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Abnormal embryos of sharpnose sharks, Rhizoprionodon porosus and Rhizoprionodon lalandii (Elasmobranchii: Carcharhinidae), from Brazilian coast, western South Atlantic

Published online by Cambridge University Press:  22 May 2014

Camila Mayumi Hirata dos Santos  and
Otto Bismarck Fazzano Gadig
Camila Mayumi Hirata dos Santos*
Affiliation:
UNESP, Campus de Rio Claro, Rua 24A n°1515, 13506-900, Rio Claro, São Paulo, Brazil Laboratório de Pesquisa de Elasmobrânquios, UNESP, Campus Experimental do Litoral Paulista, Praça Infante Dom Henrique s/n, 11330-900, São Vicente, São Paulo, Brazil
Otto Bismarck Fazzano Gadig
Affiliation:
Laboratório de Pesquisa de Elasmobrânquios, UNESP, Campus Experimental do Litoral Paulista, Praça Infante Dom Henrique s/n, 11330-900, São Vicente, São Paulo, Brazil
*
Correspondence should be addressed to: C.M.H. Santos, Laboratório de Pesquisa de Elasmobrânquios, UNESP, Campus Experimental do Litoral Paulista, Praça Infante Dom Henrique s/n, 11330-900, São Vicente, São Paulo, Brasil email: camilamhs@hotmail.com
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Abstract

This study presents the second worldwide report on abnormal embryos of the sharpnose sharks, Rhizoprionodon, based on the two species (Rhizoprionodon porosus and Rhizoprionodon lalandii) occurring on the Brazilian coast. For R. porosus two conjoined twin embryos showing complete duplication of the vertebral column, viscera and several external structures (head, first and second dorsal fins, pectoral fins), and scoliosis in both axis at the pelvic fin level are reported. The three embryos of R. lalandii exhibited numerous lordosis and kyphosis along the entire vertebral column. The possible relationship between anomalies and the human major threats to sharks is discussed based on previous reproductive, genetic and ecotoxicological studies on R. lalandii for southern Brazil.

Keywords

anomalyanatomymorphologyelasmobranchconservation
Type
Research Article
Information
Marine Biodiversity Records , Volume 7 , 2014 , e55
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Anderson, P.A., Huber, D.R. and Berzins, I.K. (2012) Correlations of capture, transport, and nutrition with spinal deformities in sandtiger sharks, Carcharias taurus, in public aquaria. Journal of Zoo and Wildlife Medicine 43, 750–758.CrossRefGoogle ScholarPubMed
Andrade, A.C., Silva-Júnior, L.C. and Vianna, M. (2008) Reproductive biology and population variables of the Brazilian sharpnose shark Rhizoprionodon lalandii (Müller & Henle, 1839) captured in coastal waters of south-eastern Brazil. Journal of Fish Biology 72, 473–484.CrossRefGoogle Scholar
Araújo, G.S., Moreira, L.B., Morais, R.D., Davansso, M.B., Garcia, T.F., Cruz, A.C.F. and Abessa, D.M.S. (2013) Ecotoxicological assessment of sediments from an urban marine protected area (Xixová-Japuí State Park, SP, Brazil). Marine Pollution Bulletin 75, 62–68.CrossRefGoogle ScholarPubMed
Ball, R.E., Jones, C.S., Lynghammar, A., Noble, L.R. and Griffiths, A.M. (2013) The first confirmed cases of full albinism in rajid species. Journal of Fish Biology 82, 1433–1440.CrossRefGoogle ScholarPubMed
Bejarano-Álvarez, M., Galván-Maganã, F. and Ocho-Baez, R. (2011) Further observations on foetal abnormalities in the blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) from north-west Mexico. Marine Biodiversity Records 4 e82, 1–3. doi: http://dx.doi.org/10.1017/S1755267211000790.CrossRefGoogle Scholar
Ben Souissi, J., Golani, D., Merji, H., Ben Salem, M. and Capapé, C. (2007) First confirmed record of the Halave's guitarfish, Rhinobatos halavi (Forsskål, 1775) (Chondrichthyes, Rhinobatidae) in the Mediterranean Sea with a description of albinism in elasmobranchs. Cahiers de Biologie Marine 48, 67–75.Google Scholar
