN), Universidad Nacional de Mar del Plata, CC 573 Correo Central,

7600 Mar del Plata, Argentina

Received 19 March 1999; accepted 23 June 1999

Abstract

This study evaluated the effect of the burrowing crab Chasmagnathus granulata on the benthiccommunity in mudflats of the Mar Chiquita coastal lagoon (Argentina, 378 459 S, 578 269 W). Asignificantly higher abundance of the polychaete Laeonereis acuta was found inside the C.granulata crab bed than outside. However, L. acuta abundance decreased in summer probably dueto the greater activity of crabs. A series of exclusion and inclusion field experiments showed acombined effect of the non-burrowing crabs Cyrtograpsus angulatus and C. granulata on thepolychaete L. acuta inside crab beds, and also, an effect of C. granulata on the polychaetes L.acuta and Heteromastus similis when added outside the crab bed. C. granulata also affectednematodes, even when experiments were of short duration. The effect of crab burrows on thesmall scale distribution of nematodes may be related to passive transport of organisms. Adults ofboth crab species, Cy. angulatus and C. granulata, also affected the settlement of Cy. angulatus.The juveniles of C. granulata showed no effect for any meiofaunal species. The results of thiswork showed that C. granulata plays an important role in determining the benthic community inmudflats of the Mar Chiquita coastal lagoon. 1999 Elsevier Science B.V. All rights reserved.

Keywords: Benthos; Bioturbation; Burrowing crabs; Chasmagnathus granulata; Community; Mudflats

1. Introduction

There are several saltmarshes between southern Brazil and northern Patagonia(Argentina) on estuaries with large discharges and prevailing brackish conditions (Adam,

*Corresponding author.E-mail address: [email protected] (F. Botto)

0022-0981/99/$ – see front matter 1999 Elsevier Science B.V. All rights reserved.PI I : S0022-0981( 99 )00089-1

264 F. Botto, O. Iribarne / J. Exp. Mar. Biol. Ecol. 241 (1999) 263 –284

1990). There is no information on the ecological processes within these estuariesappropriate to predict the ecological impact of human alterations. The burrowing crabChasmagnathus granulata (Dana) is one of the most abundant macroinvertebrates (up to40 mm carapace width) inhabiting these environments (Boschi, 1964). They aredistributed in almost all the zones of the marsh intertidal; in the mudflat and in the

22Spartina densiflora cordgrass habitats with a mean density of 20 crabs m (Spivak etal., 1994; Iribarne et al., 1997). This crab species is an important bioturbator in mudflats,

22 21removing and processing up to 5.9 kg m day of sediment (Iribarne et al., 1997).This reworking of the upper sediment layer, probably affects the sedimentary environ-ment and benthic organisms, especially during spring–autumn when crab activity isintense (pers. obs.).

Crabs are often important habitat modifiers (e.g., Montague, 1980; Bertness, 1985),significantly influencing microtopography (e.g., Bertness, 1985; Hall et al., 1991),sediment chemistry (Hoffman et al., 1984; Wolfrath, 1992) and drainage (Bertness,1985). Sediment disturbance resulting from the foraging and burrowing activities ofdecapods may have direct and indirect impacts on macroinfauna and/or meiofaunalspecies (e.g., Hoffman et al., 1984; Thrush, 1988; DePatra and Levin, 1989; Warwick etal., 1990). Such sediment-mediated interactions are common in many infaunal com-munities of mudflats and creeks (Rhoads and Young, 1970; Aller and Dodge, 1974;Kneib, 1991; Wilson, 1991).

Burrowing organisms can also affect benthic community composition by alteringrecruitment patterns, increasing mortality of settling larvae by ingestion or suffocation(Woodin, 1976), or increasing survival by providing refuge (e.g., Tamaki and Ingole,1993). Burrowing animals may also increase sediment transported through bedload(Aller and Dodge, 1974) affecting benthos indirectly by controlling food availability(Luckenbach et al., 1988; Miller and Sternberg, 1988), increasing mortality by abrasion(Miller, 1989) or predation (Grant, 1981), or directly favoring dispersion throughpassive transport (Palmer, 1988).

C. granulata, in bare mudflats of Mar Chiquita coastal lagoon (Argentina, 378 459 S,578 269 W) is a deposit feeder that excavates and maintains semi-permanent openburrows (Iribarne et al., 1997). These burrows are funnel shaped, with large entrances(up to 14 cm major axis length) and a surface sediment mound which is a product offeeding or burrow maintenance (Iribarne et al., 1997). C. granulata coexists withCyrtograpsus angulatus (Dana), another grapsid crab (up to 40 mm carapace width)which is highly mobile and does not make permanent burrows in this environment(Spivak et al., 1994). While Cy. angulatus is mainly a subtidal species, C. granulatainhabits the upper intertidal zones, and the two species overlap only during high tides.Juveniles of Cy. angulatus are confined to protected microhabitats (like areas withstones, or in crevices of the tube building polychaete Ficopomatus enigmaticus; Spivaket al., 1994), while juveniles of C. granulata live in bare mudflats with adults (Spivak etal., 1994).

