SHELL UTILIZATION PATTERNS OF A TROPICAL ROCKY INTERTIDAL HERMIT CRAB ASSEMBLAGE: I. THE CASE OF GRANDE BEACH

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1 JOURNAL OF CRUSTACEAN BIOLOGY, 21(2): , 2001 SHELL UTILIZATION PATTERNS OF A TROPICAL ROCKY INTERTIDAL HERMIT CRAB ASSEMBLAGE: I. THE CASE OF GRANDE BEACH Alexander Turra and Fosca Pedini Pereira Leite (AT, correspondence) Programa de Pós-Graduação em Ecologia, Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, CEP , CxP 6109, Brasil (turra@unicamp.br); (FPPL) Departamento de Zoologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, CEP , CxP 6109, Brasil (fosca@unicamp.br) ABSTRACT Hermit crabs depend on gastropod shells that influence many characteristics of their life histories. The relationship between shell utilization patterns and biological attributes enables comparisons among populations and discussions of the influence of the environment (shell supply) on hermit crab biology. This study was undertaken in a cobble/boulder low slope rocky shore in Grande Beach, São Sebastião, São Paulo State, Brazil. Crabs were randomly sampled, measured (shield length), and their sexes were determined. Shells were identified, sized (height, width, and aperture length), and weighed. Four hermit crab species were registered: Clibanarius antillensis, Paguristes tortugae, Pagurus criniticornis, and Calcinus tibicen. Shell use was influenced by shell availability, despite the selection of certain shell types and sizes by hermit crabs. Shells were not considered a limiting resource to this hermit crab assemblage, and shell availability was dependent on shell type and size as well as on individual size and species composition of the hermit crab assemblage (presence of competing species). Shell partitioning among crab species was recorded and associated with species coexistence in this area. Differential shell use was recorded among size and reproductive classes of C. antillensis. There was a tendency toward high numbers of ovigerous females in relatively lighter (smaller) and small-aperture shells, such as Cerithium atratum and Morula nodulosa, which was associated with growth restriction and low fecundity imposed by shell morphology. Many theories are based upon evaluation of resources and their ecological implications. Food, mates, hosts, and space are examples of resources that modulate biological interactions and population biology. Hermit crabs are highly and directly influenced by such a resource: the gastropod shells. Shells may function as a limiting resource to these crabs when in low abundance or adequacy (Kellogg, 1976). Shells may restrict crab growth (Vance, 1972a; Fotheringham, 1976a; Bertness, 1981a), enhance their predation risk (Vance, 1972b), reduce fecundity (Bertness, 1981a; Elwood et al., 1995), and modulate reproductive activity (Bertness, 1981b) and success (Hazlett, 1989; Hazlett and Baron, 1989). The trade-off imposed by shell use also dictates crab s energetic balance, i.e., larger and heavier shells furnish better protection against predators but increase the shell carrying and foraging costs (Conover, 1978). In addition, shells that prevent growth may lead the crabs to immediate reproductive investments (Bertness, 1981b). Distinct hermit crab populations may be subjected to different shell supplies that influence their biology in particular manners (Bertness, 1980). Thus, the study of gastropod assemblages, shell utilization patterns, and behavioral parameters, and the description of these populations may lead to a better understanding of the relationships between hermit crabs and gastropod shells. Questions like how are gastropod shells related to crab size, growth, or reproductive status? may be addressed. The composition of hermit crab assemblages is also influenced by shell availability (Spight, 1977). Coexisting species compete for the most adequate shells, with the dominant species or individuals within a given species holding the best ones. A vacancy chain process (Chase et al., 1988) is established with the subordinant species occupying proportionally less adequate shells that impose on them hard conditions to live (Bertness, 1981a). In this way, resource (shell) partitioning may influence hermit crab s diver- 393

2 394 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 sity, either enabling the coexistence of species or through the exclusion or reduction in abundance of such subordinant species. The partition of resources is also important in intraspecific interactions, both between sexes and individuals of different sizes. The aim of this study was to characterize the shell utilization pattern of a rocky tropical intertidal assemblage of hermit crabs focusing on the relationships between shells and crabs regarding shell use, availability, and partitioning. The influence of shell use on hermit crab biology was also discussed. MATERIALS AND METHODS This study was conducted at Grande Beach (45 24 W, S), São Sebastião, São Paulo State, Brazil, from September 1993 to June Five sampling surveys were taken during diurnal spring low tides in the intertidal region over this ten-month period. The study area is a low slope and structurally complex rocky