Gold coral (Savalia savaglia) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone

The twilight or mesophotic zone is amongst the less explored marine regions. In coastal areas, investigations and manipulative experiments on benthic biodiversity and ecosystem functioning at depths up to >50 m have been recently made possible by the progress of SCUBA techniques. In this study, we tested the effects of the presence of a gorgonian forest characterised by a large and dense population of the gold coral Savalia savaglia (Bertoloni 1819) on the benthic biodiversity (nematode species richness, and meiofauna community structure and richness of taxa), trophic guilds state (molluscs) and ecosystem functioning in the surrounding sediments. The S. savaglia colonies create elevated and complex tertiary structures. Our results indicate that the presence of these colonies was associated with a significantly increased deposition of bioavailable substrates and enhanced biodiversity, when compared with soft bottoms at the same depth but without gold corals. The higher biodiversity and altered trophic conditions resulted in higher rates of ecosystem functioning (e.g., higher benthic biomasses). These results suggest that S. savaglia should be particularly protected not only for its specific rarity, endemism and vulnerability but also because it has a prominent role in sustaining high levels of biodiversity and ecosystem functioning in the surrounding benthos of the twilight zone.

[1]  G. Sarà,et al.  Seasonal and spatial changes in the sediment organic matter of a semi-enclosed marine system (W-Mediterranean Sea) , 1999, Hydrobiologia.

[2]  R. Cattaneo-Vietti,et al.  Annual Sedimentation Rates and Role of the Resuspension Processes Along a Vertical Cliff (Ligurian Sea, Italy) , 1995 .

[3]  M. Chiantore,et al.  Community experiments using benthic chambers : 2. Meio- and macrofaunal community structure and metabolism , 1999 .

[4]  S. Beaulieu.  Life on glass houses: sponge stalk communities in the deep sea , 2001 .

[5]  S. Hurlbert.  The Nonconcept of Species Diversity: A Critique and Alternative Parameters. , 1971, Ecology.

[6]  R. Warwick,et al.  Freeliving marine nematodes. Part 1. British Enoplids. Synopses of the British Fauna No. 28 , 1983 .

[7]  R. Warwick,et al.  Freeliving marine nematodes: Part III. Monhysterida. Synopses of the British Fauna No. 53 , 1998 .

[8]  R. Warwick,et al.  Free-living marine nematodes , 1983 .

[9]  L. Langone,et al.  Biochemical composition and early diagenesis of organic matter in coastal sediments of the NW Adriatic Sea influenced by riverine inputs , 2008 .

[10]  C. Duarte,et al.  Sediment Retention by a Mediterranean Posidonia oceanica Meadow: The Balance between Deposition and Resuspension , 2001 .

[11]  B. Bett,et al.  Direct observation of episodic growth in an abyssal xenophyophore (Protista) , 1993 .

[12]  J. Southon,et al.  Gerardia: Bristlecone pine of the deep-sea? , 1995 .

[13]  Marco Ghisalberti,et al.  Flow and transport in channels with submerged vegetation , 2008 .

[14]  Peter N. Campbell,et al.  Biochemistry (2nd edn) , 1995 .

[15]  Roberto Danovaro,et al.  Effects of intensive mariculture on sediment biochemistry. , 2007, Ecological applications : a publication of the Ecological Society of America.

[16]  L. H. Allen,et al.  Environment of a Costa Rican Forest , 1972 .

[17]  O. Ocaña,et al.  A REVIEW OF GERARDIIDAE (ANTHOZOA: ZOANTHARIA) FROM THE MACARONESIAN ISLANDS AND THE MEDITERRANEAN SEA WITH THE DESCRIPTION OF A NEW SPECIES , 2004 .

[18]  E. Powell,et al.  Taphonomic signature as a function of environmental process: Shells and shell beds in a hurricane-influenced inlet on the Texas coast , 1989 .

[19]  Anselmo Peñas,et al.  Malacological marine fauna from Garraf coast (NE Iberian Peninsula) , 1997 .

[20]  W. F. Boer.  Seagrass–sediment interactions, positive feedbacks and critical thresholds for occurrence: a review , 2007, Hydrobiologia.

[21]  M. Bertolino,et al.  Epibionts of the scallop Adamussium colbecki (Smith, 1902) in the Ross Sea, Antarctica , 2006 .

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

[23]  Ricardo S. Santos,et al.  Comparison of the community structure of the marine molluscs of the “Banco D. João de Castro” seamount (Azores, Portugal) with that of typical inshore habitats on the Azores archipelago , 2007, Helgoland Marine Research.

[24]  P. Polymenakou,et al.  Effects of bottom trawling on the quantity and biochemical composition of organic matter in coastal marine sediments (Thermaikos Gulf, northwestern Aegean Sea) , 2005 .

[25]  Roberto Danovaro,et al.  Exponential Decline of Deep-Sea Ecosystem Functioning Linked to Benthic Biodiversity Loss , 2008, Current Biology.

