Redescription of the Chilean angel shark Squatina armata (Philippi, 1887) (Squatiniformes, Squatinidae)
Abstract
Angel sharks (Squatina spp. Duméril, 1805) are a group of coastal benthic sharks distributed worldwide, currently including threatened and understudied species. Two species are formally described along the East Pacific coast, the California angel shark S. californica Ayres, 1859 and the Chilean angel shark S. armata (Philippi, 1887). The latter species occurs in the southeastern Pacific and has historically been understudied. Additionally, the original description of S. armata lacks sufficient data to confidently identify individuals of this species compared to modern descriptions, and no type specimen is currently available to ensure specimen identification. Detailed morphological descriptions for identifying species are an essential resource for solving taxonomic issues in groups of morphologically similar species and to promote the conservation of critically endangered species. Therefore, a neotype from the type locality is here designated for S. armata, and a detailed and standardized morphological characterization based on modern taxonomic works is provided. This work contributes in improving the knowledge on the Chilean angel shark taxonomy and provides an improved frame of reference for identifying angel sharks in the East Pacific, especially in areas where species may occur in sympatry.
References
Acero P.A., Tavera J.J., Anguila R. & Hernández L. 2016. A new southern Caribbean species of angel shark (Chondrichthyes, Squaliformes, Squatinidae), including phylogeny and tempo of diversification of American species. Copeia 104 (2): 577–585. https://doi.org/10.1643/CI-15-292
Alvarez Perez J.A. & Wahrlich R. 2005. A bycatch assessment of the gillnet monkfish Lophius gastrophysus fishery off southern Brazil. Fisheries Research 72 (1): 81–95. https://doi.org/10.1016/j.fishres.2004.10.011
Ambily M.N., Zacharia P.U., Najmudeen T.M., Ambily L., Sunil K.T.S., Radhakrishnan M. & Kishor T.G. 2018. First record of African angel shark, Squatina africana (Chondrichthyes: Squatinidae) in Indian waters, confirmed by DNA Barcoding. Journal of Ichthyology 58: 312–317. https://doi.org/10.1134/S0032945218030013
Alioto D. 2012. A Review of the Systematics of Angel Sharks Emphasizing the Species of the Eastern Pacific Region with a Modified Set of Morphometrics for Order Squatiniformes. Master of Arts in Biology Thesis, University of California, Los Angeles.
Ayres W.O. 1859. On new fishes of the California coast. Proceedings of the California Academy of Sciences (Series 1) 2: 25–32.
Baremore I.E., Murie D.J. & Carlson J.K. 2010. Seasonal and size-related differences in diet of the Atlantic angel shark Squatina dumeril in the northeastern Gulf of Mexico. Aquatic Biology 8: 125–136. https://doi.org/10.3354/ab00214
Bigelow H.B. & Schroeder W.C. 1948. Fishes of the Western North Atlantic. Part I. Lancelets, Cyclostomes and Sharks. Memoirs of the Sears Foundation for Marine Research, New Haven, Connecticut. https://doi.org/10.5962/bhl.title.7464
Cañedo-Apolaya R.M., Ortiz-Alvarez C., Alfaro-Cordova E., Alfaro-Shigueto J., Velez-Zuazo X., Mangel J.C., Siccha-Ramirez R., Yamashiro C. & Ramirez J.L. 2021. Species delimitation of Southeast Pacific angel sharks (Squatina spp.) reveals hidden diversity through DNA Barcoding. Diversity 13 (5): 177. https://doi.org/10.3390/d13050177
Carugati L., Melis R., Cariani A., Cau A., Crobe V., Ferrari A., Follesa M.C., Geraci M.L., Iglésias S.P., Pesci P., Tinti F. & Cannas R. 2021. Combined COI barcode-based methods to avoid mislabelling of threatened species of deep-sea skates. Animal Conservation 25 (1): 38–52. https://doi.org/10.1111/acv.12716
Carvajal J. 1974. Records of Cestodes from Chilean sharks. The Journal of Parasitology 60 (1): 29–34. https://doi.org/10.2307/3278674
Castro-Aguirre J.L., Espinosa Pérez H. & Huidobro Campos L. 2006. Dos nuevas especies del género Squatina (Chondrichthyes: Squatinidae) del Golfo de México. Revista de Biología Tropical 54 (3): 1031–1040.
