IN A TROPICAL BRAZILIAN ESTUARY Roberto Sforza [PDF]

JOURNAL OF CRUSTACEAN BIOLOGY, 30(4): 597-606, 2010

DISTRIBUTION AND POPULATION STRUCTURE OF CALLINECTES DANAE (DECAPODA: PORTUNIDAE) IN A TROPICAL BRAZILIAN ESTUARY Roberto Sforza, Rosebel C. Nalesso and Jean-Christophe Joyeux (RS, RCN, J-CJ) Departamento de Oceanografia e Ecologia, Universidade Federal do Espı´rito Santo, Av. Fernando Ferrari, 514, 29.075-910, Vito´ria, ES, Brasil; (RS, corresponding author, [email protected]) Present address: Centro-TAMAR-ICMBio., Av. Paulino Muller, 1111, 29.040-715, Vito´ria, Brasil

The portunid crab Callinectes danae is abundant in Brazilian estuaries and coastal areas and is an important item to artisanal fisheries. This study investigated the distribution and population structure by sex and size, the size at sexual maturity, and sex-ratio of the species in Vito´ria Bay, Espı´rito Santo, southeastern Brazil. Crabs were collected monthly by nocturnal trawling during one year in six sampling stations distributed along an estuarine gradient and an independent depth gradient. Physico-chemical parameters of water were measured in situ on each station. A total of 3876 individuals were collected: 2537 females (1147 adults, 318 ovigerous, and 1072 juveniles), and 1339 males (444 adults and 895 juveniles). The mean carapace width (including lateral spines) at sexual maturity was 91.3 mm for males and 80.5 mm for females; the female-to-male sex ratio was 1.89:1. Adult females occurred throughout the bay and year-round, but eggbearing females were almost exclusively caught in deep and high salinity areas. Adult males and juveniles of both sexes occurred mainly in internal areas of the estuary, nearest river mouths; highest captures were registered in November. Both the scarcity of males, probably resulting from size-selective catch, and the low proportion of ovigerous females, compared with that observed in other Brazilian estuaries, suggest that the population has been overexploited.

KEY WORDS: blue crabs, Brazil, Callinectes danae, habitat partitioning, population structure, portunid crabs DOI: 10.1651/09-3223.1

Branco (1996a, b) and Branco and Verani (1997) studied the feeding ecology of C. danae at Lagoa da Conceic¸a˜o, state of Santa Catarina. Mollusca, Polychaeta, and Crustacea were the main items in stomach contents, especially during the night. This pattern varied seasonally due to prey availability and to crab ontogenic development (Branco, 1996b). Reigada and Negreiros-Fransozo (2001) registered that feeding activities of C. danae at Ubatuba, state of Sa˜o Paulo, happened mostly at night, but crabs also forage during the day if potential food items are abundant. Weber and Levy (2000) verified an important genetic heterogeneity in the population structure of C. danae in southern Brazil and stated that something associated with estuaries is restricting gene flow, preventing panmixia between populations inhabiting different estuaries. In contrast, few studies have been conducted in the Brazilian North-East, only furnishing baseline information. Thus, in the state of Alagoas, Pereira-Barros (1987) and Teixeira and Sa´ (1998) found habitat partitioning among species of Callinectes, with C. danae numerically dominant at Mundau´ lagoon, Callinectes bocourti (A. MilneEdwards, 1879) in Manguaba lagoon and C. ornatus in the channels connecting the two lagoons with the ocean. In the state of Pernambuco, Barreto et al. (2006) studied the sexual maturity of females in the estuarine system of Itamaraca´, and concluded that morphological maturity of the females of C. danae occurred before gonadal maturity. In the state of Espı´rito Santo, Carmo et al. (1994) registered C. danae as the most abundant species in the estuary of the Santa Maria da Vito´ria River.

