Reproductive parameters of the southern stingray Dasyatis americana in southern gulf of Mexico/Parametros reproductivos de la raya latigo americana Dasyatis americana en el sur del golfo de Mexico.
The southern stingray Dasyatis americana (Hildebrand & Schroeder, 1928) is distributed from New Jersey to Florida in United States, throughout the gulf of Mexico, Bahamas, and the Greater and Lesser Antilles, and bordering the northern coast of South America to southeastern Brazil (McEachran & de Carvalho, 2002). It inhabits shallow waters and feeds on bottom-dwelling invertebrates, mainly bivalves and worms (McEachran & de Carvalho, 2002). Although frequently captured near shore, this species is also found in estuaries and rivers (McEachran & Fechhelm, 1998). D. americana is abundant on sandy bottoms of the inner shelf of the gulf of Mexico (Castro-Aguirre & Espinoza-Perez, 1996). In the western Campeche Bank, in southern gulf of Mexico, D. americana is the most frequently landed among elasmobranch species, with mean landings of 1.400 ton per year in the state of Campeche according to the statistics from the regional office of SAGARPA (Secretaria de Agricultura, Ganaderia, Desarrollo Rural, Pesca y Alimentacion, 2010).
This species reaches a maximum disc width of 1520 mm (Bigelow & Schroeder, 1953). Females and males mature at 750-800 and 510 mm DW, respectively, young are 170 to 180 mm DW at birth (Bigelow & Schroeder, 1953) and fecundity range from 3 to 5 (McEachran & de Carvalho, 2002). D. americana, as the other dasyatid rays, display aplacental viviparity with trophonemata (Hamlett et al., 1996).
Reproductive parameters estimated for D. americana in captivity, showed a biannual reproductive cycle, a gestation period of 4.4-7.5 months, a fecundity of 2-10 with a linear relationship with maternal disc width, size at birth 200-340 mm disc width, and 1:1 sex ratio for neonates (Henningsen, 2000). However, an annual reproductive cycle has been observed on wild specimens from Florida and Virginia waters (Grubbs et al., 2006).
The determination of reproductive parameters are needed for assessment of elasmobranch populations by means of demographic analysis or ecological risk assessments due to the lack of time series of catch and fishing effort by species in Mexican official catch statistics. For example, Smith et al. (2008) developed age-structured demographic models for Dasyatis dipterura from the Mexican Pacific coast, concluding that this species has low intrinsic growth potential and limited resilience to fishing pressure.
D. americana is classed as Data Deficient by the International Union for Conservation of Nature, because the status of their populations is unknown and there is a lack of life history parameters throughout most of its range (Grubbs et al., 2006). Mexican fisheries for elasmobranchs have been managed since 2007 by the Mexican Official Standard NOM-029 PESC-2006, Responsible Fisheries of Sharks and Rays, Specifications for their Use (Poder Ejecutivo Federal, 2007) and available information from the Atlantic coast of Mexico indicates that landings of batoids have been declining since the late 1990's (Poder Ejecutivo Federal, 2006), which indicates that the intrinsic growth potential of the population of D. americana must be assessed to determine its vulnerability to fishing pressure. Objectives of the present study were to determine the reproductive parameters for D. americana in the southern gulf of Mexico needed to develop, in the near future, age-structured or stage-based demographic models.
MATERIALS AND METHODS
A total of 900 specimens were examined from February 2006 to December 2008. Rays were obtained from commercial catches of the small-scale fleet from San Pedro, Tabasco, in the southern gulf of Mexico (Fig. 1). Bottom-set longlines with 60 mm shank-length tune circle hooks were the primary method of capture. The catch depth ranged from 10 to 40 m.
