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Molecular testing of the São Francisco River as an ecological filter for the Brazilian large-eyed stingray Hypanus marianae (Dasyatidae, Myliobatiformes)

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Abstract

Ecological niche modeling (ENM) provides information on the potential environmental barriers to a species that can be tested in phylogeographic studies. A previous ENM analysis of the benthic coastal stingray Hypanus marianae revealed a low suitability area for its occurrence at the São Francisco River (SFR) mouth, the fourth largest river flowing into Southwestern Atlantic. Hence, phylogeographic analyses were used to test the hypothesis of two populations: one north and another south of SFR outflow. We sampled 109 specimens in six localities throughout the species’ geographic distribution and sequenced mitochondrial (cytb) and nuclear (rag1) markers. Our analyses corroborated the existence of two groups (ΦST = 0.68, P < 0.0001) within H. marianae, partially agreeing with the ENM results. The commonest mitochondrial haplotype (H2) was shared among almost all localities, except Salvador, where all individuals shared the same and unique haplotype. This group is restricted to a shallow bay area close to SFR, as predicted by the ENM. However, its plume was not effective in isolating a continental island 55 km off the Brazilian coast. While the broad north group is protected in a few Marine Protected Areas, our results suggest that the restricted southern one deserves to be managed specifically.

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Data availability

The cytb and rag1 sequences have been submitted to the GenBank databases under accession number MZ301320–MZ301428 and MZ301429–MZ301444, respectively.

References

  • Abell, R., M. L. Thieme, C. Revenga, M. Bryer, M. Kottelat, N. Bogutskaya, B. Coad, N. Mandrak, S. C. Balderas, W. Bussing, M. L. J. Stiassny, P. Skelton, G. R. Allen, P. Unmack, A. Naseka, R. Ng, N. Sindorf, J. Robertson, E. Armijo, J. V. Higgins, T. J. Heibel, E. Wikramanayake, D. Olson, H. L. López, R. E. Reis, J. G. Lundberg, M. H. Sabaj Pérez & P. Petry, 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 58: 403–414.

    Article  Google Scholar 

  • Alberoni, A. A. L., I. K. Jeck, C. G. Silva & L. C. Torres, 2020. The new Digital Terrain Model (DTM) of the Brazilian Continental Margin: detailed morphology and revised undersea feature names. Geo-Marine Letters 40: 949–964.

    Article  Google Scholar 

  • Alvarado-Serrano, D. F. & L. L. Knowles, 2014. Ecological niche models in phylogeographic studies: applications, advances and precautions. Molecular Ecology Resources 14: 233–248.

    Article  PubMed  Google Scholar 

  • Bloch, M. E. & J. G. Schneider, 1801. Systema ichthyologie iconibus CX illustratura post obitum arectories opus inchoatum obsoluit, correxit, interpohrit Jo, Gottob Schneider Sano, Berlin:

    Google Scholar 

  • Braccini, M., K. Rensing, T. Langlois & R. McAuley, 2017. Acoustic monitoring reveals the broad-scale movements of commercially important sharks. Marine Ecology Progress Series 577: 121–129.

    Article  Google Scholar 

  • Bruce, T., P. M. Meirelles, G. Garcia, R. Paranhos, C. E. Rezende, R. L. de Moura, E. O. Coni, A. T. Vasconcelos, G. Amado Filho, M. Hatay & R. Schmieder, 2012. Abrolhos Bank Reef health evaluated by means of water quality, microbial diversity, benthic cover, and fish biomass data. PLoS ONE 7: e36687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro, C. B. & D. O. Pires, 2001. Brazilian coral reefs: what we already know and what is still missing. Bulletin of Marine Science 69: 357–371.

    Google Scholar 

  • Cavalcante, G., F. Vieira, E. Campos, N. Brandini & P. R. P. Medeiros, 2020. Temporal streamflow reduction and impact on the salt dynamics of the São Francisco River Estuary and adjacent coastal zone (NE/Brazil). Regional Studies in Marine Science 38: 101363.