INTRODUCTION Portunid crabs are important fishery resources along the Brazilian coast, where six species of Callinectes can be found. Callinectes danae Smith, 1869 is one of the most common species, occurring in the western Atlantic Ocean, from Florida to Argentina. It is abundant in estuaries, mangroves, and on the continental shelf down to 70 m, and from brackish to hypersaline environments (Norse, 1977; Buchanan and Stoner, 1988; Melo et al., 1989). Despite its important role in artisanal and subsistence fisheries, few studies have focused on this species. Knowledge of the population structure, biology, and feeding ecology of Brazilian species of Callinectes is mainly from south-southeastern populations. At Sepetiba Bay, state of Rio de Janeiro, Medeiros and Oshiro (1990) verified that ovigerous females of C. danae occur throughout the year, although they are more abundant in winter time. In the same state, Keunecke et al. (2008) studied the growth of C. danae caught in shrimp trawling operations in Guanabara Bay. At Ubatuba, state of Sa˜o Paulo, Costa and Negreiros-Fransozo (1998) concluded that C. danae reproduces continuously year-round. In the same place, Negreiros-Fransozo and Fransozo (1995) detected a strong habitat partitioning between C. danae and Callinectes ornatus Ordway, 1863, with C. danae preferring areas of low salinity nearest river mouths. SeverinoRodrigues et al. (2009) determined that C. danae is the dominant species of Callinectes in the estuarine system of Iguape-Canane´ia. 597

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ABSTRACT

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In spite of the scarcity of information about their population structure and reproductive biology, portunid crabs have been intensively harvested in Vito´ria Bay, with hundreds of families depending upon their capture for food or income. However, as elsewhere, offer at local markets has strongly decreased in recent years (R. Sforza, personal observation). In other states (Sa˜o Paulo), Mantelatto and Fransozo (1999) warned about a decrease in population of portunid crabs, revealing the need for frequent monitoring of natural stocks. This work aims to evaluate the spatial and temporal distribution of C. danae population in Vito´ria North-west bay and to determine the size and sexual proportion of juveniles, adults, and egg-carrying females crabs in areas subjected to different hydrological regimes. These data will contribute to furthering knowledge of the species and will help the fishery management, contributing to the sustainability of this important resource. MATERIALS AND METHODS Study Area Vito´ria Bay, state of Espı´rito Santo, southeastern Brazil (Fig. 1) has a total open water area of 35.5 km2, with about 23 km2 of remaining mangrove forest. The internal part of Vito´ria Bay estuarine system is oriented in a northeast-southwest direction and is connected to the Atlantic Ocean by two channels. For a more detailed description of the area, see Nalesso et al. (2005) and Chagas et al. (2006). Mean annual rainfall is about 1200 mm, with the rainy season extending from September to March (more intense from November to January). The main freshwater source is the Santa Maria da Vito´ria River with a mean monthly discharge from 8 m3 s21 to 24 m3 s21 (Joyeux et al., 2004). Other freshwater inputs include the Bubu River and many domestic raw sewage outlets. The area is highly urbanized, with heavy metals concentrations above legal limits, mainly close to the ports (Jesus et al., 2004). The mean tidal water level is 0.8 m (Diretoria de Hidrografia e Navegac¸a˜o; http://dhn.mar.mil.br), and the bay is under microtidal influence (tide # 2 m).

Sterza and Loureiro-Fernandes (2006) divided the Vito´ria Bay estuary into two main parts: the lower one, with waters characterized by high salinities and dissolved oxygen and lower temperatures, greatly influenced by ocean waters influx; and the upper part characterized by waters with low salinities and dissolved oxygen and higher temperatures, mainly due to the input from rivers. Our study includes two areas in the upper part (areas A and B) and one area in the lower part (area C). The predominant sediment type is medium to fine sand, poorly sorted, but with coarse sand present locally due to the influence of rivers. High organic contents made these sediments dark and with a strong odor, typical of reduced environments (Nalesso et al., 2005). Field Collections Three sampling areas were chosen according to a salinity gradient (Fig. 1). The first, area A, was located nearest the Santa Maria da Vito´ria river mouth, with a well preserved mangrove forest. Area B was located between Santa Maria da Vito´ria River and Bubu River, and shows some mangrove remains and urbanized areas on the eastern shore. Area C is much more urbanized, near two industrial ports and subjected to marine water inflow. Each area was subdivided in two sub-areas, according to depth, with the deepest (eastern) side called ‘‘channel’’ and the shallowest (western) ‘‘shallow.’’ These sub-areas were established based on practical knowledge (the unscientific but deep ecological and biological knowledge of certain biota fishermen acquire from family and local society, and develop during years practicing their trade) since there is no published bathymetry of the inner parts of the bay. The effects of tide fluctuations were minimized collecting in the same lunar phase, i.e., first quarter. From December 2000 to November 2001, monthly samplings were conducted at each of the six sub-areas at night, from 19:00 to 05:00; preliminary tests showed higher sampling capture at night. Portunid crabs were collected with an otter trawl (2.5 cm of mesh and 12 m bottom line), trawling during 12 minutes at 1.3 knot. Captures were initially stored in ice and later either frozen or preserved in formalin 10%. The sample of area A channel, from February 2001 was lost due to storage problems. Salinity, temperature, and dissolved oxygen in the bottom layer of the water column were recorded in situ before trawling using a multiparameter device (YSI 85). Depth was measured before and after each tow with a portable Speedtech SM-5 and the mean used in further analyses. Geographic position at the beginning and final of tow was estimated with a handheld GPS receiver (Garmin 48) and tow length was estimated as a straight line between these two values. The swept area was computed as the net opening (7 m) times the tow length. In case of inconsistency in

