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Are the Madeira Skate (Raja Maderensis) and the Thornback Ray (Raja Clavata) Distinct Species?

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Are the Madeira Skate (Raja Maderensis) and the Thornback Ray (Raja Clavata) Distinct Species? Conserv Genet (2016) 17:565–576 DOI 10.1007/s10592-015-0806-1 RESEARCH ARTICLE Resolving taxonomic uncertainty in vulnerable elasmobranchs: are the Madeira skate (Raja maderensis) and the thornback ray (Raja clavata) distinct species? 1 2 3 4 Rachel E. Ball • Barbara Serra-Pereira • Jim Ellis • Martin J. Genner • 5 6 1 7,8 Samuel Igle´sias • Andrew F. Johnson • Catherine S. Jones • Rob Leslie • 9 10 11 12 Jennifer Lewis • Stefano Mariani • Gui Menezes • Francis Neat • 1 9 13 Leslie R. Noble • David W. Sims • Andrew M. Griffiths Received: 1 July 2015 / Accepted: 25 December 2015 / Published online: 11 February 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Skates and rays constitute the most speciose clavata collected across much of their geographic ranges. group of chondrichthyan fishes, yet are characterised by Genetic evidence was insufficient to support the different remarkable levels of morphological and ecological con- species designations. However regardless of putative spe- servatism. They can be challenging to identify, which cies identification, individuals occupying waters around the makes monitoring species compositions for fisheries man- Azores and North African Seamounts represent an evolu- agement purposes problematic. Owing to their slow growth tionarily significant unit worthy of special consideration for and low fecundity, skates are vulnerable to exploitation and conservation management. species exhibiting endemism or limited ranges are con- sidered to be the most at risk. The Madeira skate Raja Keywords Phylogeography Á Population genetics Á maderensis is endemic and classified as ‘Data Deficient’ by Phylogentics Á D-Loop Á Fisheries management Á Marine the IUCN, yet its taxonomic distinctiveness from the conservation morphologically similar and more wide-ranging thornback ray Raja clavata is unresolved. This study evaluated the sequence divergence of both the variable control region Introduction and cytochrome oxidase I ‘DNA barcode’ gene of the mitochondrial genome to elucidate the genetic differenti- Speciation, or the origin of species, was famously referred ation of specimens identified as R. maderensis and R. to as that ‘‘mystery of mysteries’’ (Darwin 1859; Cannon 1961) and understanding its process remains one of the greatest challenges in evolutionary biology. The biological Electronic supplementary material The online version of this article (doi:10.1007/s10592-015-0806-1) contains supplementary species concept (BSC) regards species as ‘‘groups of material, which is available to authorized users. & Rachel E. Ball 5 Muse´um national d’Histoire naturelle, De´partement Milieux [email protected] et Peuplements Aquatiques, USM 0405, Station de Biologie Marine de Concarneau and UMR 7208 CNRS/MNHN/IRD/ 1 College of Life Sciences & Medicine, School of Biological UPMC, Biologie des Organismes et Ecosystemes Aquatiques, Sciences, University of Aberdeen, Zoology Building, Concarneau, France Tillydrone Avenue, Aberdeen AB24 2TZ, UK 6 Center for Marine Biodiversity and Conservation, Scripps 2 Departamentodo Mare Recursos Marinhos, IPMA, Instituto Institution of Oceanography 0202, University of California, Portugueˆsdo Mareda Atmosfera, Av. Brasilia, San Diego, 9500 Gilman Drive, San Diego, CA 92083-0202, 1449-006 Lisboa, Portugal USA 3 Centre for Environment, Fisheries and Aquaculture Science 7 Fisheries Branch, Department of Agriculture, Forestry and (CEFAS), Pakefield Road, Lowestoft, Suffolk NR33 0HT, Fisheries, Private Bay X2, Roggebaai 8012, South Africa UK 8 Marine Research Institute, University of Cape Town, Private 4 School of Biological Sciences, University of Bristol, Bristol Bag X3, Rondebosch 7701, South Africa Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK 123 566 Conserv Genet (2016) 17:565–576 interbreeding natural populations which are reproductively skate species amounting to 16,600 tonnes (FAO 2009). isolated from other such groups’’ (Mayr 1963, 1995). Reporting species-specific landings became European law Geographic isolation is considered to play a significant role in 2009 (EC No 43/2009) however, such protective legis- in the process of speciation, which in this case can be lation requires an unambiguous definition of a species, considered a dynamic continuum throughout which a which formally encompasses all natural variation. number of stages of divergence may be observed (Mayr Raja maderensis (Lowe, 1838) is a poorly known endemic 1954). Where populations are only recently diverged they species, reportedly restricted to waters close to the island of can appear morphologically indistinguishable. This is more Madeira, however