POPULATION STRUCTURE, MORPHOMETRIC ANALYSIS AND REPRODUCTIVE BIOLOGY OF PORTUNUS SANGUINOLENTUS

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1 JOURNAL OF CRUSTACEAN BIOLOGY, 34(6), , 2014 POPULATION STRUCTURE, MORPHOMETRIC ANALYSIS AND REPRODUCTIVE BIOLOGY OF PORTUNUS SANGUINOLENTUS (HERBST, 1783) (DECAPODA: BRACHYURA: PORTUNIDAE) IN HONGHAI BAY, SOUTH CHINA SEA Chang-Ping Yang 1,2, Heng-Xiang Li 1,LuLi 1,JingXu 3,andYanYan 1, 1 Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Guangzhou , P.R. China 2 University of Chinese Academy of Sciences, 19A Yuquan Road, Beijing , P.R. China 3 Guangdong Huilai No. 2 Middle School, Jieyang , P.R. China ABSTRACT Portunus sanguinolentus (Herbst, 1783) is commercially important in China, but its yields have declined in recent years. Here, the morphometric characteristics and organ indices are analysed to obtain baseline information about the population structure, sexual maturity, and fecundity of this species. Specimens were collected monthly from the waters of Honghai Bay, off the South China Sea. A 1.26:1 male:female sex ratio was recorded. Male crabs reached sexual maturity at a carapace width (CW) of mm, while this CW range was mm for females. Fifty percent of males and females were mature at a CW of 76.4 and 82.2 mm, respectively. Spawning peaked in February (53.4%), while the smallest and largest berried female crabs were 77.1 mm CW and mm CW, respectively. A total of 58,600 to 565,000 eggs was attached to the pleopods of berried females, with female fecundity being significantly correlated to CW. The assimilated information is expected to help improve the sustainability of this crab fishery in China. KEY WORDS: morphometric analysis, population structure, Portunus sanguinolentus, reproductive biology, South China Sea DOI: / X INTRODUCTION The three-spotted (or blood-spotted) swimming crab, Portunus sanguinolentus (Herbst, 1783), is named after the three significant red to maroon spots located on the posterior part of the carapace (Carpenter and Niem, 1998). This species is widely distributed from the marine waters of East Africa, the Indio-Pacific region, to the Hawaiian Islands (Stephenson and Campbell, 1959). It typically inhabits sandy and muddy seabed of coastal waters of 10 to 30 m depth (Sumpton et al., 1989; Carpenter et al., 1997). However, berried female crabs often migrate to deeper waters to spawn. Females carry the eggs until the six stages of embryonic development are complete, and the zoeal (free-swimming) larvae hatch into the water. About days after hatching, the zoeae transform into megalopae, which occupy benthic habitats and grow into juvenile crabs (Samuel and Soundarapandian, 2009). In China, P. sanguinolentus are primarily caught as the by-catch of bottom set gill-netting and shrimp trawling. This fishery activity is mainly conducted in the South China Sea, off the provinces of Guangdong, Guangxi, and Hainan, with the Minnan-Taiwan Bank representing the northernmost limit of the distribution of this crab species. The East China Sea supports a commercial pot fishery along Minnan- Taiwan Bank, with an annual landed weight of about 6000 tons being recorded during The total landings of swimming crabs are not documented; hence, a stock assessment of commercial crabs has never been carried out in any of the Chinese waters (Ye, 1998). However, a large amount of basic information is available about the biology of P. sanguinolentus. For example, crab size at sexual maturity and fecundity represent two of the most important aspects of the reproductive biology of the swimming crab. This information may aid in inferring the main breeding season of crabs, which is important for good management of crab fisheries (Sukumaran and Neelakantan, 1997). The developmental stages of male and female gonads represent important reproductive criteria for swimming crabs, while the relative growth rate of the chelae and pleopods in relation to body size is an important criterion for males mature stage (Rasheed and Mustaquim, 2010). Many studies have been conducted on the taxonomy (Chhapgar, 1957; Stephenson and Campbell, 1959; Dai and Yang, 1991), maturation (Sumpton et al., 1989; Reeby et al., 1990), reproduction (Campbell and Fielder, 1986; Sukumaran and Neelakantan, 1997; Anonymous, 2000; Rasheed and Mustaquim, 2010) and embryonic development (Samuel and Soundarapandian, 2009) of P. sanguinolentus. However, information remains limited about P. sanguinolentus populations in Chinese waters (Huang, 1993, 2004; Ye, 1998; Hsu et al., 2000; Lee and Hsu, 2003; Yu and Song, 2006). Furthermore, the yields of this commercially important crab have declined in recent years (Soundarapandian et al., 2013). Corresponding author; The Crustacean Society, Published by Brill NV, Leiden DOI: / X