shore with boulders and cobbles that form tide pools and moist microhabitats over the whole intertidal area (Leite et al., 1998). The tides are semidiurnal with maximal amplitude of 2 m. Hermit crabs, gastropods, and empty shells were collected in 0.50-m wide randomized transects perpendicular to the water line. The size and number of transects varied at each collection as a function of tidal level and abundance of hermit crabs. The size (shield length) of the hermit crabs was measured under a stereoscopic microscope (0.01 mm). Sexes of the hermit crabs were determined. Only Clibanarius antillensis were grouped in three size classes (S-small: mm, M-medium: mm, L-large: mm). Shells were identified and then weighed (0.001 g) after drying at 100 C for 24 h. Shell height (siphonal canal to shell apex), shell width (to the widest point), and aperture length (including siphonal canal) were measured with a vernier caliper (0.05 mm). The null hypothesis that the three sympatric hermit crab populations with abundance great enough to be analyzed have equal mean sizes was tested with a one-way ANOVA followed by Scheffé s tests for multiple comparisons (Zar, 1984). The log-likelihood G test (Zar, 1984) was used to verify the null hypothesis related to shell availability that the proportion of shells used by the crabs in this intertidal assemblage was the same as that of living gastropods and empty shells. This test was also employed to verify the null hypothesis that males and ovigerous and non-ovigerous females and those crabs of different size classes were occupying similar shell types (or the same shell types in similar proportions). Shell use comparisons were also assessed using the Shannon- Wiener diversity index in decits log 10 (Bach et al., 1976; Krebs, 1989; Asakura, 1995) and Percentage of Similarity (Renkonen s index) as a niche overlap measure (Abrams, 1980; Krebs, 1989). The null hypothesis about the similarity in height of the used and available shells was tested for each shell type with ANOVA and Scheffé s test or with the Student s t test (Zar, 1984). Shell partitioning, i.e., differences in shell use, among the sympatric hermit crab species and males and ovigerous and non-ovigerous females of C. antillensis was addressed with ANOVA and Scheffé s test and with Student s t test (Zar, 1984), respectively, by testing the following null hypotheses. The mean shell weight and shell weight/shield length ratio of all shells used by crabs and the mean values of the same variables of shells of the most-used gastropod shells were the same among them. This analysis was also conducted to test the null hypothesis that all shell types used by C. antillensis showed similar shell weight/shield length ratios. The log-likelihood G test was also conducted to test the null hypothesis that the shells most used by C. antillensis shelter the same frequency of ovigerous females. Linear regression analysis (Zar, 1984) was employed to test the null hypotheses that the relationships between crab shield length and shell weight and between shield length and shell weight/shield length ratio were not significant for each studied population and reproductive classes of C. antillensis. Covariance analysis (ANCOVA, Zar (1984)) was used to test the null hypothesis that these relationships (if significant) had the same slopes and elevations (Y-intercept). The null hypothesis that individuals of different size classes (S, M, and L) used shells with equal mean values for the shell weight/shield length ratio was also tested with ANOVA and Scheffé s test. The null hypothesis that there was a relationship between the sizes of the hermit crabs and the variables of the most-used shells (including shell weight/shield length ratio) in each crab population was tested with linear regression models. The null hypotheses that there were relationships among shell variables and the shell weight/shield length ratio for the shell most used by C. antillensis were tested with Pearson s correlation coefficients (Zar, 1984). Statistical analyses were conducted at the 0.05 significance level. RESULTS Species Composition and Shell Use and Availability Four hermit crab species were collected in the study area, with Clibanarius antillensis Stimpson, 1859, being the most abundant one (303 individuals, 79.19%). This species occurred along the whole intertidal zone over the entire sampling period, even on/under cobbles or in tide pools, where many clusters were registered (Turra and Leite, 2000). Paguristes tortugae Schmitt, 1933, and Pagurus criniticornis (Dana, 1852) were less frequent (42 individuals, 10.42% and 49 individuals, 12.16%, respectively) than C. antillensis, being restricted almost exclusively to tide pools. Only nine individuals (2.23%) of Calcinus tibicen Herbst, 1791, were registered in the samples and were not included in further analysis. Size differences among the three most abundant species were recorded (ANOVA, F = , gl = 2, P < 0.001), with the individuals of P. criniticornis (2.10 ± 0.49 mm) on average being smaller than those of C. an-

