THE ECOLOGICAL SIGNIFICANCE OF GROWTH RATE, SEXUAL DIMORPHISM AND SIZE AT MATURITY OF LITTORARIA ZEBRA AND L. VARIEGATA (GASTROPODA: LITTORINIDAE) JOSE M. RIASCOS 1,2 AND PABLO A. GUZMAN 3 1 Facultad de Recursos del Mar, Instituto de Investigaciones Oceanolo´gicas, Universidad de Antofagasta, Avenida Angamos 601, Antofagasta, Chile; 2 Museo de Ciencias Naturales-INCIVA, Avenida Roosevelt 24-80, Cali, Colombia; and 3 Escuela de Estadı´stica, Facultad de Ciencias, Universidad Nacional de Colombia, Calle 65 Carrera 64 Autopista Norte, Medellı´n, Colombia Correspondence: J.M. Riascos; e-mail: jriascos@uantof.cl (Received 12 October 2009; accepted 2 March 2010) Growth rates, maturation sizes and sexual dimorphism in shell morphology (size, globosity and thickness) of Littoraria zebra and L. variegata in a mangrove forest at Malaga Bay (Pacific Coast of Colombia) were studied. The sexes of L. zebra did not show differences in growth rate or maximum size. Minimum sizes at maturity were similar; however, the mean size of mature males was smaller than that of females. Littoraria zebra did not show sexual dimorphism in shell morphology. Females of L. variegata grew almost twice as fast as males, reached larger maximum size and attained sexual maturity at a larger size than males. Females had thinner and more globose shells than males. Littoraria zebra and L. variegata reach sexual maturity at a relatively later stage than other Littorininae species, but they continue growing after maturity. The intersexual pattern of growth, in which males are smaller than females and grow more slowly, is common in Littorininae; however, L. zebra does not seem to follow this pattern. Sexual dimorphism of L. variegata can be explained by the hypothesis of fecundity selection and results from the difference in growth rates. The differences between the two species regarding shell thickness and growth rates are discussed in terms of vertical zonation and predation in the mangrove environment. INTRODUCTION Species of the genus Littoraria (Littorinidae) inhabit rocks, driftwood, saltmarsh plants and mangrove trees in the intertidal zone throughout tropical and subtropical regions (Reid, 1986, 2001). Littoraria (Littoraria) zebra (Donovan, 1825) and L. (L.) variegata (Souleyet, in Eydoux & Souleyet, 1852) are dominant species in the tropical eastern Pacific province (Reid, 1999a). They reach similar sizes and occur together at around high tide level on mangrove trees. The range of their vertical distribution is similar (Blanco and Cantera, 1999), although L. variegata tends to be located at higher levels (Reid, 1999a). Recent studies have shown a close phylogenetic relationship between the two species (Reid, 1999b; Reid, Dyal & Williams, 2010). As growth patterns and variations in shell morphology are important components of adaptation to the environment and may reveal evolutionary pathways (e.g. Vermeij, 1972, 1980; Tissot 1988; Hollander, Adams & Johannesson, 2006; Tanaka & Maia, 2006), we would expect interspecific differences in these closely related species. In turn, those differences may reveal individual strategies of resource partitioning and of the interaction of these species with their environment. On the other hand, growth patterns, shell morphology and size at maturity can also be different between the sexes, especially in animals that mature at a small size and then approach a larger asymptotic size (Stamps, 1993). These differences can be explained by a combination of ecological factors favouring the evolution of particular strategies (Hart & Begon, 1982; Stamps, 1993; Stamps, Mangel & Phillips, 1998). In littorinid snails, continuous growth has been observed after maturity (Borkowski, 1974), and females usually grow faster than males (Borkowski, 1974; Underwood & McFadyen, 1983; Maruthamuthu & Kasinathan, 1985; Reid, 1986; Chow, 1987; Johannesson, Rolán-Alvarez & Erlandsson, 1997). Females also reach a larger average size than males (Borkowski, 1974; Hamilton, 1978; Reid, 1986; Chow, 1987; Sacchi, 1994). Body and shell growth rates are the result of several physiological constraints and ecological factors (Stearns, 1976; Hart & Begon 1982; Chow, 1987; Jensen, Christensen & Macintosh, 1999). Growth rate variability in littorinids has been associated with differences in form and thickness (or weight) of the shell (Kemp & Bertness, 1984; Reid, 1986; Johnson & Black, 1998). Therefore, shell features are considered to be of adaptive value (e.g. Reid, 1992, 2001). Differences in form and thickness of the shells associated with variability in growth rate can be expected when comparing males and females of the same species, as well as different species. Protection against predation is one of the most important functions of the shell (Vermeij, 1978). Shell thickness in Littoraria commonly diminishes in species distributed in higher levels of mangrove trees, reflecting the adaptation to the severity of the predation in lower levels (Cook, Currey & Sarsam, 1985; Reid, 1986, 1992; Borjesson & Szelistowski, 1989; Duncan & Szelistowski, 1998). Shells of L. zebra have been reported to be thicker than those of L. variegata (Reid, 1999a). As the deposition of calcium carbonate is energetically costly (Palmer, 1981), species with more fragile shells may be able to invest relatively more energy in tissue growth and reproduction (Cook et al., 1985). In this context, the objectives of this study were (1) to determine maximum and minimum size at maturity in both species; (2) to compare patterns of growth and maturation between the Journal of Molluscan Studies (2010) 76: 289–295. Advance Access Publication: 29 April 2010 # The Author 2010. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. doi:10.1093/mollus/eyq011 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 ABSTRACT J. M. RIASCOS AND P. A. GUZMAN sexes for both species; (3) to test for sexual dimorphism in size, thickness and shape of the shell in each species; and (4) to compare patterns of growth between these species. MATERIAL AND METHODS Study area The study was conducted at Palito de Brea, a fringing-type mangrove forest (Von Prahl, Cantera & Contreras, 1990). This small mangrove forest (≏44,000 m2) is surrounded by cliffs supporting a tropical forest. The mangrove forest is flushed by daily tides and grows on fine mud. The dominant mangrove species are Rhizophora species, followed by Pelliciera rizhophorae, while Avicennia germinans and Laguncularia racemosa are less frequent. Littoraria zebra and L. variegata are both abundant, the former being more frequent. Palito de Brea is located in Málaga Bay (38570 N, 778190 W), Pacific coast of Colombia (Fig. 1), one of the coastal areas with the highest precipitation in the western hemisphere: the annual rainfall varies from 7,000 to 11,000 mm (Kjerfve, Seelinger & Drude De Lacerda, 2001). A full description of the geomorphology, oceanography and biotic communities of this bay was given by Von Prahl & Cantera (1986), Prahl et al. (1990) and Cantera, Thomassin & Arnaud (1999). Sexual dimorphism One hundred snails of each sex and each species covering the available size range were selected in order to evaluate the sexual dimorphism (i.e. the systematic difference in shape or size between individuals of different sex in the same species). The following individual shell traits were measured to the nearest 0.05 mm using callipers: shell thickness (T, at the middle of the outer lip of the aperture), total shell breadth (B, maximum length between external border of the aperture and the most distant point of the last whorl) and H. The linear relationship between T and H was compared between males and females using t-tests. Shell globosity (F ¼ B/H) was determined, to describe shell shape and its relationship with H was examined. The regression coefficients of the relationship were compared between males and females using t-tests. F values were arcsine-transformed (F0 ¼ arcsine F 1/2) to meet the test assumptions (Zar, 1984; Son & Hughes, 2000). Growth rate and maximum size We performed mark– recapture experiments between March 2002 and February 2003 to estimate growth rate. All the snails found on three to five randomly selected mangrove trees within the study were collected. All the snails with a shell height (maximum distance between apex and anterior lip, hereafter H; Fig. 2) larger than 8 mm were marked each month by writing