The infaunal community of mudflats of Mar Chiquita coastal lagoon and of othernorthern Argentinean estuaries (i.e., Bahia Samborombon and Bahia Blanca) have verylow diversity. Macroinfauna has a high dominance of two polychaete species(Laeonereis acuta and Heteromastus similis, Ieno and Bastida, 1998; Botto et al., 1998)

F. Botto, O. Iribarne / J. Exp. Mar. Biol. Ecol. 241 (1999) 263 –284 265

that fluctuate widely in abundance (Ieno and Bastida, 1998). The few studies ofmeiofauna in these environments showed also low diversity of ostracods (two species,Whatley et al., 1997) and nematodes (two species, Mammoli, 1992). No previous studiesof other meiofaunal organisms exist for these environments.

Due to their behavior, abundance and extensive distribution C. granulata may play adeterminant role in the intertidal mudflat communities of most SW Atlantic estuaries.Particularly, species that are sensitive to modifications of the structure, composition orchemistry of the sedimentary environment, may suffer higher mortality rate due to crabactivities (e.g., Kneib, 1991; Billick and Case, 1994). Also burrows may enhance spatialheterogeneity, in a small scale affecting meiofauna distribution (e.g., Bell, 1980). Thus,the objective of this work is to determine abundance and distribution patterns of benthicorganisms associated with areas inhabited by C. granulata, and experimentally evaluatethe effect of these crabs on benthic organisms.

2. Materials and methods

2.1. Study area

The study was performed between January 1996 and April 1997 in the Mar Chiquitacoastal lagoon, a body of brackish water (salinity range: 6 to 33‰), affected by lowamplitude ( # 1 m) tides and characterized by mudflats surrounded by large beds ofcordgrass (S. densiflora, Olivier et al., 1972a). The burrowing crab C. granulata isdistributed in both, the S. densiflora areas and mudflats (Spivak et al., 1994; Iribarne etal., 1997). However, only the part of the population living in the open intertidal mudflatswas studied.

2.2. Distribution patterns of benthic organisms associated with the presence of crabs

2.2.1. Sampling designMacroinfauna samples were taken with a core 10 cm diameter and 10 cm depth,

organisms were sieved through a 0.5-mm mesh screen. Organisms retained werepreserved in alcohol (70%) and sorted under a 20 3 dissection microscope. Meiofaunalsub-samples (core size: 2 cm diameter 10 cm depth) were taken, sieved through a0.44-mm mesh screen and then stained with bengal rose to facilitate sorting. Organismsretained were preserved with formalin (5%), identified to the major taxa, and countedunder 20 3 dissection microscope.

2.2.2. Relationship between the presence of the burrowing crab C. granulata, theabundance of other benthic organisms and sediment characteristics

A preliminary study was performed to evaluate if there was any difference in theabundance of benthic macroinfauna associated with the presence of this crab. Two areas,one inhabited by C. granulata and the other without crabs were selected. These areaswere approximately 5 ha each and were separated by 200 m. Ten macroinfauna sampleswere taken randomly in each area (separated each other at least by 10 m) at the same


intertidal level [0.5 m over mean lower low water (MLLW)]. To evaluate verticaldistribution of macroinfauna in each area, samples were divided in five depth layers of 2cm in width each. To evaluate possible temporal variations over a year, these sampleswere taken in May, July, September, November (1996), January and March (1997).

Sediment samples (10 replicates per area; 10 cm diameter and 10 cm depth) weretaken to evaluate water content, organic matter content and grain size. Water content wascalculated as the difference between wet and dry weight (after drying at 708C during 72h). Organic matter content was calculated as the percentage of ash free dry weight(AFDW), ashes were obtained after incinerating sub-samples (10 g each, at 5508Cduring 6 h). Grain size distribution was evaluated by sieve and sedimentation analysisfollowing Carver (1971).

2.2.3. Small scale patterns in meiofaunal distribution associated with burrows of C.granulata

To evaluate if there was any difference in the spatial distribution of meiofauna relatedto the presence of burrows of C. granulata, meiofaunal samples were taken at threedistances from the burrow: edge, 5 cm and 10 cm from the burrow opening. Given thatcrabs make sediment mounds on one side of the burrow entrance (Iribarne et al., 1997)which may affect meiofaunal distribution, samples at each distance were repeated on theside of the mound and on the opposite side. These samples were taken from 10 burrowsof similar shape located at the same intertidal level (approximately 0.5 m over MLLW).

