Identification complexity of critically endangered Squatina squatina (Linnaeus, 1758) and Squatina aculeata Cuvier, 1829 in the Mediterranean Sea (Turkey)

Authors

  • Inci Tuney-Kizilkaya Ege University
  • Elizabeth Grace Tunka BENGİL Girne American University

DOI:

https://doi.org/10.5281/zenodo.6522467

Keywords:

Angel Shark, COI, 16S rDNA, Eastern Mediterranean Sea

Abstract

Sharks and rays, besides their economic importance, are ecologically important organisms with a diverse group. After a pregnant Squatina sp. was captured as by-catch, Akyol et al. (2015) published this species as Squatina squatina while the COI and 16S rDNA analysis demonstrated that the species is S. aculeata. This complexity revealed that utilizing morphologic identification solely might not be enough to distinguish these two Squatina species accurately. We aim to compare morphologic and molecular techniques during species identification of critically endangered S. squatina and S. aculeata. Two different gene regions were used for molecular identification of 3 Squatina specimens obtained from the Aegean coasts of Turkey. Sequence analysis of two gene regions was conducted after PCR analysis. An aligned data set was used for creating phylogenetic trees. The results demonstrated that the previously identified S. squatina specimen was revealed as S. aculeata after molecular analysis. Two other specimens which were morphologically identified as S. squatina demonstrated the same results both with molecular and morphological analysis. Our results suggest that adopting morphological identification as the only tool is not enough to accurately determine the Squatina species; both morphological and molecular tools should be used for taxonomical identification of shark species, especially the endangered ones, to assure their conservation status.

References

Akyol, O. & Ceyhan, T. (2007). Datca-Bozburun Yarimadasi (Ege Denizi) kiyi balikciligi ve sorunlari uzerine bir arastirma. E.U. Journal of Fisheries and Aquatic Sciences, 24 (1-2), 121-126.

Akyol, O., Ünal, V., Capape, C. (2015). Occurrence and Biological Observation on Angel Shark Squatina squatina (Chondrichthyes: Squatinidae) from the Turkish waters (Eastern Mediterranean). Turkish Journal of Fisheries and Aquatic Science, 15, 931-935.

Alioto, D. (2012). A Review of the systematics of Angel Sharks emphasizes the species of the Eastern Pacific region with a modified set of morphometrics for order Squatiniformes. Ph.D., University of California, Los Angeles, USA.

Bandelt, H.J., Forster, P., Sykes, B.C., Richards, M.B. (1995). Mitochondrial portraits of human populations, Genetics, 141, 743-753.

Basusta, N. (2016). New records of neonate and juvenile sharks (Heptranchias perlo, Squatina aculeata, Etmopterus spinax) from the North-eastern Mediterranean Sea. Marine Biodiversity, 46, 525-527.

Basusta, N. (2002). Occurrence of Sawback Angelshark (Squatina aculeata Cuvier, 1829) off the Eastern Mediterranean Coast of Turkey. Turkish Journal of Veterinary and Animal Science, 26, 1177-1179.

Bulguroglu, S.Y., Korun, J., Gokoglu, M. & Ozvarol, Y. (2014). The marine leech Stibarobdella moorei (Oka, 1910) (Hirudinea, Piscicolidae) parasitic on the thornback ray Raja clavata Linnaeus, (1758) 1758 and angel shark Squatina squatina in Antalya Bay, Mediterranean Sea of Turkey. Helminthologia 51, 3, 250-252.

Capapé, C., Diatta, Y., Seck, A.A., Guelorget, O. & Ben, S. J. (ed.) (2005). Reproduction of the sawback angel shark Squatina aculeata (Chondrichthyes: Squatinidae) of Senegal and Tunisia. Cybium, 29, 2, 147-157.

Capapé, C., Quignard, J.P. & Mellinger, J. (1990). Reproduction and development of two angel sharks, Squatina squatina and S. oculata (Pisces: Squatinidae), off Tunisian coasts: Semi‐delayed vitellogenesis, lack of egg capsules, and lecithotrophy. Journal of Fish Biology, 37, 3, 347-356.

Carvalho, M.R., Faro, C. & Gomes, U.L. (2010). Comparative neurocranial morphology of angel sharks from the south-western Atlantic Ocean (Chondrichthyes, Elasmobranchii, Squatinidae): implications for taxonomy and phylogeny. Acta Zoologica, 93, 171-183.

Cavallaro, M., Danze, A., Ammendolia, G. & Navarra, E. (2015). Finding of a rare Squatina squatina (Linnaeus, 1758) (Chondrichthyes: Squatinidae) along the Tyrrhenian coast of Strait of Messina and its maintenance in an aquarium. Marine Biodiversity Records, 8, 1-4. doi:10.1017/S1755267215000226. [accessed 10 February 2020]

Coker, T. & Akyol, O. (2014) .An evaluation of the fish diversity of Gökova Bay (Aegean Sea). E.U Journal of Fisheries and Aquatic Science, 31, 3, 161-166.