a code on the shell surface (for details see Riascos, 2006). Smaller individuals could not be reliably marked and were excluded from the experiments. The shell height and sex (determined by presence/absence of penis) were individually recorded and the snails released thereafter. At monthly intervals, the recaptured snails were measured and the sex and code noted. Vernier callipers were used for length measurements. Size at sexual maturity To determine the size at sexual maturity, 25 snails (H ¼ 8 – 32 mm) of each sex and species were sampled monthly between March and November 2002. Individuals were classified as mature or immature, based on standard histological Figure 1. Location of the study area (Palito de Brea). A. Central area of the Pacific Coast of Colombia. B. Malaga Bay. 290 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 The growth rate (GR) was calculated as the ratio between height increment and the time elapsed between mark and recapture (GR ¼ H2 2 H1/t2 2 t1). The linear relationship between GR and H (Kaufman, 1981) was used for between-sex and between-species comparisons. As the assumptions of linear regression analysis were not meet, we used nonparametric methods of regression and correlation. The method described by Dietz (1989) was applied to each data set. To compare regressions we used the test of Tsutakawa & Hewett (1977), in which a common regression line is considered for both groups and they are compared by the number of points below and above the curve using a x2 test. In addition, we estimated the maximum size (Hmax) as the average of the 10 largest snails from about 700 individuals of each sex in each species (Sparre & Venema, 1995). Hmax was compared between sexes using a Student’s t-test (Zar, 1984). GROWTH AND SEXUAL DIMORPHISM OF LITTORARIA significant differences were found in Hmax between males and females of this species (Table 2). Therefore, data for both sexes was pooled and Hmax was 29.69 mm. Females of L. variegata grew significantly faster than males, and faster than both males and females of L. zebra (Fig. 3B, Table 1). Hmax of females (31.30 mm) was significantly greater than that of males (27.83 mm) (Table 2). No significant differences in GR were found between male L. variegata and males or females of L. zebra. Figure 2. Shell measurements: H, height; B, breadth; T, thickness. H and B according to Reid (1986). Left shell is Littoraria variegata, right L. zebra. Sexual dimorphism PX ¼ 1 1 þ eðb0 þb1 Sexþb2 XÞ where PX is proportion of mature individuals in each size-class, X is the mean H of each size-class, Sex is a dummy variable (female ¼ 1; male ¼ 0) and b0, b1 and b2 are parameters. For ðMÞ males, X50% was estimated as X50% ¼ b0 =b2 and for females ðFÞ as X50% ¼ ðb0 þ b1 Þ=b2 . The difference in size between sexes ðFÞ ðMÞ was estimated by DX50% ¼ X50%  X50% ¼ b1 =b2 . The logistic model was fitted under the assumptions of the generalized linear model (McCullagh & Nelder, 1989), using maximumlikelihood estimation, the logit as link function and the binomial family for error distribution. The deviance (difference of log likelihood of postulated model and full model) of the fitted model was used to test for goodness of fit, with a smaller deviance value indicating a better fit (McCullagh & Nelder, 1989). Size at sexual maturity and growth after maturity The smallest size (H) of a mature individual (Xmin) for L. zebra was 15.2 mm (males) and 16.9 mm (females), while for L. variegata the values were 15.0 mm (males) and 21.0 mm (females). The proportion of mature snails increased with size, and thus the maturity–size relationship for both species conformed to the logistic model (Fig. 6, Table 3). The estimated X50% of L. zebra differed significantly (Wald’s test ¼ 4.912, P , 0.001; Fig. 6A) between males (17.4 mm) and females (19.6 mm). Likewise, for L. variegata (Fig. 6B) the X50% differed (Wald’s test ¼ 12.451, P , 0.001) between males (17.0 mm) and females (22.0 mm). Figure 7 shows the correlation between Hmax/Xmin or ‘maturity relationship’ (Borkowski, 1974) and Hmax, which compares growth after maturity. To this figure have been added data for other species of Littorinidae. The maximum RESULTS