Limnologica Reproductive Traits of the Freshwater Shrimp Caridina

Limnologica 41 (2011) 244–248

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Limnologica

journal homepage: www.elsevier.de/limno

Reproductive traits of the freshwater shrimp Caridina fossarum Heller, 1862 (Decapoda, Caridea, Atyidae) in the Ghomp-Atashkedeh spring (Iran)

Parviz Zare a,∗, Mojtaba Naderi b, Hamidreza Eshghi c, Chryssa Anastasiadou d

a Department of Fisheries, Faculty of Fisheries and Environmental sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran b Islamic Azad University, Bandar Abbas branch, P.O. Box: 79158-93144, Iran c Department of Fisheries, Faculty of Natural Resources, University of Zabol, Zabol, Iran d Laboratory of Zoology, Department of Biological Applications and Technology, University of Ioannina, GR-451 10 Ioannina, Greece

article info abstract

Article history: In the present study, some biological traits of Caridina fossarum reproduction are studied in the Ghomp- Received 19 November 2009 Atashkedeh spring (Fasa, Shiraz, Iran), for the first time. This Iranian endemic freshwater species was Received in revised form 21 October 2010 studied from April 2007 to March 2008. Minimum sexable size (MSS) and absolute or relative size at the Accepted 17 November 2010 onset of maturity (SOM and RSOM) in terms of carapace length (CL) was found to be 2.4 mm, 4.3 mm and 55%, respectively. Sex ratio showed variations on a monthly basis. Sex reversal is a possible scenario Keywords: for C. fossarum because the size-specific sex ratio revealed a reverse pattern. Based on the proportions of Caridina fossarum ovigerous females, the main breeding season was determined to be from April to August, demonstrating a Maturity size ◦ Fecundity peak during early spring. There is a period of extended recruitment at water temperatures above 20 C. The Sex ratio size at which 50% of females are mature was estimated at CL = 5.03 mm from the proportion of ovigerous Sex reversal females during the breeding season. The pleopodal egg number varied from 3 to 75 eggs per female with a mean value 34.39 ± 14.27. The results showed that although there is a significant relationship between carapace length CL and pleopodal egg number, it is not the most important factor affecting potential fecundity in C. fossarum due to the low values of slope (= 1.51) and determination coefficient (= 0.052). © 2011 Elsevier GmbH. All rights reserved.

Introduction distribution analyses are necessary for an improved parameteriza- tion of both maturation and of the spawning processes of species Reproduction is one of the important aspects in both ecology and (Temming and Damm 2002; Siegel et al. 2008). Finally, the study of biology of species. In crustaceans, it is frequently expressed in terms the size at maturity of the various species is an important predictor of fecundity (Anger and Moreira 1998). Fecundity is related directly of the overexploitation risk (Reynolds et al. 2005). to species life strategy (Oh and Hartnoll 2004) and is of essential Family Atyidae is represented by three species, which have been importance in order to estimate the reproductive potential and reported from Iranian freshwater lotic and lentic habitats. These are the future stock size of a given species or population (Mori et al. Caridina fossarum Heller, 1862, C. babaulti Bouvier, 1981 and Atyae- 1998; Figueiredo et al. 2008). Furthermore, due to the variation in phyra desmarestii Millet, 1831 (Heller 1862; Gorgin 1996). Till now, the periods of fecundity or the fecundity dynamics among species, all the available published information has focused on taxonomic the possibility of coexistence among species is increasing (Nazari investigations and zoogeographical distribution (Heller 1862; et al. 2003). More specifically, the female size–fecundity relation- Gorgin 1996; Karami and Gorgin 2000). Moreover, ecological and ship is useful not only for conversions, but also for life-history biological data for the atyid shrimps of the Iran are totally lacking. comparisons among species and populations. The absolute (SOM) C. fossarum is an endemic species of the Iranian surface and or relative sizes (RSOM) at the onset of maturity (Wenner 1985; subterranean freshwaters, which inhabits highland ecosystems Chamov 1990) are considered as key life-history parameters that (300–1600 m above the sea level) (Karami and Gorgin 2000). reflect the longevity and life-time investment of species (Anger and High abundances have been observed in lentic habitats, which are Moreira 1998). Additionally, a comprehensive understanding of the characterized by rich aquatic vegetation. The body color of the sex ratio and the fraction of ovigerous females in size frequency species varies from green, yellow, red, grey, transparent to black. C. fossarum is usually used as an aquarium shrimp. Up until now, the species has received little interest and study. The main objective of the present study is to investigate the reproductive biology of C. fossarum, providing for the first time new information on the ∗ Corresponding author. Tel.: +98 917 375 0490. reproductive period, the sex ratio, females size at maturity and E-mail address: zare [email protected] (P. Zare). finally on fecundity.

