Skip to main content

Advertisement

Log in

Redescription of the Critically Endangered tentacled butterfly ray, Gymnura tentaculata (Valenciennes in Müller & Henle, 1841) (Myliobatiformes: Gymnuridae) from Iranian waters

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Until recently, the tentacled butterfly ray, Gymnura tentaculata (Valenciennes in Müller & Henle, 1841), had not been seen for over three decades and had been assessed as Critically Endangered–Possibly Extinct on the IUCN Red List of Threatened Species. An elasmobranch-specific monitoring program undertaken between October 2019 and July 2020 allowed the discovery of a population of the species along southern Iranian waters. This allowed for a detailed redescription of the morphology as well as generating molecular data for G. tentaculata based on material retrieved during surveys. Gymnura tentaculata is a small (to 85-cm disc width) gymnurid endemic to the northwestern Indian Ocean that can be distinguished from other Gymnura Kuhl in van Hasselt, 1823, by a combination of characteristics, including a small tentacle present on the posterior end of each spiracle, a short tail without bands, and a small dorsal fin always present at its base. Historically, the confirmed range of the species comprised coastal waters of Iran, Pakistan, and India, but it now appears limited to Iranian waters of the eastern Persian Gulf and the Gulf of Oman. Threats to this gymnurid across its current geographical range are also discussed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Bloch ME, Schneider JG (1801) M.E. Blochii, Systema Ichthyologiae iconibus cx illustratum. Post obitum auctoris opus inchoatum absolvit, correxit, interpolavit Jo. Gottlob Schneider, Saxo. Berolini. Sumtibus Austoris Impressum et Bibliopolio Sanderiano Commissum. 584 pp

  • Daliri M, Kamrani E, Paighambari SY (2015) Illegal shrimp fishing in Hormozgan inshore waters of the Persian Gulf. Egypt J Aquat Res 41(4):345–352. https://doi.org/10.1016/j.ejar.2015.11.007

    Article  Google Scholar 

  • Dor M (1984) CLOFRES: Checklist of the fishes of the Red Sea. The Israel Academy of Sciences and Humanities, Jerusalem 437 pp

  • Fowler HW (1934) Descriptions of new fishes obtained from 1907 to 1910, chiefly in the Philippine Islands and adjacent seas. Proc Acad Nat Sci Phila 85: 233–367

  • Gilchrist JDF, Thompson WW (1911) Descriptions of fishes from the coast of Natal (3). Ann S Afr Mus 11(2):29–58

  • Golani D, Bogorodsky SV (2010) The fishes of the Red Sea–reappraisal and updated checklist. Zootaxa 2463(1):1–135. https://doi.org/10.11646/zootaxa.2463.1.1

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series: 41: 95–98

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755. https://doi.org/10.1093/BIOINFORMATICS/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2021) International Union for the Conservation of Nature (IUCN) Red List of threatened species, version 2021-3. https://www.iucnredlist.org (downloaded at 1/18/2022)

  • Jabado RW, Spaet JLY (2017) Elasmobranch fisheries in the Arabian Seas Region: characteristics, trade and management. Fish Fish 18:1096–1118. https://doi.org/10.1111/faf.12227

    Article  Google Scholar 

  • Jabado RW, Kyne PM, Pollom RA, Ebert DA, Simpfendorfer CA, Ralph GM, Dulvy NK (2017) The conservation status of sharks, rays, and chimaeras in the Arabian Sea and adjacent waters. Environment Agency – Abu Dhabi, UAE and IUCN Species Survival Commission Shark Specialist Group, Vancouver, Canada 236 pp

  • Jabado RW, Kyne PM, Pollom RA, Ebert DA, Simpfendorfer CA, Ralph GM, Al Dhaheri SS, Akhilesh KV, Ali K, Ali MH, Al Mamari TMS, Bineesh KK, El Hassan IS, Fernando D, Grandcourt EM, Khan MM, Moore ABM, Owfi F, Robinson DP et al (2018) Troubled waters: threats and extinction risk of the sharks, rays and chimaeras of the Arabian Sea and adjacent waters. Fish Fish 19:1043–1062. https://doi.org/10.1111/faf.12311