    Article  Google Scholar 

  • Ceretta, B. F., C. O. Fogliarini, V. J. Giglio, M. F. Maxwell, L. S. Waechter & M. G. Bender, 2020. Testing the accuracy of biological attributes in predicting extinction risk. Perspectives in Ecology and Conservation 18: 12–18.

    Article  Google Scholar 

  • Cirano, M. & G. C. Lessa, 2007. Oceanographic characteristics of Baía de Todos os Santos, Brazil. Revista Brasileira de Geofísica 25: 363–387.

    Article  Google Scholar 

  • Clement, M., Q. Snell, P. Walke, D. Posada & K. Crandall, 2002. TCS: estimating gene genealogies. In International Parallel and Distributed Processing Symposium. IEEE Computer Society: 184.

  • Cockerham, C. C. & B. S. Weir, 1993. Estimation of gene flow from F-statistics. Evolution 47: 855–863.

    PubMed  Google Scholar 

  • Coelho, J. F. R., S. M. Q. Lima & F. F. Petean, 2020. Phylogenetic conservatism of abiotic niche in sympatric Southwestern Atlantic skates. Marine Biology Research 16: 458–473.

    Article  Google Scholar 

  • Contracting States, 1973. Convention on International Trade in Endangered Species of Wild Fauna and Flora. Contracting States: 1–14.

  • Corcoran, M. J., B. M. Wetherbee, M. S. Shivji, M. D. Potenski, D. D. Chapman & G. M. Harvey, 2013. Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana. PLoS ONE. https://doi.org/10.1371/journal.pone.0059235.

    Article  PubMed  PubMed Central  Google Scholar 

  • Costa, T. L. A., J. A. Thayer & L. F. Mendes, 2015. Population characteristics, habitat and diet of a recently discovered stingray Dasyatis marianae: implications for conservation. Journal of Fish Biology 86: 527–543.

    Article  CAS  PubMed  Google Scholar 

  • Costa, T. L. A., M. G. Pennino & L. F. Mendes, 2017. Identifying ecological barriers in marine environment: the case study of Dasyatis marianae. Marine Environmental Research 125: 1–9.

    Article  CAS  PubMed  Google Scholar 

  • Crooks, K. R., 2006. Connectivity conservation: maintaining connections for nature. In Crooks, K. R. & M. Sanjayan (eds), Connectivity Conservation. Conservation Biology Series Cambridge University Press, Cambridge: 383–405.

    Chapter  Google Scholar 

  • Cruz, V. P., A. M. C. L. Adachi, P. H. Oliveira, G. S. Ribeiro, F. G. Paim, B. C. Souza, A. S. F. Rodrigues, M. Vianna, S. M. Delpiani, J. M. D. de Astarloa, M. M. Rotundo, F. F. Mendonça, C. Oliveira, R. P. Lessa & F. Foresti, 2021. Genetic diversity in two threatened species of guitarfish (Elasmobranchii: Rhinobatidae) from the Brazilian and Argentinian coasts: an alert for conservation. Neotropical Ichthyology 19: 1–15.

    Article  CAS  Google Scholar 

  • Da Cunha, I. M. C., A. S. De Souza, E. A. Dias, K. D. J. Amorim, R. X. Soares, G. W. W. F. Da Costa, E. García-Machado, P. M. Galetti & W. F. Molina, 2014. Genetic multipartitions based on D-loop sequences and chromosomal patterns in brown chromis, Chromis multilineata (Pomacentridae), in the Western Atlantic. BioMed Research International. https://doi.org/10.1155/2014/254698.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dabruzzi, T. F., W. A. Bennett, J. L. Rummer & N. A. Fangue, 2013. Juvenile Ribbontail Stingray, Taeniura lymma (Forsskal, 1775) (Chondrichthyes, Dasyatidae), demonstrate a unique suite of physiological adaptations to survive hyperthermic nursery conditions. Hydrobiologia 701: 37–49.