Disc width (DW) was measured between the tips of the widest portion of the pectoral fins (McEachran & de Carvalho, 2002). All rays were measured and examined to quantify reproductive parameters. Maturity was assessed macroscopically for both sexes. Maturity in males was assessed by the extent of clasper calcification (Clark & Von Schmidt, 1965) and testes development (Snelson et al., 1988). Claspers were measured from the point of insertion at the cloaca to the tip of claspers. Males were assigned to one of two stages as follows: 1) immature, testes and claspers undeveloped; 2) mature, claspers fully developed, exceeding the posterior edge of the pelvic fins, presented hardened internal structure and, could be rotated toward the anterior part without bending (Clark & Von Schmidt, 1965), and had enlarged testes with prominent lobes (Snelson et al., 1988).
Maturity in females was determined by the onset of first ovulation (Walker, 2005). Follicle diameter of the largest cohort in the ovary and the width of the left uterus were measured. In uteri, the trophonemata development, presence of uterine milk, uterine eggs and embryos were recorded. Uteri were examined to determine if embryos or uterine eggs were present. When present, the sex and DW of embryos was recorded.
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Females were assigned to one reproductive status as follows: 1) immature, no ovarian development or if developed, there was no vitellogenic activity (follicles <25 mm diameter), uterus thin (<46 mm width) with trophonemata not well developed (<5 mm in length, thin and pale); 2) non-gravid mature, medium to large follicles (15-34 mm diameter) in the ovary, some with vitellogenic activity, wide uterus (23-47 mm), with trophonemata well developed and vascularized (>5 mm in length); 3) gravid, embryos in uterus, with medium to large follicles in the ovary (7-40 mm diameter).
Logistic models were used to estimate median disc width at maturity ([DW.sub.50]) according to Mollet et al. (2000) by fitting the logistic model Y = [[1 + [e.sup.-(a+bX)]].sup.-1] to the binary data of maturity (immature = 0, mature = 1). Because of the asynchronous nature of the reproductive cycle of females, the methods described by Braccinni et al. (2006) were used to determine the gestation period and the ovarian cycle. The time series of the disc width of embryos were analyzed to determine the gestation. Gravid females were assigned to one of seven categories based on the size of the embryos they carried: 1) [less than or equal to]59 mm DW, 2) 60-89 mm DW, 3) 90-119 mm DW, 4) 120-149 mm DW, 5) 150-179 mm DW, 6) 180-209 mm DW and, 7) [greater than or equal to]210 mm DW. The length of the gestation period was determined following the growth of embryos of different classes or cohorts through the time, based on the assumption that embryos from different cohorts have the same growth pattern (Braccinni et al., 2006).
To determine if ovarian cycle and gestation were concurrent or consecutive, correlation analysis was performed to assess possible relationships between follicle diameter and embryo size. The method of Braccinni et al. (2006) may be used to determine the ovarian cycle if the gestation and the ovarian cycle run concurrently. To estimate the ovarian cycle, the time series of the follicle diameter of gravid females was analyzed. Follicle diameter from the same subset of data selected for the gestation period analysis (seven categories of gravid females based on the size of embryos) was used to estimate the length of the ovarian cycle. The length of the ovarian cycle was determined following the growth of follicles of different classes or cohorts through the time, based on the assumption that the diameter of follicles from different cohorts has the same growth pattern (Braccinni et al., 2006).
The disc width range at birth was estimated based on the disc width of the largest embryo examined and the smallest free-swimming ray recorded. To determine the fecundity, the total number of embryos was counted. The null hypothesis of a sex ratio 1:1 of embryos was tested with the chi-square procedure with Yate's correction for continuity (Zar, 1984). The relationship between maternal DW and the number of embryos was plotted and fitted to a simple linear regression model.
A total of 494 females ranging from 340 to 1640 mm DW (mean = 766.5 [+ or -] 152.5) and 406 males 400-1100 mm DW (mean = 613.3 [+ or -] 69.3) were analyzed. In females, the disc width at which 50% of the population was mature was 764 mm ([DW.sub.50], 95% CI: 756-772 mm) (Fig. 2), with 288 mature and 206 immature females recorded. The smallest mature female measured 650 mm DW, had abundant uterine milk, follicles 32 mm diameter and uterus 34 mm width, and the largest immature female measured 960, had follicles 15 mm diameter and uterus 29 mm width. In males, the disc width at which 50% of the population was mature was 517 mm ([DW.sub.50], 95% CI: 510-523 mm) (Fig. 2), with 373 mature and 33 immature males recorded. The smallest mature male measured 490 mm DW (calcified claspers: 130 mm length), and the largest immature male measured 670 mm DW (partially calcified claspers: 120 mm length).
