Skip to main content
SpringerLink
Log in

Neotype designation and re-description of Forsskål’s reticulate whipray Himantura uarnak

  • Short Communication
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

A Publisher Correction to this article was published on 05 May 2021

This article has been updated

Abstract

A continuing impediment to the taxonomy of the reticulate whipray Himantura spp. species complex is the absence of a type specimen for H. uarnak (Gmelin [ex Forsskål], 1789). Here, reticulate whipray specimens were sampled from the Jeddah region in the Red Sea, the assumed type locality of H. uarnak, and characterized genetically at the cytochrome-oxidase subunit 1 (CO1) locus. One of these specimens now in the fish collection of the California Academy of Sciences was designated as neotype. The maximum-likelihood phylogeny of all available CO1 gene sequences from the genus Himantura had the following topology: ((H. leoparda, H. uarnak), (H. undulata, (Himantura sp. 2, (H. australis + Himantura sp. 1))), H. tutul), where H. uarnak haplotypes formed a distinct lineage sister to H. leoparda. Based on these CO1 gene sequences, the geographic distribution of H. uarnak includes the eastern Mediterranean, the Red Sea, the East African coast, and the Arabian Sea. At least one lineage in the reticulate whipray species complex remains to be named.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Change history

References

  • Ahmed MS, Zhilik AA, Chowdhury NZ, Ahmed S (2019) DNA barcoding of marine fishes of Bangladesh. https://www.ncbi.nlm.nih.gov/nuccore/MN013427. Accessed 20 Oct 2020

  • Appleyard SA (2017) http://www.boldsystems.org/index.php/Public_RecordView?processid=FOAO1113-18, FOAO1135-18, FOAO1142-18. Accessed 20 Oct 2020

  • Appleyard SA (2020) http://www.boldsystems.org/index.php/Public_RecordView?processid=FOAG126-07, FOAJ878-09, FOAO1107-18. Accessed 20 Oct 2020

  • Arlyza IS, Shen K-N, Solihin DD, Soedharma D, Berrebi P, Borsa P (2013) Species boundaries in the Himantura uarnak species complex (Myliobatiformes: Dasyatidae). Mol Phylogenet Evol 66:429–435

    Article  CAS  PubMed  Google Scholar 

  • Bineesh KK, Gopalakrishnan A, Akhilesh KV, Sajeela KA, Abdussamad EM, Pillai NGK, Basheer VS, Jena JK, Ward RD (2017) DNA barcoding reveals species composition of sharks and rays in the Indian commercial fishery. Mitoch DNA Pt A 28:458–472

    Article  CAS  Google Scholar 

  • Bleeker P (1852) Bijdrage tot de kennis der Plagiostomen van den Indischen archipel. Verhandel Batav Genoot Kunst Wetensch 24:1-92, pls 1-4

  • Borsa P (2017) Comments on ‘Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity’ (Weigmann, 2016). J Fish Biol 90:1170–1175

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Borsa P, Arlyza IS, Hoareau TB, Shen K-N (2018) 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 Oceanol Limnol 36:827–841

    Article  Google Scholar 

  • Bouckaert R, Vaughan TG, Barido-Sottani J, Duchene S, Fourment M, Gavryushkina A, Heled J, Jones G, Kuhnert D, De Maio N, Matschiner M, Mendes FK, Muller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu CH, Xie D, Zhang C, Stadler T, Drummond AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15:28

    Article  Google Scholar 

  • Cerutti-Pereyra F, Meekan MG, Wei N-WV, O’Shea O, Bradshaw CJA, Austin CM (2012) Identification of rays through DNA barcoding: an application for ecologists. PLoS One 7:e36479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2016) GenBank. Nucleic Acids Res 44:D67–D72

    Article  CAS  PubMed  Google Scholar 

  • Cook LG, Edwards RD, Crisp M, Hardy NB (2010) Need morphology always be required for new species descriptions? Invert Systematics 24:322–326

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Duméril A (1865) Histoire naturelle des poissons ou ichthyologie générale. Tome premier Elasmobranches. Librairie encyclopédique du Roret, Paris, p 720

    Book  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Fernando D, Brown RMK, Tanna A, Gobiraj R, Ralicki H, Jockusch EL, Ebert DA, Jensen K, Caira JN (2019) New insights into the identities of the elasmobranch fauna of Sri Lanka. Zootaxa 4585:201–238

