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Diagnostic description and geographic distribution of four new cryptic species of the blue-spotted maskray species complex (Myliobatoidei: Dasyatidae; Neotrygon spp.) based on DNA sequences

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Abstract

Nine morphologically similar but genetically distinct lineages in the blue-spotted maskray species complex, previously Neotrygon kuhlii (Müller and Henle) qualify as cryptic species. Four of these lineages have been previously described as Neotrygon australiae Last, White and Séret, Neotrygon caeruleopunctata Last, White and Séret, Neotrygon orientale Last, White and Séret, and Neotrygon varidens (Garman), but the morphological characters used in the descriptions offered poor diagnoses and their geographic distributions were not delineated precisely. The objective of the present work is to complete the description of the cryptic species in the complex. Here, an additional four lineages are described as new species on the basis of their mitochondrial DNA sequences: Neotrygon bobwardi, whose distribution extends from the northern tip of Aceh to the western coast of Sumatera; Neotrygon malaccensis, sampled from the eastern part of the Andaman Sea and from the Malacca Strait; Neotrygon moluccensis, from the eastern half of the Banda Sea; and Neotrygon westpapuensis from the central portion of northern West Papua. The geographic distributions of N. australiae, N. coeruleopunctata, N. orientale, and N. varidens are updated. For each species, a diagnosis is provided in the form of a combination of private or partly-private nucleotides at 2–4 nucleotide sites along a 519-base pair fragment of the CO1 gene. We believe that the present taxonomic revision will provide information relevant to the sound management and conservation of cryptic species of the blue-spotted maskray in the Coral Triangle region.

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References

  • Arlyza I S, Shen K N, Durand J D, Borsa P. 2013a. Mitochondrial haplotypes indicate parapatric-like phylogeographic structure in blue-spotted maskray (Neotrygon kuhlii) from the Coral Triangle region. Journal of Heredity, 104 (5): 725–733.

    Article  Google Scholar 

  • Arlyza I S, Shen K N, Solihin D D, Soedharma D, Berrebi P, Borsa P. 2013b. Species boundaries in the Himantura uarnak species complex (Myliobatiformes: Dasyatidae). Molecular Phylogenetics and Evolution, 66 (1): 429–435.

    Article  Google Scholar 

  • Aschliman N C, Nishida M, Miya M, Inoue J G, Rosana K M, Naylor G J P. 2012. Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Molecular Phylogenetics and Evolution, 63 (1): 28–42.

    Article  Google Scholar 

  • Baldwin C C, Castillo C I, Weigt L A, Victor B C. 2011. Seven new species within western Atlantic Starksia atlantica, S. lepicoelia, and S. sluiteri (Teleostei, Labrisomidae), with comments on congruence of DNA barcodes and species. ZooKeys, 79 (3): 21–72.

    Google Scholar 

  • Bauchot M L. 1994. Les poissons décrits et figurés dans les manuscrits de Quoy au cours du voyage de l’ Astrobale (1826–1829). Cybium, 18 (2 Suppl.1): 3–101.

    Google Scholar 

  • Bickford D, Lohman D J, Sodhi N S, Ng P K L, Meier R, Winker K, Ingram K K, Das I. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22 (3): 148–155.

    Article  Google Scholar 

  • Borsa P, Arlyza I S, Chen W J, Durand J D, Meekan M G, Shen K N. 2013a. Resurrection of New Caledonian maskray Neotrygon trigonoides (Myliobatoidei: Dasyatidae) from synonymy with N. kuhlii, based on cytochrome-oxidase I gene sequences and spotting patterns. Comptes Rendus Biologies, 336 (4): 221–232.

    Article  Google Scholar 

  • Borsa P, Béarez P, Paijo S, Chen W J. 2013b. Gymnocranius superciliosus and Gymnocranius satoi, two new large-eye breams (Sparoidea: Lethrinidae) from the Coral Sea and adjacent regions. Comptes Rendus Biologies, 336 (4): 233–240.