2 YANG ET AL.: BIOLOGY OF PORTUNUS SANGUINOLENTUS 723 In this paper, population structure, size at sexual maturity, allometric growth and reproductive characteristics are presented for P. sanguinolentus. In China, few studies have focused on estimating the size at which male and female P. sanguinolentus attain sexual maturity, despite this parameter representing a potentially important indicator for the utilization and management of marine biological resources. MATERIALS AND METHODS Sample Source and Measurement Between 25 November 2012 and 23 October 2013, a total of 1467 (819 male and 648 female) P. sanguinolentus was collected by monthly shrimp trawls in a constant inner-to-outer route of Honghai Bay, China (Fig. 1). The water depth is m, with a muddy or sandy substrate. Basic hydrographic data of these waters were obtained from the China Marine Environment Bulletin in The annual average temperature was ± 1.55 C and the average salinity was ± The distribution of dissolved oxygen, salinity, PH, and nutrition salt varies both seasonally and spatially in Honghai Bay. High dissolved oxygen and ph levels in the sea water rise are caused by photosynthesis and increasing temperature from north to south (Wang and Jia, 1999). The morphology of the pleon was examined to determine the sex of the crab specimens and the number of berried crabs was recorded to infer the spawning season (Rasheed and Mustaquim, 2010). Body wet weight (WW) was determined to the nearest 0.01 g with an electronic balance, while the measurement of carapace width (CW) was made between the tips of the ninth anterolateral teeth to the nearest 0.01 mm with a millimetre scale (Shields, 1992). Chelar propodus length (CPL) and pleon growth (AW) was measured from the tip of the fixed finger to the base and the greatest width of the fifth pleomere, respectively. For allometric analysis, the lengths of the first and second pleopods (FPL and SPL) of male crabs were both taken from the tip to the base. Gonadal Maturity and Fecundity The carapaces of all male and female specimens were removed using dissecting scissors to examine the gonadal condition macroscopically (by the naked eye) and differentiate mature and immature crabs. Mature males were delineated as specimens where the body cavity contained enlarged testes and swollen vas deferentia, while those females with dark yellow ovaries that occupied almost the entire hepatopancreas spaces were considered to be mature ones. Spent females can be distinguished easily by their small, translucent and greatly reduced ovaries (Soundarapandian et al., 2013). Pleopods bearing eggs were removed carefully from the body and dried by blotter paper, and then the whole mass (eggs plus pleopods) was measured to the nearest 0.01 g. Five samples of berried eggs (0.1 g) were transferred from different areas of each egg mass to a culture dish. Average number of eggs present in the samples was then calculated. In order to find out the weight of egg mass only, eggs were removed from the pleopods and the weight of the pleopods was recorded then. This was subtracted from the weight of whole egg mass to obtain the weight of eggs only. Fecundity was then calculated by the formula: N = W n/w, wherew = total weight of the egg mass only, w = average weight of the five egg samples, n = average number of eggs in the samples, N (Fecundity) = total number of eggs (Soundarapandian et al., 2013). Statistical Analyses SPSS, Microsoft Excel and Curve Expert statistical software were used for the statistical analysis. For the CW-WW and fecundity-cw relationships, the logarithmic form of the exponential equation (y = a x b ) was used by the least squares method, where y = WW or fecundity and x = CW. The value exponent b for immature and mature male crabs was compared with the predicted isometric growth constant 3 by the Student s t-test. For the relative growth rate of the chela, pleon, and pleopod, regression equations were calculated assuming an allometric growth equation: y = a + bx, where x = CW and y = organ length. The allometric coefficient was the slope of the linear equation. To determine the constant of allometry of b, all data were transformed to logarithms and log-log regression was performed following the linearized equation (Muiño et al., 1999): log y = log a + b log x. The relative growth of organs in relation to body size was estimated by the value of b.whenb is larger than 1, allometry is positive and the organ grows faster than the whole body. In contrast, allometry is negative when the organ grows slower than the body. When the value of b is equal to 1, the organ grows at the same rate as the body. Student s t-test was used to calculate the significance of the observed values (Rasheed and Mustaquim, 2010). The CW of our specimens were divided into groups by 5 mm bins starting at 42.5 mm and ending at mm. They were compared by the Student s t-test for males and females, and adults and juveniles. We compared the proportion of reproductively active males and females by Fig. 1. Map showing the sampling area of the present study (Honghai Bay).

