Phylogeography of eagle rays of the genus Aetobatus: Aetobatus narinari is restricted to the continental western Atlantic Ocean

  • João Bráullio L. SalesEmail author
  • Cintia Negrão de Oliveira
  • Wagner César Rosa dos Santos
  • Matheus Marcos Rotundo
  • Yrlene Ferreira
  • Jonathan Ready
  • Iracilda Sampaio
  • Claudio Oliveira
  • Vanessa P. Cruz
  • Raul E. Lara-Mendoza
  • Luis Fernando da Silva Rodrigues-Filho
Primary Research Paper


The biogeography and conservation of elasmobranch species was increasingly addressed in the recent past, but the southwestern Atlantic Ocean fauna is still one of the least studied. Reliable delimitation of the distribution range of species is fundamental to conservation and development of fisheries management strategies. A recent molecular study of the cryptic Aetobatus narinari species complex restricted that species to western and eastern coasts of the New World. However, the current distribution of A. narinari and phylogenetic relationships within the genus Aetobatus have yet to be clarified, the goal of this phylogeographic analysis. Using mitochondrial and nuclear markers we investigated specimens from the Atlantic coast of Brazil and the Pacific coast of Mexico and related them to previously analyzed specimens from other regions. Our analysis indicates that Aetobatus narinari is present only in the western Atlantic, formed by a single genetic lineage that ranges between Florida and southeastern Brazil, while the Pacific New World lineage is in fact assigned to Aetobatus laticeps. Analysis of divergence times revealed that biogeographic events such as the closure of the Tethys Sea, the formation of the Benguela barrier, and the Isthmus of Panama played major roles in diversification and dispersal of the genus Aetobatus.


Elasmobranchii Aetobatidae Species delimitation Conservation DNA sequences 



We are grateful to CEPNOR, in the person of Alex Klautau, for providing infrastructure and access to the Brazilian North Coast fishery fleet, Franklin Solis Carbache from Ecuador for the images of A. laticeps, Priscila Araújo at UFPE for the images of A. narinari from Pernambuco, the fishers of the “Pro-fishery = fishing for knowledge” Project, for providing samples from southeastern Brazil, and CNPq for financial support through Project Number 474843/2013-0 Granted to Luis Fernando da Silva Rodrigues-Filho.

Supplementary material

10750_2019_3949_MOESM1_ESM.jpg (169 kb)
Supplementary material 1 (JPEG 169 kb) Supplementary data S1: Species, codes used in the present study, origin of the samples, and original references for the sequences analyzed in this study. The codes for samples of the present study correspond to COI, Cytb and ITSII respectively
10750_2019_3949_MOESM2_ESM.docx (19 kb)
Supplementary material 2 (DOCX 18 kb) Supplementary data S2: Divergence time tree estimated from a strict clock analysis including all the calibration points used in the present analysis


  1. Allen, G. R., 2008. Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquatic Conservation: Marine and Freshwater Ecosystems 18: 541–556.CrossRefGoogle Scholar
  2. Amaral, A. C. Z. & S. Jablonski, 2005. Conservação da biodiversidade marinha e costeira no Brasil. Megadiversidade 1: 43–51.Google Scholar
  3. Amorim, P. F. & W. J. Costa, 2018. Multigene phylogeny supports diversification of four-eyed fishes and one-sided livebearers (Cyprinodontiformes: Anablepidae) related to major South American geological events. PLoS ONE 13: e0199201.CrossRefGoogle Scholar
