Population Structure of the Thornback Ray (Raja Clavata L.) in British Waters ⁎ Malia Chevolot A, , Jim R
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Journal of Sea Research 56 (2006) 305–316 www.elsevier.com/locate/seares Population structure of the thornback ray (Raja clavata L.) in British waters ⁎ Malia Chevolot a, , Jim R. Ellis b, Galice Hoarau a, Adriaan D. Rijnsdorp c, Wytze T. Stam a, Jeanine L. Olsen a a Department of Marine Benthic Ecology and Evolution, Center for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands b Centre for Environment Fisheries and Aquaculture Sciences (CEFAS), Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK c Wageningen Institute for Marine Resources and Ecological Studies (IMARES), Animal Sciences Group, Wageningen UR, P.O. Box 68, 1970 AB IJmuiden, The Netherlands Received 27 July 2005; accepted 24 May 2006 Available online 17 June 2006 Abstract Prior to the 1950s, thornback ray (Raja clavata L.) was common and widely distributed in the seas of Northwest Europe. Since then, it has decreased in abundance and geographic range due to over-fishing. The sustainability of ray populations is of concern to fisheries management because their slow growth rate, late maturity and low fecundity make them susceptible to exploitation as victims of by-catch. We investigated the population genetic structure of thornback rays from 14 locations in the southern North Sea, English Channel and Irish Sea. Adults comprised <4% of the total sampling despite heavy sampling effort over 47 hauls; thus our results apply mainly to sexually immature individuals. Using five microsatellite loci, weak but significant population differentiation was detected with a global FST = 0.013 (P < 0.001). Pairwise Fst was significant for 75 out of 171 comparisons. Although earlier tagging studies suggest restricted foraging distances from home areas, the absence of genetic differentiation between some distant populations suggests that a substantial fraction of individuals migrate over wide areas. Autumn/winter locations appear to have a lower level of differentiation than spring/summer, which could be due to seasonal migration. Management and conservation of thornback ray populations will be challenging as population structure appears to be dynamic in space and time. © 2006 Elsevier B.V. All rights reserved. Keywords: Elasmobranchs; Genetic structure; Microsatellite; Thornback ray; Rajidae 1. Introduction Africa (Stehmann and Bürkel, 1994), though their taxonomic status in these waters is unclear. Around Thornback ray, Raja clavata, is a widely distributed the British Isles, thornback rays are most abundant in skate (Rajiformes: Rajidae) in the eastern Atlantic, coastal waters and large bays, including The Wash, ranging from Norway and Iceland to Northwest Africa, Outer Thames Estuary, Solent, Carmarthen Bay, Cardi- including the Mediterranean and Black Seas. They may gan Bay, Liverpool Bay and Solway Firth (Ellis et al., also occur in the Atlantic and Indian Oceans of southern 2005). Prior to the 1950s, thornback rays were common and widespread in the North Sea, but have declined ⁎ Corresponding author. thereafter in distribution and abundance (Walker and E-mail address: [email protected] (M. Chevolot). Heessen, 1996; Walker and Hislop, 1998). 1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2006.05.005 306 M. Chevolot et al. / Journal of Sea Research 56 (2006) 305–316 Thornback rays are targeted in inshore longline and be rare, as well as between the English and French coasts gillnet fisheries in coastal waters of the British Isles, and across the English Channel. It was hypothesised that this are also an important component of the mixed demersal separation was probably due to the deeper waters and trawl fisheries. Despite R. clavata being one of the most strong currents in the Dover Strait (Walker et al., 1997). commercially valuable rays, the economic value of their Taken together, tagging studies suggest that R. clavata total catch is small in comparison to other demersal may have restricted ranges and potentially strong species (e.g. sole and plaice) and as such they have not localised population differentiation-particularly among been the focus of fisheries management. Between 1956 younger individuals. and 1995, R. clavata disappeared from the waters along To date, only a few population genetic studies based on the continental coasts of the North Sea and showed an nuclear markers have been conducted on elasmobranchs, overall decline of nearly 80% in this area (Walker and and all of these have been on sharks. Heist and Gold Heessen, 1996). Similarly, they are thought to have (1999) found no differentiation (three microsatellite loci) declined by approximately 45% between 1988 and 1997 in population structure of sandbar sharks (Carcharinus in the Irish Sea (Dulvy et al., 2000). This rapid decrease plumbeus) between the mid-Atlantic Bight and the has led to concern about the sustainability of ray western Gulf of Mexico. Schrey and Heist (2003) populations (Walker et al., 1997; Dulvy et al., 