Marine Biology

, 165:3 | Cite as

Contrasting evolutionary patterns in populations of demersal sharks throughout the western Mediterranean

  • Sergio Ramírez-AmaroEmail author
  • Antonia Picornell
  • Miguel Arenas
  • Jose A. Castro
  • Enric Massutí
  • M. M. Ramon
  • Bàrbara Terrasa
Original paper


The spotted catshark (Scyliorhinus canicula) and the blackmouth catshark (Galeus melastomus) are demersal sharks showing a distinct bathymetric distribution in the western Mediterranean. Together, both species represent more than 85% of the total abundance of demersal chondrichthyans in this Mediterranean basin. Our study provides a complete analysis of the genetic population structure, connectivity and demographic history of both species. Sampling was performed across four geographical subareas (GSAs) established by the General Fisheries Commission for the Mediterranean in the western Mediterranean: the northern Alboran Sea (GSA01), Alboran Island (GSA02), Balearic Islands (GSA05) and northern Spain (GSA06). Three mitochondrial fragments were analyzed for both species, and 12 microsatellite loci for S. canicula. We found contrasting patterns of population structure and connectivity in both species. Scyliorhinus canicula displayed significant genetic differences and low connectivity between some GSAs corresponding to different sub-basins (Alboran vs. Balearic). In contrast, G. melastomus showed absence of a population structure and high connectivity between GSAs. These findings are in accordance with the fact that both species exhibit different dispersal behaviors, which leads to distinct bathymetric distributions. Contrasting demographic histories were also identified: Scyliorhinus canicula revealed a recent stable population, with evidence of bottlenecks in the past, which may be related to Pleistocene glacial periods; whereas G. melastomus showed a recent population expansion. Altogether, our findings indicate a mismatch between fishery subareas and population structure for both sharks, which must be considered for fisheries management purposes.



The authors wish to thank all participants in the MEDITS surveys, as well as the crew of R/V Cornide de Saavedra and the Genetics Laboratory team of the Universitat de les Illes Balears. We also thank Dr. Ioanna Manolopoulou for extensive help with the BPEC analyses and Prof. Antonio Amorim for helpful comments. Three anonymous reviewers and the Editor are also greatly acknowledged for their constructive comments in improving the quality of the manuscript.

Compliance with ethical standards


This research was supported in part by the Consejo Nacional de Ciencia y Tecnología (CONACyT) of Mexico, through the FPI Fellowship of SRA, the Direcció General de Innovació i Recerca del Govern de les Illes Balears and the European Regional Development Fund (FEDER), through the Special Actions “Introducción de las técnicas moleculares en la identificación de stocks y conectividad de poblaciones marinas” (AAEE030/2012) and “Mejora de los estudios de diversidad íctica en las Islas Baleares mediante técnicas morfológicas y moleculares” (AAEE7/2015), the project DEMBAGOL funded by the European Commission and the Instituto Español de Oceanografía through the Data Collection Framework and the projects ECLIPSAME and CLIFISH funded by the Spanish Ministry of Economy and Competitiveness (Plan Estatal I + D + I; CTM2012-37701 and CTM2015-66400-C3-1R, respectively). MA was supported by the Fundação para a Ciência e a Tecnologia (FCT) of the Portuguese Government through the FCT Starting Grant IF/00955/2014 and by the Spanish Government through the fellowship “Ramón y Cajal” RYC-2015-18241.

