Advertisement

Coral Food, Feeding, Nutrition, and Secretion: A Review

  • Walter M. Goldberg
Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 65)

Abstract

Tropical scleractinian corals are dependent to varying degrees on their photosymbiotic partners. Under normal levels of temperature and irradiance, they can provide most, but not all, of the host’s nutritional requirements. Heterotrophy is required to adequately supply critical nutrients, especially nitrogen and phosphorus. Scleractinian corals are known as mesozooplankton predators, and most employ tentacle capture. The ability to trap nano- and picoplankton has been demonstrated by several coral species and appears to fulfill a substantial proportion of their daily metabolic requirements. The mechanism of capture likely involves mucociliary activity or extracoelenteric digestion, but the relative contribution of these avenues have not been evaluated. Many corals employ mesenterial filaments to procure food in various forms, but the functional morphology and chemical activities of these structures have been poorly documented. Corals are capable of acquiring nutrition from particulate and dissolved organic matter, although the degree of reliance on these sources generally has not been established. Corals, including tropical, deep- and cold-water species, are known as a major source of carbon and other nutrients for benthic communities through the secretion of mucus, despite wide variation in chemical composition. Mucus is cycled through the planktonic microbial loop, the benthos, and the microbial community within the sediments. The consensus indicates that the dissolved organic fraction of mucus usually exceeds the insoluble portion, and both serve as sources for the growth of nano- and picoplankton. As many corals employ mucus to trap food, a portion is taken back during feeding. The net gain or loss has not been evaluated, although production is generally thought to exceed consumption. The same is true for the net uptake and loss of dissolved organic matter by mucus secretion. Octocorals are thought not to employ mucus capture or mesenterial filaments during feeding and generally rely on tentacular filtration of weakly swimming mesozooplankton, particulates, dissolved organic matter, and picoplankton. Nonsymbiotic species in the tropics favor phytoplankton and weakly swimming zooplankton. Azooxanthellate soft corals are opportunistic feeders and shift their diet according to the season from phyto- and nanoplankton in summer to primarily particulate organic matter (POM) in winter. Cold-water species favor POM, phytodetritus, microplankton, and larger zooplankton when available. Antipatharians apparently feed on mesozooplankton but also use mucus nets, possibly for capture of POM. Feeding modes in this group are poorly known.

Keywords

Mesoplankton Microplankton Nanoplankton Picoplankton Microbial loop Dissolved and particulate organic carbon Nitrogen Phosphorus Mucus secretion Tentacle capture Mesenterial filaments Tropical Temperate and polar scleractinians Octocorals Antipatharians 

References

  1. Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alldredge A, Carlson C, Carpenter R (2013) Sources of organic carbon to coral reef flats. Oceanography 26:108–113CrossRefGoogle Scholar
  3. Allers E, Niesner C, Wild C, Pernthaler J (2008) Microbes enriched in seawater after addition of coral mucus. Appl Environ Microbiol 74:3274–3278PubMedPubMedCentralCrossRefGoogle Scholar
  4. Al-Moghrabi S, Allemand D, Couret JM, Jaubert J (1995) Fatty acids of the scleractinian coral Galaxea fascicularis: effect of light and feeding. J Comp Physiol B 165:183–192CrossRefGoogle Scholar
  5. Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Biol Ecol 232:85–106CrossRefGoogle Scholar