    Article  Google Scholar 

  • Borsa P, Béarez P. 2016. Notes on the origin of Müller and Henle’s illustration and type material of the blue-spotted maskray Neotrygon kuhlii (Myliobatoidei: Dasyatidae). Cybium, 40: 40–255.

    Google Scholar 

  • Borsa P, Durand J D, Chen W J, Hubert N, Muths D, Mou-Tham G, Kulbicki M. 2016a. Comparative phylogeography of the western Indian Ocean reef fauna. Acta Oecologica, 72: 72–86.

    Article  Google Scholar 

  • Borsa P, Durand J D, Shen K N, Arlyza I S, Solihin D D, Berrebi P. 2013c. Himantura tutul sp. nov. (Myliobatoidei: Dasyatidae), a new ocellated whipray from the tropical Indo-West Pacific, described from its cytochrome-oxidase I gene sequence. Comptes Rendus Biologies, 336 (2): 82–92.

    Article  Google Scholar 

  • Borsa P, Fauvelot C, Tiavouane J, Grulois D, Wabnitz C, Abdon Naguit M R, Andréfouët S. 2015. Distribution of Noah’s giant clam, Tridacna noae. Marine Biodiversity, 45 (2): 339–344.

    Article  Google Scholar 

  • Borsa P, Sembiring A, Fauvelot C, Chen W J. 2014. Resurrection of Indian Ocean humbug damselfish, Dascyllus abudafur (Forsskål) from synonymy with its Pacific Ocean sibling, Dascyllus aruanus (L.). Comptes Rendus Biologies, 337 (12): 709–716.

    Article  Google Scholar 

  • Borsa P, Shen K N, Arlyza I S, Hoareau T B. 2016b. Multiple cryptic species in the blue-spotted maskray (Myliobatoidei: Dasyatidae: Neotrygon spp.): an update. Comptes Rendus Biologies, 339 (9–10): 417–426.

    Article  Google Scholar 

  • Borsa P. 2017. Comment on ‘Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity by Weigmann (2016)’. Journal of Fish Biology, 90 (4): 1 170–1 175, https://doi.org/10.1111/jfb.13235.

    Article  Google Scholar 

  • Brower A V Z. 2010. Alleviating the taxonomic impediment of DNA barcoding and setting a bad precedent: names for ten species of ‘Astraptes fulgerator’ (Lepidoptera: Hesperiidae: Eudaminae) with DNA-based diagnoses. Systematics and Biodiversity, 8 (4): 485–491.

    Article  Google Scholar 

  • Bull C M. 1991. Ecology of parapatric distributions. Annual Review of Ecology and Systematics, 22: 19–36.

    Article  Google Scholar 

  • Cerutti-Pereyra F, Meekan M G, Wei N W V, O’Shea O, Bradshaw C J A, Austin C M. 2012. Identification of rays through DNA barcoding: an application for ecologists. PLoS One, 7 (6): e36479.

    Article  Google Scholar 

  • Chen X, Xiang D, Yu J Q, Ding W Y, Zhang S L. 2014. Complete mitochondrial genome of the blue-spotted stingray Neotrygon kuhlii (Myliobatiformes: Dasyatidae). Mitochondrial DNA, 25 (6): 429–430.

    Article  Google Scholar 

  • Cook L G, Edwards R D, Crisp M D, Hardy N B. 2010. Need morphology always be required for new species descriptions? Invertebrate Systematics, 24 (3): 322–326.

    Article  Google Scholar 

  • Craig M T, Hastings P A. 2007. A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini. Ichthyological Re s earch, 54 (1): 1–17.

    Article  Google Scholar 

  • de Castelnau F. 1873. Contribution to the ichthyology of Australia. No. III. Supplement to the fishes of Victoria. Proceedings of the Zoological and Acclimatisation Society of Victoria, 2: 2–37.

    Google Scholar 

  • Dumont d’Urville J. 1833. Atlas hydrographique du voyage de découvertes exécuté sur la corvette l’Astrolabe. J Tastu, Paris, 25 p.