3 724 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014 χ 2 -analysis (Sforza et al., 2010). The size of 50% mature specimens of the different size groups was estimated by evaluating the logistic curve (Rasheed and Mustaquim, 2010). RESULTS Population Structure In total, 819 males (623 adults and 196 juveniles) and 648 females (459 adults and 189 juveniles) were collected, representing 55.8% and 44.2% of all specimens, respectively. More males than females were collected in all months, except February and June (Fig. 2). The overall male: female sex ratio was 1.26:1, which significantly differed to the expected 1:1 ratio (χ 2 = , df = 11, P<0.01). Threehundred and sixty-six specimens (24.9%) had at least one broken lateral spine; thus, 1101 crabs were used in the subsequent analyses. The CW of the smallest and largest male crabs was 49.5 and mm, respectively, while that of females was 44.3 and mm, respectively. Twenty-one CW classes were delineated, ranging from 42.5 to mm (Fig. 3). The mean size of adult males (97.52 ± 9.32 mm CW) was significantly smaller (t = 12.51; df = 796; P < 0.01) compared to that of females ( ± mm CW). There was no size difference in the juveniles of both sexes (t = 1.31; df = 253; P = 0.195; males: ± 7.86 mm; females: ± mm). Relationship Between Carapace Width and Wet Weight Crabs (550 males with mm CW, 551 females with mm CW) were measured and weighed. The scatter diagram of CW-WW relationship indicates that there is a positive and highly significant relationship between CW and total WW (Fig. 4A, 4B). The exponential values b in all males and females (3.054 and ) markedly deviated from the isometric growth pattern. The Student s t- test indicated that b significantly differs from 3 (t = and for males and females, respectively; α = 0.05, P < 0.01) in both sexes, and was significantly different between males and females (t = 7.355, α = 0.05). The value of the regression coefficient b for immature and mature male crabs was and , respectively, both of which were significantly different from 3 (t = and , respectively; α = 0.05, P < 0.01). The b value for immature and mature females ( and , respectively) indicated that the significant deviation from isometric growth is only in evident in mature females (t = and , respectively; α = 0.05, P < 0.01). A sudden change was observed between immature and mature male crabs in the mm CW size range (t = , α = 0.05), and female crabs in the mm CW size range (t = , α = 0.05) (Table 1). Chela Allometry The relative growth of the chela was measured in a total of 550 and 530 males and females, respectively. The CPL of both sexes exhibited positive allometry. The b values of immature and mature male crabs were and , respectively, both of which significantly differed from 1 (t = and for immature and mature males, respectively; α = 0.05, P < 0.01). The b values between immature and mature males significantly differed (t = , α = 0.05, P < 0.01), indicating a sudden change between these two periods (Fig. 5A; Table 2). Thus, male P. sanguinolentus may undergo pubertal moult at in a CW range of mm. Females CW ranged from 49.3 mm to mm. The regression coefficient b was , and was significantly different from 1 (t = 5.922, α = 0.05, P < 0.01). Therefore, a positive growth rate is present in females, with no sudden increase in chela length in female crabs (Fig. 5B; Table 2). Pleopod Allometry A total of 400 males (135 and 235 immature and mature individuals) with mm CW were measured to determine the relative growth of the first and second pleopods. The b values for the growth of the first pleopods were and for immature and mature males, respectively. Thus, FPL exhibited positive allometry in immature crabs and became negative in mature crabs. Both periods were significantly different from 1 (t = and for immature and mature males; α = 0.05, P<0.01), showing that the growth of the first pleopod is not isometric with CW. The Student s t-test revealed a significantly different regression coefficient b for immature and mature males (t = , α = 0.05, P<0.01) (Fig. 6A; Table 2). In contrast, no sudden change in growth rate was observed for the SPL between immature and mature