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versión On-line ISSN 0718-560X
Lat. Am. J. Aquat. Res. v.39 n.1 Valparaíso 2011
Lat. Am. J. Aquat. Res., 39(1): 184-188, 2011
First record of morphological abnormality in embryos of Urotrygon rogersi (Jordan & Starks, 1895) (Myliobatiformes: Urotrygonidae) in the Tropical Eastern Pacific
Primer registro de anomalía morfológica en embriones de Urotrygon rogersi (Jordan & Starks, 1895) (Myliobatiformes: Urotrygonidae) en el Pacífico oriental tropical
Paola A. Mejía-Falla1, Andrés F. Navia1 & Luis A. Muñoz1
1 Colombian Foundation for Research and Conservation of Sharks, Skates and Rays SQUALUS Carrera 79 N° 6-37 Cali, Valle del Cauca, Colombia
ABSTRACT. This is the first report of morphological abnormalities in embryos of Roger's roundray Urotrygon rogersi in the Tropical Eastern Pacific. The embryos of two pregnant females caught in artisanal shrimp trawl nets had incomplete, deformed pectoral fins that were separated from the head along the anterior margin. Moreover, one of the embryos presented a fm-like extensión in the dorsal surface. Although the mouths of the embryos were normal and well-formed, the malformations in the pectoral fins could affect their mobility, limiting their capacity to capture preys and escape of predators.
Keywords: batoids, stingrays, Urotrygon rogersi, deformities, Tropical Eastern Pacific, Colombia.
RESUMEN. Este estudio constituye el primer registro de anormalidad morfológica en embriones de Urotrygon rogersi en el Pacífico oriental tropical. Dos hembras grávidas capturadas con redes de arrastre de camarón en pesca artesanal, presentaron embriones con aletas pectorales deformes e incompletas, y con el margen anterior separado de la cabeza; uno de ellos también presentó una extensión a manera de aleta en la superficie dorsal. Aunque la boca de los embriones fue normal y bien desarrollada, las malformaciones en las aletas pectorales podrían afectar su movilidad, limitando así la capacidad para capturar sus presas y escapar de pre dadores.
Palabras clave: batoideos, rayas espinosas, Urotrygon rogersi, deformidades, Pacífico oriental tropical, Colombia.
The thorny stingray or Roger's round ray Urotrygon rogersi (Jordan & Starks, 1895) is distributed in the Eastern Pacific Ocean, from Southern Baja California and the Gulf of California to Ecuador (Robertson & Alien, 2008), and inhabits soft bottoms among 2-30 m depth. U. rogersi is one of the common species in incidental capture in trawl gilí nets used by industrial and artisanal fisheries in the Tropical Eastern Pacific coast, and does not have commercial importance (Navia et al., 2009; Smith et al., 2009).
Reported morphological abnormalities for elasmo-branchs correspond to occurrences of bicephalia (Castro-Aguirre & Torres-Villegas, 1979; Goto et al., 1981; Bornatowski & Abilhoa, 2009), albinism (Joseph, 1961; Talent, 1973; De Jesus-Roldán, 1990; Ben-Brahim et al., 1998; Clark, 2002; Ferreira & Goes, 2002; Rider et al., 2002; Saidi et al., 2006; Sandoval-Castillo et al., 2006; Bottaro et al., 2005, 2008), anophthalmy (Gomes et al., 1991; Ribeiro-Prado et al., 2008) and deformities in the axial skeleton (Springer, 1960; Bensam, 1965; Du Built, 1978; Mancini et al., 2006). However, the most common abnormalities in skates (Order Rajiformes) and rays (Order Myliobatiformes) is where the pectoral fins are not fused to the head. This type of abnormality had been recorded by different authors (i.e. Templeman, 1965; Honma & Sugihara, 1971; Lamilla et al., 1995; Rosa et al., 1996; Oldfield, 2005; Ribeiro-Prado et al., 2008; Escobar-Sánchez et al., 2009) for several species of the family Rajidae (i.e. Raja brachyura, R. asterias, R. davala, R. radula, R. radíala, R. miraletus, Amblyraja radíate, Atlantoraja castelnaui, A. cyclophor, A. plátano), Torpedinidae (Torpedo marmorata), Rhinobatidae (Rhynchobatus djiddensis), Gymnuridae (Gymnura poecilura), Pota-motrygonidae (Potamotrygon motoro), Dasyatidae (Dasyatis longa, D. dipterura, D. akajei, Himantura uarnak, Pteroplatytrygon violácea) and this paper reported it for first time to family Urotrygonidae, specifically to Urotrygon rogersi in the Tropical Eastern Pacific, its known distribution área.