Castro Romero R. & Baeza Kuroki H. 1987. Eudactylina tuberifera n. sp. (Copepoda, Eudactylinidae) parasitic on Squatina armata (Philippi) (Pisces, Squatinidae) in Chilean Waters. Crustaceana 52 (2): 163–171.
Chai A., Yamaguchi A., Furumitsu K. & Zhang J. 2016. Mitochondrial genome of Japanese angel shark Squatina japonica (Chondrichthyes: Squatinidae). Mitochondrial DNA Part A, 27 (2): 832–833. https://doi.org/10.3109/19401736.2014.919463
Colonello J.H., Lucifora L.O. & Massa A.M. 2007. Reproduction of the angular angel shark (Squatina guggenheim): geographic differences, reproductive cycle, and sexual dimorphism. ICES Journal of Marine Science 64 (1): 131–140. https://doi.org/10.1093/icesjms/fsl004
Compagno L.J.V. 1984. FAO Species Catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 1 – Hexanchiformes to Lamniformes. FAO Fisheries Synopsis 125: 1–249. Rome, FAO.
Compagno L.J.V., Dando M. & Fowler S. 2005. A Field guide to the Sharks of the World. HarperCollins Publishers Ltd., London.
Concha F.J., Caira J.N., Ebert D.A. & Pompert J.H.W. 2019. Redescription and taxonomic status of Dipturus chilensis (Guichenot, 1848), and description of Dipturus lamillai sp. nov. (Rajiformes: Rajidae), a new species of long-snout skate from the Falkland Islands. Zootaxa 4590 (5): 501–524. https://doi.org/10.11646/zootaxa.4590.5.1
Conix S. 2019. Taxonomy and conservation science: interdependent and value-laden. History and Philosophy of the Life Sciences 41: 15. https://doi.org/10.1007/s40656-019-0252-3
Corrigan S., Yang L., Cosmann P.J. & Naylor G.J.P. 2016. A description of the mitogenome of the Endangered Taiwanese angelshark, Squatina formosa. Mitochondrial DNA Part A 27 (2): 1305–1306. https://doi.org/10.3109/19401736.2014.945568
Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109
Dubois A. 2003. The relationships between taxonomy and conservation biology in the century of extinctions. Comptes Rendus Biologies 326: 9–21. https://doi.org/10.1016/S1631-0691(03)00022-2
Dulvy N.K., Sadovy Y. & Reynolds J.D. 2003. Extinction vulnerability in marine populations. Fish and Fisheries 4 (1): 25-64. https://doi.org/10.1046/j.1467-2979.2003.00105.x
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. & White W.T. 2014. Extinction risk and conservation of the world’s sharks and rays. eLife 3: e00590. https://doi.org/10.7554/eLife.00590
Dulvy N.K., Acuña E., Bustamante C., Cevallos A., Herman K., Navia A.F., Pardo S.A. & Velez-Zuazo X. 2020. Squatina armata. The IUCN Red List of Threatened Species 2020: e.T44571A116831653. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T44571A116831653.en
Dulvy N.K., Pacoureau N., Rigby C.L., Pollom R.A., Jabado R.W., Ebert D.A., Finucci B., Pollock C.M., Cheo J., Derrick D.H., Herman K.B., Sherman C.S., VanderWright W.J., Lawson J.M., Walls R.H.L., Carlson J.K., Charvet P., Bineesh K.K., Fernando D., Ralph G.M., Matsushiba J.H., Hilton-Taylor C., Fordham S.V. & Simpfendorfer C.A. 2021. Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology 31 (21): 4773–4787.e8. https://doi.org/10.1016/j.cub.2021.08.062
Ebert D.A., Dando M. & Fowler S. 2021. Sharks of the World: A Complete Guide. Wild Nature Press.
Elliott-Rodríguez W. & Paredes-Bulnes F. 1997. Características de la estructura especiológica del subsistema demersal durante el invierno de 1996. Informe del Instituto del Mar del Perú 124: 57–70.
