Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic)

Cold-water corals are widely considered as important structural components of benthic habitats, potentially enhancing local abundance in a variety of fish and invertebrate species. Yet, current knowledge of the taxonomic diversity and distribution patterns of these vulnerable, slow-growing organisms is scarce and fragmented, limiting the effectiveness of spatial management and conservation measures. We have conducted an exhaustive compilation of records of alcyonaceans, antipatharians, scleractinians and stylasterids available through present day to assess the diversity, distribution and spatial structure of coral assemblages in the Azores exclusive economic zone (EEZ). The resulting database comprises 2501 entries concerning historical oceanographic expeditions and other published sources, as well as unpublished data from bottom longline by-catch. Our taxonomic inventory appears to be fairly complete for the explored habitats, accounting for 164 species (79 alcyonaceans, 58 scleractinians, 18 antipatharians and 9 stylasterids), nine of which were documented for the first time. The Azores EEZ harbours a mixed coral fauna with several zoogeographic origins, showing the closest affinity with the Lusitanian–Mediterranean region. Very few apparent endemics were found (14%), and only in part supported by consistent sampling. Coral diversity is particularly high between 300 and 900 m depths, in areas recognized as traditional fishing grounds or exploitable fish habitat within the 100-mile limit of the EEZ. The composition of coral assemblages shows significant geographical structure among longitudinal sections of the study area at comparable depths (100–1500 m). There is no evidence of a possible role of the Mid-Atlantic Ridge or latitudinal effects underlying this pattern, which suggests that it may instead reflect assemblage variability among features. Stronger changes in species composition were found along the bathymetric gradient. Notwithstanding the mix of partially overlapping steno- and eurybathic species that characterize the vertical distribution of corals, there is a distinct transition from shallow (100–600 m) to intermediate (600–1000 m) depths. The analysis presented here constitutes a valuable contribution for efficient conservation policies of coral-associated vulnerable marine ecosystems and their sustainable use as fishing areas.

[1]  Nuno Lourenco,et al.  Morpho-tectonic analysis of the Azores Volcanic Plateau from a new bathymetric compilation of the area , 1998 .

[2]  T. O’hara Seamounts : centres of endemism or species richness for ophiuroids? , 2007 .

[3]  N. Hareide,et al.  The distribution and catch rates of deep water fish along the Mid-Atlantic Ridge from 43 to 61°N , 2001 .

[4]  K. Gjerde,et al.  Management and Conservation of Seamounts , 2008 .

[5]  Jaime S. Davies,et al.  Deep-sea coral distribution on seamounts, oceanic islands, and continental slopes in the Northeast Atlantic , 2007 .

[6]  N. Boury-Esnault,et al.  Les démosponges littorales de l'archipel des Açores , 1985 .

[7]  R. Waller Deep-water Scleractinia (Cnidaria: Anthozoa): current knowledge of reproductive processes , 2005 .

[8]  Fred N. Spiess,et al.  Corals on seamount peaks provide evidence of current acceleration over deep-sea topography , 1986, Nature.

[9]  M. Carreiro-Silva,et al.  The association between a deep-sea gastropod Pedicularia sicula (Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa: Stylasteridae) in the Azores , 2011 .

[10]  A. Agassiz List of the echinoderms sent to different institutions in exchange for other specimens, with annotations , 1863 .

[11]  J. Marques,et al.  The Benthic Amphipod Fauna of the Azores (Portugal): an Up-To-Date Annotated List of Species, and Some Biogeographic Considerations , 1993 .

[12]  T. Pitcher,et al.  Can We Protect Seamounts for Research? A Call for Conservation , 2010 .

[13]  D. Wagner,et al.  Sexual reproduction of the Hawaiian black coral Antipathes griggi (Cnidaria: Antipatharia) , 2012, Coral Reefs.

[14]  K. R. Clarke,et al.  On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages , 2006 .

[15]  F. Stokvis,et al.  New and redescribed encrusting species of Alcyonium from the Atlantic Ocean (Octocorallia: Alcyonacea: Alcyoniidae) , 2006 .

[16]  J. Guinan,et al.  Quantifying relationships between video observations of cold-water coral cover and seafloor features in Rockall Trough, west of Ireland , 2009 .

[17]  A. Foubert,et al.  Hydrodynamics and cold-water coral facies distribution related to recent sedimentary processes at Galway Mound west of Ireland , 2007 .

[18]  S. Cairns A generic revision of the Stylasteridae (Coelenterata: Hydrozoa). Part 2. Phylogenetic analysis , 1984 .

[19]  A. Milne-edwards,et al.  Expéditions scientifiques du Travailleur et du Talisman pendant les années 1880, 1881, 1882, 1883 , 1888 .

[20]  S. Cairns Deep-water corals: An overview with special reference to diversity and distribution of deep-water scleractinian corals , 2007 .

