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Marine Biology

, 165:135 | Cite as

Population genetics of Narella versluysi (Octocorallia: Alcyonacea, Primnoidae) in the Bay of Biscay (NE Atlantic)

  • Chris Yesson
  • Erin Wright
  • Andreia Braga-Henriques
Original paper

Abstract

Octocoral species are globally distributed in all oceans and may form dense communities known as vulnerable marine ecosystems. Despite their importance as deep-water habitats, the underlying genetic structure and gene-flow patterns of most deep-water populations remain largely unknown. Here, we evaluated genetic connectivity of the primnoid octocoral Narella versluysi across the continental shelf of Bay of Biscay, spanning 360 km (95 samples from submarine canyons, ranging from 709–1247 m depths). We report 12 novel microsatellite markers which were used to genotype 83 samples from 6 populations. Sixteen samples were sequenced for three mitochondrial DNA regions (Folmer region of COI with an adjacent intergenic region igr1, MT-ND2 gene, and mtMutS homolog 1 region). All sequence haplotypes and genetic clusters were found in multiple sites spanning more than 200 km. Overall, our analyses suggest that there is high gene flow between colonies of N. versluysi among all study sites. There is no significant geographic structure and no pattern of isolation by distance or depth. Connectivity is facilitated by the prevailing current which runs along the shelf break, and could be a mechanism to connect all of the sampled locations. The high connectivity over large geographic distance is a positive sign for a potentially vulnerable organism and may provide some resilience to disturbance. This information is crucial for a better understanding of how this fragile benthic fauna may respond to climatic and anthropogenic disturbances, which is a cornerstone for effective habitat management.

Notes

Acknowledgements

Thanks go to the crew of “NO Porquois Pas?”, ROV pilots, and researchers on the BobEco cruise. This work was supported by the European Community’s Seventh Framework Programme (FP7/2007–2013) under grant agreement number 213144, the “CoralFISH” Project. Thanks also to Dada Gottelli, Rob Yarlett, and Meesha Patel for assistance in the lab. ABH was partly supported by (1) an FRCT grant of the Government of the Azores (ref. M3.1.2/F/016/2008), (2) the Oceanic Observatory of Madeira project (M1420-01-0145-FEDER-000001-Observatório Oceânico da Madeira-OOM) co-financed by the Madeira Regional Operational Programme (Madeira 14-20) under the Portugal 2020 strategy through the European Regional Development Fund, and (3) the Portuguese Foundation for Science and Technology (FCT, Portugal), through the strategic project UID/MAR/04292/2013 granted to MARE.

Funding

This study was funded by European Community’s Seventh Framework Programme (FP7/2007–2013) under grant agreement number 213144, the “CoralFISH” Project.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the sampling, care, and use of organisms were followed. Approval for this work was obtained from the institutions of all participants.

