The Symbiosis between Lophelia pertusa and Eunice norvegica Stimulates Coral Calcification and Worm Assimilation

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Mueller, Christina E ^a   Lundälv, Tomas ^b   Middelburg, Jack J ^c   van Oevelen, Dick ^a  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b GÖTEBORG UNIVERSITY   (Sweden)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; NITROGEN 15;

ALGA; ARTEMIA; ARTICLE; CALCIFICATION; CARBON FIXATION; CONTROLLED STUDY; CORAL; CORAL CALCIFICATION; CORAL REEF; CORAL RESPIRATION; EUNICE NORVEGICA; FOOD INTAKE; LOPHELIA PERTUSA; METABOLISM; NITROGEN FIXATION; NONHUMAN; POLYCHAETA; POPULATION ABUNDANCE; RESOURCE PARTITIONING; SKELETON; SYMBIOSIS; ZOOPLANKTON;

ANIMALS; ANTHOZOA; CALCIFICATION, PHYSIOLOGIC; ECOSYSTEM; FEEDING BEHAVIOR; POLYCHAETA; SYMBIOSIS; TEMPERATURE;

EID: 84874911185     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058660     Document Type: Article

References (58)

1. Buhl-Mortensen P, Hovland M, Brattegard T, Farestveit R, (1995) Deep water bioherms of the scleractinian coral Lophelia pertusa (L.) at 64° N on the Norwegian shelf: structure and associated megafauna. Sarsia 80: 145-158.
2. Buhl-Mortensen L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, et al. (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Marine Ecology-an Evolutionary Perspective 31: 21-50.
3. Freiwald A, Fosså JH, Grehan A, Koslow T, Roberts JM (2004) Cold-water coral reefs. UNEP-WCMC, Cambridge, UK.
4. Frederiksen R, Jensen A, Westerberg H, (1992) The distribution of the scleractinian coral Lophelia pertusa around the Faroe Islands and the relation to internal tidal mixing. Sarsia 77: 157-171.
5. Henry LA, Roberts JM, (2007) Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep-Sea Research Part I-Oceanographic Research Papers 54: 654-672.
6. Jonsson LG, Nilsson PG, Floruta F, Lundalv T, (2004) Distributional patterns of macro- and megafauna associated with a reef of the cold-water coral Lophelia pertusa on the Swedish west coast. Marine Ecology-Progress Series 284: 163-171.
7. Roberts JM, Wheeler AJ, Freiwald A, (2006) Reefs of the deep: The biology and geology of cold-water coral ecosystems. Science 312: 543-547.
8. Buhl-Mortensen L, Buhl-Mortensen P, (2004) Symbiosis in deep-water corals. Symbiosis 37: 33-61.
9. Roberts JM, Wheeler A, Freiwald A, Crains S, editors (2009) Cold-Water Corals, The Biology and Geology of Deep-Sea Coral Habitats: Cambridge University Press.
10. van Oevelen D, Duineveld G, Lavaleye M, Mienis F, Soetaert K, et al. (2009) The cold-water coral community as a hot spot for carbon cycling on continental margins: A food-web analysis from Rockall Bank (northeast Atlantic). Limnology and Oceanography 54: 1829-1844.
11. Buhl-Mortensen P, Fosså JH (2006) Species diversity and spatial distribution of invertebrates on deep-water Lophelia reefs in Norway. Proceedings of the 10th International Coral Reef Symposium. pp.1849-1868.
12. Wilson JB, (1979) Distribution of the coral Lopehlia pertusa (L) L. prolifera (Pallas) in the Northeast Atlantic. Journal of the Marine Biological Association of the United Kingdom 59: 149-164.
13. Zibrowius SES, Day JH, (1975) New observation on a little-known species of Lumbrineris (Polychaeta) living on various cnidarians, with notes on its recent and fossil scleractinian hosts. Journal of the Marine Biological Association of the United Kingdom 55: 83-114.
14. Winsnes IM, (1989) Eunicid polychaetes (Annelida) from the scandinavian and adjacent waters: Family Eunicidae Zoologica Scripta. 18: 483-500.
15. Buhl-Mortensen P, (2001) Aquarium observations on the deep-water coral Lophelia pertusa (L., 1758) (scleractinia) and selected associated invertebrates. Ophelia 54: 83-104.
