Combined COI barcode-based methods to avoid mislabelling of threatened species of deep-sea skates L. Carugati, R. Melis, A. Cariani, A. Cau, V. Crobe, A. Ferrari, M. Follesa, M. Geraci, S. Iglésias, P. Pesci, et al. To cite this version: L. Carugati, R. Melis, A. Cariani, A. Cau, V. Crobe, et al.. Combined COI barcode-based methods to avoid mislabelling of threatened species of deep-sea skates. Animal Conservation, Wiley, 2021, 10.1111/acv.12716. hal-03278950 HAL Id: hal-03278950 https://hal.sorbonne-universite.fr/hal-03278950 Submitted on 6 Jul 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Animal Conservation. Print ISSN 1367-9430 Combined COI barcode-based methods to avoid mislabelling of threatened species of deep-sea skates L. Carugati1 , R. Melis1 , A. Cariani2 , A. Cau1 , V. Crobe2 , A. Ferrari2 , M. C. Follesa1 , M. L. Geraci3,4 , S. P. Iglesias 5 , P. Pesci1 , F. Tinti2 & R. Cannas1 1 Department of Life and Environmental Sciences, University of Cagliari, Cagliari, Italy 2 Department of Biological, Geological and Environmental Sciences (BiGeA), University of Bologna, Bologna, Italy 3 Department of Biological, Geological and Environmental Sciences (BiGeA) – Marine biology and fisheries laboratory, University of Bologna, Fano (PU), Italy 4 Institute for Biological Resources and Marine Biotechnologies (IRBIM), National Research Council (CNR), Mazara del Vallo (TP), Italy 5 Institut de Systematique, Evolution, Biodiversite (ISYEB), Museum national d’Histoire naturelle, CNRS, Sorbonne Universite, EPHE, Universite des Antilles, Station Marine de Concarneau, Concarneau, France Keywords Abstract conservation; deep sea; Dipturus; DNA barcoding; species delimitation; specimen Skates are characterised by conservative body morphology which hampers identifi- assignment; species identification; skates. cation and leads to frequent taxonomic confusion and market mislabelling. Accu- rate specimen classification is crucial for reliable stock assessments and effective Correspondence conservation plans, otherwise the risk of extinction could be unnoticed. The mis- Rita Cannas, Department of Life and classification issue is evident for the genus Dipturus, distributed worldwide, from Environmental Sciences, University of the continental shelf and slope to the deep sea. In this study, barcode cytochrome Cagliari, Via T. Fiorelli 1, 09126 Cagliari, Italy. oxidase I gene (COI) sequences were used along with species delimitation and Tel. +390706758004 specimen assignment methods to improve taxonomy and zoogeography of species Email: [email protected] of conservation interest inhabiting the Atlantic Ocean and Mediterranean Sea. In this study, we provided new evidence of the occurence of D. nidarosiensis in the Editor: Jeff Johnson Central-Western Mediterranean Sea and the lack of Atlantic-Mediterranean genetic Associate Editor: Matt Fujita divergence. The Atlantic endangered species D. laevis and D. batis clustered L. Carugati and R. Melis are equally together under the same molecular operational taxonomic unit (MOTU) with any contributed. delimitation methods used, while the assignment approach correctly discriminated specimens into the two species. These results provided evidence that the presence Received 07 December 2020; accepted 20 of the barcode gap is not an essential predictor of identification success, but the May 2021 use of different approaches is crucially needed for specimen classification, espe- cially when threshold- or tree-based methods result less powerful. The analyses doi:10.1111/acv.12716 also showed how different putative, vulnerable, species dwelling across South- Western Atlantic and South-Eastern Pacific are frequently misidentified in public sequence repositories. Our study emphasised the limits associated to public data- bases, highlighting the urgency to verify and implement the information deposited therein in order to guarantee accurate species identification and thus effective con- servation measures for deep-sea skates. fl Introduction However, due to their conserved dorsoventrally attened body morphology, the identification of skates based solely Skates are cartilaginous fish of the family Rajidae (order on morphological characters can be problematic (Geraci Rajiformes) which includes more than 150 described species, et al., 2017). belonging to 17 genera (Last et al., 2016a). Most of them The identification of species boundaries is fundamental for are benthic organisms with restricted