  6. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253PubMedCrossRefPubMedCentralGoogle Scholar
  7. Aylward FO, Boeuf D, Mende DR et al (2017) Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone. Proc Natl Acad Sci USA 114:11446–11451PubMedCrossRefPubMedCentralGoogle Scholar
  8. Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–792PubMedCrossRefPubMedCentralGoogle Scholar
  9. Azam F, Fenchel T, Field JG et al (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  10. Bachar A, Achituv Y, Pasternak Z, Dubinsky Z (2007) Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J Exp Mar Biol Ecol 349:295–298CrossRefGoogle Scholar
  11. Bak RPM, Joenje M, de Jong I et al (1998) Bacterial suspension feeding by coral reef benthic organisms. Mar Ecol Prog Ser 175:285–288CrossRefGoogle Scholar
  12. Baker DM, Freeman CJ, Wong JCY et al (2018) Climate change promotes parasitism in a coral symbiosis. ISME J 12(3):921–930.  https://doi.org/10.1038/s41396-018-0046-8CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bathmann UV, Scharek R, Klass C et al (1997) Spring development of phytoplankton biomass and composition in major water masses of the Atlantic sector of the Southern Ocean. Deep-Sea Res 44:51–57Google Scholar
  14. Battey JF, Patton JS (1984) A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar Biol 79:27–38CrossRefGoogle Scholar
  15. Baumann J, Grotolli AG, Hughes AD, Matsui Y (2014) Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. J Exp Mar Biol Ecol 461:469–478CrossRefGoogle Scholar
  16. Bednarz VN, Naumann MS, Niggl W, Wild C (2012) Inorganic nutrient availability affects organic matter fluxes and metabolic activity in the soft coral genus Xenia. J Exp Biol 215:3672–3679PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bednarz VN, Grover R, Maguer J-F et al (2017) The assimilation of diazotroph-derived nitrogen by scleractinian corals depends on their metabolic status. MBio 8(1):e02058-16 http://mbio.asm.org/content/8/1/e02058-16.fullPubMedPubMedCentralCrossRefGoogle Scholar
  18. Benavides M, Houlbrèque F, Camps M et al (2016) Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata. J Exp Biol 219:2608–2612PubMedCrossRefPubMedCentralGoogle Scholar
  19. Benavides M, Bednarz VN, Ferrier-Pagès C (2017) Diazotrophs: overlooked key players within the coral symbiosis and tropical reef ecosystems? Front Mar Sci 4(10).  https://doi.org/10.3389/fmars.2017.00010
  20. Benson AA, Muscatine L (1974) Wax in coral mucus: energy transfer from corals to reef fishes. Limnol Oceanogr 19:810–814CrossRefGoogle Scholar
  21. Bessell-Brown P, Fisher R, Duckworth A, Jones R (2017) Mucous sheet production in Porites: and effective bioindicator of sediment-related pressures. Ecol Indicators 77:276–285CrossRefGoogle Scholar
  22. Bo M, Tazoli S, Spano BG (2008) Antipathella subpinnata (Antipatharia, Myriopathidae) in Italian seas. Ital J Zool 75:185–195CrossRefGoogle Scholar
  23. Boschma H (1925) On the feeding reactions and digestion in the coral polyp Astrangia danæ, with notes on its symbiosis with zoöxanthellæ. Biol Bull 49:407–439CrossRefGoogle Scholar
  24. Bourne DG, Garren M, Work TM et al (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562PubMedCrossRefPubMedCentralGoogle Scholar
  25. Bourne DG, Morrow KM, Webster NS (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70:317–340PubMedCrossRefPubMedCentralGoogle Scholar
  26. Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448CrossRefGoogle Scholar
  27. Briand MJ, Bonnet X, Goiran C et al (2015) Major sources of organic matter in a complex coral reef lagoon: identification from isotopic signatures (δ13C and δ15N). PLoS One 10(7): e0131555. doi: https://doi.org/10.1371/journal.pone.0131555
  28. Brown BE, Blythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309CrossRefGoogle Scholar