    Article  CAS  Google Scholar 

  • Dambach, J. & D. Rödder, 2011. Applications and future challenges in marine species distribution modeling. Aquatic Conservation: Marine and Freshwater Ecosystems 21: 92–100.

    Article  Google Scholar 

  • Domingues, R. R., A. W. S. Hilsdorf, M. M. Shivji, F. V. H. Hazin & O. B. F. Gadig, 2017. Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic Ocean. Reviews in Fish Biology and Fisheries 28(5): 1–15.

    Google Scholar 

  • Dominguez, J. M. L. & A. C. S. P. Bittencourt, 2009. Geologia. In Andrade, J. & V. Hatje (eds), Baía de Todos os Santos: aspectos oceanográficos EDUFBA, Salvador: 27–66.

    Google Scholar 

  • Dominguez, J. M. L. & J. K. Guimarães, 2021. Effects of Holocene climate changes and anthropogenic river regulation in the development of a wave-dominated delta: the São Francisco River (eastern Brazil). Marine Geology 435: 106456.

    Article  CAS  Google Scholar 

  • Dulvy, N. K., S. L. Fowler, J. A. Musick, R. D. Cavanagh, P. M. Kyne, L. R. Harrison, J. K. Carlson, L. N. K. Davidson, S. V. Fordham, M. P. Francis, C. M. Pollock, C. A. Simpfendorfer, G. H. Burgess, K. E. Carpenter, L. J. V. Compagno, D. A. Ebert, C. Gibson, M. R. Heupel, S. R. Livingstone, J. C. Sanciangco, J. D. Stevens, S. Valenti & W. T. White, 2014. Extinction risk and conservation of the world’s sharks and rays. eLife e00590: 1–35.

    Google Scholar 

  • Duncan, K. M., A. P. Martin, B. W. Bowen & H. G. De Couet, 2006. Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology 15: 2239–2251.

    Article  CAS  PubMed  Google Scholar 

  • Escobar, N. F. C., J. M. L. Dominguez, M. R. do Zucchi, A. E. G. de Azevedo, A. G. A. N. de Rangel & R. C. Rebouças, 2020. Organic matter in the deltaic clinoform of the São Francisco River (Eastern Brazil). Geo-Marine Letters 40: 879–895.

    Article  CAS  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes, L., A. Green, J. Tanzer, A. T. White, P. M. Aliño, J. Jompa, P. Lokani, A. Soemodinoto, M. Knight, R. S. Pomeroy & H. Possingham, 2012. Biophysical Principles for Designing Resilient Networks of Marine Protected Areas to Integrate Fisheries, Biodiversity and Climate Change Objectives in the Coral Triangle. Coral Triangle Partnership.

  • Figueiredo, I., T. Moura, A. Neves & L. S. Gordo, 2008. Reproductive strategy of leafscale gulper shark Centrophorus squamosus and the Portuguese dogfish Centroscymnus coelolepis on the Portuguese continental slope. Journal of Fish Biology 73: 206–225.

    Article  Google Scholar 

  • Floeter, S. R., R. Z. Guimarães, L. A. Rocha, C. E. Ferreira, C. A. Rangel & J. L. Gasparini, 2001. Geographic variation in reef-fish assemblages along the Brazilian coast. Global Ecology and Biogeography 10: 423–431.

    Article  Google Scholar 

  • Flowers, K. I., M. J. Ajemian, K. Bassos-Hull, K. A. Feldheim, R. E. Hueter, Y. P. Papastamatiou & D. D. Chapman, 2016. A review of batoid philopatry, with implications for future research and population management. Marine Ecology Progress Series 562: 251–261.

    Article  Google Scholar 

  • Gaither, M. R., M. A. Bernal, R. R. Coleman, B. W. Bowen, S. A. Jones, W. B. Simison & L. A. Rocha, 2015. Genomic signatures of geographic isolation and natural selection in coral reef fishes. Molecular Ecology 24: 1543–1557.

