Journal of Biology Advance Access published 7 July 2017 Journal of

The Crustacean Society Crustacean Biology Journal of Crustacean Biology, 37(4), 465–472, 2017. doi:10.1093/jcbiol/rux045

Size at sexual maturity, breeding season, and fecundity of

the intertidal xanthid Leptodius exaratus (H. Milne Downloaded from https://academic.oup.com/jcb/article-abstract/37/4/465/3934667 by guest on 22 September 2019 Edwards, 1834) (: Brachyura) in the Persian Gulf, Iran

Neda Fahimi1, Jafar Seyfabadi1 and Alireza Sari2 1Department of Marine Biology, Faculty of Marine Sciences, Tarbiat Modares University, P.O. Box 64414-356, Noor, Mazandaran, Iran; and 2School of Biology and Centre of Excellence in Phylogeny of Living Organisms, College of Sciences, University of Tehran, Tehran, Iran.

Correspondence: Jafar Seyfabadi; e-mail: [email protected]; [email protected] (Received 29 July 2015; accepted 25 April 2017)

ABSTRACT Size at reproductive maturity of the xanthid crab Leptodius exaratus (H. Milne Edwards, 1834) was determined by comparing gonadal development and the relative growth of gonopods and chelae in males and abdomens and chelae in females from August 2012 to August 2013. The size at which 50% of the of males and females were found to be mature was at carapace lengths (CL) of 16mm and 13mm, respectively. The smallest ovigerous female was 9.6mm CL. The ovigerous females were found throughout the year with a peak in August2013.The numbers of eggs varied between 600 and 9,000 in individuals 9.6 mm and 20 mm CL, respec- tively. The monthly changes of gonadal indices in males and females indicated that mating was at its peak in spring and summer. The ovaries began to develop in March 2013. The results suggest that some females may spawn more than one batch of eggs per year. Fecundity as measured by the number of eggs was lower than in other xanthid , perhaps as a result of the high temperatures in the Persian Gulf. Key Words: gonads, gonopods, reproductive biology,

INTRODUCTION The fecundity and breeding season of a species is an impor- tant aspect in the study of its population dynamics. A transition Leptodius exaratus (H. Milne-Edwards, 1834) is one of the most in growth patterns of the reproductive structures often occurs at common xanthid crabs on the intertidal rocky shores along the the puberty molt, so called because it divides the pre- and post- coasts of the Persian Gulf (Naderloo & Türkay, 2012). Crabs puberty phases of the life of , which is commonly asso- remains under small or medium-size boulders and live in bur- ciated with physiological and functional changes related to sexual rows throughout the day during both low and high tides (Kneib & maturity (Moriyasu et al., 2002). Weeks, 1990). Although L. exaratus has a wide distribution through- Because temperature and salinity in the Persian Gulf are rela- out tropical and subtropical coasts in the Indo-West Pacific region tively high, we hypothesized that these factors could affect the size (Dai & Yang, 1991), its reproductive biology and ecology are rela- of L. exaratus at the onset of sexual maturity. Therefore, we studied tively little known (Watanabe et al., 1990). the size at sexual maturity of this crab as determined by relative Sexual maturity is dependent on the size of individuals growth and condition of the gonad, breeding season, and fecundity. (Watanabe et al., 1990), and relative growth of the chelae and first gonopods (the intermittent organ in males) with respect to body size. In females, relative growth of abdominal width with respect to body size was examined to find the size at which sexual maturity is MATERIALS AND METHODS attained or the puberty molt occurs. Size at onset of sexual maturity and fecundity should, therefore, be considered as important aspects Sampling of the reproductive biology of brachyuran crabs. Such information Crabs were collected manually from August 2012 to August can be obtained through direct observation of the appearance of 2013 during the low tide from the rocky shores of Hormuz the gonads and associated reproductive organs (Hartnoll, 2015). Island (Fig. 1), which is located at the entrance to the Strait of © The Author 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: [email protected] N. FAHIMI ET AL.

