Biology 67 (2017) 319–330 brill.com/ab

Population structure and morphometric variation in the sand-bubbler Scopimera crabricauda (Brachyura: )

Sana Sharifian1, Vahid Malekzadeh2, Ehsan Kamrani2,∗ and Mohsen Safaie2 1 Department of Marine Biology, University of Hormozgan, Bandar Abbas, Iran 2 Fishery Department, University of Hormozgan, Bandar Abbas, Iran Submitted: September 2, 2017. Final revision received: November 4, 2017. Accepted: November 8, 2017

Abstract In the present study, population ecology and relationships between various morphometric characters of the sand-bubbler crab Scopimera crabricauda from the Persian Gulf (Iran) were studied. were collected monthly by excavating nine quadrats in high-density areas of open burrows at low, mid and high intertidal levels during spring low tides for one year. A total of 534 crabs was collected, of which 70% were males (and 30% females). Mean carapace width and total weight in both sexes showed significant differences. Crabs with a carapace width ranging from 5 to 7 mm were the dominant crabs in the population. The highest numbers of crabs were found in the higher intertidal area. The mean size of crabs decreased towards the sea. The aggregation of small crabs was found towards sea in female crabs. Juveniles were abundantly found from January to March whereas the sub-adults and adults were mostly found from April to January. The carapace length to carapace width relationship differed between males and females, as did the carapace width and carapace length to total weight relationships. Finally, the relationship between carapace width and weight for both sexes showed that the growth of this species is allometric.

Keywords Bandar Abbas; dotillid crabs; growth; isospatial; population ecology; sandy shores; tidal zone

Introduction Dotillid crabs are common dwellers of tropical sandy and muddy shores, mangrove swamps (Hartnoll, 1973), estuaries and backwaters of tropical and subtropical re- gions (Kemp, 1919). Dotillid crabs include several genera of very small crabs such

∗ ) Corresponding author; e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2017 DOI 10.1163/15707563-00002539

Downloaded from Brill.com09/29/2021 06:49:55AM via free access 320 S. Sharifian et al. / Animal Biology 67 (2017) 319–330 as Dotilla and Scopimera, which have the greatest number of species. The crab Scopimera crabricauda is a deposit feeder, active diurnally, at low tide, and inhab- its restricted and sandy estuarine areas. Their range extends further east than that of Dotilla crabs (Barnard, 1950; Serene & Moosa, 1981). Dotillid crabs produce pseudofaecal pellets while feeding at low tide and are generally restricted to muddy shores; however, some genera, including Dotilla and Scopimera, prefer a sandy en- vironment. Moreover, crabs including D. fenestrate subsist in mangrove swamps (Macnae, 1968). Sandy shores may be a favorable environment for crabs of the Scopimera, a deposit-feeding organism, since habitats suitable for their for- aging are the ones that enable them to sort sand with high efficiency and extract the small amount of organic material (Tweedie, 1950; Ono, 1965). These crabs have gained the ability to inhabit the intertidal zone by various morphological, physi- ological, and behavioral adaptations (Gherardi & Russo, 2001). They can display an isospatial strategy, which means they alternate their location between exposure to air and water while remaining within a belt along the sea-land axis (Vannini & Chelazzi, 1985). In , as growth progresses, certain dimensions of the animal’s body may grow much more than others, resulting in a phenomenon known as allome- try (Hartnoll, 1974). Crabs, as most free-living crustaceans, are ideal subjects for morphometric studies because of the ease with which fast and precise measure- ments can be made on their hard exoskeleton (Ledesma et al., 2010). In population studies, morphometric analysis provides a powerful complement to genetic and environmental stock identification approaches (Cadrin, 2000) and length-weight re- lationships allow the conversion of growth-in-length equations to growth-in-weight for use in a stock assessment model (Moutopoulos & Stergiou, 2002). It can be useful to convert to length (width), when only the weight is known and the length- weight regression may be extensively used to estimate length from weight (Sangun et al., 2009; Oluwatoyin et al., 2013). Knowledge of these characters and size relationships has a particular impor- tance in the study of crustaceans that play an important rle in an ecosystem. The length/width-weight relationship is expected to be a suitable tool for evaluating populations (Gorce et al., 2006; Fumis et al., 2007; Sangun et al., 2009, Josileen, 2011; Sahoo et al., 2011; Oluwatoyin et al., 2013; Safaie et al., 2013; Shar- ifian & Kamrani, 2015). Information about the individual body weight-length/width relationship in populations is important for estimating the population size of a stock. Hence, the study of the length-weight relationship in aquatic has been widely used in delineating the growth patterns during their developmental pathways (Bagenal, 1978). To date, few studies have been performed of the population structure of crabs of the genus Scopimera (Fielder, 1970; Yamaguchi & Tanaka, 1974; Wada, 1981; Clayton & Al-Kindi, 1998). Most studies have been performed on distribution (Silas & Sankarankutty, 1967; Fielder, 1971; Wada, 1976; Wada, 1983a, b), feeding (Fielder, 1970; Zimmer-Faust, 1987), mating (Yamaguchi et al., 1979; Koga et al.,