    Article  CAS  PubMed  Google Scholar 

  • Gomes, U. L., R. S. Rosa & O. B. F. Gadig, 2000. Dasyatis marianae sp. n.: a new species of stingray (Chondrichthyes: Dasyatidae) from the Southwestern Atlantic. Copeia 2000: 510–515.

    Article  Google Scholar 

  • Graham, R. T., M. J. Witt, D. W. Castellanos, F. Remolina, S. Maxwell, B. J. Godley & L. A. Hawkes, 2012. Satellite tracking of manta rays highlights challenges to their conservation. PLoS ONE 7: e36834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith, E. & C. H. Smith, 1834. The class Pisces, arranged by the Baron Cuvier, with supplementary additions, by Edward Griffith and Lieut.-Col. Charles Hamilton Smith. In Cuvier, G. (ed), The Animal Kingdom, Arranged in Conformity with Its Organization, by the Baron Cuvier, Member of the Institute of France, with Supplementary Additions to Each Order, by Edward Griffith and Others. Whittaker & Co., London: 1–680.

  • Guillot, G., A. Estoup, F. Mortier & J. F. Cosson, 2005a. A spatial statistical model for landscape genetics. Genetics 170: 1261–1280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillot, G., F. Mortier & A. Estoup, 2005b. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5: 712–715.

    Article  CAS  Google Scholar 

  • Hazkani-Covo, E., R. M. Zeller & W. Martin, 2010. Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genetics 6: e1000834.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hildebrand, S. F. & W. C. Schroeder, 1928. Fishes of Chesapeake Bay. US Government Printing Office.

  • Jaine, F. R. A., C. A. Rohner, S. J. Weeks, L. I. E. Couturier, M. B. Bennett, K. A. Townsend & A. J. Richardson, 2014. Movements and habitat use of reef manta rays off eastern Australia: offshore excursions, deep diving and eddy affinity revealed by satellite telemetry. Marine Ecology Progress Series 510: 73–86.

    Article  Google Scholar 

  • Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Mentjies & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Knoppers, B., P. R. P. Medeiros, W. F. L. De Souza & T. Jennerjahn, 2006. The São Francisco estuary. In Brazil Handbook of Environmental Chemistry: Water Pollution, Vol. 5. SCImago: 51–70.

  • Knowles, L. L., B. C. Carstens & M. L. L. Keat, 2007. Coupling genetic and ecological-niche models to examine how past population distributions contribute to divergence. Current Biology 17: 940–946.

    Article  CAS  PubMed  Google Scholar 

  • Last, P. R., B. Séret & G. J. P. Naylor, 2016. A new species of guitarfish, Rhinobatos borneensis sp. nov. with a redefinition of the family-level classification in the order Rhinopristiformes (Chondrichthyes: Batoidea). Zootaxa 4117: 451–475.

    Article  PubMed  Google Scholar 

  • Le Port, A. & S. Lavery, 2012. Population structure and phylogeography of the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the southern hemisphere. Journal of Heredity 103: 174–185.

    Article  PubMed  Google Scholar 

  • Leão, Z. M., R. K. Kikuchi & V. Testa, 2003. Corals and coral reefs of Brazil. In Latin American Coral Reefs. Elsevier Science, Amsterdam: 9–52.

  • Leigh, J. W. & D. Bryant, 2015. PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.

    Article  Google Scholar 

  • Ludt, W. B. & L. A. Rocha, 2015. Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal of Biogeography 42: 25–38.

    Article  Google Scholar 

  • Maddison, W. & L. Knowles, 2006. Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55: 21–30.

    Article  PubMed  Google Scholar 

  • Mallet, J., 2001. Gene flow. In Insect Movement: Mechanisms and Consequences: 337–360.

  • Matute, D. R., 2013. The role of founder effects on the evolution of reproductive isolation. Journal of Evolutionary Biology 26: 2299–2311.