Filatov D.A. 2009. Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25 (23): 3189–3190. https://doi.org/10.1093/bioinformatics/btp572
Fouts W.R. & Nelson D.R. 1999. Prey capture by the Pacific angel shark, Squatina californica: visually mediated strikes and ambush-site characteristics. Copeia 1999 (2): 304–312. https://doi.org/10.2307/1447476
Fricke R., Eschmeyer W.N. & Van der Laan R. (eds) 2023. Eschmeyer’s Catalog of Fishes: Genera, Species, References. Available from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp [accessed 28 Nov. 2023].
Gabbanelli V., Díaz de Astarloa J., González-Castro M., Vázquez D. & Mabragaña E. 2018. Almost a century of oblivion: Integrative taxonomy allows the resurrection of the longnose skate Zearaja brevicaudata (Marini, 1933) (Rajiformes; Rajidae). Comptes Rendus Biologies 341 (9–10): 454–470. https://doi.org/10.1016/j.crvi.2018.10.002
Gao Y., Liu T., Wei T., Geng X., Wang J. & Ma H. 2016. Complete mitochondrial genome of clouded angelshark (Squatina nebulosa). Mitochondrial DNA Part A 27 (3): 1599–1600. https://doi.org/10.3109/19401736.2014.958687
Hernández S., González M.T., Villarroel J.C. & Acuña E. 2010. Seasonal variation in fish bycatch associated with an artisanal flounder fishery on Coquimbo Bay, Chile. Revista de Biología Marina y Oceanografía 45 (Supl. 1): 695–703. https://doi.org/10.4067/S0718-19572010000400013
Hiddink J.G., Shepperson J., Bater R., Goonesekera D. & Dulvy N.K. 2019. Near disappearance of the Angelshark Squatina squatina over half a century of observations. Conservation Science and Practice 1 (9): e97. https://doi.org/10.1111/csp2.97
ICZN 1999. International Code of Zoological Nomenclature, 4th Edition. The International Trust for Zoological Nomenclature, London. https://doi.org/10.5962/bhl.title.50608
Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33 (7): 1870–1874. https://doi.org/10.1093/molbev/msw054
Last P.R. & White W.T. 2008. Three new angel sharks (Chondrichthyes: Squatinidae) from the Indo-Australian region. Zootaxa 1734: 1–26. https://doi.org/10.11646/zootaxa.1734.1.1
Last P.R., White W.T., Pogonoski J.J. & Gledhill D.C. 2008. New Australian skates (Batoidea: Rajoidei) — background and methodology. In: Last P.R., White W.T., Pogonoski J.J. & Gledhill D.C. (eds) Descriptions of New Australian Skates (Batoidea: Rajoidei). CSIRO Marine & Atmospheric Research Paper 021: 1–8.
Last P.R., White W.T., Carvalho M.R. de, Séret B., Stehmann M.F.W. & Naylor G.J.P. (eds) 2016. Rays of the World. CSIRO Publishing, Melbourne. https://doi.org/10.1071/9780643109148
Lawson J.M., Pollom R.A., Gordon C.A., Barker J., Meyers E.K.M., Zidowitz H., Ellis J.R., Bartolí Á., Morey G., Fowler S.L., Jiménez Alvarado D., Fordham S.V., Sharp R., Hood A.R. & Dulvy N.K. 2019. Extinction risk and conservation of critically endangered angel sharks in the Eastern Atlantic and Mediterranean Sea. ICES Journal of Marine Science 77 (1): 12–29. https://doi.org/10.1093/icesjms/fsz222
Long D.J., Ebert D.A., Tavera J., Acero P.A. & Robertson D.R. 2021. Squatina mapama n. sp., a new cryptic species of angel shark (Elasmobranchii: Squatinidae) from the southwestern Caribbean Sea. Journal of the Ocean Science Foundation 38: 113–130. https://doi.org/10.5281/ZENODO.5806693
López-Romero F.A., Stumpf S., Pfaff C., Marramà G., Johanson Z. & Kriwet J. 2020. Evolutionary trends of the conserved neurocranium shape in angel sharks (Squatiniformes, Elasmobranchii). Scientific Reports 10: 12582. https://doi.org/10.1038/s41598-020-69525-7
Mace G.M. 2004. The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society B: Biological Sciences 359 (1444): 711–719. https://doi.org/10.1098/rstb.2003.1454
Maddison W.P. & Maddison D.R. 2017. Mesquite: a modular system for evolutionary analysis. Version 3.31. Available from http://mesquiteproject.org [accessed 28 Nov. 2023].