males. The b value was , which was significantly less than 1 (t = 9.334, α = 0.05, P<0.01) (Fig. 6B; Table 2). Percentage of males and females in monthly collected P. sanguino- Fig. 2. lentus. Pleon Allometry A sudden change in pleon width was documented between 76 mm and 92 mm CW. The regression coefficient b value was and for immature and mature females, respectively, both of which were significantly different from 1(t = and for immature and mature females, respectively; α = 0.05, P<0.01). Pleon width had slightly positive allometry during immature period (CW < 77 mm), becoming more positive during the mature period (CW > 92 mm). The significant difference (t = , α = 0.05, P < 0.01) between these two b values indicates that the

4 YANG ET AL.: BIOLOGY OF PORTUNUS SANGUINOLENTUS 725 Fig. 3. Proportions of sexually matured crabs, estimated by evaluating by the logistic curve with the model: y = a/(1+b exp( cx)). A,males;B, females. Parameter Correlated data for male Correlated data for female a b 10,377, ,899, c SE Correlation coefficient puberty moult occurs between 76 mm and 92 mm CW in females (Fig. 7; Table 2). Condition of the Gonads A total of 550 male crabs ( mm) and 551 female crabs ( mm) were dissected to assess the condition of the gonads. The CW of the smallest mature and largest immature male was 68.8 and 88.8 mm, respectively, compared to 68 and 93.1 mm for females. The percentage of mature males and females in the different sizes group shows that the first five classes only contained immature individuals of both sexes. Only mature males were present when CW > 92.5 mm, whereas only mature females were present when CW > 97.5 mm. The middle size groups were composed of immature and mature crabs of both sexes. Size at 50% maturity was 76.4 mm CW for males and 82.2 mm CW for females (Fig. 3). Spawning Season and Fecundity Berried females were captured in all months expect September, with numbers peaking in February. One-hundred out of 611 captured females were berried, representing 16.4% out of all crabs (Fig. 8). Out of the 100 berried females, 79 were used in the fecundity analysis. The smallest and largest berried females were 77.1 mm CW and mm CW, respectively, corresponding to the minimum fecundity (58,600) and the maximum fecundity (565,000). The mean fecundity of berried female crabs was 231,922, with a standard error of 12,447. There was a typical power function relationship between female fe- Fig. 4. Relationships between wet weight and carapace width in immature and mature P. sanguinolentus. A, male; B, female.

5 726 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014 Table 1. Analysis of allometric and log-transformed equations of carapace-wet weight relationship in males and females of P. sanguinolentus. a Coefficient of determination; b regression coefficient; c standard error of b; d Student s t-test for comparison the b-value and 1; e allometric level: (+) positive and ( ) negative; f Student s t-test when compare two value of b; indicates positive allometry, significant at the 5% level. y-variable Sex and maturity Carapace width (CW, mm) Allometric equation N R 2a b b SE b c t(b = 3) d AL e t(b = b) f Wet weight (WW) Immature male WW = CW log WW = log CW Mature male WW = CW log WW = log CW Immature female WW = CW log WW = log CW Mature female WW = CW log WW = log CW Total male WW = CW log WW = log CW Total female WW = CW log WW = log CW Table 2. Analysis of linear and log-transformed regression equations of relationship between organ and carapace width in P. sanguinolentus. a Coefficient of determination; b regression coefficient; c standard error of b; d Student s t-test for comparison the b-value and 1; e allometric level: (+) positive and ( ) negative; f Student s t-test when compare two value of b; indicates positive allometry, significant at the 5% level. y-variable Sex and maturity Carapace width (CW, mm) Allometric equation N R 2a b b SE b c t(b = 1) d AL e t(b = b) f Chelar propodus length (CPL) Immature male CPL = CW log CPL = log CW Mature male CPL = CW log CPL = log CW Total female CPL = 0.527CW log CPL = log CW First pleopod length (FPL) Immature male FPL = CW log FPL = log CW Mature male FPL = CW log FPL = log CW Second pleopod length (SPL) Total male SPL = CW log SPL = log CW Abdomen width (AW) Immature female AW = CW log AW = log CW Mature female AW = 0.379CW log AW = log CW