Hormuz, Persian Gulf, Iran (27°6´25″ to 27°2´7″ N, 56°30´8″ to of females (AW) from the maximum width of the fifth segment 56°25´1″E). The region is arid to semi-arid, with a mean annual (Rasheed & Mustaquim, 2010). The body and gonad weights were rainfall of 229 mm (http://www.irimet.net). Crabs were sexed, measured with a digital balance to the nearest 0.01 g. measured, and weighted in the laboratory. Sex was determined by examining the abdominal morphology. The number of ovigerous Gonadal maturity females in the samples was also noted for determining breeding season. The carapaces of specimens were removed to examine gonads macroscopically, which allowed recognition of differentiation between immature and mature gonads. Males having anterior and Measurements middle vas differentia enlarged and white in color were regarded The carapace length (CL) of the crabs ranged from 8.25 to as mature (Rasheed & Mustaquim, 2010). Females with large, 22.00 mm in males (N = 304) and 6.43 to 20.1 mm in females orange, and granular ovaries occupying the gastric, posterior, (N = 275). The specimens were fixed in 5% seawater formalin and intestinal cavities were considered as mature (de Lestang et

solution, followed by measuring chelae, abdomen, male first gono- al., 2003). The spent females were easily recognized by their semi- Downloaded from https://academic.oup.com/jcb/article-abstract/37/4/465/3934667 by guest on 22 September 2019 pod, and carapace for morphometric analyses. Carapace length transparent ovaries. Maturity stages fell into four classes following and width were measured using a digital caliper to the nearest Kumar et al. (2003) and de Lestang et al. (2003). Ovarian devel- 0.01 mm. Length of chelar propodus (CPL) was taken from the opment was classified by size and color of the ovary as follows: tip of propodus (fixed finger) to the base where it articulates with Stage 1, immature, ovary very thin and transparent (colorless); the carpus. Length of the male first gonopods (GL) was taken Stage 2, maturing, ovary changes to creamy color, but not extend- from the tip to the base of the gonopod and abdominal width ing into hepatic region; Stage 3, maturing, ovary enlarged and

Figure 1. Location of Hormoz Island in the Persian Gulf, Iran.

466 REPRODUCTIVE BIOLOGY OF LEPTODIUS yellow, extending to cover 1/3–1/4 of the hepatic region; Stage When the b value equals 1 then it is assumed as isometry and the 4, mature, ovary orange or reddish orange and occupies most of organ and the body are growing at the same rate (Hartnoll, 1982). the hepatic region. The ovary and vas deferens were removed and weighed. The gonadosomatic index (GSI) was calculated based on Quinn & Kojis (1987) as: RESULTS GSI =× gonad weight /% total weight 100 Sexual maturity of males The size at which male Leptodius exaratus reached sexual maturity was determined by examining the condition of the testes of male Fecundity individuals. The size at which 50% of the males were morphologi- cally mature (Fig. 2A) was 16 mm (CL). The onset of sexual matu- Fecundity, defined as the number of eggs (Hartnoll, 2015) pro- rity in the males showed no related noticeable changes in CW and duced by a female, has been adopted by many carcinologists abdominal width (AW) relative to CL, but was associated with the

