Resurrection of the sixgill shark Hexanchus vitulus Springer & Waller, 1969 (Hexanchiformes, Hexanchidae), with comments on its distribution in the northwest Atlantic Ocean
- 731 Downloads
The sixgill sharks of the genus Hexanchus (Hexanchiformes, Hexanchidae) are large, rarely encountered deep-sea sharks, thought to comprise just two species: the bluntnose sixgill Hexanchus griseus (Bonaterre, 1788) and the bigeye sixgill Hexanchus nakamurai (Teng, 1962). Their distribution is putatively worldwide in tropical and temperate waters, but many verified records for these species are lacking, and misidentification is common. Taxonomic uncertainty has long surrounded H. nakamurai in particular, with debate as to whether individuals from the Atlantic constitute a separate species. Using 1,310 base pairs of two mitochondrial genes, COI and ND2, we confirm that bigeye sixgill sharks from the Atlantic Ocean (Belize, Gulf of Mexico, and Bahamas) diverge from those in the Pacific and Indian Oceans (Japan, La Reunion, and Madagascar) with 7.037% sequence divergence. This difference is similar to the genetic distance between both Atlantic and Indo-Pacific bigeye sixgill sharks and the bluntnose sixgill shark (7.965% and 8.200%, respectively), and between the entire genus Hexanchus and its sister genus Heptranchias (8.308%). Such variation far exceeds previous measures of species-level genetic divergence in elasmobranchs, even among slowly-evolving deep-water taxa. Given the high degree of morphological similarity within Hexanchus, and the fact that cryptic diversity is common even among frequently observed shark species, we conclude that these results support the resurrection of the name Hexanchus vitulus Springer and Waller, 1969 for bigeye sixgill sharks in the northwest Atlantic Ocean. We propose the common name “Atlantic sixgill shark” for H. vitulus, and provide new locality records from Belize, as well as comments on its overall distribution.
KeywordsSystematics Mitochondrial DNA Phylogenetics Speciation Elasmobranchs
The authors thank the Save Our Seas Foundation, the Summit Foundation, the International Union for Conservation of Nature, the Rufford Foundation, the University of West Florida, Florida Institute of Technology, and the Deep-C Consortium through the Gulf of Mexico Research Initiative who provided financial support for this project. I.E.B. and R.T.G. thank the Belize Fisheries Department and the fishers and captains in Belize, especially D. Castellanos, R. Lima, E. Muschamp, M. Alamina, E. Cuevas, and D. Garbutt. R.D.G. thanks E. and A Brooks, S. Williams, D, Chapman, L, Howey-Jordan, D, Abercrombie and L. Jordan for assistance in collecting samples in the Bahamas, and J. Imhoff and C. Peterson for assistance in collecting samples from the Gulf of Mexico. T.D.E. thanks J. Eble, M. Pfleger, C. Hitchcock, and A. Koch for help with genetic analyses, M. Boudreau and C. Meyer for logistical support, and J. Kiszka for H. nakamurai tissue from La Reunion. Thanks also to J. Carlson, who oversaw the bottom longline observer program and implemented program-wide biological sampling. S.J.B.G. and M.P.E. thank the observers, C. Aguero, P. Bear, J. Combs, M. Lee and J. Patterson, and port sampler D. Fable for collecting the samples. Sixgill sharks were captured in Belize under Fisheries Permit 9-16 and in the USA under NOAA Fisheries Highly Migratory Species Division Exempted Fishing Permits and the US Federal Register (HMS-EFP-07-01, HMS-EFP-08-01, HMS-EFP-09-01, FR Doc. E9-20489).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
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 acknowledgements, if applicable.
- Castro JI (2010) The sharks of North America. Oxford University Press, OxfordGoogle Scholar
- Clark E, Kristof E (1990) Deep-sea elasmobranchs observed from submersibles off Bermuda, Grand Cayman, and Freeport, Bahamas. In: Pratt Jr HL, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in biology, ecology, systematics and the status of the fisheries. NOAA Technical Report 90. NOAA Fisheries,Silver Spring, pp 269–284Google Scholar
- Compagno LJV (1984) Sharks of the world: an annotated and illustrated catalogue of shark species known to date. Part 1: Hexanchiformes to Lamniformes vol 4. FAO species catalogue. FAO Fisheries Synopsis (125) vol 4. FAO, RomeGoogle Scholar
- Ebert DA (1990) The taxonomy, biogeography and biology of cow and frilled sharks (Chondrichthyes: Hexanchiformes). Dissertation. Rhodes University, GrahamstownGoogle Scholar
- Ebert DA, Fowler SL, Compagno LJV (2016) Sharks of the world: a fully illustrated guide. Wild Nature Press, PlymouthGoogle Scholar
- Enzenauer MP, Deacy BM, Carlson JK (2015) Characterization of the shark bottom longline fishery, 2014. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory, Panama CityGoogle Scholar
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
- Gulak SJB, Enzenauer MP, Carlson JK (2013) Characterization of the shark and reef fish bottom longline fisheries: 2012. NOAA Tech Memo NMFS-SEFSC 652:42Google Scholar
- Hale LF, Hollensead LD, Carlson JK (2007) Characterization of the shark bottom longline fishery, 2007. NOAA Technical Memorandum NMFS-SEFSC-564. US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory, Panama CityGoogle Scholar
- McLaughlin DM, Morrissey JF (2004) New records of elasmobranchs from the Cayman trench, Jamaica. Bull Mar Sci 75:481–485Google Scholar
- Morgan A, Cooper PW, Curtis T, Burgess GH (2009) Overview of the US east coast bottom longline shark fishery, 1994–2003. Mar Fish Rev 71:23–38Google Scholar
- 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 1–262. doi: https://doi.org/10.1206/754.1
- Pfleger MO, Grubbs RD, Daly-Engel TS (in press, 2018) Squalus clarkae sp. nov., a new dogfish shark from the Northwest Atlantic and Gulf of Mexico, with comments on the Squalus mitsukurii species complex. ZootaxaGoogle Scholar
- Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://www2.stat.duke.edu/~scs/Projects/Trees/Phylogenetic/MrBayes_manual.pdf
- Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes 3.1 manual, pp 1–69Google Scholar
- Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90Google Scholar
- Scott-Denton E et al (2011) Descriptions of the US Gulf of Mexico reef fish bottom longline and vertical line fisheries based on observer data. Mar Fish Rev 73:1–26Google Scholar
- Springer S, Waller RA (1969) Hexanchus vitulus, a new sixgill shark from the Bahamas. Bull Mar Sci 19:159–174Google Scholar
- Taniuchi T, Tachikawa H (1991) Hexanchus nakamurai, a senior synonym of H. vitulus (Elasmobranchii), with notes on its occurrence in Japan. Jap J Ichthyol 38:57–60Google Scholar
- Teng HT (1962) Studies on classification and distribution of chondrichthyan fishes of Taiwan. Photo dissertation, Kyoto University, KyotoGoogle Scholar
- Ward RD, Holmes BH, Zemlak TS, Smith PJ (2007) Part 12—DNA barcoding discriminates spurdogs of the genus Squalus. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new dogfishes of the genus Squalus (Squaloidea: Squalidae). CSIRO Marine and Atmospheric Research, Hobart, pp 117–130Google Scholar
- White WT, Corrigan S, Yang L, Henderson AC, Bazinet AL, Swofford DL, Naylor GJP (2017) Phylogeny of the manta and devilrays (Chondrichthyes: Mobulidae), with an updated taxonomic arrangement for the family. Zool J Linnean Soc 82:65–73Google Scholar