6 YANG ET AL.: BIOLOGY OF PORTUNUS SANGUINOLENTUS 727 Fig. 5. Relationship between chelar propodus length and carapace width in immature and mature P. sanguinolentus. A, males; B, females. cundity and CW, with the estimated equation: Fecundity = CW (R 2 = ) (Fig. 9). DISCUSSION The sexual population structure of P. sanguinolentus in Honghai Bay varies across the months of the year, with the overall male:female ratio being 1.26:1, which differs to the expected 1:1 ratio. The results of this study support those recorded for P. sanguinolentus by Sumpton (1989) in Australia (Queensland) and Wenner (1972) in the USA (Hawaii), but differs to those recorded by Pillai (Pillai and Thirumilu, 2012) in southern India (Chennai) and those for Carcinus aestuarii (Nardo, 1847) in Turkey (Tahir et al., 2009). Wenner (1972) suggested that differences in the mortality, sex-specific habit segregation and single-sex migration might explain the skewed sex-ratio, which is recorded in many marine crustaceans. In fact, females prefer higher salinity than males and they often inhabit in deeper waters (Campbell and Fielder, 1986), and this can explain the higher ratio of male crabs in present study. Furthermore, as the temperature increases in February (Wang and Jia, 1999), berried female crabs migrated to inshore waters to seek food or a sandy substrate for successfully extruding their eggs and attaching them on the pleopods, and this behaviour led to a higher ratio of females in this month. Knowledge about the morphometric changes and size at maturity of sexually mature individuals is of particular importance in the study of commercially valuable crustaceans. Portunidae are distinguished by an enlarged and flattened dactylus on the fifth pereiopod, which facilitates swimming (Jose, 2011). In population studies, morphometric analysis provides a powerful complement to genetic and environmental stock identification approaches (Cadrin, 2000), with width-weight relationships allowing the conversion of growth-in-width equations to growth-in-weight for use in stock assessment models (Moutopoulos and Stergiou, 2002). Length/width-weight relationships are regarded as more suitable for evaluating crustacean populations (Olmi and Bishop, 1983; Suhalya and Rashan, 1986). In the cur- Fig. 6. A, first pleopod length/carapace width relationship in immature and mature males; B, second pleopod length/carapace width relationship in males.

7 728 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014 Fig. 7. Relationship between pleon width and carapace width in immature and mature female P. sanguinolentus. rent study, the width-weight relationship analysis of P. sanguinolentus indicated that weight gain is not uniform between juveniles and adults in either sex. Furthermore, the growth rate of all males combined was slightly higher than that of females, supporting the observations for P. pelagicus (Linnaeus, 1758) and P. sanguinolentus in India (Cochin) (Thomas, 1984), for P. sanguinolentus in India (Mangalore) (Sukumaran et al., 1986), and for C. aestuarii in Turkey (Homa Lagoon) (Tahir et al., 2009). Sukumaran (1997) suggested that the differences in the exponential values in juveniles, adult males, and adult females is due to different diets, which influence the body size, cheliped strength, foraging behaviour, and metabolic rate of the animal. In addition, the relatively larger size of male chela probably causes the difference in the CW-WW relationship of the two sexes (Sumpton et al., 1989). The relative size of the chela and pleon represent important indicators of sexual maturity in most brachyurans. Because there are some changes in allometry between immature and mature individuals, the size at sexual maturity of males and females can be inferred from the relative growth rates (Hartnoll, 1974). For male crabs, the relative growth Fig. 8. month. Percentage of egg-bearing female P. sanguinolentus in different Fig. 9. Size-fecundity relationship of female