Reproductive Biology of Hepatus Pudibundus (Crustacea: Brachyura), the Most Abundant Crab on the Southeastern Brazilian Coast

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Biologia 69/2: 219—227, 2014 Section Zoology DOI: 10.2478/s11756-013-0301-4

Reproductive biology of Hepatus pudibundus (Crustacea: Brachyura), the most abundant crab on the southeastern Brazilian coast

Paloma Aparecida de Lima1,GiovanaBertini2, Vivian Fransozo3, Rafael Augusto Gregati4, Lissandra Correaˆ Fernandes-Góes5 &AntônioLeao˜ Castilho1 NEBECC (Crustacean Biology, Ecology and Culture Study Group)

1Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de Botucatu, São Paulo, Brazil; e-mail: [email protected] 2Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus Experimental de Registro. Registro, São Paulo, Brazil 3Universidade Estadual do Sudoeste da Bahia, Vitória da Conquista, Bahia, Brazil 4Universidade Estadual do Centro-Oeste do Paraná, Guarapuava, Paraná, Brazil 5Universidade Estadual do Piauí. Parnaíba, Piauí, Brazil

Abstract: This study analyzed the size at sexual maturity and reproductive period of populations of Hepatus pudibundus in three bays on the northern coast of S˜ao Paulo, Brazil. Crabs were collected monthly and the bottom-water temperature was measured at each collection point. The animals were sexed, measured for carapace width (CW), and their gonadal stages were determined. A total of 8,674 specimens were collected (2,435 males and 6,239 females). Adult males showed the highest mean CW; the size at maturity for both sexes was 32.5 mm CW. Reproduction was continuous and peaked in spring and summer, because of the greater availability of plankton food for the larvae. This pattern is typical in tropical and subtropical regions, unlike the seasonal reproduction found in temperate regions. Reproductive activity of females was not signiﬁcantly correlated with bottom-water temperatures. Immatures and individuals in all stages of gonadal development were found throughout the sampling period and at all depths, probably because the species completes its entire reproductive cycle in that area. Key words: crab; breeding season; bycatch; gonadal development; sexual maturity

Introduction nates the crustacean bycatch in Ubatuba (Bertini et al. 2010a). It is subject to the same impacts that affect Among the groups that comprise the shrimp fishery commercially important crustaceans harvested by the bycatch in the state of São Paulo, Brazil, brachyuran non-selective trawl fishery. crustaceans are prominent in both biomass and species Knowledge of reproductive biology is fundamental diversity (Severino-Rodrigues et al. 2002). The flecked for understanding the life cycle of marine organisms, for box crab Hepatus pudibundus (Herbst, 1785) belongs to administering controlled and sustainable fisheries, and the brachyuran superfamily Aethroidea, which includes for the preservation of other species that have no com- seven recent genera (Ng et al. 2008). Of these, only mercial interest, but are directly involved in the trophic Hepatus (H. pudibundus, H. scaber Holthuis, 1959 and chain (Emmerson 1994). Important components of re- H. gronovii Holthuis, 1959) and Osachila (O. antillensis productive biology, the beginning, duration and end of Rathbun, 1916 and O. tuberosa Stimpson, 1871) occur the breeding cycle and its seasonality are often ana- along the Brazilian coast (Melo 1996). Hepatus pudi- lyzed (e.g., Haefner 1978; Choy 1988; Yau 1992; Costa bundus is distributed in the western Atlantic from Geor- & Fransozo 2004; Castilho et al. 2008a, b; Bertini et al. gia (USA), the Gulf of Mexico, the Antilles, Venezuela, 2010a). and the Guianas to the entire coast of Brazil (Amapá The factors involved in the reproductive period of to Rio Grande do Sul), and in the eastern Atlantic marine crustaceans are of two types: proximal factors from Guinea to South Africa (Melo 1996). Along the (temperature and other environmental variables) that southeastern coast of Brazil, it is the most abundant influence both the beginning and the end of the incu- crab species and plays an important ecological role in bation and spawning periods; and ultimate factors (se- the fauna of marine unconsolidated substrates. Hepatus lective pressure) that determine the reproductive sea- pudibundus is not commercially marketed, but domi- son, which coincides with the period of greatest avail-

c 2013 Institute of Zoology, Slovak Academy of Sciences 220 P. Aparecida de Lima et al.