    Google Scholar 

  • Durand J D, Borsa P. 2015. Mitochondrial phylogeny of grey mullets (Acanthopterygii: Mugilidae) suggests high proportion of cryptic species. Comptes Rendus Biologies, 338 (4): 266–277.

    Article  Google Scholar 

  • Durand J D, Chen W J, Shen K N, Fu C, Borsa P. 2012. Genuslevel taxonomic changes implied by the mitochondrial phylogeny of grey mullets (Teleostei: Mugilidae). Comptes Rendus Biologies, 335 (10–11): 687–697.

    Article  Google Scholar 

  • Fahmi W W T, Jacobsen I P. 2015. Neotrygon kuhlii. The IUCN Red List of Threatened Species. e. T161590A68636167.

    Google Scholar 

  • Garman S. 1885. Notes and descriptions taken from selachians in the U.S. National Museum. Proceedings of the United States National Museum, 8 (482): 39–44.

    Article  Google Scholar 

  • International Commission on Zoological Nomenclature. 1999. International code of zoological nomenclature. 4 th edn. The International Trust for Zoological Nomenclature, London, 306p.

    Google Scholar 

  • International Commission on Zoological Nomenclature. 2012. Amendment of Articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Zookeys, (219): 1–10.

    Article  Google Scholar 

  • Jordan D S. 1888. A Manual of the Vertebrate Animals of the Northern United States, Including the District North and East of the Ozark Mountains, South of the Laurentian Hills, North of the Southern Boundary of Virginia, and East of the Missouri River, Inclusive of Marine Species. 5 th edn. A.C. McClurg and Company, Chicago, 375p.

    Book  Google Scholar 

  • Jörger K M, Schrödl M. 2013. How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10: 59.

    Article  Google Scholar 

  • Knowlton N. 1993. Sibling species in the sea. Annual Review of Ecology and Systematics, 24: 24–189.

    Article  Google Scholar 

  • Krishnamurthy P K, Francis R A. 2012. A critical review on the utility of DNA barcoding in biodiversity conservation. Biodiversity and Conservation, 21 (8): 1 901–1 919.

    Article  Google Scholar 

  • Last P R, White W T, Caira J N, Dharmadi Fahmi, Jensen K, Lim A P K, Manjaji-Matsumoto B M, Naylor G J P, Pogonoski J J, Stevens J D, Yearsley G K. 2010. Sharks and Rays of Borneo. CSIRO, Collingwood (Victoria), 304p.

    Google Scholar 

  • Last P R, White W T, Séret B. 2016. Taxonomic status of maskrays of the Neotrygon kuhlii species complex (Myliobatoidei: Dasyatidae) with the description of three new species from the Indo-West Pacific. Zootaxa, 4083 (4): 533–561.

    Article  Google Scholar 

  • Lim K C, Lim P E, Chong V C, Loh K H. 2015. Molecular and morphological analyses reveal phylogenetic relationships of stingrays focusing on the family Dasyatidae (Myliobatiformes). PLoS One, 10 (5): e0120518.

    Article  Google Scholar 

  • Manwell C, Baker C M A. 1963. A sibling species of sea cucumber discovered by starch gel electrophoresis. Comparative Biochemistry and Physiology, 10 (1): 39–53.

    Article  Google Scholar 

  • McDonald J H, Koehn R K. 1988. The mussels Mytilus galloprovincialis and M. trossulus on the Pacific coast of North America. Marine Biology, 99 (1): 111–118.

    Article  Google Scholar 

  • Müller J, Henle F G J. 1841. Systematische Beschreibung der Plagiostomen, Mit Sechzig Steindrucktafeln. Veit und Comp, Berlin, xxii+200p.

    Google Scholar 

  • Naylor G J P, Caira J N, Jensen K, Rosana K A M, White W T, Last P R. 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, 367: 1–262.

    Article  Google Scholar 

  • Nygren A. 2014. Cryptic polychaete diversity: a review. Zoologica Scripta, 43 (2): 172–183.