  4. Arlyza, I. S., K. N. Shen, D. D. Solihin, D. Soedharma, P. Berrebi & P. Borsa, 2013. Species boundaries in the Himantura uarnak species complex (Myliobatiformes: Dasyatidae). Molecular Phylogenetics and Evolution 66: 429–435.CrossRefGoogle Scholar
  5. Aschliman, N. C., M. Nishida, M. Miya, J. G. Inoue, K. M. Rosana & G. J. Naylor, 2012. Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Molecular Phylogenetics and Evolution 63: 28–42.CrossRefGoogle Scholar
  6. Bacon, C. D., D. Silvestro, C. Jaramillo, B. T. Smith, P. Chakrabarty & A. Antonelli, 2015. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proceedings of the National Academy of Sciences 112: 6110–6115.CrossRefGoogle Scholar
  7. Bellwood, D. R. & P. C. Wainwright, 2002. The History and Biogeography of Fishes on Coral Reefs. Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem, 5–32.Google Scholar
  8. Berthe, C., J. Mourier, D. LeCChini, J. L. Rummer, D. Y. Sellos & S. P. Iglésias, 2016. DNA barcoding supports the presence of the cryptic ocellated eagle ray, Aetobatus ocellatus (Myliobatidae), in French Polynesia, South Pacific. CYBIUM 40: 181–184.Google Scholar
  9. Betancur-R, R. & J. W. Armbruster, 2009. Molecular clocks provide new insights into the evolutionary history of Galeichthyine sea catfishes. Evolution 63: 1232–1243.CrossRefGoogle Scholar
  10. Bigelow, H. B., & W. C. Schoroeder, 1953. Sawfish, guitarfish, skates and rays. Fishes of the Wester North Atlantic. Part 2. Memmoir Sears Foundation for Marine Research. Yale University, New Haven: 588.Google Scholar
  11. Bineesh, K. K., A. Gopalakrishnan, K. V. Akhilesh, K. A. Sajeela, E. M. Abdussamad, N. G. K. Pillai, V. S. Basheer, J. K. Jena & R. D. Ward, 2017. DNA barcoding reveals species composition of sharks and rays in the Indian commercial fishery. Mitochondrial DNA Part A 28: 458–472.CrossRefGoogle Scholar
  12. Bornatowski, H., R. R. Braga & J. R. S. Vitule, 2014. Threats to sharks in a developing country: the need for effective simple conservation measures. Natureza & Conservação 12: 11–18.CrossRefGoogle Scholar
  13. Briggs, J. C. & B. W. Bowen, 2012. A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography 39: 12–30.CrossRefGoogle Scholar
  14. Carmona, N., I. Sampaio, S. Santos, R. F. C. Souza & H. Schneider, 2008. Identificação de arraias marinhas comerciais da costa norte brasileira com base em sequências deDNA mitocondrial. Boletim Técnico-Científico do CEPNOR 8: 1–10.CrossRefGoogle Scholar
  15. Chabot, C. L. & L. G. Allen, 2009. Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Molecular Ecology 18: 545–552.CrossRefGoogle Scholar
  16. Clarke, T. M., M. Espinoza, R. Ahrens & I. S. Wehrtmann, 2016. Elasmobranch bycatch associated with the shrimp trawl fishery off the Pacific coast of Costa Rica, Central America. Fishery Bulletin 114: 1–17.CrossRefGoogle Scholar
  17. Clarke, T. M., M. Espinoza, R. R. Chaves & I. S. Wehrtmann, 2018. Assessing the vulnerability of demersal elasmobranchs to a data-poor shrimp trawl fishery in Costa Rica, Eastern Tropical Pacific. Biological Conservation 217: 321–328.CrossRefGoogle Scholar
  18. Compagno, L. J. V. & P. R. Last, 1999. Myliobatidae. Eagle rays. In Carpenter, K. E. & V. Niem (eds), FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific. Food and Agricultural Organization, Rome: 1511–1519.Google Scholar