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Fig. 1. Map of northwest Vito´ria Bay, southeastern Brazil, showing the areas (A, B and C) where portunid crabs Callinectes danae were collected.

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Table 1. Results of ANOVA for depth and Kruskal-Wallis test for salinity, temperature and dissolved oxygen of bottom water at Vito´ria North-west bay, Brazil. d.f., degrees of freedom; F or H, value of the statistic; P, probability associated with the test. N 5 72.

Depth (m) (mean 6 SD)

Factor

A A B B C C

Dissolved oxygen (mg l21) (mean 6 SD)

Temperature (uC) (mean 6 SD)

A channel: 26.15 6 6.55 A shallow: 23.90 6 7.90 B channel: 28.72 6 4.24 B shallow: 25.22 6 8.01 C channel: 30.33 6 4.19 C shallow: 30.34 6 4.83 Statistics

A A B B C C

channel: 25.27 6 1.65 shallow: 25.56 6 1.80 channel: 25.06 6 1.64 shallow: 25.28 6 1.98 channel: 24.72 6 1.34 shallow: 24.61 6 1.69

A channel: 3.54 6 3.08 A shallow: 3.50 6 2.20 B channel: 2.44 6 1.34 B shallow: 3.90 6 1.47 C channel: 3.56 6 0.98 C shallow: 4.46 6 1.65

d.f. 11

F 0.720

P 0.714

d.f. 11

H 37.58

P 0.0001

d.f. 11

H 61.15

P 0.0000

d.f. 11

H 25.50

P 0.008

2

1.32

0.286

2

16.22

0.0003

2

2.63

0.2685

2

4.33

0.115

1 5

142.23 29.55

0.000 0.000

1 5

1.23 18.77

0.2671 0.0021

1 5

0.099 2.80

0.7524 0.7301

1 5

5.05 12.01

0.025 0.035

55

1.00

0.500

geographic position (N 5 8), we used the data from a mechanic flow meter (General Oceanics 2030R) previously secured to one of the trawl tow lines. Laboratory Procedure Crabs were sexed according to pleon morphology. Adults were distinguished from juveniles by their detached pleon (juveniles have the pleon sealed). Ovigerous females were also registered. The carapace width was measured (with a 0.5 mm precision Vernier caliper) as the distance between the tips of the lateral spines. Crabs with broken spines were not used in analyses using carapace width. The number of crabs was standardized per 100 m2 (CPUE or density) of area trawled. Statistical Analyses Depths of channel and shallow areas had normal distributions and were tested for differences among areas, sub-areas, months and interactions by ANOVA. Kruskal-Wallis tests were done for salinity, temperature, and dissolved oxygen due to data heteroscedasticity (Zar, 1996). Crab carapace widths (CW) were compared through Student t test for males and females, both adults and juveniles. ANOVA was used to compare CW among areas and months. The sample CPUEs, i.e., densities in number per 100 m2, for juveniles and adults of both sexes and for ovigerous females were tested for normality and homocedasticity through the Shapiro-Wilks and Levene Tests. Because none of these premises were met (even after tentative data transformation), both Kruskal-Wallis and post-hoc multiple comparisons Dunn tests were used to compare crab CPUEs among sub-areas and months. (Zar, 1996). Spearman’s correlation test was used to evaluate the relationships between biotic variables (CPUEs) and abiotic water parameters. We compared the sexual proportion between males and females by x2, and the difference in mean carapace width between males and females with Student t test. The mean size at first maturation was determined for both sexes as the point when 50% of individuals have the pleon detached, based on the linear decomposition of a logistic curve (King, 1995).