(e.g., Negreiros-Fransozo et al., 1992; Pinheiro & Fransozo, 1995). relative changes in the size of the propodus and gonopods. The Downloaded from https://academic.oup.com/jcb/article-abstract/37/4/465/3934667 by guest on 22 September 2019 Fecundity is estimated using mathematical models fitted to scatter regression equations for the mature and immature phases (sepa- plots relating number of eggs (EN) to size (usually carapace width, rated visually) are given in Table 1. The estimated regression for CW, or carapace length, CL). In general, fecundity is positively the propodus (RPL and LPL) and gonopods indicated two statisti- correlated with size or weight of the ovigerous female (Ogawa & cally different lines between the maturation phases (P < 0.05). In Rocha, 1976, Pinherio & Terceiro, 2000) and can be markedly the relationship between carapace length (CL) and left and right affected by particular environmental factors. propodus lengths (RPL and LPL, respectively) of mature and Only ovigerous females having bright yellow or bright orange immature males (Figs. 3, 4), the value of regression coefficient b eggs, indicating that the eggs were deposited recently, were used was found to be 1.057 for immature males and 1.036 for mature in the analysis. Egg-bearing pleopods were carefully removed and males. These values were significantly different from 1 (t = 13.71 the weight of the whole egg mass (egg + pleopod) was taken to for immature males and 5.77 for mature males; P < 0.05), show- the nearest 0.0001g on a top loading electronic balance before the ing that the length of the right propodus was allometric in imma- eggs were fixed in 4% formalin. Three samples were taken from ture and mature, with a slightly positive value. Coefficient b for each egg mass, a general method followed by other workers (i.e., LPL and CL was found to be 1.34 for immature males and 1.04 Kumar et al., 2003; Rasheed & Mustaquim, 2010). The number of for mature males. These values were significantly different from eggs in these samples was counted in a counting tray under a ster- 1 (t = 21.13 for immature male and 5.87 for mature males; eomicroscope and the average number of eggs present in the three P < 0.05). The length of the left propodus, allometric in both samples was then calculated. The total weight of the egg mass was immature and mature males, was slightly positive. Males showed obtained by removing the eggs from the pleopods; the weight of positive allometric growth during both phases. the pleopod was taken and then subtracted from the weight of the The regression equations show positive gonopodal growth in whole egg mass. Fecundity was then calculated by the following both mature and immature phases (Table 1). The value of regres- formula (Kumar et al., 2003, Oliveira et al., 2005): sion coefficient b (Fig. 5) was significantly different from 1 for n immature (t = 32.43; P < 0.05) and mature individuals (t = 48.12; N =× W P < 0.05). w Where N = total number of eggs, or fecundity; W = total weight Sexual maturity of females of the egg mass; n = average number of eggs in the samples; w = average weight of the three egg samples. Sexual maturity in females was accompanied by a change in abdominal width (AW) and the relative changes in size of the pro- Statistical analysis podus length (PL) in relation to carapace length (CL). The size at which 50% of the females were morphologically mature (Fig. 2B) The statistical analysis was carried out using SPSS (Statistical was 13 mm (CL). The regression equations are given in Table 1. Package for the Social Science, Version 17) and Excel was used In the relationship between CL and right and left propodus length for the graphs. The data related to different variables were plot- of mature females (Fig. 6), the value of regression coefficient b ted in a scatter plot, in both linear regression and log-transformed was found to be 1.36 for RPL and CL and 1.09 for LPL and CL. state. Student’s t-test was used to test the statistical significance of These values were significantly different from 1 (t = 20.75 for the the observed values (Zar, 1995). In both cases the value of b allo- right chela and 21.33 for left; P < 0.05), showing that the growth cates the type of allometric growth. A value greater than 1 shows was positive (Figs. 6, 7). The regressions were computed separately a positive allometry (meaning that the organ in question is grow- for both mature and immature phases (Table1). The value b was ing faster than the body), whereas a value less than 1 indicates a significantly different from 1 for immature (t = 3.85; P < 0.05) and negative allometry with the organ growing slower than the body. mature individuals (t = 51.13; P < 0.05). The regression equations

Figure 2. Relationship between carapace length (CL) and percentage of adult males (A) and females (B) of Leptodius exaratus.

467 N. FAHIMI ET AL.

Table 1. Relationships between morphometric parameters and carapace length in Leptodius exaratus by means of the allometric technique; * t test, p < 0.05; a, coefficient of determination; b, regression coefficient (slope of the line); c, Student’s t-test when comparing the b value with 1; d, allometry level: (+) posi- tive and (–) negative allometry.