  19. Cronin, T. M. & H. J. Dowsett, 1996. Biotic and oceanographic response to the Pliocene closing of the Central American Isthmus. Evolution and Environment in Tropical AMERICA: 76–104.Google Scholar
  20. Cuevas-Zimbrón, E., J. C. Pérez-Jiménez & I. Méndez-Loeza, 2011. Spatial and seasonal variation in a target fishery for spotted eagle ray Aetobatus narinari in the southern Gulf of Mexico. Fisheries Science 77: 723.CrossRefGoogle Scholar
  21. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. Scholar
  22. Davidson, L. N., M. A. Krawchuk & N. K. Dulvy, 2016. Why have global shark and ray landings declined: improved management or overfishing? Fish and Fisheries 17: 438–458.CrossRefGoogle Scholar
  23. Domingues, R. R., A. W. S. Hilsdorf & O. B. F. Gadig, 2017. The importance of considering genetic diversity in shark and ray conservation policies. Conservation Genetics 19: 1–25.Google Scholar
  24. Drummond, A. & A. G. Rodrigo, 2000. Reconstructing genealogies of serial samples under the assumption of a molecular clock using serial-sample UPGMA. Molecular Biology and Evolution 17: 1807–1815.CrossRefGoogle Scholar
  25. Drummond, A., R. Forsberg & A. G. Rodrigo, 2001. The inference of stepwise changes in substitution rates using serial sequence samples. Molecular Biology and Evolution 18: 1365–1371.CrossRefGoogle Scholar
  26. Drummond, A. J. & A. Rambaut, 2007. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.CrossRefGoogle Scholar
  27. Dulvy, N. K., S. L. Fowler, J. A. Musick, R. D. Cavanagh, P. M. Kyne, L. R. Harrison, J. K. Carlson, L. N. Davidson, S. V. Fordham, M. P. Francis, et al., 2014. Extinction risk and conservation of the world’s sharks and rays. Elife. 3: e00590.CrossRefGoogle Scholar
  28. Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. Scholar
  29. Eschmeyer, W. N., 2009. The Catalogue of Fishes 162 online. (California Academy of Sciences: San Francisco) Available from: july, 2019).
  30. Euphrasen, B. A., 1790. Raja (narinari). Kongl Vet Acad Handl. 11:217–219.Google Scholar
  31. Excoffier, L., G. Laval & S. Schneider, 2005. An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.Google Scholar
  32. Feitosa, L. M., A. P. B. Martins, T. Giarrizzo, W. Macedo, I. L. Monteiro, R. Gemaque, J. L. S. Nunes, F. Gomes, H. Schneider, I. Sampaio, R. Souza, J. B. L. Sales, et al., 2018. DNA-based identification reveals illegal trade of threatened shark species in a global elasmobranch conservation hotspot. Scientific Reports 8: 3347.CrossRefGoogle Scholar
  33. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.CrossRefGoogle Scholar
  34. Floeter, S. R., L. A. Rocha, D. R. Robertson, J. C. Joyeux, W. F. Smith-Vaniz, P. Wirtz, et al., 2008. Atlantic reef fish biogeography and evolution. Journal of Biogeography 35: 22–47.Google Scholar
  35. Forsskål, P., 1775. Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quae in itinere orientali observavit. Post mortem auctoris edidit Carsten Niebuhr. Hauniae: 164.Google Scholar
  36. Fowler, H. W., 1941. The fishes of the groups Elasmobranchii, Holocephali, Isospondyli, and Ostariophysi obtained by United States Bureau of Fisheries Steamer Albatross in 1907 to 1910, chiefly in the Philippine Islands and adjacent seas. Bulletin of the United States National Museum 13: 1–879.Google Scholar
  37. Frankham, R., J. D. Ballou & D. A. Briscoe, 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge (UK).CrossRefGoogle Scholar