Compagno L. Dando, M. & Fowler, S. (2005). Sharks of the World. Princeton Field Guides.

Corsini, M. & Zava, B. (2007). Recent capture of Squatina oculata and Squatina aculeata from Dodecanese Islands (SE Aegean Sea, Eastern Mediterranean). Biologia Marina Mediterranea, 14, 2, 352-353.

Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of Linnean Society, 85, 407–415.

Ebert, D.A., Stehmann, M.F.W. (2013) Sharks, batoids, and chimeras of the North Atlantic FAO Species Catalogue for Fishery Purposes. Food and Agriculture Organization of the United Nations, 7, pp. 523.

Economidis, P.S. (1973). Catalogue des passions de la Grece. Oceanology Limnology, 11, 421-600.

Erguden, D. & Bayhan,. YK. (2015). Three Fish Species Known to be Rare for Turkey, Captured from the Northeastern Mediterranean Coast of Turkey, Mersin Bay, Sudis hyalina Rafinesque, Chlopsis bicolor Rafinesque, Squatina aculeata Cuvier. International Journal of Scientific and Technological Research, 1,4, 1-8.

Ferretti, F., Morey, G., Serena, F., Mancusi, C. & Fowler, S.L. (ed) (2015). Squatina squatina. The IUCN Red List of Threatened Species 2015. e.T39332A48933059. http://dx.doi.org/10.2305/IUCN.UK.2015-1.RLTS.T39332A48933059.en. [accessed 11 November 2019]

Filiz, H., Irmak, E. & Mater, S. (2005). Occurrence of Squatina aculeata Cuvier, 1829 (Elasmobranchii, Squatinidae) from the Aegean Sea, Turkey. E.U Journal of Fisheries and Aquatic Sciences, 22, 2-3, 451-452.

Fitzpatrick, C.K., Finnegan, K.A., Osaer, F., Nervaez, K. & Shivji, M.S. (2017). The complete mitochondrial genome of the Critically Endangered Angelshark, Squatina squatina. Mitochondrial DNA Part B, 2, 1, 212-213.

Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome coxidase subunit I from diverse metazoan invertebrates. Molecular and Marine Biology and Biotechnology, 3, 5, 294-299.

Fortibuoni, T., Borme, D., Franceschini, G., Giovanardi, O. & Raicevich, S. (2016). Common, rare or extirpated? Shifting baselines for common angelshark, Squatina squatina (Elasmobranchii: Squatinidae), in the Northern Adriatic Sea (Mediterranean Sea). Hydrobiologia, 772, 1, 247-259.

Garcia-Vazquez, E., Machado-Schiaffino, G., Campo, D. & Juanes, F. (2012). Species misidentification in mixed hake fisheries may lead to overexploitation and population bottlenecks. Fisheries Research, 114, 52-55.

Golani, D. (1996). The marine ichtyofauna of the Eastern Levant. History, inventory and characterization. Israel Journal of Zoology, 42, 15-55.

Harsan, R. & Petrescu-Mag, I.V. (2008). Endangered fish species of the world. Aquaculture, Aquarium, Conservation and Legislation Journal of Bioflux Society, 1, 2, 193-215.

Holcer, D. & Lazar, B. (2017). New data on the occurrence of the critically endangered common angelshark, Squatina squatina, in the Croatian Adriatic Sea. Natura Croatica: Periodicum Musei Historiae Naturalis Croatici, 26, 2, 313-320.

Ismen, A., Yigin, C.C., Altinagac, U. & Ayaz, A. (2009). Length-weight relationships for ten shark species from Saros Bay (North Aegean Sea). Journal of Applied Ichthyology, 25, 1, 109-112.

Kabasakal, H. (2002). Elasmobranch species of the seas of Turkey. Annales Series Historia Naturalis, 12, 1, 15-2.

Kabasakal, H. (2003). Historical and contemporary records of sharks from the Sea of Marmara, Turkey. Annales Series Historia Naturalis, 13, 1, 4-18.

Kabasakal, H. & Kabasakal, O. (2014). Status of angel shark, Squatina squatina (Elasmobranchii: Squatiniformes: Squatinidae) in the Sea of Marmara. Annales Series Historia Naturalis, 24, 41-46.

Kabasakal, H. & Karhan, S.I. (2015). Shark Biodiversity in the Sea of Marmara: departures and arrivals over a century. Marine Biodiversity Records, 8, 1-9.

Karakulak, F.S., Erk, H. & Bilgin, B. (2006). Length-weight relationships for 47 coastal fish species from the northern Aegean Sea, Turkey. Journal of Applied Ichthyology, 22, 274-278.

Keskin, C. (2010). A review of fish fauna in the Turkish Black Sea. Journal of the Black Sea/Mediterranean Environment, 16, 2, 1965-210.