The pregnant females were caught by artisanal fishermen who use trawl gilí net (2.75 inch mesh size) to catch shrimp. One of them was captured in December 2007 in El Tigre (3°52'N, 77°19'W), the and another one in April 2008 in El Bajo de Punta Soldado (3°47'N, 77°11'W), central Pacific coast of Colombia. The females were dissected and their embryos were photographed and preserved in 10% formalin. The species identification was based on characters described by McEachran & Di Sciara (1995) and Robertson & Alien (2008). These U. rogersi were distinguished from other species of the genus, for showing small denticles on snout along the margin of disc, the area behind scapular región at midline of disc; a row of thorns from nape along middle of the back and top of the tail to base of spine; denticles arranged in longitudinal rows on top of body cavity; a plain light brown to brown coloration without distinctive marks in the top and white below. Morphometric measurements of the females and embryos were taken to the nearest 0.1 mm according to McEachran & Di Sciara (1995).
A pregnant female was 29.0 cm total length (TL), 15.5 cm disc width (DW) and 151 g, with two male embryos in the left uterus. One of the males was well developed (12 cm TL, 7.5 cm DW, 8 g) (Fig. 1a), but the smaller one (9.5 cm TL, 6.0 cm DW, 5 g) presented abnormality in the disc. The left pectoral fin was neither well-formed nor fused in front of its head, its snout was not completely free, and only its right pectoral fin was projected forward on side; also the pelvic fins were rounded and not located at the same level; and the spiracles were very open (Fig.1b). In addition, its dorsum presented a finlike projection or "dorsal fold" in the middle zone (Fig. 1c), and its mouth and nostrils were well developed.
Figure. 1. Sibling embryos of Urotrygon rogersi with differential development. a) Dorsal view of the normal male embryo of 12 cm TL, b) Dorsal view of the abnormal embryo of 9.5 cm TL, c) Lateral view of the last one, showing a projection like-fin on the dorsum.
Figura. 1. Embriones hermanos de Urotrygon rogersi con desarrollo diferencial, a) Vista dorsal del embrión macho normal de 12 cm TL, b) Vista dorsal del embrión anormal de 9,5 cm TL, c) Vista lateral del último embrión mostrando una proyección dorsal en forma de aleta.
The smaller pregnant female (23.2 cm TL, 12.5 cm DW and 65.44 g) had one abnormal developing male embryo of 6.2 cm TL, 3.7 cm DW and 0.9 g in the left uterus. This embryo also presented a left pectoral fin not fused in front of its head, its snout was not completely free, and only its right pectoral fin was projected forward on side (Fig. 2a). The nostrils and mouth were well developed, although the last one was slightly to one side, but apparently functional (Fig. 2b).
Figure. 2. Dorsal a) and b) ventral view of an abnormal developing male embryo of Urotrygon rogersi of 6.2 cm TL.
Figura. 2. Vista dorsal a) y ventral b) de un embrión macho en desarrollo de Urotrygon rogersi de 6,2 cm TL.
How was cited above, the morphological abnormalities more frequent in rays correspond to the pectoral fins non-adherent to the head which is produced in the early development and is known as "Barman" ray; in this abnormality, the rays present its snout free and its pectoral fins projected forward on each side. In the two found abnormal embryos, only the left pectoral fin was not fused to the head, its snout was not completely free, and only its right pectoral fin was projected forward on side. Those characteristics could be indicating an interruption on the early development; however, the fin-like projection on the disc in one of them could correspond to a malformation, which not presented its bigger and well-developed sib.