3 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 395 Table 1. Shell utilization by the four hermit crab species collected in the intertidal region of Grande Beach. (Sfb, soft bottom; Hdb, hard bottom; Al, algae.) Hermit crab species Gastropod Origin* Clibanarius Calcinus Paguristes Pagurus antillensis tibicen tortugae criniticornis Total Anachis lyrata (Sowerby, 1832) Hdb/Al Cerithium atratum (Born, 1778) Sfb Columbella mercatoria (Linnaeus, 1758) Hdb/Al 1 1 Costoanachis catenata (Sowerby, 1844) Hdb/Al Cymathium partenopeum (von Salis, 1793) Hdb/Sfb 1 1 Hastula cinerea (Born, 1778) Sfb Leucozonia nassa (Gmelin, 1791) Hdb Littoraria flava King and Broderip, 1832 Hdb 2 2 Morula nodulosa (C. B. Adams, 1845) Hdb Pisania auritula (Link, 1807) Hdb Pisania pusio (Linnaeus, 1758) Hdb 1 1 Polinices hepaticus (Roding, 1798) Sfb Stramonita haemastoma (Linnaeus, 1767) Hdb Strombus pugilis Linnaeus, 1758 Sfb 1 1 Tegula viridula (Gmelin, 1791) Hdb Fragmented 1 1 Total * Habitat of gastropods based on Rios (1994). tillensis (3.04 ± 1.04 mm) and P. tortugae (3.79 ± 1.11 mm; Scheffé s test, P < and P < 0.001, respectively). Individuals of C. antillensis were also smaller on average than individuals of P. tortugae (P < 0.001). Hermit crabs of this assemblage occupied 15 types of gastropod shells, with those of Tegula viridula (Gmelin, 1791) being the most used (Table 1). The hermit crabs also frequently occupied shells of Cerithium atratum (Born, 1778), Leucozonia nassa (Gmelin, 1791), Morula nodulosa (C. B. Adams, 1845), and Stramonita (= Thais) haemastoma (Linnaeus, 1767). Despite the high utilization of shells of rocky shore gastropods (Table 1), the crabs also used shells of soft-bottom organisms such as C. atratum and Hastula cinerea (Born, 1778). Shell use was strongly influenced by shell availability. This was evidenced by the fact that shells utilized by hermit crabs presented high similarities with the intertidal gastropod community (Renkonen s index: 75.67%, original data transformed to percentage) and with the pool of empty shells (62.44%). A comparison between the use and availability (empty shells or living gastropods) of different shell types revealed that the crabs did not occupy shells at random (used vs. living gastropods: G = 96.32, d.f. = 5, P < 0.001; used vs. empty: G = 1,249.58, d.f. = 5, P < 0.001) (Fig. 1). In addition, hermit crabs used more shell types and a more diverse shell resource (n = 15, H = 0.732) than would be expected by the species composition of the gastropod assemblage (n = 7, H = 0.472) and the pool of empty shells (n = 12, H = 0.611) on this rocky shore. Shell height showed considerable variation between available and used (by all crab species) shells of M. nodulosa, T. viridula, and S. haemastoma (Table 2). No variation was recorded in shells of L. nassa. In general, available shells (living gastropods and/or empty shells) were on average larger than the shells used by the hermit crabs (Table 2). Paguristes tortugae used shells of T. viridula of the same height as the available ones, while C. antillensis and P. criniticornis occupied smaller shells than would be expected by shell availability (Fig. 2). Shell Partitioning A comparison of the shell utilization pattern among the three most abundant species of hermit crabs revealed that they used this resource similarly. The similarity in shell use (original data transformed to percentage) was high between C. antillensis and P. tortugae (Renkonen s index: 78.13%) and P. criniticornis (75.07%), as well as between the last two species (77.00%). Shell weight and the shell weight/shield length ratio differed among the three hermit

4 396 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 Fig. 1. Comparison of the shell utilization pattern by hermit crabs with shell availability as living gastropods and empty shells. (Hermit crabs, 403 individuals; Gastropods, 554; Empty: 171.) (Tegu, Tegula viridula; Moru, Morula nodulosa; Leuc, Leucozonia nassa; Stra, Stramonita haemastoma; Ceri, Cerithium atratum; Pisa, Pisania auritula; Bull, Bulla striata.) crab species (Table 3), with P. tortugae occupying heavier shells than did C. antillensis and P. criniticornis. The weight of the shells also differed between these two latter species. Shells were proportionally heavier (in relation to crab size) to P. criniticornis than to the two other species. Clibanarius antillensis also used relatively heavier shells when compared to P. tortugae. The parameters of T. viridula were compared among the three species (Table 3). In general, P. tortugae used larger shells than did C. antillensis and larger and heavier shells than did P. criniticornis. Moreover, C. antillensis used larger and heavier shells than did P. criniticornis. Paguristes tortugae and C. antillensis used shells of the same relative weight, but proportionally heavier (higher shell weight/ shield length ratio) than those used by P. criniticornis. Table 2. Comparison of the height (mm) of the shells occupied by hermit crabs and available as gastropods and empty shells. (Superscript figures indicate the results of the Scheffé s test for pairwise comparison at α = 0.05.) Hermit crabs Gastropods Empty shells Shell type n 8 SD n 8 SD n 8 SD Statistic d.f. P L. nassa M. nodulosa T. viridula (1) (2) (3) <0.001 S. haemastoma (1) (1) (2) <0.001 Student s t test. ANOVA.