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Figure 1. Sampling locations at southern Golshahr, Bandar Abbas, Iran, on the Persian Gulf for the species Scopimera crabricauda Alcook, 1900 from January 2016 to January 2017.

1993), breeding biology (Yamaguchi & Tanaka, 1974; Wada, 1981; Suzuki, 1983; Henmi & Kaneto, 1989), and various aspects of their ecology (Takahasi, 1935; Harada & Kawanabe, 1955; Ono, 1965; Fielder, 1970). Some population aspects of S. crabricauda were studied in an estuarine habitat in Oman (Clayton & Al-Kindi, 1998). In the present study, we investigated the population structure and the relationships between various morphometric characters (carapace width/length and body weight) of S. crabricauda from the sandy shores of the Persian Gulf. This knowledge can be useful in studies of resource management.

Material and methods The sampling area was the sandy shores of the Persian Gulf at southern Golshahr, Bandar Abbas, Iran (27¡11N 56¡20E; Fig. 1). The climate of this area is tropical and the annual water temperature varies from 25 to 35¡C. Samples were taken monthly from January 2016 to January 2017. The sampling was performed by excavating nine quadrats (100 × 100 × 20 cm deep; three for each intertidal level) in high-density areas of open burrows, and collecting the crabs after sieving the sand (Hails & Aziz, 1982) at three intertidal levels - low, mid and high - during spring low tides. At the sampling site, crabs were sexed and counted for each intertidal level. The carapace width (CW) and carapace length (CL) were measured using a Vernier caliper (± 0.01 mm accuracy), with terminology based on Ng (1988). The total body weight (TW) was measured using a standard electric balance with 0.1mg accuracy. Then, the crabs were released back into the field. Indi- viduals (both male and female) smaller than the smallest captured ovigerous female