The time series of the embryos disc width (Fig. 3a) showed the asynchronous nature of the reproductive cycle of D. americana. The gestation lasts approximately 7-8 months. The development of embryos was traced following three cohorts through time (Figs. 4a and 4b). A first cohort could be traced from early October 2006 to late May 2007 (Fig. 4a); a second cohort from early February to late September 2008; and a third cohort from early July 2008 to late January 2009 (Fig. 4b).
The ovarian cycle could not be determined because this period does not occur concurrently with the gestation period, and the asynchronous nature of the reproductive cycle prevents it by analyzing the time series of follicle diameter of non-gravid mature females. The follicle diameter of gravid females does not show a relationship with the categories of gravid females (based on the size of the embryos they carried), as would be expected if gestation and the ovarian cycle were concurrent (Fig. 3b).
Although the correlation between the disc width of embryos and follicle diameter was significant, the degree of association is weak (r = 0.49, P < 0.001), because there exist a large variability, and only some gravid females containing full term embryos (>175 mm DW) had large follicles (Fig. 5). Therefore, the ovarian cycle and gestation were consecutive, the follicles and embryos do not develop at the same time. Apparently, however, the follicle development begins towards the end of gestation and follicles continue growing after the 7-8 months of gestation. If it is assumed that the ovarian cycle continues several months after parturition, then it could be hypothesized that females of D. americana reproduce annually.
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Disc width at birth was 230-340 mm. Fecundity ranged from two to seven embryos (mean = 2.5 [+ or -] 0.99). The 74.6% of gravid females carried two embryos. The most frequent number of follicles in gravid females was also two (30% of females). As the maternal DW increased, fecundity also increased (fecundity = 0.004 DW-1.41, [r.sup.2] = 0.46, [F.sub.1,9] = 46.99, P < 0.001) (Fig. 6). In total, 77 females and 79 males embryos were recorded, resulting in a sex ratio not significantly different from 1:1 (chi-square = 0.03, P > 0.05).
[FIGURE 5 OMITTED]
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Before this study, nothing was known about the reproductive parameters of D. americana in the gulf of Mexico. Disc width at maturity for females and males, estimated in the present study, was similar to that documented by Bigelow & Schroeder (1953) and MacEachran & de Carvalho (2002) for specimens collected from northwestern to southwestern Atlantic, and also similar to that estimated by Henningsen & Leaf (2010) for captive specimens (Table 1). However, because it is unclear if the criteria to determine maturity used by Bigelow & Schroeder (1953) and McEachran & de Carvalho (2002) was the same of that used in the present study, we recommend that a future study that uses the same criteria to determining the disc width at maturity among regions should be carried out to test for regional differences.
Gestation periods are slightly longer in wild (7-8 months) than in captive specimens (4.4-7.5 months) (Table 1). The difference is probably associated with environmental conditions, in particular temperature. Mahon et al. (2004) documented that gestation in captive spotted eagle ray, Aetobatos narinari, is related to water temperature, being longer at lower temperatures (11-12.5 months at 19.8-29.4[degrees]C) than at higher temperatures (6-6.2 months at 28.1-30.1[degrees]C). Temperature was not provided by Henningsen (2000), however, Henningsen & Leaf (2010) indicate that temperature was maintained at 24-25[degrees]C in their study. Surface temperatures ranges between 23.9-28.7[degrees]C in the western Campeche Bank (Cuevas-Zimbron et al. 2011) and are closely similar to the northern Campeche Bank where they fluctuate between 23.5-29.5[degrees]C, while bottom temperatures, in the second region, ranges between 22.9-24.5[grados]C (Pineiro et al., 2001). If the same bottom temperatures were observed in the western Campeche Bank, specimens of D. americana are apparently exposed to slightly lower temperatures in the wild, which could explain that gestation is longer in wild specimens. Henningsen et al. (2004), indicate that temperature has an effect on gestation, decreasing with an increase in temperature, such as occurs in A. narinari (Mahon et al., 2004).