Growth rates and maximum size In the mark –recapture experiment, 137 Littoraria zebra and 135 L. variegata were marked, of which 52.6% (72 individuals) and 48.9% (66 individuals) were recaptured, respectively. The relationship between GR and H did not differ significantly between males and females of L. zebra (Fig. 3A, Table 1). No Figure 3. Relationship between growth rate and shell height. A. Males and females of Littoraria zebra. B. Males and females of L. variegata. The Spearman correlation coefficient were: L. zebra, males: rs ¼ 20.728, P , 0.0001; L. zebra, females rs ¼ 20.735, P , 0.0001; L. variegata, males: rs ¼ 20.621, P , 0.0001; L. variegata, females: rs ¼ 20.776, P , 0.0001. 291 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 The relationship between T and H was fitted (r 2 ¼ 0.77) to a semi-logarithmic model for L. zebra (Fig. 4), and there was no significant difference between the regression coefficients for males and females (t196 ¼ 0.781, P ¼ 0.436). In contrast, the relationship between T and H for L. variegata was fitted (r 2 ¼ 0.67) to a logarithmic (i.e. allometric) model (Fig. 4) and the regression coefficients were significantly different between males and females (t196 ¼ 2.032, P ¼ 0.043). The shell thickness of L. zebra was greater than that of L. variegata (Fig. 4). No significant relationship was found between F and H for L. zebra (Fig. 5A), thus precluding comparison between the sexes. Conversely, a significant inverse relationship was found for L. variegata (Fig. 5B). The absolute value of the slope for males (20.47) was significantly higher (t196 ¼ 22.643, P ¼ 0.009) than that for females (20.33). This implies that male shells become less globose (i.e. more narrow) than female shells throughout life. gonad examinations (for details see Guzmán, 2003). The minimum size (Xmin, the smallest mature individual) and the average size at maturity (X50%, the size at which 50% of the individuals were mature; Roa, Ernst & Tapia, 1999) were estimated. To estimate X50% the proportion of mature males and females in different size-classes were fitted to a logistic model: J. M. RIASCOS AND P. A. GUZMAN reproduction before females, which results in slower growth from earlier sizes. In contrast, females grow fast until they reach belated sexual maturity. Littoraria zebra showed a different pattern; although it exhibited sexual dimorphism in size at Table 1. Comparison of growth rates of males and females of both Littoraria zebra and L. variegata [ x2 values of nonparametric test of Tsutakawa & Hewett (1977) used to compare the lines of regression in Fig. 3]. L. zebra male L. zebra female L. variegata male L. zebra male – L. zebra 2.57 (P ¼ 0.109) – 0.01 (P ¼ 0.938) 0.22 (P ¼ 0.641) 20.12 (P , 0.001) 20.11 (P , 0.001) female L. variegata – male L. variegata 46.54 (P , 0.001) female Degrees of freedom ¼ 1. Figure 4. Relationship between the thickness of shell and shell height for each sex of both species. The coefficients of determination (r 2) are: Littoraria zebra males: r 2 ¼ 0.773; L. zebra females: r 2 ¼ 0.789; L. variegata males: r 2 ¼ 0.721; L. variegata females: r 2 ¼ 0.673. All the regressions were significant (P , 0.001). DISCUSSION Stamps (1993) observed that when sexual dimorphism exists in size, the larger sex grows more slowly. The opposite is common in littorinids, in which males are usually smaller and grow more slowly than females (Borkowski, 1974; Underwood & McFadyen, 1983; Maruthamuthu & Kasinathan, 1985; Chow, 1987; Johannesson et al., 1997). Reid (1986) found that in 14 out of 19 species of Littoraria in the Indo-Pacific region, females were on average larger than males. According to our results, this intersexual pattern in growth also applies for L. variegata in Málaga Bay. Females of this species grew almost twice as fast as males and reached a maximum size 11.2% larger than males. However, L. zebra did not show this pattern of sexual dimorphism; males and females showed similar growth rates. Sexual maturity is the point at which an organism begins to spend some energy on reproduction that was previously directed towards growth (Day & Taylor, 1997; Stamps et al., 1998). In organisms with indeterminate growth, like