    Article  Google Scholar 

  • Forsskål P (1775) Descriptiones animalium, avium, amphibiorum, piscium, insectorum, vermium; quae in itinere orientali observavit Petrus Forskål (post mortem auctoris edidit Carsten Niebuhr). Adjuncta est materia medica kahirina atque tabula maris Rubri geographica. Mölleri, Hauniae, xxxiv+164 p

  • Fricke R (2008) Authorship, availability and validity of fish names described by Peter (Pehr) Simon Forsskål and Johann Christian Fabricius in the ‘Descriptiones animalium’ by Carsten Niebuhr in 1775 (Pisces). Stuttg Beitr Naturk A Neue Ser 1:1–76

    Google Scholar 

  • Fricke R, Eschmeyer WN, van der Laan R (eds) (2021) Eschmeyer’s catalog of fishes: genera, species, references (http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 22 Feb 2021

  • Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62:707–724

    Article  PubMed  PubMed Central  Google Scholar 

  • Gmelin JF (1789) Caroli a Linné […] Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species; cum characteribus, differentiis, synonymis, locis. Editio decimo tertia, aucta, reformata, vol 1, pars III. GE Beer, Lipsiae:1033–1516

  • Gouws G (2020) http://www.boldsystems.org/index.php/Public_RecordView?processid=SAIAB712-08, SAIAB713-08, SAIAB714-08, SAIAB715-08. Accessed 20 Oct 2020

  • Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hanner R (2020) http://www.boldsystems.org/index.php/Public_RecordView?processid=IRREK171-08, IRREK193-08, IRREK662-08, IRREK678-08, IRREK679-08, IRREK687-08, IRREK741-08, IRREK752-08, IRREK829-08. Accessed 20 Oct 2020

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • ICZN (1999) International code of zoological nomenclature, 4th edn. International Trust for Zoological Nomenclature, London, p 306

  • Klausewitz W (1960) Die Typen und Typoide des Naturmuseums Senckenberg, 23: Pisces, Chondrichthyes, Elasmobranchii. Senckenberg Biol 41:289–296

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Adhavan D, Vinuganesh A, Prakash S (2020) DNA barcoding revealed first record of the ‘fine spotted whipray’ Himantura tutul (Myliobatoidei: Dasyatidae) in the Indian coastal waters. J Appl Ichthyol 36:515–518

    Article  CAS  Google Scholar 

  • Last PR, Compagno LJV (1999) Dasyatidae - Stingrays. In: Carpenter KE, Niem VH (eds) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 3. Batoid fishes, chimaeras and bony fishes part 1 (Elopidae to Linophrynidae). FAO, Rome, pp 1479–1505

    Google Scholar 

  • Last PR, Naylor GJP, Manjaji-Matsumoto BM (2016a) A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa 4139:345–368

    Article  PubMed  Google Scholar 

  • Last PR, White WT, Naylor G (2016b) Three new stingrays (Myliobatiformes: Dasyatidae) from the Indo-West Pacific. Zootaxa 4147:377–402

    Article  PubMed  Google Scholar 

  • Last PR, White WT, de Carvalho MR, Séret B, Stehmann MFW, Naylor GJP (eds) (2016c) Rays of the World. CSIRO Publishing, Melbourne, p 790

    Google Scholar 

  • Lim KC, Lim PE, Chong VC, Loh KH (2015) Molecular and morphological analyses reveal phylogenetic relationships of stingrays focusing on the family Dasyatidae (Myliobatiformes). PLoS One 10:e0120518

    Article  PubMed  PubMed Central  Google Scholar 

  • Manjaji BM (2004) Taxonomy and phylogenetic systematics of the Indo-Pacific whip-tailed stingray genus Himantura Müller and Henle 1837 (Chondrichthyes: Myliobatiformes: Dasyatidae). PhD Thesis, University of Tasmania, xxii+607 p

  • Manjaji-Matsumoto BM, Last PR (2008) Himantura leoparda sp. nov., a new whipray (Myliobatoidei: Dasyatidae) from the Indo-Pacific. CSIRO Mar Atmosph Res Pap 22:292–301

    Google Scholar 

  • McGrouther MA (2020) http://www.boldsystems.org/index.php/Public_RecordView?processid=AMS045-06. Accessed 20 Oct 2020