[21]  H. Zibrowius Les scléractiniaires de la Méditerranée et de l'Atlantique nord-oriental , 1980 .

[22]  T. T. Suttona,et al.  Vertical structure , biomass and topographic association of deep-pelagic fishes in relation to a mid-ocean ridge system , 2008 .

[23]  J. Thomson Alcyonaires provenant des campagnes scientifiques du Prince Albert 1er de Monaco , 1927 .

[24]  Evan N. Edinger,et al.  Ages and growth rates of some deep-sea gorgonian and antipatharian corals of Newfoundland and Labrador , 2009 .

[25]  David S.M. Billett,et al.  Depth-related distribution and abundance of seastars (Echinodermata: Asteroidea) in the Porcupine Seabight and Porcupine Abyssal Plain, N.E. Atlantic , 2002 .

[26]  A. Gebruk,et al.  Bathyal benthic fauna of the Mid-Atlantic Ridge between the Azores and the Reykjanes Ridge , 2009, Journal of the Marine Biological Association of the United Kingdom.

[27]  E. Pante,et al.  Deep-sea octocorals and antipatharians show no evidence of seamount-scale endemism in the NW Atlantic , 2009 .

[28]  D. Opresko Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae , 2001 .

[29]  J. Jullien,et al.  Bryozoaires provenant des campagnes de l'Hirondelle (1886-1888) , 1903 .

[30]  E. Pante,et al.  Biology of deep-water octocorals. , 2011, Advances in marine biology.

[31]  Hans van Haren,et al.  Downwelling and deep‐water bottom currents as food supply mechanisms to the cold‐water coral Lophelia pertusa (Scleractinia) at the Mingulay Reef Complex , 2009 .

[32]  C. McClain,et al.  Patterns in Deep-Sea Macroecology , 2009 .

[33]  A. Tixier-Durivault,et al.  Les Octocoralliaires de la campagne Biaçores , 1974 .

[34]  O. Ocaña,et al.  An occurrence of ring sea anemones (Anthozoa, Actiniaria) in the Azores region , 2007 .

[35]  S. Ávila Shallow-water marine molluscs of the Azores : biogeographical relationchips. , 2000 .

[36]  A. Rowden,et al.  Out of Their Depth? Isolated Deep Populations of the Cosmopolitan Coral Desmophyllum dianthus May Be Highly Vulnerable to Environmental Change , 2011, PloS one.

[37]  Marina Carreiro-Silva,et al.  Carrying behavior in the deep-sea crab Paromola cuvieri (Northeast Atlantic) , 2011, Marine Biodiversity.

[38]  G. Somero Cold Ocean Physiology: Adaptation to cold and depth: contrasts between polar and deep-sea animals , 1998 .

[39]  Biogeographic Affinities of the North Atlantic Deep-Water Scleractinia , 2001 .

[40]  I. Stevens,et al.  A fine resolution model of the eastern North Atlantic between the Azores, the Canary Islands and the Gibraltar Strait , 2000 .

[41]  J. Koslow,et al.  Diversity and endemism of the benthic seamount fauna in the southwest Pacific , 2000, Nature.

[42]  G. Menezes,et al.  Demersal fish on a mid-ocean ridge: Distribution patterns and structuring factors , 2008 .

[43]  A. Foubert,et al.  The distribution of scleractinian corals in the Bay of Biscay, NE Atlantic , 2008 .

[44]  L. Lundsten,et al.  Endemicity, Biogeography, Composition, and Community Structure On a Northeast Pacific Seamount , 2009, PloS one.

[45]  David A. Mucciarone,et al.  Extreme longevity in proteinaceous deep-sea corals , 2009, Proceedings of the National Academy of Sciences.

[46]  Ana Colaço,et al.  Mapping Condor Seamount Seafloor Environment and Associated Biological Assemblages (Azores, NE Atlantic) , 2012 .

[47]  Robert K. Colwell,et al.  Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness , 2001 .

[48]  P. Snelgrove,et al.  Distributional patterns of deep-sea coral assemblages in three submarine canyons off Newfoundland, Canada , 2012 .

[49]  S. Gaines,et al.  The relationship between dispersal ability and geographic range size. , 2007, Ecology letters.

[50]  Gilles Reverdin,et al.  North Atlantic Ocean surface currents , 2003 .

[51]  M. Sigler,et al.  Structure and zonation of demersal fish assemblages off the Azores Archipelago (mid-Atlantic) , 2006 .

[52]  Alan Williams,et al.  Seamount benthic macrofauna off southern tasmania: community structure and impacts of trawling , 2001 .

[53]  G. Duineveld,et al.  Hydrodynamic controls on cold-water coral growth and carbonate-mound development at the SW and SE Rockall Trough Margin, NE Atlantic Ocean , 2007 .

