JOURNAL OF CRUSTACEAN BIOLOGY, 22(1): 157–161, 2002
REPRODUCTIVE CYCLE AND RECRUITMENT PERIOD OF OCYPODE QUADRATA (DECAPODA, OCYPODIDAE) AT A SANDY BEACH IN SOUTHEASTERN BRAZIL Maria Lucia Negreiros-Fransozo, Adilson Fransozo, and Giovana Bertini (MLNF, AF, GB) NEBECC (Núcleo de Estudos em Biologia, Ecologia e Cultivo de Crustáceos); (MLNF, AF) Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista, UNESP, 18618-000 Botucatu, SP, Brasil (e-mail:
[email protected]) A B S T R A C T The reproductive cycle and recruitment period of a ghost crab population from Ubatuba, São Paulo, Brazil were investigated by means of examining the developmental stages of gonads of breeding crabs and the ingress of young recruits to the studied population. Monthly collections over a one-year period were carried out during nocturnal low-tide periods at “Vermelha” beach. The morphology of the abdomen and pleopods was used for sex determination. All captured crabs were measured for carapace width and dissected for the determination of the development stage of the gonads. A total of 582 specimens was captured: 271 males, 241 females, and 70 juveniles. Size ranged from 8.5 to 37.5 mm for males, from 9.5 to 39.2 mm for females, and from 5.8 to 12 mm for early juveniles. Median size of males and females did not differ statistically. The frequency of ovigerous females was markedly low. The onset of sexual maturity in females is achieved at around 23 mm of carapace width. Mature females with advanced gonad stages were not recorded from May to September. Recruitment of young was highest during summer, but the presence of early and late juvenile specimens throughout the year indicates that continuous recruitment is taking place in the studied population.
Crabs of the genus Ocypode Fabricius, 1798, known as ghost crabs, are commonly found in tropical and subtropical sandy beaches around the world. This genus is represented in the Western Atlantic by Ocypode quadrata (Fabricius, 1787) which occurs from Rhode Island, U.S.A. (42°N and 70°W) to Rio Grande do Sul, Brazil (30°S and 50°W) (Melo, 1996). Despite its broad geographic distribution, little is known about the reproduction of members of Ocypode in the Americas. Haley (1969, 1972) studied the reproductive biology of O. quadrata along the Central Texas coast, but the wide range of distribution of this species justifies other studies in distinct geographic areas to investigate any possible variation or patterns. Reproductive periodicity has been studied in several brachyuran species by monthly sampling for the frequency of ovigerous females over a year. There are species with females reproducing year-round, others with reproduction occurring each year in one or more seasons, and still others in which the reproductive period occurs every other year in one season (usually spring). All of these patterns are correlated with favorable local environmental conditons. According to Costa
and Negreiros-Fransozo (1998), portunid crabs commonly reproduce continuously in subtropical and tropical regions because environmental conditions are generally favorable for feeding, gonad development, and larval release, whereas in temperate regions reproduction is often restricted to the warmer months. Ovigerous females of O. quadrata possibly might remain in their burrows while incubating, like in other ocypodid species (Christy, 1982). In this sense, an investigation of its reproductive cycle would be more accurate if based on combined results from gonad-development analyses and frequency estimates of first juveniles than based only on a seasonal account of the ovigerous-ratio. Reproductive cycle and recruitment of young were studied for the ghost crab O. quadrata at “Vermelha” beach (23°27′36″S and 45°02′54″W), Ubatuba, southeastern Brazil, by means of obtaining monthly records of gonad developmental stages and juvenile frequency within the studied population. MATERIALS AND METHODS Climate conditions at Ubatuba are typical of a subtropical region. Mean temperature of the surface waters is around 18°C in winter and about 29°C in summer (Negreiros-Fransozo et al., 1999). The shallow waters (< 10
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m) at the São Paulo northern coast may be relatively cold during summer due to the intrusion of South Atlantic Central Current Waters (Pires, 1992). All emergent crabs were collected during nocturnal low tide periods throughout 1998, at “Vermelha” beach, Ubatuba, São Paulo. A transect of 9 m × 500 m along the beach was scanned for crabs by three collectors each month. Captured individuals were placed in separate labeled plastic bags and frozen until later analysis. In the laboratory, crabs were coded, and their maximum carapace width (CW) measured with a caliper (0.1 mm). Crabs were examined under stereomicroscope in order to check the development of abdominal appendages as follows: early juveniles = pleopods