Shell occupation by the endemic western Atlantic hermit crab Isocheles sawayai ( Diogenidae ) from Caraguatatuba ,

The aim of this study was to characterize the pattern of shell occupation by the hermit crab Isocheles sawayai Forest and Saint-Laurent, 1968, from the Caraguatatuba region. The percentage of shell types that were occupied and the morphometric relationships between hermit crabs and occupied shells were analyzed from systematized collections that were conducted monthly from July 2001 to June 2003. A total of 373 individuals were captured (297 males, 41 non-ovigerous females, 25 ovigerous females and 10 intersexes), occupying 17 species of gastropod shells. Stramonita haemastoma (Linnaeus, 1767) (49.87%) was the significantly most occupied species (χ = 89.30; P < 0.05) followed, with no significant difference, by Phalium granulatum (Born, 1778) (11.53%), Polinices hepaticus (Roding, 1798) (8.31%) and Cymatium parthenopeum (von Salis, 1793) (6.97%). All the morphometric relationships between hermit crabs and occupied shells showed high (r > 0.68) and significant (P < 0.05) correlation values, which is an important indication that in this I. sawayai population the animals occupied adequate shells. The high number of occupied shell species and relative plasticity indicated that, for the studied population, occupation is influenced by the shell availability.


Introduction
The intriguing mechanism of shell occupation developed by hermit crabs is intimately related to the protection of the non-calcified abdomen against predators (Reese, 1969;Vance, 1972a) and other hermit crabs (Conover, 1978), and against mechanic abrasions, desic-cation, osmotic and thermal stress (Reese, 1969;Bollay, 1964;Bertness, 1981a;1982).However, the shell may limit the hermit crab growth (Markham, 1968;Vance, 1972a), influence the fecundity and the spawn size and restrict reproduction and population growth (Provenzano, After collection the specimens were sorted, frozen and transported to the laboratory where they were removed form their shells, counted, weighed (wet weight, WW), measured for the shield length (SL) and width (SW), and the left chelar propodus length (LPL).The sex was identified by the gonopore position.
The species of occupied gastropod shells were identified according to Rios (1994), and measured for the aperture length (SAL) and width (SAW), and dry weight (SDW).The shell internal volume (SIV) was obtained according to Bertness (1981b), modified by Mantelatto and Garcia (2000), determining the sand volume (diameter of 0.25 to 0.125 mm) required to fill the empty shell.Occurrence of epibionts on the external surface of occupied shells was checked with no characterization of the position of infestation.Epibionts were identified at the major group level and the percentage of each group was calculated.
The percentage of the different occupied shell species was tested by the chi-square, and the size of occupied shells was evaluated by ANOVA on Ranks.Relationships between occupied shells and hermit crab dimensions were verified by regression analysis and correlation coefficients.The level of significance adopted was 0.05 (Zar, 1996).The specimens collected are deposited in the Crustacean Collection of the Biology Department of the Faculty of Philosophy, Sciences and Letters of Ribeirão Preto, University of São Paulo, Brazil (CCDB/FFCLRP/USP, accession numbers 1687-1691).
Isocheles sawayai Forest and Saint-Laurent, 1968 is a filter infralittoral benthic species that lives partially buried in sand bottom, in moderate and low profundities (Melo, 1999).The geographical distribution of this species is restricted to the western Atlantic coast, from Venezuela to Brazil (Santa Catarina) (Coelho and Ramos, 1972;Nucci and Melo, 2000).
The pattern of shell occupation of I. sawayai previously described by other authors in Brazil was made through a concentrated effort of capture during a specific period, which may not reflect all the necessary information about this aspect.In this context, this paper characterized the pattern of gastropod shell occupation by I. sawayai, in the Caraguatatuba region, northern littoral of São Paulo state coast, by systematized collection and analysis, using the percentage of shell occupation and demonstrating the shell variables that best fit the hermit crabs.Such information contributes to a better understanding of the poor knowledge of the biology of this species as well as of other shallow water ones on the western coast.