molluscs (Sebens, 1987; Johannesson et al., 1997), there is a gradual decline in the energy reserved for growth and a corresponding increase in energy devoted to reproduction (Day & Taylor, 1997). The larger sex usually matures at a larger size than the smaller one (Stamps et al., 1998). The minimum and average sizes of maturity in L. variegata conform to this pattern; females grew faster than males and matured at a significantly larger size. The underlying explanation for this pattern seems to be that males and females spend similar amounts of energy on growth and reproduction as they approach maturity (Stamps, 1993). Males that mature at smaller size expend energy on Figure 5. Relationship between shell globosity (B/H, arcsine transformation) and shell height (H). A. Males and females of Littoraria zebra. B. Males and females of L. variegata. Table 2. Estimation of the maximum size (Hmax, mm) from the 10 largest snails in samples of each sex of the populations of Littoraria zebra and L. variegata. L. zebra Males L. variegata Females Both sexes Males Females Hmax + SD 29.20 + 0.261 29.07 + 1.087 29.69 + 0.609 27.83 + 0.962 31.30 + 0.968 Range 28.8 – 29.55 27.80 – 31.20 29.15 – 31.20 26.60 –29.00 30.20 –32.70 t-test t ¼ 0.410, df ¼ 10, P ¼ 0.690 (different variances) t ¼ 28.041, df ¼ 18, P , 0.001 (same variances) Abbreviations: SD, standard deviation; df, degrees of freedom. 292 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 growth after maturity for the species studied here was that of males of L. zebra, which grew twice their Xmin, while the minimum growth was for females of L. variegata, which grew 1.5 times their Xmin. Even though L. zebra and L. variegata reach larger sizes than other Littorinidae, they exhibit a low Hmax/Xmin. GROWTH AND SEXUAL DIMORPHISM OF LITTORARIA Figure 6. Variation of the proportion of mature snails with height of the shell. A. Males and females of Littoraria zebra. B. Males and females of L. variegata. Table 3. Parameters of the logistic model, model fit estimation (deviance) and estimates of the average size of sexual maturity (X50%) for males and females of Littoraria zebra and L. variegata. Parameter L. zebra (SE) L. variegata (SE) b0 213.090 (1.420)* 216.732 (2.049)* b1 21.674 (0.374)* 25.020 (0.730)* b2 0.752 (0.079)* 0.987 (0.117)* x237 ¼ 28.555, P ¼ 0.839 x231 ¼ 11.885, P ¼ 0.999 X50% females (mm) 19.64 (0.310) 22.03 (0.280) X50% males (mm) 17.42 (0.333) 16.95 (0.310) Deviance DX50% (mm) 2.23 (0.454)* 5.08 (0.408)* *P , 0.0001. Figure 7. Relationship between maximum height and minimum size at maturity (Hmax/Xmin) and Hmax for different species of Littorininae in the tropical Eastern Pacific and western Atlantic (Littoraria), the tropical western Atlantic (Echinolittorina and Cenchritis) and temperate north Atlantic (Littorina). Data for L. zebra and L. variegata without an asterisk were taken from this study (M ¼ males, H ¼ females); *from Reid (1999a); **from Borkowski (1974); ***from Williams (1964); ****from Cronin, Myers & O’Riordan (2000). 293 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 maturity, both sexes reached similar maximum sizes. The minimum sizes of maturity were slightly different and the average sizes significantly so between males and females. This suggests that the rate of energy accumulation of mature males was higher than that of females, although not sufficient to change the maximum size of the sexes. The present study shows sexual dimorphism in size and the morphology of the shell in L. variegata, but not in L. zebra, a sympatric and closely related species. Unfortunately there is no information available on these littorinids of the tropical eastern Pacific to allow comparisons. Although Cruz (1987) described the morphometry and growth of L. variegata in Costa Rica, he did not evaluate sexual dimorphism in size, or compare growth for each sex. Sexual dimorphism, especially in body size, has frequently been explained by the hypothesis of sexual selection and there is evidence for this in some gastropods (Erlandsson & Johannesson, 1994; Fairbairn, 1997; Erlandsson & RolánAlvarez, 1998; Son & Hughes, 2000; Cruz, Rolán-Álvarez & Garcı́a, 2001). The increase of fecundity of