Bícego, M.C., Taniguchi, S., Yogui, G.T., Montone, R.C., Silva, D.A.M., Lourenço, R.A., Martins, C.C., Sasaki, S.T., Pellizari, V.H. and Weber, R.R. (2006) Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Marine Pollution Bulletin 52, 1784–1832.CrossRefGoogle Scholar
Bornatowski, H. and Abilhoa, V. (2008) Record of an anomalous embryo of Rhinobatos percellens in the southern coast of Brazil. Marine Biodiversity Records 2 e36, 1–3. doi:10.1017/S1755267209000414.Google Scholar
Castro-Aguirre, J.L. and Torres-Villegas, J.R. (1979) Sobre un caso de bicefalia functional en Rhinoptera steindachneri Evermann y Jenkins (Chondrichthys, Elasmobranchii Batoidei), capturado en la costa occidental de Baja California, Mexico. Ciencias Marinas 6, 27–41 CrossRefGoogle Scholar
Delpiani, S.M., Antoni, M.Y.D., Barbini, S.A. and Figueroa, D.E. (2011) First record of a dicephalic specimen of tope Galeorhinus galeus (Elasmobranchii: Triakidae). Journal of Fish Biology 78, 941–944.CrossRefGoogle ScholarPubMed
Driggers, W.B. III., Hannan, K.M., Hoffmayer, E.R. and Jensen, J. (2012) Abnormal blacktip shark, Carcharhinus limbatus, embryo from the northern Gulf of Mexico. Journal of Applied Ichthyology 28, 827–828.CrossRefGoogle Scholar
Dulvy, N.K., Fowler, S.L., Musick, J.A., Cavanagh, R.D., Kyne, P.M., Harrison, L.R., Carlson, J.K., Davidson, L.N.K., Fordham, S.V., Francis, M.P., Pollock, C.M., Simpfendorfer, C.A., Burgess, G.H., Carpenter, K.E., Compagno, L.J.V., Ebert, D.A., Gibson, C., Heupel, M.R., Livingstone, S.R., Sanciangco, J.C., Stevens, J.D., Valenti, S. and White, W.T. (2014) Extinction risk and conservation of the world's sharks and rays. eLife. doi:10.7554/eLife.00590.CrossRefGoogle ScholarPubMed
Ebert, D.A., Fowler, S. and Compagno, L.J.V. (2013) Sharks of the world: a fully illustrated guide. Plymouth, UK: Wild Nature Press.Google Scholar
El Kamel, O., Mnasri, N., Boumaïza, M. and Capapé, C. (2009) Atypical abnormality in a common torpedo, Torpedo torpedo (Chondrichthyes: Torpedinidae) from the Lagoon of Bizerte (northern Tunisia, central Mediterranean). Cahiers de Biologie Marine 50, 97–101.Google Scholar
Escobar-Sánchez, O., Galván-Magaña, F., Downton-Hoffman, C.A., Carrera-Fernández, M. and Alatorre-Ramírez, V.G. (2009) First record of a morphological abnormality in the longtail stingray Dasyatis longa (Myliobatiformes: Dasyatidae) in the Gulf of California, Mexico. Marine Biodiversity Records 2 e26. doi: http://dx.doi.org/10.1017/S1755267208000304.CrossRefGoogle Scholar
Evermann, B.W. and Jenkins, O.P. (1891) Report upon a collection of fishes made at Guaymas, Sonora, Mexico, with descriptions of new species. Proceedings of the United States National Museum 14, 121–165.CrossRefGoogle Scholar
Ferreira, B.P. (1988) Ciclo reprodutivo de Rhizoprionodon lalandei (Valenciennes) e R. porosus (Poey) (Selachii, Carcharhinidae) na região de Barra de Guaratiba, RJ. Anais da Academia Brasileira de Ciências 60, 91–101.Google Scholar
Figueiredo, J.L. (1977) Manual de peixes marinhos do sudeste do Brasil. São Paulo: Museu de Zoologia, Universidade de São Paulo.CrossRefGoogle Scholar
Ford, E. (1930) Some abnormal fishes received at the Plymouth Laboratory. Journal of the Marine Biological Association of the United Kingdom 17, 53–64.CrossRefGoogle Scholar
Galván-Magaña, F., Escobar-Sánchez, O. and Carrera-Fernández, M. (2011) Embryonic bicephaly in the blue shark, Prionace glauca, from the Mexican Pacific Ocean. Marine Biodiversity Records 4 e1, 1–4. doi: http://dx.doi.org/10.1017/S1755267210001120.CrossRefGoogle Scholar
Garrick, J.A.F. (1982) Sharks of the genus Carcharhinus . NOAA Technical Report, National Marine Fisheries Service 445, 1–194.Google Scholar
Gelsleichter, J. and Walker, C.J. (2010) Pollutant exposure and effects in sharks and their relatives. In Carrier, J.C., Musick, J.A. and Heithaus, M.R. (eds) Sharks and their relatives. II: biodiversity, adaptive physiology, and conservation. CRC Marine Biology Series. Boca Raton, FL: CRC Press, pp. 491–537.CrossRefGoogle Scholar