2.3. Experiments

2.3.1. Experimental designsAll experiments described below were performed as follows: inclusion and exclusion

treatment plots of adult crabs were performed with completely closed wire cages(50 3 50 cm area, with a mesh size of 5 mm). Cages had 60 cm length sides which werepushed into the sediment to a depth of 40 cm with 20 cm protruding above the surface.This design was performed to avoid crabs passing through their burrows. In inclusiontreatments six individuals of the corresponding species (three males and three females)within a size range of 30 to 35 mm were included. In exclusion treatment, crabs wereextracted using dead fish tied at the end of a cord as bait. In all cases treatments had 10replicates and were randomly distributed and separated each other by 10 m.

2.3.2. Discriminating the effect of crabs on benthic organisms inside crab bedsA field experiment was performed during summer 1996 to discriminate the effect of

C. granulata from the effect of other predators on benthic organisms. This experimentlasted 80 days (starting on 15 February) to ensure the presence of all predators in thearea. This experiment was run on the open mudflat with the following treatments: (1)exclusion of crabs, (2) inclusion of C. granulata; (3) inclusion of Cy. angulatus; (4)exclusion of big fishes and birds with ceilings of 50 3 50 cm standing 5 cm over thesediment by PVC pipes, (5) control for cage effect (border without ceilings), and (6)control (50 3 50 cm previously marked areas without any manipulation). Birds excludedin this experiment were principally plovers (e.g., Charadrius spp., Pluvialis squatarola),


sandpipers (Calidris spp.) and yellowlegs (Tringa spp.). Fishes were croaker (Micro-pogonias furnieri) and mullet (Mugil platanus). At the end of the experiment,macroinfauna and meiofauna samples were taken from the center of each plot.

2.3.3. Effect of C. granulata on infaunal organisms living at different depths insediment

Given that the previous experiment showed the effect of this species on benthic fauna,an experiment was performed during summer 1997 to evaluate if this effect varies withsediment depths. The experiment had two treatments: (1) exclusion and (2) inclusion ofC. granulata. The experiment ran from 18 January to 10 February (1997). Samples ofmacroinfauna and meiofauna were taken from the center of each treatment and weredivided into two layers (5 cm each) to evaluate if effect differs between depth.

2.3.4. Effect of crabs on recruitment of Cy. angulatusGiven that recruitment of the crab Cy. angulatus occurs mainly at the end of the

summer–early autumn (Luppi et al., 1994), an experiment similar to the previous oneswas performed to evaluate the effect of C. granulata and Cy. angulatus on crabrecruitment. The experiment had a duration of 40 days (starting on 2 March and includedthe recruitment period) and consisted of three treatments: (1) inclusion of C. granulata;(2) inclusion of Cy. angulatus; and (3) exclusion of crabs.

2.3.5. Inclusion of crabs in an area not inhabited by crabsPrevious experiments were performed in areas inhabited (and therefore disturbed) by

the burrowing crab C. granulata. However, areas not inhabited by crabs present theopportunity to evaluate their actual effect on the environment. Therefore, an experimentwas performed in an intertidal zone close to crab beds (distant 200 m), with the sametidal regime, and similar sediment characteristics, but not disturbed by crabs. Thisexperiment consisted of a C. granulata inclusion treatment and control treatment (similarclosed cages without crabs). Macroinfauna and meiofauna samples were taken after 40days (when placement of crabs in the new habitat was evident) and samples weredivided into two depth layers (5 cm each).

2.3.6. Effect of juvenile crabs on abundance of meiofaunal organismsA field experiment was performed to evaluate the effect of juveniles of C. granulata

on meiofaunal organisms. The experiment consisted of three treatments: (1) inclusion ofcrabs of 12 to 15 mm carapace width, (2) inclusion of crabs of 7 to 10 mm carapacewidth, and (3) control. All treatments consisted of PVC pipes (10 cm diameter 15 cmdepth), covered at the top with a plastic net (1 mm mesh size) and inserted 12 cm insidethe substrate. Four crabs were included in the two first treatments while no crabs wereadded in controls. Treatments were arranged in the intertidal zone inhabited by adults of

22this species. Cores were homogeneously perforated all around (0.5 perforations cm ) toallow water flow through sediment during the tidal cycle. The experiment had 10replicates and was run during 20 days, after which samples of meiofauna were taken anddivided into two depth layers (5 cm each).


2.4. Statistical analysis

A fixed factor MANOVA was performed to evaluate differences in polychaeteabundance between areas and among months and depth layers in Section 2.2.2.Percentage of water content and AFDW were compared between areas with t-tests (Zar,1984) and differences in grain size distribution between areas was evaluated with aKolmogorov–Smirnov two-sample test (Conover, 1980).

In Section 2.2.3 differences in mean abundance of meiofaunal organisms amongdistances from crab burrows and in both directions were evaluated with a two-fixedfactors analysis of variance (ANOVA) and a posteriori Tukey multiple comparison test(Zar, 1984).

