Fish Sci (2011) 77:915–927 DOI 10.1007/s12562-011-0408-x

ORIGINAL ARTICLE

Fisheries

Fishery biology of mud crabs Scylla spp. at Iriomote Island, Japan: species composition, catch, growth and size at sexual maturity Cynthia Yuri Ogawa • Katsuyuki Hamasaki Shigeki Dan • Shuichi Kitada

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Received: 10 June 2011 / Accepted: 30 August 2011 / Published online: 25 September 2011 Ó The Japanese Society of Fisheries Science 2011

Abstract The fishery biology of mud crabs Scylla spp. was examined using baited traps and gill nets from September 2001 to August 2005 at Iriomote Island, Japan. To elucidate the growth of the crabs, artificially produced S. serrata juveniles were released and recaptured at the study site. The sizes at which 50% of females and males of S. serrata reached sexual maturity (SM50) were estimated as an external carapace width (ECW) based on the morphology of the abdomen and the chela respectively. Two species, S. serrata and S. olivacea, were identified in the area with S. serrata being the dominant species ([95% of the catch). Changes in the mean ECW and the results of the release and recapture experiments suggested that the recruitment of young crabs to the fishery occurred from December/January to April/May. The SM50 of females and males occurred at 132.4 and 150.7 mm ECW respectively. The body size composition of S. serrata revealed that immature crabs comprised approximately 40 and 65% of the catch for females and males respectively. To maintain a sustainable fishery for S. serrata, a minimum landing size based on the SM50 estimates should be implemented as a fishing regulation.

Electronic supplementary material The online version of this article (doi:10.1007/s12562-011-0408-x) contains supplementary material, which is available to authorized users. C. Y. Ogawa  K. Hamasaki (&)  S. Kitada Department of Marine Biosciences, Tokyo University of Marine Science and Technology, Minato, Tokyo 108-8477, Japan e-mail: [email protected] S. Dan Tamano Laboratory, National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Tamano, Okayama 706-0002, Japan

Keywords Baited traps  Chela allometry  CPUE  Generalised additive model  Gill net  Minimum landing size  Juvenile release

Introduction Mud crabs of the genus Scylla de Hann are large portunids that live in estuaries and coastal waters throughout the tropical to warm temperate zone in the Pacific and Indian Oceans [1–3]. Mud crabs are acknowledged for their commercial importance as food, and overfishing of mud crab species has been observed at varying levels in different countries in accordance with the development of both national and international markets [4]. Mud crab overfishing has resulted in the decreased size and abundance of mud crabs in many fisheries, making them an increasingly scarce resource throughout the Indo-Pacific region [4–16]. Fishing regulations, such as prohibiting the capture of immature crabs, should be indispensable for sustainable utilisation of mud crab resources [5, 8, 14]. Traditionally, mud crabs were grouped into one species, Scylla serrata [17]. However, the species identification of the genus Scylla has been controversial [18, 19], and the researchers have reported that mud crabs include several species/morphs in many places including the Philippines [20], Vietnam [21], Malaysia [22], India [23] and Japan [3, 18, 24]. Recently, taxonomy of the genus Scylla has been resolved as four distinct species, i.e., S. serrata (Forska˚l), S. tranquebarica (Fabricius), S. olivacea (Herbst) and S. paramamosain Estampador by Keenan et al. [2] based on both morphometric and genetic characteristics. Since then, biological and ecological studies in relation to fisheries have focused on individual mud crab species in several countries and regions [3–16], including Japanese waters