[54]  Erik Cordes,et al.  Reproduction and growth of Anthomastus ritteri (Octocorallia: Alcyonacea) from Monterey Bay, California, USA , 2001 .

[55]  J. Galbraith,et al.  Patterns of distribution of deepwater demersal fishes of the North Atlantic mid-ocean ridge, continental slopes, islands and seamounts , 2012 .

[56]  M. Boisselier,et al.  Seamount endemism questioned by the geographic distribution and population genetic structure of marine invertebrates , 2006 .

[57]  S. Ávila,et al.  BIOGEOGRAPHICAL RELATIONSHIPS OF THE MOLLUSCAN FAUNA OF THE ORMONDE SEAMOUNT (GORRINGE BANK, NORTHEAST ATLANTIC OCEAN) , 2003 .

[58]  H. Westerberg,et al.  The distribution of the scleractinian coral Lophelia pertusa around the Faroe islands and the relation to internal tidal mixing , 1992 .

[59]  A. B. Hernández,et al.  Corales de las Islas Canarias: antozoos con esqueleto de los fondos litorales y profundos = Corals of the Canary Islands : skeleton anthozoa of the littoral and deep bottoms , 2004 .

[60]  M. Aurivillius The Gorgonarians from Dr. Sixten Bock's expedition to Japan and Bonin Islands 1914 , 1931 .

[61]  T. Pitcher,et al.  Abundance and distribution of seamounts in the Azores , 2008 .

[62]  S. Cairns A Generic Revision of the Stylasteridae (Coelenterata: Hydrozoa) Part 3 Keys to the Genera , 1984 .

[63]  T. Schlacher,et al.  Squat lobster assemblages on seamounts differ from some, but not all, deep-sea habitats of comparable depth , 2010 .

[64]  P. Auster,et al.  Definition and detection of vulnerable marine ecosystems on the high seas: problems with the “move-on” rule , 2011 .

[65]  G. Calado,et al.  Molluscan diversity in the North Atlantic Ocean: new records of opisthobranch gastropods from the Archipelago of the Azores , 2009 .

[66]  Ch. Gravier Madréporaires provenant des Campagnes des yachts Princesse-Alice et Hirondelle II (1893-1913) , 1920 .

[67]  M. Grasshoff Die Gorgonaria der Expeditionen von « Travailleur » 1880-1882 und « Talisman » 1883 (Cnidaria, Anthozoa) , 1986, Bulletin du Muséum national d'histoire naturelle.

[68]  A. Verdière,et al.  Instability dynamics of a subtropical jet and applications to the azores front current system : Eddy-driven mean flow , 1999 .

[69]  Paul J. B. Hart,et al.  Biogeography and Biodiversity of Seamounts , 2008 .

[70]  Marina Carreiro-Silva,et al.  Variability in growth rates of long-lived black coral Leiopathes sp. from the Azores , 2013 .

[71]  Th. Studer Alcyonaires provenant des campagnes de l'Hirondelle (1886-1888) , 1901 .

[72]  F. Tempera,et al.  New occurrences of Corallium spp. (Octocorallia, Coralliidae) in the Central Northeast Atlantic , 2009 .

[73]  C. McClain,et al.  The dynamics of biogeographic ranges in the deep sea , 2010, Proceedings of the Royal Society B: Biological Sciences.

[74]  Raymond R. Wilson,et al.  Seamount Biota and Biogeography , 2013 .

[75]  E. Kenchington,et al.  Reproductive biology of the deep-water coral Acanella arbuscula (Phylum Cnidaria: Class Anthozoa: Order Alcyonacea), northwest Atlantic , 2012 .

[76]  J. Dauvin,et al.  Can seamounts provide a good habitat for polychaete annelids? Example of the northeastern Atlantic seamounts , 2008 .

[77]  M. Carreiro-Silva,et al.  Isozoanthus primnoidus, a new species of zoanthid (Cnidaria: Zoantharia) associated with the gorgonian Callogorgia verticillata (Cnidaria: Alcyonacea) , 2011 .

[78]  Lene Buhl-Mortensen,et al.  Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins , 2010 .

[79]  Robert K. Colwell,et al.  INTERPOLATING, EXTRAPOLATING, AND COMPARING INCIDENCE-BASED SPECIES ACCUMULATION CURVES , 2004 .

[80]  H. Harring Report of the Canadian Arctic Expedition 1913-1918 , 2009 .

[81]  F. Tempera,et al.  First record of Antipathella subpinnata (Anthozoa, Antipatharia) in the Azores (NE Atlantic), with description of the first monotypic garden for this species , 2014 .

[82]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[83]  Great Britain. Foreign Office. Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873-76. Zoology , 1880 .

[84]  K. Speer,et al.  Directly measured mid-depth circulation in the northeastern North Atlantic Ocean , 2002, Nature.