In all experiments, treatment effect was evaluated independently for each species witht-tests or ANOVAs (Zar, 1984) and abundances were then compared between depthlayers with paired t-tests (Zar, 1984), taking each sample as a pair. When assumptionswere not met, transformations were performed or, when the problem persisted thenon-parametric Mann–Whitney or Kruskall–Wallis test (Conover, 1980) were used. ATukey test (Zar, 1984) or a non-parametric multiple comparison test (Conover, 1980)was performed after ANOVA or Kruskall–Wallis, respectively.

In Sections 2.3.2, 2.3.3 and 2.3.5, abundance of benthic organisms in experimentswere also evaluated with non-metric multi-dimensional scaling ordination (MDS), usingthe Bray–Curtis similarity measure (Warwick and Clarke, 1991). Then, the significanceof differences between treatments were evaluated with one-way ‘‘analysis of similarity’’(ANOSIM) following Clarke (1993).

3. Results

3.1. Distribution patterns of benthic organisms associated with the presence of crabs

3.1.1. Relationship between the presence of the burrowing crab C. granulata, theabundance of polychaetes and sediment characteristics

The only species found in all sampling periods was the polychaete L. acuta(Treadwell). The MANOVA showed effects of months and areas but did not showeffects of depth (Table 1; Fig. 1). Also, interactions were found between month anddepth and area and month and all three factors (Table 1). A posteriori Tukey test showedthat polychaetes were more abundant in May, July, September and November than in theother months inside the crab bed (Fig. 1). However, outside crab bed, L. acuta densityremained constant all year around (Fig. 1). In May and July abundance of polychaeteswere greater in the upper layers inside crab beds (Fig. 2). In September samples weretaken after a period of low rainfall and sediment was much dryer than in the othersampling periods. In this month, abundance increased in the deepest layers inside thecrab bed (Fig. 2). Outside crab bed no differences among depth layers were found in anymonth sampled.

The analysis of sediment characteristics showed no differences in organic mattercontent between areas (t 5 0.31, df 5 12, P . 0.05; Fig. 3A). However, sediment water


22Fig. 1. Density (ind m ) of the polychaete L. acuta in different months of the year inside (IN) and outside(OUT) crab bed. Lines connect no significant differences (P , 0.05; Tukey test) among months at each area(lines outside graph) and between areas for each month (lines inside graph). Here and thereafter box plots areconstructed with limits of boxes being the 75th and 25th percentile, lines represent 10th and 90th percentiles,lines or points inside boxes are medians, circles are outliers (StatSoft, 1998).

content was significantly greater inside the area inhabited by crabs than outside (t 5 5.1,df 5 8, P , 0.05; Fig. 3B). Grain size distribution differed between areas (T 5 0.42,n 5 26, n 5 33; P , 0.05; Fig. 3C). Sediment in the area inhabited by crabs was1 2

mainly silt (80% silt, 16% sand) and outside crab beds, it was mainly sand (58% sandand 40% silt).

3.1.2. Small scale patterns in meiofaunal distribution associated with burrows of C.granulata

In this sampling site, the most abundant organisms recorded were nematodes. Thetwo-way fixed factor ANOVA showed only interaction effects (data were log trans-formed to meet the assumptions of homocedasticity; direction: F 5 4.5, df 5 1, 42,

Table 1Results of MANOVA analysis (* 5 P , 0.05)

Source of variation df MS F

EffectMonth 5 96.028 13.478*Area 1 498.719 69.989*Depth 4 12.291 1.7255Month–area 5 84.738 11.892*Month–depth 20 21.110 2.962*Area–depth 4 14.369 2.016Month–area–depth 20 19.484 2.734*

Error 380 7.126


22Fig. 2. Density (ind m ) of the polychaete L. acuta in each depth layer inside (IN) and outside (OUT) crabbed and in each sampling month: May (A), July (B), September (C), November (D), January (E) and March(F).

P . 0.05; distance: F 5 3.51, df 5 2, 42, P . 0.05; interaction: F 5 14.4, df 5 2, 42,P , 0.05; Fig. 4). Interaction was important indicating that distance has different effectsdepending on if we consider mound or no mound direction. The multiple meancomparison Tukey test performed taking both factors jointly (Neter et al., 1990), showedthat in the mound direction the lower abundance was at the edge of the burrow and themaximum was at 10 cm. However, in the opposite direction, the lower abundance was at5 cm, and it increased at the edge of the burrow (Fig. 4). The abundance of ostracodswas lower, and no effect was found (direction: F 5 2.44, df 5 1, 42, P . 0.05; distance:F 5 2.08, df 5 2, 42, P . 0.05; interaction: F 5 0.8, df 5 2, 42, P . 0.05; Fig. 4).Copepods and amphipods were not present in this sampling.