  29. Browne NK, Precht E, Last K, Todd PA (2014) Photo-physiological costs associated with acute sediment stress events in three near-shore turbid water corals. Mar Ecol Prog Ser 502:129–143CrossRefGoogle Scholar
  30. Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477PubMedPubMedCentralCrossRefGoogle Scholar
  31. Bythell JC, Wild C (2011) Biology and ecology of coral mucus release. J Exp Mar Biol Ecol 408:88–93CrossRefGoogle Scholar
  32. Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 157:157–167CrossRefGoogle Scholar
  33. Cardini U, Bednarz VN, Foster RA et al (2014) Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol Evol 4:1706–1727PubMedPubMedCentralCrossRefGoogle Scholar
  34. Cardini U, Bednarz VN, Naumann MS et al (2015) Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc R Soc B 282:20152257.  https://doi.org/10.1098/rspb.2015.2257CrossRefPubMedPubMedCentralGoogle Scholar
  35. Carlier A, Le Guilloux E, Olu K et al (2009) Trophic relationships in a deep Mediterranean cold-water bank (Santa Maria di Leuca, Ionian Sea). Mar Ecol Prog Ser 397:125–137CrossRefGoogle Scholar
  36. Carlson CA, Hansell DA (2015) DOM sources, sinks, reactivity and budgets. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Elsevier, Amsterdam, pp 65–126CrossRefGoogle Scholar
  37. Carpenter FW (1910) Feeding reactions of the rose coral (Isophyllia). Proc Am Acad Arts Sci 46:149–162CrossRefGoogle Scholar
  38. Charpy L, Blanchot J (1999) Picophytoplankton biomass, community structure and productivity in the Great Astrolabe Lagoon, Fiji. Coral Reefs 18:255–262CrossRefGoogle Scholar
  39. Charpy-Roubaud C, Charpy L, Larkum AWD (2001) Atmospheric dinitrogen fixation by benthic communities of Tikehau lagoon (Tuamotu Archipelago, French Polynesia) and its contribution to benthic primary production. Mar Biol 139:991–997CrossRefGoogle Scholar
  40. Clayton WS, Lasker HR (1982) Effects of light and dark treatments on feeding by the reef coral Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 63:269–279CrossRefGoogle Scholar
  41. Cocito S, Ferrier-Pagès C, Cupido R et al (2013) Nutrient acquisition in four Mediterranean gorgonian species. Mar Ecol Prog Ser 473:179–188CrossRefGoogle Scholar
  42. Coddeville B, Maes E, Ferrier-Pagès C, Guerardel Y (2011) Glycan profiling of gel forming mucus layer from the scleractinian symbiotic coral Oculina arbuscula. Biomolecules 12:2064–2073Google Scholar
  43. Coffroth MA (1984) Ingestion and incorporation of coral mucus aggregates by a gorgonian soft coral. Mar Ecol Prog Ser 17:193–199CrossRefGoogle Scholar
  44. Coffroth MA (1990) Mucus sheet formation on poritid corals- an evaluation of mucus as a nutrient source on reefs. Mar Biol 105:39–49CrossRefGoogle Scholar
  45. Coma R, Gili J-M, Zabala M, Riera T (1994) Feeding and prey capture cycles in the aposymbiotic gorgonian Paramuricea clavata. Mar Ecol Prog Ser 155:257–270CrossRefGoogle Scholar
  46. Coma R, Ribes M, Gili JM, Zabala M (1998) An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Mar Ecol Prog Ser 162:89–103CrossRefGoogle Scholar
  47. Coma R, Ribes M, Gili J-M, Hughes RN (2001) The ultimate opportunists: consumers of seston. Mar Ecol Prog Ser 219:305–308CrossRefGoogle Scholar
  48. Cook PLM, Kessler AJ, Eyre BD (2017) Does denitrification occur within porous carbonate grains? Biogeosciences 14:4061–4069CrossRefGoogle Scholar
  49. Cooper TF, Lai M, Ulstrup KE et al (2011) Symbiodinium genotypic and environmental controls on lipids in reef building corals. PLoS One 6(5):e20434.  https://doi.org/10.1371/journal.pone.0020434CrossRefPubMedPubMedCentralGoogle Scholar
  50. Courtial L, Ferrier-Pagès C, Jacquet S et al (2017) Effects of temperature and UVR on organic matter fluxes and the metabolic activity of Acropora muricata. Biol Open 6:1190–1199PubMedPubMedCentralCrossRefGoogle Scholar