The causal factors of malformations could be parasitic infection, arthritis, injury, tumors, bad nutrition, congenital abnormality (Heupel et al., 1999), or unfavorable environmental conditions during embryonic development, such as pollution (Haaker, 1977; Rodríguez-Romero et al., 1990; Grady, 1992). Although in the case of U. rogersi, the cause of morphological deformities is uncertain, could be suggested, initially, that a bad nutrition and/or a congenital abnormality could be the causes of this malformation. The first reason can be considered by the presence of another well developed embryo (sib), which could have taken more feed from its mother, securing its development and better growing, supported that by the bigger length and weight. However, the second reason is supported by the presence of a fin-like projection or "dorsal fold" that is not present in these species, so corresponding to a congenital abnormality; this malformation had been recorded to Gymnura micrura in Brazilian waters (Silva-Nunes & Magalhães-Piorski, 2009). On the same way, the other unique embryo appeared to have a faster embryonic grow than the average of that population, since with only 6.1 cm TL, it presented a light brown dorsum, while others embryos of similar size have a light pink dorsum (pers. obs.) indicating an earlier development state. However, this faster growth was not an advantage to this animal, since it was not a well-developed embryo. Taking this into conside-ration, it is suggested that the cause of the morphological deformities during embryonic development in these individuals could be a congenital abnormality and not caused by bad or poor nutrition.
The unfavorable environmental conditions are discard, not only because the other embryo was well developed, but also because the areas where the pregnant females were captured are conserved zones, without contamination, industrial discharges, and at present one of them is in process of be declared natural reserve (INVEMAR et al., 2006).
Rosa et al. (1996) propose that this type of abnormality does not affect the survival of individuals of Potamotrygon motoro based on the capture of juveniles and adults alive with this malformation; while Escobar-Sánchez et al. (2009) suggest that specimens of Dasyatis longa may die before reaching the adulthood. Based on the degree of deformity in the disc of the analyzed embryos and since the mobility of U. rogersi is specially based on the undulation of pectoral fins (rather than the tail) (Wilga & Lauder, 2004), it is possible that these individuals had difficulties in swimming and escaping from potential predators (sharks), and secondly, its capabilities as a predator would be significantly limited, even with their well-formed mouths that will allow them to feed on their prey such as polychaetes, shrimps and crabs (Naviaeía/.,2009).
Finally, one record of similar abnormality was presented in a male embryo of Pteroplatrygon violacea captured in southeastern Brazil, which presented an incomplete fusión of the left pectoral fin and the body and also an asymmetry regarding the pectoral fins (Ribeiro-Prado et al., 2008); the authors proposed trian the percentage of this abnormality is low for this specie (1.3%), even being the highest from other species of the same área. Although that authors proposed that the percentage of abnormalities estimated in several studies are not representative of the real number, because in all cases samples carne from fisheries, where the capture total are uncertain, in this study, the samples were collected from monthly scientific surveys during three years, obtaining a low percentage of this abnormality to U. rogersi (0.31%), suggesting that in the study área this embryonic abnormality is not frequent. However, it is suggested to evalúate the presence of abnormalities in other sympatric species of the genera Dasyatis, Gymnura, Narcine and Rhinobatos, comparing them with abnormalities recorded in other áreas of the world, and including radiographies and dissections to try to assess the causes of that abnormalities.
We thank Hernán Paredes and Florentino Cuero, fishermen of the localities of Juanchaco and La Bocana, respectively, who captured and donated us the female specimens; C. Mejia for the revision of the English. The samples were collected during the field phase of the research project "Biodiversity and life history of rays of the Pacific Coast of the Valle of Cauca, Colombia" developed for the SQUALUS Foundation, which is co-financed for PADI Foundation and the Initiative to threaded species (IEA).