Y-Variable Group Size range Regression equation R2 ()a B(b) t(c) *Al(d)

Right propodus length (Rpl) Immature male < 8 mm Rpl = 0.734cl + 0.817 0.804 1.057 13.71 + logRpl = log0.189 + 0.783 logCL 0.840 Mature male > 10 mm Rpl = 1.106Cl – 1.868 0.914 1.036 5.77 + logRPL = log – 0.202 + 1.164logCL 0.929 Female 6–20 mm Rpl = 1.185Cl – 3.567 0.889 1.36 20.75 + logRpl = log – 503 + 1.417logCL 0.903

Left propodus length (Lpl) Immature male < 8 mm Lpl = 0.800Cl – 0.011 0.844 1.34 21.13 + Downloaded from https://academic.oup.com/jcb/article-abstract/37/4/465/3934667 by guest on 22 September 2019 logLpl = log – 0.159 + 1.073logCL 0.859 Mature male > 10 mm Lpl = 1.071Cl – 1.329 0.923 1.04 5.87 + logLpl = log – 0.164 + 1.133logCL 0.937 Female 6 – 20 mm Lpl = 1.027Cl – 1.41 0.889 1.09 21.33 + logLpl = log – 0.231 + 1.74logCL 0.899 Gonopod length (Gl) Immature male < 8 mm Gl = 0.453Cl – 1.145 0.879 1.25 32.43 + logGl = log – 1.113 + 1.691logCL 0.888 Mature male > 10 mm Gl = 0.403Cl + 0.312 0.861 1.47 48.12 + logGl = log – 0.385 + 1.010logCL 0.87 Abdomen width (Aw) Immature female < 6 mm Aw = 0.313Cl - 0.626 0.729 0.336 3.85 – logAW = log – 1.198 + 1.660logCL 0.850 Mature female 6–20 mm Aw = 0.390Cl – 0.413 0.880 1.99 51.13 + logAW = log – 0.371 + 0.929logCL 0.742

The size of the 100 ovigerous females that were used for count- ing the number of eggs varied from 9.48 mm to 21.86 mm CW. The number of eggs ranged from 600 to 9000, the number being generally greater in the larger individuals (Fig.10). The scatter plot shows a trend by power function on egg numbers and shows that the two variables, viz. carapace width and fecundity, are strongly correlated ( R2 = 0.800).

DISCUSSION The chelae of males and the abdomen in females are consid- ered secondary sexual characters in brachyuran crabs because of their functions in reproduction (Hartnoll, 1978). The secondary sexual development of the chelipeds helps male crabs in territo- rial defense, conflict, mating, and courtship as well as carrying and holding the female during copulation (Hartnoll, 2006, 2009). The setose pleopods in the abdomen of adult females form an incu- bation chamber for the developing eggs. The increase in relative growth of the male chelae and female abdomen at the puberty molt brings these structures to full functional size at sexual matu- rity (Rasheed & Mustaquim, 2010). The relative growth of chelae in males and abdomen in females has thus been used to deter- Figure 3. Relationship between carapace length (CL) and length of the mine size at which puberty molt occurs or functional maturity is right propodus (RPL) in male Leptodius exaratus. attained. Change in the length of the male first gonopod is consid- ered as the best external indicator of puberty molt. We observed show that the growth of AW in immature females was negative that the functional and physiological maturities in L. exaratus but positive in the mature ones (Fig. 8). occurred almost at the same size, which agree with the results in the same species by Watanabe et al. (1990), and in Platyxanthus Fecundity patagonicus (A. Milne-Edwards, 1879) by Carsen et al. (1996). Our results show that males and females attain full functional as well as The gonadal indices (GI) of males varied between 0 and 0.2 physiological maturity at 13 mm CL and 16 mm CL, respectively. (Fig. 9C). Males with high GI were found in all seasons except The size at which the xanthid crabs reach sexual maturity can during the winter months (December 2012 to February 2013). vary with location, depending on seasonal and annual variations Females showed higher GI during August 2012 to November 2012 in temperature and salinity (Fisher, 1999). The size of the smallest to (0–0.9: Fig. 9A). Ovigerous females showed increased GI values ovigerous female in this study was 9.6 mm and the largest female in May 2013 and August 2013 (0–0.8; Fig. 9B). was 20 mm CL. Watanabe et al. (1990) found that the smallest size

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Figure 4. Relationship between carapace length (CL) and left propodus Figure 7. Relationship between carapace length (CL) length of right pro- length (LPL) in male Leptodius exaratus. podus (RPL) in female Leptodius exaratus.

