A CASE OF HERMAPHRODITISM IN TORTONESE’S STINGRAY, DASYATIS TORTONESEI (ELASMOBRANCHII: RAJIFORMES: DASYATIDAE) FROM THE LAGOON OF BIZERTE, TUNISIA

A normal hermaphrodite Tortonese’s stingray, Dasyatis tortonesei Capapé, 1975, captured in the brackish Lagoon of Bizerte (north-eastern Tunisia) is described in this note. It was a large specimen measuring 685 mm total length, 350 mm disk width, and 2190 g of the total body mass. The specimen externally presented medial cuspidate tooth rows on both jaws, and two claspers were present, that were rigid and calcified although shorter than those observed in normal specimens. The dissection of the abdominal cavity revealed on each side, an ovary normally developed that contained yolked oocytes, a complete genital tract and an uterus less developed than in normal adult. Conversely the testes were rudimentary, both Leydig’s glands were developed and a complete, slightly convoluted, male duct existed on the left side only. In all, 13 cases of normal (4) and abnormal (9) hermaphroditism, including the Tunisian D. tortonesei, have been found in batoid species, to date, confirming that the phenomenon is very rare among these chondrichthyan fishes..

Morphometric measurements (in mm and as % TL), meristic counts and masses recorded in the hermaphrodite specimen of Dasyatis tortonesei (FSB-D-tort 03) and comparison with two specimens (FSB-D-tort 04, FSB-D-tort 05)) from the Lagoon of Bizerte were added for comparison. The parameters presented in Table 1 were consistent with previous accounts of D. tortonesei provided by Capapé (1977) and Mc Eachran and Capapé (1984). The three specimens were preserved and deposited in the Ichthyological Collection of the Faculté des Sciences de Bizerte, with catalogue numbers, FSB-D-tort 03, 04, and 05 respectively. The analysis of the medial tooth rows on both jaws of the abnormal specimen showed that they were the typical cuspidate teeth of males, described in dasyatid species (Mc Eachran and Capapé 1984). Both claspers were present, rigid and calcified but shorter than those observed in normal specimens (Capapé 1983); additionally their distal end was not elongate and sharp but broadly rounded, although entirely covered by skin; no scar was visible; the teeth were probably functional (Fig. 4). Both claspers were measured following methodology of Collenot (1969), the left clasper, 90 mm, being slightly smaller than the right one, 92 mm. Additionally, the clasper of the hermaphrodite specimen was smaller that this of the normal specimen of similar size ( Table 1). The loss of tail clasper was the consequence of an abnormal development during growth, and not the result of a predation, such pat-tern was rather reported for tail of skate species (Mnasri et al. 2009, Orlov 2011. Dissection of the abdominal cavity allowed the primary sexual characters to be investigated (Fig. 5). Two ovaries were present and contained large yolked oocytes (Fig. 6); the left ovary weighed 35.9 g and contained 16 oocytes ranging in diameter from 17 to 21 mm, the right ovary weighed 22.9 g and contained 16 oocytes ranging in diameter from 13 to 18 mm. Both spermiducts were developed, the oviducal gland was more developed in the right side, while two uteri were present, the left uterus appeared to be more developed than the right one, but less than those generally observed in normal female specimens. Occurrence of two ovaries and two uteri could be considered a morphological aberration in a dasyatid species, in which only a single ovary and a single uterus are functional in large specimens (Mellinger 1989).
The specimen exhibited two Leydig's gland normally developed and two rudimentary testes, both spermiducts were present and slightly convoluted, although no sperm was found in either ducts. In adult male of D. tortonesei, as in other dasyatid species, the genital apparatus is typically fully developed on both sides (Capapé 1978, Fig. 4. Claspers of the hermaphrodite specimen of Dasyatis tortonesei caught in the Lagoon of Bizerte, Tunisia; Scale bar = 20 mm Mellinger 1989). The liver mass was 123.9 g, the digestive tract mass was 67.7 g. The gut contained remains of food totally digested and unidentifiable, weighing approximately 1 g.