  51. Crandall JB, Teece MA (2012) Urea is a dynamic pool of available nitrogen on coral reefs. Coral Reefs 31:207–214CrossRefGoogle Scholar
  52. Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42CrossRefGoogle Scholar
  53. Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol 60:81–90CrossRefGoogle Scholar
  54. D’Elia CF (1977) The uptake and release of dissolved phosphorus by reef corals. Limnol Oceanogr 22:301–315CrossRefGoogle Scholar
  55. D’Elia CF, Domotor SL, Webb KL (1983) Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar Biol 75:157–167CrossRefGoogle Scholar
  56. Dai C-F, Lin M-C (1993) The effects of flow on feeding of three gorgonians from southern Taiwan. J Exp Mar Biol Ecol 173:57–69CrossRefGoogle Scholar
  57. Darwin C (1842) The structure and distribution of coral reefs. Smith, Elder and Co, London (Reprinted 1962, University of California Press)Google Scholar
  58. Davies PL (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2:181–186Google Scholar
  59. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–262PubMedPubMedCentralCrossRefGoogle Scholar
  60. de Goeij J, Van den Berg H, Van Oostveen M et al (2008) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357:139–151CrossRefGoogle Scholar
  61. den Haan J, Huisman J, Brocke HJ et al (2016) Nitrogen and phosphorous uptake rates from different species from a coral reef community after a nutrient pulse. Sci Rep 6:28821CrossRefGoogle Scholar
  62. Dodds LA, Black KD, Orr H, Roberts JM (2009) Lipid biomarkers reveal geographic differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar Ecol Progr Ser 397:113–124CrossRefGoogle Scholar
  63. Dubinsky Z, Jokiel PL (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324Google Scholar
  64. Ducklow HW, Mitchell R (1979) Composition of mucus released by reef coelenterates. Limnol Oceanogr 24:706–714CrossRefGoogle Scholar
  65. Duerden JE (1902) West Indian madreporarian polyps. Mem Natl Acad Sci 7:309–649Google Scholar
  66. Duerden JE (1906) The role of mucus in corals. Quart J Microsc Sci 49:591–614Google Scholar
  67. Duineveldt GCA, Jeffreys RM, Lavaleye MSS et al (2012) Mar Ecol Prog Ser 444:97–115CrossRefGoogle Scholar
  68. Edmunds PJ, Davies PS (1989) An energy budget for Porites porites (Scleractinia) growing in a stressed environment. Coral Reefs 8:37–43CrossRefGoogle Scholar
  69. Einbinder S, Mass T, Brokovich E et al (2009) Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar Ecol Prog Ser 381:167–174CrossRefGoogle Scholar
  70. Elias-Piera F, Rossi S, Gili J-M, Orejas C (2013) Trophic ecology of seven Antarctic gorgonian species. Mar Ecol Prog Ser 477:93–106CrossRefGoogle Scholar
  71. Erler BD, Santos IR, Eyre D (2014) Inorganic transformations within permeable carbonate sands. Cont Shelf Res 77:69–80CrossRefGoogle Scholar
  72. Eyal G, Wiedenmann J, Grinblat M et al (2015) Spectral diversity and regulation of coral fluorescence in a mesophotic reef habitat in the Red Sea. PLoS One 10(6):e0128697.  https://doi.org/10.1371/journal.pone.0128697CrossRefPubMedPubMedCentralGoogle Scholar
  73. Fabricius K, Alderslade P (2001) Soft corals and sea fans. Australian Institute of Maine Sciences, TownsvilleGoogle Scholar
  74. Fabricius KE, Dommisse M (2000) Depletion of suspended particulate matter over coastal reef communities dominated by zooxanthellate soft corals. Mar Ecol Prog Ser 196:157–167CrossRefGoogle Scholar
  75. Fabricius KE, Klumpp DW (1995) Widespread mixotrophy in reef-inhabiting soft corals: the influence of depth, and colony expansion and contraction on photosynthesis. Mar Ecol Prog Ser 125:195–204CrossRefGoogle Scholar
  76. Fabricius KE, Benayahu Y, Genin A (1995a) Herbivory in asymbiotic soft corals. Science 268:90–92PubMedCrossRefPubMedCentralGoogle Scholar