  38. Frédou, F. L. & M. Asano-Filho, 2006. Recursos pesqueiros da região norte. In: Ministério do Meio Ambiente, (eds), Secretaria de Qualidade Ambiental. Programa REVIZEE: Avaliação do Potencial Sustentável de Recursos Vivos na Zona Economica Exclusiva: Relatório Executivo/MMA, Ministério do Meio Ambiente, Brasilia, Brazil: 121–152.Google Scholar
  39. García-De León, F. J., C. Galván-Tirado, L. S. Velasco, C. A. Silva-Segundo, R. Hernández-Guzmán, I. de los Barriga-Sosa, P. D. Jaimes, M. Canino & P. Cruz-Hernández, 2018. Role of oceanography in shaping the genetic structure in the North Pacific hake Merluccius productus. PLoS ONE 13: e0194646.CrossRefGoogle Scholar
  40. Garman, S., 1913. The Plagiostomia (sharks, skates and rays). Memoirs of the Museum of Comparative Zoology, Harvard 36: 1–515.Google Scholar
  41. Gemaque, R., I. L. Monteiro, F. Gomes, D. Sodré, I. Sampaio, J. B. L. Sales & L. F. S. Rodrigues-Filho, 2017. Why implement measures to conserve the diversity of Elasmobranchs? The case of the northern coast of Brazil. Revista da Biologia 17: 1–7. Scholar
  42. Goren, M. & M. Dor, 1994. An Updated Checklist of the Fishes of the Red Sea (CLOFRES II). The Israel Academy of Sciences and Humanities, Jerusalem, Israel: 120.Google Scholar
  43. Guidon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordjik & O. Gascuel, 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307.CrossRefGoogle Scholar
  44. Herrera-Valdivia, E., J. López-Martínez, Castillo S. Vargasmachuca & A. R. García-Juárez, 2016. Taxonomic and functional diversity of the bycatch fishes community of trawl fishing from Northern Gulf of California, Mexico. Revista de biologia Tropical 64: 587–602.CrossRefGoogle Scholar
  45. Ho, S. Y. W., M. J. Phillips, A. Cooper & A. J. Drummond, 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divrgence time. Molecular Biology and Evolution 22: 1561–1568.CrossRefGoogle Scholar
  46. Hoeksema, B. W., 2007. Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In: Biogeography, Time, and Place: Distributions, Barriers, and Islands. Springer, Dordrecht: 117–178.Google Scholar
  47. Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. D. T. Thierer, B. Asthon, P. Meintjes & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.CrossRefGoogle Scholar
  48. Knowlton, N., L. A. Weigt, L. A. Solorzano, D. K. Mills & E. Bermingham, 1993. Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science, New Series 260: 1629–1632.Google Scholar
  49. Kottelat, M., 2013. The fishes of the inland waters of Southeast Asia: a catalogue and core bibliography of the fishes known to occur in freshwaters, mangroves and estuaries. The Raffles Bulletin of Zoology 27: 1–663.Google Scholar
  50. Kuhl, H. in van Hasselt, J.C., 1823. Uittreksel uit een’ brief van Dr. J. C. van Hasselt, aan den Heer C. J. Temminck. Algemein Konst- en Letter-bode I Deel (no. 20): 315–317.Google Scholar
  51. Kyne, P. M. & C. A. Simpfendorfer, 2007. A collation and summarization of available data on deepwater chondrichthyans: biodiversity, life history and fisheries. A report prepared by the IUCN SSC Shark Specialist Group for the Marine Conservation Biology Institute: 137.Google Scholar
  52. Kyne, P. M., H. Ishihara, S. F. J. Dudley & W. T. White, 2006. Aetobatus narinari. 2007 IUCN red list of threatened species. Available from: URL Accessed August 02 2018.