Of the three categories of abnormalities reported by Dawson (1964Dawson ( , 1966Dawson ( , 1971) and Dawson and Heal (1971) in chondrichthyans, hermaphroditism is probably the most interesting due to the fact that it directly concerns reproductive organs and reproduction. Atz (1964) noted that hermaphroditism was rarely recorded in chondrichthyans. Two types of hermaphroditism are generally reported in chondrichthyans such as 'abnormal hermaphrodite' and 'normal hermaphrodite' following Atz (1964) and Iglésias et al. (2005), defined also as 'pseudo-hermaphrodite' and 'true hermaphrodite' by Irvine et al. 2002. Normal hermaphrodites or true-hermaphrodites exhibit internally both sexes with claspers and when mature it could assume functions of both male and female, all other cases of hermaphroditism would be defined as abnormal or pseudohermaphroditism (Irvine et al. 2002, Iglésias et al. 2005. Additionally, Atz (1964) and Bortone and Davis (1994) noted that intersexuality is considered when primary or secondary characters of both sexes are present in a same specimen.
Externally, the studied specimen exhibited, male secondary characters such as cuspidate teeth and claspers. Internally, it possessed developed female organs and yolked oocytes of ovulatory size; so it could be considered a functioning adult female. On the other hand, the male reproductive organs are consistent with a sub-adult male, totally developed in the left side only, even if the structure of both claspers are characteristic of an adult Hermaphroditism in Dasyatis tortonesei 145  male. It appears that the specimen could subsequently assume the function of male, but such hypothesis remains suitable. The specimen was a normal or true hermaphrodite following the definitions of Atz (1964), Irvine et al. (2002), and Iglésias et al. (2005). The presently reported observation is likely to be the first case of a true hermaphrodite in a dasyatid species. Previously, Ribeiro-Prado et al. (2009) described an abnormal hermaphrodite of the pelagic stingray, Pteroplatytrygon violacea (Bonaparte, 1832). Although such abnormalities are considered rare in chondrichthyans, a high percentage of true hermaphrodites were observed in the brown lantern shark, Etmopterus unicolor (Engelhardt, 1912), by Yano and Tanaka (1989) and the black dogfish, Centroscyllium fabricii (Reinhardt 1825), by Yano (1995), while Iglésias et al. (2005) stated that hermaphroditism is the normal condition of reproduction in the longhead catshark, Apristurus longicephalus Nakaya, 1975. No similar patterns were reported in batoid species, from which, few instances were recorded, only 15, to date ( Table 2).
The causes of hermaphroditism in chondrichthyans remain obscure. Atz (1964) noted that they may be due to endogenous-, hormonal-, or genetic factors as in other vertebrate species. Abnormalities in fish species occur during the early stages of development and could constitute an important indicator on unfavourable environmental conditions and pollutants, induced stress in the wild (Sfakianakis et al. 2004). Heavy metals such as Cd, Pb, Zn, and Cu are suspected to cause reduction or absence of fins (Sloof 1982). Several cases of abnormalities were described from animal species collected in the Lagoon of Bizerte, a restricted brackish area polluted by both inorganic and organic nutriments and heavy metals (Mzoughi et al. 2002, Harzallah 2003. Louiz et al. (2007) noted that skeletal deformities observed in 3 gobiid species were significantly higher in the areas severely polluted. Such pollution could explain why abnormal specimens of Torpedo torpedo (L.) were reported from the Lagoon of Bizerte (Ben Brahim and Capapé 1997, Ben Brahim et al. 1998, El Kamel et al. 2009b, Mnasri et al. 2010, El Kamel-Moutalibi et al. 2011, common torpedoes such as stingrays live buried in sandy bottoms, known to accumulate pollutants. The role of pollution in hermaphroditism concerning elasmobranch species seems to be worth further investigations.