On the capture of a large pregnant Bathytoshia lata (Chondrichthyes: Myliobatiformes: Dasyatidae) from the coast of Çeşme, Izmir (Aegean Sea, Turkey)

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J. Black Sea/Mediterranean Environment Vol. 23, No. 1: 92-99 (2017) SHORT COMMUNICATION On the capture of a large pregnant Bathytoshia lata (Chondrichthyes: Myliobatiformes: Dasyatidae) from the coast of Çeşme, Izmir (Aegean Sea, Turkey) Okan Akyol 1*, İlker Aydın 1, Ali Ulaş 1, Christian Capapé 2 1 Faculty of Fisheries, Ege University, 35440, Urla, Izmir, TURKEY 2 Laboratoire d'ichtyologie, case 104, Université Montpellier II, Sciences et Techniques du Languedoc, 34095, Montpellier cedex 5, FRANCE * Corresponding author: okan.akyol@ege.edu.tr Abstract The authors report in this paper the capture of a large female of Bathytoshia lata (Garman 1880) measuring 2220 mm in disc width and weighing approximatively 350 kg. It was a pregnant female at the end of the gestation which carried six near-term embryos. The specimen and its capture are described, indicating that the species is probably threatened but not totally extinct. Keywords: Size, measurements, pregnancy, distribution, Mediterranean Sea Received: 31.01.2017, Accepted: 01.03.2017 Of the seven dasyatid species found in Turkish waters, common stingray Dasyatis pastinaca (Linnaeus 1758) is the single one commonly caught in the area (Bilecenoglu et al. 2014). The other six species are only occasionally captured. One of them is roughtail stingray, Bathytoshia lata (Garman 1880), previously identified as D. centroura (Mitchill 1815) by Capapé (1977), Mc Eachran and Capapé (1986) and Weigmann (2016). Following Kottelat (2013), Last et al. (2016a,b) noted that the genus Bathytoshia Whitley 1933 was formerly considered as a junior synonym of the genus Dasyatis which includes a small group of very large and widely distributed roughtail stingrays. Molecular data showed that the species centroura is now included in the genus Bathytoshia which occurs only in the western Atlantic; while its congener Bathytoshia lata is widely distributed in the eastern Atlantic, Mediterranean Sea and Indo-Pacific (Last et al. 2016a,b). 92

In the wake of a collaboration with local fishermen aware of fishing grounds, we were informed that a large female carrying embryos was caught in Turkish waters where only four reports on Bathytoshia lata have been documented (Figure 1 and Table 1). The specimen is the first pregnant female recorded to date in the area. It is succinctly described in this paper, with its distribution discussed. Additionally, the biological observations carried out are herein presented and compared with similar traits reported from other marine areas, especially the Tunisian coast (Capapé 1993). Authors Table 1. Comparison of data concerning Bathytoshia lata recorded from the Mediterranean Sea. TL = total length, DW = disc width Region Size (mm) Weight (kg) Sex Number of specimens DW at birth (mm) Capapé (1993) Tunisian coast 1470 DW - Female 1 137 Jardas (1996) Adriatic Sea 2100 DW - Unsexed 1 - Basusta and Erdem (2000) Iskenderun Bay 498 TL - Unsexed 1 - Dulcic et al. (2003) Adriatic Sea 2600 DW 290 Female 1 - Basusta and Sulikowski (2012) Iskenderun Bay 1790 DW 127 Unsexed 1 - Deval et al.(2014) Gulf of Antalya 1411-2200 6.68- TL 35.50 Unsexed 4 - Özbek et al.(2015) Gulf of Antalya 860-1700 DW - Unsexed 5 - This study Aegean Sea, off Cesme 2200 DW 350* Female 1 280-330 * observed by fishermen, remains disputable, see Discussion On 11 November 2016, a pregnant female roughtail stingray Bathytoshia lata measuring 2220 mm in disc width (DW) (Figure 2) was captured by commercial trawl net having 44 mm mesh size in the coastal waters off Çeşme, Izmir, in the Aegean Sea (38 25'N, 26 16'E) at a depth of 70 m. Main measurements were made to the nearest millimetre on the individual, which weighed about 350 kg, according to the fishermen who caught it. Prior to be discarded at sea, the female expelled on board, six embryos; for each of them, the disc width was measured to the nearest millimetre and the weight recorded to the nearest gram. The specimen was identified following Capapé (1977), Mc Eachran and Capapé (1986), and Last et al. (2016b) by combination of morphological characters, as: disc rhomboid, anterior margins more or less straight, posterior margins slightly convex, snout obtuse and produced; nasal curtain broadly skirt shaped, mouth rather broad and depressed, tail with a relatively long membrane below starting at level of spine, no fold or ridge above; dorsal surface with large tubercles or bucklers on snout, around orbits and spiracles; large thorns along top and sides; color olive-brown with reddish areas in the present juvenile specimens. 93