RESULTS Physico-Chemical Parameters of Water Salinity and dissolved oxygen were the most variable abiotic parameters, principally at area A and B. Salinity values during rainy months (October, November, December) were lower than 20 (down to 5.4) and significantly different from that recorded during autumn and winter

months (May to September), typically above 30 (KruskalWallis: P , 0.001) (Table 1; Fig. 2). Area A presented lower values, followed by area B, while area C had higher values (. 30), due to coastal water input (Kruskal-Wallis: P , 0.05) (Table 1). Dissolved oxygen was lower in rainy months (November and December) but also during winter months (June to August; Kruskal-Wallis: P , 0.05) (Fig. 2). The temperature, which varied from 22.5uC to 28.2uC, differed among months (Kruskal-Wallis: P , 0.001) but not among areas (P . 0.05) (Fig. 2). The mean (6 SD) depth in channel sub-areas was (4.84 6 0.97 m), significantly deeper than in shallow areas (2.37 6 0.8 m; P , 0.001), with no differences among months (P . 0.05) (Table 1; Fig. 2). Crab Population A total of 3876 C. danae was caught along the 12 months sampled, being 2537 females (1465 adults and 1072 juveniles), corresponding to 65.5% of the total, and 1339 males (444 adults and 895 juveniles), corresponding to 34.5% of the total (Fig. 3). Some 429 specimens (11.1%) had at least one of the lateral spines broken. Thus, 3447 intact crabs are included in the following analyses. The carapace width (CW) of the smallest and largest male was 24.9 and 128.0 mm respectively, compared to 23.1 and 118.6 mm for females (Fig. 4). The mean size of adult was higher (Student t 5 27.79; d.f. 5 104; P , 0.001) in males (103.2 6 9.9 mm) than in females (93.1 6 8.6 mm CW). CW of males at first sexual maturity was 91.3 mm and only 80.5 mm for females (Fig. 5). Juveniles of both sexes where equal in size (66.8 6 10.3 mm for females and 68.4 6 14.3 mm for males) (Student t 5 21.28; d.f. 5 87; P . 0.05). The mean size of male and female crabs, either juveniles or adults, did not show variations among areas or months (ANOVA: P . 0.05). Ovigerous females (N 5 318) corresponded to 21.7% of adult females, 12.5% of total females and 8.2% of the population sampled (Fig. 6). They ranged in size from 75 to 115 mm CW, with a mean of 94.4 6 6.5 mm, being 38% in the 95 mm size class.

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Month Area (A–B–C) Channel 3 Shallow Sub-Area Month 3 Sub-Area

channel: 4.80 6 0.63 shallow: 1.93 6 0.73 channel: 5.12 6 1.48 shallow: 2.38 6 0.77 channel: 4.59 6 0.49 shallow: 2.79 6 0.74

Salinity (mean 6 SD)

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were significantly more abundant at area A and B, at both the shallow and channel sub-areas (P , 0.001) (Fig. 8), with no differences among months (P . 0.05). Juvenile male crabs had a spatial and temporal distribution similar to that of juvenile female crabs, but showed density lower than that of females. Adult males had the lowest density, representing 30% of adult females (or 38.7% when excluding ovigerous individuals). Their distribution followed that of juvenile crabs, and they were concentrated in areas A and B, at both the shallow and channel sub-areas, and more abundant in December (Table 2 and Fig. 7). Overall, shallow subareas of A and C showed higher density of crabs, due to juveniles and egg-bearing females, respectively (Fig. 8). CPUEs of juvenile females, juvenile males, and adult males were negatively correlated with salinity (Spearman correlation: r 5 20.767, 20.694 and 20.650, respectively), reflecting their higher densities in areas A and B. No correlation was found with temperature and dissolved oxygen.

Fig. 2. Temperature (uC), salinity and dissolved oxygen (mg.L21) of bottom water and depth (m) at sampling stations (sub-areas) in northwest Vito´ria Bay, southeastern Brazil, during the year (N 5 72).

