STUDY OF DERMAL DENTICLE MORPHOLOGY AS CHARACTERS OF TAXONOMIC IMPORTANCE IN ENDANGERED SHARKS AND RAYS FROM SOUTHERN OF BRAZIL
DOI:
https://doi.org/10.26462/33.1.1Keywords:
Chondrichthyes, Taxonomic identification, Conservation, South Atlantic, ElasmobranchsAbstract
The aim of this study was to use the dermal denticles as taxonomic identification tools, in shark and rays species gutted and processed for human consumption. The specimens come from surveillance actions by environmental protection agencies between 2018 and 2020 in South Brazil. For the dermal denticles analyses, skin samples were extracted and submitted to protocol for Scanning Electronic Microscopy (SEM). Whenever possible, the validation of the identification was done with base on published references. The identification within the Carcharhiniformes was challenging due to similarities among denticles of the different families, but the only characteristic shared by this order was the presence of crests, which varied in shape and size. The Squaliformes, represented by S. megalops, varied considerably in shape. In the Squatiniformes the denticles were robust and oval shaped. Through the analysis of a remaining piece of skin on a muscle sample already processed for consumption, the identification to genus was possible, revealing that the individual was Squatina. This study demonstrated that dermal denticles are key tools for the taxonomic identification in absence of external morphologic characters that would lead to the direct species identification. In most cases, the identification was possible at least to genus. The identified genera were: Atlantoraja, Myliobatis, Sphyrna, Squalus and Squatina. Furthermore, it was observed that the more complex is the taxonomic identification of a taxon, such as genus Squalus, the more is the difficulty in the identification to species with the dermal denticles.
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Ankhelyi, M.V., Wainwright, D.K., & Lauder, G.V. (2018). Diversity of dermal denticle structure in sharks: skin surface roughness and three dimensional morphology. Journal of morphology, 279(8), 1132-1154.
Awruch, C.A., Barreto, R., Charvet, P., Chiaramonte, G.E., Cuevas, … Rincon, G. 2019. Squatina occulta. The IUCN Red List of Threatened Species (2019): e.T39331A2899669. https://dx.doi.org/10.2305/IUCN.UK.2019-1.RLTS.T39331A2899669.en. Accessed on 06 February 2022.
Brugnoli, E. (2015). Ciencias marino-costeras en el umbral del siglo XXI: Desafíos en Latinoamérica y el Caribe.
Carlson, J., Charvet, P., Avalos, C., Blanco-Parra, … Pollom, R. (2021). Myliobatis freminvillei (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021:e.T161568A201183089. https://dx.doi.org/10.2305/IUCN.UK.2021-2.RLTS.T161568A201183089.en. Accessed on 06 February 2022.
Castro, L.A.S. (2002). Processamento de amostras para microscopia eletrônica de varredura. Embrapa Clima Temperado -Fôlder/Folheto/Cartilha (INFOTECA-E).
Compagno, L.J. (2005). Checklist of living Chondrichthyes. Reproductive biology and phylogeny of chondrichthyes. Sharks, batoids and chimaeras, 503-548.
Ebert, D.A., White, W.T., Goldman, K.J., Compagno, L.J.V., Daly-Engel, T.S., & Ward, R.D. (2010). Resurrection and redescription of Squalus suckleyi (Girard, 1854) from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae. Zootaxa, (2612), 22–40. https://doi.org/10.11646/zootaxa.2612.1.2
de Lima Viliod, M.C., Rangel, B.D.S., Rocha, L.C., dos Santos Domingos, J.F., Malavasi Bruno, C.E., ... & Ciena, A.P. (2021). Ecomorphological, space, and mineral relations of dermal denticles in angular angel shark (Squatin12valiação12im). Microscopy Research and Technique, 84(9), 2017-2023.
Feitosa, L.M., Martins, A.P.B., Giarrizzo, T., Macedo, W., Monteiro, I.L., Gemaque, R., ... & Carvalho-Costa, L.F. (2018). DNA-based identification reveals illegal trade of threatened shark species in a global elasmobranch conservation hotspot. Scientific reports, 8(1), 3347.
Feld, K., Kolborg, A.N., Nyborg, C.M., Salewski, M., Steffensen, J.F., & Berg-Sørensen, K. (2019). Dermal denticles of three slowly swimming shark species: microscopy and flow visualization. Biomimetics, 4(2), 38.
Ferrón, H.G., Paredes-Aliaga, M.V., Martínez-Pérez, C., & Botella, H. (2018). Bioluminescent-like squamation in the galeomorph shark Apristurus ampliceps (Chondrichthyes: Elasmobranchii). Contributions to Zoology, 87(3), 187-196.