absent; late juveniles = developing pleopods; adult crabs = fully developed pleopods. Condition of gonad development was also verified under stereomicroscope following, in general, the criteria suggested by Haley (1972) and Costa and Negreiros-Fransozo (1998). The gonads were classified according to shape, size, and color as follows: Females: Immature (I) = ovary thin and translucent, undifferentiated; Initial Maturing (IM) = color ranging from opaque white to pale-yellow, ovary branches and their connection clearly visible; Advanced Maturing (AM) = ovary fills almost whole thorax cavity, bright orange coloured, lobes are evident. Males: Immature (I) = testicles and deferent ducts cannot be observed; Initial Maturing (IM) = testicles are recognized only under magnification, gonad filamentous and transparent or whitish; Advanced Maturing (AM) = testicles are fully developed, bright white deferent ducts can be clearly divided in their front, median and back portions. Environmental data (air temperature, water surface temperature, and pluviosity) were provided by the “Instituto Oceanográfico” of “Universidade de São Paulo.” A Kruskal-Wallis test was used for comparing median size among individual categories (P < 0.05) (Sokal and Rohlf, 1995). Pearson’s correlation analysis was used for testing the association between air temperature, sea water surface temperature, and pluviosity with the percentage of functionally mature females bearing advanced maturing gonads (α = 0.05) (Sokal and Rohlf, 1995).
RESULTS A total of 582 crabs, comprising 271 males, 241 females, and 70 early juveniles, was obtained. Males and females were recorded in all samples, but early juvenile crabs were not recorded in April, July, or December (Table 1). Ovigerous females comprised a very small percentage (2.6%) of the total sampled population and of all females captured (6.2%). Size-frequency distribution using 3 mmwide size classes indicate a bimodal distribution in the population probably corresponding to two age-groups (Fig. 1). Crabs of both sexes with maturing (= developed) gonads were found. By analyzing the frequency of maturing individuals in each size class, we concluded that the beginning of gonad maturation occurs at a mean size of about 20 mm for males and 23 mm for females.
Table 1. Number of Ocypode quadrata collected each month throughout 1998 at “Vermelha” beach, São Paulo, Brazil.
Month
Early juvenile crabs
Males
Non-ovigerous females
Ovigerous females
Total
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
21 25 6 0 2 6 0 2 3 2 3 0 70
30 37 49 15 15 14 10 22 14 15 30 20 271
29 7 28 23 21 10 27 26 13 9 16 17 226
0 3 5 4 1 0 0 0 0 1 1 0 15
80 72 88 42 39 30 37 50 30 27 50 37 582
Size range within each population category is 8.5–37.5 mm for males, 9.5–39.2 for females, and 5.8–12 mm for early juveniles. The median sizes of males and females did not differ statistically (P > 0.05) (Fig. 2). Carapace width of the ovigerous crabs was 30.4 ± 4.3 mm and varied from 24.5 to 39 mm. Juvenile and adult crabs were found throughout the year; however, the highest captures occurred in austral summer (from January to March) (Fig. 3). The temporal frequency of early juveniles indicates that the highest recruitment period occurs during summer months. Gonads of crabs collected during summer, early fall, and early spring were found to span all developmental stages independently of sex (Fig. 4a, b). For females, all stages of gonad development co-occurred from October to April, but apparently there were two pulses of ovigerous females (one from February to May and another from October to November). The relative frequency of functionally mature females with advanced mature gonads tends to increase with increasing air temperature and sea water surface temperature (Fig. 5) (correlation coefficient r = 0.60 for air temperature, r = 0.64 for water surface temperature (P < 0.05)). Additionally, the correlation coefficient for pluviosity was r = 0.67 (P < 0.05). DISCUSSION The size-frequency distribution of the sampled population of O. quadrata at “Vermelha” beach shows a bimodal distribution that could
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Fig. 1. Seasonal size-frequency distributions of Ocypode quadrata (n = 512). Sex and stages of gonad development are distinguished. Monthly sample sizes in Table 1.
indicate two different age-groups during the study period. Alberto and Fontoura (1999), who studied a more southern Brazilian ghost crab population, found the same pattern of size distribution of this species. However, it should be pointed out that the low incidence of crabs from 16.6 to 24.5 mm of CW in the present work, particularly in the case of fe-
males, might be due to their cryptic habit. This could indicate the existence of a critical phase when crabs remain in their burrows to avoid predation, thus making their capture more difficult compared to other crabs.
