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Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Cephalopod biodiversity of the Kermadec Islands: implications for conservation and some future taxonomic priorities

Heather E. Braid https://orcid.org/0000-0003-0428-5800 A B and Kathrin S. R. Bolstad A
+ Author Affiliations
- Author Affiliations

A AUT Lab for Cephalopod Ecology & Systematics, Institute for Applied Ecology New Zealand, Auckland University of Technology, Private Bag 92006, 1142 Auckland, New Zealand.

B Corresponding author. Email: heather.braid@gmail.com

Invertebrate Systematics 33(2) 402-425 https://doi.org/10.1071/IS18041
Submitted: 7 May 2018  Accepted: 9 October 2018   Published: 9 April 2019

Abstract

In order to establish the Kermadec–Rangitāhua Ocean Sanctuary, which will protect a large, unique, near-pristine section of New Zealand’s marine environment, an improved understanding of the marine biodiversity of this area is required. Over 150 cephalopod specimens were collected from the Kermadecs during a recent biodiversity survey, providing the first opportunity in over a century to directly assess locally occurring taxa. Specimens were morphologically identified and DNA barcoded. DNA sequences were analysed using the Barcode Index Number (BIN) system in the Barcode of Life Data System. This study nearly doubles the previously known cephalopod biodiversity of the Kermadecs, adding 28 species (bringing the total to 70), and reporting three cephalopod orders from this area for the first time. The BIN analysis highlighted several taxa that are badly in need of revision, including some supposedly monotypic genera that now appear to contain multiple species, and at least five species that may be new to science. The Kermadec region also hosts 34 cephalopod species not known to occur elsewhere in New Zealand waters. Most taxa reported herein are deep-sea species whose habitat is not protected by the existing marine reserve; we therefore strongly support the establishment of the proposed Sanctuary.

Additional keywords: Cephalopoda, DNA barcoding, marine sanctuary.


References

Allcock, A. L., Barratt, I., Eleaume, M., Linse, K., Norman, M. D., Smith, P. J, Steinke, D., Stevens, D. W., and Strugnell, J. M. (2011). Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Research Part II: Topical Studies in Oceanography 58, 242–249.
Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life.Crossref | GoogleScholarGoogle Scholar |

Berry, S. S. (1913). Nematolampas, a remarkable new cephalopod from the South Pacific. The Biological Bulletin 25, 208–212.
Nematolampas, a remarkable new cephalopod from the South Pacific.Crossref | GoogleScholarGoogle Scholar |

Berry, S. S. (1914). Notes on a collection of cephalopods from the Kermadec Islands. Transactions and Proceedings of the New Zealand Institute 46, 134–149.

Berry, S. S. (1916). Cephalopoda of the Kermadec Islands. Proceedings. Academy of Natural Sciences of Philadelphia 68, 45–66.

Bolstad, K. S. (2007). Systematics and distribution of the New Zealand onychoteuthid fauna (Cephalopoda: Oegopsida), including a new species, Notonykia nesisi sp. nov. Reviews in Fish Biology and Fisheries 17, 305–335.
Systematics and distribution of the New Zealand onychoteuthid fauna (Cephalopoda: Oegopsida), including a new species, Notonykia nesisi sp. nov.Crossref | GoogleScholarGoogle Scholar |

Bolstad, K. S. (2008). Two new species and a review of the squid genus Onychoteuthis Lichtenstein, 1818 (Oegopsida: Onychoteuthidae) from the Pacific Ocean. Bulletin of Marine Science 83, 481–529.

Bolstad, K. S. R. (2010). Systematics of the Onychoteuthidae Gray, 1847 (Cephalopoda: Oegopsida). Zootaxa 2696, 1–186.

Bolstad, K. S. R. (2016). Cephalopod fauna of the Kermadec Islands: much left to learn. In ‘Proceedings of Kermadec – Discoveries and Connections’. (Eds B. Golder, and A. Connell.) pp. 64–65 (The Pew Charitable Trusts Wellington, New Zealand.)