Fig. 1. Map showing the location of Ghomp-Atashkadeh spring in Iran.

Materials and methods follows: = × L∞−1 Study site – sampling RSOM SOM where L∞ is the asymptotic carapace length of the von Bertalanffy Qhomp-Atashkadeh spring (Fig. 1) is located 20 km northern growth equation. Size and period specific sex ratio of C. fossarum ◦ ◦ of Fasa city (29 08 41 N, 53 37 23 E) between Toodaj and Khar- was also studied. Chi-square test was used to examine differences man mountains and is about 1523 m above the sea level. It is a in the male and female abundance through the sampling period, on permanent shallow spring with a maximum depth of 2.5 m and a the monthly base. 2 total surface area of about 3 km . From a hydrological viewpoint, Fecundity was derived directly from the number of bearing eggs the spring inflows are influenced by the annual precipitation and for each ovigerous female. In order to determine the relationship ◦ ◦ snowfall. Water temperature ranges from 13 Cto15 C during win- between egg number and body length the following equation was ◦ ◦ ter and from 19 Cto22 C during spring and summer. Rocks are used: calcareous and the substratum is sandy. Samples were taken on a b monthly base, from April 2007 to March 2008. The specimens were Y = aX , collected from a depth of 0.8 m by means of a hand net with a mesh where y is pleopodal egg number, x is carapace length, a is intercept size of 1 mm. The shrimps were preserved in 4% neutralized for- and b is considered a constant rate of increase. For the relationship malin solution and then transferred to the laboratory for further carapace length–fecundity the pattern of allometry was established analysis. for both species by the b-value slope (b = 3, isometry; b < 3, negative allometry, b > 3, positive allometry). Furthermore, the size of 50% of the ovigerous females was estimated as well as the % of Laboratory analysis – data processing the ovigerous females for the size distribution during the breeding period. For estimating length at sexual maturity of female shrimps, The sex was identified through microscopic inspection of the the following equation was used: endopod’s shape of the first pleopod and the presence/absence of appendix masculina of the second pleopod. Carapace length P = 1 , (CL) was measured using Vernier digital calliper (±0.01 mm), from 1 + exp[a + b CL] the orbit to the mid-dorsal posterior edge of the carapace. Total where p is the predicted mature proportion, a and b the estimated weight (TW) was estimated to the nearest 0.01 g using an electronic coefficients of the logistic equation, and CL is the carapace length. balance. Damaged individuals were discarded. Individuals’ size at Size at sexual maturity (CL50), corresponding to a proportion of 0.5 onset maturity (SOM), relative SOM (RSOM) and minimum sexable sexually mature individuals, was estimated as follows: size (MSS) were estimated for the collected specimens. Individuals a with smaller size than MSS, which were morphologically similar to CLm =− young females, were counted as females. RSOM was calculated as b 246 P. Zare et al. / Limnologica 41 (2011) 244–248

Table 1 Sample size, ranges of carapace length (CL, mm) and total weight (TW, g), and size at maturity (SOM-CL and SOM-TW) according to CL and TW, respectively, by biological category. NI: number of individuals.

Biological category NI CL (min–max) (mm) TW (min–max) (g) SOM-CL (mm) SOM-TW (g)

Males 333 2.4–6.2 0.03–0.2 – – Females 533 2.2–7.2 0.02–0.32 – – Females ovigerous 94 – – 4.3 0.11