Gomes, U.L., Santos, H.R.S. and Medina, A.E. (1991) Anophthalmia in Dasyatis sayi (LeSueur, 1817) (Myliobatiformes, Dasyatidae). Anais da Academia Brasileira de Ciências 63, 307–313.Google Scholar
Gopalan, U.K. (1971) On two abnormal sharks from Gujarat. Journal of the Bombay Natural History Society 68, 465–466.Google Scholar
Goto, M., Taniuchi, T., Kuga, N. and Iwata, M. (1981) Four dicephalous specimens of the blue shark, Prionace glauca, from Japan. Japanese Journal of Ichthyology 28, 157–165.Google Scholar
Guida, L., Walker, T.L. and Reina, R.D. (2013) First record of a bicephalic chondrichthyan found in Australian waters, the southern fiddler ray, Trigonorrhina dumerili (Chondrichthyes, Rhinobatidae). Marine and Freshwater Research. doi: 10.1071/MF13198.Google Scholar
Heupel, M.R., Simpfendorfer, C.A. and Bennett, M.B. (1999) Skeletal deformities in elasmobranchs from Australian waters. Journal of Fish Biology 54, 1111–1115.CrossRefGoogle Scholar
Hevia-Hormazábal, V., Pastén-Marambio, V. and Alonso, V. (2011) Registro de un monstruo diprósopo de tiburon azul (Prionace glauca) en Chile. International Journal of Morphology 29, 509–513.CrossRefGoogle Scholar
Hoenig, J.M. and Walsh, H.A. (1983) Skeletal lesions and deformities in large sharks. Journal of Wildlife Diseases 19, 27–33.CrossRefGoogle ScholarPubMed
Joseph, B. (1961) An albino cownose ray, Rhinoptera bonasus (Mitchill) from Chesapeake Bay. Copeia 4, 482–483.CrossRefGoogle Scholar
Kamiya, T., Miyazaki, N. and Shiraga, S. (1981) First case of dicephaly in odontoceti. Scientific Reports of the Whales Research Institute 33, 127–129.Google Scholar
Kaufman, M.H. (2004) The embryology of conjoined twins. Child's Nervous System 20, 508–525.CrossRefGoogle ScholarPubMed
Kompanje, E.J.O. (2005) A case of symmetrical conjoined twins in a bottlenose dolphin Tursiops truncatus (Mammalia, Cetacea). DEINSEA 11, 147–150.Google Scholar
Lacerda, L.D., Paraquetti, H.H.M., Marins, R.V., Rezende, C.E., Zalmon, I.R., Gomes, M.P. and Farias, V. (2000) Mercury contents in shark species from the south-eastern Brazilian coast. Revista Brasileira de Biologia 60, 571–576.CrossRefGoogle ScholarPubMed
Lessa, R.P. (1988) Premières observations sur la biologie reproductive de Rhizoprionodon lalandei (Valenciennes, 1839) (Pisces, Carcharhinidae) de la côte nord du Brésil—Maranhão. Revista Brasileira de Biologia 48, 721–730.Google Scholar
Linnaeus, C. (1758) Systema Naturae, Ed. X. (Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata.). Holmiae [Stockholm]: Laurentii Salvii.Google Scholar
Mancini, P.L., Casas, A.L. and Amorim, A.F. (2006) Morphological abnormalities in a blue shark Prionace glauca (Chondrichthyes: Carcharhinidae) foetus from southern Brazil. Journal of Fish Biology 69, 1881–1884.CrossRefGoogle Scholar
Mattos, S.M.G., Broadhurst, M.K., Hazin, F.H.V. and Jonnes, D.M. (2001) Reproductive biology of the Caribbean sharpnose shark, Rhizoprionodon porosus, from northern Brazil. Marine and Freshwater Research 52, 745–52.CrossRefGoogle Scholar
Mejía-Falla, P., Navia, A.F. and Muñoz, L.A. (2011) First record of morphological abnormality in embryos of Urotrygon rogersi (Jordan & Starks, 1895) (Myliobatiformes: Urotrygonidae) in the Tropical Eastern Pacific. Latin American Journal of Aquatic Research 39, 184–188.CrossRefGoogle Scholar
Mendonça, J.T. and Miranda, L.V. (2008) Estatística pesqueira do litoral sul de São Paulo: subsídios para gestão compartilhada. Pan-American Journal of Aquatic Sciences 3, 152–173.Google Scholar
Mendonça, F.F., Oliveira, C., Gadig, O.B.F. and Foresti, F. (2013) Diversity and genetic population structure of the Brazilian sharpnose shark Rhizoprionodon lalandii . Aquatic Conservation: Marine and Freshwater Ecosystems 23, 850–857.CrossRefGoogle Scholar