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[3, 18, 19, 24–26]. In Japan, S. serrata, S. paramamosain and S. olivacea inhabit coastal inlets and support commercially important fisheries on a local scale in warm temperate zones, including Lake Hamana in Shizuoka Prefecture and Urado Bay in Kochi Prefecture, where several studies have been conducted to reveal the species composition of the catch and growth of mud crabs [25, 26]. Furthermore, mud crabs are commercially fished in subtropical waters in Ryukyu Archipelago, which is located in southern Japan [24]. However, little is known about the fishery biology, such as the species composition of the catch, catch per unit effort (CPUE) and growth, of mud crab species in Japanese subtropical waters. Therefore, we studied the fishery biology of mud crabs in Ryukyu Archipelago and selected Iriomote Island as the study area. Iriomote Island is located at the southernmost end of the Ryukyu Archipelago (24°200 N and 123°490 E) (Fig. 1). The island has several river estuaries with mangrove forests where mud crabs are abundant. We characterised the fishery of mud crabs for fishing gear used as well as the species composition, CPUE, sex ratio and body size (carapace width) of the mud crabs caught in the area. To elucidate the growth of mud crabs before and at recruitment to the fishery, release and recapture experiments using artificially produced juveniles of the dominant mud crab species S. serrata were conducted. Juveniles were released into an open natural tidal flat and in a net enclosure set on a natural tidal flat in Iriomote Island. The mud crabs were then recaptured and measured. Furthermore, the size of S. serrata at sexual maturity was examined as the basis for setting a minimum landing size as a fishing regulation for this species in Iriomote Island.

Materials and methods Collection of fishery data In Iriomote Island, mud crabs were caught using baited traps and gill nets. Commercial rectangular traps (45 cm wide 9 60 cm long 9 20 cm high) with two slit entrances were used throughout the year during the period of this study. The galvanised rod frame of the trap was covered with a black polyethylene square-shaped mesh net with a stretched mesh diameter of 2 cm. Bait consisted of pieces of fish resulting from the by-catch and skip jack. The gill nets were made of monofilament nylon (dimension of one unit being 1.8 m wide 9 25 m long) with a stretched mesh size of 6 cm. Local legislation restricted the use of gill nets from October to May. Each trap was connected to a polyethylene rope, marked with a buoy, and individually deployed alongside the river margin near the mangrove forest, and gill nets were placed at the mouth of the river.

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An overnight soaking time was utilised for both types of fishing gear. The most active crab fisherman, who employed both fishing gears to catch mud crabs in the northwestern fishing grounds, including the Nakara and Kuira Rivers and their adjacent waters as well as the Amitori and Sakiyama Bays in Iriomote Island (Fig. 1), was selected to collect the fishery data. Fishing activity was monitored for four successive years from September 2001 to August 2005. A fisherman was trained to record the following data on a daily basis: the type of fishing gear and the number of fishing gear units as well as the species, sex and external carapace width (ECW) including the anterolateral spines to the nearest 0.5 cm of each individual captured mud crab. Species identification was performed according to Keenan et al. [2] and Keenan [27]. Analyses of fishery data The following data were summarised on a monthly basis: the number of fishing gear units, the number of operation days for traps and gill nets, and species composition. Catch data from each fishing gear were standardised as the CPUE on each operation day (number of crabs gear unit-1 day-1). The sex ratio was calculated as the number of males divided by the total number of crabs caught in each month of each year. To detect the yearly and seasonal fluctuations of the monthly species composition, the daily CPUE, the monthly sex ratio and the individual ECW data for mud crabs caught by each type of fishing gear, generalised additive models (GAMs) using the ‘‘mgcv’’ package [28] for the R language [29] were employed. A GAM is a nonparametric extension of the generalised liner model. This modelling approach allows the relationship between explanatory variables and the response variable to be analysed by a linear and/or nonlinear smoothing function, and this approach is flexible regarding distributions of data [28, 30]. GAMs have been applied to temporal datasets to detect yearly and seasonal trends in biological data [30]. In the GAM analysis for this study, the proportion data on species composition and the sex ratio in addition to the number of crabs (daily catch data) and ECW values of individual males and females were used as the response variables. The explanatory variables included two temporal variables: year and month. The year variable had integer values between 1 and 4 (corresponding to the first to fourth survey years with each year being defined as the period from September to the following August), and the month variable had values between 1 (September) and 12 (following August). GAMs consisting of a binomial error distribution with a logistic-link function, Poisson error distribution with a log-link function and a Gaussian error distribution with an identical link function were assumed