Figure 5. Relationship between carapace length (CL) and gonopod length Figure 8. Relationship between carapace length (CL) and abdominal in male Leptodius exaratus. width (AW) in female Leptodius exaratus.

of an ovigerous L. exaratus in Japan was 11.8 mm CW (range of 11.8–26.2mm CW). Their results show that females attain their maturity earlier than the males, whereas we found that males and females attained sexual maturity more or less at the same size. The proportion of the right and left propodus to the carapace length were positive in both mature and immature L. exaratus, which corresponds to values observed in other xanthoid crabs, such as Eriphia gonagra (Krauss, 1843) (Góes & Fransozo, 1997), Eurytium limosum (Say, 1818) (Guimarães& Negreiros-Fransozo, 2002), and M. nodifrons (Stimpson, 1859) (Bertini et al., 2007). This positive allometric growth is indicative that these structures have an important role in agonistic behaviors. The regression analysis of carapace length to gonopod length for L. exaratus showed positive allometric growth dur- ing the juvenile and adult phases. Our result for the juvenile phase (puberty molt occurring between 8 and 10 mm CL in males) is similar to values given by Góes & Fransozo (1997) for Eriphia gonagra and Bertini et al. (2007) for Menippe nodifrons. Figure 6. Relationship between carapace length (CL) and length of left This suggests that the noticeable positive allometry in the propodus (LPL) in female Leptodius exaratus. immature phase of L. exaratus could be an advantage in that

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Figure 9. Changes of gonadal indices in females (A), ovigerous females (B), and males (C) of Leptodius exaratus during sampling periods.

crabs (Hartnoll, 1965; Pinheiro & Fransozo, 1995; Fransozo et al., 2002). The ontogenic changes in the abdomen of female L. exara- tus are associated with the capacity of carrying their egg mass, fol- lowing the common pattern of most brachyuran species. Breeding seasons in brachyuran crabs are classified on the basis of the presence or absence of ovigerous females in the periods at which samples from the population are taken throughout the year. Individuals of L. exaratus in the studied areas were found oviger- ous all year round (with peak in August 2013), indicating a con- tinuous breeding, which agrees with data from Japan on the same species (Watanabe et al., 1990). Brachyurans inhabiting tropical waters usually breed throughout the year, which also applies to another xanthoid crab, Eriphia smithii (MacLeay, 1838) (Tomikawa Figure 10. Relationship between fecundity and carapace width (CW) in & Watanabe, 1992), the majid Tiarinia cornigera (Latreille, 1825) in Leptodius exaratus. Japan (Tsuchida & Watanabe, 1991), and the portunid Thalamita pelsarti (Montgomery, 1931) (Norman et al., 1996), all in Japan. Body size is the principal determining factor of fecundity in males could reach sexual maturity at a smaller size than in brachyuran crabs (Hines, 1989), and in L. exaratus as in most other the females, allowing males to successfully compete with other xanthid crabs thus far investigated (Watanabe et al., 1990; Carsen males in efforts to copulate with the mature females (Bertini et al., 1996; Litulo, 2005), fecundity was highly correlated with et al., 2007). body size. The number of eggs attached to the pleopods of L. The regression analysis of carapace length to abdominal width exaratus was found to vary from 600 to 9000. The fecundity of L. in female L. exaratus showed negative allometric growth during exaratus as estimated in this study was relatively lower when com- the juvenile phase and positive for the adult phase. This allomet- pared with that of other xanthids of similar body-size range (9.6 ric growth is often used to identify the puberty molting in female to 20 mm CL): 610 to 10,110 (body size 11.80–26.20 mm CW) in 470 REPRODUCTIVE BIOLOGY OF LEPTODIUS