Motta, F.S., Gadig, O.B.F., Braga, F.M.S. and Namora, R.C. (2005) Size and sex compositions, length–weight relationship, and occurrence of the Brazilian sharpnose shark, Rhizoprionodon lalandii, caught by artisanal fishery from southeastern Brazil. Fisheries Research 74, 116–126.CrossRefGoogle Scholar
Motta, F.S., Namora, R.C., Gadig, O.B.F. and Braga, F.M.S. (2007) Reproductive biology of the Brazilian sharpnose shark (Rhizoprionodon lalandii) from southeastern Brazil. ICES Journal of Marine Sciences 64, 1829–1835.CrossRefGoogle Scholar
Müller, J. and Henle, F.G.J. (1839) Systematische Beschreibung der Plagiostomen. Berlin: Veit und Comp.Google Scholar
Muñoz-Osorio, L.A., Mejía-Falla, P.A. and Navia, A.F. (2013) First record of a bicephalic embryo of smalltail shark Carcharhinus porosus . Journal of Fish Biology 82, 1753–1757.CrossRefGoogle ScholarPubMed
Nakaya, K. (1973) An albino zebra shark Stegostoma fasciatum from the Indian Ocean, with comments on albinism in elasmobranchs. Japanese Journal of Ichthyology 20, 120–122.Google Scholar
Pastore, M. and Prato, E. (1989) A teratologic case in a shark. Thalassia Salentina 19, 87–92.Google Scholar
Pereyra, S., Garcia, G., Miller, P., Oviedo, S. and Domingo, A. (2010) Low genetic diversity and population structure of the narrownose shark (Mustelus schmitti). Fisheries Research 106, 468–473.CrossRefGoogle Scholar
Petrescu-Mag, I.V., Păsărin, B., Hoha, G., Hărşan, R. And Odagiu, A.M. (2011) New contributions to knowledge of embryonic malformations in guppies. Aquaculture, Aquarium, Conservation & Legislation—International Journal of the Bioflux Society 4, 216–228.Google Scholar
Poey, F. (1861) Memorias sobre la historia natural de la Isla de Cuba, acompañadas de sumarios Latinos y extractos en Francés. Tomo 2. Havana: Imprenta de Barcina.Google Scholar
Rafinesque, C.S. (1810) Indice d'ittiologia siciliana; ossia, catalogo metodico dei nomi latini, italiani, e siciliani dei pesci, che si rinvengono in Sicilia disposti secondo un metodo naturale e seguito da un appendice che contiene la descrizione de alcuni nuovi pesci siciliani. Messina: G. del Nobolo.Google Scholar
Ribeiro-Prado, C.C., Oddone, M.C., Gonzalez, M.M.B., Amorim, A.F. and Capapé, C. (2008) Morphological abnormalities in skates and rays (Chondrichthyes) from off southeastern Brazil. Arquivos de Ciências do Mar 41, 21–28.Google Scholar
Rosa, R.S., Gomes, U.L. and Gadig, O.B.F. (1996) Um caso de teratogenia na raia e água doce Potamotrygon motoro (Natterer in Müller e Henle, 1841) (Chondrichthyes: Potamotrygonidae). Revista Nordestina de Biologia 11, 125–132.Google Scholar
Rüppell, W.P.E.S. (1837) Neue Wirbelthiere zu der Fauna von Abyssinien gehörig. Fische des Rothen Meeres. Frankfurt am Main: Siegmund Schmerber.Google Scholar
Spencer, R. (2000) Theoretical and analytical embryology of conjoined twins: Part I: embryogenesis. Clinical Anatomy 13, 36–53.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Springer, V.G. (1964) A revision of the carcharhinid shark genera Scoliodon, Loxodon, and Rhizoprionodon . Proceedings of the United States National Museum 115, 559–632.CrossRefGoogle Scholar
Tate, E.E., Anderson, P.A., Huber, D.R. and Berzins, I.K. (2013) Correlations of swimming patterns with spinal deformities in the sand tiger shark, Carcharias taurus . International Journal for Comparative Psychology 26, 75–82.CrossRefGoogle Scholar
Teixeira, S.F. and Araújo, M.L.G. (2002) First record of albinism in the smooth dogfish Mustelus schmitti Springer, 1939 (Carcharhiniformes, Triakidae) from southern Brazil. Brazilian Archives of Biology and Technology 45, 241–243.CrossRefGoogle Scholar
Wagner, C.M., Rice, P.H. and Pease, A.P. (2013) First record of dicephalia in a bull shark Carcharhinus leucas (Chondrichthyes, Carcharhinidae) foetus from the Gulf of Mexico, U.S.A. Journal of Fish Biology 82, 1419–1422.CrossRefGoogle Scholar
Whitley, G.P. (1929) Additions to the check-list of the fishes of New South Wales. No. 2. Australian Zoologist 5, 353–357.Google Scholar