References

  1. Althaus F, Williams A, Schlacher TA, Kloser RJ, Green MA, Barker BA, Bax NJ, Brodie P, Schlacher-Hoenlinger MA (2009) Impacts of bottom trawling on deep-coral ecosystems of seamounts are long-lasting. Mar Ecol Prog Ser 397:279–294CrossRefGoogle Scholar
  2. Arnaud-Haond S, Van den Beld IM, Becheler R, Orejas C, Menot L, Frank N, Grehan A, Bourillet JF (2017) Two “pillars” of cold-water coral reefs along Atlantic European margins: prevalent association of Madrepora oculata with Lophelia pertusa, from reef to colony scale. Deep Sea Res II Top Stud Oceanogr 145:110–119CrossRefGoogle Scholar
  3. Ayata S-D, Lazure P, Thiébaut É (2010) How does the connectivity between populations mediate range limits of marine invertebrates? A case study of larval dispersal between the Bay of Biscay and the English Channel (North-East Atlantic). Prog Oceanogr 87:18–36CrossRefGoogle Scholar
  4. Baco AR, Cairns SD (2012) Comparing molecular variation to morphological species designations in the deep-sea coral Narella reveals new insights into seamount coral ranges. PLoS ONE 7(9):e45555CrossRefPubMedPubMedCentralGoogle Scholar
  5. Baco AR, Etter RJ, Ribeiro PA, Von Der Heyden S, Beerli P, Kinlan BP (2016) A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design. Mol Ecol 25:3276–3298CrossRefPubMedGoogle Scholar
  6. Barnett TP, Pierce DW, AchutaRao KM, Gleckler PJ, Santer BD, Gregory JM, Washington WM (2005) Penetration of human-induced warming into the world’s oceans. Science 309(5732):284–287CrossRefPubMedGoogle Scholar
  7. Baums IB, Hughes CR, Hellberg ME (2005) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 288:115–127CrossRefGoogle Scholar
  8. Becheler R, Cassone AL, Noël P, Mouchel O, Morrison CL, Arnaud-Haond S (2017) Low incidence of clonality in cold water corals revealed through the novel use of a standardized protocol adapted to deep sea sampling. Deep Sea Res II Top Stud Oceanogr 145:120–130CrossRefGoogle Scholar
  9. Benayahu Y, Loya Y (1985) Settlement and recruitment of a soft coral: why is Xenia macrospiculata a successful colonizer? Bull Mar Sci 36(1):177–188Google Scholar
  10. Bourillet JF, Reynaud JY, Baltzer A, Zaragosi S (2003) The ‘Fleuve Manche’: the submarine sedimentary features from the outer shelf to the deep-sea fans. J Quat Sci 18(3–4):261–282CrossRefGoogle Scholar
  11. Bradbury IR, Laurel B, Snelgrove PVR, Bentzen P, Campana SE (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proc R Soc B Biol Sci 275:1803–1809CrossRefGoogle Scholar
  12. Braga-Henriques A (2014) Cold-water coral communities in the Azores: diversity, habitat and conservation. Ph.D. Thesis. University of the Azores, Portugal. http://hdl.handle.net/10400.3/3615
  13. Braga-Henriques A, Pereira JN, Tempera F, Porteiro FM, Pham C, Morato T, Santos RS (2011) Cold-water coral communities on Condor Seamount: initial interpretations. In: Giacomello E, Menezes G (eds) CONDOR observatory for long-term study and monitoring of azorean seamount ecosystems. Final Project Report, Arquivos do DOP, Série Estudos 1/2012, Horta, Portugal, pp 105–114Google Scholar
  14. Braga-Henriques A, Porteiro FM, Ribeiro PA, de Matos V, Sampaio Í, Ocaña O, Santos RS (2013) Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic). Biogeosciences 10:4009–4036CrossRefGoogle Scholar
  15. Brazeau DA, Lasker HR (1989) The reproductive cycle and spawning in a Caribbean gorgonian. Biol Bull 176:1–7CrossRefGoogle Scholar
  16. Brito TAS, Tyler PA, Clarke A (1997) Reproductive biology of the Antarctic octocoral Thouarella variabilis Wright & Studer, 1889. In: den Hartog JC (ed) Coelenterate biology: proceedings of the 6th international congress of coelenterate biology. Nationaal Natuurhistorisch Museum, Leiden, pp 63–69Google Scholar