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Fig. 1 Iriomote Island. The white, black and grey circles indicate the sites for rearing juveniles before release, releasing juveniles, and rearing crabs in the net enclosure after release at the tidal flat in the Nakara River respectively

for proportion data, catch data and ECW data respectively. In the GAMs, the number of crabs caught was standardised by the offset variable of the number of fishing gear units [30]. The models were fitted using quasi-frameworks for binomial and Poisson GAMs with overdispersion of the data taken into consideration [30]. The maximum number of degrees of freedom of a smooth term for the month variable was set at four in each GAM to avoid overfitting and to infer the seasonal fluctuation. The significance of each explanatory variable in the model was evaluated by the approximate F test using the ‘‘mgcv’’ package. Release and recapture experiments Release and recapture experiments using artificially produced juveniles were conducted for S. serrata, which was the dominant mud crab species in the study area. Broodstock management and larval rearing to produce juvenile crabs were conducted according to the methods of Hamasaki [31] and Hamasaki et al. [32]. Approximately 270,000 juveniles in the first to second crab stages were stocked in five net pens with bottom nets (4-mm mesh size; 10 9 10 9 2 m) set at a tidal flat (Fig. 1) on May 27, 2003. Crabs were fed with minced krill. After 1 month of culture, juvenile crabs grew to a mean ECW of 23 mm, and 18,330 crabs were released into an open tidal flat at the mouth of the Nakara River on June 26, 2003 (Fig. 1). Moreover, 5,390 crabs that were each injected with a coded wire tag (CWT) [33]

were released at the same site of the Nakara River on June 27, 2003. A total of 970 crabs with CWTs were stocked in a net enclosure (5-mm mesh size; 20 9 20 9 2 m) without a bottom net set at a tidal flat of the Nakara River (Fig. 1) on June 27, 2003. The CWT consisted of a small piece of stainless steel wire with a diameter of 0.25 mm and a length of 1.1 mm, and it was detected in animals using a magnetic detection device (Northwest Marine Technology). After the initiation of the experiments, the mud crabs were recaptured by hand near the release site at low tide during the day or at night on June 26, June 29, July 10, August 22 and September 24, 2003. Sampling was also conducted in the net enclosure at low tide during the day on September 24 and October 22, 2003. The ECW of the captured crabs was measured to the nearest 0.1 mm, and their CWTs were detected with a magnetic detection device. Estimation of size at sexual maturity of mud crabs The size at sexual maturity was estimated for the dominant mud crab species, S. serrata. A total of 54 females and 64 males were obtained from the above mentioned fisherman from May to September 2010. For each crab, the ECW and internal carapace width (ICW), excluding the anterolateral spines, were measured using a Vernier calliper to the nearest 0.1 mm. The highest point of the crushing chela, excluding dorsal spines of males (CH), and the widest portion of the fifth abdominal segments of females (AW)

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were also determined for the analysis of maturity classes (see below). The abdomen of female brachyuran crabs becomes larger in width to accommodate an egg incubation chamber at the pubertal moult [34]. Female mud crabs can be assigned to one of the following three maturity classes based on abdominal shape: mature females with broad U-shaped abdominal flaps, immature females with narrow abdominal flaps, and prepubertal females with intermediate abdominal shapes between immature and mature forms [8]. However, Hamasaki et al. [14] suggested that the intermediate-form females should be treated as premature because of their low reproductive ability. Therefore, to estimate the maturity size of S. serrata in this study, only two groups (mature and immature) were considered, and prepubertal females were considered immature. Allometric relationships between ECW (x) and AW (y) were examined for females at immature and mature stages by a linear regression equation using log-transformed data as follows: lny = alnx ? lnb. Parameters were estimated by the ordinary least squares method. Analysis of covariance (ANCOVA) was performed to detect the differences in slopes and intercepts of the regression equations between different maturity stages. Although the sexual maturity of male crabs is not easily determined by external characteristics, allometric change in the growth of chelae has been analysed to detect the size at sexual maturity of males [34]. The chelae of males have an important role in pre- and/or post-copulatory mate guarding of female crabs. The chelae markedly increase relative to body size growth at the pubertal moult. Pre- and post-copulatory mate guarding of females by males also occurs in mud crabs [35]. The morphometric maturity of males was estimated by the ratio of chela height to body size [8, 14, 36]. Allometric relationships between ECW (x) and CH (y) were examined for males according to Sampedro et al. [37] and Corgos and Freire [38]. Using the log-transformed data of ECW and CH, a principal component analysis (PCA) was performed resulting in two distinguishable groups, which corresponded to immature and mature crabs. With the use of a non-hierarchical classification procedure (k-means cluster with two predetermined groups) based on the scores on the two axes of the PCA, animals were classified as immature or mature, and the parameters of the linear regression equations (lny = alnx ? lnb) for the two male groups were then estimated. These two regression equations were compared with ANCOVA. For both females and males, a generalised linear model consisting of a binomial error distribution with a logisticlink function [30] was applied to determine the size at which 50% of the crabs underwent allometric change of AW or CH. The allometric relationship (lny = alnx ? lnb) between ECW (x) and ICW (x) was also analysed to calculate the ICW from ECW measurements for comparisons

