Infaunal recruitment patterns in soft bottom habitats of the Patos Lagoon estuary , southern Brazil : influence of Chasmagnathus granulata ( Brachyura , Grapsidae ) disturbance

A comparative study of the infaunal recruitment patterns among disturbed surface sediment mounds around Chasmagnathus granulata Dana, 1851 burrows and undisturbed adjacent sediments was done in two intertidal soft bottom habitats (an upper and a lower mudflat zone) in an estuarine inlet of Patos Lagoon, southern Brazil. The most abundant infaunal organisms were recruits of the polychaete Laeonereis acuta Treadwell, 1923 and of the tanaid Kalliapseudes schubartii Mañé-Garzón, 1949. The densities of these species did not differ significantly between upper and lower mudflat habitats. These species showed lower densities around crab burrows than in adjacent areas, where differences in sediment characteristics were observed as well. The results indicate that C. granulata disturbances may play an important role in regulating the soft bottom benthic community by controlling infaunal recruitment in the estuarine intertidal mudflats of the Patos Lagoon.

In spite of its behavior, abundance and extensive distribution, little information is available about the effects of this crab on the structure of the benthic community in the intertidal areas of the Patos Lagoon estuary.Studies performed in other regions have not evaluated their effects on macrofaunal recruitment (IRIBARNE et al., 1997;BOTTO & IRIBARNE, 1999).The aim of the present study is to compare the infaunal recruitment pattern among disturbed sediment mounds around C. granulata burrows and undisturbed adjacent sediments in two intertidal soft bottom habitats (an upper and a lower mudflat zone) in an estuarine inlet of Patos Lagoon.

MATERIAL AND METHODS
The study was performed in January/2000 (summer) in an area located near the east margin of Pólvora Island, Patos Lagoon, southern Brazil (fig.1).Two habitats were selected along the intertidal area: (1) an upper mudflat zone and (2) a lower mudflat zone.The mean density of crab burrows in these habitats was 34 (± 3.5) and 14 (± 2.2) burrows m -2 , respectively.
In each habitat nine samples were taken at each of two locations: in disturbed sediment mounds around crab burrows and in undisturbed adjacent areas distant approximately 30 cm from the burrow.The samples were collected with a corer of 2.6 cm inner diameter.The first 2 cm of the collected material were preserved with formalin (4%) and stained with the vital stain Bengal Rose.Abiotic parameters such as pH and potential redox (Eh) were measured with an electronic meter.Surface sediment samples (from the first 2 cm) were collected in order to determine the granulometry and organic matter content.
At the laboratory, the samples were washed in a series of sieves with apertures of 500, 250, 125 and 63 µm.The use of different mesh sizes, smaller than that traditionally used (0.5 mm) for macrofaunal studies recent settlers.Mesh size was used to determine the size classes of infaunal organisms during their recruitment period.Infaunal size class was defined by mesh size in which the individuals were retained.The retained material in each mesh was sorted, identified and quantified with a stereoscopic microscope.
Granulometric data were obtained through sieving and pipette analysis.Dried sub-samples were then burned at 550°C for 60 min in order to determine organic content through weight loss (SUGUIO, 1973).
Two-way ANOVA was used to test for differences in both abiotic parameters and biological data (i.e., each infaunal size class as dependent variable) among habitats (upper and lower mudflat zones) and locations (undisturbed adjacent areas and sediment mound).All data were tested for normality (Kolmogorov-Smirnov test) and homogeneity of variances (Cochran test and standard deviations-means plots) prior to their use in statistical tests (UNDERWOOD, 1997).Data were transformed to assure variance homogeneity and distribution normality when necessary.In cases in which the ANOVA result was significant (p<0.05), the Tukey's HSD post hoc test was applied (UNDERWOOD, 1997).