    Article  CAS  PubMed  Google Scholar 

  • Melo-Merino, S. M., H. Reyes-Bonilla & A. Lira-Noriega, 2020. Ecological niche models and species distribution models in marine environments: a literature review and spatial analysis of evidence. Ecological Modelling 415: 35.

    Article  Google Scholar 

  • MMA, 2014. Ministério do Meio Ambiente do Brasil. Portarias Nos. 443, 444, 445, de 17 de Dezembro de 2014, Diário Oficial da União. 245.

  • Motta, F. S., R. L. Moura, R. B. Francini-Filho & R. C. Namora, 2009. Notas sobre a biologia reprodutiva e alimentar de elasmobrânquios no Parque Estadual Marinho Parcel Manoel Luís, Maranhão-Brasil. Pan-American Journal of Aquatic Sciences 4: 593–598.

    Google Scholar 

  • Nakaya, K., W. T. White & H. C. Ho, 2020. Discovery of a new mode of oviparous reproduction in sharks and its evolutionary implications. Scientific Reports 10: 1–12.

    Article  CAS  Google Scholar 

  • Nanninga, G. B., P. Saenz-Agudelo, A. Manica & M. L. Berumen, 2014. Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea. Molecular Ecology 23: 591–602.

    Article  PubMed  Google Scholar 

  • Nosal, A. P., D. C. Cartamil, J. W. Long, M. Lührmann, N. C. Wegner & J. B. Graham, 2013. Demography and movement patterns of leopard sharks (Triakis semifasciata) aggregating near the head of a submarine canyon along the open coast of southern California, USA. Environmental Biology of Fishes 96: 865–878.

    Article  Google Scholar 

  • Oliveira, C. D. L., C. Y. B. Oliveira, J. P. G. Camilo & V. da Silva Batista, 2021. Demographic analysis reveals a population decline of the Longnose stingray Hypanus guttatus in Northeastern Brazil. Regional Studies in Marine Science 41: 101554.

    Article  Google Scholar 

  • Petean, F. F., G. J. P. Naylor & S. M. Q. Lima, 2020. Integrative taxonomy identifies a new stingray species of the genus Hypanus Rafinesque, 1818 (Dasyatidae, Myliobatiformes) from the Tropical Southwestern Atlantic. Journal of Fish Biology 97: 1120–1142.

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro, H. T., L. A. Rocha, R. M. Macieira, A. Carvalho-Filho, A. B. Anderson, M. G. Bender, F. Di Dario, C. E. L. Ferreira, J. Figueiredo-Filho, R. Francini-Filho, J. L. Gasparini, J. C. Joyeux, O. J. Luiz, M. M. Mincarone, R. L. Moura, J. A. C. C. de Nunes, J. P. Quimbayo, R. S. Rosa, C. L. S. Sampaio, I. Sazima, T. Simon, D. A. Vila-Nova & S. R. Floeter, 2018. South-western Atlantic reef fishes: zoogeographical patterns and ecological drivers reveal a secondary biodiversity centre in the Atlantic Ocean. Diversity and Distributions 24: 951–965.

    Article  Google Scholar 

  • Pollom, R., R. Barreto, P. Charvet, V. Faria, K. Herman, F. Marcante & G. Rincon, 2020. Hypanus marianae. The IUCN Red List of Threatened Species 2020, e.T45925A104130004.

  • Portnoy, D. S., J. B. Puritz, C. M. Hollenbeck, J. Gelsleichter, D. Chapman & J. R. Gold, 2015. Selection and sex-biased dispersal in a coastal shark: the influence of philopatry on adaptive variation. Molecular Ecology 24: 5877–5885.

    Article  CAS  PubMed  Google Scholar 

  • Puckridge, M., P. R. Last, W. T. White & N. Andreakis, 2013. Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecology and Evolution 3: 217–232.