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between different studies. All analyses were performed using the R language [29], and the level of significance was assessed at a = 0.05.

Results Fishery data Two species of the mud crab, S. serrata and S. olivacea, were identified in the fishing activity at Iriomote Island. The total number of crabs caught by traps and gill nets was 3,490 and 671 respectively. S. serrata was the dominant species, accounting for 95.8 and 99.4% of the catches by traps and gill nets respectively. The sex ratio (males to total crabs) was 0.56 for S. serrata in both gear types, and the sex ratio was 0.91 and 1.0 for S. olivacea caught in traps and gill nets respectively. A null hypothesis (H0; sex ratio = 0.5) was rejected by the binomial test for both species excluding gill nets for S. olivacea with a small sample size (S. serrata caught by trap, P \ 0.0001; S. serrata caught by gill net, P = 0.0011; S. olivacea caught by trap, P \ 0.0001; and S. olivacea caught by gill net, P = 0.125). In both species, berried females were not collected. The ECW of most of the S. serrata crabs was between 100 and 170 mm, and the ECW of most of the S. olivacea crabs was between 100 and 150 mm (Fig. 2). Only four S. olivacea crabs were captured using gill nets, so the GAM analysis for species composition was performed using trap data. The composition of species fluctuated yearly and seasonally. The number of S. olivacea crabs decreased towards the end of the survey with the number largely decreasing after May (Fig. 3). The number of gear units used for both traps and gill nets in addition to the number of fishing operation days seasonally fluctuated, and they tended to peak between June and August (Fig. 4). Data analyses were performed for the dominant S. serrata species. In general, the CPUEs increased when fishing activities were high (Fig. 5a). The GAM analysis detected similar fluctuations in catches of S. serrata by both fishing gear types with higher catches found in the first survey year (Fig. 5b, d). The catches tended to be low from January/February to March/April; then, they increased each month, peaking in August and May in traps and gill nets respectively (Fig. 5c, e). There were no evident modal progressions in the monthly size-frequency distributions for S. serrata (supplementary material; Fig. S1) with the modes for both sexes remaining around ECW values of 120 and 160 mm throughout the study period. However, the mean ECW values of the females and males seasonally fluctuated (Fig. 6a, b). The GAM analysis detected the crab growth

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the sex ratios of crabs caught with traps, and no significant fluctuations by year and season were found in the sex ratios of crabs caught with gill nets (Fig. 7b, d, e). The proportion of males caught by traps increased from February to June (Fig. 7c).

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At the tidal flat of the Nakara River, a total of 115 mud crabs were captured. Crabs with CWTs were recaptured on June 26, July 26 and August 22, 2003 with two, four and two crabs captured on each date respectively. Crabs grew exponentially with ECW values increasing from 21 to 70 mm in 3 months (Fig. 8a). In the net enclosure at the tidal flat, the mean ECW of stocked S. serrata reached 62 and 71 mm on September 24 and October 22, 2003 respectively. At both survey dates, the retention rate of CWTs was 84%. Crabs with ECW values greater than 100 mm, which was the approximate minimum size caught with traps and gill nets, were found in the size-frequency distributions for animals sampled at the end of the experiments in September and October (Fig. 8b). Size at sexual maturity