Figure 1. The capture sites of the specimens of Bathytoshia lata in the eastern Mediterranean: (1) Karataş, Iskenderun Bay, caught between December 1994-November 1996 (Başusta and Erdem, 2000), (2) Gulf of Antalya, caught between August 2009 and April 2010 (Özbek et al. 2015), (3) Gulf of Antalya, caught between October 2009 and February 2011 (Deval et al. 2014), (4) Iskenderun Bay, caught on June 2011 (Başusta and Sulikowski 2012), (5) off Çeşme, İzmir, caught on 11 September 2016 (this study). Figure 2. The individual of Bathytoshia lata in this study, caught in the coast off Çeşme, Izmir, Aegean Sea (scale bar: 100 mm) 94

The tail of the specimen was truncated intra-vitam just before the first dorsal fin. Similar patterns were observed in skates and rays (Clark 1926; Soto and Mincarone 2001; Mnasri et al. 2009; Capapé et al. 2015a,b). Some specimens are tailless and the remain of tail is a stump like structure showing in its distal end a healed scar (Orlov 2011; Capapé et al. 2015a,b). Total or partial lack of tail is probably a consequence of the competition pressure for food with predators such as shark species (Mnasri et al. 2009). Abnormalities were also observed at the distal end of tail, such as lack or a typical characteristic of dorsal fins (Mnasri et al. 2010; Capapé et al. 2015a,b). These explain why DW is used as reference to measure rajiformes species rather than TL (Clark 1926). The measurements recorded in the present specimen on board were: DW (2220 mm), body height (510 mm), body height (510 mm), eye diameter (30 mm) and interorbital length (370 mm). TL was also measured; it reached 2510 mm, but the tail being truncated, such measurement could not be really taken into consideration. The present Bathytoshia is the largest specimen known in the Turkish waters and the eastern Mediterranean. The largest specimen in the Mediterranean basin, however, was recorded in the Adriatic Sea, measured 2600 mm in DW and weighed 290 kg (Dulcic et al. 2003). No larger specimen was recorded to date throughout the world. The present specimen weighed about 350 kg, according to the fishermen who caught it. It is the highest weight recorded to date for the species (Table 1), probably due to the fact the female carried embryos. However, an overestimation of this weight by the fishermen cannot be totally ruled out. The six expelled embryos were fully developed and without remain of yolk sac (Figure 3), and could be considered as near-term (see Capapé 1993). They ranged between 280 and 330 mm in diameter and weighed between 370 and 400 g, and are larger than those reported by Capapé (1993) who noted that birth occurred at 137 mm DW, off the Tunisian coast. Litter size of the present specimen reached six; Capapé (1993) noted that uterine fecundity ranged from 5 to 8, higher than litter size, 2-3 maximum. Such differences could be explained by that fact that some yolky oocytes could not be ovulated and became atretic, and abortions could not be avoided. Additionally, in elasmobranch viviparous species, it appears a relationship between size of females and litter size, the latter is higher in large females which give birth to larger free-swimming specimens (Mellinger 1989). Observations carried out on specimens from the Tunisian coast, showed that female maturation occurred between 660 and 1000 mm DW, all males and females having a DW greater than 800 mm and 1000 mm, respectively were adults, the largest male and the largest female had 1040 mm and 1345 mm DW, respectively. Struhsaker (1969) noted that males and females from the southeastern United States matured at a larger size, 1450 mm DW and 1500 mm DW, respectively, and, consecutively reached a larger maximal size, 2000 mm DW. Together with Tortonese (1956), Zupanovic (1961), Bullis and Struhsaker 95