  77. Fabricius KE, Genin A, Benayahu Y (1995b) Flow-dependent herbivory and growth in a zooxanthellae-free soft coral. Limnol Oceanogr 40:1290–1301CrossRefGoogle Scholar
  78. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and energetics of a symbiotic coral. Bioscience 34:705–709CrossRefGoogle Scholar
  79. Fenchel T (1982) Ecology of heterotrophic microflagellates. 1. Some important forms and their functional morphology. Mar Ecol Prog Ser 8:211–223CrossRefGoogle Scholar
  80. Ferrier MD (1991) Net uptake of dissolved free amino acids by four scleractinian corals. Coral Reefs 10:183–187CrossRefGoogle Scholar
  81. Ferrier-Pagès C, Furla P (2001) Pico- and nanoplankton biomass and production in the two largest atoll lagoons of French Polynesia. Mar Ecol Prog Ser 211:63–76CrossRefGoogle Scholar
  82. Ferrier-Pagès C, Gattuso J-P (1998) Biomass, production and grazing rates of pico- and nanoplankton in coral reef waters (Miyako Island, Japan). Microb Ecol 35:46–57PubMedCrossRefPubMedCentralGoogle Scholar
  83. Ferrier-Pagès C, Gatusso J-P, Cauwet G et al (1998a) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274CrossRefGoogle Scholar
  84. Ferrier-Pagès C, Allemand D, Gattuso J-P et al (1998b) Microheterotrophy in the zooxanthellate coral Stylophora pistillata: effects of light and ciliate density. Limnol Oceanogr 43:1639–1648CrossRefGoogle Scholar
  85. Ferrier-Pagès C, Leclercq N, Jaubert J, Pelegri SP (2000) Enhancement of pico- and nanoplankton growth by coral exudates. Aquat Microb Ecol 21:203–209CrossRefGoogle Scholar
  86. Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240CrossRefGoogle Scholar
  87. Ferrier-Pagès C, Rottier C, Beraud E, Levy O (2010) Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol 390:118–124CrossRefGoogle Scholar
  88. Ferrier-Pagès C, Hoogenboom M, Houlbrèque F (2011a) The role of plankton in coral trophodynamics. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 215–229CrossRefGoogle Scholar
  89. Ferrier-Pagès C, Peirano A, Abbate M et al (2011b) Summer autotrophy in the temperate symbiotic coral Cladocora cespitosa. Limnol Oceanogr 56:1429–1438CrossRefGoogle Scholar
  90. Ferrier-Pagès C, Reynaud S, Beraud E et al (2015) Photophysiology and daily primary production of a temperate symbiotic gorgonian. Photosynth Res 123:95–1204PubMedCrossRefPubMedCentralGoogle Scholar
  91. Ferrier-Pagès C, Godinot C, D’Angelo C (2016) Phosphorus metabolism of reef organisms with algal symbionts. Ecol Monogr 86:262–277CrossRefGoogle Scholar
  92. Fonvielle JA, Reynaud S, Jaquet S et al (2015) First evidence of an important organic matter trophic pathway between temperate corals and pelagic microbial communities. PLoS One 10(10):e0139175.  https://doi.org/10.1371/journal.pone.0139175CrossRefPubMedPubMedCentralGoogle Scholar
  93. Frazão B, Vasconcelos V, Antunes A (2012) Sea anemone (Cnidaria, Anthozoa, Actiniaria) toxins: an overview. Mar Drugs 10(8):1812–1851.  https://doi.org/10.3390/md10081812CrossRefPubMedPubMedCentralGoogle Scholar
  94. Furnas MJ, Mitchell AW (1986) Phytoplankton dynamics in the central Great Barrier Reef-I. Seasonal changes in biomass and community structure and their relation to intrusive activity. Cont Shelf Res 6:363–384CrossRefGoogle Scholar
  95. Garren M, Azam F (2011) New directions in coral reef microbial ecology. Environ Microbiol 14:833–844PubMedCrossRefPubMedCentralGoogle Scholar
  96. Gattuso J-P, Yellowlees D, Lesser M (1993) Depth- and light-dependent variation of carbon partitioning and utilization in the zooxanthellate coral Stylophora pistillata. Mar Ecol Prog Ser 92:267–276CrossRefGoogle Scholar
  97. Genin A, Monismith SG, Reidenbach MA et al (2009) Intense benthic grazing of phytoplankton in a coral reef. Limnol Oceanogr 54:938–951CrossRefGoogle Scholar