Gestation ranges from 3 to 12 months in wild specimens and from 2 to 7.5 months in captive specimens of dasyatids (Table 2). D. americana from the southern gulf of Mexico (present study) is among dasyatids (D. centroura, D. chrysonota, D. longa and D. sayi) with gestation of 8 months or longer. In addition, D. americana has the longest gestation period (4.4-7.5 months) reported for captive dasyatid rays (Table 2). According to Henningsen et al. (2004) the temperature may have a profound effect on development. So, variation in gestation could be linked to this variable, as have been reported for captive specimens (Henningsen et al., 2004; Mahon et al., 2004). Comparisons of the differences in the length of gestation among species in wild specimens is difficult because a detailed characterization of the habitat is needed for every species.
Reproductive cycle of D. americana differs among wild (annual) and captive specimens (biannual). Grubbs et al. (2006) suggest an annual cycle of reproduction for wild specimens of D. americana in Florida and Virginia, eastern coast of USA. An annual cycle of reproduction has also been documented for other dasyatids, such as D. sayi, D. sabina and D. chrysonota (Snelson et al., 1989; Johnson & Snelson, 1996; Ebert & Cowley, 2008). The biannual reproductive cycle for wild specimens has been suggested for two species only, D. marianae and D. guttata (Yokota & Lessa, 2007), and for captive specimens, it has been determined for three species, D. americana, D. kuhlii and Pteroplatytrygon violacea (Henningsen, 2000; Mollet et al., 2002; Janse & Schrama, 2009). An uncommon triannual cycle of reproduction among elasmobranchs has been suggested for D. marmorata in wild specimens (Capape & Zaouali, 1995), however, the authors do not explore the possibility of an asynchronous reproductive cycle for this species, in which case, a different methodology must be used, such as the proposed by Braccinni et al. (2006).
Differences in the reproductive cycle between captive and wild specimens are well documented for elasmobranchs (Henningsen et al., 2004). In captive animals, Henningsen et al. (2004) indicate that several species were observed to mate immediately following parturition, whereas a longer gap it is observed in the wild (as is the case of D. americana). In addition, the effect of some environmental variables (e.g. temperature) should be explored in future studies to explain for differences among species.
The reproductive cycle is synchronous in several dasyatid species, D. sayi, D. sabina, D. marianae, D. guttata and D. chrysonota (Snelson et al., 1989; Johnson & Snelson, 1996; Yokota & Lessa, 2007; Ebert & Cowley, 2008). The asynchronous reproductive cycle has been determined for D. americana (present study), D. kuhlii, D. zugei, Himantura walga (White & Dharmadi, 2007) and P. violacea (Veras et al., 2009). In sharks, females are asynchronous in some species inhabiting tropical waters, where stable environmental conditions and abundant food throughout the year allow reproduction and birth to occur year around (Castro, 2009). The species of dasyatids inhabits tropical waters, which could explain that the asynchronous reproductive cycle is very common in these elasmobranchs.
Ovarian cycle and gestation were consecutive for D. americana in the wild (present study) and concurrent in captive environment (Henningsen, 2000). Also, in D. sabina has been determined that vitellogenesis and gestation was consecutive (Table 2). The relationship of these periods is an important feature in the reproductive cycle. The reproductive cycle can be defined by how often a species breeds and consist of two periods: the ovarian cycle (vitellogenesis period) and gestation (Castro, 2009). The length of the reproductive cycle depends on the duration of the ovarian cycle and gestation, and whether the two periods are concurrent or consecutive. The duration of these periods depends on how the mother can sequester energy from the environment and transfer it to the developing oocytes and embryos (Castro, 2009), and the stable conditions in captivity probably allows D. americana to reduce the time of gestation and the simultaneous development of oocytes and embryos.