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External carapace width (mm) Fig. 2 Size-frequency distributions for Scylla serrata females and males caught using traps (a) and gill nets (b) and for Scylla olivacea females and males caught with both fishing gear types (c)

trend (Fig. 6c–j). The ECW values of the females and males caught by traps were smaller in the second and third survey years when compared with the other years (Fig. 6c, g), and there was no yearly fluctuation of growth in the crabs caught by gill nets (Fig. 6e, i). Similar seasonal fluctuations were detected in females and males caught with both gear types (Fig. 6d, f, h, i). The ECW of crabs caught in both gear types decreased from December/January to April/May, and the ECW of crabs caught in the traps increased after this time peaking in November/ December. The sex ratios of S. serrata with sample sizes are shown in Fig. 7a. No significant fluctuations by year were found in

Based on abdomen morphology, immature females had ECW values between 97.3 and 133.1 mm, and mature females had ECW values between 128.1 and 195.2 mm respectively. The linear regression equations between logtransformed ECW and AW data for immature and mature females had significantly different slopes (F1,50 = 6.74 and P = 0.0123) (Fig. 9a). As analysed by ECW, the size at which 50% of females reached maturity (SM50) was 132.4 mm (95% CI 128.6–136.2 mm) (Fig. 10). Males were classified by PCA and k-means classification analysis into two groups corresponding to morphologically immature and mature stages (Fig. 9b). Immature males had ECW values ranging between 101.0 and 160.6 mm, and mature males had ECW values ranging between 139.6 and 193.5 mm. Mature males had chelae that were larger than 51.5 mm. The slopes of the linear regression equations between log-transformed data corresponding to the ECW and CH for immature and mature males were not significantly different (F1,59 = 0.336 and P = 0.564), but the intercepts were significantly different (F1,60 = 119.7 and P \ 0.0001). As analysed by ECW values, the SM50 occurred at 150.7 mm (95% CI 146.5–155.0 mm) (Fig. 10). The allometric equations between ECW (x) and ICW (y) were determined for females and males as follows: females, lny = 1.0270lnx - 0.1987 (n = 54, R2 = 0.9979, and P \ 0.0001); and males, lny = 1.0434lnx - 0.2707 (n = 64, R2 = 0.9964, and P \ 0.0001).

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Fig. 3 Species composition of the monthly catches by traps (a), and the relationships between the smoothed component (solid line) of the explanatory variables (x-axis, year and month) used in the fitted generalised additive model and the following response variable: species composition (b year, c month). The y-axis is the normalised effect of the variable with zero corresponding to no effect of the covariate on the estimated response. Values greater than zero indicate a positive correlation, and values less than zero indicate a negative correlation. The estimated degree of freedom (edf) and F value with probability are shown in the graph. Dashed lines indicate ±2 SE or approximately 95% CI

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Fig. 5 Changes in mean (±SE) catch per unit effort (CPUE) on a monthly basis for Scylla serrata caught by traps and gill nets (a), and the relationships between the smoothed component (solid line) of the explanatory variables (x-axis, year and month) used in the fitted generalised additive model and the following response variables: CPUE values for traps (b year, c month) and gill nets (d year, e month). More information is provided in Fig. 3

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Discussion In trap and gill net fisheries at Iriomote Island, two mud crab species, S. serrata and S. olivacea, were found. S. serrata was the dominant species, accounting for 95.8

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and 99.4% of the mud crabs caught with traps and gill nets respectively. This was consistent with the predominance of S. serrata over other mud crab species in tropical oceanic islands, including Palau [12] and Kosrae [13]. Keenan et al. [2] suggested that S. serrata is the most widespread and

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edf = 3.53; F = 6.19; P = 7.47 x 10-5