5 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 397 Fig. 2. Comparison of the height (mm) of shells of T. viridula among hermit crab species, living gastropods, and empty shells. (Labels indicate significant differences calculated by the Scheffé s test for multiple pairwise comparisons; Bars indicate +1 Standard error.) Linear models were fitted between crab size and shell weight (Fig. 3) for the three studied crab species and all used shells. Larger individuals used heavier shells than did the smaller ones (C. antillensis: n = 284, r 2 = 0.823, P < 0.001; P. criniticornis: n = 48, r 2 = 0.288, P < 0.001; P. tortugae: n = 32, r 2 = 0.738, P < 0.001). Paguristes tortugae presented similar relationships between these variables with both C. antillensis and P. criniticornis (Covariance analysis: slope, P = ns, elevation, P = ns ; slope, P = ns, elevation, P = ns, respectively). However, C. antillensis showed a higher increase in shell weight in relation to its size in comparison with P. criniticornis (Covariance analysis: slope, P = 0.009, elevation, P = ns ). The shield length of these three Table 3. Comparison (ANOVA) of the weight and shell weight/shield length ratio of all shells and the parameters [Shell height (mm), Width (mm), Aperture length (mm), weight (g) and shell weight/shield length ratio (g mm 1 )] of shells of T. viridula between hermit crab species. (8 = Mean; SD = Standard deviation.) (Superscript figures indicate the results of the Scheffé s test for pairwise comparison at α = 0.05.) C. antillensis P. criniticornis P. tortugae Shell Parameter 8 SD 8 SD 8 SD F d.f. P All shells n = 284 n = 48 n = 42 Weight* 1.48 (1) (2) (3) <0.001 length ratio* (1) (2) (3) <0.001 T. viridula n = 141 n = 26 n = 23 Shell height (1) (2) (3) <0.001 Width (1) (2) (3) <0.001 Aperture length 9.67 (1) (2) (1) <0.001 Weight 1.76 (1) (2) (1) <0.001 length ratio (1) (2) (1) <0.001 * Ln transformation.