larger females confers higher fitness on larger individuals (Shine, 1989; Ilano, Fujinaga & Nakao, 2004). Erlandsson & Johannesson (1994) demonstrated sexual selection in Littorina littorea; the largest females are preferred for copulation and fecundity correlated positively with the size. It is probable, therefore, that selective pressure has favoured higher growth rates that allow females of L. variegata to reach adult size in shorter time. The sexual differences in globosity can also be explained under the hypothesis of fecundity selection, since females with relatively more spherical shells have larger internal volume (Kemp & Bertness, 1984; Son & Hughes, 2000), which holds more reproductive tissue (Son & Hughes, 2000). On the other hand, growth differences between males and females of L. variegata are also related to sexual dimorphism of shell globosity and thickness. Females grow faster and show a relatively thinner and more spherical shell than males. Kemp & Bertness (1984) found the same trend in Littorina littorea; at faster growth rates the shell was more spherical with a larger volume available to store a larger body mass. Assuming that the availability of calcium carbonate is the same for males and females, to produce a more spherical shell the same quantity of calcium carbonate should be distributed over a larger surface; this may explain why the shell is thinner. Consequently, spherical shells maximize the available internal volume for a given body mass, J. M. RIASCOS AND P. A. GUZMAN ACKNOWLEDGEMENTS This study was financed by the Instituto para la Investigación y Preservación del Patrimonio Cultural y Natural del Valle del Cauca (INCIVA) and Universidad del Valle (Colombia). We would like to thank David Reid for providing useful literature and Efraı́n Rubio for valuable comments on an earlier version of this manuscript. We also thank Paola Andrea Gonzalez for her assistance in field work. REFERENCES BLANCO, J.F. & CANTERA, J.R. 1999. The vertical distribution of mangrove gastropods and environmental factors relative to tidal 294 Downloaded from https://academic.oup.com/mollus/article/76/3/289/1046730 by guest on 06 July 2022 level at Buenaventura Bay, Pacific coast of Colombia. Bulletin of Marine Science, 65: 617– 630. BORJESSON, D.L. & SZELISTOWSKI, W.A. 1989. Shell selection, utilization and predation in the hermit crab Clibanarius panamensis Stimpson in a tropical mangrove estuary. Journal of Experimental of Marine Biology and Ecology, 133: 213 –228. BORKOWSKI, T.V. 1974. Growth, mortality, and productivity of south Floridian Littorinidae (Gastropoda: Prosobranchia). Bulletin of Marine Science, 24: 409–438. CANTERA, J.R., THOMASSIN, B.A. & ARNAUD, P.M. 1999. Faunal zonation and assemblages in the Pacific Colombian mangroves. Hydrobiologia, 413: 17–33. CHOW, V. 1987. 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Von Bertalanffy’s growth equation should not be used to model age and size at maturity. American Naturalist, 149: 381–393 DIETZ, E.J. 1989. Teaching regression in a nonparametric statistics course. American Statistician, 43: 35–40. DUNCAN, R.S. & SZELISTOWSKI, W.A. 1998. Influence of puffer predation on vertical distribution of mangrove littorinids in the Gulf of Nicoya, Costa Rica. Oecologia, 117: 433–442. ERLANDSSON, J. & JOHANNESSON, K. 1994. Sexual selection on female size in a marine snail, Littorina littorea (L.). Journal of Experimental Marine Biology and Ecology, 181: 145–157. ERLANDSSON, J. & ROLÁN-ALVAREZ, E. 1998. Sexual selecction and assortative mating by size and roles in the maintenance of a polymorphism in Swedish Littorina saxatilis populations. Hydrobiologia, 378: 59–69. FAIRBAIRN, D.J. 1997. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics, 28: 659–687. GUZMÁN, P.A. 2003. Crecimiento, madurez sexual y dimorfismo sexual de Littoraria zebra y L. variegata (Mollusca: Mesogastropoda) en un manglar de Bahı´a Málaga, Pacı´fico de Colombia. Tesis de Pregrado, Universidad del Valle, Cali, Colombia. HAMILTON, P.V. 1978. Intertidal distribution and long-term movements of Littorina irrorata (Mollusca: Gastropoda). Marine Biology, 46: 49–58. HART, A. & BEGON, M. 1982. The status of general reproductive strategy theories, illustrated in winkles. Oecologia, 52: 37– 42. HOLLANDER, H., ADAMS, D.C. & JOHANNESSON, K. 2006. Evolution of Adaptation through allometric shifts in a marine snail. Evolution, 60: 2490–2497. ILANO, A.