[26]  C. Salas.  Marine bivalves from off the Southern Iberian Peninsula collected by the Balgim and Fauna 1 expeditions , 1996 .

[27]  C. Allgén.  Freeliving marine nematodes , 1959 .

[28]  J. Gillan.  The twilight zone. , 1995, Nursing times.

[29]  J. Seinhorst.  A Rapid Method for the Transfer of Nematodes From Fixative To Anhydrous Glycerin , 1959 .

[30]  B. Bett,et al.  Organic biogeochemistry of the Darwin Mounds, a deep-water coral ecosystem, of the NE Atlantic , 2004 .

[31]  J. R. Vallentyne,et al.  Biogeochemistry of organic matter—I , 1960 .

[32]  R. Pyle.  Assessing undiscovered fish biodiversity on deep coral reefs using advanced self-contained diving technology , 2000 .

[33]  Johanna H. Rosman,et al.  Spatial patterns of flow and their modification within and around a giant kelp forest , 2007 .

[34]  A. Baco,et al.  Reproductive Morphology of Three Species of Deep-water Precious Corals from the Hawaiian Archipelago: Gerardia Sp., Corallium Secundum, And Corallium Lauuense , 2007 .

[35]  MC Gambi,et al.  Flume observations on flow dynamics in Zostera marina (eelgrass) beds , 1990 .

[36]  M. Astraldi,et al.  Some observations on current measurements on the East Ligurian Shelf, Mediterranean Sea , 1983 .

[37]  C. Heip,et al.  The ecology of marine nematodes , 1985 .

[38]  J. Lawton,et al.  Organisms as ecosystem engineers , 1994 .

[39]  R. Margalef,et al.  Information theory in ecology , 1958 .

[40]  Donald Voet,et al.  Biochemistry, 2nd ed. , 1995 .

[41]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[42]  R. Danovaro,et al.  Detritus rolling down a vertical cliff of the Ligurian Sea (Italy) : the ecological role in hard bottom communities , 1991 .

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

[44]  R. Grigg.  Precious Corals in Hawaii: Discovery of a New Bed and Revised Management Measures for Existing Beds , 2002 .

[45]  Deborah K. Steinberg,et al.  Revisiting Carbon Flux Through the Ocean's Twilight Zone , 2006, Science.

[46]  A. Warén,et al.  Revision of the northeast Atlantic bathyal and abyssal Aclididae, Eulimidae, Epitoniidae (Mollusca, Gastropoda) / , 1986 .

[47]  P. Lambshead.  Marine nematode biodiversity. , 2004 .

[48]  Steven D. Gaines,et al.  Marine community ecology , 2001 .

[49]  R. Danovaro,et al.  Quantity and bioavailability of sediment organic matter as signatures of benthic trophic status , 2009 .

[50]  Oliver C Peppe,et al.  Monitoring environmental variability around cold-water coral reefs: the use of a benthic photolander and the potential of seafloor observatories , 2005 .

[51]  J. Vallentyne.  Biogeochemistry of organic matter—II Thermal reaction kinetics and transformation products of amino compounds , 1964 .

[52]  Robert E. Ulanowicz,et al.  Information Theory in Ecology , 2001, Comput. Chem..

[53]  H. L. Sanders,et al.  Marine Benthic Diversity: A Comparative Study , 1968, The American Naturalist.

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

[55]  A. Wheeler,et al.  Influence of benthic sediment transport on cold‐water coral bank morphology and growth: the example of the Darwin Mounds, north‐east Atlantic , 2008 .

[56]  J. Bruno,et al.  Patch-size dependent habitat modification and facilitation on New England cobble beaches by Spartina alterniflora , 2000, Oecologia.

[57]  George A. Jackson,et al.  Effect of a kelp forest on coastal currents , 1983 .

[58]  M. Rao.  Organic Matter in Marine Sediments Off East Coast of India: GEOLOGICAL NOTES , 1960 .

[59]  S. Gofas.  Rissoidae (Mollusca: Gastropoda) from northeast Atlantic seamounts , 2007 .

[60]  A Peter,et al.  Sediment destabilization by animal tubes , 1981 .

[61]  Michael P. Lesser,et al.  Ecology of mesophotic coral reefs , 2009 .

[62]  A. Hastings,et al.  Using ecosystem engineers to restore ecological systems. , 2006, Trends in ecology & evolution.

[63]  Robert B. Dunbar,et al.  Radiocarbon-based ages and growth rates of Hawaiian deep-sea corals , 2006 .

[64]  N. Shashar,et al.  Hydromechanical boundary layers over a coral reef , 1996 .

[65]  Z. X. Chen,et al.  Nematology: advances and perspectives. Volume 1: Nematode morphology, physiology, and ecology , 2004 .

[66]  R. Warwick,et al.  Freeliving marine nematodes: Part II. British Chromadorida. Synopses of the British Fauna No. 38 , 1988 .

[67]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[68]  R. Danovaro,et al.  Community Experiments Using Benthic Chambers: Microbial Significance in Highly Organic Enriched Sediments , 1999 .