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Taxonomy Is Destiny: Resolving the Systematics of Unstable Squid Families Using Integrative Taxonomy to Aid Cephalopod Conservation

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Whole thesis(4.7 MB)

Date

2018

Authors

Supervisor

Bolstad, Kat S. R.
Towns, Dave

Item type

Thesis

Degree name

Doctor of Philosophy

Journal Title

Journal ISSN

Volume Title

Publisher

Auckland University of Technology

Abstract

The waters around New Zealand host one of the highest biodiversities of squid and octopus species in the world, yet until the late 1990s, little taxonomic work was published on this unique assemblage. While some groups have recently been (or are in the process of being) resolved, others remain poorly understood, and certain regions also remain insufficiently studied. Accurate portraits of these regions’ teuthofauna have historically been precluded both by limited sample availability, and by lack of taxonomic clarity in the locally occurring groups. The infrequent capture and fragmentary nature of deep-sea squid specimens have also contributed to systematic confusion, but the field of integrative taxonomy (using molecular data in combination with traditional morphological characters) shows great promise as a tool for resolving cephalopod taxonomy at both the species and higher levels. This thesis uses integrative taxonomy to remedy some of the greatest knowledge gaps in our understanding of the New Zealand (and wider Pacific) teuthofauna, by assessing the cephalopod diversity of the Kermadec Islands region, following much-needed studies on the ecologically important (but taxonomically problematic) deep-sea squid clades Histioteuthidae and the chiroteuthid families. The Kermadec Islands in northern New Zealand waters are in a near-pristine environment that has barely begun to be explored. In order to protect the biodiversity of this area, the Kermadec–Rangitāhua Ocean Sanctuary has been proposed, to extend the area of protection offered by the existing Kermadec Marine Reserve. However, the cephalopod biodiversity of this area—especially the deep-sea taxa—remains poorly known, and a better understanding is required for the establishment of the Sanctuary. Specimens collected on the recent expedition titled ‘Biodiversity of the Kermadec Islands and offshore waters of the Kermadec Ridge—a coastal, marine mammal and deep-sea survey (TAN1612)’ enabled an integrative taxonomic approach to critically appraise the region’s cephalopod fauna. However, several groups considered likely to occur in the region were known to require taxonomic attention; thus, studies were first undertaken to improve the systematic resolution in the taxonomically unstable ‘chiroteuthid families’ and the histioteuthids, in order to increase the accuracy of this appraisal. The deep-sea chiroteuthid families represent a clade of taxonomically problematic squids, united by their tentacle-club morphology, and include the Chiroteuthidae, Mastigoteuthidae, Joubiniteuthidae, Promachoteuthidae, Batoteuthidae, and Magnapinnidae. These families are all poorly known, but following a recent review of the Mastigoteuthidae, the Chiroteuthidae is the most speciose family and the one most in need of taxonomic attention. In order to test whether oegopsid species-level systematic resolution could be improved using a combination of three mitochondrial genes (cytochrome c oxidase subunit I [COI], 16S rRNA, and 12S rRNA) and morphological characters, Asperoteuthis lui was used as a case study. This large, enigmatic chiroteuthid was previously only known from its holotype (a partial specimen taken from a fish stomach). This species now appears to have a circumglobal austral distribution rather than being a New Zealand endemic, as was previously reported, and is the most commonly consumed asperoteuthid in the diets of several apex predators. Results from a wider study of the chiroteuthids in the Pacific Ocean, using morphology in combination with the same three mitochondrial genes, reveal that two genera in the Chiroteuthidae, Chiroteuthis and Asperoteuthis, appear polyphyletic and are in need of further systematic attention. A potentially endemic Chiroteuthis species that appears new to science (C. aff. veranyi) is now known from New Zealand waters. This study also nearly doubles the number of publicly available sequences for this clade. Out of the three mitochondrial genes, 12S rRNA showed the least interspecific variation; in combination with morphology, COI and 16S rRNA are therefore likely to suffice for both systematic and ecological applications. Squids in the family Histioteuthidae represent a substantial biomass in the deep sea, and play an important role in marine food webs as prey for apex predators. This family was last reviewed nearly 20 years ago, based solely on morphology, and unnamed species are known to exist; within the New Zealand region, these animals are the primary prey of sperm whales, and have high importance for a variety of other vertebrate predators. Herein, a global integrative taxonomic analysis of the Histioteuthidae was undertaken, using 16S rRNA and the COI to test the hypothesis of morphological species groups as genera. This analysis recognises Calliteuthis, Stigmatoteuthis, Histioteuthis, Histiothauma, Fragariateuthis gen. nov., and Navia gen. nov. The number of species in this family has increased from 19 to 25–29, with at least nine now known to occur in the New Zealand region. Both 16S rRNA and COI are useful for ecological studies and taxonomy (especially since many gut content analyses of squid predators use 16S rRNA), but given the high congruence observed between Barcode Index Numbers (BINs) and morphological species distinctions, basic species identification can be likely also be achieved using just COI and morphology. Following these focused taxonomic studies, the cephalopod biodiversity of the Kermadec Islands region was catalogued using morphology and COI, and critically compared with the few existing earlier reports. Results indicate that the cephalopod diversity in the region is nearly double what was previously believed, raising the known total from 42 to at least 70 species. In addition, 28 species are reported for the first time from the Kermadec region, 13 of which represent new records for the entire New Zealand EEZ, and five of which are potentially new to science. Thirty-four species found in the Kermadecs have not been reported anywhere else in New Zealand’s EEZ; thus, the proposed Kermadec–Rangitāhua Ocean Sanctuary would protect habitat utilised by over 50% of New Zealand’s known cephalopod diversity, including 17 possibly endemic species. This thesis has provided new insight into two of the most abundant and ecologically important squid clades (both in New Zealand and in the wider Pacific), and also the most accurate review of the cephalopod diversity in the Kermadec Islands region, supporting the establishment of the Kermadec–Rangitāhua Ocean Sanctuary. DNA barcode reference libraries have been established for the Histioteuthidae and the chiroteuthid families. The histioteuthid species complexes and the Chiroteuthidae are still in need of full revision. For this to be possible, continued collections for new specimens will be required to enable further integrative taxonomic analyses. Future studies should investigate the dietary habits of these clades to fully understand their role in the ecosystem.

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Keywords

Cephalopoda, Integrative taxonomy, DNA barcoding, Oegopsida

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Permanent link

https://hdl.handle.net/10292/11903

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Doctoral Theses