  98. Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:2280–2292PubMedPubMedCentralCrossRefGoogle Scholar
  99. Godinot C, Ferrier-Pagès C, Grover R (2009) Control of phosphate uptake by zooxanthellae and host cells in the scleractinian coral Stylophora pistilata. Limnol Oceanogr 54:1627–1633CrossRefGoogle Scholar
  100. Godinot C, Grover R, Allemand D, Ferrier-Pagès C (2011) High phosphate uptake requirements of the scleractinian coral Stylophora pistillata. J Exp Biol 214:2749–2754PubMedCrossRefPubMedCentralGoogle Scholar
  101. Godinot C, Gaysinki M, Thomas OP et al (2016) On the use of 31P NMR for the quantification of hydrosoluble phosphorous-containing compounds in coral host tissues and cultured zooxanthellae. Sci Rep 6:21760PubMedPubMedCentralCrossRefGoogle Scholar
  102. Goldberg WM (2002a) Feeding behavior, epidermal structure and mucus cytochemistry of the scleractinian Mycetophyllia reesi, a coral without tentacles. Tissue Cell 24:232–245CrossRefGoogle Scholar
  103. Goldberg WM (2002b) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral without tentacles. Tissue Cell 34:246–261PubMedCrossRefPubMedCentralGoogle Scholar
  104. Goldberg WM (2004) Epidermal structure of the scleractinian coral Mycetophyllia ferox: light-induced vesicles, copious mucocytes, and sporadic tentacles. Hydrobiologia 530:451–458Google Scholar
  105. Goldberg WM, Taylor GT (1989a) Cellular structure and ultrastructure of the black coral Antipathes aperta: 1. Organization of the tentacular epidermis and nervous system. J Morphol 202:239–253PubMedCrossRefPubMedCentralGoogle Scholar
  106. Goldberg WM, Taylor GT (1989b) Cellular structure and ultrastructure of the black coral Antipathes aperta: 2. The gastrodermis and its collar cells. J Morphol 202:255–269PubMedCrossRefPubMedCentralGoogle Scholar
  107. Goldberg WM, Taylor GT (1996) Ultrastructure of the spirocyst tubule in black corals (Coelenterata: Antipatharia) and its taxonomic implications. Mar Biol 125:655–662CrossRefGoogle Scholar
  108. Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260CrossRefGoogle Scholar
  109. Gori A, Grover R, Orejas C et al (2014) Uptake of dissolved free amino acids by four cold-water coral species from the Mediterranean Sea. Deep Sea Res 99:42–50CrossRefGoogle Scholar
  110. Gottfried M, Roman MR (1983) Ingestion and incorporation of coral-mucus detritus by zooplankton. Mar Biol 72:211–218CrossRefGoogle Scholar
  111. Granek EF, Compton JE, Phillips DL (2009) Mangrove-exported nutrient incorporation by sessile coral reef invertebrates. Ecosystems 12:462–472CrossRefGoogle Scholar
  112. Grossowicz M, Benayahu Y (2012) Differential morphological features of two Dendronepthya soft coral species suggest differences in feeding niches. Mar Biodiv 42:65–72CrossRefGoogle Scholar
  113. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Montipora verrucosa and Porites compressa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  114. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefPubMedCentralGoogle Scholar
  115. Grover R, Maguer J-F, Reynard-Vaganay S, Ferrier-Pagès C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790CrossRefGoogle Scholar
  116. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C (2003) Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–2274CrossRefGoogle Scholar
  117. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 332:216–225CrossRefGoogle Scholar
  118. Grover R, Maguer JF, Allemand D, Ferrier-Pagès C (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865PubMedCrossRefPubMedCentralGoogle Scholar
  119. Grover R, Ferrier-Pagès C, Maguer J-F et al (2014) Nitrogen fixation in the mucus of Red Sea corals. J Exp Biol 217:3962–3963PubMedCrossRefPubMedCentralGoogle Scholar