    Article  Google Scholar 

  • Pante E, Schoelinck C, Puillandre N. 2015. From integrative taxonomy to species description: one step beyond. Systematic Biology, 64 (1): 152–160.

    Article  Google Scholar 

  • Pons J, Barraclough T G, Gomez-Zurita J, Cardoso A, Duran D P, Hazell S, Kamoun S, Sumlin W D, Vogler A P. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55 (4): 595–609.

    Article  Google Scholar 

  • Puckridge M, Last P R, White W T, Andreakis N. 2013. Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecology and Evolution, 3 (2): 217–232.

    Article  Google Scholar 

  • Quoy J R C, Gaimard J P. 1835. Voyage de découvertes de l’Astrolabe exécuté par ordre du Roi, pendant les années 1826-1827-1828-1829, sor le commandement de M. J. Dumont d’Urville. Zoologie, Mollusques, Tastu, Paris, 1 344p.

    Google Scholar 

  • Randall J E, Victor B C. 2015. Descriptions of thirty-four new species of the fish genus Pempheris (Perciformes: Pempheridae), with a key to the species of the western Indian Ocean. Journal of the Ocean Science Foundation, 18: 1–77.

    Google Scholar 

  • Ratnasingham S, Hebert P D N. 2007. BOLD: the Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Resources, 7 (3): 355–364.

    Google Scholar 

  • Ratnasingham S, Hebert P D N. 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS One, 8 (7): e66213.

    Article  Google Scholar 

  • Saltford J. 2003. The United Nations and the Indonesian takeover of West Papua, 1962–1969. Routledge, London, 256p.

    Google Scholar 

  • Shen K N, Chang C W, Delrieu-Trottin E, Borsa P. 2017. Lemonpeel (Centropyge flavissima) and yellow (C. heraldi) pygmy angelfishes each consist of two geographically isolated sibling species. Marine Biodiversity, https://doi.org/10.1007/s12526-016-0509-y.

    Google Scholar 

  • Shen K N, Chang C W, Tsai S Y, Wu S C, Lin Z H, Chan Y F, Chen C H, Hsiao C D, Borsa P. 2016. Next generation sequencing yields complete mitogenomes of leopard whipray (Himantura leoparda) and blue-spotted stingray (Neotrygon kuhlii) (Chondrichthyes: Dasyatidae). Mitochondrial DNA Part A, 27 (4): 2 613–2 614.

    Article  Google Scholar 

  • Steinke D, de Waard J R, Gomon M F, Johnson J W, Larson H K, Lucanus O, Moore G I, Reader S, Ward R D. 2017. DNA barcoding the fishes of Lizard Island (Great Barrier Reef). Biodiversity Data Journal, 5: e12409.

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12): 2 725–2 729.

    Article  Google Scholar 

  • Tamura K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution, 9 (4): 678–687.

    Google Scholar 

  • Tautz D, Arctander P, Minelli A, Thomas R H, Vogler A P. 2003. A plea for DNA taxonomy. Trends in Ecology & Evolution, 18 (2): 70–74.

    Article  Google Scholar 

  • Van Campenhout J, Derycke S, Moens T, Vanreusel A. 2014. Differences in life-histories refute ecological equivalence of cryptic species and provide clues to the origin of bathyal Halomonhystera (Nematoda). PLoS One, 9 (11): e111889.

    Article  Google Scholar 

  • Vogler A P, Monaghan M T. 2006. Recent advances in DNA taxonomy: fortschritte in der DNA-taxonomie. Journal of Zoological Systematics and Evolutionary Research, 45 (1): 1–10.

    Article  Google Scholar 

  • Wang Z D, Guo Y S, Liu X M, Fan Y B, Liu C W. 2012. DNA barcoding South China Sea fishes. Mitochondrial DNA, 23 (5): 405–410.

    Article  Google Scholar 

  • Ward R D, Hanner R, Hebert P D N. 2009. The campaign to DNA barcode all fishes, FISH-BOL. Journal of Fish Biology, 74 (2): 329–356.