Conflict of interest

All authors declare they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2017_3254_MOESM1_ESM.pdf (519 kb)
Supplementary material 1 (PDF 520 kb)


  1. Alcántara-Carrió J, Albarracín S, Montoya-Montes I, Flor-Blanco G, Fontán-Bouzas A, Rey-Salgado J (2013) An indurated Pleistocene coastal barrier on the inner shelf on the Gulf of Valencia (western Mediterranean): evidence for a prolonged relative sea-level stillstand. Geo Mar Lett 33:209–216CrossRefGoogle Scholar
  2. Arenas M, Ray N, Currat M, Excoffier L (2012) Consequences of range contractions and range shifts on molecular diversity. Mol Biol Evol 29:207–218CrossRefGoogle Scholar
  3. Arenas M, Mona S, Trochet A, Sramkova Hanulova A, Currat M, Ray N, Chikhi L, Rasteiro R, Schmeller DS, Excoffier L (2014) The scaling of genetic diversity in a changing and fragmented world. In: Henle K, Potts SG, Kunin WE, Matsinos YG, Similä J, Pantis JD, Grobelnik V, Penev L, Settele J (eds) Scaling in ecology and biodiversity conservation. Pensoft Publishers, Sofia, pp 55–60Google Scholar
  4. Barbieri M, Maltagliati F, Roldán MI, Castelli A (2014) Molecular contribution to stock identification in the small-spotted catshark, Scyliorhinus canicula (Chondrichthyes, Scyliorhinidae). Fish Res 154:11–16CrossRefGoogle Scholar
  5. Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographic patterns across the Atlantic–Mediterranean divide. J Evol Biol 16:1149–1158CrossRefGoogle Scholar
  6. Baro J, Rueda JL, Díaz del Río V (2012) South Iberian submarine canyons in the Alborán sea: geohabitats, associated communities and fisheries resources. In: Würtz M (ed) Mediterranean submarine canyons: ecology and governance. IUCN, Malaga, pp 145–156Google Scholar
  7. Bertrand JA, Gil de Sola L, Papaconstantinou C, Relini G, Souplet A (2002) The general specifications of the MEDITS surveys. Sci Mar 66:9–17CrossRefGoogle Scholar
  8. Botsford LW, Hastings A, Gaines SD (2001) Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecol Lett 4:144–150CrossRefGoogle Scholar
  9. Camhi M, Fowler S, Musick J, Bräutigam A, Fordham S (1998) Sharks and their relatives: ecology and conservation. IUCN/SSC Shark Specialist Group, CambridgeGoogle Scholar
  10. Capapé C, Mnasri-Sioudi N, Kamel-Moutalibi O, Boumaïza M, Ben Amor MM, Reynaud C (2014) Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (Central Mediterranean). J Ichthyol 54:111–126CrossRefGoogle Scholar
  11. Carbonell A, Alemany F, Merella P, Quetglas A, Román E (2003) The by-catch of sharks in the western Mediterranean (Balearic Islands) trawl fishery. Fish Res 61:7–18CrossRefGoogle Scholar
  12. Cardinale M, Osio GC (2013) State of fish stocks and fisheries in European waters: status of Mediterranean and Black Sea resources in European waters in 2013. European Commission Joint Research Center, IspraGoogle Scholar
  13. Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu Rev Mar Sci 7:547–570CrossRefGoogle Scholar
  14. Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705CrossRefGoogle Scholar
  15. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  16. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefGoogle Scholar
  17. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  18. Corrigan S, Huveneers C, Stow A, Beheregaray B (2016) A multilocus comparative study of dispersal in three codistributed demersal sharks from eastern Australia. Can J Fish Aquat Sci 73:1–10CrossRefGoogle Scholar
  19. Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859CrossRefGoogle Scholar
  20. Cunha RL, Coscia I, Madeira C, Mariani S, Stefanni S, Castilho R (2012) Ancient divergence in the trans-oceanic deep-sea shark Centroscymnus crepidater. PLoS One 7:e49196CrossRefGoogle Scholar
  21. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  22. Drummond A, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefGoogle Scholar
  23. Dudgeon CL, Broderick D, Ovenden R (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Mol Ecol 18:248–261CrossRefGoogle Scholar