Bolstad, K. S. R., Braid, H. E., Strugnell, J. M., Lindgren, A. R., Lischka, A., Kubodera, T., Laptikhovsky, V. L., and Roura Labiaga, A. (2018). A mitochondrial phylogeny of the family Onychoteuthidae Gray, 1847 (Cephalopoda: Oegopsida). Molecular Phylogenetics and Evolution 128, 88–97.

Braid, H. E. (2017). Resolving the taxonomic status of Asperoteuthis lui Salcedo-Vargas, 1999 (Cephalopoda, Chiroteuthidae) using integrative taxonomy. Marine Biodiversity 47, 621–635.
Resolving the taxonomic status of Asperoteuthis lui Salcedo-Vargas, 1999 (Cephalopoda, Chiroteuthidae) using integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |

Braid, H. E., and Bolstad, K. S. R. (2015). Systematics of the family Mastigoteuthidae (Cephalopoda: Oegopsida) in New Zealand waters. New Zealand Journal of Zoology 42, 187–256.
Systematics of the family Mastigoteuthidae (Cephalopoda: Oegopsida) in New Zealand waters.Crossref | GoogleScholarGoogle Scholar |

Braid, H. E., McBride, P. D., and Bolstad, K. S. R. (2014). Molecular phylogenetic analysis of the squid family Mastigoteuthidae (Mollusca, Cephalopoda) based on three mitochondrial genes. Hydrobiologia 725, 145–164.
Molecular phylogenetic analysis of the squid family Mastigoteuthidae (Mollusca, Cephalopoda) based on three mitochondrial genes.Crossref | GoogleScholarGoogle Scholar |

Braid, H. E., Kubodera, T., and Bolstad, K. S. R. (2017). One step closer to understanding the chiroteuthid families in the Pacific Ocean. Marine Biodiversity 47, 659–683.
One step closer to understanding the chiroteuthid families in the Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Carlini, D. B., and Graves, J. E. (1999). Phylogenetic analysis of cytochrome c oxidase I sequences to determine higher-level relationships within the coleoid cephalopods. Bulletin of Marine Science 64, 57–76.

Clark, M. R., Trnski, T., Constantine, R., Aguirre, J. D., Barker, J., Betty, E., Bowden, D. A., Connell, A., Duffy, C., George, S., Hannam, S., Liggins, L., Middleton, C., Mills, S., Pallentin, A., Riekkola, L., Sampey, A., Sewell, M., Spong, K., Stewart, A., Stewart, R., Struthers, C., and van Oosterom, L. (2017). Biodiversity of the Kermadec Islands and offshore waters of the Kermadec Ridge: report of a coastal, marine mammal and deep-sea survey (TAN1612). Ministry for Primary Industries, Wellington, New Zealand.

Collins, M. A., and Villanueva, R. (2006). Taxonomy, ecology and behaviour of the cirrate octopods. Oceanography and Marine Biology – an Annual Review 44, 277–322.
Taxonomy, ecology and behaviour of the cirrate octopods.Crossref | GoogleScholarGoogle Scholar |

Dell, R. K. (1952). The recent Cephalopoda of New Zealand. Dominion Museum Bulletin 16, 1–157.

Duffy, C. A. J., and Ahyong, S. T. (2015). Annotated checklist of the marine flora and fauna of the Kermadec Islands Marine Reserve and northern Kermadec Ridge, New Zealand. Bulletin of the Auckland Museum 20, 19–124.

Evans, A. B. (2018). A systematic review of the squid family Cranchiidae (Cephalopoda: Oegopsida) in the Pacific Ocean. PhD Thesis. (Auckland University of Technology, Auckland, New Zealand.)

Fernández-Álvarez, F. A. (2008). An onto-phylogenetic journey through the life history of flying squids (Cephalopoda: Ommastrephidae). PhD Thesis. (Universidad Politécnica de Cataluña, Barcelona, Spain.)

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Freeman, D., Schnabel, K., Marshall, B., Gordon, G., Wing, S., Tracey, D., and Hitchmough, R. (2014). Conservation Status of New Zealand Marine Invertebrates, 2013. New Zealand Threat Classification Series 9, Department of Conservation, Wellington.