    Article  Google Scholar 

  • Ward R D, Holmes B H, White W T, Last P R. 2008. DNA barcoding Australasian chondrichthyans: results and potential uses in conservation. Marine and Freshwater Research, 59 (1): 57–71.

    Article  Google Scholar 

  • White W T, Last P R. 2012. A review of the taxonomy of chondrichthyan fishes: a modern perspective. Journal of Fish Biology, 80 (5): 901–917.

    Article  Google Scholar 

  • Woodland D J, Anderson R C. 2014. Description of a new species of rabbitfish (Perciformes: Siganidae) from southern India, Sri Lanka and the Maldives. Zootaxa, 3811 (1): 129–136.

    Article  Google Scholar 

  • Yagishita N, Furumitsu K, Yamaguchi A. 2009. Molecular evidence for the taxonomic status of an unde-scribed species of Dasyatis (Chondrichthyes: Dasyatidae) from Japan. Species Diversity, 14 (3): 157–164.

    Article  Google Scholar 

  • Zemlak T S, Ward R D, Connell A D, Holmes B H, Hebert P D N. 2009. DNA barcoding reveals overlooked marine fishes. Molecular Ecology Resources, 9 (S1): 237–242.

    Article  Google Scholar 

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Acknowledgements

This paper is a contribution of a collaborative project on the population genetics of stingrays in the Indonesian archipelago (PARI), run jointly by IRD UMR 250 and LIPI-P2O. We thank R. K. Hadiaty (LIPI, Cibinong) for allocating MZB collection numbers to the holotypes and paratypes of the four new species described in the present paper. We had valuable discussions with P. Béarez (MNHN, Paris), P. Berrebi (CNRS, Montpellier), W.-J. Chen (NTU, Taipei), J.-D. Durand (IRD, Montpellier), N. Hubert (IRD, Cibinong) and R. D. Ward (CSIRO, Hobart). We are also grateful to two anonymous reviewers for insightful comments. We took criticism from P. Last (CSIRO, Hobart), B. Séret (MNHN, Paris), S. Weigmann (Elasmo-Lab, Lüneburg) and W. T. White (CSIRO, Hobart) as encouragement. Our background map of the Indo-West Pacific was edited from images downloaded from Digital Vector Maps, San Diego (http://digital-vector-maps.com/). Several books including J. Dumont d’Urville’sVoyage de l’Astrolabe and J. Müller and F. G. J. Henle’s Systematische Beschreibung der Plagiostomen were consulted from the Biodiversity Heritage Library website (http://www.biodiversitylibrary.org). Designed the study: PB. Contributed materials or data or analysis tools: ISA, PB, TBH, KNS. Wrote the paper: PB. The authors declare no financial conflict of interest.

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Authors and Affiliations

  1. Institut de Recherche pour le Développement (IRD), UMR 250 “Ecologie Marine Tropicale des Océans Pacifique et Indien”, BP A5, 98848, Nouméa, New Caledonia

    Philippe Borsa

  2. Lembaga Ilmu Pengetahuan Indonesia (LIPI), Pusat Penelitian Oseanografi(P2O), Jakarta, Indonesia

    Irma S. Arlyza

  3. Molecular Ecology and Evolution Programme, Department of Genetics, University of Pretoria, Pretoria, South Africa

    Thierry B. Hoareau

  4. Aquatic Technology Laboratories, Agricultural Technology Research Institute, Taiwan, China

    Kang-Ning Shen

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  1. Philippe Borsa
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  2. Irma S. Arlyza
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  3. Thierry B. Hoareau
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  4. Kang-Ning Shen
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Correspondence to Philippe Borsa.

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Supported by the IRD, LIPI-P2O, Universiteit Pretoria, and NTOU. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Borsa, P., Arlyza, I.S., Hoareau, T.B. et al. Diagnostic description and geographic distribution of four new cryptic species of the blue-spotted maskray species complex (Myliobatoidei: Dasyatidae; Neotrygon spp.) based on DNA sequences. J. Ocean. Limnol. 36, 827–841 (2018). https://doi.org/10.1007/s00343-018-7056-2

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