  53. Last, P. R., G. J. P. Naylor & M. Manjaji-Matsumoto, 2016. A revised classification of the family Dasyatidae (Chondrychthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa 4139: 345–368.CrossRefGoogle Scholar
  54. Lessa, R., V. S. Batista & F. M. Santana, 2016. Close to extinction? The collapse of the endemic daggernose shark (Isogomphodon oxyrhynchus) off Brazil. Global Ecology and Conservation 7: 70–81.CrossRefGoogle Scholar
  55. Lessios, H. A., 2008. The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology, Evolution, and Systematics 39: 63–91.CrossRefGoogle Scholar
  56. Lim, K. C., P. E. Lim, V. C. Chong & K. H. Loh, 2015. Molecular and morphological analyses reveals phylogenetic relationships of stingrays focusing on the Family Dasyatidae (Myliobatiformes). PLoS ONE 10: e0120518.CrossRefGoogle Scholar
  57. Marie, A. D. & J. L. Justine, 2005. Monocotylids (Monogenea: Monopisthocotylea) from Aetobatus cf. narinari off New Caledonia, with a description of Decacotyle elpora n. sp. Systematic Parasitology 60: 175–185.CrossRefGoogle Scholar
  58. Marlow, J. R., C. B. Lange, G. Wefer & A. Rosell-Melé, 2000. Upwelling intensification as part of the Pliocene-Pleistocene climate transition. Science 290: 2288–2291.PubMedGoogle Scholar
  59. Mayr, E., 1968. The role of systematics in biology. Science 159: 595–599.CrossRefGoogle Scholar
  60. McEachran, J. D. & M. R. Carvalho, 2002. Myliobatidae p.578-582 In: Carpenter, K. E. 2002. The living marine resources of the Western Central Atlantic. Volume 1: Introduction, mollusks, crustaceans, hagfishes, sharks, batoid fishes, and chimaeras. FAO Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. Rome, FAO: 600.Google Scholar
  61. Meneses, T. S., F. N. Santos & C. W. Pereira, 2005. Fauna de Elasmobrânquios do litoral do estado de Sergipe, Brasil. Arquivos de Ciências do Mar 38: 79–83.Google Scholar
  62. Monteiro-Neto, C., R. A. Tubino, L. E. Moraes, J. P. D. Mendonça-Neto, G. V. Esteves & W. L. Fortes, 2008. Associations de peixes na região costeira de Itaipu, Niterói, RJ. Iheringia, Série Zoologia 98: 50–59.CrossRefGoogle Scholar
  63. Nosil, P., 2008. Speciation with gene flow could be common. Molecular Ecology 17: 2103–2106.CrossRefGoogle Scholar
  64. Oliver, S., M. Braccini, S. J. Newman & E. S. Harvey, 2015. Global patterns in the bycatch of sharks and rays. Marine Policy 54: 86–97.CrossRefGoogle Scholar
  65. Palacios-Barreto, P., V. P. Cruz, F. Foresti, B. D. S. Rangel, M. Uribe-Alcocer & P. Diaz-Jaimes, 2017. Molecular evidence supporting the expansion of the geographical distribution of the Brazilian cownose ray Rhinoptera brasiliensis (Myliobatiformes: Rhinopteridae) in the western Atlantic. Zootaxa 4341: 593–600.CrossRefGoogle Scholar
  66. Palmeira, C. A. M., L. F. S. Rodrigues-Filho, J. B. L. Sales, M. Vallinoto, H. Schneider & I. Sampaio, 2013. Commercialization of a critically endangered species (largetooth sawfish, Pristis perotetti) in fish markets of northern Brazil: authenticity by DNA analysis. Food Control 34: 249–252.CrossRefGoogle Scholar
  67. Pérez-Losada, M., A. Guerra & A. Sanjuan, 2002. Allozyme divergence supporting the taxonomic separation of Octopus mimus and Octopus maya from Octopus vulgaris (Cephalopoda: Octopoda). Bulletin of Marine Science 71: 653–664.Google Scholar
  68. Pinhal, D., M. S. Shivji, M. Vallinoto, D. D. Chapman, O. B. F. Gadig & C. Martins, 2012. Cryptic hammerhead shark lineage occurrence in the Western South Atlantic revealed by DNA analysis. Marine Biology 159: 829–836.CrossRefGoogle Scholar
  69. Polidoro, B. A., T. Brooks, K. E. Carpenter, G. J. Edgar, S. Henderson, J. Sanciangco & D. R. Robertson, 2012. Patterns of extinction risk and threat for marine vertebrates and habitat-forming species in the Tropical Eastern Pacific. Marine Ecology Progress Series 448: 93–104.CrossRefGoogle Scholar
  70. Rambaut, A., 2000. Estimating the rate of molecular evolution: incorporating non contemporaneous sequences into maximum likelihood phylogenies. Bioinformatics 16: 395–399.CrossRefGoogle Scholar