-S., FUJINAGA, K. & NAKAO, S. 2004. Mating, development and effects of female size on offspring number and size in the neogastropod Buccinum isaotakii (Kira, 1959). Journal of Molluscan Studies, 70: 277–282. JENSEN, P.D., CHRISTENSEN, J.T. & MACINTOSH, D.J. 1999. Growth and survival in the mangrove snail Littoraria intermedia (Philippi, 1846). Phuket Marine Biological Center Special Publication, 19: 69– 73. JOHANNESSON, K., ROLÁN-ALVAREZ, E. & ERLANDSSON, J. 1997. Growth rate differences between upper and lower shore ecotypes of the marine snail Littorina saxatilis (Olivi) (Gastropoda). Biological Journal of the Linnean Society, 61: 267– 279. while they minimize the quantity of calcium carbonate required to enclose this body mass (Kemp & Bertness, 1984). Palmer (1981) found a relationship between growth rate and thickness of the shell. The assimilation of calcium carbonate limits growth rates, so that species with thick shells grow slower than species with thinner shells. This relationship may explain the faster growth and smaller thickness of female shells of L. variegata in comparison with males and females of L. zebra. Due to the absence of data on growth rates in small males (,17 mm) of L. variegata (Fig. 3) it is not possible to determine conclusively that the same relationship applies. Nevertheless, since shells of male L. variegata are also thinner than the shells of L. zebra, differences in its rate of growth could also be expected. Therefore, L. zebra seems to allocate more energy to thicken its shell, with correspondingly lower growth rates, while L. variegata invests less energy in building shells, thus permitting higher growth rates. Strategies of energy allocation for growth and thickening of the shell in each species could be explained by the hypothesis that relates vertical zonation and predation. Predation seems to be more intense at lower levels of the intertidal zone (Cook et al., 1985; Reid, 1986, 1992; Borjesson & Szelistowski, 1989; Duncan & Szelistowski, 1998). It has been observed that species of Littoraria living in lower levels show thicker shells than species living at higher levels, where predation is low (Reid, 1986, 1992, 2001). However, the relative vertical distribution of L. zebra and L. variegata is not very clear regarding this hypothesis (Reid, 1999a); their vertical zonation was similar in the mangroves of Buenaventura Bay (Pacific of Colombia) (Blanco & Cantera, 1999), although Reid (1999a) observed L. variegata above L. zebra in swamps of Costa Rica. Also, L. zebra frequently moves towards low levels during low tide, while L. variegata remains on the aerial roots and foliage of mangrove trees for most of the time (P.A. Guzmán, unpubl.). This suggests that vertical distribution of these species can vary between localities and according to tidal phase. Further studies on vertical distributions are necessary to test this hypothesis in L. zebra and L. variegata (Reid, 1999a). Additionally, it is desirable to compare growth rates, shell morphology and predation patterns at different temporal and spatial scales in order to determine if the findings depicted here are valid only for the study site or in a more general context. If the hypothesis of the relationship between vertical zonation and predation can explain the growth patterns and shell thickness in L. zebra and L. variegata, then the interspecific differences in growth rates reflect differential use of the available resources for survival. The strategy used by L. zebra provides better protection against predation during early stages of life, while L. variegata (located at higher levels where predation intensity is reduced) invests less energy to thicken the shell and uses it instead for faster growth to reach maturity. GROWTH AND SEXUAL DIMORPHISM OF LITTORARIA SEBENS, K.P. 1987. The ecology of indeterminate growth in animals. Annual Review Ecology and Systematics, 18: 371–407. SHINE, R. 1989. 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