  17. Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water Scleractinian corals. Bull Mar Sci 81:311–322Google Scholar
  18. Cairns SD (2012) The Marine Fauna of New Zealand: New Zealand Primnoidae (Anthozoa: Alcyonacea). Part 1. Genera Narella, Narelloides, Metanarella, Calyptrophora, and Helicoprimnoa. NIWA Biodiversity Memoir. NIWA (National Institute of Water and Atmospheric Research Ltd), Wellington, pp 1–126Google Scholar
  19. Cairns SD, Baco A (2007) Review and five new Alaskan species of the deep-water octocoral Narella (Octocorallia: Primnoidae). Syst Biodivers 5(4):391–407CrossRefGoogle Scholar
  20. Cairns SD, Bayer FM (2003) Studies on western Atlantic Octocorallia (Coelenterata: Anthozoa). Part 3: The genus Narella Gray, 1870. Proc Biol Soc Wash 116(3):617–648Google Scholar
  21. Cairns SD, Bayer FM (2008) A review of the Octocorallia (Cnidaria: Anthozoa) from Hawai’i and adjacent seamounts: the genus Narella. Pac Sci 62:83–115CrossRefGoogle Scholar
  22. Cairns SD, Bayer FM (2009) A generic revision and phylogenetic analysis of the Primnoidae (Cnidaria: Octocorallia). Smithson Contrib Zool 629:1–79CrossRefGoogle Scholar
  23. Cardona Y, Ruiz-Ramos DV, Baums IB, Bracco A (2016) Potential connectivity of coldwater black coral communities in the Northern Gulf of Mexico. PLoS ONE 11(5):e0156257CrossRefPubMedPubMedCentralGoogle Scholar
  24. Clark MR, Schlacher TA, Rowden AA, Stocks KI, Consalvey M (2012) Science priorities for seamounts: research links to conservation and management. PLoS ONE 7:e29232CrossRefPubMedPubMedCentralGoogle Scholar
  25. Clark MR, Althaus F, Schlacher TA, Williams A, Bowden DA, Rowden AA (2016) The impacts of deep-sea fisheries on benthic communities: a review. ICES J Mar Sci 73:51–69.  https://doi.org/10.1093/icesjms/fsv123 CrossRefGoogle Scholar
  26. Constantini F, Rossi S, Pintus E, Cerrano C, Gili J-M, Abbiati M (2011) Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations. Coral Reefs 30:991–1003CrossRefGoogle Scholar
  27. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466CrossRefGoogle Scholar
  28. Dahl MP, Pereyra RT, Lundälv T, André C (2012) Fine-scale spatial genetic structure and clonal distribution of the cold-water coral Lophelia pertusa. Coral Reefs 31(4):1135–1148CrossRefGoogle Scholar
  29. Daly M, Brugler MR, Cartwright P, Collins AG, Dawson MN, Fautin DG, France SC, McFadden CS, Opresko DM, Rodriguez E, Romano SL (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182Google Scholar
  30. Devlin B, Risch N (1995) A comparison of linkage disequilibrium measures for fine-scale mapping. Genomics 29(2):311–322CrossRefPubMedGoogle Scholar
  31. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Res 14(1):209–214CrossRefGoogle Scholar
  32. Etter RJ, Bower AS (2015) Dispersal and population connectivity in the deep North Atlantic estimated from physical transport processes. Deep Sea Res I 104:159–172CrossRefGoogle Scholar
  33. Faurby S, Barber PH (2012) Theoretical limits to the correlation between pelagic larval duration and population genetic structure. Mol Ecol 21:3419–3432CrossRefPubMedGoogle Scholar
  34. Foley N, Armstrong CW (2010) The ecological and economic value of cold-water coral ecosystems. Ocean Coast Manag 53:313–326.  https://doi.org/10.1016/j.ocecoaman.2010.04.009 CrossRefGoogle Scholar
  35. France SC, Hoover LL (2002) DNA sequences of the mitochondrial COI gene have low levels of divergence among deep-sea octocorals (Cnidaria: Anthozoa). Hydrobiologia 471(1-3):149–155CrossRefGoogle Scholar
  36. Genin A, Dayton PK, Spiess FN (1986) Corals on seamount peaks provide evidence of current acceleration over deep-sea topography. Nature 322:59–61CrossRefGoogle Scholar
  37. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 12 Jan 2016
  38. Goudet J, Jombart T (2015) hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.04-22. http://CRAN.R-project.org/package=hierfstat. Accessed 12 Jan 2016