Gleadall, I. G. (2016). Octopus sinensis d’Orbigny, 1841 (Cephalopoda: Octopodidae): valid species name for the commercially valuable east Asian common octopus. Species Diversity 21, 31–42.
Octopus sinensis d’Orbigny, 1841 (Cephalopoda: Octopodidae): valid species name for the commercially valuable east Asian common octopus.Crossref | GoogleScholarGoogle Scholar |

Golder, B. (2016). Discoveries and connections. In ‘Proceedings of Kermadec – Discoveries and Connections’. (Eds B. Golder, and A. Connell.) (The Pew Charitable Trusts: Wellington, New Zealand.)

Horstkotte, J. (2008). The systematics and ecological role of Histioteuthis (Cephalopoda: Histioteuthidae) in New Zealand waters. M.Sc. Thesis. (Leibniz-Institut für Meereswissenschaften an der Universität Kiel, Kiel, Germany.)

House, M. R. (2010). Geographic distribution of Nautilus shells. In ‘Nautilus’. (Eds W. B. Saunders, N. H. Landman.) pp. 53–64. (Springer: Netherlands.)

Hoving, H. J. T., Perez, J. A. A., Bolstad, K. S. R., Braid, H. E., Evans, A. B., Fuchs, D., Judkins, H., Kelly, J. T., Marian, J. E., Nakajima, R., Piatkowski, U., Reid, A., Vecchione, M., and Xavier, J. C (2014). The study of deep-sea cephalopods. Advances in Marine Biology 67, 235–359.
The study of deep-sea cephalopods.Crossref | GoogleScholarGoogle Scholar |

Imber, M. J. (1978). The squid families Cranchiidae and Gonatidae (Cephalopoda: Teuthoidea) in the New Zealand region. New Zealand Journal of Zoology 5, 445–484.
The squid families Cranchiidae and Gonatidae (Cephalopoda: Teuthoidea) in the New Zealand region.Crossref | GoogleScholarGoogle Scholar |

Jereb P., and Roper, C. F. E. (2010). ‘Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 2. Myopsid and oegopsid squids.’ FAO Species Catalogue for Fishery Purposes, 4(2). (FAO: Rome, Italy.)

Jereb, P., Roper, C. F. E., Norman, M. D., and Finn, J. K. (Eds) (2014). ‘Cephalopods of the world. An annotated and illustrated catalogue of cephalopod species known to date. Volume 3. Octopods and Vampire Squids.’ FAO Species Catalogue for Fishery Purposes, 4(3). (FAO: Rome, Italy.)

Kubodera, T., and Okutani, T. (2011). New additions of luminous bobtail squids to the Japanese cephalopod fauna (Sepiolida: Sepiolidae: Heteroteuthinae). Venus (Tokyo) 69, 145–161.

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |

Lindgren, A. R. (2010). Molecular inference of phylogenetic relationships among Decapodiformes (Mollusca: Cephalopoda) with special focus on the squid Order Oegopsida. Molecular Phylogenetics and Evolution 56, 77–90.
Molecular inference of phylogenetic relationships among Decapodiformes (Mollusca: Cephalopoda) with special focus on the squid Order Oegopsida.Crossref | GoogleScholarGoogle Scholar | 20348002PubMed |

Mangold, K. M., Vecchione, M., and Young, R. E. (2016). Tremoctopodidae Tryon, 1879. Tremoctopus Chiaie 1830. Blanket octopus. Available at: http://tolweb.org/Tremoctopus [Verified 7 July 2017]

May, R. (1990). Taxonomy as destiny. Nature 347, 129–130.
Taxonomy as destiny.Crossref | GoogleScholarGoogle Scholar |

MFTE (2016). About the proposed Kermadec Ocean Sanctuary. Ministry for the Environment. Available at: http://www.mfe.govt.nz/marine/kermadec-ocean-sanctuary/about-sanctuary [Verified 3 March 2018]

Ministry for Primary Industries (2017). Arrow squid (SQU). Available at: http://fs.fish.govt.nz/Doc/24290/04_SQU_2017.pdf.ashx [Verified 11 September 2017]

Murray, J. (1895). A summary of the scientific results obtained at the sounding, dredging, and trawling stations of H.M.S. Challenger. Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873–76, VI.