Downloaded from Brill.com09/29/2021 06:49:55AM via free access 322 S. Sharifian et al. / Animal Biology 67 (2017) 319–330 were classified as juveniles. Recruitment was assessed by calculating the propor- tion of juveniles in the samples. The overall size and weight frequency distributions were tested for normality using the Kolmogorov-Smirnov (Lilliefors) (D)test(Zar, 1999). The overall size and weight frequencies showed normal and non-normal distributions, and subsequently were subjected to parametric and non-parametric methods, respectively. The mean size of males and females was compared using the independent-samples (Student’s) t-test. The mean weight of males and females was compared using the two-independent-samples test (Mann-Whitney U). The mean size of both sexes during the different months and at the three intertidal levels was tested using a one-way ANOVA followed by Tukey’s post-hoc test and F statistic. The mean weight of both sexes during the different months and at the three inter- tidal levels was tested using a non-parametric test followed by the Kruskal-Wallis test and chi-square (χ 2). Mean ± standard error is presented throughout the text. The CW to CL relationship was estimated in each sex, using the linear equation y = a + bx and the correlation coefficient (R2), where y is the carapace width in mm, x is the carapace length in mm, and a and b are constants. The CW to TW and CL to TW relationships were estimated according to the formula W = aLb (Pauly, 1983) and the correlation coefficient (R2), where W is the total weight in mg, L is the length or width of the carapace in mm, a is the intercept (condition factor) and b is the slope (growth coefficient). If the value b is equal or close to 3, the growth of species is isometric, but if it is substantially different from 3, then growth is allometric. This formula is known as the allometric formula and b is also known as the allometric coefficient (Cadima, 2003). A linear equation (log TW = log a + b log CW) was fitted to data transformed to a logarithmic scale. Deviation of the estimated value b from the isometric value 3 was tested using the t-test: sd(CW) b − 3 √ t = × √ × n − 2 sd(TW) 1 − r2 where sd(CW) is the standard deviation of values of log CW, sd(TW) the standard deviation of values of log TW, and n is the number of crabs used. The value b will be different from 3 if t is greater than the table value of t for n − 2df (Pauly, 1983).

Results Population structure A total of 534 crabs were collected: 375 males (70%) and 159 females (30%). Malesrangedfrom3.46to8.43mmCW(mean5.97± 0.05 mm) and females from 3.29 to 6.75 mm CW (mean 5.13 ± 0.06 mm). Regarding the CL, males ranged from 2.30 to 6.01 mm (mean 3.97 ± 0.03 mm) and females ranged from 2.27 to 5.22 mm (mean 3.45 ± 0.04 mm). Males and females differed significantly in CW (t = 9.11, P<0.05) and CL (t = 7.86, P<0.05). The TW of males ranged from 0.01 to 0.50 g (mean 0.19 ± 0.005 g) and in females it ranged from 0.01 to 0.22 g

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Figure 2. (A) Mean size of carapace width (CW) and carapace length (CL) with standard error for both sexes. (B) Mean total weight (TW) with standard error for both sexes.

(mean 0.08 ± 0.003 g). Males and females differed significantly in TW (Wilcoxon: Z =−10.87, P<0.05). Comparison of CW and CL during the different months showed significant dif- ferences (ANOVA: df = 12, F = 9.28, P<0.05; df = 12, F = 3.85, P<0.05, respectively) (Fig. 2A). The CW varied from 4.90 mm in January 2016 to 6.43 mm in June. Moreover, CW and CL showed significant differences during the differ- ent seasons (ANOVA: F = 20.70, P<0.05; F = 6.27, P<0.05, respectively). The CW varied between 5.17 mm in winter 2016 and 6.18 mm in spring 2016. Comparison of the TW during the different months showed significant differences 2 = (χ12 116.39, P<0.05; Fig. 2B). It varied between 0.06 g in January 2016 and 0.22 g in June. Moreover, TW showed significant differences during the different 2 = seasons (χ5 84.14; P<0.05). The TW varied between 0.10 g in winter 2016 to 0.19 g in spring 2016. Comparison of the mean CW at three intertidal levels showed no significant differences (ANOVA: F = 2.3; P = 0.09) nor did comparison of the 2 = = mean TW at the three intertidal levels (χ2 3.08, P 0.21). The number of crabs collected from the three intertidal levels was largest at the high intertidal level (224 crabs) and smallest at the low intertidal level (123 crabs) (187 crabs at the mid tidal level; Fig. 3). Among the ovigerous female crabs, which were captured from March to April (2016) (N = 11 crabs), the smallest was 4.88 mm. Crabs smaller than this size were considered juveniles and larger ones as sub-adults (5.5-7 mm for male crabs and 4.5-5 mm for female crabs) or adults (7-8.5 mm for male crabs and 6-7.5 mm for female crabs). Figures 4A, B show the number of crabs collected during the sampling period. Sub-adult crabs were found to be the dominant crabs in the population in both sexes. Figures 5A, B show the number of crabs at the three intertidal levels. The male crabs were less abundant toward the lower intertidal area. Adult female crabs were more abundant at the higher level, while sub-adults and juveniles showed the reverse trend.