6 398 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 Fig. 3. Regression analysis between ln shield length (mm) of C. antillensis (solid line, Y = X, n = 284, r 2 = 0.823, P < 0.001), P. tortugae (dotted line, Y = X, n = 32, r 2 = 0.738, P < 0.001), and P. criniticornis (dashed line, Y = X, n = 48, r 2 = 0.288, P < 0.001) and the ln shell weight (g) of all shells used by these crabs. hermit crab species was also contrasted to shell weight/shield length ratio (Fig. 4). Significant but not similar regression lines were registered for C. antillensis and P. tortugae (n = 284, r 2 = 0.679, P < and n = 32, r 2 = 0.417, P < 0.001, respectively; Covariance analysis: slope, F = , d.f. = 1, P < 0.001, Y-intercept, F = 0.096, d.f. = 1, P = 0.757), indicating that larger individuals used relatively heavier shells than smaller ones and that this increase was pronounced for C. antillensis. The regression line fitted for P. criniticornis was not significant (n = 48, r 2 = 0.073, P = 0.062) and revealed that crabs of different sizes used shells of the same weight in relation to their size. Males and females of C. antillensis differed in shell use (G = 34.22, d.f. = 8, P < 0.001), while ovigerous females occupied the same shell types in similar proportions as did nonovigerous females (G = 7.50, d.f. = 4, ns) (Fig. 5). Males were found more frequently in shells of T. viridula and S. haemastoma, whereas females were more frequently in L. nassa, C. atratum, and M. nodulosa. The five shells most used by C. antillensis sheltered a great number of ovigerous females (over 50%) (Fig. 6). However, differences in the proportion of ovigerous females were verified only between C. atratum and L. nassa. The ratio between shell weight and shield length of C. antillensis differed among the shells most used by this species (ANOVA, F = , d.f. = 4, P < 0.001). Shells of S. haemastoma and T. viridula were proportionally heavier in relation to the other shell types (Fig. 7). Shell weight also differed between sexes of C. antillensis (Table 4), with males occupying heavier shells than females. Non-ovigerous females also used heavier shells than ovigerous females. Comparisons of the shell weight/shield length ratio between sexes showed that females occupied proportionally lighter shells than males. Ovigerous females also used proportionally lighter shells than

7 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 399 Fig. 4. Regression analysis between ln shield length (mm) of C. antillensis (solid line, Y = X, n = 284, r 2 = 0.679, P < 0.001), P. tortugae (dotted line, Y = X, n = 32, r 2 = 0.417, P < 0.001), and P. criniticornis (dashed line, Y = X, n = 48, r 2 = 0.073, P = 0.062) and the ln shell weight/shield length ratio (g mm 1 ) of all shells used by these crabs. Fig. 5. Frequency of gastropod shells utilized by non-ovigerous females (F, n = 56), ovigerous females (FOV, n = 121), and males (M, n = 126) of Clibanarius antillensis collected at the intertidal region of Grande Beach, São Sebastião, São Paulo, Brazil.

8 400 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 Fig. 6. Comparison (log-likelihood G test) of the frequency of ovigerous females of Clibanarius antillensis in the most-used shell types collected at the intertidal region of Grande Beach, São Sebastião, São Paulo, Brazil. non-ovigerous females. The parameters of T. viridula shells were also compared between the sexes of C. antillensis (Table 4). Males occupied larger and heavier shells than females, whereas non-ovigerous females used larger, wider, and proportionally lighter shells than ovigerous females. Aperture length and shell weight did not vary between ovigerous and non-ovigerous females. The size of males and females of C. antil- Fig. 7. Comparison of the mean shell weight/shield length ratio (g mm 1 ) of C. antillensis among the most used shells at the intertidal region of Grande Beach, São Sebastião, São Paulo, Brazil. (Labels indicate significant differences calculated by the Scheffé s test for multiple pairwise comparisons; Bars indicate +1 Standard error.)

9 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 401 Table 4. Comparison (Student s t test) of the weight and shell weight/shield length ratio of all shells and the parameters [Shell height (mm), Width (mm), Aperture length (mm), shell weight (g) and shell weight/shield length ratio (g mm 1 )] of T. viridula between males and all females and between ovigerous and non-ovigerous females of Clibanarius antillensis. (8 = Mean; SD = Standard deviation.) Males Females Ovigerous females Non-ovigerous females Shell parameter 8 SD 8 SD t d.f. P 8 SD 8 SD t d.f. P All shells n = 119 n = 164 n = 111 n = 53 Weight < length ratio < <0.001 T. viridula n = 79 n = 62 n = 21 n = 41 Shell height Width Aperture length Weight length ratio lensis increased with the weight of the occupied shells in the same way (Ln transformation, n = 119, r 2 = 0.856, P < and n = 165, r 2 = 0.752, P < 0.001, respectively; Covariance analysis: slope, P = ns ; elevation, P = ns ), as well as for ovigerous and non-ovigerous females (Ln transformation, n = 113, r 2 = 0.732, P < and n = 52, r 2 = 0.813, P < 0.001, respectively; Covariance