Fecundity estimated in the present study (2-7) was smaller to that documented by Henningsen (2000) of 2-10, but higher to that documented by McEachran & de Carvalho (2002) of 3-5. The relationship between fecundity and maternal disc width was linear for D. americana in the present study and captivity (Henningsen, 2000). A significant linear relationship has also been estimated for D. marmorata (Capape & Zaouali, 1995), and non significant for D. sabina, D. sayi, D. centroura, P. violacea and D. chrysonota (Snelson et al., 1988; Snelson et al., 1989; Capape, 1993; Hemida et al., 2003; Ebert & Cowley, 2008). This feature is important in demographic analysis, because a larger fecundity is assigned to larger females, and for management purposes the protection of these females may have a positive effect on the population.
Fecundity in dasyatids ranges from 1 to 7 in the wild and from 1 to 10 in captivity (Table 2). D. americana has the highest fecundity reported among captive dasyatid rays (maximum 10), and among the highest fecundity reported in the wild for dasyatids (maximum 7). However, the average fecundity in wild specimens is very low for D. americana (2.5 embryos), as in other dasyatids (Table 2). Female dasyatids easily abort embryos because of stress during capture (Struhsaker, 1969; Capape, 1993; Snelson et al., 1988). It was commonly observed embryos aborted over the sides of fishing boats during landing. For this reason, it is often difficult to estimate fecundity of myliobatiform rays (Smith et al., 2007).
In general, the reproductive parameters of dasyatid species are similar to that of shark species with low biological productivity (Walker, 1998). For example, Smith et al. (2008) determine that D. dipterura from the Mexican Pacific coast, has low intrinsic growth potential and limited resilience to fishing pressure, and several dasyatids around the world have been classed as Vulnerable or Endangered by the International Union of the Conservation of Nature, indicating that these batoids need more attention in countries where intensive fisheries exploits them directly or incidentally. In particular, the status of the population of D. americana is of concern in the southern gulf of Mexico because it is the most landed elasmobranch by some small-scale fleets, and its reproductive parameters suggest that this dasyatid has low biological productivity and probably limited resilience to fishing pressure.
We thank fishermen of the artisanal fleet from San Pedro, Tabasco for allowing us to collect biological material. Special thanks to E. Segura, A. Hernandez, A. Romero, W. Arevalo and I. Mendez for their help at field. Funding was provided by Bureau of Forest and Fisheries Development (SEDAFOP) of the Tabasco State Government, project "Marine smallscale fisheries of Tabasco", and also by Fondo Mixto Conacyt-Gobierno del Estado de Tabasco, project "TAB-2007-C09-74601, Biologia y pesqueria de tiburones y rayas en las costas de Tabasco".