Nesis, K. N. (1977). Mastigoteuthis psychophila sp. n. (Cephalopoda, Mastigoteuthidae) from the Southern Ocean. Zoologicheskij Zhurnal 56, 835–842.

Nesis, K. N. (1987). ‘Cephalopods of the World; Squids, Cuttlefishes, Octopuses, and Allies.’ (TFH Publications: Neptune City, NJ.)

Norman, M. D., and Hochberg, F. G. (2005). The current state of octopus taxonomy. Research Bulletin – Phuket Marine Biological Center 66, 127–154.

O’Shea, S. (1999). ‘The marine fauna of New Zealand: Octopoda (Mollusca: Cephalopoda).’ National Institute of Water and Atmosphere, Wellington. Biodiversity Memoir 112, 1–280.

Powell, A. W. B. (1979). ‘New Zealand Mollusca: Marine, Land, and Freshwater Shells.’ (Collins: Auckland.)

Quetglas, A., de Mesa, A., Ordines, F., and Grau, A. (2010). Life history of the deep-sea cephalopod family Histioteuthidae in the western Mediterranean. Deep-sea Research. Part I, Oceanographic Research Papers 57, 999–1008.
Life history of the deep-sea cephalopod family Histioteuthidae in the western Mediterranean.Crossref | GoogleScholarGoogle Scholar |

Ratnasingham, S., and Hebert, P. D. (2007). BOLD: The Barcode of Life Data System (http://www. barcodinglife. org). Molecular Ecology Notes 7, 355–364.
BOLD: The Barcode of Life Data System (http://www. barcodinglife. org).Crossref | GoogleScholarGoogle Scholar | 18784790PubMed |

Ratnasingham, S., and Hebert, P. D. N. (2013). A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS One 8, e66213.
A DNA-based registry for all animal species: the barcode index number (BIN) system.Crossref | GoogleScholarGoogle Scholar | 24358363PubMed |

Reid, A. (2016). Post-mortem drift in Australian cuttlefish sepions: its effect on the interpretation of species ranges. Molluscan Research 36, 9–21.
Post-mortem drift in Australian cuttlefish sepions: its effect on the interpretation of species ranges.Crossref | GoogleScholarGoogle Scholar |

Reid, A. L., and Wilson, N. G. (2015). Octopuses of the Kermadec Islands: discovery and description of a new member of the Octopusvulgaris’ complex (O. jollyorum, sp. nov.) and the first description of a male Callistoctopus kermadecensis (Berry, 1914). Bulletin of the Auckland Museum 20, 349–368.

Riddell, D. J. (1985). The Enoploteuthidae (Cephalopoda: Oegopsida) of the New Zealand region. Fisheries Research Bulletin 27, 1–52.

Spencer, H. G., Willan, R. C., Marshall, B. A., and Murray, T. J. (2017). Checklist of the living Mollusca recorded from the New Zealand Exclusive Economic Zone. Available at: http://www.molluscs.otago.ac.nz/ [Verified 10 August 2017]

Sweeney, M. J., and Roper, C. F. E. (1998). Classification, type localities and type repositories of recent Cephalopoda. Smithsonian Contributions to Zoology 586, 561–595.

Sweeney, M. J., and Young, R. E. (1998). Taxa associated with the Family Vampyroteuthidae. Available at: http://tolweb.org/accessory/Vampyroteuthidae_Taxa?acc_id=2420 [Verified 7 September 2017]

Sweeney, M. J., and Young, R. E. (2003a). Taxa associated with the Family Bathyteuthidae Pfeffer, 1900. Available at: http://tolweb.org/accessory/Bathyteuthidae_Taxa?acc_id=1799 [Verified 7 September 2017]

Sweeney, M. J., and Young, R. E. (2003b). Taxa associated with the Family Spirulidae Owen, 1836. Available at: http://tolweb.org/accessory/Spriulidae_Taxa?acc_id=2337 [Verified 30 September 2018]