2000), observed evidence of population differentiation (four especially given their low fecundity, slow growth, and microsatellite loci) in shortfin mako shark (Isurus late maturity, which makes them potentially vulnerable oxyrinchus) between the North Atlantic and North Pacific. to exploitation (Brander, 1981; Heist, 1999). Feldheim et al. (2001) found weak but significant The fecundity of R. clavata is thought to be in the population structure (four microsatellite loci) in the range of 48–150 eggs per year (Holden, 1975; Ryland lemon shark (Negaprion brevirostris) in the western and Ajayi, 1984; Ellis and Shackley, 1995). Following Atlantic Ocean. Keeney et al. (2005) also found a weak mating in early spring, eggs are deposited regularly, with but significant population structure (8 microsatellite loci the spawning season occurring between February and and control region of the mtDNA) in the blacktip shark September (Holden, 1975), though the egg-laying (Carcharinus limbatus) between nine nursery areas periods of individuals may be more restricted (Holden (Northwestern Atlantic, Eastern, Western Gulf of Mexico, et al., 1971; Ellis and Shackley, 1995). Fertilised eggs North Yucatan and Belize). In studies where nuclear and are deposited as egg cases on the seabed and, after 4– mitochondrial markers were used, evidence for male- 5 months incubation, fully formed rays (ca. 8 cm disc biased dispersal and female philopatry has been suggested width) hatch (Ellis and Shackley, 1995). Tagging studies for white shark Carcharodon carcharias (Pardini et al., have shown that juveniles tend to remain in shallow 2001), shortfin mako (Schrey and Heist, 2003), lemon waters (10–30 m deep) for several years, with shark (Feldheim et al., 2001) and blacktip shark (Keeney recaptured individual close to the point of release et al., 2005). Only one population structure study has been (Walker et al., 1997). conducted on a Rajidae by Blake (1976) on thornback R. clavata matures at between 9 and 12 y of age rays in the Irish Sea using a eye-lens protein. No (Nottage and Perkins, 1983). At this stage, adults show differentiation was found, probably due to the lack of seasonal movements, from deeper waters (10 to 30 m) in polymorphism of the allozyme. winter, to shallower waters (<10 m) in spring, where they Here, we investigate the population genetic structure are presumed to mate and spawn (Walker et al., 1997). of R. clavata in the southern North Sea, English Despite these seasonal movements, past tagging experi- Channel, and Irish Sea using five microsatellite loci. ments indicated that 100% of the individuals remained The objectives were to determine the spatial scale of R. within a 60 nautical miles (nmi) area and 80% remained clavata population differentiation, assess the home within 20 nmi. This ‘home range’ has since been extended range based on assignment tests, and to compare to a maximum travelling distance of 70 nmi from studies migratory movements based on genetic data with using Data Storage Tags (DSTs) (Hunter et al., 2005b). those based on earlier tagging data. Their study also confirmed the seasonal movement pattern of thornback for mature and immature individuals 2. Material and methods (30–60 cm total length), and showed a philopatric behaviour as most individual rays were found in the 2.1. Sampling and DNA extraction same area during spring/summer time every year (Hunter et al., 2005a). Wider-ranging migrations between the A total of 483 immature rays were sampled from 14 southern North Sea and the English Channel appeared to locations during standard, annual bottom trawl surveys M. Chevolot et al. / Journal of Sea Research 56 (2006) 305–316 307 conducted by various fisheries institutes from 2002 to was determined using internal lane standard (GENES- 2004 (Table 1). Five out of the 14 locations were CAN™ 350 ROX™) and GENESCAN™ software. sampled at different time period (Fig. 1, Table 1). Adults were only rarely represented in the sampling (N = 20) 2.3. Data analysis and, therefore, not included in the population structure analysis. Individuals were classified as adult or The software package MICRO-CHECKER 2.2.1 (Van immature based on reproductive criteria, i.e., presence Oosterhout et al., 2004) was used to check for of fully differentiated shell glands for females and fully genotyping errors due to null alleles, stuttering, and developed testes and claspers for males (Stehmann, large allele drop-out for all loci and all locations. 1995). If reproductive data were not available, total Allelic diversity was calculated and corrected for length (<55 cm for immature) was substituted. sample size using GENCLONE β version (Arnaud-Haond Sampling was not easy as any single haul (fishing and Belkhir, available on request). In order to compare for 30 min at 4 nmi/h) provided only a small number of diversity among populations of different sample sizes, individuals (mean=4.7 individuals/haul, SD=5.8). the program performs a jacknife re-sampling of Single hauls producing >20 individuals occurred only individuals at each location.