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Figure 3. Number of individuals of S. crabricauda collected from January 2016 to January 2017.

Figure 4. Collected number of males (A) and females.

Figure 5. Number of males (A) and females collected at three intertidal levels.

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Figure 6. Length to width relationship in male (A) and female (B) crabs.

Morphometric characteristics CL to CW relationship The relation between CL (range: 2.30-6.01 mm, mean: 3.97 ± 0.03 mm) and CW (range: 3.46-8.43 mm; mean: 5.97 ± 0.05 mm) for 375 males is shown in Fig. 6A. There was a high correlation between carapace length and width (R2 = 0.92, P<0.05). For the 159 females the relationship between CL (range: 2.27-5.22 mm, mean: 3.45 ± 0.04 mm) and CW (range: 3.29-6.75 mm; mean: 5.13 ± 0.06 mm) is presented in Fig. 6B. There was a weak correlation between carapace length and width (R2 = 0.64, P>0.05). Relationship CW (CL) to TW The relation of CW (CL) to TW (range: 0.01-0.50 g, mean: 0.19 ± 0.005 g) for 375 males is displayed in Figs 7A, B. The correlation coefficient between carapace width and the total weight was high (R2 = 0.91, P<0.05); the correlation be- tween carapace length and total weight (R2 = 0.84, P<0.05) was relatively high. Figures 8A, B show the relation between CW (CL) and TW (range: 0.01-0.22 g, mean: 0.08 ± 0.003 g) in 159 females. Carapace width and the total weight were

Figure 7. (A) Carapace width to total weight relationship and (B) Carapace length to total weight relationship in male crabs.

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Figure 8. (A) Carapace width to total weight relationship and (B) Carapace length to total weight relationship in female crabs. highly correlated (R2 = 0.82, P<0.05), but no correlation was found between the carapace length and the total weight (R2 = 0.47, P>0.05). In summary, the different morphometric relationships showed that the CW to TW relation for both the sexes had a high R2 value and the exponent was signif- icantly different from 3 (P<0.05). Therefore, it was assumed that the growth of this species is allometric. The linear relationship between carapace length and width in males and females had an R2 value of 0.92 and 0.64, respectively, showing weak and strong correlation in females and males, respectively.

Discussion

The current study showed a clear sexual dimorphism, with males larger than fe- males (significant differences of CW and CL between sexes). This agrees with the findings of Clayton and Al-Kindi (1998) that showed that the largest individuals were males. This study showed that crabs ranging from 5 to 7 mm CW were the dominant crabs in the population. The range of CW for the crabs S. crabricauda and D. sulcata from the Gulf of Oman was reported as 2.2-5.9 mm and 2.1-10.3 mm, respectively (Clayton & Al-Kindi, 1998). The results on crabs collected from three intertidal levels showed that the higher intertidal area had the highest number of crabs. Clayton and Al-Kindi (1998) re- ported that S. crabricauda was distributed at tidal heights above that of D. sulcata in the Gulf of Oman. The lowest number of S. crabricauda crabs in the lower in- tertidal area may indicate a tendency of the crabs to run parallel to the shoreline rather than run at angles to the shore. Sediment grade is another major factor de- termining the crabs’ position on the shore (Titgen, 1982). It seems that crabs of the genus Scopimera prefer well-drained, clean, medium- and fine-grained sands (Tit- gen, 1982; Wada, 1982), which correspond to the higher intertidal area in our study. It can also be related to sex, as Fielder (1970) reported a tendency where males of Scopimera inflata occur on the landward side and females on the seaward side.