    Article  Google Scholar 

  • Jabado RW, Rezaie-Atagholipour M, Kyne PM (2021) Gymnura tentaculata. The IUCN red list of threatened species 2021: e.T161516A124498408. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T161516A124498408.en

  • Jacobsen I, Bennett M (2009) A taxonomic review of the Australian butterfly ray Gymnura australis (Ramsay & Ogilby, 1886) and other members of the family Gymnuridae (order Rajiformes) from the Indo-West Pacific. Zootaxa 2228(1): 1–28. https://doi.org/10.11646/zootaxa.2228.1.1

  • Kabir S, Shahriar M, Kabir ANMH, Uddin MG (2006) High salt SDS-based method for the direct extraction of genomic DNA from three different gram-negative organisms. CDR J 1(2):57–64

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120. https://doi.org/10.1007/BF01731581

    Article  CAS  PubMed  Google Scholar 

  • Linnaeus C (1758) Systema Naturae per regna tria naturae, regnum animale, secundum classes, ordines, genera, species, cum characteribus differentiis synonymis, locis. Ed X, 1: 824 p. Stockholm (L. SALVIUS)

  • Manjaji BM (2004) Taxonomy and phylogenetic systematics of the indo-pacific whip-tailed stingray genus Himantura Müller & Henle 1837 [Chondrichthyes: Myliobatiformes: Dasyatidae]. PhD Thesis, University of Tasmania, Hobart 640 pp

  • Moore ABM, McCarthy ID, de Carvalho GR, Peirce R (2012) Species, sex, size and male maturity composition of previously unreported elasmobranch landings in Kuwait, Qatar and Abu Dhabi Emirate. J Fish Biol 80:1619–1642. https://doi.org/10.1111/j.1095-8649.2011.03210.x

    Article  CAS  PubMed  Google Scholar 

  • Müller J, Henle J (1841) Systematische Beschreibung der Plagiostomen. Verlag Von Veit Und Comp, Berlin, 200pp

    Book  Google Scholar 

  • Owfi F (2020) Biological hazards and threats to coastal-marine ecosystems in Iranian seas from fisheries-environmental perspective, Analytical report. Iranian Fisheries Science Research Institute, Tehran 48 pp (in Persian)

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256. https://doi.org/10.1093/MOLBEV/MSN083

    Article  CAS  PubMed  Google Scholar 

  • Ramsay EP, Ogilby JD (1886) Descriptions of new or rare Australian fishes. Proceedings of the Linnean Society of New South Wales, ser. 1,10: 575–579

  • Shaw G (1804) General zoology or systematic natural history (volume 5, part 2). G. Kearsley, London

  • Rezaie-Atagholipour M, Jabado RW, Owfi F, Askari Hesni M, Ebert DA (2021) Lost and found: rediscovery of the extinct tentacled butterfly ray Gymnura tentaculata in Iranian waters. Oryx 55(4):489–490. https://doi.org/10.1017/S0030605321000521

    Article  Google Scholar 

  • Sherman CS, Akhilesh KV, Bin Ali A, Bineesh KK, Derrick D, Dharmadi, Ebert DA, Fahmi, Fernando D, Haque AB, Maung A, Seyha L, Tanay D, Tesfamichael D, Utzurrum JAT, Valinassab T, Vo VQ, Yuneni RR (2021) Gymnura poecilura. The IUCN Red List of Threatened Species 2021: e.T60117A124440205. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T60117A124440205.en

  • Smith WD, Bizzarro JJ, Richards VP, Nielsen J, Márquez- Flarías F, Shivji MS (2009) Morphometric convergence and molecular divergence: the taxonomic status and evolutionary history of Gymnura crebripunctata and Gymnura marmorata in the eastern Pacific Ocean. J Fish Biol 75(4):761–783. https://doi.org/10.1111/j.1095-8649.2009.02300.x

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/MOLBEV/MST197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/NAR/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Hasselt JC (1823) Uittreksel uit een’ brief van Dr. J. C. van Hasselt, aan den Heer C. J. Teminich. Algem. Konst Letter-bode I Deel (no. 20), 315–317