Fig. 1. Map of Ubatuba Bay, northern São Paulo state, indicating the location of the sampling transects. ability of plankton food (Sastry 1983). Environmen- for two years, in three areas near Ubatuba, São tal factors that may influence reproductive patterns of Paulo. marine crustaceans include temperature, salinity, light, and food availability (Bauer & Vega 1992; Bauer & Lin Material and methods 1994). Sampling of crabs and environmental variables Size at maturity is an important factor in deter- The specimens were collected monthly from January 1998 mining the reproductive capacity of a species (Hart- through December 1999, in Ubatumirim, Ubatuba and Mar noll & Gould 1988; Hines 1989). In brachyuran crabs, Virado bays on the northern coast of São Paulo state. Each this can be estimated by observing the external mor- bay was separated into two areas, which were identified as phology and size, stage of development and functioning sheltered (transects at 5, 7.5 and 10 m depth) and exposed condition of the gonads (Reigada & Negreiros-Fransozo (10, 15 and 20 m) to currents and waves (Fig. 1). Each 1999). depth level was sampled in the morning, using a shrimp Numerous studies have treated aspects of the re- boat equipped with a double-rig trawl net with a mouth approximately 4.5 m in diameter and mesh of 20 mm between production of brachyuran crabs. Examples in Brazil in- opposite knots and 15 mm in the cod end. At each depth, clude the reproductive cycle of Callinectes danae Smith, the trawl covered approximately 2 km (30 min of trawling), 1869 (Costa & Negreiros-Fransozo 1998), fertility and i.e., an area of 18,000 m2. reproduction of Arenaeus cribrarius Lamarck, 1818 During the trawls, an ecobathymeter coupled with a (Pinheiro & Terceiro 2000), sexual and functional matu- GPS (Global Positioning System) was used to record the rity of Chaceon affinis (A. Milne-Edwards & Bouvier, depth (m) at the sampling sites. In each bay and transect, surface- and bottom-water samples were taken with a 1894) (Fernándes-Vergaz et al. 2000), growth and re- ◦ production of Charybdis bimaculata (Miers, 1886) (Doi Nansen bottle, and temperature ( C) and salinity were mea- et al. 2008), physiological maturity and the relationship sured with a mercury thermometer and an optical refrac- tometer, respectively. As H. pudibundus is a benthic species, of growth and reproduction of Goniopsis cruentata (La- only the bottom measurements were used in the statistical treille, 1802) (Cobo & Fransozo 2005) and reproductive analyses, while both surface and bottom measurements were period and size at maturity of Persephona mediterranea used to characterize the study area. (Herbst, 1794) (Bertini et al. 2010b). Sediment samples were obtained during each season The abundance of H. pudibundus on the northern with a 0.06 m2 Van Veen grab, to analyze sediment grain- coast of São Paulo (Bertini & Fransozo 2004) makes size composition and organic-matter content. The texture this crab an accessible and valuable subject for study. and organic-matter content of the sediment were measured Some aspects of the population and general biology as described by Bertini et al. (2001) and Almeida et al. of H. pudibundus have been studied by Mantelatto (2012). & Fransozo (1994: relative growth and sexual dimor- Biological material phism); Mantelatto et al. (1995a, b: distribution and The specimens of H. pudibundus were identified according to population structure), Reigada & Negreiros-Fransozo Melo (1996), sexed, and measured for carapace width (CW) (1995: fecundity); Reigada & Negreiros-Fransozo (1999 with a caliper (0.1 mm). Males and females were categorized and 2000: sexual maturity and reproductive cycle). as immature or adult based on macroscopic observations of the shape and adherence of the abdomen to the thoracic These studies took place in one region and at shal- sternites (Taissoun 1969). All crabs were dissected and their low depths. The present study determined the size gonads were classified macroscopically in four stages (im- at which males and females of H. pudibundus reach mature, rudimentary, developing and advanced) depending sexual maturity, and investigated their reproductive on the shape, color and volume, according to Reigada & period with a spatial approach (different depths) Negreiros-Fransozo (2000). Reproductive biology of Hepatus pudibundus 221