The sexual proportion, 1.89 female per male, was significantly skewed (x2 5 317.89; d.f. 5 11; P , 0.05). Females generally predominated over males (reaching 10.45 per male in January) except on March, April, June, September and November in which no significant difference (P . 0.05) was observed. The mean density of crabs (CPUE) was 1.66 1022 m2 (6 2.13 1022) with higher densities in November (H 5 27.14; d.f. 5 11; P , 0.05) (Table 2; Fig. 7) mainly due to juvenile recruitment and high number of ovigerous females. Female crabs had the highest density (0.71 1022 m2 6 1.31 1022). Ovigerous females were collected almost year-round, with non-significant (P . 0.05) peaks in CPUE in February, July, and October (Fig. 7). Unberried adult females predominated over egg-bearing ones, excepted in February, and were concentrated at area C during all months, and in shallow areas (P , 0.001). Juvenile females

Fig. 4. Number of crabs (axis Y) by carapace width (axis X, in cm) of Callinectes danae collected in northwest Vito´ria Bay, southeastern Brazil (N 5 3447).

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Fig. 3. Proportion of females and males of Callinectes danae through the year in northwest Vito´ria Bay, southeastern Brazil.

SFORZA ET AL.: POPULATION STRUCTURE OF CALLINECTES DANAE

DISCUSSION Salinity varied seasonally, in response to pluviometric precipitation, and spatially, due to river discharge. The main freshwater inputs enter the system as the discharge of the Santa Maria da Vito´ria River (Chagas et al., 2006) and this causes a salinity gradient to develop towards the south. Despite many pollution sources, mean dissolved oxygen of bottom water was below critical levels (2 mg.L21) in only 14% of the samples. Salinity was negatively correlated with crab CPUE and this reflects juvenile preference for estuarine grounds, as observed by other authors (Chacur and Negreiros-Fransozo, 2001; Severino-Rodrigues et al., 2009). The spatial distribution of C. danae in Vito´ria Bay varied among the three sampled areas. In particular, the sexual structure of the population strongly differed between brackish and more marine waters. Males, both juveniles and adults, and juvenile females were strongly concentrated in the areas of lowest salinity in the inner bay (A and B). Adult females, on the contrary, were more commonly found in the higher salinity zone of the bay (C), mainly in shallow areas. This partial sexual segregation is related to the reproductive cycle, and was observed in other estuarine or coastal regions (Pita et al., 1985; Branco and Thives, 1991; Branco and Masunari, 2000; Baptista-Metri et al., 2005; Severino-Rodrigues et al., 2009) and in other species of Callinectes, such as C. sapidus Rathbun, 1896 (Hines et al., 1987). Egg-bearing females were concentrated in the southern area of Vito´ria Bay, where salinity was consistently high (. 30). The congeneric species C. similis Williams, 1966 (Hsueh et al., 1993) and C. sapidus (Lipicus and Van Engel, 1990; Hsueh et al., 1993; Aguilar et al., 2005) migrate to waters of higher and constant salinities to extrude and carry their eggs. Female migration to high salinities water probably improves their reproductive success, because eggs and larvae will be subjected to less fluctuation of physical and chemical parameters and would experience reduced predation pressure (Hines et al., 1987). Our observations suggest that if, similar to C. similis and C. sapidus, females of C. danae migrate into deeper water, this descent should occur down-estuary from our sampling area, possibly into the harbor channel, Espı´rito Santo Bay, or even in near-shore coastal waters.

Fig. 6. Proportion of ovigerous and non-ovigerous females of Callinectes danae in northwest Vito´ria Bay, southeastern Brazil, through the year.