Material and Methods
The hermit crabs were collected monthly from July 2001 to June 2003, in the Caraguatatuba region (23° 36' 08"-23° 47' 07" S and 45° 20' 03"-45° 08' 30" W), on the northern littoral coast of São Paulo state, using a fishing boat with two double-rig trawl nets (20 mm mesh size in the net body and 15 mm in the cod end).Each sample was of approximately 30 minutes, at two knots main velocity.intersexes = 4) (Table 1).A greater shell species diversity occupation was observed for intermediate sized individuals (4.4-8.6 mm of SL) (Figure 2).
The shells occupied by males, ovigerous females and intersexes were not significantly different for aperture length and dry weight but were significantly larger than those occupied by non-ovigerous females.Shells occupied by males and intersexes had similar aperture width which were significantly larger than those occupied by females (non ovigerous and ovigerous).Shell internal volume was not significantly different among the groups of individuals.
Epibionts occurred on the external surface of 57.37% (n = 214) of I. sawayai occupied shells, and on 14 of ing 5.36% of the total occupied shell species, and were grouped and named as others.
Males and non-ovigerous females were observed inhabiting 14 and 10 of the 17 shell species occupied by I. sawayai, respectively, which represents a more diversified occupation pattern than that exhibited by the other groups of individuals (ovigerous females = 5; high (r > 0.68) and significant correlation coefficients (Table 2).Among them, the relationships with the shell internal volume (SIV) showed the highest values of correlation coefficients.In relation to the animals' dimensions, the relationships of the wet weight (WW) exhibited the highest values of correlation coefficients.Thus, SIV x WW was the relationship that best described the association between the hermit crabs and the occupied shells.Regression analyzes of the four most occupied shell species by I. sawayai (S. haemastoma, P. granulatum, P. hepaticus and C. parthenopeum) were evaluated and, all analyzed relations showed significant correlations (P < 0.05) (Table 2).The lowest correlation coefficients were verified by animals inhabiting P. granulatum (Table 2).