Sweeney, M. J., and Young, R. E. (2009). Taxa associated with the Family Chtenopterygidae Grimpe, 1922. Available at: http://tolweb.org/notes/?note_id=5305 [Verified 30 September 2018]

Tsuchiya, K. (2014). Enoploteuthis semilineata Alexeyev 1994. Available at: http://tolweb.org/Enoploteuthis_semilineata/19714 [Verified 6 September 2017]

Tsuchiya, K., and Young, R. E. (2012). Enoploteuthis reticulata Rancurel 1970. Available at: http://tolweb.org/Enoploteuthis_reticulata/19713 [Verified 6 September 2017]

Vecchione, M., Young, R. E., and Roper, C. F. E. (2013). Heteroteuthis dagamensis Robson 1924. Available at: http://www.tolweb.org/Heteroteuthis_dagamensis/20053 [Verified 8 September 2017]

Voss, G. L. (1976). Two new species of octopods of the genus Graneledone (Mollusca: Cephalopoda) from the southern Ocean. Proceedings of the Biological Society of Washington 88, 447–458.

Voss, N. A. (1980). A generic revision of the Cranchiidae (Cephalopoda; Oegopsida). Bulletin of Marine Science 30, 365–412.

Voss, N. A., Stephen, S. J., and Dong, Zh. (1992). Family Cranchiidae, Prosch, 1849. In ‘Larval and Juvenile Cephalopods: a Manual for their Identification’. (Eds M. J. Sweeney, C. F. E. Roper, K. M. Mangold, M. R. Clarke, and S. von Boletzky.) Smithsonian Contributions to Zoology 513. pp. 187–210. (Smithsonian Institution Press: Washington D. C., USA.)

Voss, N. A., Nesis, K. N., and Rodhouse, P. G. (1998). The cephalopod family Histioteuthidae (Oegopsida): systematics, biology, and biogeography. Smithsonian Contributions to Zoology 586, 293–372.

Young, R. E. (1972). The systematic and areal distribution of pelagic cephalopods from the seas off southern California. Smithsonian Contributions to Zoology 97, 1–159.
The systematic and areal distribution of pelagic cephalopods from the seas off southern California.Crossref | GoogleScholarGoogle Scholar |

Young, R. E. (1991). Chiroteuthid and related paralarvae from Hawaiian waters. Bulletin of Marine Science 49, 162–185.

Young, R. E., and Mangold, K. M. (2011a). Galiteuthis Joubin, 1898. Available at: http://tolweb.org/Galiteuthis/19557 [Verified 12 August 2017]

Young, R. E., and Mangold, K. M. (2011b). Taonius Steenstrup, 1861. Available at: http://tolweb.org/Taonius/19558 [Verified 1 September 2017]

Young, R. E., and Vecchione, M. (2010). Chtenopterygidae Grimpe 1922. Chtenopteryx Appellof 1890. Combfin squid. Available at: http://tolweb.org/Chtenopterygidae/19430 [Verified 17 July 2017]

Young, R. E., and Vecchione, M. (2000). Histioteuthis corona (Voss and Voss 1962). Available at: http://tolweb.org/Histioteuthis_corona/19804 [Verified 19 October 2017]

Young, R. E., and Vecchione, M. (2015). Enoploteuthid families. Available at: http://tolweb.org/Enoploteuthid_families/19413 [Verified 17 July 2017]

Young, R. E., and Vecchione, M. (2016). Bathyteuthoidea Vecchione, Young and Sweeney, 2004. Available at: http://tolweb.org/Bathyteuthoidea/19421 [Verified 12 September 2017]

Young, R. E., Lindgren, A., and Vecchione, M. (2008). Mastigoteuthis microlucens, a new species of the squid family Mastigoteuthidae (Mollusca: Cephalopoda). Proceedings of the Biological Society of Washington 121, 276–282.
Mastigoteuthis microlucens, a new species of the squid family Mastigoteuthidae (Mollusca: Cephalopoda).Crossref | GoogleScholarGoogle Scholar |

Zachos, F. E. (2013). Species splitting puts conservation at risk. Nature 494, 35.
Species splitting puts conservation at risk.Crossref | GoogleScholarGoogle Scholar | 23389532PubMed |