  24. Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan JAT, Tillett BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. J Fish Biol 80:1789–1843CrossRefGoogle Scholar
  25. Duncan KM, Martin AP, Bowen BW, Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251CrossRefGoogle Scholar
  26. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  27. Ebert DA, Fowler S, Compagno L (2013) Sharks of the world. Wild Nature Press, PlymouthGoogle Scholar
  28. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  29. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50CrossRefGoogle Scholar
  30. Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA (1999) Do population size bottlenecks reduce evolutionary potential? Anim Conserv 2:255–260CrossRefGoogle Scholar
  31. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  32. Gaida IH (1997) Population structure of the Pacific angel shark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia 1:738–744CrossRefGoogle Scholar
  33. Gaines SD, White C, Carr MH, Palumbi SR (2010) Designing marine reserve networks for both conservation and fisheries management. Proc Natl Acad Sci 107:18286–18293CrossRefGoogle Scholar
  34. Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114CrossRefGoogle Scholar
  35. Griffiths AM, Casane D, McHugh M, Wearmounth VJ, Sims DW, Genner MJ (2011) Characterisation of polymorphic microsatellite loci in the small-spotted catshark (Scyliorhinus canicula). Conserv Genet Resour 3:705–709CrossRefGoogle Scholar
  36. Griffiths AM, Jacoby DMP, Casane D, McHugh M, Croft DP, Genner MJ, Sims DW (2012) First analysis of multiple paternity in an oviparous shark species, the small-spotted catshark (Scyliorhinus canicula L.). J Hered 103:166–173CrossRefGoogle Scholar
  37. Gubili C, Sims DW, Veríssimo A, Domenici P, Ellis J, Grigoriou P, Johnson AF, McHugh M, Neat F, Satta A, Scarcella G, Serra-Pereira B, Soldo A, Genner MJ, Griffiths AM (2014) A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe. R Soc Open Sci 1:140175CrossRefGoogle Scholar
  38. Gubili C, Macleod K, Perry W, Hanel P, Batzakas I, Farrell ED, Lynghammar A, Mancusi C, Mariani S, Menezes GM, Neat F, Scarcella G, Griffiths AM (2016) Connectivity in the deep: phylogeography of the velvet belly lanternshark. Deep Sea Res I 115:233–239CrossRefGoogle Scholar
  39. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  40. Hanski I (1998) Metapopulation dynamics. Nature 396:41–49CrossRefGoogle Scholar
  41. Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600Google Scholar
  42. Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642CrossRefGoogle Scholar
  43. Kousteni V, Kontopoulou M, Megalofonou P (2010) Sexual maturity and fecundity of Scyliorhinus canicula (Linnaeus, 1758) in the Aegean Sea. Mar Biol Res 6:390–398CrossRefGoogle Scholar
  44. Kousteni V, Kasapidis P, Kotoulas G, Megalofonou P (2014) Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114:333–343CrossRefGoogle Scholar
  45. Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770CrossRefGoogle Scholar
  46. Le Port A, Lavery S (2012) Population structure and phylogeography in the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the Southern hemisphere. J Hered 103:174–185CrossRefGoogle Scholar
  47. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  48. Lleonart J, Maynou F (2003) Fish stock assessments in the Mediterranean: state of the art. Sci Mar 67:37–49CrossRefGoogle Scholar
  49. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  50. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247CrossRefGoogle Scholar
  51. Lykousis V (2009) Sea-level changes and shelf break prograding sequences during the last 400 ka in the Aegean margins: subsidence rates and palaeogeographic implications. Cont Shelf Res 29:2037–2044CrossRefGoogle Scholar