100 * 90 * Results * 80 C. fossarum CLs were varied from 2.2 to 7.2 mm and TWs from 0.2 70 ** to 0.32 g (Table 1). The species females and males were found with 60 Female CLs ranging from 2.2 to 7.2 mm and from 2.4 to 6.2, respectively. 50 * Male According to the TWs, male individuals ranged from 0.03 to 0.2 g 40 * while female individuals weighted between 0.02 and 0.32 g. Size at 30 * the onset of maturity (SOM) in terms of CL and TW was determined 20 * Number of individuals (%) * to be 4.3 mm and 0.11 g, respectively (Table 1). RSOM in terms of 10 CL obtained the 55% for C. fossarum species. MSS is not necessarily 0 identical to male SOM. In our study, only one individual was found > 3.5 3.5-4.0 4-4.5.0 4.5-5.0 5-5.5 5.5-6.0 6 < to be smaller than the smallest identifiable male. The asymptotic Length range (mm) carapace length (CL∞) of the modified von Bertalanffy growth equation (VBGE) was estimated at 7.8182 mm by the ELEFAN analysis of Fig. 3. Sex ratio of C. fossarum in relation to size classes (stars show significant length frequency data for female’s data. difference). In order to study the size at sexual maturity, a total of 240 female specimens of C. fossarum, 130 of which were sexually mature, were used. Fig. 2 shows the proportion of sexually mature higher than that of females. Sex ratio at size class 4–5 mm for the females within each size class. The relationship between carapace CL did not demonstrate any significant difference. For the speci- length (CL) and the proportion of mature females (P) was calcu- menswithCL>5mm(Fig. 3), females dominated significantly when lated by fitting a logistic function to the size-specific maturity data, compared to males. Ovigerous females have been recorded from P = 1/(1 + exp[8.339 − 1.657CL]) (r2 = 0.91, P < 0.001). Size at which April to October (Fig. 4). Higher percentage sample representation 50% of females are mature was estimated at 5.03 mm ± 0.48 mm. of ovigerous females has been measured in April (86.67%) while the lower percentage in October (1.64%). During summer months, the Sex ratio female species population is characterized almost by 50% of berried females. Ovigerous females CLs ranged from 4.3 to 6.6 mm. The sex ratio variation by month and size is presented in Figs. 3 and 4, respectively. A total of 877 specimens were measured for the sex ratio study. Of these, 541 were females (61.69%) and Fecundity 366 were males (38.31%). Total sex ratio was estimated at 1.61, 1, which is not far away from the theoretical one 1, 1. A chi-square The mean pleopodal egg number was 34.39 (S.D. = 14.27), with a test revealed that the number of females was significantly higher range of 3 at CL = 5.3 mm to 75 at CL = 5.8 mm. In the present study, than that of males (2 = 47.92, P < 0.0001). Females are dominant the potential fecundity was related to carapace length and body from April to August (P < 0.05) while during autumn and winter wet weight (P < 0.05). The relationship between female size versus the sex ratio was estimated to be near 1, 1 (P > 0.05). For the small pleopodal egg number is given in Fig. 5. The results show that there size groups (CL < 4 mm) the proportion of males was significantly was the negative allometry in the relationship CL/NEggs of C. fossarum, because the slope is smaller than 3 (1.5155). However, there is an increase of NEggs following the increase of carapace length (Table 2). Additionally, high variability in NEggs was recorded for similar body sizes (Table 2).

Fig. 2. Logistic function ﬁtting the proportion of mature C. fossarum females to carapace length from breeding season survey data. a ± S.E. = 8.339 ± 1.97, Fig. 4. Monthly variations in sex ratio of C. fossarum. M, males; OF, ovigerous 2 b ± S.E. = −1.657 ± 0.37, r = 0.91, and CL50 = 5.03. females; NOF, non-ovigerous females. P. Zare et al. / Limnologica 41 (2011) 244–248 247