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Fig. 6 Changes in mean (±SE) external carapace width (ECW) on a monthly basis for female (a) and male (b) Scylla serrata caught by traps and gill nets and the relationships between the smoothed component (solid line) of the explanatory variables (x-axis, year and month) used in the fitted generalised additive model and the following

response variables: ECWs for females caught by traps (c year, d month) and gill nets (e year, f month); and ECWs for males caught by traps (g year, h month) and gill nets (i year, j month). More information is provided in Fig. 3

dominant species in oceanic conditions with full salinity ([34%), and other species are commonly associated with estuarine habitats that have seasonal reductions in salinity due to rainfall. S. olivacea is also closely associated with mangroves and typically occupies burrows within the mangrove habitat [5, 20, 24]. No fishing activities were observed inside the mangroves located at Iriomote Island. Consequently, the species composition obtained through fishing activities in the present study may underestimate the abundance of S. olivacea in mud crabs inhabiting Iriomote Island. Yearly and seasonal fluctuations of the species composition of the mud crabs caught by traps in Iriomote Island were found. S. olivacea decreased year by year with a large decrease after May of each survey year. In the Mekong Delta located in Vietnam, S. paramamosain dominated and comprised over 95% of the catch of mud crabs [8]. S. olivacea

was also present but at a low frequency with a yearly variation [8]; the frequency of S. olivacea decreased from 3.2 to less than 0.1% when the mean monthly salinity decreased from 7 to 4 ppt. Walton et al. [8] also suggested that relatively high salinity conditions may be the reason why S. olivacea is the dominant species on the southeast coast but not in the Mekong Delta in Vietnam. The annual amount of rainfall at Iriomote Island was 1,355, 1,622, 1,957 and 3,087 mm for each of the four survey years (September 2001–August 2005) respectively, and the mean monthly total amount of rainfall largely increased after May as shown in Fig. 11 (data from the Japan Meteorological Agency; http://www.data.jma.go.jp). Thus, salinity fluctuations may be one of the causes for yearly and seasonal variations of S. olivacea occurrence at Iriomote Island. The CPUE values for S. serrata caught with both types of fishing gear were low during the period from January/

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Fig. 7 Sex ratio (SR) of the monthly catches for Scylla serrata with number of crabs (N) caught by traps and gill nets (a) and the relationships between the smoothed component (solid line) of the explanatory variables (x-axis, year and month) used in the fitted generalised additive model and the following response variables: SRs for traps (b year, c month) and gill nets (d year, e month). More information is provided in Fig. 3

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February to March/April, but the values increased after this period. There were no available data for water temperature at Iriomote Island, but the temperature data at the neighbouring Ishigaki Island (Fig. 1) (data from the Japan Oceanographic Data Center; http://www.jodc.go.jp) could represent the temperatures present at Iriomote Island (Fig. 11). Thus, the catch rate of the crabs was generally

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low during the winter when temperatures were lower, and it increased during the summer when temperatures increased. The increased catch rate in the summer has been previously reported for mud crab species [6, 39]. Modal progressions in the monthly size-frequency distributions of S. serrata caught with both fishing gear types in Iriomote Island were not observed. However, clear

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80

(a)

70 60

Net enclosure

31

lnAW

ECW (mm)

Nakara River

40 30

4.6

Immature

4.4

Mature

4 3.8

49

3.6

18

20

3.4

10

3.2

0 8-Jun

30

Immature: y = 1.6403x - 4.1569 (n = 42, R 2 = 0.8983, P < 0.0001)

3 28-Jun

18-Jul

7-Aug

27-Aug

16-Sep

6-Oct

26-Oct

15-Nov

4.4

(b)

4.6

15 10

5.2

5.4

4.2

lnCH

Frequency (%)

Net enclosure: Oct (n = 25)

20

5

Mature: y = 1.2005x - 1.9526 (n = 28, R 2 = 0.7414, P < 0.0001)

4.4

Net enclosure: Sep (n = 31)

4.8

(b)

4.6 Tidal flat: Sep (n = 7)

25

Mature: y = 1.3209x - 2.4464 (n = 12, R 2 = 0.9694, P < 0.0001)

4.2

31 10

50

(a)

4.8

25

7

4 3.8 3.6

5

Immature: y = 1.3595x - 2.9848 (n = 36, R2 = 0.8488, P < 0.0001)

3.4

0

3.2 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115

3

External carapace width (mm)