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Received: 24 June 2011; Accepted: 19 May 2012
Edith Ramirez-Mosqueda (1), Juan Carlos Perez-Jimenez (1) & Manuel Mendoza-Carranza (2)
(1) departamento de Aprovechamiento y Manejo de Recursos Acuaticos El Colegio de la Frontera Sur (ECOSUR), Unidad Campeche, Calle 10 #264, Col. Centro, Campeche, Mexico
(2) Departamento de Aprovechamiento y Manejo de Recursos Acuaticos El Colegio de la Frontera Sur (ECOSUR), Unidad Villahermosa, Carretera Villahermosa-Reforma km 15.5 Rancheria Guineo, seccion II, 86280 Villahermosa, Mexico
Corresponding author: J.C. Perez-Jimenez (email@example.com)
Tabla 1. Comparacion de los parametros reproductivos entre el sur del golfo de Mexico (presente estudio), Atlantico oeste y especimenes en cautiverio de la raya latigo americana Dasyatis americana. Table 1. Comparison of reproductive parameters among southern gulf of Mexico (present study), western Atlantic and captive specimens of the southern stingray Dasyatis americana. Parameters Southern gulf From Chesapeake Captive of Mexico Bay to Brazil specimen (present study) (1,2) (3,4) [DW.sub.50] at 775 unknown unknown maturity of females (mm) [DW.sub.50] at 517 unknown unknown maturity of males (mm) Smallest mature 650 750 (1) 750 (4) female Largest 960 800 (1) 800 (4) immature female Smallest mature 490 510 (1) 480 (4) male Largest 670 unknown 520 (4) immature male Gestation period 8 unknown 4.4-7.5 (3) (months) Size at birth 230-340 170-180 (1) 200-340 (3) (mm DW) Fecundity 2-7 3-5 (1,2) 2-10 (3) Sex ratio of 1:1 unknown 1:1 (3) embryos Maternal DW vs Yes unknown Yes (3) fecundity relationship Reproductive cycle annual unknown Biannual (3) Tabla 2. Ciclo reproductivo, periodo de gestacion y fecundidad de dasyatidos de vida libre y cautiverio. Table 2. The reproductive cycle, gestation period, and fecundity of wild and captive dasyatid rays. Species Reproductive Gestation Gestation-ovarian cycle (month) cycle Dasyatis annual 7-8 consecutive americana Dasyatis annual 4.4-7.5 ** unknown americana Dasyatis biannual 4.4-7.5 concurrent americana * Dasyatis annual? 9-11 concurrent? centroura Dasyatis unknown at least 4 concurrent centroura Dasyatis annual 9 concurrent chrysonota Dasyatis biannual 5-6 concurrent guttata Dasyatis unknown unknown unknown kuhlii Dasyatis biannual 4.5-5.5 concurrent kuhlii * Dasyatis unknown 10-11 unknown longa Dasyatis biannual 5-6 concurrent marianae Dasyatis triannual? 3 concurrent marmorata Dasyatis annual 4-4.5 consecutive sabina Dasyatis annual 3.5-4 consecutive sabina Dasyatis annual 4 n/a sabina Dasyatis annual 12 concurrent sayi Dasyatis unknown unknown unknown zugei Pteroplatytrygon biannual 2 concurrent? violacea * Pteroplatytrygon biannual? aprox. 4 concurrent violacea Pteroplatytrygon unknown unknown concurrent violacea Himantura walga unknown unknown unknown Species Fecundity Author (mean) Dasyatis 2-7 (2.5) Present study americana Dasyatis 2-7 (4.2) Grubbs et al. americana (2006) Dasyatis 2-10 (4.2) Henningsen americana * (2000) Dasyatis 4-6 Struhsaker centroura (1969) Dasyatis 2-6 (2.2) Capape centroura (1993) Dasyatis 1-7 (2.8) Ebert & Cowley chrysonota (2008) Dasyatis 1 Yokota & Lessa guttata (2007) Dasyatis 1 White & Dharmadi kuhlii (2007) Dasyatis 1 Janse & Schrama kuhlii * (2009) Dasyatis 1-5 Villavicencio-Garayzar longa et al. (1994) Dasyatis 2 Yokota & Lessa marianae (2007) Dasyatis 2-4 (2.9) Capape & Zaouali marmorata (1995) Dasyatis 1-4 (2.6) Snelson et al. sabina (1988) Dasyatis 1-3 (2.3) Johnson & Snelson sabina (1996) Dasyatis n/a Tricas et al. sabina (2000) Dasyatis 1-6 (3.5) Snelson et al. sayi (1989) Dasyatis 1-4 (2.1) White & Dharmadi zugei (2007) Pteroplatytrygon 2-7 Mollet et al. violacea * (2002) Pteroplatytrygon 2-7 Hemida et al. violacea (2003) Pteroplatytrygon (3.7) Veras et al. violacea (2009) Himantura walga 1-2 (1.4) White & Dharmadi (2007) * captive specimens, ** from the study of Henningsen (2000).