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The size frequency classes in S. crabricauda showed that the distribution of the size classes in both sexes declined from the higher to the lower intertidal area. Re- garding females, small crabs tend to be aggregated towards the sea, so their highest frequency was observed in the lower intertidal area. Warner (1969) explained the correlation of size and distribution by the fact that larger crabs are not subject to the same degree of desiccation as are smaller crabs. This pattern was also observed in the crab Scopimera inflata from the eastern Australian coast: larger crabs tended to occur on the landward side, and the average size decreased towards the seaward margin (Fielder, 1970). The averages of CW and CL and the frequency of size classes in S. crabricauda showed that juveniles were abundant from January (2016) to March (2016), whereas sub-adults and adults were mostly found from April (2016) to January (2017). This indicates that S. crabricauda had a single recruitment period from January to March (in winter). The recruitment of juvenile S. crabricauda in Oman was reported as September to October (Clayton & Al-Kindi, 1998), which differed with our finding. The different breeding season between the two populations may be the reason for the difference. The highest number of ovigerous S. crabricauda in the Gulf of Oman was found in September (Clayton & Al-Kindi, 1998), while in our findings the ovigerous females were collected from March to April (2016). In the , Scopimera globosa, at Tomioka Bay, Japan (Suzuki, 1983), in the freshwater crab Sodhiana iranica from Iran (Sharifian et al., 2017), and in Portunus pelagicus from India (Sahoo et al., 2011), a single recruitment period was observed, but the latter species displayed two recruitment periods in Suez Bay (Zaghloul, 2003). The length relationships are often used to calculate the standing stock’s biomass, condition indices, the ontogenetic changes and several other aspects of fish or crus- tacean population dynamics (Oluwatoyin et al., 2013). In addition, for management of the populations, crabs caught can be weighed by groups or individually by fish- ermen, then catches under the size limits can be returned to the habitat. If an organism grows equally along all dimensions of the body, this means that the growth is relatively constant and with a doubling of length, its weight will increase directly proportional to the increase in volume (23) (Cadima, 2003). In isometric steady growth, there is a cubic relationship between length and weight, and the curve will be a power or non-linear function (King, 1996). The current study showed allometric growth for crabs S. crabricauda in both sexes. This means that increases of weight and length are not coordinated in S. crabricauda and the allometric constant (b) has a value far from 3, but generally ranged between 2.5 and 3.5. In this study, the value of b varied between 2.5 and 3.6, which represents a clear allometric relation in both sexes. The value depends on different factors including temperature, salinity, sex, food, stage of maturity and season (Gorce et al., 2006). Our results show that growth in S. crabricauda is allometric, representing an unequal rate in the growth of body dimensions. Josileen (2011), in a study on morphometric relationships of Portunus pelagicus from India, described allomet- ric relationships and showed a highly significant difference of growth between the

Downloaded from Brill.com09/29/2021 06:49:55AM via free access 328 S. Sharifian et al. / Animal Biology 67 (2017) 319–330 sexes. A difference in growth rate by sex in adults of Scopimera globosa during the reproductive period was reported by Yamaguchi & Tanaka (1974), with males growing more rapidly than females. The significant difference in mean total weight, beside the unequal value of a between males and females of S. crabricauda, indi- cates that the weight of both sexes is unequal. The linear relationship between carapace width and length had a high and a low correlation coefficient in males and females of S. crabricauda, of 0.92 and 0.64, respectively. The relationship between CL and CW in Portunus pelagicus from In- dia was linear and growth was isometric (Sahoo et al., 2011). For brachyurans in general, when two carapace dimensions are correlated (e.g., CW and CL), changes during ontogeny do not occur because the growth tends to be isometric (Fumis et al., 2007). The weak correlation between CW and CL in females of S. crabricauda was in agreement with the findings of Josileen (2011), Sahoo et al. (2011) and Oluwatoyin et al. (2013). This study provides data on the population ecology of S. crabricauda from the Persian Gulf. The results of the relationship between the carapace width and weight enables the length in these crabs to be estimated. Weighed crabs do not need to be measured, so the results of this study provide useful information for effective management of this species along the southern shores of Iran on the Persian Gulf.

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