3.2. Experiments

3.2.1. Discriminating the effect of crabs on benthic organisms inside crab bedsThe benthic organisms found in the experimental sites were: nematodes, ostracods,

copepods, the polychaetes L. acuta, Nephtys fluviatilis (Monro) and H. similis (Soath-ern), the amphipod Corophium insidiosus and a nemertean non-identified species.

When each species was evaluated independently, treatment effects were found for L.


Fig. 3. Sediment characteristics INSIDE and OUTSIDE crab beds. (A) Percentage of AFDW (mean 1 1 SD),(B) percentage of water content (mean 1 1 SD); and (C) grain size distribution. Lines connect no significantdifferences (P . 0.05).

acuta (Kruskall–Wallis test; H 5 11.22, df 5 5, 60; P , 0.05), increasing the density inthe total exclusion treatment compared with the control and the exclusion of fishes andbirds (Fig. 5A). Differences among treatments were also found for nematodes (Kruskall–Wallis test; H 5 12.25, df 5 5, 60; P , 0.05; Fig. 6A), where differences were due to anincrease of this group in the exclusion treatment in comparison with the treatment withenhanced density of C. granulata. No differences existed among treatments for H.similis (Kruskall–Wallis test; H 5 2.45, df 5 5, 60, P . 0.05; Fig. 5B), copepods(Kruskall–Wallis test; H 5 4.7, df 5 5, 60, P . 0.05; Fig. 6B) ostracods (Kruskall–

22Wallis test; H 5 4.9, df 5 5, 60, P . 0.05; Fig. 6C), N. fluviatilis (x 5 6.4 ind m ,SD 5 27.9, Kruskall–Wallis test: H 5 3.1, df 5 5, 60, P . 0.05), Co. insidiosus (x 5 18

22ind m , SD 5 45, Kruskall–Wallis test: H 5 2.11, df 5 5, 60, P . 0.05) or the22nemertean non-identified species (x 5 22.7 ind m , SD 5 48.9, Kruskall–Wallis test:

H 5 8.6, df 5 5, 60, P . 0.05).


22Fig. 4. Density of nematodes and ostracods (ind cm ) at different distances from the burrow, in the mounddirection (mound) and in the opposite one (no mound). Equal letters indicate no significant differences(P . 0.05).

MDS ordination of samples showed no treatment effect on the benthic communitystructure (Fig. 7) and this was confirmed by ANOSIM (R 5 0.09; P . 0.01).

3.2.2. Effect of C. granulata on infaunal organisms living at different depths insediment

The most abundant organisms found during this experiment were nematodes and thepolychaete L. acuta. When each species was evaluated, no effect was found on theabundance of L. acuta at any depth layer [upper layer: data were transformed; x9 5 log(x 1 1), t 5 1.6, df 5 16; lower layer: Mann–Whitney U 5 44.5, n 5 9, n 5 10; P .1 2

0.05; Fig. 8A). No difference was found in abundance of this polychaete between bothdepth layers [transformed data x9 5 log (x 1 1), t 5 1.98, df 5 18, P . 0.05; Fig. 8A).However, nematodes significantly increased in abundance in the upper layer (data werelog transformed, t 5 2.4, df 5 18, P , 0.05), while no difference were found betweentreatments in the lower layer (log transformed data, t 5 2 0.75, df 5 17, P . 0.05; Fig.8B). Abundance of nematodes was greater in the upper layer than in the lower layer(t 5 8.42, df 5 21, P , 0.05; Fig. 8B). Other organisms found in the upper layer without


Fig. 5. Results on macroinfauna of the experiment to discriminate the effect of crabs. Box plots show the22abundance (ind m ) of the polychaetes (A) L. acuta and (B) H. similis in each treatment: control (CON),

birds and fishes exclusion (B&F EXC), C. granulata inclusion (CG INC), Cy. angulatus inclusion (CA INC),cage control (CAGE CON), and total exclusion (EXC). Lines connect no significant differences (P . 0.05).

22differences in abundance between treatments were: ostracods (x 5 0.7 ind cm , SD 5220.8, t 5 1.67, df 5 17; P . 0.05); copepods (x 5 1.5 ind cm , SD 5 1.34, t 5 0.75,

22df 5 17; P . 0.05); N. fluviatilis (x 5 6.36 ind m , SD 5 28.48, t 5 1, df 5 9; P .c220.05) and Co. insidiosus (x 5 25.4 ind m , SD 5 66.6, t 5 0.8, df 5 12.7; P . 0.05).c

22Also, no treatment effect was found for H. similis (x 5 95.5 ind m , SD 5 48.3,22t 5 1.3, df 5 18; P . 0.05) and the nemertean non-identified species (x 5 9.1 ind m ,c