    Article  PubMed  Google Scholar 

  • Rizo-Fuentes, M. A., C. A. Correa-Cardenas, C. A. Lasso, M. A. Morales-Betancourt, D. C. Barragan-Barrera & S. Caballero, 2020. Phylogeography, genetic diversity and population structure of the freshwater stingray, Paratrygon aiereba (Müller & Henle, 1841) (Myliobatiformes: Potamotrygonidae) in the Colombian Amazon and Orinoco Basins. Mitochondrial DNA: Part A, DNA Mapping, Sequencing, and Analysis 32: 1–14.

    Google Scholar 

  • Rosa, R. S., O. B. F. Gadig & U. L. Gomes, 2000. The correct name for a recently described stingray (Chondrichthyes: Dasyatidae) from the Southwestern Atlantic. Copeia 2000: 889–890.

    Article  Google Scholar 

  • Rosa, R. S., N. A. Menezes, H. A. Britski, W. J. E. M. Costa & F. Groth, 2003. Diversidade, padrões de distribuição e conservação dos peixes da Caatinga. In Leal, I. R., M. Tabarelli & J. M. C. Silva (eds), Ecologia e conservação da Caatinga Editora Universitária, Universidade Federal de Pernambuco, Recife: 135–180.

    Google Scholar 

  • Sales, J. B. L., C. N. de Oliveira, W. C. R. dos Santos, M. M. Rotundo, Y. Ferreira, J. Ready, I. Sampaio, C. Oliveira, V. P. Cruz, R. E. Lara-Mendoza & L. F. da Silva Rodrigues-Filho, 2019. Phylogeography of eagle rays of the genus Aetobatus: Aetobatus narinari is restricted to the continental western Atlantic Ocean. Hydrobiologia 836: 169–183.

    Article  Google Scholar 

  • Sandoval-Castillo, J. & L. B. Beheregaray, 2020. Oceanographic heterogeneity influences an ecological radiation in elasmobranchs. Journal of Biogeography 47: 1599–1611.

    Article  Google Scholar 

  • Sandoval-Castillo, J. & A. Rocha-Olivares, 2011. Deep mitochondrial divergence in Baja California populations of an aquilopelagic elasmobranch: the golden cownose ray. Journal of Heredity 102: 269–274.

    Article  CAS  PubMed  Google Scholar 

  • Sandoval-Castillo, J., A. Rocha-Olivares, C. Villavicencio-Garayzar & E. Balart, 2004. Cryptic isolation of Gulf of California shovelnose guitarfish evidenced by mitochondrial DNA. Marine Biology 145: 983–988.

    Article  CAS  Google Scholar 

  • Schwanck, T. N., M. Schweinsberg, K. P. Lampert, T. L. Guttridge, R. Tollrian & O. O’Shea, 2020. Linking local movement and molecular analysis to explore philopatry and population connectivity of the southern stingray Hypanus americanus. Journal of Fish Biology 96: 1475–1488.

    Article  PubMed  Google Scholar 

  • Sequeira, A. M. M., C. Mellin, D. A. Fordham, M. G. Meekan & C. J. A. Bradshaw, 2014. Predicting current and future global distributions of whale sharks. Global Change Biology 20: 778–789.

    Article  PubMed  Google Scholar 

  • Setyawan, E., A. B. Sianipar, M. V. Erdmann, A. M. Fischer, J. A. Haddy, C. S. Beale, S. A. Lewis & R. Mambrasar, 2018. Site fidelity and movement patterns of reef manta rays (Mobula alfredi: Mobulidae) using passive acoustic telemetry in Northern Raja Ampat, Indonesia. Nature Conservation Research 3: 17–31.

    Article  Google Scholar 

  • Sevilla, R. G., A. Diez, M. Norén, O. Mouchel, M. Jérôme, V. Verrez-Bagnis, H. Van Pelt, L. A. Favre-Krey, G. Krey, T. F. Consortium & J. M. Bautista, 2007. Primers and polymerase chain reaction conditions for DNA barcoding teleost fish based on the mitochondrial cytochrome b and nuclear rhodopsin genes. Molecular Ecology Notes 7: 730–734.