Ben-Brahim, R., A.A. Secka & C. Capapé. 1998. Albinisme chez une torpille ocellée Torpedo torpedo. Cybium, 22(1): 83-86. [ Links ]
Bensam, P. 1965. On a freak embryo of grey shark Carcharhinus limbatus (Muller & Henle). J. Mar. Biol. Assoc. Indian, 7: 206-207. [ Links ]
Bornatowski, H. & V. Abilhoa. 2009. Record of an anomalous embryo of Rhinobatos percellens (Elasmobranchii: Rhinobatidae) in the southern coast of Brazil. Mar. Biodivers. Rec., 2: e36. [ Links ]
Bottaro, M., S. Ferrando, L. Gallus, L. Girolsi & M. Vacchi. 2005. First record of albinism in the deep water shark Dalatias licha. JMBA2 Biod. Rec., [www.mba.ac.uk/jmba/jmba2biodiversityrecords]. Reviewed: 15 December 2009. [ Links ]
Bottaro, M., I. Consalvo, S. Ferrando, L. Gallus, L. Girolsi, P.N. Psomadakis, CJ.L. Atkinson & M. Vacchi. 2008. New records of blonde ray (Raja brachyura) from the Lingurian Sea. Mar. Biodivers. Rec., 1 :e72. [ Links ]
Castro-Aguirre, J.L. & J.R. Torres-Villegas. 1979. Sobre un caso de bicefalia funcional en Rhinoptera steindachneri Evermann & Jenkins (Chondrichthyes, Elasmobranchii, Batoidea), capturado en la costa occidental de Baja California, México. Cienc. Mar., 6:27-41. [ Links ]
Clark, S. 2002. First report of albinism in the white-spotted bamboo shark, Chiloscyllium plagiosum, with review of reported color aberrations in elasmobranch. Zoo. Biol., 21:519-524. [ Links ]
De Jesús-Roldan, M. 1990. An albino bat ray Myliobatis californica, from the Pacific coast of Baja California Sur, Mexico. Calif. Fish Game, 76(2): 126-127. [ Links ]
Du Built, M.H. 1978. Quelques anomalies anatomiques chez les raies. B. Peen Tunisie, 2: 89-96. [ Links ]
Escobar-Sánchez, O., F. Galván-Magaña, CA. Downton-Hoffmann, M. Carrera-Fernández & V.G. Alatorre-Ramírez. 2009. First record of a morphological abnormality in the longtail stingray Dasyatis longa (Myliobatiformes: Dasyatidae) in the gulf of California, Mexico. Mar. Biodivers. Rec., 2: e26. [ Links ]
Ferreira, S. & M. Góes. 2002. First record of albinism in the smooth dogfish Mustelus schimitti from Southern Brazil. Braz. Arch. Biol. Technol., 45(2): 241-243. [ Links ]
Gomes, U.L., H.R.S. Santos & A.E. Medina. 1991. Anophthalmia in Dasyatis sayi (Le Sueur, 1817) (Myliobatiformes, Dasyatidae). An. Acad. Bras. Cien., 63(3): 307-313. [ Links ]
Goto, M., T. Taninuchi, N. Kuga & M. Iwata. 1981. Four dicephalous specimens of blue shark, Prionace glauca, from Japan. Japan. J. Ichthyol., 28(2): 157-165. [ Links ]
Grady, S.W. 1992. Morphological deformities in brown bullhead administered dietaryb-naphthoflavone. J. Aquat. Anim. Health, 4: 7-16. [ Links ]
Haaker, P.L. 1977. Abnormal vertebral development in northern anchovy, Engraulis mordax Girard. Calif. Fish Game, 63: 182-185. [ Links ]
Heupel, M.R., CA. Simpfendorfer & M.B. Bennet. 1999. Skeletal deformities in elasmobranchs from Australian water. J. Fish Biol., 54(5): 1111-1115. [ Links ]
Honma, Y. & C. Sugihara. 1971. A stingray, Dasyatis akajaei, with aberrant pectoral fins from the Japan Sea. Japan. J. Ichthyol., 18(1): 187-189. [ Links ]
INVEMAR, UNIVALLE & INCIVA. 2006. Biomálaga: Valoración de la biodiversidad marina y costera de Bahía Málaga (Valle del Cauca), como uno de los instrumentos necesarios para que sea considerada un área protegida. Informe Científico Final. INVEMAR-UNIVALLE-INCIVA Joseph, E. 1961. An albino cownose ray, Rhinoptera bonasus (Mitchill) from Chesapeake Bay. Copeia, 1961:482-283. [ Links ]
Lamilla, J., G. Pequeño & I.U. Kong. 1995. Dasyatis brevis (Garman, 1880) segunda especie de Dasyatidae registrada para Chile (Chondrichthyes, Myliobatiformes). Estud. Oceanol., 14, 23-27. [ Links ]