analysis: slope, P = ns ; elevation, P = ns ). Individuals of different sizes (S, M and L) of C. antillensis used different shell resources (G = , d.f. = 8, P < 0.001) (Fig. 8). Smaller individuals used more types of shells and shells of C. atratum and M. nodulosa more frequently than did medium- and largesized individuals. Shells of T. viridula were the main resource occupied by the M and L individuals while the utilization of shells of S. haemastoma increased with increasing hermit crab size. There was little overlap in shell utilization between S and M (G = , d.f. = 4, P < 0.001), S and L (G = , d.f. = 4, P < 0.001), and M and L individuals (G = , d.f. = 3, P = 0.001). These size groups also occupied shells of different weights in relation to their shield length (shell weight/ shield length ratio) (ANOVA: F = , d.f. = 2, P < 0.001). The smallest individuals utilized relatively lighter (0.255 ± g mm 1 ) shells than did the medium (0.446 ± g mm 1 ; Scheffé s test, P < 0.001) and the largest ones (0.768 ± g mm 1 ; P < 0.001). The shells occupied by the mediumsized individuals were also relatively lighter than those used by the largest ones (P < 0.001). In general, shield length of the three species of hermit crabs showed a positive and significant correlation with the parameters of the most-used shells in the field (Table 5). However, individuals of C. antillensis in shells of C. atratum and M. nodulosa presented low determination coefficients (r 2 ), especially regarding to shell aperture and shell weight/shield length ratio. Individuals of P. criniticornis and P. tortugae in shells of T. viridula also presented lower coefficients than C. antillensis in this shell. DISCUSSION Shell Use and Availability Shell use by hermit crabs was influenced in this study by shell availability, as was also

10 402 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 Fig. 8. Frequency of gastropod shells utilized by individuals of different size classes of Clibanarius antillensis (S; small, n = 52, mm; medium, n = 99, mm; large, n = 153, mm) collected at the intertidal region of Grande Beach, São Sebastião, São Paulo, Brazil. suggested by Bertness (1982), Wilber and Herrnkind (1982), and Leite et al. (1998). This was evident in the studied area due to the high similarity between shell use and availability given the fact that the most-used shell at Grande Beach corresponded to the most abundant gastropod and empty shell, Tegula viridula. However, shell use was not at random as also recorded by Leite et al. (1998) for some hermit crab populations in São Sebastião Channel. Hermit crabs showed shell preferences due to the fact that some gastropod shells, mainly those of soft bottom such as Cerithium atratum and Hastula cinerea, were used more frequently than would be expected by their availability. In addition, shells of Bulla striata Bruguière, 1792, were never utilized despite their high availability in this area (Fig. 1). This occurred probably because the shell architecture of B. striata is not adequate for crab attachment and protection. This opistobranch gastropod lacks columella, making crab attachment to the shells difficult, and presents very thin walls, which increases predation risks and damages due to wave action. Emmerson and Alexander (1986) also reported the low utilization of thin-walled shells by hermit crabs. Additional evidence that hermit crabs are selecting shell types in this area, i.e., using shells in a different proportion than that found in nature, arises from the comparison between the number (or diversity) of shells used by the crabs and that of living gastropods and empty shells. Hermit crabs utilized 15 shell types, while 12 types were found empty and only seven as living gastropods. These data revealed that many types of shells used by hermit crabs in this rocky shore are imported from adjacent areas, as also recorded by Leite et al. (1998) and Walters and Griffiths (1987). In this latter work the authors found that only 5 of 20 shell types used by the crabs were present as living gastropods in the studied area. Such imported shells are probably obtained by crab migrations to other areas or are brought by currents and waves. Hermit crabs (except P. tortugae) also selected shells on the basis of shell size. Clibanarius antillensis and P. criniticornis used smaller shells of T. viridula than would be expected by shell availability in the study area. Some studies revealed that the amount of empty shells is generally low (Vance, 1972a; Bach et al., 1976) and, when shells are scarce, hermit crabs are forced to use small and inadequate ones (Conover, 1978). According to Spight (1985), the rate with which shells become available is very slow and directly dependent on death rates of snails. In addition, he emphasized that such shells stay available for short periods before they are