Discussion
Isocheles sawayai occupied 17 gastropod shell species in the Caraguatatuba region, a great number when compared with a previous study that recorded I. sawayai occupying only six gastropod shell species (Pinheiro et al., 1993) probably as a result of a non systematized effort of collection.Stramonita haemastoma was the one most occupied by the studied population (49.87%).This occupation percentage can be considered moderate when compared to other I. sawayai populations and other hermit crab species, which inhabited the most occupied shell species in higher percentages (60.6 to 90%) (Hebling and Wernick, 1974;Pinheiro et al., 1993;Bertini and Fransozo, 2000;Floeter et al., 2000;Biagi et al., 2006;Terossi et al., 2006).Considering that some shell species were occupied accidentally and almost half of the population inhabited one shell species in particular, I. sawayai showed a high plasticity in relation to shell diversity occupation which was also exhibited by this hermit crab population in Venezuela (Galindo et al., 2008).A similar pattern of plasticity on shell occupation was related for other shallow water hermit crab species (Mantelatto and Garcia, 2000;Mantelatto and Dominciano, 2002;Mantelatto and Meireles, 2004;Meireles, 2006, respectively) on the northern littoral coast of São Paulo state.
All regression analysis between hermit crabs and shell measures for the total occupied shells exhibited 3.7 -l 4.4 4.4 -l 5.1 5.1 -l 5.8 5.8 -l 6.5 6.5 -l 7.2 7.2 -l 7.9 7.9 -l 8.  (Mantelatto and Garcia, 1999).Furthermore ovigerous females occupied shells with aperture length and dry weight significantly higher than non-ovigerous females.Ovigerous females occupying shells larger than the adequate ones may represent high energetic costs for carrying the shell, to keep it clean of sediment, to defend it during a competition, and to look for food, which may reduce the reproductive output (Fotheringham, 1976a).On the other hand, occupying larger shells may allow the animal to reach its potential growth (Markham, 1968), offer greater protection against predators (Reese, 1969;Vance, 1972b;Siu and Lee, 1992), and specially for the ovigerous females the occupancy of larger shells can result in a fecundity increase (Mantelatto et al., 2002), probably due to greater available space and egg protection (Mantelatto and Garcia, 1999;Mantelatto and Dominciano, 2002).Furthermore, according to Hahn (1998), hermit crabs that occupy heavier shells do not have high energetic costs to carry this shell if the food is transported by water flows, allowing reduced movement, which may probably occur with I. sawayai, a hermit crab species that partially buried with its filtering antennas vertically positioned to the water current (Melo, 1999).
A differential pattern of shell occupation among the sexes should be related to male and female different preferences, to a competitive dominance of a sex, to both factors (Yoshino et al., 2001), or to different size rates among sexual groups (Abrams, 1988).Males hermit crabs are usually larger than females (Fransozo and Mantelatto, 1998;Manjón-Cabeza and García-Raso, 1998;Mantelatto and Sousa, 2000;Garcia and Mantelatto, 2001;Branco et al., 2002;Martinelli et al., 2002;Litulo, 2005a;2005b;Mantelatto et al., 2005;Biagi et al., 2006) mainly because of the differential energy investment they present, females must divert part of this energy to the reproductive process while males invest in Although the occurrence of another seven hermit crab species in the studied non-consolidated infrallitoral region was registered (Meireles et al., in press), interspecific competition should be a factor with little or no influence in the pattern of shell occupation of the studied population.Such inference is based on the differential spatial distribution, where the specimens of I. sawayai occurred more frequently at a lower depth (5 m) than the coexistent hermit crab species in the Caraguatatuba region, such as Dardanus insignis (Saussure, 1858), Pagurus exilis (Benedict, 1892) and Loxopagurus loxochelis (Moreira, 1901), and that were registered frequently at 15-20 m of depth (Meireles, 2006;Meireles et al., 2006;Ayres-Peres and Mantelatto, 2008, respectively).
The high number of occupied shell species and relative plasticity indicated that, for the studied population, occupation is influenced by the shell availability.However, considering that almost half of the population occupied S. haemastoma shells, we can infer that there is preference and adaptation of I. sawayai to this shell species.Furthermore, the studies of Hebling and Wernick (1974) and Pinheiro et al. (1993) showed that 67.5 and 80.27% of I. sawayai individuals occupied S. haemastoma shells in Peruíbe and Ubatuba, respectively, and this shell species was also occupied by I. sawayai population from Margarita Island, Venezuela (Galindo et al., 2008), observations that corroborated the preference and adaptation to this shell species.
Stramonita haemastoma was significantly the most occupied shell species by all groups of interest, but the patterns of shell occupation that they have exhibited were different.Ovigerous females inhabited lower shell species diversity than males and non ovigerous females, occupying only five of the 17 species occupied by this population.This lower diversity of shell occupation by ovigerous females was similar to that related for Calcinus tibicen (Herbst, 1791) (Garcia and Mantelatto, 2000) and P. exilis (Terossi et al., 2006).This fact consti-which was similar to that observed for L. loxochelis (Martinelli and Mantelatto, 1998).According to these authors, the occupation of shells covered by bryozoans can be due to the great abundance of these epibionts in the environment, and is related to the burying behavior of some hermit crab species, such as I. sawayai, conferring camouflage on sand.
Regression analysis between all hermit crabs and shell dimensions showed significant and high correlation coefficient values.This fact is an important indication that, although there is a reduced number of resources available in the environment (Meireles, 2006), the hermit crabs were occupying adequate shells.
Therefore, we can infer that I. sawayai shows a high plasticity in the pattern of shell occupation that is related to the resource availability in the environment and to a possible preference for S. haemastoma.Furthermore, the fact of occupying adequate shells may represent that, for this population, the shells may not be considered a limiting resource, but laboratory experiments are needed for a better understanding of the shell preference and adequacy for the I. sawayai population studied.
growth (Abrams, 1988;Mantelatto and Martinelli, 2001;Fransozo et al., 2003).Furthermore, the larger sized males have a greater probability of success in copulating because they can fertilize females of different sizes as well as having the advantage in fighting for acquiring females (Hazlett and Baron, 1989).Differential growth patterns between the sexes may influence shell species occupation (Abrams, 1988) and this may be the most probable cause of the different pattern of shell occupation exhibited by the studied population associated to the possible competitive dominance of males over females in the shell fighting process.
In the present study, the same shell species was the most occupied by all groups of interest, which is an indication that there are no differential preferences among the sexes determining different patterns of occupation.In this way, the most probable reason for the occupation difference was the differential growth among the sexes and the competitive dominance of larger males, factors that could be related to the occupation of different shell species and sizes between sexes.
In relation to the shell occupation by individuals of different size classes it was verified that intermediate sized individuals of this population occupied a greater diversity of shell species, a fact that was also observed in the studies realized with Petrochirus diogenes (Linnaeus, 1758), C. tibicen, Paguristes tortugae Schmitt, 1933, Pagurus brevidactylus (Stimpson, 1859) and Paguristes calliopsis Forest and Saint Laurent (1968) (Bertini and Fransozo, 2000;Mantelatto and Garcia, 2000;Mantelatto and Dominciano, 2002;Mantelatto and Meireles, 2004;Biagi et al., 2006, respectively).This can be related to the reduced intraspecific shell competition capacity against the largest individuals for the most adequate shells (Dowds and Elwood, 1983), or to the presence of a greater number of intermediate sized shell species available in the environment (Mantelatto and Garcia, 2000), since the smaller the hermit crabs is, the greater is the shell diversity it can find (Reese, 1969).Thus, small hermit crabs may not be considered so dependent on a determinate gastropod shell species as the big ones are (Bollay, 1964), and are frequently encountered inhabiting adequate shells when compared to the larger individuals, mainly because of the greater shell availability to the small and intermediate individuals (Vance, 1972a;Bertness, 1980).
According to Conover (1979), the epibionts that inhabit a gastropod shell are influenced by the shell size and by the presence or absence of a hermit crab, and also some symbionts have a greater survival probability when associated to a hermit crab.Little is known about the costs and benefits of the association between hermit crabs and other invertebrates, but their presence can affect shell selection and occupation by hermit crabs (Martinelli and Mantelatto, 1998).More than half (57.37%) of the I. sawayai studied population occupied infested shells.Bryozoans were the epibiont group with greatest occurrence being present in 42.36% of the occupied shells,

Figure 1 .Figure 2 .
Figure 1.Isocheles sawayai.Size frequency distribution for each group of interest of individuals collected in Caraguatatuba region (SP).

Table 2 .
Isocheles sawayai.Regression equations for the relations between hermit crabs and the four most occupied shell species dimensions, in Caraguatatuba region (SP).