[85]  J. V. D. Land Report on the CANCAP-Project for Marine Biological research in the Canarian - Cape Verdean Region of the North Atlantic Ocean (1976-1986). Part I. List of stations , 1987 .

[86]  E. Pante,et al.  Limitations of mitochondrial gene barcoding in Octocorallia , 2011, Molecular ecology resources.

[87]  Benjamin S. Halpern,et al.  Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation , 2007, Proceedings of the National Academy of Sciences.

[88]  R. Tong,et al.  Multivariate Statistical Analysis of Distribution of Deep-Water Gorgonian Corals in Relation to Seabed Topography on the Norwegian Margin , 2012, PloS one.

[89]  E. Edinger,et al.  Distribution of deep-sea corals in the Newfoundland and Labrador region , Northwest Atlantic Ocean , 2008 .

[90]  T. Molodtsova,et al.  Anthozoa from the northern Mid-Atlantic Ridge and Charlie-Gibbs Fracture Zone , 2008 .

[91]  A. Wheeler,et al.  Reefs of the Deep: The Biology and Geology of Cold-Water Coral Ecosystems , 2006, Science.

[92]  J. Hamel,et al.  Planulation periodicity, settlement preferences and growth of two deep-sea octocorals from the northwest Atlantic , 2010 .

[93]  F. Bayer Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa , 1981 .

[94]  P. B. Mortensen,et al.  Occurrence of deep-water corals on the Mid-Atlantic Ridge based on MAR-ECO data , 2008 .

[95]  F. Bayer,et al.  Illustrated trilingual glossary of morphological and anatomical terms applied to Octocorallia , 1983 .

[96]  L. Roule Description des Antipathaires et Cérianthaires recueillis par S.A.S. le Prince de Monaco dans l'Atlantique nord. (1886-1902) ... , 1905 .

[97]  J. Drazen,et al.  Depth zonation and bathymetric trends of deep-sea megafaunal scavengers of the Hawaiian Islands , 2009 .

[98]  A. Metaxas,et al.  Predicting suitable habitat for deep-water gorgonian corals on the Atlantic and Pacific Continental Margins of North America , 2007 .

[99]  A. Shanks Pelagic Larval Duration and Dispersal Distance Revisited , 2009, The Biological Bulletin.

[100]  Clark,et al.  The Science behind the Guidelines: A Scientific Guide to the FAO Draft International Guidelines (December 2007) for the Management of Deep-Sea Fisheries in the High Seas and Examples of How the Guidelines may be Practically Implemented. , 2008 .

[101]  J. Hamel,et al.  Contrasting reproductive strategies in three deep-sea octocorals from eastern Canada: Primnoaresedaeformis, Keratoisis ornata, and Anthomastus grandiflorus , 2011, Coral Reefs.

[102]  S. Campana,et al.  Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history , 2008, Proceedings of the Royal Society B: Biological Sciences.

[103]  Elizabeth E. Boyle,et al.  Phylogeography of a pan‐Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic , 2011, Molecular ecology.

[104]  P. Tyler,et al.  Megafauna from sublittoral to abyssal depths along the Mid-Atlantic Ridge south of Iceland , 1996 .

[105]  Pål Buhl-Mortensen,et al.  Using EUNIS habitat classification for benthic mapping in European seas: present concerns and future needs. , 2012, Marine pollution bulletin.

[106]  L. Monteiro,et al.  Marine research, resources and conservation in the Azores , 1995 .

[107]  T. Morato,et al.  Cold-water corals landed by bottom longline fisheries in the Azores (north-eastern Atlantic) , 2012, Journal of the Marine Biological Association of the United Kingdom.

[108]  Virginie Lafon,et al.  Sea surface temperature distribution in the Azores region. Part II: space-time variability and underlying mechanisms. , 2004 .

[109]  Elizabeth E. Boyle,et al.  Bathymetric and geographic population structure in the pan‐Atlantic deep‐sea bivalve Deminucula atacellana (Schenck, 1939) , 2006, Molecular ecology.

[110]  J. Hall‐Spencer,et al.  In situ observations of fish associated with coral reefs off Ireland , 2011 .

[111]  De Pourtals,et al.  Deep-Sea Corals , 2011 .

[112]  Vonda E. Wareham,et al.  Deep cold‐water corals as nurseries for fish larvae , 2012 .

[113]  S. Cairns,et al.  Revision of the northeast Atlantic and Mediterranean Stylasteridae (Cnidaria: Hydrozoa) , 1992 .

[114]  Lene Buhl-Mortensen,et al.  Distribution of deep-water gorgonian corals in relation to benthic habitat features in the Northeast Channel (Atlantic Canada) , 2004 .

[115]  L. Nøttestad,et al.  Distribution and abundance of fish in deep-sea coral habitats , 2002, Hydrobiologia.