Juveniles and adult males were more abundant in internal estuarine areas (areas A and B) while adult females, including egg-bearing ones, were more abundant at area C. Thus, contrary to C. sapidus whose adult males occur in both the upper and lower estuary (Hines et al., 1987), in C. danae the partitioning of habitat occur only with adult females. It is probably advantageous for adult males to stay where immature females are concentrated because copulation only occurs when females undergo the pubertal molt (Jivoff and Hines, 1998). The preference of juvenile C. danae for low salinity areas has been reported for other estuarine regions in Brazil, such as Santos, Ubatuba, and Canane´ia-Iguape, state of Sa˜o Paulo, (Pita et al., 1985; Negreiros-Fransozo and Fransozo, 1995; Chacur and Negreiros-Fransozo, 2001; Severino-Rodrigues et al., 2009, respectively), in Santa Catarina (Branco and Thives, 1991; Branco and Masunari, 2000), and in Ruppia maritima meadows at Patos Lagoon, Rio Grande do Sul (Garcia et al., 1996). This spatial pattern of distribution is common in other congeneric species. For example, on the Eastern coast of United States (Tagatz, 1968) and the Gulf of Mexico (Hsueh et al., 1993; McClintock et al., 1993), C. sapidus also uses estuarine areas as nursery grounds. The preference for low salinity areas can be related to the osmoregulation ability in species of Callinectes (Hsueh et al., 1993) but may also be related to shelter and food availability in estuaries (Lipicus and Van Engel, 1990) and the high productivity that promotes high growth rates (Hines et al., 1987). Hines et al. (1987) proposed that, among others reasons, juvenile of some species of portunid crabs preferentially utilize brackish habitats as molting grounds, possibly due to osmotic advantage (because of the need to take up large quantities of water to expand the exoskeleton immediately after ecdysis) and also due to low predation rates in these habitats. Buchanan and Stoner (1988) stated that small crabs survive better where there are fewer predators and better protection in spite of more variable and potentially stressful environmental conditions. Our sampling gear (otter trawl) was not adapted to efficiently collect crabs smaller than 25 mm carapace width. Assuming that C. danae in Vito´ria Bay displays the same behavior as C. sapidus of juvenile development in low salinity areas (Posey et al., 2005), it is probable that the

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Fig. 5. Proportion of crabs sexually matured by 10 mm-classes of carapace width for male and female Callinectes danae in northwest Vito´ria Bay, southeastern Brazil.

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Table 2. Results of Kruskal-Wallis tests (N 5 71; a 5 0.05) and homogeneous groups determined through post-hoc Dunn tests (a 5 0.10) for the number (CPUE) of portunid crabs Callinectes danae from Vito´ria North-west bay, Brazil. d.f., degrees of freedom; F, value of the KW statistic; P, probability associated with the test. s 5 shallow area; c 5 channel area. Categories are listed from higher (on left) to lower (right) mean and homogeneous groups are indicated by the superscript letters. Kruskal-Wallis Factor

Month

d.f.

F

P

Total of portunid crabs 0.0044

27.135

Sub-Area

5

14.464

0.0129

Month Sub-Area

11 5

17.629 10.900

Adult Females 0.0906 0.0534

Month Sub-Area

11 5

25.8779 25.4823

Juvenile Females 0.0068 0.0001

Month Sub-Area

11 5

6.2250 21.3225

Ovigerous Females 0.8579 0.0007

Month Sub-Area

11 5

19.2385 25.4164

Adult Males 0.0569 0.0001

Month Sub-Area

11 5

17.6349 32.2869

Juvenile Males 0.0905 0.0000

Nova Octa Deca,b Jula,b Feba,b Auga,b Maya,b Apra,b Sepa,b Juna,b Janb Marb Asa Bsa Aca Csa,b Bca,b Ccb Not tested Not tested No significant differences detected at a 5 0.10 Asa Aca Bsa Bca Csb Ccc Not tested Csa Ccb Bsb Acb Asb Bcb Not tested Aca Asa Bsa Bca,b Csb Ccb Not tested Asa Aca,b Bsa,b Bcb,c,d Csc Ccd

Fig. 7. Mean density (CPUE, number per 102 m22) of Callinectes danae at Vito´ria north-west bay, southeastern Brazil, by month. Vertical bars show the standard deviation.