(1961) and Struhsaker (1969), Capapé (1993) suggested that size at birth, size at sexual maturity and maximal size allow to admitting the existence of an American form of the species formerly identified as Dasyatis centroura different from the Mediterranean form. They noted that the "thorny tail stingray complex" needs additional study, considering that the populations from Atlanto- Mediterranean area and the western Atlantic may represent different species, such hypothesis was corroborated by the recent studies of Last et al. (2016a,b). Figure 3. Parturition scene of Bathytoshia lata (a) half near-term embryo, (b) entire nearterm embryo, (c) complete litter comprising six near-term embryos on board (scale bars: 50 mm) The captures of large specimens of Bathytoshia lata reported by Dulcic et al. (2003) and in the present paper do not confirm such hypothesis despite it cannot be totally ruled out. Decreasing in size observed in Mediterranean specimens could be due to the intense fishing pressure occurring locally since several decades: the larger specimens being more intrinsically vulnerable to depletion than the smaller specimens. Surveys carried out in some Mediterranean regions showed that the percentage presence for this species was one of lowest registered (Rosa et al. 2007). Additionally, Bathytoshia lata as other elasmobranch species is vulnerable to fishing pressure in the Mediterranean as well as other oceans and seas where the species was reported (Rosa et al. 2007), as a consequence of its K-selected characteristics, such as long reproductive cycle, large size at maturity and low fecundity enhancing that it is strongly threatened. Conversely, the finding of a large pregnant female shows that, fortunately the species is not totally extinct in the study area and probably in the 96

entire Mediterranean, therefore a strong monitoring of Bathytoshia lata and its related dasyatid species in needed prior their total collapse. İzmir Çeşme kıyılarında hamile büyük bir dişi Bathytoshia lata nın (Chondrichthyes: Myliobatiformes: Dasyatidae) yakalanması üzerine Öz Bu makalede yazarlar Bathytoshia lata (Garman, 1880) nın 2220 mm DW ve yaklaşık 350 kg ağırlığında ölçülmüş büyük bir dişi bireyinin yakalanışını rapor etmektedir. Bu, altı embriyosunu taşıyan gebelik süresinin sonunda bir hamile dişiydi. Bu tehdit altında fakat tamamen tükenmemiş olan tür tanımlanmış, yakalanışı tartışılmış ve yorumlanmıştır. Anahtar Kelimeler: Boyut, ölçüm, hamilelik, dağılım, Akdeniz References Başusta, N., Erdem, Ü. (2000) A study on the pelagic and demersal fishes of Iskenderun Bay. Tr. J. Zool. 24(Suppl.):1-19. (in Turkish) Başusta, N., Sulikowski, J.A. (2012) The oldest estimated age for roughtail stingray, Dasyatis centroura (Mitchill, 1815), from the Mediterranean Sea. J. Appl. Ichthyol. 28: 641-642. Bilecenoğlu, M., Kaya, M., Cihangir, B., Çiçek, E. (2014) An updated checklist of the marine fishes of Turkey. Tr. J. Zool. 38: 901-929. Bullis, H.R., Struhsaker, P. (1961) Life history notes on the roughtail stingray, Dasyatis centroura (Mitchill). Copeia 1961(2): 232-234. Capapé, C. (1977) Les espèces du genre Dasyatis Rafinesque, 1810 (Pisces, Rajiformes) des côtes tunisiennes. Cybium 3(2): 75-105. Capapé, C. (1993) New data on the reproductive biology of the thorny stingray, Dasyatis centroura (Mitchill, 1815), from off the Tunisian coasts. Environ. Biol. Fish 38: 73-80. Capapé, C., Ali, M., Saad, A., Reynaud, C. (2015a) Tail abnormalities in thornback ray Raja clavata (Chondrichthyes:Rajidae) from the coast of Syria (eastern Mediterranean). Cah. Biol. Mar. 56: 155-161. 97

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