  • Vossoughi GH, Vosoughi A (1999) Study of batoid fishes in northern part of Hormoz Strait, with emphasis on some species new to the Persian Gulf and Sea of Oman. Indian J Fish 46(3):301–306

    Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360(1462):1847–1857. https://doi.org/10.1098/RSTB.2005.1716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokota L, de Carvalho MR (2017) Taxonomic and morphological revision of butterfly rays of the Gymnura micrura (Bloch & Schneider 1801) species complex, with the description of two new species (Myliobatiformes: Gymnuridae). Zootaxa 4332(1): 1–74. https://doi.org/10.11646/zootaxa.4332.1.1

  • Yokota L, White WT, de Carvalho MR (2016) Butterfly rays, Family Gymnuridae. In: Last PR, White WT, de Carvalho MR, Séret B, Stehmann MFW, Naylor GJP (eds) Rays of the world. CSIRO Publishing, Melbourne, pp 511–521

    Google Scholar 

Download references

Acknowledgements

We are very grateful to the Iranian Fisheries Science Research Institute (IFSRI) and its research centers in the southern coastal provinces for facilitating sample collection from traditional local shrimp trawlers and also the Ferdows-1 research trawling vessel. We warmly thank the Future For Nature Foundation, Prince Bernhard Nature Fund, and Anderson Cabot Center for Ocean Life in New England Aquarium, who supported the shark and ray conservation project that led us to rediscover tentacled butterfly rays in Iranian waters. We warmly thank Linnean Society of London and Systematics Association for supporting our taxonomic investigations. The first author kindly thanks Idea Wild for providing a laptop that facilitated writing this manuscript. This study could not have been completed without the helpful and timely assistance of many good friends; far too many to list individually. Nonetheless, we especially appreciate support from Mohammadamin Samiei, Najmeh Sabbah, Mohammad Rajabi, Roohollah Sharifizadeh, and Poorya Mohammadzadeh from Shahid Bahonar University of Kerman. We warmly thank Dr. Mehdi (Khosrow) Rajabizadeh who kindly examined the syntype specimens from MNHN. We kindly appreciate the handling editor, Dr. Peter Kyne, and two anonymous reviewers for their constructive comments on the manuscript. We are very grateful to Ms. Zouhaira Gabsi and Mr. Philippe Keith from MNHN Ichthyology Collection for granting access to the syntype specimens.

Funding

The taxonomic study was supported by a Systematics Research Fund grant (Linnean Society of London and Systematics Association). Field surveys to collect specimens were funded by the Prince Bernhard Nature Fund and Marine Conservation Action Fund (Anderson Cabot Center for Ocean Life in New England Aquarium). Idea Wild also supported the project by providing field equipment. The first author M. R-A received a Future For Nature Award 2021 for this conservation project. None of the supporters had any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohsen Rezaie-Atagholipour.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgments, if applicable. This study is compliant with CBD and Nagoya protocols.

Data availability

All data generated or analyzed during this study are included in this published article. All sequence data generated for the species are available in GenBank with accession numbers ON849063 to ON849068.

Author contribution

MRA and RWJ conceived the study. MRA led and participated in all the field and laboratory work. FO participated in the fieldwork. MAH participated in the laboratory work. ERP conducted molecular analyses and contributed parts of the manuscript. MRA and DAE analyzed morphological data. MRA wrote the initial version of the manuscript. All authors revised and approved the final manuscript.

Additional information

Communicated by P. M. Kyne

Publisher’s note

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

This article is a contribution to Topical Collection Systematics and Biodiversity of Indian Ocean Sharks, Rays, and Chimaeras (Chondrichthyes)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rezaie-Atagholipour, M., Jabado, R.W., Askari Hesni, M. et al. Redescription of the Critically Endangered tentacled butterfly ray, Gymnura tentaculata (Valenciennes in Müller & Henle, 1841) (Myliobatiformes: Gymnuridae) from Iranian waters. Mar. Biodivers. 53, 6 (2023). https://doi.org/10.1007/s12526-022-01303-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12526-022-01303-2

Keywords

Navigation