  52. Magoulas A, Castilho R, Caetano S, Marcato S, Patarnello T (2006) Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus). Mol Phylogenet Evol 39:734–746CrossRefGoogle Scholar
  53. Malak DA, Livingstone SR, Pollard D, Polidoro BA, Cuttelod A, Bariche M, Bilecenoglu M, Carpenter KE, Collette BB, Francour P, Goren M, Kara MH, Massutí E, Papaconstantinou C, Tunesi L (2011) Overview of the conservation status of the marine fishes of the Mediterranean Sea. IUCN, GlandGoogle Scholar
  54. Manolopoulou I, Emerson BC (2012) Phylogeographic ancestral inference using the coalescent model on haplotype trees. J Comput Biol 19:745–755CrossRefGoogle Scholar
  55. Manolopoulou I, Legarreta L, Emerson BC, Brooks S, Tavaré S (2011) A Bayesian approach to phylogeographic clustering. Interface Focus 1:909–921CrossRefGoogle Scholar
  56. Massutí E, Olivar MP, Monserrat S, Rueda L, Oliver P (2014) Towards understanding the influence of environmental conditions on demersal resources and ecosystems in the western Mediterranean: motivations, aims and methods of the IDEADOS project. J Mar Syst 138:3–19CrossRefGoogle Scholar
  57. Millot C (1999) Circulation in the western Mediterranean Sea. J Mar Syst 20:423–442CrossRefGoogle Scholar
  58. Mona S, Ray N, Arenas M, Excoffier L (2014) Genetic consequences of habitat fragmentation during a range expansion. Heredity 11:291–299CrossRefGoogle Scholar
  59. Monserrat S, López-Jurado JL, Marcos M (2008) A mesoscale index to describe the regional circulation around the Balearic Islands. J Mar Syst 71:413–420CrossRefGoogle Scholar
  60. Moranta J, Stefanescu C, Massutí E, Morales-Nin B, Lloris D (1998) Fish community structure and depth-related trends on the continental slope of the Balearic Islands (Algerian basin, western Mediterranean). Mar Ecol Prog Ser 171:247–259CrossRefGoogle Scholar
  61. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  62. Musick JA, Harbin MM, Compagno LJV (2004) Historical zoogeography of the Selachii. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 33–78CrossRefGoogle Scholar
  63. Nielsen EE, Nielsen PH, Meldrup D, Hansen M (2004) Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol Ecol 13:585–595CrossRefGoogle Scholar
  64. Ordines F, Bauzá M, Sbert M, Roca P, Gianotti M, Massutí E (2014) Red algal beds increase the condition of nekton-benthic fish. J Sea Res 95:115–123CrossRefGoogle Scholar
  65. Ovenden JR, Berry O, Welch DJ, Buckworth R, Dichmont M (2015) Ocean’s eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish Fish 16:125–159CrossRefGoogle Scholar
  66. Padrón M, Guizien K (2016) Modelling the effect of demographic traits and connectivity of the genetic structuration of marines metapopulations of sedentary benthic invertebrates. ICES J Mar Sci 73(7):1935–1945CrossRefGoogle Scholar
  67. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  68. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  69. Pinot JM, López-Jurado JL, Riera M (2002) The CANALES experiment (1996–1998). Interannual, seasonal and mesoscale variability of the circulation in the Balearic Channels. Prog Oceanogr 55:335–370CrossRefGoogle Scholar
  70. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  71. Portnoy DS, Heist EJ (2012) Molecular markers: progress and prospects for understanding reproductive ecology in elasmobranchs. J Fish Biol 80:1120–1140CrossRefGoogle Scholar
  72. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  73. Rambaut A, Drummond AJ (2009) Tracer version 1.5. [computer program]
  74. Ramírez-Amaro S, Ordines F, Terrasa B, Esteban A, García C, Guijarro B, Massutí E (2015) Demersal chondrichthyans in the western Mediterranean: assemblages and biological parameters of their main species. Mar Freshw Res 67:636–652CrossRefGoogle Scholar
  75. Ramón M, Abelló P, Ordines F, Massutí E (2014) Deep epibenthic communities in two contrasting areas of the Balearic Islands (western Mediterranean). J Mar Syst 138:182–193CrossRefGoogle Scholar