Gemaque, R., Monteiro, I.L.P., Gomes, F., Sodré, D., Sampaio, ... & Rodrigues-Filho, L.D.S. (2017). Why implement measures to conserve the diversity of Elasmobranchs? The case of the northern coast of Brazil. Revista da Biologia, 17(2), 1-7.
Gilligan, J.J., & Otway, N.M. (2012). Comparison of dorsal and pectoral fin denticles for grey nurse, great white, and six whaler sharks from east Australian waters. In Journal and Proceedings, 144(3&4), 66-82.
Gravendeel, R., Van Neer, W., & Brinkhuizen, D. (2002). An identification key for dermal denticles of Rajidae from the North Sea. International Journal of Osteoarchaeology, 12(6), 420-441.
Haimovici, M., MACEIRA, R.P. Observações sobre a seleção a bordo e rejeição na pesca de arrasto de fundo no Rio Grande do Sul. In: Congresso Brasileiro de Engenharia de Pesca. 1981. p. 401-412.
Heemstra, P.C. (1997). A review of the smooth-hound sharks (genus Mustelus, family Triakidae) of the western Atlantic Ocean, with descriptions of two new species and a new subspecies. Bulletin of Marine Science, 60(3), 894-928.
Instituto Chico Mendes de Conservação da Biodiversidade (2014). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Disponível em: https://www.icmbio.gov.br/portal/images/storie13valiação13sa13valiação13se13valiação13ses -diversas/livro_vermelho_2018_vol1.pdf. (Acesso em: 02/12/2021).
Instituto Chico Mendes de Conservação da Biodiversidade. (2016). Avaliação do risco de extinção dos elasmobrânquios e quimeras no Brasil: 2010- 2012. Disponível em: https://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/trabalhos_tecnicos/pub_2016_avaliacao_elasmo_2010_2012.pdf. Acesso em: 06/02/2022.
IUCN (2021). The IUCN Red List of Threatened Species. Version2021-2. https://www.iucnredlist.org. Downloaded on [02/12/2021].
Kanagusuku, K., Dufflocq, P., Sánchez-Rea, A., Huamantinco, A.A., & Ramírez-Amaro, S. (2021). Morphological characterization of dermal denticles of the Broadnose Sevengill Shark Notoryn chuscepedianus (Elasmobranchii: Hexanchidae). Universitas Scientiarum, 26(3), 261-279.
Kemp, N.E. (1999). Integumentary system and teeth. En: Hamlett WC (ed). Sharks, skates and rays.
Laranjeira, M.E., Guimarães, J.P., Amorim, A.F., Rotundo, M., Rici, R.E.G., & Mari, R.B. (2015). Ultrastructure of dermal denticles in sharpnose shark (Rhizoprionodon lalandii) (Elasmobranchii, Carcharhinidae). Microscopy research and technique, 78(10), 859-864.
Last, P.R., Weigmann, S., & Yang, L. (2016). Changes to the nomenclature of the skates (Chondrichthyes: Rajiformes). Rays of the World: Supplementary Information. Clayton: CSIRO Special Publication, 11-34.
Macías Cuyare, M., & Oddone, M.C. (2022). Morphological pattern of the dermal denticles of the Southern sawtail catshark Galeus mincaronei Soto, 2001. Journal of Morphology, 283(8), 1120-1134.
Marino, I.A.M., Finotto, L., Colloca, F., Di Lorenzo, M., Gristina, M., ... & Mazzoldi, C. (2018). Resolving the ambiguities in the identification of two smooth-hound sharks (Mustelus mustelus and Mustelus punctulatus) using genetics and morphology. Marine Biodiversity, 48(3), 1551-1562.
Muniz, P., Brugnoli, E., Venturini, N. & Conde, D. (2019). Ciencias marino-costeras en el umbral del Siglo XXI Desafíos en Latinoamérica y el Caribe.
Muñoz-Chápuli, R., Ramos, F. (1989). Morphological comparison of Squalus blainvillei and S. megalops in the eastern Atlantic, with notes on the genus. Japanese Journal of Ichthyology, 36(1), 6-21.
Oddone, M.C., Paesch, L., & Norbis, W. (2005). Size at first sexual maturity of two species of rajoid skates, genera Atlantoraja and Dipturus (Pisces, Elasmobranchii, Rajidae), from the south western Atlantic Ocean. Journal of Applied Ichthyology, 21(1), 70-72.
Oddone, M.C., & Vooren, C.M. (2005). Reproductive biology of Atlantoraja cyclophora (Regan 1903) (Elasmobranchii: Rajidae) off southern Brazil. ICES Journal of Marine Science, 62(6), 1095-1103.
Oddone, M., Awruch, C.A., Barreto, R., Charvet, P., Chiaramonte, … & Vooren, C.M. 2019. Squatina guggenheim. The IUCN Red List of Threatened Species 2019: e.T130393378A130393975. https://dx.doi.org/10.2305/IUCN.UK.2019-1. RLTS.T130393378A130393975.en. Accessed on 06 February 2022.