    Article  CAS  Google Scholar 

  • Sexton, J. P., S. B. Hangartner & A. A. Hoffmann, 2014. Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68: 1–15.

    Article  CAS  PubMed  Google Scholar 

  • Slatkin, M., 1987. Gene flow and the geographic structure of natural populations. Science 236: 787–792.

    Article  CAS  PubMed  Google Scholar 

  • Smith, W. D., J. J. Bizzarro, V. P. Richards, J. Nielsen, F. Márquez-Farías & M. S. Shivji, 2009. Morphometric convergence and molecular divergence: the taxonomic status and evolutionary history of Gymnura crebripunctata and Gymnura marmorata in the eastern Pacific Ocean. Journal of Fish Biology 75: 761–783.

    Article  CAS  PubMed  Google Scholar 

  • Song, H., J. E. Buhay, M. F. Whiting & K. A. Crandall, 2008. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105: 13486–13491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Souza, W. F. & B. Knoppers, 2011. Fluxos de água e sedimentos à costa Leste do Brasil: relações entre a tipologia e pressões antrópicas. Geochimica Brasiliensis 17: 57–74.

    Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W (improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice). Nucleic Acids Research 22: 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tilley, A., J. López-Angarita & J. R. Turner, 2013. Diet reconstruction and resource partitioning of a Caribbean marine mesopredator using stable isotope Bayesian modelling. PLoS ONE 8: 1–10.

    Article  CAS  Google Scholar 

  • Wang, I. J., 2013. Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution 67: 3403–3411.

    Article  PubMed  Google Scholar 

  • Wang, I. J. & G. S. Bradburd, 2014. Isolation by environment. Molecular Ecology 23: 5649–5662.

    Article  PubMed  Google Scholar 

  • Xiao, Y. F., 1997. Electrophysiological properties of different cell types in the shark rectal gland. Life Sciences 60: 2231–2243.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Y., L. Duvaux, G. Ren, L. Zhang, O. Savolainen & J. Liu, 2017. Importance of incomplete lineage sorting and introgression in the origin of shared genetic variation between two closely related pines with overlapping distributions. Heredity 118: 211–220.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank everyone who contributed directly and indirectly, in the laboratories and in the field, especially the team from the Laboratório de Ictiologia Sistemática e Evolutiva (LISE/UFRN) and Laboratório do Oceano (LOC/UFRN), for so many hours of interaction and learning, as well as all the fishermen who contributed to the capture of specimens throughout the northeastern Brazil. In particular, we need to thank C.L.S. Sampaio (UFAL), R.P.T. Lessa, and M.L. Araújo for making the Laboratório de Dinâmica de Populações Marinhas (DIMAR/UFRPE) a logistic support; M.B.S. Barbosa (PARNAMAR Abrolhos) for the help in the fieldtrip; F. Buloto, for making the expedition to Abrolhos feasible, receiving the field team at his house; T.S. Leite (UFSC) e F.D. Lima for the partnership and all contributions throughout the work through the Projeto Ciências do Mar II (23038.004807/2014-01). We would also like to sincerely thank both anonymous reviewers and the editor, Cécile Fauvelot, for their time and constructive comments in improving this manuscript. This study is part of the Ph.D. Thesis of T.L.A.C. at the Graduate Program of Ecology at the Universidade Federal do Rio Grande do Norte.

Funding

T.L.A. Costa, F.F. Petean, and W.M. Berbel-Filho received financial support from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Award Number 001). S.M.Q. Lima and A.M. Solé-Cava receive CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) Research Productivity Grants (313644/2018-7 and 303300/2019-1, respectively).

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Correspondence to Flávia F. Petean.

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Costa, T.L.A., Petean, F.F., Berbel-Filho, W.M. et al. Molecular testing of the São Francisco River as an ecological filter for the Brazilian large-eyed stingray Hypanus marianae (Dasyatidae, Myliobatiformes). Hydrobiologia 849, 2435–2448 (2022). https://doi.org/10.1007/s10750-022-04828-6

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