SD 5 6.6, t 5 1.9, df 5 9; P . 0.05), which were both present in the lower layers.c

MDS and ANOSIM showed significant grouping of treatments (stress 5 0.001; R 5

0.39 P , 0.01; Fig. 9), indicating differences between treatments in the communitystructure.

3.2.3. Effect of crabs on recruitment of Cy. angulatusJuveniles of the crab Cy. angulatus (carapace width: x 5 5.82 mm, SD 5 1.35, n 5 18)

22were found only in the control treatment (density: x 5 165.5 ind m , SD 5 46.7,


22Fig. 6. Results on meiofauna of the experiment to discriminate the effect of crabs. Density (ind cm ) of (A)nematodes, (B) copepods and (C) ostracods in each experimental treatment: C. granulata inclusion (CG INC),birds and fishes exclusion (B&F EXC), control (CON), cage control (CAGE CON), Cy. angulatus inclusion(CA INC), and total exclusion (EXC). Lines connect no significant differences (P . 0.05).

n 5 10). These crabs made superficial burrows that covered the entire control areas. Themost abundant infaunal organisms in this period were H. similis, copepods andnematodes. No differences among treatments were found for H. similis at any depthlayer (ANOVA: superficial layer: F 5 2.56, df 5 2, 17; deep layer: F 5 4.36, df 5 2, 17;P . 0.05; Fig. 10A). Abundance of this polychaete was the same in both depth layers(t 5 0.08, df 5 29; P . 0.05). However, copepods were found only in the upper layer,


Fig. 7. MDS ordination of replicates of the different treatments in the experiment to discriminate the effect ofcrabs from other predators. C. granulata inclusion (CG INC), birds and fishes exclusion (B&F EXC), control(CON), cage control (CAGE CON), Cy. angulatus inclusion (CA INC), and total exclusion (EXC).

and no significant differences in abundance among treatments were found (logtransformed data: ANOVA F 5 2.59, df 5 2, 24, P . 0.05; Fig. 10B). Nematodesdecreased significantly in the upper layer when Cy. angulatus crabs were included (logtransformed data, ANOVA: F 5 4.01, df 5 2, 20, P , 0.05, Fig. 10C). However, notreatment effect was found at the lower layer (ANOVA: F 5 0.75, df 5 2, 20, P . 0.05).Nematodes were more abundant in the superficial layer (t 5 2.76, df 5 24, P , 0.05; Fig.10C). Other organisms found in this experiment in low abundance with no differences

22between treatments were the polychaete Neanthes succinea (x 5 46.7 ind m , SD 52278.3; Kruskall–Wallis test: H 5 0.75 ind m , df 5 2, 30, P . 0.05), L. acuta (x 5 25.47

22ind m , SD 5 77.7; Kruskall–Wallis: H 5 0.67, df 5 2, 30, P . 0.05), Co. insidiosus22 22(x 5 11 ind cm , SD 5 22; Kruskall–Wallis: H 5 4 ind m , df 5 2, 30, P . 0.05) and

22the nemertean non-identified species (x 5 21.2 ind m , SD 5 48.2; Kruskall–Wallis:H 5 4.5, df 5 2, 30, P . 0.05).

3.2.4. Inclusion of crabs in an area not inhabited by crabsThe most abundant infauna in this experiment were the polychaetes H. similis and L.

acuta, nematodes and copepods. Both polychaete species were found only in thesuperficial layer and significantly decreased in abundance in the inclusion treatment (H.similis: log transformed data t 5 2 2.46, df 5 12; Fig. 11A; L. acuta: t 5 2 2.34,df 5 14; P , 0.05; Fig. 11B). Copepods were also found only in the upper layer, but nosignificant differences between treatments were found (log transformed data: t 5 0.86,df 5 12, P . 0.05; Fig. 11C). Nematodes were found in both depth layers but were moreabundant in the superficial layer (t 5 5.88, df 5 13, P , 0.05). These organisms showed


Fig. 8. Results of the experiment to evaluate crab effect on organisms living at two depths in sediment.22 22Density of (A) the polychaete L. acuta (ind m ) and (B) nematodes (ind cm ), in exclusion and inclusion

treatments and at both depth layers. Lines connect no significant differences (P . 0.05).

Fig. 9. MDS of experiment samples of EXCLUSION and INCLUSION of C. granulata.


22 22Fig. 10. Density of (A) the polychaete H. similis (ind m ), (B) copepods (ind cm ) and (C) nematodes (ind22cm ), in the three treatments, and at both depth layers. Lines connect no significant differences.

no differences in abundance between treatments at any layer (upper layer: t 5 2 0.35,df 5 12; lower layer: t 5 0.84, df 5 12; P . 0.05, Fig. 11D). Other organisms found in

22low density without differences between treatments were ostracods (x 5 0.13 ind cm ,22SD 5 22; t 5 0.6, df 5 12, P . 0.05) Co. insidiosus (x 5 27.2 ind m , SD 5 54.2;

22t 5 0.61, df 5 12, P . 0.05) and the nemertean non-identified species (x 5 27.2 ind m ,SD 5 54.2; t 5 0.6, df 5 12, P . 0.05).