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11

Dunn test

SFORZA ET AL.: POPULATION STRUCTURE OF CALLINECTES DANAE

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upper portion of the Santa Maria da Vito´ria River functions as a nursery area for small individuals. This hypothesis, however, remains to be tested. Females reached sexual maturity (LC50) at about 80.5 mm CW and males at 91.3 mm while the smallest adult female and male were 64.7 mm and 68.3 mm CW, respectively. At Conceic¸a˜o Lagoon, Santa Catarina, the mean size at first maturation is larger, 84 mm for females and 94 mm for males, when crabs were 1.6 years old (Branco and Avila, 1992). However, at Babitonga Bay, less than 200 km north, sexual maturity was lower: 71 mm for females and 86 mm for males (Pereira et al., 2009). Size at first maturation in Santos, Sa˜o Paulo, was 76.2 mm for females and 92.3 mm for males (Pita et al., 1985, modified by Branco and Thives, 1991). However, Baptista-Metri et al. (2005) found mature crabs well below this size. The knowledge of size at first maturation is fundamental to the management of portunid crabs stocks (Branco et al., 2002), but differences in size at sexual maturity can be found both intraspecifically and latitudinally, due to environmental factors such as salinity, temperature, or luminosity (Baptista-Metri et al., 2005). Reproduction was continuous throughout the year probably due to low variations in water temperature. Even southern Brazilian populations of portunid crabs, including C. danae, exhibit this pattern (Branco and Masunari, 2000;

Baptista-Metri et al., 2005) in spite of the important seasonal variation (higher than 15uC) in these subtropical regions. This strongly contrasts with temperate regions where temperature could seasonally range from 0uC to 2829uC, with the reproductive season of C. sapidus restricted to late spring and summer months (Hsueh et al., 1993; Carver et al., 2005). Egg-carrying females were found almost year-round (except in November), with abundance peaks in February, July, and October. These findings are similar to other studies in southern Brazil, such as Costa and Negreiros-Fransozo (1998), Branco and Masunari (2000), Chacur and Negreiros-Fransozo (2001) and Baptista-Metri et al. (2005), although Negreiros-Fransozo and Fransozo (1995) did find berried females only in winter. Thus, C. danae reproduces continuously, as do most tropical brachyurans. However, the proportion of ovigerous females to total females at Vito´ria Bay was 21.7%, well below the 29%, 31%, 47.6% and 51% found, respectively, in Sa˜o Paulo by Costa and Negreiros-Fransozo (1998), Parana´ by Baptista-Metri et al. (2005), Santa Catarina by Branco and Masunari (2000) and south of Sa˜o Paulo by Severino-Rodrigues et al. (2009). Costa and NegreirosFransozo (1998) found egg-bearing females with developed ovaries in all months and suggested that females of this species are able to produce multiple spawns in the same season and intermoult period.

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Fig. 8. Mean density (CPUE, number per 1022 m2) of Callinectes danae at Vito´ria North-west bay, southeastern Brazil, by area. Vertical bars show the standard deviation.

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recursos-pesqueiros/download/429/), they are routinely caught any way. The fishery, done at night in shallow areas, is sizeselective, i.e., removes the bigger (male) crabs. Selective catches of bigger males C. sapidus in Chesapeake Bay, USA, induced a reduction in size and density of male crabs and an increase in the proportion of females with deleterious consequences onto the mean size of the population and its reproductive behavior (Carver et al., 2005). Selective removal is especially worrisome for C. danae because it is possible that mixing does not occur between populations from different estuaries. Weber and Levy (2000) found a high genetic heterogeneity in this species, due to low adult migration and also due to the requirement of estuaries as reproductive areas, and to larval and post-larval retention processes. This could result in future local population extinction. The complex reproductive cycle of C. danae should be further investigated, especially in mangrove and coastal areas, environments that were not sampled in this research. When compared with other populations, the relatively small size of C. danae in Vito´ria Bay, the low male density, the sex-ratio strongly biased towards female dominance, and the low frequency of ovigerous females are indications of over-fishing. The economic and social sustainability of this fishery has being affected by such unsustainable practices such as shrimp trawling and malefocused size-selective fishery. Fishery yields have dropped and portunid crabs have become more and more scarce in local markets (R. Sforza, personal observation). So, the two main fishing practices should be reviewed by management authorities. Also, more studies on the distribution and the reproductive biology of C. danae along all the estuarine system are required in order to provide information on the planktonic phase and the recruitment of juveniles.

ACKNOWLEDGEMENTS We thank the graduate students Bruno Bicalho Pereira, Hilton Gomes de Almeida, Raphael Mariano Macieira, Aguilar de Oliveira Sant’Anna, and Henrique Rosa Filgueiras for their participation in sampling, sorting, and laboratory processing, ‘Zinho’ Hernando Figueira Santo Ju´nior for his boat and his expertise, Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renova´veis (IBAMA) for the sampling authorization (02009.002102/00). J. C. Joyeux gratefully acknowledges financial support by the CNPq (301390 / 2007-0).