Patricia, F.W., Guzman, D., Iñigo, B., Urtzi, I., Maria, B.J., & Manu, S. (2019). Morphological characterization and hydrodynamic behavior of shortfin mako shark (Isurus oxyrinchus) dorsal fin denticles. Journal of Bionic Engineering, 16(4), 730-741.
Pollom, R., Barreto, R., Charvet, P., Chiaramonte, G.E., Cuevas, Rincon, G. (2020). Atlantoraja castelnaui. The IUCN Red List of Threatened Species 2020: e.T44575A152015479. https://dx.doi.org/10.2305/IUCN.UK.2020-.RLTS.T44575A152015479.en. Accessed on 06 February 2022.
Pollom, R., Barreto, R., Charvet, P., Chiaramonte, G.E., Cuevas, ... & Rincon, G. (2020). Mustelus schmitti. The IUCN Red List of Threatened Species2020: e.T60203A3092243. https://dx.doi.org/10.2305/IUCN.UK.20203.RLTS.T60203A3092243.en. Accessed on 06 February 2022.
Pollom, R., Barreto, R., Charvet, P., Chiaramonte, G.E., Cuevas, J, ... & Rincon, G. (2020). Myliobatis ridens. The IUCN Red List of Threatened Species2020: e.T104025473A104025749. https://dx.doi.org/10.2305/IUCN.UK.2020-3.RLTS.T104025473A104025749.en. Acessed on 06 February 2022.
Rangel, B.D.S., Wosnick, N., Magdanelo Leandro, R., Amorim, A. F. D., Kfoury Junior, … & Rici, R.E.G. (2016). Thorns and dermal denticles of skates A. tlantoraja cyclophora and A. castelnaui: implications. Microscopy Research and Technique, 79(12), 1133-1138.
Raschi, W., & Tabit, C. (1992). Functional aspects of placoid scales: a review and update. Marine and Freshwater Research, 43(1), 123-147.
Reif, W.E. (1985). Functions of scales and photophores in mesopelagic luminescent sharks. Acta Zoologica, 66(2), 111-118.
Rigby, C.L., Barreto, R., Carlson, J., Fernando, D., Fordham, S., Herman, K., … & Winker, H. (2019). Sphyrna zygaena. The IUCN Red List of Threatened Species 2019: e.T39388A2921825. https://dx.doi.org/10.2305/IUCN.UK.2019-.RLTS.T39388A2921825.en. Accessed on 06 February 2022.
Rigby, C.L., Dulvy, N.K., Barreto, R., Carlson, J., Fernando, D., Fordham, S., & Winker, H. (2019). Sphyrna lewini. The IUCN Red List of Threatened Species 2019: e.T39385A2918526. Accessed on 06 February 2022.
Santos, H.R.S., & Charvet-Almeida, P. (2007). Description of females of the stingray Dasyatis colarensis Santos, Gomes & Charvet-Almeida, 2004 (Chondrichthyes, Myliobatiformes, Dasyatidae). Arquivos do Museu Nacional, 65(1).
Santos, C.C., & Coelho, R. (2018). Migrations and habitat use of the smooth hammerhead shark (Sphyrna zygaena) in the Atlantic Ocean. PLoS One, 13(6), e0198664.
Sokal, R.R., & Rohlf F.J. (1998). Biometry: The principles and practice of statistics in biological research. New York: Freeman.
Vaz, D.F., & De Carvalho, M.R. (2013). Morphological and taxonomic revision of species of Squatina from the Southwestern Atlantic Ocean (Chondrichthyes: Squatiniformes: Squatinidae). Zootaxa, 3695(1), 1-81.
Viana F.L., Lisher, S.T., de Carvalho, M.R. (2018). Two new species of short-snouted dogfish sharks of the genus Squalus Linnaeus, 1758, from southern Africa (Chondrichthyes: Squaliformes: Squalidae). Marine Biodiversity, 48(4), 1787-1814.
Vooren, C.M., Naves, L.C., & Romay, A.F.L. (2003). Guia para a identificação de tubarões e raias em desembarques da pesca no Rio Grande do Sul. Ed. FURG.
Vooren, C.M., & Klippel, S. (Eds.). (2005). Ações para a conservação de tubarões e raias no sul do Brasil. Sandro Klippel.
Vooren, C.M., & Oddone, M.C. (2019). La diversidad de los condrictios del extremo sur de Brasil: las especies, sus orígenes, y sus modos reproductivos. Ciencias marino-costeras en el umbral del siglo XXI Desafíos en Latinoamérica y el Caribe, Capítulo, 1, 171-214.