16. Roberts JM, (2005) Reef-aggregating behaviour by symbiotic eunicid polychaetes from cold-water corals: do worms assemble reefs? Journal of the Marine Biological Association of the United Kingdom 85: 813-819.
17. De Bary A (1879) Die Erscheinung der Symbiose: Verlag von Karl J. Trübner.
18. Paracer S, Ahmadjian V, editors (2000) Symbiosis: an Introduction to Biological Associations. 2nd ed. New York: Oxford University Press.
19. Dales RP (1957) Interactions of organism. a. Commensalism; Hedgepeth J, editor. New York: Geological Society of America.
20. Addicott JF (1984) Mutualistic interactions in population and community processes; Price PW, Slobodchikoff, C. N., Gaud, W. S., editor. New York: Willey.
21. Martin D, Britayev TA, (1988) Symbiotic Polychaetes: Review of known species. Oceanography and Marine Biology Annual Review 36: 217-340.
22. Stachowicz JJ, (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51: 235-246.
23. Dodds LA, Black KD, Orr H, Roberts JM, (2009) Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Marine Ecology-Progress Series 397: 113-124.
24. Duineveld GCA, Jeffreys RM, Lavaleye MSS, Davies AJ, Bergman MJN, et al. (2012) Spatial and tidal variation in food supply to shallow cold-water coral reefs of the Mingulay Reef complex (Outer Hebrides, Scotland). Marine Ecology-Progress Series 444: 97-115.
25. Duineveld GCA, Lavaleye MSS, Berghuis EM, (2004) Particle flux and food supply to a seamount cold-water coral community (Galicia Bank, NW Spain). Marine Ecology-Progress Series 277: 13-23.
26. Furla P, Galgani I, Durand I, Allemand D, (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. Journal of Experimental Biology 203: 3445-3457.
27. Lavaleye M, Duineveld G, Lundälv T, White M, Guihen D, et al. (2009) Cold-Water Corals on the Tisler Reef- preliminary observations on the dynamic reef environment. Oceanography 22: 76-84.
28. Wagner H, Purser A, Thomsen L, Jesus CC, Lundälv T, (2011) Particulate organic matter fluxes and hydrodynamics at the Tisler cold-water coral reef. Journal of Marine Systems 85: 19-29.
29. Duineveld GCA, Lavaleye MSS, Bergman MIN, De Stigter H, Mienis F, (2007) Trophic structure of a cold-water coral mound community (Rockall Bank, NE Atlantic) in relation to the near-bottom particle supply and current regime. Bulletin of Marine Science 81: 449-467.
30. Kiriakoulakis K, Fisher E, Wolff GA, Freiwald A, Grehan A, et al. (2005) Lipids and nitrogen isotopes of two deep-water corals from the North-East Atlantic: initial results and implications for their nutrition; Freiwald ARJM, editor. 715-729 p.
31. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH, editors. Culture of Marine Invertebrate Animals. New York: Plenum Press. pp.26-60.
32. Naumann MS, Orejas C, Wild C, Ferrier-Pagès C, (2011) First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral. Journal of Experimental Biology 214: 3570-3576.
33. Purser A, Larsson AI, Thomsen L, van Oevelen D, (2010) The influence of flow velocity and food concentration on Lophelia pertusa (Scleractinia) zooplankton capture rates. Journal of Experimental Marine Biology and Ecology 395: 55-62.
34. Tsounis G, Orejas C, Reynaud S, Gili JM, Allemand D, et al. (2010) Prey-capture rates in four Mediterranean cold water corals. Marine Ecology-Progress Series 398: 149-155.
35. de Goeij JM, Moodley L, Houtekamer M, Carballeira NM, van Duyl FC, (2008) Tracing C-13-enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge Halisarca caerulea: Evidence for DOM feeding. Limnology and Oceanography 53: 1376-1386.
36. Moodley L, Boschker HTS, Middelburg JJ, Pel R, Herman PMJ, et al. (2000) Ecological significance of benthic foraminifera: C-13 labelling experiments. Marine Ecology-Progress Series 202: 289-295.