P. sanguinolentus. rate of the chela and first pleopod are considered to be important secondary sexual characteristics. The chela is often used for territorial defence, combat, mating, and courtship. The first pleopod latter serves as the organ for intercourse, being inserted into the genital aperture of the female during copulation (Rasheed and Mustaquim, 2010). In this study, the relative growth of chela between immature and mature males was observed with a sudden change, which supported those findings of Sukumaran and Neelakantan (1996) and Rasheed and Mustaquim (2010). During copulation, the male crab extends the pleon and inserts the first copulatory pleopod into the genital apertures of the female, with the second pleopod plunging back and forth to transfer the spermatophores from the cirrus to the spermathecae of female (Fielder and Eales, 1972). The sudden change in the growth rate of the first pleopod of males occurs at nearly at the same CW size as chela growth. Thus, the development of physiological and functional maturity in male P. sanguinolentus is synchronised. This result supports those of Reeby et al. (1990) for male P. pelagicus and P. sanguinolentus in India (Karawar), and Rasheed and Mustaquim (2010) for P. sanguinolentus in Pakistan (Karachi). However, the relative growth rate of SPL was similar for both immature and mature males in this study, indicating that this parameter is not suitable for estimating the size at sexual maturity for male P. sanguinolentus. CPL is a secondary sexual characteristic indicator in male crabs, with pleon width having the same function in females. This study showed that male and female crabs reach full sexual maturity (functional and physiological) at and mm CW, respectively. The size at which sexual maturity is reached by brachyuran crabs varies with location, which may be due to abiotic factors, acting locally and seasonally (Wenner et al., 1974). Sumpton et al. (1989) reported that male and female P. sanguinolentus reached physiological maturity at 83 and 74 mm, respectively in Australia (Queensland). Thus, females mature earlier than males, which is contrary to the results of the present investigation. Fisher (1999) found that the size of female Callinectes sapidus (Rathbun, 1896) at sexual maturity varied in nine Texas bay systems with temperature and salinity conditions. Hines (1989) observed that four out of

8 YANG ET AL.: BIOLOGY OF PORTUNUS SANGUINOLENTUS 729 five species of brachyuran crabs exhibited differences in the size at sexual maturity along the east and west coast of North America and suggested that the differences may be attributed to variation in moult increment and the number of moults. Rasheed and Mustaquim (2010) reported that male and female P. sanguinolentus in Karachi, Pakistan were fully mature at and mm, respectively. These ranges are similar to those recorded in the present study. Furthermore, 50% of male P. sanguinolentus matured at a smaller size compared to females (60.8 mm SCW versus 63.5 mm SCW; SCW is the distance between the bases of the ninth anterolateral teeth), again reflecting the results of the current study (76.4 mm CW versus 82.2 mm CW). In this study, egg bearing females were recorded throughout the year, indicating that this species exhibits continuous spawning, rather than discontinuous spawning, with the peak number of berried females occurring from January to March. Similarly, Sukumaran and Neelakantan (1999) recorded peak spawning activity from the Karnataka coast during December-February, based on the high incidence of mature and spent crabs along with maximum GSI (gonadosomatic index) values. In contrast, Rasheed and Mustaquim (2010) reported the highest percentage of berried females in Karachi waters at different times of the year (September and May in 2004 and July in 2005). According to Pillai and Nair (1971), peaks of higher spawning intensity may be associated with variation in temperature, salinity, food availability, rainfall and photoperiod. Brachyuran crabs inhibiting tropical waters tend to spawn year-round because environmental conditions remain favourable for gonad development (Emmerson, 1994), whereas those inhabiting