McNeely J.A. 2002. The role of taxonomy in conserving biodiversity. Journal for Nature Conservation 10 (3): 145–153. https://doi.org/10.1078/1617-1381-00015
Meyers E.K.M., Tuya F., Barker J., Jiménez Alvarado D., Castro-Hernández J.J., Haroun R. & Rödder D. 2017. Population structure, distribution and habitat use of the Critically Endangered Angelshark, Squatina squatina, in the Canary Islands. Aquatic Conservation: Marine and Freshwater Ecosystems 27 (6): 1133–1144. https://doi.org/10.1002/aqc.2769
Naylor G.J.P., Ryburn J.A., Fedrigo O. & López J.A. 2005. Phylogenetic relationships among the major lineages of modern elasmobranchs. In: Hamlett W.C. (ed.) Reproductive Biology and Phylogeny of Chondrichthyes 3, CRC Press, Boca Raton. https://doi.org/10.1201/9781439856000
Naylor G.J.P., Caira J.N., Jensen K., Rosana K.A.M., Straube N. & Lakner C. 2012. Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier J.C., Musick J.A. & Heithaus M.R. (eds) Biology of Sharks and their Relatives 2nd Ed.: 31–56. CRC Press, Boca Raton. https://doi.org/10.1201/b11867
Padial J.M., Miralles A., De la Riva I. & Vences M. 2010. The integrative future of taxonomy. Frontiers in Zoology 7: 16. https://doi.org/10.1186/1742-9994-7-16
Norman J.R. 1937. Coast fishes. Part II. The Patagonian region. Discovery Reports 16: 1–150. https://doi.org/10.5962/bhl.part.29326
Ottoni F.P., South J., Azevedo-Santos V.M., Henschel E. & de Bragança P.H.N. 2023. Editorial: freshwater biodiversity crisis: multidisciplinary approaches as tools for conservation. Frontiers in Environmental Science 11: 1155608. https://doi.org/10.3389/fenvs.2023.1155608
Palumbi S.R., Martin A.P., Romano S., McMillan W.O., Stice L. & Grabowski G. 1991. The Simple Fool’s Guide to PCR, version 2.0. Published and distributed by the authors. Available from https://searchworks.stanford.edu/view/9267895 [accessed 28 Nov. 2023].
Philippi R.A. 1887. Historia natural: sobre los tiburones i algunos otros peces de Chile. Anales de la Universidad de Chile (1887) 71 (sección 1): 535–574. Available from https://doi.org/10.5354/0717-8883.1887.23750 [accessed 15 Apr. 2024]-
Puentes V., Madrid N. & Zapata L.A. 2007. Catch composition of the deep sea shrimp fishery (Solenosera agassizi Faxon, 1893; Farfantepenaeus californiensis Holmes, 1900 and Farfantepenaeus brevirostris Kinglsey, 1878) in the Colombian Pacific Ocean. Gayana 71 (1): 84–95. https://doi.org/10.4067/S0717-65382007000100009
Quero J.-C. 1998. Changes in the Euro-Atlantic fish species composition resulting from fishing and ocean warming. Italian Journal of Zoology 65 (Supp. 1): 493–499. https://doi.org/10.1080/11250009809386873
Rambaut A. 2016. FigTree: tree figure drawing tool. Available from http://tree.bio.ed.ac.uk/software/figtree/ [accessed 15 Apr. 2024].