Data analysis The 5% significance level was used for all tests. The samples obtained from the transects at Ubatumirim, Ubatuba and Mar Virado were used as replicates, so that each transect provided three replicates for each month. The monthly means were used in graphing the data. Initially, the as- sumptions of homoscedasticity (Levene test) and normal- ity (Shapiro-Wilks test) were tested, and the data were log(x+1) transformed prior to analysis (Zar 1999). The differences in abundance of demographic groups (immature specimens, adult males, adult females and ovigerous females) were compared between areas (sheltered and exposed) and transects (5, 7.5, 10s, 10e, 15 and 20 m), between years (1998 and 1999) and among seasons (sum- Fig. 2. Granulometric fractions, organic matter (%OM) content mer: January to March; autumn: April – June; winter: July – and the mean of phi for each transect. Grain-size classes (%): September and spring: October – December). For these com- Class A: medium sand, coarse sand, very coarse sand and gravel; parisons, we used a factorial analysis of variance (ANOVA) Class B: fine sand and very fine sand; Class C: silt + clay. followed by multiple comparison tests (Tukey). The reproductive period was estimated from the proportions of ovigerous females and specimens with advanced (or fully developed) gonads (AD) during the two years. The correlation analysis. The carapace width was compared for relationship between the different stages of gonadal devel- each sex through the Mann-Whitney test (Zar 1999). opment and the seasons during the two years was evaluated To determine the curve of sexual maturity, males and by Correspondence Analysis (CA) (Leps & Smilauer 2003). females were analyzed separately and the specimens divided The proportion of individuals with advanced gonads into immatures and adults. The relative frequency (%) of in- and ovigerous females was compared with the mean monthly dividuals in each size class was plotted on a graph, and a values for the environmental factors (bottom-water temper- sigmoid curve resulting from the logistic equation, where ature and salinity, organic matter and phi) by Spearman CW50 = the carapace width at which 50% of individuals

Fig. 3. Seasonal variations of the surface and bottom temperatures (median, percentiles, and range). 222 P. Aparecida de Lima et al. attain sexual maturity, and r = the slope of the curve, was ﬁtted by the least-squares method (Aguilar et al. 1995; Vaz- zoler 1996).

Results

Environmental variables The granulometric composition of the sediment var- ied among transects, with a predominance of fine and very fine sand and silt + clay, except on the 20-m transect where the sediment was more heterogeneous (Fig. 2). Transects in the sheltered area contained more organic matter than those in the exposed area (means 5.4 ± 0.7 and 3.9 ± 0.9, respectively). The highest (6.2%) and lowest (2.9%) percentages of organic matter were recorded at depths of 10 m (sheltered area) and 20 m (exposed area), respectively. The exposed area had the lowest mean phi (4.1 ± 1.0), indicating coarser sediment than in the sheltered area (5.1 ± 0.5). The warmest bottom- and surface-water temperatures were recorded in the summers of 1998 (25.3 ± 3.2; 28.8 ± 1.0, respectively) and 1999 (26.2 ± 2.9; 29.2 ± 0.9, respectively). Bottom- and surface-water temperatures differed most in summer and least in winter. The bottom water was usually coldest in the deeper areas, with a maximum on the 20-m transect in spring (16 ◦C) (Fig. 3).