  39. Grasshoff M (1982) Die Gorgonaria, Pennatularia, und Antipatharia des Tiefwassers der Biskaya (Cnidaria, Anthozoa). II: Taxonomischer Teil. Bull Mus Natl Hist Nat Paris 4e Sér 3 (Sect A) 4:941–978Google Scholar
  40. Guinotte JM, Orr J, Cairns S, Freiwald A, Morgan L, George R (2006) Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals? Front Ecol Environ 4:141–146CrossRefGoogle Scholar
  41. Hartnoll RG (1975) The annual cycle of Alcyonium digitatum. Estuar Coast Shelf Sci 3:71–78CrossRefGoogle Scholar
  42. Herrera S, Shank TM, Sánchez JA (2012) Spatial and temporal patterns of genetic variation in the widespread antitropical deep-sea coral Paragorgia arborea. Mol Ecol 21(24):6053–6067CrossRefPubMedGoogle Scholar
  43. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226CrossRefGoogle Scholar
  44. Hilário A, Metaxas A, Gaudron SM, Howell KL, Mercier A, Mestre NC, Ross RE, Thurnherr AM, Young C (2015) Estimating dispersal distance in the deep sea: challenges and applications to marine reserves. Front Mar Sci 2:00006CrossRefGoogle Scholar
  45. Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27(21):3070–3071CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefPubMedPubMedCentralGoogle Scholar
  47. Jones GP, Srinivasan M, Almany GR (2007) Conservation of marine biodiversity. Oceanography 20(3):100CrossRefGoogle Scholar
  48. Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, Van Oppen MJ, Willis BL (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28(2):307–325CrossRefGoogle Scholar
  49. Kahng SE, Benayahu Y, Lasker HR (2011) Sexual reproduction in octocorals. Mar Ecol Prog Ser 443:265–283CrossRefGoogle Scholar
  50. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  51. Koutsikopoulos C, Le Cann B (1996) Physical processes and hydrological structures related to the Bay of Biscay Anchovy. Sci Mar 60:9–19Google Scholar
  52. Lacharité M, Metaxas A (2013) Early life history of deep-water gorgonian corals may limit their abundance. PLoS ONE 8(6):e65394:1–e65394:10CrossRefGoogle Scholar
  53. Larsson AI, van Oevelen D, Purser A, Thomsen L (2013) Tolerance to long-term exposure of suspended benthic sediments and drill cuttings in the cold-water coral Lophelia pertusa. Mar Pollut Bull 70(1–2):176–188CrossRefPubMedGoogle Scholar
  54. Lasker HR (1984) Asexual reproduction, fragmentation, and skeletal morphology of a plexaurid gorgonian. Mar Ecol Prog Ser 19:261–268CrossRefGoogle Scholar
  55. Le Goff-Vitry MC, Rogers AD (2005) Molecular ecology of Lophelia pertusa in the NE Atlantic. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Erlangen Earth conference series. Springer, Berlin, pp 771–805Google Scholar
  56. Le Goff-Vitry MC, Pybus OG, Rogers AD (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 13(3):537–549CrossRefPubMedGoogle Scholar
  57. Lett C, Ayata SD, Huret M, Irisson JO (2010) Biophysical modelling to investigate the effects of climate change on marine population dispersal and connectivity. Prog Oceanogr 87(1–4):106–113CrossRefGoogle Scholar
  58. Lindner A, Cairns S, Cunningham CW (2008) From offshore to onshore: multiple origins for shallow water corals from deep-sea ancestors. PLoS ONE 3:e2429CrossRefPubMedPubMedCentralGoogle Scholar
  59. McFadden CS, Tullis ID, Hutchinson MB, Winner K, Sohm JA (2004) Variation in coding (NADH dehydrogenase subunits 2, 3, and 6) and noncoding intergenic spacer regions of the mitochondrial genome in Octocorallia (Cnidaria: Anthozoa). Mar Biotechnol 6(6):516–526CrossRefPubMedGoogle Scholar
  60. McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Res 11(1):19–31CrossRefGoogle Scholar