REFERENCES Aguilar, R., A. H. Hines, T. G. Wolcott, D. L. Wolcott, M. A. Kramer, and R. N. Lipicus. 2005. The timing and route of movement and migration of post-copulatory female blue crabs, Callinectes sapidus Rathbun, from upper Chesapeake Bay. Journal of Experimental Marine Biology and Ecology 319: 117-128. Baptista, C., M. A. A. Pinheiro, A. Blankensteyn, and C. A. Borzone. 2003. Estrutura populacional de Callinectes ornatus Ordway (Crustacea, Portunidae) no Balnea´rio Shangri-la´, Pontal do Parana´, Parana´, Brasil. Revista Brasileira de Zoologia 20: 661-666. ———, ———, ———, and ———. 2005. Biologia populacional e reprodutiva de Callinectes danae Smith (Crustacea, Portunidae) no Balnea´rio de Shangri-la´, Pontal do Parana´, Parana´, Brasil. Revista Brasileira de Zoologia 22: 446-453.

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The sex-ratio for Vito´ria Bay C. danae was strongly skewed towards female dominance over males (1.89:1), when considering the total number of crabs sampled. Meanwhile, in some months the sex ratio was more balanced (March, September and November) but completely independent from CPUE. Other authors also find females dominating over males: Keunecke et al. (2008) at Guanabara Bay and Severino-Rodrigues et al. (2009) in the lagoon-estuarine system of Iguape-Canane´ia (3.9:1 and 1.94:1, respectively). This contrasts with other regions where sex ratio is more equilibrated or even in favor of males such as Ubatuba, Sa˜o Paulo (female to male ratio 1.3:1; Costa and Negreiros-Fransozo, 1998), Santa Catarina (1:1.19; Branco and Masunari, 2000; 1:3.88; Pereira et al., 2009), Parana´ (1:0.9; Baptista-Metri et al., 2005) and Venezuela (0.8:1; Carmona-Sua´rez and Conde, 2002). Such differences are difficult to explain because each local has its own peculiarities, such as salinity and fishing pressure, but has also been sampled differently. (Mantelatto and Fransozo (1996) verified that males of C. ornatus exhibited greater activity during the daytime). However, it is probable that the presence of mangrove (with different levels of conservation) enables male crabs to take refuge, limiting their capture and, actually, the three sites with strong female dominance have extensive mangroves and, additionally high salinities (preferred by adult females). In other species of Callinectes, reported sex-ratio was always more balanced than that observed for C. danae at northwestern Vito´ria Bay (Hsueh et al., 1993; Mantelatto and Fransozo, 1999; Negreiros-Fransozo et al., 1999; Baptista et al., 2003). Carver et al. (2005) stated that a reduced density of males in a population may reduce the encounter rate, thus preventing females to find mates. They also observed that, due to the scarcity of males of C. sapidus in areas subjected to a high selective pressure for larger specimens (mainly males), smaller males reproduce but pass less sperm to females (than would larger ones). This could limit egg production because female body size is the primary determinant of fecundity in portunid crabs (Hines, 1982) and small males can not mate with the large females that produce a greater number of eggs (Branco and Avila, 1992). Species that have a limited window for mating are especially susceptible to sperm limitation (Hines et al., 2003). The spermatozoa from one mating can fertilize a number of batches of eggs (Hartnoll, 1985) and females can produce more than one clutch during a single reproductive season (Costa and Negreiros-Fransozo, 1998). In C. ornatus in aquaria, two periods of extrusion of egg masses have been observed without moulting or copulation (Mantelatto and Fransozo, 1999). Such consecutive egg extrusions would not be achieved under conditions of sperm limitation. Northwestern Vito´ria Bay has been subjected to intensive fishing pressure, mostly using illegal gear such as otter-trawl for shrimp. Portunid crabs, mainly immature individuals, are caught as by-catch (R. Sforza, personal observation), contributing to losses in food and biodiversity. Additionally, there also occurs an intense artisanal fishery for C. danae that uses hand-held baited gear, and in spite of Brazilian legal restrictions for captures of portunid crabs below 120 mm (www.ibama.gov.br/

SFORZA ET AL.: POPULATION STRUCTURE OF CALLINECTES DANAE

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RECEIVED: 26 September 2009. ACCEPTED: 17 March 2010.

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