temperate waters only spawn in certain months (Sarada, 1998). In general, both continuous and seasonal reproductive patterns are found in subtropical and tropical regions (Warner, 1977). The continuous spawning activity recorded in the present work was in accordance with the climatic features of the study area (Honghai Bay), which is located in the subtropical region of the South China Sea. The fecundity of decapod crustaceans tends to be positively correlated with the body size and the weight of females (Erdman and Blake, 1988). There is latitudinal variation in the fecundity of similar species (Sastry, 1983). For instance, Sukumaran et al. (1986) found that the fecundity of P. sanguinolentus ranged from 300,000 to 700,000 (CW of 83 to 113 mm) in one area of India (South Kanara). In comparison, Reeby et al. (1990) recorded 158,608 to 712,526 (CW of 79 to 126 mm) eggs in another area of India (Karawar), while Rasheed and Mustaquim (2010) recorded 272,000 to 1,395,000 (CW of 63 to 120 mm) eggs in Pakistan (Karachi). The results of our study are similar to the former two studies but lower than the third, with egg numbers ranging from 58,600 to 565,000 (for females with a CW of 77.1 mm and mm, respectively). However, Sastry (1983) considered food availability as the most important factor influencing fecundity, because feeding is essential for yolk formation. Other environmental factors may also contribute, including habitat structure, predation, parasite load, and temperature. These parameters may influence the balance between the optimal number and size of eggs, or may cause the loss of eggs during the incubation period. In addition, handling may reduce egg numbers, as the crabs used in these studies were obtained from commercial landings (Soundarapandian et al., 2013). To date, information about the fishery for P. sanguinolentus in the marine waters of China has remained limited (Huang, 1993, 2004; Ye, 1998; Hsu et al., 2000; Lee and Hsu, 2003; Yu and Song, 2006). Therefore, the lack of relevant knowledge has made it difficult to manage this commercial species appropriately. The basic 3-S restrictions (Size, Sex and Season) proposed by Helliwell (2009) to manage the commercial crab fishery has been successfully implemented by many countries to sustain their crab resources in recent years. This study is the first to report the population structure, sexual maturity, spawning season, allometric growth and fecundity of P. sanguinolentus in the coastal waters of China. Based on the results, it is recommended that February should be added to the fishing moratorium, with the fishing of immature P. sanguinolentus smaller than 86 mm CW being prohibited, in the waters of Honghai Bay in the South China Sea. ACKNOWLEDGEMENTS This study was supported by the National Natural Science Foundation of China (Nos , ) and the Natural Science Foundation of Guangdong Province, China (No. s ), which are gratefully acknowledged. REFERENCES Anonymous Fisheries Administration. Year-Books of Council of Agriculture, Taipei. Cadrin, S. X Advances in morphometric identification of fishery stocks. Reviews in Fish Biology and Fisheries 10: Campbell, G. R., and D. R. Fielder Size at sexual maturity band occurrence of ovigerous females in three species of commercially exploited portunid crabs in S.E. Queensland. Proceedings of the Royal Society of Queesland 97: Carpenter, K. E., F. Krupp, D. A. Jones, and U. Zajonz FAO species identification field guide for fishery purposes. 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Eales Observations on courtship, mating and sexual maturity in Portunus pelagicus (L., 1766) (Crustacea, Portunidae). Journal of Natural History 6: Fisher, M. R Effect of temperature and salinity on size at maturity of female blue crabs. Transactions of the American Fisheries Society 128: Hartnoll, R. G Variation in growth pattern between some secondary sexual characters in crabs (Decapoda, Brachyura). Crustaceana 27: Helliwell, V Fisheries management for California Dungeness crab adapting to change. Coastal Management 37: Herbst, J. F. W Kritisches Verzeichniß meiner Insektensammlung. Archiv der Insectengeschichte, Zürich 4: 1-72.