  • Miesen FW, Droppelmann F, Hüllen S, Hadiaty RK, Herder F (2016) An annotated checklist of the inland fishes of Sulawesi. Bonn Zool Bull 64:77–106

    Google Scholar 

  • Mohd Arshaad W (2020) http://www.boldsystems.org/index.php/Public_RecordView?processid=JTFR099-17, JTFR112-17. Accessed 20 Oct 2020

  • Mohd Arshaad W, Jamaludin N-A (2018) DNA barcoding of rays in Malaysia. https://www.ncbi.nlm.nih.gov/nuccore/MG774902, MG774903, MG774913, MG774915, MG774922, MG792078, MG792101, MG792110, MG792112, MG792113, MG792123, MG792124, MG792125. Accessed 20 Oct 2020

  • Muktha M, Akhilesh KV, Sandhya S, Jasmin F, Jishnudev MA, Kizhakudan SJ (2018) Re-description of the longtail butterfly ray, Gymnura poecilura (Shaw, 1804) (Gymnuridae: Myliobatiformes) from Bay of Bengal with a neotype designation. Mar Biodivers 48:1085–1096

    Article  Google Scholar 

  • Müller J, Henle FGJ (1837) Ueber die Gattungen der Plagiostomen. Arch Naturg 3:394–401

  • Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR (2012) A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull Am Mus Nat Hist 367:1–262

    Article  Google Scholar 

  • Pavan-Kumar A, Kumar R, Pitale P, Shen K-N, Borsa P (2018) Neotrygon indica sp. nov., the Indian-Ocean blue spotted maskray (Myliobatoidei, Dasyatidae). C R Biol 341:120–130

    Article  PubMed  Google Scholar 

  • Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609

    Article  PubMed  Google Scholar 

  • Priyanga K, Thangaraj M, Singh R (2013) Molecular identification of Urogymnus asperrimus (family: Dasyatidae) using cytochrome oxidase I (COI) as a molecular marker. https://www.ncbi.nlm.nih.gov/nuccore/KC508509. Accessed 20 Oct 2020

  • Puckridge M, Last PR, White WT, Andreakis N (2013) Phylogeography of the Indo-West PAcific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecol Evol 3:217–232

    Article  PubMed  Google Scholar 

  • Puillandre N, Brouillet S, Achaz G (2021) ASAP: assemble species by automatic partitioning. Mol Ecol Resour 21:609–620

    Article  PubMed  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 20 Oct 2020

  • Ratnasingham S, Hebert PD (2007) BOLD: the barcode of life data system (http://www.barcodinglife.org). Mol Ecol Notes 7:55–364

  • Ravi RK, Venu S, Bineesh KK, Akhilesh KV, Sajeela KA, Basheer VS, Gopalakrishnan A (2019) https://www.ncbi.nlm.nih.gov/nuccore/MK422130. Accessed 20 Oct 2020

  • Rüppell E (1837) Neue Wirbelthiere zu der Fauna von Abyssinien gehörig. Fische des rothen Meeres. Siegmund Schmerber, Frankfurt am Mein, ii+148 p, 33 pl

  • Santos MD, Asis AMM, Lacsamana JKM (2014) Illegal trade of regulated and protected aquatic species in the Philippines detected by DNA barcoding. https://www.ncbi.nlm.nih.gov/nuccore/KC970332. Accessed 20 Oct 2020

  • Segura-Garcia I, Yain Tun T (2018) Unscrambling Myanmar marine fishery biodiversity using DNA barcoding. https://www.ncbi.nlm.nih.gov/nuccore/MH235646, MH235647. Accessed 20 Oct 2020

  • 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 the complete mitogenomes of leopard whipray (Himantura leoparda) and blue-spotted maskray (Neotrygon kuhlii) (Chondrichthyes: Dasyatidae). Mitoch DNA Pt A 27:2613–2614

    Article  CAS  Google Scholar 

  • Steinke D, Zemlak TS, Connell AD, Heemstra PC, Hebert PDN (2011) https://www.ncbi.nlm.nih.gov/nuccore/JF493651, JF493652. Accessed 20 Oct 2020

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Phil Trans Roy Soc Lond B 360:1847–1857

    Article  CAS  Google Scholar 

  • Ward RD, Holmes BH, White WT, Last PR (2008) DNA barcoding Australasian chondrichthyans: results and potential uses in conservation. Mar Freshw Res 59:57–71