Biological material During the study period, a total of 432 trawls resulted in 8,674 crabs collected, including 2,092 adult males, 5,031 adult females, 718 ovigerous females and 833 immatures (343 males and 490 females). Of the total, 4,228 were captured in 1998 and 4,446 in 1999. The mean numbers of individuals per demographic category, area and transect are shown in Fig. 4. Imma- ture crabs were more abundant in the sheltered area (ANOVA, P = 0.0002, F = 13.37), while adult males and ovigerous females were more abundant (although not signiﬁcantly) in the exposed area (ANOVA, P = 0.098, F = 2.75; P = 0.50, F = 0.46, respectively). Spa- tially, males (ANOVA, P = 0.000, F = 11.30) and adult females (ANOVA, P = 0.041, F = 4.16) were captured in larger numbers on the 10-m transect (sheltered area) and at the 15- and 20-m depths (exposed area); oviger- Fig. 4. Hepatus pudibundus. Mean number of individuals (immatures, adult males and females and ovigerous females) and ous females were more numerous at the 15- and 20-m standard deviation on each transect, from January 1998 through depths (Tukey, P < 0.05). December 1999. Immature individuals and adults in every stage of gonadal development were caught throughout the sampling period (Fig. 5). Immature crabs were more abun- tively related to winter, spring and autumn, and DE dant in summer (329 individuals). and RU males were positively related to summer. The results of the correspondence analysis (CA) The proportions of males and females with devel- for adult males and females through each season of 1998 oped gonads and of ovigerous females were analyzed in and 1999 are shown in Fig. 6. For females, axis 1 ex- relation to changes in the environment, using the Spear- plained 74.48% of the variation, and we observed the man correlation. Males exhibited a negative correlation following positive relationships: ovigerous females (OF) with bottom-water temperature (Spearman, P = 0.01, were related to summer, AD (advanced/developed) fe- r = –0.12) and a positive correlation with phi (Spear- males to spring, RU (rudimentary) females to autumn, man, P = 0.000, r = 0.24). The analyses involving fe- and DE (developing) females to winter. With regard to males indicated no correlation with the environmental males, axis 1 explained 85.81%; AD males were posi- factors. Reproductive biology of Hepatus pudibundus 223

Fig. 5. Hepatus pudibundus. Monthly variation of the mean number of individuals in diﬀerent stages of gonadal development and standard deviations, from January 1998 through December 1999. 224 P. Aparecida de Lima et al.

Table 1. Hepatus pudibundus. Number of individuals (N), mean and standard deviation (SD), and minimum and maximum carapace width (mm) in each demographic group.

Demographic group N CW (mm) means ± SD Minimum (mm) Maximum (mm)

Juvenile males 114.3 ± 40.8 29.0 ± 4.8 5.4 40.6 Adult males 697.3 ± 161.4 50.7 ± 8.8 27.8 75.2 Juvenile females 163.3 ± 38.2 29.7 ± 4.6 9.7 54.0 Adult females 1677.0 ± 105.5 47.1 ± 6.4 28.4 66.2 Ovigerous females 239.3 ± 24.4 49.2 ± 6.2 22.6 81.4

Fig. 7. Hepatus pudibundus. Hypothetical graphical representa- tion of the maturity curve according to carapace width (mm) of males and females at all collection points from January 1998 through December 1999.

Fig. 6. Hepatus pudibundus. Correspondence Analysis (CA), cor- responding to the number of males and females in diﬀerent stages H. pudibundus reached maturity in the same size range, of gonadal development (RU: rudimentary, DE: developing, AD: 32.46 mm CW for males and 32.51 mm for females. advanced, OF: ovigerous female) by season in 1998 and 1999 (Su: summer; A: autumn; W: winter; Sp: spring). Discussion Carapace width ranged from 5.4 to 81.4 mm (Table 1), and the mean CW was larger for males The presence of ovigerous females and individuals with (47.7 mm) than for females (46.0 mm) (Mann-Whitney, advanced gonads has been used to estimate the repro- P < 0.001). ductive cycles of brachyuran crabs (Batoy et al. 1987; The distribution of individuals at diﬀerent stages Mantelatto & Fransozo 1999; Reigada & Negreiros- of gonadal development (RU, DE and AD) and the per- Fransozo 1999). In the bays at Ubatuba, immatures and cent variation of males, females with advanced-stage go- individuals in all stages of gonadal development (RU, nads and ovigerous females on each transect are shown DE, AD) were found during the two years of sampling in Table 2. On all transects, we found ovigerous fe- and on all transects of both exposed and protected ar- males and individuals in rudimentary, developing and eas, because the species completes its entire reproduc- advanced stages. tive cycle in the study area. The size at which 50% of individuals attain sexual The presence of males and females showing re- maturity is represented in Fig. 7. Males and females of productive activity throughout the study period sug- Reproductive biology of Hepatus pudibundus 225