Raoult V., Peddemors V. & Williamson J.E. 2017. Biology of angel sharks (Squatina sp.) and sawsharks (Pristiophorus sp.) caught in south-eastern Australian trawl fisheries and the New South Wales shark-meshing (bather-protection) program. Marine and Freshwater Research 68: 207–212. https://doi.org/10.1071/MF15369
Richards V.P., Henning M., Witzell W. & Shivji M.S. 2009. Species delineation and evolutionary history of the globally distributed spotted eagle ray (Aetobatus narinari). Journal of Heredity 100 (3): 273–283. https://doi.org/10.1093/jhered/esp005
Rokas A. & Carroll S.B. 2005. More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Molecular Biology and Evolution 22 (5): 1337–1344. https://doi.org/10.1093/molbev/msi121
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61 (3): 539–542. https://doi.org/10.1093/sysbio/sys029
Stelbrink B., von Rintelen T., Cliff G. & Kriwet J. 2010. Molecular systematics and global phylogeography of angel sharks (genus Squatina). Molecular Phylogenetics and Evolution 54 (2): 395–404. https://doi.org/10.1016/j.ympev.2009.07.029
Vaz D.F.B. & 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. https://doi.org/10.11646/zootaxa.3695.1.1
Vaz D.F.B. & de Carvalho M.R. 2018. New species of Squatina (Squatiniformes: Squatinidae) from Brazil, with comments on the taxonomy of angel sharks from the Central and Northwestern Atlantic. Copeia 106 (1): 144–160. https://doi.org/10.1643/CI-17-606
Velázquez-Chiquito V.M., Méndez-Macías J.S., Estupiñán-Montaño C. & Galván-Magaña F. 2021. Dietary ecology and trophic level of adults of the Chilean angel shark Squatina armata Philippi 1887 in the Central-Eastern Pacific Ocean. Regional Studies in Marine Science 43: 101675. https://doi.org/10.1016/j.rsma.2021.101675
Vélez-Zuazo X. & Agnarsson I. 2011. Shark tales: a molecular species-level phylogeny of sharks (Selachimorpha, Chondrichthyes). Molecular Phylogenetics and Evolution 58 (2): 207–217. https://doi.org/10.1016/j.ympev.2010.11.018
Walsh J.H. & Ebert D.A. 2007. A review of the systematics of western North Pacific angel sharks, genus Squatina, with redescriptions of Squatina formosa, S. japonica, and S. nebulosa (Chondrichthyes: Squatiniformes, Squatinidae). Zootaxa 1551 (1): 31–47. https://doi.org/10.11646/zootaxa.1551.1.2
Walsh J.H., Ebert D.A. & Compagno L.J.V. 2011. Squatina caillieti sp. nov. a new species of angel shark (Chondrichthyes: Squatiniformes: Squatinidae) from the Philippine Islands. Zootaxa 2759 (1): 49–59. https://doi.org/10.11646/zootaxa.2759.1.2
Weigmann S. 2016. Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. Journal of Fish Biology 88 (3): 837–1037. https://doi.org/10.1111/jfb.12874
Weigmann S., Vaz D.F.B., Akhilesh K.V., Leeney R.H. & Naylor G.J.P. 2023. Revision of the Western Indian Ocean angel sharks, genus Squatina (Squatiniformes, Squatinidae), with description of a new species and redescription of the African angel shark Squatina africana Regan, 1908. Biology 12 (7): 975. https://doi.org/10.3390/biology12070975
White W.T., Last P., Naylor G., Jensen K. & Caira J. 2010. Clarification of Aetobatus ocellatus (Kuhl, 1823) as a valid species, and a comparison with Aetobatus narinari (Euphrasen, 1790) (Rajiformes: Myliobatidae). In: Last P., White W.T. & Pogonoski J.J. (eds) Descriptions of New Sharks and Rays from Borneo: 141–164.. CSIRO Marine and Atmospheric Research Paper no. 32. Available from http://hdl.handle.net/102.100.100/107849?index=1 [accessed 28 Nov. 2023].
White W.T., Furumitsu, K. & Yamaguchi, A. 2013. A new species of eagle ray Aetobatus narutobiei from the Northwest Pacific: an example of the critical role taxonomy plays in fisheries and ecological sciences. PLoS ONE 8 (12): e83785. https://doi.org/10.1371/journal.pone.0083785
Xia X. 2017. DAMBE6: new tools for microbial genomics, phylogenetics, and molecular evolution. Journal of Heredity 108 (4): 431–437. https://doi.org/10.1093/jhered/esx033
Yáñez P.A. 1951. Algunos datos y observaciones sobre nuestro pez ángel (Squatina armata (Phil. 1887). Revista de Biología Marina y Oceanografía 3: 150–153. Available from https://rbmo.uv.cl/escaneados/3-150.pdf [accessed 15 Apr. 2024].
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