9 730 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014 Hines, A. H Geographic variation in size at maturity in brachyuran crabs. Bulletin of Marine Science 45: Hsu, C. C., H. C. Chang, and H. C. Liu Sex-variant morphometrics of the swimming crab, Portunus sanguinolentus (Herbst), from the waters off Northern Taiwan. Journal of the Fisheries Society of Taiwan 27: Huang, M. Z Study on feeding habit and nutrient level of Portunus argentatus, P. sanguinolentus and Charybdis feriatu in Fujian sea area. Journal of Oceanography In Taiwan Strait 23: Huang, R. F Studies on the taxonomy and distribution of the portunid crabs (Crustacea: Decapoda: Brachyura) in Taiwan. Doctoral Dissertation of National Taiwan Ocean University, 235 pp. [In Chinese]. Jose, J Morphometrics and length-weight relationship in the blue swimmer crab, Portunus pelagicus (Linnaeus, 1758) (Decapoda, Brachyura) from the Mandapam Coast, India. Crustaceana 84: Lee, H. H., and C. C. Hsu Population biology of the swimming crab Portunus sanguinolentus in the waters off northern Taiwan. Journal of Crustacean Biology 23: Linnaeus, C Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Edition 10, 1: i-iii, Moutopoulos, D. K., and K. I. Stergiou Length-weight and lengthlength relationships of fish species from the Aegean Sea (Greece). Journal of Applied Ichthyology 18: Muiño, R. L., L. Fernández, E. González-Gurriarán, J. Freire, and J. A. Vilar Size at maturity of Liocarcinus depurator (Brachyura: Portunidae): a reproductive and morphometric study. Journal of the Marine Biological Association of the United Kingdom 79: Nardo, D Sinonimia moderna delle specie registrate nell opera intitolata: Descrizione de Crostacei, de Testacei e de Pesci che abitano le Lagune e Golfo Veneto, rappresentati in figure, a chiaroscuro ed a colori dall Abate Stefano Chiereghini Ven. Clodiense applicata per commissione governativa; Venezia pp. i-xi, Olmi, E. J., and J. M. Bishop Total width-length relationships of the blue crab Callinectes sapidus Rathbun from the Ashely River, South Carolina. Journal of Shellfish Research 3: 99. Pillai, S. L., and P. Thirumilu Fishery, biology and yield estimates of Portunus sanguinolentus off Chennai. Journal of Marine Biology Assessment 54: Pillay, K. K., and N. B. Nair The annual reproductive cycles of Uca annulipes, Portunus pelagicus and Metapenaeus affinis (Decapoda: Crustacea) from the south-west coast of India. Marine Biology 11: Rasheed, S., and J. Mustaquim Size at sexual maturity, breeding season and fecundity of three-spot swimming crab Portunus sanguinolentus (Herbst, 1783) (Decapoda, Brachyura, Portunidae) occurring in the coastal waters of Karachi, Pakistan. Fisheries Research 103: Rathbun, M. J The genus Callinectes. Proceedings of the United States National Museum 18: , pls Reeby, J., P. N. Prasad, and N. 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Indian Journal of Fisheries 43: ,and Age and growth in two marine portunid crabs, Portunus (Portunus) sanguinolentus (Herbst) and Portunus (Portunus) pelagicus (Linnaeus) along the southwest coast of India. Indian Journal of Fisheries 44: , and Spawning biology of two marine portunid crabs, Portunus (Portunus) sanguinolentus (Herbst) and Portunus (Portunus) pelagicus (Linnaeus) from the Karnataka coast. The Fourth Indian Fisheries Forum Proceedings 26: , K. Y. Telang, and D. Thippeswamy On the fishery and biology of the crab Portunus sanguinolentus (Herbst) along the south Kanara coast. Indian Journal of Fisheries 33: Sumpton, W. D., G. S. Smith, and M. A. Potter Notes on the biology of the portunid crab, Portunus sanguinolentus (Herbst), in subtropical queensland waters. Marine and Freshwater Research 40: Tahir, Ö., B. Kerem, and K. Tuncer Length/width-weight relationships of the Mediterranean green crab Carcinus aestuarii Nardo, 1847 in the Homa Lagoon, Aegean sea, Turkey. Journal of Fisheries Sciences 3: 1-4. Thomas, M Studies on portunid crabs (Crustacea: Decapoda: Brachyura). Ph.D. Thesis, Department of Marine Sciences, University of Cochin, Cochin, 155 pp. Wang, X. P., and X. P. Jia The distribution of feature and relationship between the dissolved oxygen, salinity, ph and nutrition salts in the waters of Honghai Bay. Marine Science Bulletin 18: [In Chinese]. Warner, G. F The Biology of Crabs. Paul Elek, London. Wenner, A. M Sex ratio as a function of size in marine Crustacea. American Naturalist 106: , C. Fusaro, and A. Oaten Size at onset of sexual maturity and growth rate in crustacean populations. Canadian Journal of Zoology 52: Ye, S. Z Fisheries biology of red spot swimming crab, Portunus sanguinolentus, on the Minnan-Taiwan bank fishing ground. Marine Fisheries 20: [In Chinese]. Yu, C. G., and H. T. Song Composition and distribution of economic crab species in the East China Sea. Oceanologia et Limnologia Sinica 37: RECEIVED: 10 May ACCEPTED: 26 July AVAILABLE ONLINE: 9 September 2014.

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