Mancini, P.L., A.L. Casas & A.F. Amorim. 2006. Morphological abnormalities in a blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) fetus from southern Brazil. J. FishBiol., 69(6): 1881-1884. [ Links ]
McEachran, J.D. & N. Di Sciara. 1995. Peces Batiodeos. In: W. Fischer, F. Krupp, W. Schneider, C. Sommer, K. Carpenter & V. Niem (eds.). Guía para la identificación de especies para los fines de la pesca, Pacífico Centro Oriental. FAO, Roma, pp. 746-792. [ Links ]
Navia, A.F., P.A. Mejía-Falla, L.A. Zapata, S. Bessudo, G. Soler & E. Rubio. 2009. Estado del conocimiento sobre tiburones y rayas del Pacífico colombiano. In: V. Puentes, A.F. Navia, P.A. Mejía-Falla, J.P. Caldas, M.C. Diazgranados & L.A. Zapata (eds.). Avances en el conocimiento de tiburones, rayas y quimeras de Colombia. Fundación SQUALUS, Ministerio de Ambiente Vivienda y Desarrollo Territorial, Instituto Colombiano Agropecuario, Colciencias, Conservación Internacional, WWF Colombia, Bogotá, pp. 133-194. [ Links ]
Oldfield, R.G. 2005. Biology, husbandry, and reproduction of freshwater stingrays. Trop. Fish Hobbyist, 53: 114-116. [ Links ]
Rider, S., M. Athorn & G. Bailey. 2002. First record of a white tiger shark Galeocerdo cuvier, from the northeastern Gulf of Mexico. Fla. Sci., 65(1): 13-15. [ Links ]
Robertson, D.R. & G. Alien. 2008. Peces costeros del Pacífico Oriental Tropical: Un sistema de información en línea. Versión 1.0. Balboa, Panamá: Instituto Smithsonian de Investigaciones Tropicales. www.stri.org/sftep. Revised: 25 August 2009. [ Links ]
Rodríguez-Romero, J., R. Ramírez-Sevilla & G. Núñez-Márquez. 1990. Deformación de la boca en un juvenil de Atherinops affinis (Ayres) (Pisces: Atherinidae) desarrollado en laboratorio. Invest. Mar. CICIMAR, 5: 143-146. [ Links ]
Rosa, R.S., U.L. Gomes & O.B.F. Gadig. 1996. Um caso de teratogenia na raia de agua doce Potamotrygon motor o (Natterer in Muller & Henle, 1841) (Chondrichthyes: Potamotrygonidae). Rev. Nordest. Biol., 11: 125-132. [ Links ]
Sa'idi, B.M.N., A. Brada'i, S. Marouani, O. Guélorget & C. Capapé. 2006. Atypical characteristics of an albino embryo of Carcharhinus plumbeus (Chondrichthyes: Carcharhinidae) from the Gulf of Gabe's (southern Tunisia, central Mediterranean). Acta Adriatica, 47: 167-174. [ Links ]
Sandoval-Castillo, J., E. Mariano-Meléndez & CJ. Villavicencio-Garayzar. 2006. New records of albinism in two elasmobranchs: the tiger shark Galeocerdo cuvier and the giant electric ray Narcine entemedor. Cybium, 30(2): 191-192. [ Links ]
Silva-Nunes, J.L. & N. Magalhães-Piorski. 2009. A dorsal fold in Gymnura micrura (Bloch and Scheneider, 1801) (Chondrichthyes: Gymnuridae). Braz. Arch. Biol. Technol., 52(2): 479-482. [ Links ]
Smith, W.D., JJ. Bizarro & G.M. Cailliet. 2009. The artisanal elasmobranchs fishery on the east coast of Baja California, México: characteristics and management considerations. Cienc. Mar., 35(2): 209-236. [ Links ]
Springer, S. 1960. Natural history of the sandbar shark Eulamia milberti. Fish. Bull., 61: 1-38. [ Links ]
Talent, L.G. 1973. Albinism in embryo gray smoothhound shark, Mustelus californicus from Elkhorn Slough, Monterey Bay, California. Copeia, 1973(3): 595-597. [ Links ]
Templeman, W. 1965. Some abnormalities in skates (Raja) of the Newfoundland area. J. Fish. Res. Bd. Canada, 22(1): 237-238. [ Links ]
Wilga, C.A.D. & G.V. Lauder. 2004. Biomechanics of locomotion in sharks, rays and chimaeras. In: J.F. Carrier, J.A. Musick & M.R. Heithaus (eds.). Biology of sharks and their relatives. CRC Press, Boca Raton, pp. 139-164. [ Links ]
Received: 10 February 2010; Accepted: 26 December 2010
Corresponding author: Paola A. Mejía-Falla (firstname.lastname@example.org)