37. Gontikaki E, Mayor DJ, Thornton B, Black K, Witte U, (2011) Processing of C-13-labelled diatoms by a bathyal community at sub-zero temperatures. Marine Ecology-Progress Series 421: 39-50.
38. Allemand D, Tambutté E, Girard JP, Jaubert J, (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: Role in biomineralization and potential target of the organotin tributyltin. Journal of Experimental Biology 201: 2001-2009.
39. Adkins JF, Boyle EA, Curry WB, Lutringer A, (2003) Stable isotopes in deep-sea corals and a new mechanism for "vital effects". Geochimica Et Cosmochimica Acta 67: 1129-1143.
40. Tambutté E, Allemand D, Bourge I, Gattuso JP, Jaubert J, (1995) An improves 45 Ca protocol for investigating physiological meachnism in coral calcification Marine Biology. 122: 453-459.
41. Maier C, Hegeman J, Weinbauer MG, Gattuso JP, (2009) Calcification of the cold-water coral Lophelia pertusa under ambient and reduced pH. Biogeosciences 6: 1671-1680.
42. Miyajima T, Yamada Y, Hanba YT, Yoshii K, Koitabashi T, et al. (1995) Determining the stable isotope ratio of total dissolved inorganic carbon in lake water by GC/C/IRMS. Limnology and Oceanography 40: 994-1000.
43. Anderson MJ (2005) User guide of the computer program PERMANOVA for permutational multivariate analysis of variance. Department of Statistics, University of Auckland.
44. Shimeta J, Jumars PA, (1991) Physical mechanisms and rates of particle capture by suspension feeders. Oceanography and Marine Biology 29: 191-257.
45. Shimeta J, Koehl MAR, (1997) Mechanisms of particle selection by tentaculate suspension feeders during encounter, retention, and handling. Journal of Experimental Marine Biology and Ecology 209: 47-73.
46. Sanderson S, Stebar M, Ackermann K, Jones S, Batjakas II, et al. (1996) Mucus entrapment of particles by suspension-feeding Tilapia (Pisces: Cichlidae). Journal of Experimental Biology 199: 1743-1756.
47. Naumann MS, Richter C, el-Zibdah M, Wild C, (2009) Coral mucus as an efficient trap for picoplanktonic cyanobacteria: implications for pelagic-benthic coupling in the reef ecosystem. Marine Ecology-Progress Series 385: 65-76.
48. Herndl GJ, Velimirov B, Krauss RE, (1985) Heterotrophic nutrition and control of bacterial density in the coelenteron of the giant sea anemone Stoichactis giganteum. Marine Ecology-Progress Series 22: 101-105.
49. Lewis JB, Price WS, (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. Journal of Zoology 176: 527-544.
50. Form AU, Riebesell U, (2012) Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Global Change Biology 18: 843-853.
51. Maier C, Watremez P, Taviani M, Weinbauer MG, Gattuso JP, (2012) Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals. Proceedings of the Royal Society B-Biological Sciences 279: 1716-1723.
52. Dodds LA, Roberts JM, Taylor AC, Marubini F, (2007) Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. Journal of Experimental Marine Biology and Ecology 349: 205-214.
53. Bergsma GS, Martinez CM, (2011) Mutualist-induced morphological changes enhance growth and survival of corals. Marine Biology 158: 2267-2277.
54. Gochfeld DJ, (2010) Territorial damselfishes facilitate survival of corals by providing an associational defense against predators. Marine Ecology-Progress Series 398: 137-148.
55. Suttle KB, Thomsen MA, Power ME, (2007) Species interactions reverse grassland responses to changing climate. Science 315: 640-642.
56. Osinga R, Schutter M, Griffioen B, Wijffels RH, Verreth JAJ, et al. (2011) The Biology and Economics of Coral Growth. Marine Biotechnology 13: 658-671.
57. Patton WK (1967) Studies on Domecia acanthophora, a commensal crab from Puerto Rico, with particular reference to modifications of the coral host and feeding habits. Biological Bulletin 132: 56-&.
58. Rinkevich B, Loya Y, (1985) Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66: 100-105.