4.4

seasonal variations were detected in the mean ECW values of S. serrata caught with both gear types, indicating a high growth rate during the summer from April to May. In contrast, decreases in the mean ECW values occurred during the winter from December to January. The following reasons may explain the decreased mean ECW values: natural death of larger (older) crabs and/or recruitment of young crabs to the fishery. In the release and recapture experiments at the natural tidal flat in this study, some of the juveniles, which moulted to the first and second crab stages in late May, reached a recruitment size (ECW) of 100 mm after 4 months. Captive S. serrata females obtained from Iriomote Island spawn year round according to laboratory experiments, but main spawning is observed in the warmer season from April to November, peaking around August [40, 41]. Furthermore, the larval developmental period from hatching to the first crab stage ranges between 22 and 42 days at water temperatures ranging between 23 and 32°C [31]. Together, these findings suggest that the decreased mean ECW values found from

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4.6

4.8

5

5.2

5.4

lnECW Fig. 9 Relationships between log-transformed data of external carapace width (ECW) and fifth abdominal width (AW) of Scylla serrata females (a). Relationships between log-transformed data of ECW and chela height (CH) of Scylla serrata males (b) Immature (0) or mature (1) of crabs

Fig. 8 Results of release and recapture experiments using artificially produced Scylla serrata juveniles. Mean (±SE) external carapace width (ECW) of crabs captured over time after being released at the natural tidal flat in the Nakara River (a). The size-frequency distributions of the crabs recovered in September and October from the natural tidal flat and the net enclosure set at the natural tidal flat in the Nakara River (b). Numbers in the graph (a) indicate the number of samples captured and measured

1

0.5

Female Male Female Male

0 90

110

130

150

170

190

210

External carapace width (mm)

Fig. 10 Maturity or immaturity of Scylla serrata females and males according to their external carapace width

December/January to April/May are due to the recruitment of young crabs to the fishery. Yearly fluctuations were observed in the catch rate and body size of S. serrata in Iriomote Island. As compared to the other survey years, the catch rate was higher in the first survey year with both fishing gear types. Compared to the

Fish Sci (2011) 77:915–927

Amount of rainfall (mm)

500

925

(a)

400

300

200

100

0 Sep Oct Nov Dec Jan Feb Mar Apr May Jun

Water temperature (°C)

30

Jul

Aug

Jul

Aug

(b)

28

26

24

22

20 Sep Oct Nov Dec Jan Feb Mar Apr May Jun

Month

Fig. 11 Mean (±SE) monthly total amount of rainfall from September 2001 to August 2005 at Iriomote Island (a) and mean (±SE) water temperature each month from January 2002 to December 2005 at Ishigaki Island (24°200 N and 124°080 E) (b) (data from the Japan Meteorological Agency; http://www.data.jma.go.jp)

first and fourth survey years, the body size of crabs caught with the trap fishing gear was smaller in the second and third survey years. Water temperature affects the catch rate of mud crabs, and it may affect the growth rate of the crabs [42]. Water temperature data at Ishigaki Island are available from January 2002 onward, but they are not available between September and December in 2001. Consequently, to compare water temperature data between different survey years in this study, the mean water temperature from January to August was used and calculated to be 21.6, 21.7, 22.0 and 21.7°C for each year in the four survey years respectively. According to these calculations, the mean water temperature did not vary greatly between years, and it did not affect yearly fluctuations of catch and growth of S. serrata at Iriomote Island during the study period. However, there may have been another possible cause of the smaller ECW values found in the second and third survey years. Artificially produced S. serrata juveniles were stocked in the Nakara and Kuira Rivers at Iriomote Island in late July 2001 (7,789 crabs with a mean ECW of 29 mm), early June 2002 (35,410 crabs with a mean ECW of 25 mm), and late June 2003 (28,650 crabs with a mean