  71. Rambaut, A. & A. J. Drummond, 2007. Tracer v.1.5. Available from Accessed June 03 2018.
  72. Richards, V. P., M. Henning, W. Witzell & M. S. Shivji, 2009. Species delineation and evolutionary history of the globally distributed spotted eagle ray (Aetobatus narinari). Journal of Heredity 100: 273–283.CrossRefGoogle Scholar
  73. Rocha, L. A., D. R. Robertson, C. R. Rocha, J. L. Van Tassell, M. T. Craig & B. W. Bowen, 2005. Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Molecular Ecology 14: 3921–3928.CrossRefGoogle Scholar
  74. Rodrigues-Filho, L. F. S., T. C. D. Rocha, P. S. D. Rêgo, H. Schneider, I. Sampaio & M. Vallinoto, 2009. Identification and phylogenetic inferences on stocks of sharks affected by the fishing industry off the Northern coast of Brazil. Genetics and Molecular Biology 32: 405–413.CrossRefGoogle Scholar
  75. Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Hohn, B. Larget, L. Liu, M. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 22: 539–542. Scholar
  76. Sales, J. B. L., L. F. S. Rodrigues-Filho, Y. D. S. Ferreira, J. Carneiro, N. E. Asp, P. W. Shaw, et al., 2017. Divergence of cryptic species of Doryteuthis plei Blainville, 1823 (Loliginidae, Cephalopoda) in the Western Atlantic Ocean is associated with the formation of the Caribbean Sea. Molecular Phylogenetics and Evolution 106: 44–54.CrossRefGoogle Scholar
  77. Salzburger, W., G. B. Ewing & A. Von Haeseler, 2011. The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20: 1952–1963.CrossRefGoogle Scholar
  78. Shepherd, T. D. & R. A. Myers, 2005. Direct and indirect fishery effects on small coastal elasmobranchs in the northern Gulf of Mexico. Ecology Letters 8: 1095–1104.CrossRefGoogle Scholar
  79. Schluessel, V., 2008. Life history, population genetics and sensory biology of the white spotted eagle ray Aetobatus narinari (Euphrasen, 1790) with emphasis on the relative importance of olfaction. PhD dissertation, The University of Queensland, Brisbane: 368.Google Scholar
  80. Schluessel, V., D. Broderick, S. P. Collin & J. R. Ovenden, 2010. Evidence for extensive population structure in the white-spotted eagle ray within the Indo-Pacific inferred from mitochondrial gene sequences. Journal of Zoology 281: 46–55.CrossRefGoogle Scholar
  81. Schultz, J. K., K. A. Feldheim, S. H. Gruber, M. V. Ashley, T. M. McGovern & B. W. Bowen, 2008. Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology 17: 5336–5348.CrossRefGoogle Scholar
  82. Shannon, L. V., 1985. The Benguela ecosystem Part 1. Evolution of the Benguela, physical features and processes. Oceanography and Marine Biology 23: 105–182.Google Scholar
  83. Simpfendorfer, C. A., M. R. Heupel, W. T. White & N. K. Dulvy, 2011. The importance of research and public opinion to conservation management of sharks and rays: a synthesis. Marine and Freshwater Research 62: 518–527.CrossRefGoogle Scholar
  84. Steininger, F. F. & F. Rogl, 1984. Paleography and palinpastic reconstruction of the Neogene of the Mediterranean and Paratethys. In Dixon, J. E. & A. H. F. Robertson (eds), The Geological Evolution of the Eastern Mediterranean. Blackwell Scientific Publication, Oxford: 6–36.Google Scholar
  85. Steinke, D., T. S. Zemlak, A. D. Connell, P. C. Heemstra & P. D. N. Hebert, 2011. DNA Barcodes: Linking Adults and Immatures of Marine Fishes. Unpublished. Submitted to the EMBL/GenBank/DDBJ databases.Google Scholar
  86. Stevens, J. D., R. Bonfil, N. K. Dulvy & P. A. Walker, 2000. The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57: 476–494.CrossRefGoogle Scholar