MDS ordination did not show grouping of treatments (stress 5 0.00001; ANOSIM:R 5 0.09, P . 0.01; Fig. 12).

3.2.5. Effect of juvenile crabs on abundance of meiofaunal organismsDuring this experiment, the meiofauna was composed only by nematodes. These

organisms were significantly more abundant in the upper layer than in the lower layer


22 22 22Fig. 11. Density of (A) H. similis (ind m ), (B) L. acuta (ind m ), (C) copepods (ind cm ) and (D)22nematodes (ind cm ), in INCLUSION and CONTROL treatments outside crab bed, and at both depth layers.

Lines connect no significant differences.

[t 5 5.04, df 5 9, P , 0.05; data were transformed by x9 5 log (x 1 1) to meet normali-ty]. However, no effect of juvenile crabs was found at any layer (upper layer: ANOVA:F 5 2.96, df 5 2, 27; lower layer: log transformed data, ANOVA: F 5 0.44, df 5 2, 27;P . 0.05; Fig. 13). Copepods and ostracods were also found in this experiment, but dueto their low density no statistical analysis was performed.

4. Discussion

Results showed that the polychaete L. acuta was more abundant in the crab bed wheresediment was finer and with a higher water content. However, inside crab bed, this


Fig. 12. MDS of experiment samples of INCLUSION of C. granulata and CONTROL treatment in an areauninhabited by crabs.

polychaete species was affected by the activity of the crab C. granulata. This crab alsoaffected nematode abundance in the superficial layer and their distribution on a smallscale around burrows. The recruitment of the crab Cy. angulatus was also affected byadults of the same species and of C. granulata. When adults of C. granulata were addedin an area previously not inhabited by crabs, the abundance of the polychaetes L. acutaand H. similis decreased. Juveniles of C. granulata did not affect meiofauna.

Many studies have shown that large scale patterns in abundance are often correlated

22Fig. 13. Density of nematodes (ind cm ) when juveniles of C. granulata of 12 to 15 mm (12–15 mmCRABS) and of 7 to 10 mm (7–10 mm CRABS) in carapace width were added, and when no crabs wereadded (CONTROL). Lines connect no significant differences.


with changes in sediment grain size and sediment sorting (Logbottom, 1970; Posey,1986), principally affecting the distribution of some deposit feeders (Whitchlach, 1981;Taghon, 1982). Deposit feeders, moreover, are known to strongly influence the physicalcharacteristics of the environment, particularly through active burrowing (Rhoads andYoung, 1970; Posey, 1986; Levinton, 1989). The most common effects are an increasein water content (specially in sediments with high contents of silt and clay; Rhoads andYoung, 1970) and the redistribution of sediment particles (Levinton, 1989). Thesecommon effects of deposit feeders on sediment, suggest that sediment characteristicsfound in our study could be in part caused by the burrowing activity of C. granulata,especially considering that these crabs rework large amounts of sediment (Iribarne et al.,1997). Previous studies showed an enhanced content of organic matter associated withthese organisms (Rhoads and Young, 1970), but we found no increases in organic mattercontent inside crab beds. However, burrows of C. granulata, in this environment, workas traps for detritus (Iribarne et al., 1997), which suggest that organic matter mayconcentrate inside burrows and decrease at the surface.

The effect of C. granulata on sediment, therefore, may determine the distribution ofother deposit feeders. Trophic group amensalism hypothesis predicts patterns of infaunaldistribution where trophic modes are separate (Rhoads and Young, 1970; Posey, 1990).Although no studies exist in this environment about trophic modes of most organismsfound, sediment observed in the gut of the polychaete L. acuta (F.B., pers. obs.) suggeststhat these organisms deposit feed in mudflats. This polychaete showed a largerabundance inside crab beds, probably favored by reworked sediment. Although organicmatter content did not vary, availability may be lower outside crab beds due to largergrain size, since most deposit feeders collect particles greater than 100 mm withdifficulty (Levinton, 1989).

Although crabs could benefit the polychaete L. acuta by making sediment environ-ment more suitable for them, manipulative experiments showed that polychaetes arenegatively affected by crab activity. Also the fact that polychaete abundance greatlydecreased during summer may be in part caused by the increase of crab activity duringthis period. In the experiment to discriminate the effect of crabs, the polychaete L. acutaincreased its density in the exclusion treatment, compared with the control and theexclusion of birds and fishes treatment, indicating that vertebrates did not affect theirabundance. No effect was found when each crab species was included, indicating thatprobably the effect was due to a combined effect of both crab species. In the otherexperiments inside crab beds, no effect was found for C. granulata on L. acuta possiblybecause the density of this polychaete was too low to enable effect to be evaluated.However, crabs added to an undisturbed sediment greatly decreased the abundance of L.acuta. The same pattern occurs with the polychaete H. similis which was not affected bycrabs inside crab beds.