  61. Mengerink KJ, Van Dover CL, Ardron J, Baker M, Escobar-Briones E, Gjerde K, Koslow JA, Ramirez-Llodra E, Lara-Lopez A, Squires D, Sutton T (2014) A call for deep-ocean stewardship. Science 344(6185):696–698CrossRefPubMedGoogle Scholar
  62. Mercier A, Hamel JF (2011) Contrasting reproductive strategies in three deep-sea octocorals from eastern Canada: Primnoa resedaeformis; Keratoisis ornata, and Anthomastus grandiflorus. Coral Reefs 30:337–350CrossRefGoogle Scholar
  63. Miller KJ, Gunasekera RM (2017) A comparison of genetic connectivity in two deep sea corals to examine whether seamounts are isolated islands or stepping stones for dispersal. Sci Rep 7:46103CrossRefPubMedPubMedCentralGoogle Scholar
  64. Miller K, Williams A, Rowden AA, Knowles C, Dunshea G (2010) Conflicting estimates of connectivity among deep-sea coral populations. Mar Ecol 31(s1):144–157CrossRefGoogle Scholar
  65. Miller KJ, Rowden AA, Williams A, Haussermann V (2011) Out of their depth? Isolated deep populations of the cosmopolitan coral Desmophyllum dianthus may be highly vulnerable to environmental change. PLoS ONE 6(5):e19004CrossRefPubMedPubMedCentralGoogle Scholar
  66. Mokhtar-Jamaï K, Coma R, Wang J, Zuberer F, Feral J-P, Aurelle D (2013) Role of evolutionary and ecological factors in the reproductive success and the spatial genetic structure of the temperate gorgonian Paramuricea clavata. Ecol Evol 3(1765):1779Google Scholar
  67. Morrison CL, Eackles MS, Johnson RL, King TL (2008) Characterization of 13 microsatellite loci for the deep-sea coral, Lophelia pertusa (Linnaeus 1758), from the western North Atlantic Ocean and Gulf of Mexico. Mol Ecol Res 8(5):1037–1039CrossRefGoogle Scholar
  68. Morrison CL, Ross SW, Nizinski MS, Brooke S, Järnegren J, Waller RG, Johnson RL, King TL (2011) Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 12(3):713–729CrossRefGoogle Scholar
  69. Orejas C, Gili JM, Lopez-Gonzalez PJ, Hasemann C, Arntz WE (2007) Reproduction patterns of four Antarctic octocorals in the Weddell Sea: an inter-specific, shape, and latitudinal comparison. Mar Biol 150:551–563CrossRefGoogle Scholar
  70. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420CrossRefPubMedGoogle Scholar
  71. Pey A, Catanéo J, Forcioli D, Merle PL, Furla P (2013) Thermal threshold and sensitivity of the only symbiotic Mediterranean gorgonian Eunicella singularis by morphometric and genotypic analyses. Comptes Rendus Biol 336(7):331–341CrossRefGoogle Scholar
  72. Quattrini AM, Baums IB, Shank TM, Morrison CL, Cordes EE (2015) Testing the depth-differentiation hypothesis in a deepwater octocoral. Proc R Soc B 282:20150008CrossRefPubMedGoogle Scholar
  73. Rex MA, Etter RJ (2010) Deep-sea biodiversity: pattern and scale. Harvard University Press, CambridgeGoogle Scholar
  74. Roberts JM (2009) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  75. Roberts JM, Cairns SD (2014) Cold-water corals in a changing ocean. Curr Opin Environ Sustain 7:118–126CrossRefGoogle Scholar
  76. Rosen BR, Taylor JD (1969) Reef coral from Aldabra: new mode of reproduction. Science 166:119–121CrossRefPubMedGoogle Scholar
  77. Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Res 6:600–602Google Scholar
  78. Sammarco PW (1982) Polyp bail-out: an escape response to environmental stress and a new means of reproduction in corals. Mar Ecol Prog Ser 10:57–65CrossRefGoogle Scholar
  79. Soetaert K, Mohn C, Rengstorf A, Grehan A, van Oevelen D (2016) Ecosystem engineering creates a direct nutritional link between 600-m deep cold-water coral mounds and surface productivity. Sci Rep 6:35057CrossRefPubMedPubMedCentralGoogle Scholar
  80. Taylor ML, Rogers AD (2017) Primnoidae (Cnidaria: Octocorallia) of the SW Indian Ocean: new species, genus revisions and systematics. Zool J Linn Soc 181:70–97CrossRefGoogle Scholar