L. exaratus (Watanabe et al., 1990); 3,800–20,300 (body size 15.00– Góes, J.M., Fransozo, A. & Fernandes- Góes, L.C. 2005. Fecundity of 29.50 mm CW) in Paraxanthias taylori (Stimpson, 1861)in California Eriphia gonagra (Fabricius, 1781) (Crustacea, Brachyura, Xanthidae) in (Knudsen, 1960); 15,000–30,000(body size 5.80–25.00 mm CW) the Ubatuba region, Sao Paulo, Brazil, State of São Paulo. Nauplius, in Neopanop sayi (Smith, 1869) in Virginia, USA(Swartz, 1978); 13: 127–136. 5,300–73,500 (body size 25.00–53.00 mm CW) in Eriphia smithii in Góes, J.M. & Fransozo, A. 1997. Relative growth of Eriphia gonagra (Fabricius, 1781) (Crustacea, Decapoda, Xanthidae) in Ubatuba, State Japan (Tomikawa & Watanabe, 1992); and 3,000–113,000 (body of São Paulo. Nauplius, 5: 85–98. size 23.00–43.00 mm CW) in Panopeus herbstii (H. Milne Edwards, Guimarães, F.J. & Negreiros-Fransozo, M.L. 2002. Sexual maturity of 1834) in South Carolina, USA (McDonald, 1982). Eurytium limosum (Say,1818) from a subtropical mangrove in Brazil. Fecundity can also vary with environmental conditions, includ- In: Modern approaches to the study of Crustacea (E. Escobar-Briones & F. ing temperature, which is particularly important (Fisher, 1999). Alvarez, eds.), pp.157–161. Kluwer Academic/Plenum, New York. Because temperature has an important effect on the other physi- Hartnoll, R.G. 1965. Notes on the marine grapsid crabs of Jamaica. ochemical parameters of water, the changes of these parameters Proceedings of the Linnean Society of London, 176: 113–147. are dependent on temperature amplitude (de Lestang et al., 2003). Hartnoll, R.G. 1978. The determination of relative growth in Crustacea. Crustaceana, 34: 281–293. The relatively lower fecundity of L. exaratus observed in this study Downloaded from https://academic.oup.com/jcb/article-abstract/37/4/465/3934667 by guest on 22 September 2019 Hartnoll, R.G. 1982. Growth. In: The biology of Crustacea, Volume 2: could probably be attributed to the relatively higher temperatures Embryology, morphology, and genetics (D.E. Bliss & L.G. Abele, eds.), pp. in the Persian Gulf, with a typical surface temperatures of approx- 111–196. Academic Press, New York. imately 33 °C on average in summer and even reaching > 35°C in Hartnoll, R.G. 2006. Reproductive investment in Brachyura. Hydrobiologia, the shallow basins (Reynolds, 1993). Somatic growth rate increases 557:31–40. with temperature, and therefore energy needed to produce eggs is Hartnoll, R.G. 2015. Postlarval life histories of Brachyura. In: Treatise on lower than in low temperatures (Diaz, 1980). Furthermore, reduc- Zoology - Anatomy, , Biology. The Crustacea (P. Castro, P.J.F. Davie, tion in energy for egg production may result from the inability of D. Guinot, F.R. Schram & J.C. von Vaupel Klein, eds.), vol. 9C-1, pp. females to mobilize sufficient food reserves to keep pace with the 375–416. Brill, Leiden & Boston. increased number of broods produced under high compared with Hartnoll, R.G. 2009. Sexual maturity and reproductive strategy of the rock crab Grapsus adscensionis (Osbeck, 1765) (Brachyura, Grapsidae) on lower temperatures (Wear, 1974). Although the water temperature Ascension Island. Crustaceana, 82: 275–291. is considerably higher in the summer, most evaporation occurs in Hines, A.S. 1989. Geographical variation in size at maturity in brachyuran the winter due mainly to higher wind speeds, which might sup- crabs. Bulletin of Marine Science, 45: 356–368. press egg production or increase loss during incubation, as envi- Kneib, R.T. & Weeks, C.A. 1990. Intertidal distribution and feeding habits ronmental factors, high temperature and salinity as high as 48‰ of the mud crab, Eurytium limosum. Estuaries, 13: 462–468. (Coles, 2003), can affect the biology and life cycle of the species Knudsen, J.W. 1960. 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