Table 2. Hepatus pudibundus. Distribution of individuals (mean ± standard deviation) in diﬀerent stages of gonadal development (RU: rudimentary, DE: developing, AD: advanced, OF: ovigerous female) on transects from January 1998 through December 1999.

Areas / Transects Individuals Gonad Sheltered Exposed 5 m 7.5 m 10 m 10 m 15 m 20 m

IM 12.3 ± 19.6 31.7 ± 28.1 32.3 ± 31.8 6.0 ± 3.6 23.0 ± 14.4 9.0 ± 6.0 RU 10.7 ± 11.5 20.7 ± 6.4 40.7 ± 29.0 11.7 ± 5.0 44.0 ± 13.1 31.0 ± 17.1 Males DE 10.3 ± 7.5 17.7 ± 5.5 40.3 ± 27.9 15.3 ± 4.0 46.3 ± 15.6 40.3 ± 18.4 AD 38.0 ± 14.8 40.0 ± 6.2 967.7 ± 54.5 39.0 ± 11.5 95.0 ± 50.3 58.7 ± 29.6

IM 19.0 ± 26.9 46.7 ± 46.2 39.7 ± 22.7 10.3 ± 5.0 31.0 ± 20.1 16.7 ± 12.5 RU 46.0 ± 16.7 50.0 ± 13.2 105.0 ± 63.0 43.0 ± 10.5 156.7 ± 68.8 129.3 ± 57.2 Females DE 47.7 ± 35.8 34.7 ± 4.6 84.3 ± 31.5 27.7 ± 14.4 134.0 ± 19.9 106.74 ± 26.1 AD 76.7 ± 59.1 61.0 ± 9.2 131.3 ± 64.0 58.0 ± 44.4 190.7 ± 23.6 194.3 ± 32.9 FO 32.3 ± 22.5 24.7 ± 13.5 46.3 ± 22.2 19.3 ± 19.1 68.7 ± 11.2 48.0 ± 10.5