11 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 403 Table 5. Determination coefficients (r 2 ) of the linear regressions between shield lengths of C. antillensis, P. criniticornis, and P. tortugae and the parameters of the most-used shells in the field. Shell height (mm) Width (mm) Aperture length (mm) Weight (g) length ratio (g mm 1 ) Hermit crab Shell type n r 2 P n r 2 P n r 2 P n r 2 P n r 2 P C. antillensis C. atratum < ns M. nodulosa < ns ns T. viridula < < < < <0.001 L. nassa < < < < <0.001 S. haemastoma < < < < <0.001 P. criniticornis T. viridula < P. tortugae T. viridula < < ns buried, eroded, or broken. However, a high availability of gastropod shells (171 empty shells and 466 gastropods compared to 403 hermit crabs) was registered in the studied area, as was also seen in other studies (Markham, 1968; Kellogg, 1976; Conover, 1978). This high availability of shells can be inferred from the data on shell adequacy to the crabs, based on Scully (1979). He suggested that high availability of shells may be correlated with the frequent occupancy of adequate shells and shells in good physical condition. According to Scully (1983), a good shell adequacy to the crabs can be associated with the strong and significant relationships (regression analysis) between shell parameters and crab size. This was the case of C. antillensis and P. tortugae, at least, in the studied area. In addition, available shells were generally larger than those used by the crabs, suggesting that this hermit crab assemblage is not limited by shell supply. Availability also depended on hermit crab species and on the size of living gastropod and empty shells, as also pointed out by Bertness (1980) and Leite et al. (1998). Hermit crab populations with different-sized individuals also need shells of different sizes. Available shells of T. viridula were of the same size of the individuals of P. tortugae and larger than those of C. antillensis and P. criniticornis. This indicates that shell limitation, if it exists, would be stronger in these last two species. Coexistence of hermit crab species may also influence shell availability so that it may not directly correspond to the availability of new shells to all crabs of all populations coexisting at a given site. Crabs that are better competitors may use this new resource to the exclusion of less competitive crabs, leaving only worse shells for other species or individuals (Bach et al., 1976; Bertness, 1980; Asakura, 1995). Therefore, it is possible to find crabs in inadequate shells at sites with high shell availability. The crabs of this assemblage had different mean sizes but showed an overlap in size distributions. Thus, competition for shells among the crabs in the overlapping size classes would be expected. However, high shell availability and shell partitioning among crab species and among size and reproductive classes may act together in reducing intra- and interspecific competitive interactions in this assemblage.

12 404 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 2, 2001 Table 6. species. Pearson s correlation coefficients (r) and associated probabilities of shell parameters for each gastropod Shell height (mm) Width (mm) Aperture length (mm) Weight (g) Shell type/parameters r P r P r P r P C. atratum (n = 27) Width <0.001 Aperture length Weight < < length ratio < <0.001 M. nodulosa (n = 40) Width Aperture length < Weight < < length ratio < < <0.001 L. nassa (n = 39) Width <0.001 Aperture length < <0.001 Weight < < <0.001 length ratio < < < <0.001 T. viridula (n = 133) Width <0.001 Aperture length < <0.001 Weight < < <0.001 length ratio < < < <0.001 S. haemastoma (n = 27) Width <0.001 Aperture length < <0.001 Weight < < <0.001 length ratio < < < <0.001 Shell Partitioning Shell partitioning among these three hermit crab populations was more evident in relation to shell dimensions than to shell types. Pagurus criniticornis utilized relatively lighter (Table 3) and, consequently, smaller (Table 6) shells than the two other species. The use of relatively lighter shells by the smallest individuals of this assemblage was directly associated to the allometric relationships between crab sizes and shell weights (slope > 1) (Fig. 4). Clibanarius antillensis and P. tortugae showed a better fit with shell weight than P. criniticornis. When considering crabs in shells of T. viridula, both P. tortugae and P. criniticornis had lower values of r 2 between their sizes and the weight of the shells in relation to C. antillensis. Shell fit appeared to depend on crab species and indicated that C. antillensis used better shells than P. tortugae that, in turn, used better shells than P. criniticornis. Bach et al. (1976) studied hermit crab assemblages in different areas in Florida and showed that shell fit was also dependent on the presence and competitive abilities of coexisting species. This work also showed that C. antillensis was dominated by Clibanarius tricolor, which was dominated by Calcinus tibicen, and that hierarchy was directly related to data on shell fit. In this way, a hierarchical order may be proposed for the assemblage at Grande Beach based on the shell fit to the coexisting species. Clibanarius antillensis dominates P. tortugae, which dominates P. criniticornis. Clibanarius antillensis was the subordinant species in one assemblage (Bach et al., 1976) but is supposed to be the dominant one at our study site. This reaffirms that shell fit (Bach et al., 1976), as well as crab hierarchy, to hermit crabs is dependent on the composition of the hermit assemblages, and that shell partitioning may enable species coexistence (Gherardi and Nardone, 1997). Males and females of the C. antillensis population had different sizes (Turra and Leite, 1999) and used different shell types,