  87. Tagliafico, A., N. Rago, S. Rangel & J. Mendoza, 2012. Exploitation and reproduction of the spotted eagle ray (Aetobatus narinari) in the Los Frailes Archipelago, Venezuela. Fishery Bulletin 110: 307–316.Google Scholar
  88. Weir, B. S. & W. G. Hill, 2002. Estimating F-statistics. Annual Review of Genetics 36: 721–750.CrossRefGoogle Scholar
  89. Willughby, F., 1686. De historia piscium libri quatuor, jussu & sumptibus Societatis Regiæ Londinensis editi. Totum opus recognovit, coaptavit, supplevit, librum etiam primum & secundum integros adjecit Johannes Raius e Societate Regia. Theatro Sheldoniano, Oxonii (Oxford). 1: 343.Google Scholar
  90. White, W. T., 2014. A revised generic arrangement for the eagle ray family Myliobatidae, with definitions for the valid genera. Zootaxa 3860: 149–166.CrossRefGoogle Scholar
  91. White, W. T. & A. B. Moore, 2010. Redescription of Aetobatus flagellum (Bloch & Schneider, 1801), an endangered eagle ray (Myliobatoidea: Myliobatidae) from the Indo-West Pacific. Zootaxa 3752: 199–213.CrossRefGoogle Scholar
  92. White, W. T., P. R. Last, G. J. Naylor, K. Jensen & J. N. Caira, 2010. Clarification of Aetobatus ocellatus (Kuhl, 1823) as a valid species, and a comparison with Aetobatus narinari (Euphrasen, 1790) (Rajiformes: Myliobatidae). Descriptions of new sharks and rays from Borneo. CSIRO Marine and Atmospheric Research Paper 32: 141–164.Google Scholar
  93. White, W. T., K. Furumitsu & A. Yamaguchi, 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: 1–11.CrossRefGoogle Scholar
  94. White, W. T. & P. Last, 2016. Family Aetobatidae. In Last, P., G. Naylor, B. Séret, W. White, M. de Carvalho & M. Stehmann (eds), Rays of the World. Csiro Publishing, Clayton.Google Scholar
  95. White, W. T. & G. J. P. Naylor, 2016. Resurrection of the family Aetobatidae (Myliobatiformes) for the pelagic eagle rays, genus Aetobatus. Zootaxa 4139: 435–438.CrossRefGoogle Scholar
  96. White, W. T., S. Corrigan, L. Yang, A. C. Henderson, A. L. Bazinet, D. L. Swofford & G. J. P. Naylor, 2018. Phylogeny of the manta and devilrays (Chondrichthyes: mobulidae), with an updated taxonomic arrangement for the family. Zoological Journal of the Linnean Society 182: 50–75.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • João Bráullio L. Sales
    • 1
    • 2
    Email author
  • Cintia Negrão de Oliveira
    • 2
  • Wagner César Rosa dos Santos
    • 3
  • Matheus Marcos Rotundo
    • 4
  • Yrlene Ferreira
    • 5
  • Jonathan Ready
    • 1
  • Iracilda Sampaio
    • 5
  • Claudio Oliveira
    • 6
  • Vanessa P. Cruz
    • 6
  • Raul E. Lara-Mendoza
    • 7
  • Luis Fernando da Silva Rodrigues-Filho
    • 8
  1. 1.Laboratory of Lepidopterology and Integrated Ichthyology, Center of Advanced Biodiversity Studies (CEABIO)Universidade Federal do ParáBelémBrazil
  2. 2.Faculty of Natural SciencesUniversidade Federal do ParáBrevesBrazil
  3. 3.Northern Brazilian Center of Fishery Research and Extension (CEPNOR)Universidade Federal Rural da Amazonia (UFRA)BelemBrazil
  4. 4.Zoological CollectionUniversidade Santa Cecília (AZUSC-UNISANTA)SantosBrazil
  5. 5.Laboratory of Phylogenomics and BioinformaticsUFPA-IECOSBragançaBrazil
  6. 6.Laboratory of Fish Biology and Genetics, Botucatu Institute of BiosciencesUniversidade Estadual PaulistaBotucatuBrazil
  7. 7.Centro Regional de Investigación Pesquera - Ciudad del Carmen, Instituto Nacional de Pesca. sagarpaCampecheMexico
  8. 8.Graduate Course in Biological SciencesUniversidade Federal Rural da AmazôniaCapanemaBrazil

Personalised recommendations