a similar form has also been recorded likely to occur in taxa that demonstrate a high degree of from the Azores (Stehmann 2009). It is classified as ‘Data morphological conservatism and do not rely on visual cues Deficient’ by the IUCN red list of threatened species (Steh- for reproductive interactions (Bickford et al. 2007). mann 2009), which considers factors such as geographic Skates (Order Rajiformes, Class: Chondrichthyes) are extent of range and abundance to determine extinction risk. characterised by a highly conserved morphology. The Its vulnerability is therefore currently unknown and more identification of species boundaries, fundamental for data concerning its biology and ecology is required to effective conservation management, is therefore challeng- establish responsible management. In particular, the taxo- ing. This issue is reflected in market mis-labelling of nomic status of skates identified as R. maderensis in the commercial landings (Igle´sias et al. 2010; Griffiths et al. Azores needs to be resolved, especially as recent molecular 2013). Complementary molecular approaches can assist evidence suggested little difference between R. clavata and a with defining these boundaries and verifying species specimen identified as R. maderensis landed in a Portuguese identifications. In particular, the mitochondrial ‘barcoding’ fish market (Serra-Pereira et al. 2011). The distinct dorsal gene, cytochrome c oxidase subunit I (COI), can reveal pattern (Fig. S1) of R. maderensis reportedly distinguishes it differentiation at fine taxonomic levels, yet usefully from the morphologically highly similar thornback ray (R. diverges little within species (Hebert et al. 2003). COI clavata). However, the thornback ray is noticeably variable barcoding has recently proven a successful tool for vali- with regard to its general morphology when compared to dating skate identification in a number of fisheries (Spies many other European rajiids, with polychromatism recorded et al. 2006; Serra-Pereira et al. 2011; Coulson et al. 2011; in the Mediterranean (Mnasri et al. 2009) and a number of Mabragan˜a et al. 2011; Lynghammar et al. 2014). recognised patterns relatively widely known in the UK Like many elasmobranchs worldwide, skate populations (Pritchard 1977), as well as documented cases of albinism in Europe have experienced significant declines, and in (Ball et al. 2013). It also occupies a much greater geo- some cases even local extirpation, owing to historic and graphical range, particularly in terms of latitude, than many current high levels of fishing pressure (Brander 1981; other skates. The thornback ray is distributed from Norway Dulvy et al. 2000). The reproductive strategy of skates is and Iceland to Northwest Africa, including the Mediter- characterised by late maturity and low fecundity, which ranean and Black Seas, and until recently was considered to coupled with susceptibility to capture, makes them argu- inhabit waters as far south as southern Africa (Froese and ably some of the most vulnerable of all exploited marine Pauly 2011). The latter records most likely represented mis- fishes (Dulvy et al. 2014). Their commercial importance is identifications of the recently diverged and morphologically often low compared to other demersal fisheries, resulting in similar biscuit skate, Raja straeleni, distributed in southern historically poor management of this group (Dulvy et al. Africa (Pasolini et al. 2011). Similarly, the rough ray (Raja 2000). Despite this, catches remain significant, with the radula), restricted to the Mediterranean (Morey et al. 2009) total weight of all landings of the most common European is regarded as a sister species to R. clavata. This species is considered to have split from the main lineage (Valsecchi et al. 2005), following re-colonisation of the western 9 The Laboratory, Marine Biological Association of the United Kingdom, Plymouth PL1 2PB, UK Mediterranean basin by R. clavata after the Late Miocene Messinian salinity crisis, around 5 Myr ago (Rogl 1998; 10 Ecosystems & Environment Research Centre, School of Environment & Life Sciences, University of Salford, Duggen et al. 2003). The question of whether R. maderensis Greater Manchester M5 4WT, UK represents a distinct species, or merely another morpholog- 11 Department of Oceanography and Fisheries, Centre of IMAR ical variant of the polytypic thornback ray, therefore remains of the University of the Azores, Rua Prof. Doutor Frederico unanswered. Clearly, there is a need to sample R. clavata and Machado, 9901-862 Horta, Azores, Portugal R. maderensis across their geographical range and assess 12 Marine Laboratory, Marine Scotland Science, their genetic relatedness in comparison to other closely P.O. Box 101, Aberdeen AB119DB, UK related species, such as R. straeleni and R. radula. 13 School of Biosciences, University of Exeter, Exeter,
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