sex reversal of the species individuals mainly when a scarcity of females occurs in the population (Wenner 1972). Despite this ini- tial assumption for C. fossarum, it cannot be ruled out. Laboratory experiments and gonadal histology may help to elucidate this the- ory. Our data show that the growth rate of males was lower than that of females. This should lead to a sex ratio skewed in favor of males (Berglund 1981). However, this was not observed in our data (Table 2). Variation in sex ratio may also be explained as differential mortality or migration pattern between sexes (Oh et al. 2002). As far as concerns the breeding season, C. fossarum was mainly restricted to the wet season, having a decrease of ovigerous females at low temperatures. Similar patterns have been reported for the atyid shrimp (Dudgeon 1985; De Silva 1988; Johnson et al. 1998; Yam and Dudgeon 2005). In a variety of crustacean species, temper- Fig. 5. The relationship between log carapace length and log pleopodal egg number ature, day length, and food condition are the major environmental in C. fossarum. factors of the reproductive cycle (Sastry 1983). Yam and Dudgeon (2005) noted that the increase in temperature coincides with the Discussion reproductive period of atyids shrimps in tropical fresh waters. Fecundity is a phenotypic characteristic that is affected by The present paper is aimed at elucidating the biological traits numerous factors and intensities by specific features of differ- of the reproduction of the Iranian endemic freshwater shrimp C. ent environments (Hines 1991) and directly influenced by natural fossarum. The species reproduction is studied for the first time, giv- selection (Stearns 1977). The maximum fecundity of C. fossarum ing the opportunity to make useful comparisons with the other was higher than that of C. cantonensis and C. serrata, although species of the genus (Hart 1981; Yam and Dudgeon 2005). The data mean length of C. fossarum was smaller than them. However, when of our present study reveal that MSS and SOM values are the smaller compared with Caridina nilotica, fecundity was much lower in C. recorded values till now for the genus Caridina (Yam and Dudgeon fossarum. The results also showed that although the increase in 2005). More specifically, C. fossarum was 15–26% smaller than other the mean pleopodal egg number follows the increase in carapace species of the genus. C. fossarum RSOM was identical with 55%, a length, it is not the most important factor which affects the poten- percentage which is typical for the Crustacea group (Chamov 1990). tial fecundity of C. fossarum because the slope was smaller than The size where 50% of the specimens are mature was measured at 3. The correlation analyses showed that r2 (log CL/NEggs) value CL = 5.03 mm. Since the “maturity” classification is based only on was very low in C. fossarum. This was attributed to the high vari- the presence of the attached eggs, it should rather be termed as ability of individual fecundity of this species. Although clutch size “apparent maturity”. In comparison to the crangonid species, e.g. P. is highly correlated with the size of individuals in malacostracan trispinosus, 50% of mature individuals arises in considerably smaller crustaceans (Corey and Reid 1991; Chockley and Mary 2003), C. sizes, CL = 3.7 mm (Oh and Hartnoll 1999). fossarum fecundity does not seems to be correlated strongly to The sex ratio in C. fossarum population was in favor of females, female CL, due to low values of slope and correlation coefficient. The with a total sex ratio of 1.61, 1 (female, male). Similar sex ratios difference in the maximum fecundity and length–fecundity rela- have been observed also in other atyids (Yam and Dudgeon 2005), tionship among species is affected by a number of factors including and related caridean families (Guerao et al. 1994; Oh et al. 2002; body length, length and volume of the abdomen, length of the Fransozo et al. 2004; Mantelatto and Barbosa 2005). According to pleopods, egg mortality, number of spawns in a single reproductive Fransozo et al. (2004), this fact may characterize a restructuring of period, food availability, environmental factors, latitudinal distri- the group in terms of total abundance, in order to increase the num- bution and adaptation to habitat (Annala 1991; Corey and Reid ber of recruits via reproduction. While Kim et al. (2008) obtained 1991; Mantelatto and Fransozo 1997; Oh and Hartnoll 1999; Oh a larger number of males in the population of Palaemon pauci- et al. 2002). These factors except female length were not considered dens. The sex ratio was reserved with more females’ C. fossarum in the present study. than males caught during the peak breeding season. This could be attributed to the fact that there is a constant strategy for the reproductively mature females of many species to increase their References abundance during reproductive periods. In the early life stages, the number of males was higher than females (Fig. 3), while the Anger, K., Moreira, G.S., 1998. Morphometric and reproductive traits of tropical abundance of females in late life stages increases. This may suggest caridean shrimps. J. Crustac. Biol. 4, 823–838. Annala, J.H., 1991. Factors influencing fecundity and egg production of Jasus species. In: Wenner, A., Kuris, A. (Eds.), Crustacean Egg Production. A.A. Balkema, Rot- terdam, pp. 301–315. Table 2 Berglund, A., 1981. 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Studies on Atyidae (Decapoda, Caridea) of Sri Lanka IV. Some 94 4.3–6.6 34.39 (14.27) aspects of the population ecology of the endemic freshwater shrimp Caridina pristis Roux, 1913. Crustaceana 54, 225–243. log ab(±S.E.) R2 F-Value P-Value Dudgeon, D., 1985. The population dynamics of some freshwater carideans (Crus- tacea, Decapoda) in Hong Kong, with special reference to Neocaridina serrata CL/NEggs 0.3869 1.5155 (±0.67) 0.0522 5.063 0.0268 (Atyidae). Hydrobiologia 120, 141–149. 248 P. Zare et al. / Limnologica 41 (2011) 244–248

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