  76. Reiss H, Hoarau G, Dickey-Collas M, Wolff WJ (2009) Genetic population structure of marine fish: mismatch between biological and fisheries management units. Fish Fish 10:361–395CrossRefGoogle Scholar
  77. Rey J, Massutí E, Gil de Sola L (2005) Distribution and biology of the blackmouth catshark Galeus melastomus in the Alborán Sea (southwestern Mediterranean). J Northwest Atl Fish Sci 35:215–223CrossRefGoogle Scholar
  78. Rodríguez-Cabello C, Sánchez F, Fernández A, Olaso I (2004) Is the lesser spotted dogfish (Scyliorhinus canicula) from the Cantabrian Sea a unique stock? Fish Res 69:57–71CrossRefGoogle Scholar
  79. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  80. Rohling EJ, Foster GL, Grant KM, Marino G, Roberts AP, Tamisiea ME, Williams F (2014) Sea-level and deep-sea temperature variability over the past 5.3 million years. Nature 508:432–477CrossRefGoogle Scholar
  81. Rozenfeld AF, Arnaud-Haond S, Hernández-García E, Eguíluz VM, Serrão EA, Duarte CM (2008) Network analysis identifies weak and strong links in a metapopulation system. Proc Natl Acad Sci 105:18824–18829CrossRefGoogle Scholar
  82. Scacco U, La Messa G, Vacchi M (2010) Body morphometrics, swimming diversity and niche in demersal sharks: a comparative case study from the Mediterranean Sea. Sci Mar 74:37–53CrossRefGoogle Scholar
  83. Simpfendorfer CA, Kyne PM (2009) Limited potential to recover from overfishing raises concerns for deep-sea sharks, rays and chimaeras. Environ Conserv 36:97–103CrossRefGoogle Scholar
  84. Sims DW, Nash JP, Morritt D (2001) Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation. Mar Biol 139:1165–1175CrossRefGoogle Scholar
  85. Soria G, Torre-Cosio J, Munguia-Vega A, Marinone SG, Lavín MF, Cinti A, Moreno-Báez M (2014) Dynamic connectivity patterns from an insular marine protected area in the Gulf of California. J Mar Syst 129:248–258CrossRefGoogle Scholar
  86. Stefanescu C, Lloris D, Rucabado J (1992) Deep-living demersal fishes in the Catalan Sea (western Mediterranean) below a depth of 1000 m. J Nat Hist 26:197–213CrossRefGoogle Scholar
  87. Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  88. Terrasa B, Pérez-Mellado V, Brown RP, Picornell A, Castro JA, Ramon MM (2009) Foundations for conservation of intraspecific genetic diversity revealed by analysis of phylogeographical structure in the endangered endemic lizard Podarcis lilfordi. Divers Distrib 15:207–221CrossRefGoogle Scholar
  89. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  90. Treml EA, Halpin PN (2012) Marine population connectivity indentifies ecological neighbors for conservation planning in the Coral Triangle. Conserv Lett 5:441–449CrossRefGoogle Scholar
  91. Veríssimo A, McDowell JR, Graves JE (2010) Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution. Mol Ecol 19:1651–1662CrossRefGoogle Scholar
  92. Veríssimo A, McDowell JR, Graves JE (2011) Population structure of a deep-water squaloid shark, the Portuguese dogfish (Centroscymnus coelolepis). ICES J Mar Sci 68:555–563CrossRefGoogle Scholar
  93. Vignaud T, Maynard JA, Leblois R, Meekan MG, Vázquez-Juárez R, Ramírez-Macías D, Pierce S, Rowat D, Berumen ML, Beeravolu C, Baksay S, Planes S (2014) Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline. Mol Ecol 23:2590–2601CrossRefGoogle Scholar
  94. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790CrossRefGoogle Scholar
  95. Würtz M (2012) Mediterranean submarine canyons: ecology and governance. IUCN, GlandGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Laboratori de GenèticaUniversitat de les Illes BalearsPalma de MallorcaSpain
  2. 2.Instituto Español de OceanografíaCentre Oceanogràfic de les BalearsPalma de MallorcaSpain
  3. 3.Department of Biochemistry, Genetics and ImmunologyUniversity of VigoVigoSpain
  4. 4.Instituto de Investigação e Inovação em Saúde (i3S)University of PortoPortoPortugal
  5. 5.Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP)PortoPortugal

Personalised recommendations