13 TURRA AND LEITE: SHELL UTILIZATION BY ROCKY INTERTIDAL HERMIT CRABS 405 while ovigerous and non-ovigerous females strongly overlapped in their size and in shell use. However, females used relatively lighter (smaller) shells than males as well as did ovigerous females in relation to non-ovigerous females. Shell partitioning was also verified among individuals of C. antillensis of different size classes with the largest individuals occupying different types and relatively heavier shells than medium- and smallsized ones. The allometric relationships between shield length and shell weight (slope > 1) also caused the use of relatively lighter shells by females of C. antillensis in relation to males given their size differences (females smaller than males). This was also applicable to individuals in the smallest size class (S) in relation to medium- and large-sized crabs (M and L). Shell partitioning among sexes of C. antillensis revealed that shells of C. atratum, M. nodulosa, and L. nassa sheltered a greater number of females in relation to males. These three shell types were relatively lighter (smaller) in relation to crab size and also sheltered mainly individuals classified as smalland medium-sized, i.e., mainly females. However, shells of C. atratum and M. nodulosa showed a tendency to be occupied by ovigerous females in higher frequency than others as also registered by Bach et al. (1976) for other high spired gastropods. Shell Use and Hermit Crab Biology Shells of C. atratum and M. nodulosa were considered inadequate to C. antillensis given the low values of the determination coefficient (as suggested by Scully, 1983) between shell aperture and shield length. Turra and Leite (1999) showed those females of this C. antillensis population occupying shells of C. atratum and M. nodulosa produced smaller clutches than females in T. viridula. The use of inadequate shells prevents growth (Fotheringham, 1976a; Bertness, 1981b) and leads such females to produce smaller broods than would be produced if they were able to grow and reproduce as a large-size female. It is particularly true given fecundity of this population of C. antillensis is directly related to the size of their individuals (Turra and Leite, 1999). Ovigerous females were collected in relatively lighter shells than were non-ovigerous females despite their similar sizes. These relatively lighter shells were also smaller due to the high correlation coefficients between all shell parameters (Table 6). In fact, regression analysis between shield length of C. antillensis and shell weight (using all shells) revealed slightly better fits for males and nonovigerous females than for ovigerous females (see Results). This smaller shell fit (inadequacy) suggests that ovigerous females are occupying poorer shells than the other crabs, which may also be leading them to undergo immediate reproduction instead of growing (Bertness, 1981b; Turra and Leite, 1999). The use of shells of C. atratum, a highspire gastropod, enables the crabs to optimize retraction and protection, as suggested by the mathematical model elaborated by Lively (1988). However, high-spired shells also expose the crabs to wave action (Vermeij, 1978). Moreover, shells of C. atratum (as well as M. nodulosa and L. nassa) were proportionally lighter in relation to crab size of C. antillensis than were other shell types. This fact, according to Hahn (1998), suggests that crabs in such shells are more susceptible to displacement by water movements. Shells of low-spired gastropods such as T. viridula may expose the crabs to a high desiccation risk (Lively, 1988), but may also enable crab growth due to their relatively higher internal volume in relation to shell weight (Osorno et al., 1998). In addition, intertidal hermit crabs subjected to strong water currents select relatively heavier shells than crabs in still water (Hahn, 1998). Shells of T. viridula and S. haemastoma where relatively heavier than the other shells used by C. antillensis. Thus, the high use of shells of T. viridula (low spire) by this species and by this hermit crab assemblage may be influenced by shell availability in this area but also by the moderate hydrodynamism of this rocky shore (Leite et al., 1998). Vermeij (1978) and Bertness (1980) suggested that hermit crab preferences for narrow-aperture shells is an adaptation against predation by shell-crushing crabs. In addition, Fotheringham (1976b) suggested that such kind of shell might reduce the access of egg predators or parasites. As a consequence of the fact that the shells of C. atratum and M. nodulosa had small apertures in relation to their heights, their apertures also had low linear relationships with crab sizes (Table 5). In this way, these shells may be advantageous to the ovigerous females of C. antillensis despite the growth restriction imposed to them.

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