Local studies on stomach contents of Cy. angulatus showed that this species feeds onworms and detritus (Olivier et al., 1972b), thus, this crab is probably preying on L.acuta. Several previous studies have reported predation on polychaetes by crabs (e.g.,Virnstein, 1977; Kneib and Weeks, 1990). The burrowing crab C. granulata is a depositfeeder and no evidence exists that shows that this crab preys upon polychaetes (Olivieret al., 1972b; Iribarne et al., 1997), even though there is evidence that bioturbators affect


polychaetes (Brenchley, 1981; Posey et al., 1991). The different effects inside or outsidecrab beds may be interpreted as the result of greater bioturbation when crabs areexcavating new burrows (Posey et al., 1991). Outside the crab bed, sediments were morecompact, probably reducing mobility of polychaetes and thus making them moresusceptible to sediment disturbances associated with burrow digging (Tamaki, 1988).

Samples of meiofauna collected at different distances from burrow entrances of C.granulata showed that meiofaunal distribution patterns are influenced by the presence ofburrow structures. Posey (1986) suggested that small scale patterns in species abundancein soft sediments could be the result of current velocity directly affecting larval transportand settlement. Meiofaunal animals although lacking pelagic larval stages are themselvesso small that even as adults they might disperse transported while suspended in the watercolumn (Gerlach, 1977; Palmer, 1988). Nematodes are highly susceptible to beingpassively transported (DePatra and Levin, 1989) and given that depressions in surfacesediments enhance the deposition of suspended material by decreasing shear stress(DePatra and Levin, 1989), depressions like burrow entrances may increase thedeposition of nematodes (DePatra and Levin, 1989; Sun and Fleeger, 1994; Iribarne etal., 1997). The low abundance of nematodes in the mound direction could be due to thecontinuous deposition of sediments on this side by crabs which may be enhancing thesuspension of nematodes and their transport to other sites or just affecting their survival.As suggested by DePatra and Levin (1989) low densities of nematodes may also be aresponse to decreased food supply.

Another important result is the effect of both crab species C. granulata and Cy.angulatus on settlement of Cy. angulatus. Juveniles of Cy. angulatus in this environmentare confined to areas with refuges, like areas with stones, or in crevices of Ficopomatusenigmaticus, a tube building polychaete (Spivak et al., 1994). This pattern of distributioncould be the result of active habitat selection by megalopae, or differential survivorship.Several field and laboratory studies have shown that megalopae are capable of selectingsettling sites on the bases of their physical or chemical conditions (Castro, 1978; Jensen,1991; Boudreau et al., 1993; Fernandez et al., 1993). A recent study in this environmentshowed that megalopae of Cy. angulatus due to their swimming ability under flowvelocities, are able to maneuver and select settlement sites (Valero et al., 1997). In thepresent study, experimental cages may have been detected as refuges, favoringsettlement inside them. However, no larvae survived when adult crabs were present,indicating that predation by C. granulata and cannibalism are important regulatingfactors. Cannibalism was also demonstrated under laboratory conditions (Luppi et al.,1995), and as with other crab species (Fernandez et al., 1993; Moksnes et al., 1997) maybe important in the regulation of settlement success.

All the evidence accumulated in the present study strongly suggests that, similarly toother burrowing crustaceans (i.e., Callianassa and Upogebia; Callianassidae; Posey,1986; Posey et al., 1991) C. granulata has an important effect on the sedimentcomposition, habitat structure and on some benthic organisms. Although multivariateanalyses did not showed effect on the benthic community structure in most cases, thelow diversity suggest that an effect on the most abundant organisms (i.e., polychaetesand nematodes) may have important implications in the whole community. For example,the decrease of polychaetes produces the decrease of food available for shorebirds. All


these evidences suggest that C. granulata, mainly due to their bioturbation activities,may be considered an important species on SW Atlantic marshes. Thus, we suggest thatthis species should be considered in any marsh conservation endeavor.

Acknowledgements

We gratefully acknowledge G. Palomo, J.Valero, J. Gutierrez and L. Lucifora for fieldassistance and M. Kittlein for advice in statistical analysis. We also thank twoanonymous reviewers for their helpful comments. This project was supported by the

Úniversidad Nacional de Mar del Plata (051/94), Fundacion Antorchas (13016/1-00012) and the International Foundation for Science (No. A/2501-1). F.B. was

´supported by a scholarship from the Consejo Nacional de Investigaciones Cientıficas y´Tecnicas (CONICET).

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