Kumar, S., Stecher, G. & Tamura, K. (2015). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Molecular Biology and Evolution, 28, 2731-2739.

Moftah, M., Abdel, A.S.H., Elramah, S. & Favereaux, A. (2011). Classification of Sharks in the Egyptian Mediterranean Waters Using Morphological and DNA Barcoding Approaches. Public Library of Science ONE, 6, 11, e27001. doi:10.1371/journal.pone.0027001

Narváez, K. & Osaer, F. (2017). The marine leech Branchellion torpedinis parasitic on the angel shark Squatina squatina and the marbled electric ray Torpedo marmorata. Marine Biodiversity, 47, 3, 987-990.

Naylor, G.J., Caira, J.N., Jensen, K., Rosana, K.A.M. & White, W.T. (ed.) (2012). A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bulletin of the American Museum of Natural History, pp. 1-262, USA.

Ogretmen, F., Yılmaz, F. & Torcu, K.H. (2005). An investigation on fishes of Gökova Bay (Southern Aegean Sea). BAU Fen Bilimleri Dergisi, 7, 2, 19-36.

Palumbi, S.R., Martin, A.P., Romano, S.L., McMillan, W.O. & Stice, L. (ed.) (1991) The Simple Fool’s Guide to PCR. Dept. of Zoology, University of Hawaii, Honolulu

Ramírez-Amaro, S., Ramírez-Macías, D., Vázquez-Juárez, R., Flores-Ramírez, S. & Galván-Magaña, F. (ed.) (2017). Population structure of the Pacific angel shark (Squatina californica) along the northwestern coast of Mexico based on the mitochondrial DNA control region. Ciencias Marinas, 43, 1, 69-80.

Saglam, N.E., Akyol, O. & Ceyhan, T. (2008). İstanbul balık halinde 1998–2007 yılları arasında i̇şlem gören türler üzerine bir değerlendirme. E.U. Journal of Fisheries and Aquatic Sciences, 25, 1-2, 169-172.

Serena, F. (2005). Field identification guide to the sharks and rays of the Mediterranean and the Black Sea. FAO species identification guide for fishery purposes. Food and Agriculture Organization of the United Nations, Rome, pp. 97.

Shirai, S. (1992). Squalean phylogeny: a new framework of "squaloid" sharks and related taxa. Hokkaido University Press, pp. 151.

Soldo, A. & Bariche, M. (2015). Squatina aculeata. The IUCN Red List of Threatened Species 2015: e.T61417A48957735. [accessed on 18 November 19]

Stelbrink, B., Von, R.T., Cliff, G. & Kriwet, J. (2009). Molecular systematics and global phylogeography of angel sharks (genus Squatina). Molecular Phylogenetics and Evolution, 54, 2, 395-404.

Strauss, R. & Bond, C. (1990). Taxonomic methods: morphology. In: CB. Schreck, PB. Moyle, eds. Methods for fish biology American Fisheries Society, pp. 109–140.

Tekinay, A.A., Alpaslan, M., Özen, Ö., Akyüz, P.E. & Kahyaoğlu, G. (ed.) (2003) A Comparative Analysis of Istanbul Fish Market Records Between 1998 and 2001. E.U. Journal of Fisheries and Aquatic Sciences, 20, 3-4, 413-418.

Turan, C. (2007). Molecular Systematic Analyses of Mediterranean Skates (Rajiformes). Turkish Journal of Zoology, 32, 437-442.

Turan, C. & Erguden, D. (2012). İskenderun Körfezi̇’nde nesli̇ tehli̇ke altinda olan kikirdakli balık türleri. Conference paper.

Unal, V., Acarli, D. & Gordoa, A. (2010). Characteristics of Marine Recreational Fishing in the Canakkale Strait (Turkey). Mediterranean Marine Science, 11, 2, 315-330.

Velez-Zuazo, X. & Agnarsson, I. (2011) Shark tales: A molecular species-level phylogeny of sharks (Selachimorpha, Chondrichthyes). Molecular Phylogenetics and Evolution, 58, 207-217.

Ward, R.D., Hanner, R. & Hebert, P.D. (2009). The campaign to DNA barcode all fishes, Journal of Fish Biology, 74, 329–356.

Zava, B., Fiorentino. F. & Serena, F. (2016). Occurrence of juveniles Squatina oculata Bonaparte, 1840 (Elasmobranchii: Squatinidae) in the Strait of Sicily (Central Mediterranean), Cybium, 40, 4, 341-343.

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Published

2022-03-09

How to Cite

Tuney-Kizilkaya, I. ., & BENGİL, E. G. T. . (2022). Identification complexity of critically endangered Squatina squatina (Linnaeus, 1758) and Squatina aculeata Cuvier, 1829 in the Mediterranean Sea (Turkey). Journal of Wildlife and Biodiversity, 6(4), 9–27. https://doi.org/10.5281/zenodo.6522467