  81. Taylor ML, Roterman CN (2017) Invertebrate population genetics across Earth’s largest habitat: the deep-sea floor. Mol Ecol 26(19):4872–4896CrossRefPubMedGoogle Scholar
  82. Thiem Ø, Ravagnan E, Fosså JH, Berntsen J (2006) Food supply mechanisms for cold-water corals along a continental shelf edge. J Mar Syst 60(3–4):207–219CrossRefGoogle Scholar
  83. Treml EA, Halpin PN, Urban DL, Pratson LF (2008) Modelling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landsc Ecol 23:19–36CrossRefGoogle Scholar
  84. van den Beld IMJ, Guillaumont B, Menot L, Bayle C, Arnaud-Haond S, Bourillet J-F (2017a) Marine litter in submarine canyons of the Bay of Biscay. Deep Sea Res II Top Stud Oceanogr 145:142–152.  https://doi.org/10.1016/j.dsr2.2016.04.013 CrossRefGoogle Scholar
  85. van den Beld IMJ, Bourillet J-F, Arnaud-Haond S, de Chambure L, Davies JS, Guillaumont B, Olu K, Menot L (2017b) Cold-water coral habitats in submarine canyons of the Bay of Biscay. Front Mar Sci 4:118.  https://doi.org/10.3389/fmars.2017.00118 CrossRefGoogle Scholar
  86. Van Rooij D, De Mol L, Le Guilloux E, Wisshak M, Huvenne VAI, Moeremans R, Henriet JP (2010) Environmental setting of deep-water oysters in the Bay of Biscay. Deep Sea Res I Oceanogr Res Pap 57:1561–1572CrossRefGoogle Scholar
  87. Waller RG, Tyler PA (2005) The reproductive biology of two deep-water, reef-building scleractinians from the NE Atlantic Ocean. Coral Reefs 24:514–522CrossRefGoogle Scholar
  88. Waller RG, Tyler PA, Gage JD (2002) Reproductive ecology of the deep-sea solitary coral Fungiacyathus marenzelleri (Scleractinia) in the northeast Atlantic Ocean. Coral Reefs 21(4):325–331Google Scholar
  89. Waller RG, Stone RP, Johnstone J, Mondragon J (2014) Sexual reproduction and seasonality of the Alaskan red tree coral, Primnoa pacifica. PLoS ONE 9:e90893CrossRefPubMedPubMedCentralGoogle Scholar
  90. Wang S, Zhang L, Matz M (2009) Microsatellite characterization and marker development from public EST and WGS databases in th reef-building coral Acropora millepora (Cnidaria, Anthozoa, Scleractinia). J Hered 100(3):329–337CrossRefPubMedGoogle Scholar
  91. Wheeler AJ, Bett BJ, Billett DSM, Masson DG, Mayor D (2005) The impact of demersal trawling on northeast Atlantic deepwater coral habitats: the case of the Darwin Mounds, United Kingdom. In: Thomas J, Barnes P (eds) Benthic habitats and the effects of fishing, vol 41. American Fisheries Society symposium, Bethesda MD, USA, pp 807–817Google Scholar
  92. White HK, Hsing P-Y, Cho W, Shank TM, Cordes EE, Quattrini AM, Nelson RK, Camilli R, Demopoulos AWJ, German CR, Brooks JM, Roberts HH, Shedd W, Reddy CM, Fisher CR (2012) Impact of the deep-water horizon oil spill on a deep-water coral community in the Gulf of Mexico. Proc Natl Acad Sci USA 109(50):20303–20308CrossRefPubMedGoogle Scholar
  93. Wright EP, Kemp K, Rogers AD, Yesson C (2015) Genetic structure of the tall sea pen Funiculina quadrangularis in NW Scottish sea lochs. Mar Ecol 36(3):659–667CrossRefGoogle Scholar
  94. Yeoh SR, Dai CF (2010) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Mar Biol 157:351–359CrossRefGoogle Scholar
  95. Yesson C, Taylor ML, Tittensor DP, Davies AJ, Guinotte J, Baco A, Black J, Hall-Spencer JM, Rogers AD (2012) Global habitat suitability of cold-water octocorals. J Biogeogr 39(7):1278–1292CrossRefGoogle Scholar
  96. Zardus JD, Etter RJ, Chase MC, Rex MA, Boyle EE (2006) Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Mol Ecol 15(3):639–651CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of ZoologyZoological Society of LondonLondonUK
  2. 2.MARE-Marine and Environmental Sciences CentreEstação de Biologia Marinha do FunchalFunchalPortugal
  3. 3.ARDITI-Regional Agency for the Development of Research, Technology and InnovationOceanic Observatory of Madeira (OOM)FunchalPortugal

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