geographical distribu- undertaking effective conservation and management mea- tions, living between the shoreline and >4000 m depth sures. The difficulties encountered among this family have (Orlov, Cotton and Byrkjedal, 2006; Ebert and Compagno, led to a high degree of mislabelling in scientific trawl sur- 2007). Despite their apparent restrictive habitat preferences veys (Cariani et al., 2017) and commercial landings (Iglesias (e.g., soft bottom substrates), skates exhibit a high degree of et al., 2010; Griffiths et al., 2013). Skates are rarely specifi- biodiversity and endemism (Ebert and Compagno, 2007). cally targeted by fisheries, but their high susceptibility to by- Animal Conservation (2021) – ª 2021 The Authors. Animal Conservation published by John Wiley & Sons Ltd on behalf of Zoological Society of London 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Avoid mislabelling of threatened deep-sea skates CARUGATI et al. catch make them some of the most vulnerable marine fishes intermedius mainly appears along the Western and Northern (Stevens et al., 2000; Dulvy et al., 2016). Accurate species coasts of Scotland (Neat et al., 2015), while D. batis dwells identification of individuals is thus needed and is critical for mostly in the Celtic Sea (Lynghammar et al., 2014). Both reliable conservation plans and stock assessments, otherwise species are still very occasionally found in other parts of the declines, especially of threatened taxa, could be unnoticed. North Atlantic Ocean. The misclassification problem is particularly evident in the Previous studies (Compagno and Ebert, 2007) reported genus Dipturus (Griffiths et al., 2010; Iglesias et al., 2010) that D. batis was often confused with the barndoor skate, D. which includes more than 40 species (Last et al., 2016a), laevis (Mitchill, 1818), which is distributed in the North- which are widely distributed from temperate to tropical Western Atlantic (Leavitt et al., 2018), usually caught as regions, from continental shelves and slopes to the deep sea bycatch and classified as ‘Endangered’ (EN), and with the (Ebert and Compagno, 2007; Follesa et al., 2019). According slime skate, D. pullopunctatus (Smith, 1964), which is a to the current state of knowledge (Last et al., 2016a), in the common endemic Southern African skate, classified at ‘Least European waters (considering Mediterranean and Black Sea, Concern’ (LC) in the International Union for Conservation North-Eastern Atlantic Ocean), Dipturus currently encom- of Nature (IUCN) Red List (Pollom et al., 2020). In addi- passes three species of conservation concern: the longnosed tion, the slime skate presents an overlap in the geographical skate, Dipturus oxyrinchus (Linnaeus, 1758), the Norwegian distribution with D. nidarosiensis, which has been found also skate, Dipturus nidarosiensis (Storm, 1881), and the common off South-Eastern Africa and frequently confused with other skate, Dipturus batis (Linnaeus, 1758). skates (Last et al., 2016a; Geraci et al., 2019). The longnosed skate is distributed in both the Mediter- Reporting species-specific landings became European law ranean and North-Eastern Atlantic, to depths of 900 m (Ser- in 2009 (EC No 43/2009); however, such legislation requires ena, 2005; Ebert and Stehmann, 2013; Ellis et al., 2015; an unambiguous classification of the individuals. DNA bar- Mulas et al., 2015). The Norwegian skate was thought to coding has been proven a smart and integrative taxonomic inhabit only the North-Eastern Atlantic and Bay of Biscay toolbox that can effectively contribute to species identifica- (Priede et al., 2010; Rodrıguez-Cabello, Perez and Sanchez, tion among closely related skates (Serra-Pereira et al., 2011; 2013), but its occurrence has been recently reported in differ- Lynghammar et al., 2014; Frodella et al., 2016; Cariani ent areas of the Western Mediterranean (Cannas et al., 2010; et al., 2017). This approach relies on the concept that the Cariani et al., 2017; Ramirez-Amaro et al., 2017; Carbonara genetic variation, that is the ‘barcode gap’, between species et al., 2019). Their presence in the Mediterranean Sea has is larger than that within species (although this term should been further confirmed by the recent finding of paintings in be treated with caution, see e.g., Moritz and Cicero 2004; manuscripts by Cuvier and Valenciennes (Ms-535), unpub- Meyer and Paulay, 2005). Previous studies demonstrated the lished in their Histoire naturelle des