Fig. 2. Ocypode quadrata. Size comparison among population categories (* indicates significant difference; P < 0.05). Sample sizes in Table 1.
Fig. 3. Ocypode quadrata. Montly relative frequency of each population category during the study period. Sample sizes in Table 1.
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Fig. 5. Association between environmental temperature (air and surface water) with proportion of mature females throughout the year.
Fig. 4. Ocypode quadrata. Proportion of crabs bearing gonads in each developmental stage during the study period. a, Females; b, Males (* indicates the presence of ovigerous females). Monthly sample sizes in Table 1.
Environmental conditions are commonly mentioned as influencing some physiological processes (Sastry, 1983). Reproductive periodicity of marine organisms is usually associated with variations of certain environmental variables, such as temperature. In the southeastern Brazilian region, upwelling of the South Atlantic Central Water current is responsible for the decrease of coastal water temperature during summer, among other alterations of bottom-water characteristics (Pires, 1992). As a result, surface-water temperature often follows an equivalent seasonal trend, which directly influences the biology of the littoral ghost crab O. quadrata.
As pointed by Alberto and Fontoura (1999) for a southern Brazilian ghost crab population, the reproductive activity of O. quadrata in Ubatuba is also characterized by a heterogeneity in female gonad maturation, which is represented by an extended reproductive period (from October to May). Based on the temporal variation of the proportions of crabs (males and females) with advanced maturing gonads, it is assumed that reproduction follows a seasonal trend in the Ubatuba region. However, early juveniles are present yearround, indicating continuous recruitment to the adult population. The fact that the abundance of females with fully developed gonads is positively correlated with air temperature, surface water temperature, and pluviosity (P < 0.05) may indicate that better conditions for gonad development are met during the warmer and rainy season. On the other hand, a decrease of water temperature caused by the South Atlantic Central Waters in the warmer months could delay larval release by ovigerous females, diminishing juvenile recruitment. Comparatively, the ghost crabs studied in the North Western Atlantic are bigger than those studied in the South Western Atlantic. The maximum sizes attained by the adult crabs of O. quadrata on the Brazilian coast have been 39.7 mm of CW (Alberto and Fontoura, 1999), 40.7 mm of CW (Corrêa and Fransozo, 2000), and 39.2 mm of CW (present study). On the other hand, Milne and Milne (1946) found a ghost crab as large as 48 mm of CW, and Haley (1969) recorded another one with 53.5 mm of maximum CW. In our study area, O. quadrata attains maturity at a smaller size than that determined by
NEGREIROS-FRANSOZO ET AL.: REPRODUCTIVE CYCLE AND RECRUITMENT OF O. QUADRATA
Haley (1969 and 1972) on the Texas central coast (males ≥ 24 mm and females ≥ 26 mm of CW). Whether such difference represents genotypic variations or environmental constraints, e.g., different availability of food resources between these studied areas as found for other brachyuran crabs (Conde and Díaz, 1989; Díaz and Conde, 1989), awaits further research. However, there are at least two papers (Wolcott, 1978; Robertson and Pfeiffer, 1982) that discuss different kinds of feeding behavior for O. quadrata (predators, scavengers, or deposit feeders) as a function of food availability in the habit. While remaining in their burrows throughout brooding, female ocypodid crabs may either incubate their eggs without feeding (e.g., Uca pugilator, Christy, 1982; O. ceratophthalmus, Haley, 1973), or feed actively during such period (e.g., U. vocans, Salmon, 1984). The small number of ovigerous crabs obtained in this investigation suggest that they can stay in their burrows for brood protection. Those females were probably just leaving their burrows for larval release when they were captured. Further evidence of such cryptic habit is provided by the fact that all ovigerous females collected were carrying eggs about to hatch. Another possibility concerning the low occurrence of ovigerous crabs could be an artifact of small sample size; however, other studies on this species (Alberto and Fontoura, 1999; Corrêa and Fransozo, 2000) also found a low percentage of this demographic category. ACKNOWLEDGEMENTS To FAPESP (Fundação de Amparo à Pesquisa no Estado de São Paulo) for providing good infrastructure conditions for investigation (#94/4878-8; #95/8520-3) and FUNDUNESP (Fundação de Amparo à Pesquisa na Universidade Estadual Paulista) for financial support to the first author to attend The Crustacean Society 1999 Summer Meeting. Authors are grateful to Rogério C. Costa for his help during samplings.