RESULTS
All abiotic parameters varied significantly between the habitats (tab.I).Sediment composition ranged from moderately sorted fine sand in the lower mudflat to very poorly sorted finest sand in the upper mudflat zone.Fine fractions and organic matter increase from lower to upper mudflat zone, while redox potential (Eh) and pH decreased (tab.I).Comparing among locations only fine fractions  had 250 and 500 µm size classes, respectively.For K. schubartii, 14 %, 55 % and 31 % of recruits had 125, 250 and 500 µm size classes, respectively.ANOVA results showed that differences in the densities of all size classes were not significant among habitats for both species (tab.III).Also, significant differences were found among locations for both species (tab.III).In both habitats, all L. acuta size classes had higher densities at adjacent areas than on sediment mounds (figs.2, 3).For K. schubartii, higher densities were also found at adjacent areas than on mounds, except for individuals of 125 µm size class (figs. 4, 5).
densities around crab burrows than in adjacent areas, thus suggesting a possible effect of the burrowing crab Chasmagnathus granulata on recruitment of infaunal organisms.Also, there were found differences in sediment properties among locations (i.e., lower fines proportion at sediment mounds than at adjacent areas).
Both infaunal species are commonly found in high densities in shallow water flats of the Patos Lagoon estuary (BEMVENUTI, 1997).As the temperature increases in late spring and early summer, the reproductive activity of infaunal species increases, resulting in dense recruitment in the estuarine inlets of the region (BEMVENUTI, 1987;1997).During the recruitment period these species are also subjected to strong populational control by epifaunal macropredators (BEMVENUTI, 1987;1997).
The burrowing crab C. granulata is a depositfeeder but, despite deposit feeders can indirectly ingest newly settled organisms (WOODIN, 1976), did not exist evidence that this crab selectively preys upon infaunal organisms (D'INCAO et al., 1990;IRIBARNE et al., 1997;BOTTO & IRIBARNE, 1999).The effects of this crab on infaunal recruitment are mainly related to an intense sediment disturbance because of the burrowing activities.
The crabs activities increase the sediment instability and thus inhibit the settlement and/or persistence of infaunal recruits.Studies have shown that interactions with burrowing organisms affect recruitment rates (PETERSON, 1982;PETERSON & BLACK, 1993;ÓLAFSSON et al., 1994;THRUSH et al., 1996), limiting infaunal density through bioturbation (BRENCHLEY, 1981;POSEY, 1986;POSEY et al., 1991).BRENCHLEY (1981) experimentally demonstrated that the addition of macroinfaunal or macroepifaunal organisms affects the infauna, resulting in lower densities, especially of tube-building organisms.This effect was also related to increasing sediment instability promoted by burrowing activities.
The crab disturbance caused by continuous sediment deposition around the burrows could also increase mortality of infaunal recruits by suffocation.Alterations of sediment properties by crab activities could indirectly affect infaunal recruitment.Both L. acuta and K. schubartii are tube builders and need fine sedimentary fractions for constructing their tubes (BEMVENUTI, 1997;ROSA-FILHO & BEMVENUTI, 1998).Consequently, undisturbed adjacent areas, which have more fine proportions than sediment mounds, are more suitable for their recruitment.
BOTTO & IRIBARNE (1999) evaluated the C. granulata effects on macrofauna community in a coastal lagoon of Argentina.These authors verified that L. acuta densities greatly decreased during summer inside crab beds.The decrease of polychaete densities was attributed to increase of crab activity during summer period, although their field experiments (i.e., the use of exclusion cages) failed to detect significant effects.The undetected effects in BOTTO & IRIBARNE'S (1999) experiments, where the faunal samples were washed in a 500 µm mesh size, are probably related to methodological problems.
The present results demonstrated that most L. acuta recruits (> 50 %) were retained in 125 µm mesh size and only 6 % in 500 µm.Therefore, the utilization of an 500 µm mesh size seems inappropriate for evaluating the effects of burrowing crabs on infauna during the recruitment period.In this way, lower polychaete densities observed in summer by BOTTO & IRIBARNE (1999) may be consequence of crab effects on infaunal recruitment.We suggest that the burrowing crab C. granulata may play an important role in regulating local soft bottom benthic communities by controlling infaunal recruitment in the estuarine intertidal mudflats of the Patos Lagoon.

Figs. 2
Figs. 2, 3. Mean density (ind.10 cm -2 ) of the different size classes of the polychaete Laeonereis acuta in undisturbed adjacent areas (empty bars) and crab mounds (closed bars) at: 2, lower mudflat; 3, upper mudflat zone.Error bars are ± 1 SD.Asterisks indicate significant differences (p<0.05)among locations on the same size class determinated by Tukey post hoc test.

Table II .
Infaunal recruitment patterns in soft bottom habitats of the Patos Lagoon estuary,... varied significantly, with higher values in adjacent areas than on sediment mounds (tab.I).Habitats vs. locations interactions were not significant for any parameter and mean values of each parameter are given in tab.II.Mean values and standard deviation (in parenthesis) of abiotic parameters measured in both locations at each habitat.