    Article  CAS  Google Scholar 

  • Weigmann S (2016) Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. J Fish Biol 88:837–1037

    Article  CAS  PubMed  Google Scholar 

  • Yucel N, Sakalli A, Karahan A (2017) First record of the honeycomb stingray Himantura leoparda (Manjaji-Matsumoto & Last, 2008) (Myliobatoidei: Dasyatidae) in the Mediterranean Sea, confirmed by DNA barcoding. J Appl Ichthyol 33:530–532

    Article  Google Scholar 

Download references

Acknowledgements

Foremost, thanks are due to M. Tietbohl for donating tissue samples, assisting in field collections, and providing laboratory assistance. Additionally, we are grateful to J. Spaet and members of KAUST’s Reef Ecology Lab for their support at various stages of this project; to D. Catania and L.A. Rocha for allocating a CAS collection number to the neotype of H. uarnak; to X. Chen for sharing reticulate whipray sequences; to M. Bennett-Smith for sharing excellent photographs; to S. Bogorodsky, H. Debelius, and R. Fricke for insightful discussions about the taxonomy and nomenclature of reticulate whiprays; to G. Lim (ICZN) for confirming the validity of the present neotype designation. Useful taxonomic literature was communicated to us by C.-W. Chang, K.-N. Shen, and an anonymous reviewer. Several books including P. Forsskål’s Descriptiones animalium, J.F. Gmelin’s Systema naturae, and Rüppell’s Fische des rothen Meeres were accessed from the Biodiversity Heritage Library website (http://www.biodiversitylibrary.org/).

Funding

Support to this study was provided by the King Abdullah University of Science and Technology (KAUST) through baseline funding to MLB and Institut de recherche pour le développement, Marseille to PB.

Author information

Authors and Affiliations

  1. Institut de recherche pour le développement, IRD-UMR 250 ‘Écologie marine tropicale des océans Pacifique et Indien’, 34394, Montpellier, France

    Philippe Borsa

  2. Division of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900, Saudi Arabia

    Collin T. Williams, Ashlie J. McIvor & Michael L. Berumen

  3. MARE - Marine and Environmental Sciences Centre, Agência Regional para o Desenvolvimento da Investigação Tecnologia e Inovação (ARDITI), Edifício Madeira Tecnopolo, Caminho da Penteada, 9020-105, Funchal, Madeira, Portugal

    Ashlie J. McIvor

  4. Department of Biochemistry, Genetics and Microbiology, University of Pretoria, X20, Hatfield, 0028, Pretoria, South Africa

    Thierry B. Hoareau

Authors
  1. Philippe Borsa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Collin T. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ashlie J. McIvor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thierry B. Hoareau
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael L. Berumen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philippe Borsa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Reticulate whipray specimens were captured in accordance with KAUST’s institutional animal care and use committee (IACUC) under animal study proposal # 18IACUC14.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities through KAUST. The study is compliant with CBD and Nagoya protocols.

Data availability

All data generated during this study are included in this published article or in the appended Supplementary Tables. Sequences produced through the present study have been deposited in GenBank (https://www.ncbi.nlm.nih.gov/nucleotide/) under accession nos. MW178184-MW178196. Photographs of all specimens are available from the authors upon request.

Author contribution

AJM and CTW participated in the design of the study, collected and measured specimens, did the molecular analyses, and participated in the writing. MLB contributed funding and laboratory facilities and supervised the study. PB designed the study, provided directions, compiled and analyzed the data, and led the writing. TBH ran additional data analyses. All authors read, edited, and approved the final version of the manuscript.

Additional information

Communicated by P. Martínez Arbizu

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The online version of this article contained a number of typesetting errors which the editor wished to rectify, but it was inadvertently sent for publication before the required corrections were implemented.

This article is registered in ZooBank under http://zoobank.org/B2113697-5EBF-4364-B50C-63019A1A076A

Supplementary Information

Table S1

(PDF 243 kb)

Table S2

(PDF 281 kb)

Table S3

(PDF 136 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Borsa, P., Williams, C.T., McIvor, A.J. et al. Neotype designation and re-description of Forsskål’s reticulate whipray Himantura uarnak. Mar. Biodivers. 51, 28 (2021). https://doi.org/10.1007/s12526-021-01180-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12526-021-01180-1

Keywords

Search

Navigation