LITERATURE CITED Alberto, R. M. F., and N. F. Fontoura. 1999. Distribuição e estrutura etária de Ocypode quadrata (Fabricius, 1787) (Crustacea, Decapoda, Ocypodidae) em praia arenosa do litoral sul do Brasil.—Revista Brasileira de Biologia 59: 95–108. Christy, J. H. 1982. Burrow structure and use in the sand fiddler crab, Uca pugilator (Bosc).—Animal Behavior 30: 687–694. Conde, J. E., and H. Díaz. 1989. Productividad del habitat e historias de vida del cangrejo de mangle Aratus pisonii (H. Milne Edwards) (Brachyura, Grapsidae).—
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Boletín del Instituto Oceanografico de Venezuela, Univ. Oriente 28: 113–120. Costa, T. M., and M. L. Negreiros-Fransozo. 1998. The reproductive cycle of Callinectes danae Smith, 1869 (Decapoda, Portunidae) in the Ubatuba region, Brazil.—Crustaceana 71: 615–627. Corrêa, M. O. D. A., and A. Fransozo. 2000. Spatial and temporal distribution of Ocypode quadrata (Fabricius, 1787) (Crustacea, Decapoda, Ocypodidae) from the northern coast of São Paulo state, Brazil.—Abstracts of The Crustacean Society 2000 Summer Meeting, Puerto Vallarta, Mexico. p. 21. [Unpublished.] Díaz, H., and J. E. Conde. 1989. Population dynamics and life history of the mangrove crab Aratus pisonii (Brachyura, Grapsidae) in a marine environment.— Bulletin of Marine Science 45: 148–163. Haley, S. R. 1969. Relative growth and sexual maturity of the Texas ghost crab, Ocypode quadrata (Fabr.) (Brachyura, Ocypodidae).—Crustaceana 17: 285–297. ———. 1972 Reproductive cycling in the ghost crab, Ocypode quadrata (Fabr.) (Brachyura, Ocypodidae).— Crustaceana 23: 1–11. ———. 1973. On the use of morphometric data as a guide to reproductive maturity in the ghost crab, Ocypode ceratophthalmus (Pallas) (Brachyura, Ocypodidae).— Pacific Science 27: 350–362. Melo, G. A. S. 1996. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. Ed. Plêiade, São Paulo, SP, Brazil. 604 pp. Milne, L. J., and M. J. Milne. 1946. Notes on the behavior of the ghost crab.—The American Midland Naturalist 80: 362–380. Negreiros-Fransozo, M. L., J. M. Nakagaki, and A. L. D. Reigada. 1999. Seasonal occurrence of decapods in shallow waters of a subtropical area. Pp. 351–361 in J. C. von V. Klein and F. R. Schram, eds. The Biodiversity Crisis and Crustacea. Crustacean Issues 12. A. A. Balkema, Rotterdam/Brookfield, The Netherlands. Pires, A. M. S. 1992. Structure and dynamics of benthic megafauna on the continental shelf offshore of Ubatuba, southeastern Brazil.—Marine Ecology Progress Series 86: 63–76. Robertson, J. R., and W. J. Pfeiffer. 1982. Deposit feeding by the ghost crab Ocypode quadrata (Fabricius).— Journal of Experimental Marine Biology and Ecology 56: 165–177. Salmon, M. 1984. The courtship, aggression and mating system of a “primitive” fiddler crab (Uca vocans: Ocypodidae).—Transactions of the Zoological Society of London 37: 1–50. Sastry, A. N. 1983. Ecological aspects of reproduction. Pp. 179–270 in W. B. Vernberg, ed. The Biology of Crustacea. Vol. 8. Environment Adaptations. Academic Press, New York. Sokal, R. R., and R. J. Rohlf. 1995. Biometry. Third Edition. W. H. Freeman and Co., New York. Wolcott, D. L., and T. G. Wolcott. 1987. Nitrogen limitation in the herbivorous land crab Cardisoma guanhumi.—Physiology and Zoology 60: 262–268. Wolcott, T. G. 1978. Ecological role of ghost crabs, Ocypode quadrata (Fabricius) on an ocean beach: scavengers or predators?—Journal of Experimental Marine Biology and Ecology 31: 67–82. RECEIVED: 11 August 2000. ACCEPTED: 21 June 2001.