ECW of 23 mm) (K. Hamasaki; unpublished data from 2001, 2002 and 2003), showing higher numbers of released juveniles in 2002 and 2003 than in 2001. Crabs in the first to second stage were recruited to the fishery after 4 months. Therefore, the stock enhancement programme may have decreased the mean ECW of the crabs by increasing the recruitment of small crabs. Yearly fluctuations of S. serrata catch numbers and body size should be evaluated using more long-term data that includes variable ocean environmental conditions. The overall sex ratio of S. serrata caught in traps and gill nets in Iriomote Island was slightly male-biased (0.56). In addition, seasonal variation of the sex ratio was observed in traps with high values from February to June, indicating that females were inactive and/or males were active and could be caught in baited traps in this period. Similarly, overall and seasonal male-biased sex ratios have been reported for S. olivacea in the Andaman Sea (Thailand) depending on offshore migration of females for spawning [7]. In this study, no ovigerous females were caught. S. serrata females are expected to migrate offshore for spawning, which has been reported for mud crab species [7, 43, 44] all year round, especially in the main spawning period from April to November [40, 41]. Female feeding activity may decrease before offshore spawning and/or males may become active for copulating with females. In this study, the sex ratio of S. olivacea, which was mainly caught using traps, was highly biased towards males (0.96). Such a heavy male-biased sex ratio may be a specific trait of the local fishery because it has not been previously reported for mud crab species [6, 7, 11]. The discontinuity of the two regression lines of carapace width (ECW) and AW in females demonstrated the occurrence of a puberty moult over the ECW range of 128.1–133.1 mm (ICW ranging between 119.7 and 124.5 mm, which was calculated from a regression equation between log-transformed data of ECW and ICW in the present study), and the ECW at which 50% of females reached morphological maturity (SM50) was estimated at 132.4 mm (ICW of 123.8 mm) for S. serrata at Iriomote Island. The SM50 value in the present study was larger than that estimated for mud crab females from South Africa (ECW of 123 mm) [35] where S. serrata is the only species present [2]. The SM50 of S. serrata females in the present study was also larger than that estimated for S. paramamosain (ICWs of 110.5 and 105.6 mm in Bandon Bay, Thailand [5, 14]; and ICW of 102.3 mm in Mekong Delta, Vietnam [8]) and S. olivacea (ICW of 91.2 mm in Bandon Bay [5]; and ECW of 95.5 mm in Klong Ngao mangrove swamp in Andaman Sea, Thailand [15]). As for male sexual maturity, the ECW/CH relationships suggested that the two different morphometric forms (mature and immature) overlapped between ECWs of 139.6 and 160.6 mm

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(ICWs between 132.0 and 152.7 mm), and the SM50 was estimated at an ECW of 150.7 mm (ICW of 142.9 mm). Robertson and Kruger [35] evaluated the functional maturity size of South African S. serrata males by the presence of mating scars on the front of the first pair of walking legs, which are formed by the rubbing of the female carapace on the legs of the male during the precopulatory embrace. They reported that mating scars on males were most frequently found on larger animals with ECWs greater than 135 mm. Knuckey [36] estimated the morphological maturity size at ICW values between 146 and 149 mm by the ratio of chela height to the ICW of males. Moreover, in mud crabs from Australia, where the S. serrata species is dominant [2, 4], mating scars are more common in males with ICWs greater than 140 mm [36]. Thus, the maturity size of S. serrata males at Iriomote Island was similar to that of Australian mud crabs, which have a larger maturity size than the South African mud crabs. The SM50 of S. serrata males was larger than that estimated for S. paramamosain (ICW of 101.9 mm in Mekong Delta [8] and ECW of 106.4 mm in Bandon Bay [14]). Immature females and males, which had overall sizefrequency distributions less than the SM50 classes of S. serrata (Fig. 2), comprised approximately 37 and 66% of the catch by traps respectively, and 41 and 64% of the catch by gill nets respectively. Both fishing gear types caught more immature male crabs than female crabs. Prohibitions on the capture of immature crabs based on the SM50 values estimated for S. serrata females and males in the present study should be implemented in the fishery management of S. serrata to sustain the resources of Iriomote Island. Thus, this study suggested that the minimum size for capture, as measured by ECWs, should be 140 mm for females and 160 mm for males (higher than the upper limit of 95% CI for the estimates of SM50) to allow almost all individuals to achieve a functional maturity size (Fig. 10). Acknowledgments We gratefully acknowledge the help of Mr. Choji Ishigaki for collecting fishery data during the surveys.

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