gests that H. pudibundus reproduces continuously in According to Bauer (1992), the relatively constant Ubatuba. This concords with the findings of Reigada high temperatures in tropical regions during the year & Negreiros-Fransozo (2000), who studied the repro- allow continuous breeding in a variety of marine in- ductive cycle of H. pudibundus; Santos & Negreiros- vertebrates. Reproduction occurs when conditions are Fransozo (1999) for Achelous spinimanus (Latreille, favorable for both adults and larvae; for the latter to 1819); Bertini et al. (2010b) for Persephona mediter- hatch, a suitable planktonic food supply is needed (Sas- ranea; and Rasheed & Mustaquim (2010) for Portunus try 1983). The temporal variation in larval food supply, sanguinolentus (Herbst, 1783). Continuous reproduc- i.e., the seasonal pattern of primary and secondary pro- tion is commonly found in brachyuran crabs of tropical duction, would then be an important selective pressure and subtropical regions (Costa & Negreiros-Fransozo acting to regulate the reproductive cycle in marine ben- 1998). thic invertebrates with planktotrophic larvae (Castilho The presence of crabs of both sexes with advanced et al. 2007). gonads and ovigerous females in all months of the year The sexual dimorphism observed in H. pudibun- has also been observed for other brachyurans in the dus in relation to the mean carapace width proba- Ubatuba area, as in Callinectes danae studied by Costa bly occurs because males direct their energy intake & Negreiros-Fransozo (1998), Achelous spinimanus in- toward somatic growth, territory defense and protec- vestigated by Santos et al. (1994), and Persephona tion of females (Mantelatto & Fransozo 1996). In con- mediterranea studied by Bertini et al. (2010b). trast, the females invest in reproduction as soon as they The factors responsible for controlling the repro- reach adulthood, as is typical for brachyurans (Hartnoll ductive period of marine organisms have drawn atten- 1985). Exogenous parameters such as temperature and tion since the beginning of the last century (Orton the related photoperiod can affect the metabolic rates 1920). Orton pointed out that, in the tropics, animals and individual growth in populations from different re- reproduce continuously or for long periods of the year, gions. This results in different sizes at the start of mat- as opposed to the seasonal reproduction found in cooler uration, as found by Hines (1989) in some species of temperate regions. However, in this study we found Brachyura from the west coast of the USA. Other fac- no significant relationship between the reproductive tors also may influence the size at sexual maturity, such activity of females and water temperatures, similarly as salinity and food availability (D’Incao et al. 1993). to Reigada & Negreiros-Fransozo (2000). The highest Although the sizes of males and females differed percentage of ovigerous females of H. pudibundus was significantly, sexual maturity was reached at a simi- found in spring, and of AD and ovigerous females in lar size in both sexes (32.5 mm CW, approximately), the summer of both years. This probably results from as also found by Reigada & Negreiros-Fransozo (1999) the higher plankton productivity during the summer in Ubatuba (23◦26 S). However, Carvalho & Couto in Ubatuba, when the South Atlantic Central Water (2006), studying H. pudibundus in Ilhéus (14◦47 S), (SACW) penetrates the bottom layer over the conti- Bahia, found different results. The size at which 50% of nental shelf and reaches the coast (Pires-Vanin & Mat- individuals reached sexual maturity was larger for both suura 1993). The SACW is a nutrient-rich water mass sexes: 37 mm CW for females and 38 mm for males. with an N:P ratio (nitrogen: phosphorus) of approxi- This contradicts the paradigm that species inhabiting mately 16:1, favoring primary productivity (Odebrecht lower latitudes reach sexual maturity at smaller sizes, & Castello 2001). According to Vega-Perez (1993), the as demonstrated by Castilho et al. (2007) for Artemesia presence of this water mass in Ubatuba is responsible, longinaris Bate, 1888, in which females at a lower lati- among other factors, for the increase in chlorophyll con- tude (southeast coast of Brazil, 23◦37 S) reach sexual tent, and consequently the increase in phytoplankton maturity at a smaller size than those at a higher lati- growth. tude (Mar del Plata, province of Buenos Aires, 37◦59 226 P. Aparecida de Lima et al.

S). Several investigators have suggested a latitudinal Exp. Mar. Biol. Ecol. 182 (2): 205–222. DOI: 10.1016/0022- paradigm in population dynamics of crustaceans (Bauer 0981(94)90052-3 1992; Bauer & Vega 1992; Boschi 1997; Gavio & Boschi Bauer R.T. & Vega W.T. 1992. Pattern of reproduction and recruitment in two sicyoniid shrimp species (Decapoda: Pe- 2004; Costa & Fransozo 2004; Costa et al. 2005; Castillo naeoidea) from a tropical seagrass habitat. J. Exp. Mar. Biol. et al. 2007). Knowledge of these factors is important Ecol. 161 (2): 223–240. DOI: 10.1016/0022-0981(92)90099-V for effective management of natural marine resources Bertini G. & Fransozo A. 2004. Bathymetric distribution of (Bauer & Vega 1992; Kuhlmann & Walker 1999), since brachyuran crab (Crustacea, Decapoda) communities on coastal soft bottoms off southeastern Brazil. Mar. Ecol. Prog. it clarifies the possible variations in the size at which Ser. 279: 193–200. 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Received March 20, 2013 Accepted August 16, 2013