  120. Gustafsson MSM, Baird ME, Ralph PJ (2013) The interchangeability of autotrophic and heterotrophic nitrogen sources in scleractinian coral symbiotic relationships: a numerical study. Ecol Model 250:183–194CrossRefGoogle Scholar
  121. Haas AF, Wild C (2010) Composition analysis of organic matter released by cosmopolitan coral reef-associated green algae. Aquat Biol 10:131–138CrossRefGoogle Scholar
  122. Haas AF, Naumann MS, Struck U et al (2010) Organic matter release by coral reef associated benthic algae in the northern Red Sea. J Exp Mar Biol Ecol 389:53–60CrossRefGoogle Scholar
  123. Haas AF, Nelson CE, Wegley Kelly L et al (2011) Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity. PLoS One 6:e27973PubMedPubMedCentralCrossRefGoogle Scholar
  124. Hanson CE, McLaughlin MJ, Hyndes GA, Strzelecki J (2009) Selective uptake of prokaryotic picoplankton by a marine sponge (Callyspongia sp.) within an oligotrophic coastal system. Estuar Coast Shelf Sci 84:289–297CrossRefGoogle Scholar
  125. Hata H, Setsuko K, Yamano H et al (2002) Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Mar Ecol Prog Ser 232:129–140CrossRefGoogle Scholar
  126. Hatcher BG (1988) Coral reef primary productivity: a beggar’s banquet. Trends Ecol Evol 3:106–111PubMedCrossRefPubMedCentralGoogle Scholar
  127. Hatcher BG (1990) Coral reef primary productivity. A hierarchy of pattern and process. Trends Ecol Evol 5:149–155PubMedCrossRefPubMedCentralGoogle Scholar
  128. Heck KL, Carruthers TJB, Duarte CM et al (2008) Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial communities. Ecosystems 11:1198–1210CrossRefGoogle Scholar
  129. Heidelberg KB, Sebens KP, Purcell JE (2004) Composition and sources of near-reef zooplankton on a Jamaican reef along with implications for coral feeding. Coral Reefs 23:263–276CrossRefGoogle Scholar
  130. Hessinger DA (1988) Nematocyst venoms and toxins. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 333–368CrossRefGoogle Scholar
  131. Hii Y-S, Soo C, Liew H (2009) Feeding of scleractinian coral, Galaxea fascicularis, on Artemia salina nauplii in captivity. Aquacult Int 17:363–376CrossRefGoogle Scholar
  132. Hoer DR, Gibson PJ, Tommerdahl JP et al (2018) Consumption of dissolved organic carbon by Caribbean reef sponges. Limnol Oceanogr 63:337–351CrossRefGoogle Scholar
  133. Hoogenboom M, Rodolfo-Metalpa R, Ferrier-Pagès C (2010) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J Exp Biol 213:2399–2409PubMedCrossRefPubMedCentralGoogle Scholar
  134. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17PubMedCrossRefPubMedCentralGoogle Scholar
  135. Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C (2004a) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469PubMedCrossRefPubMedCentralGoogle Scholar
  136. Houlbrèque F, Tambutté E, Richard C, Ferrier-Pagès C (2004b) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282:151–160CrossRefGoogle Scholar
  137. Houlbrèque F, Delesalle B, Blanchot J et al (2006) Picoplankton removal by the coral reef community of La Prévoyante, Mayotte Island. Aquat Microb Ecol 44:59–70CrossRefGoogle Scholar
  138. Huettel M, Wild C, Gonelli S (2006) Mucus trap in coral reefs: formation and temporal evolution of particle aggregates caused by coral mucus. Mar Ecol Prog Ser 307:69–84CrossRefGoogle Scholar
  139. Hughes AD, Grottoli AG (2013) Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS One 8:e81172PubMedPubMedCentralCrossRefGoogle Scholar
  140. Imbs AB, Yakovleva IM (2012) Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 31:41–53CrossRefGoogle Scholar
  141. Imbs AB, Latyshev NA, Dautova TN (2010) Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser 409:65–75CrossRefGoogle Scholar
  142. Imbs AB, Demidkpva DA, Dautova TN (2016) Lipids and fatty acids of cold-water soft corals and hydrocorals: a comparison with tropical species and implications for coral nutrition. Mar Biol 163:202–213CrossRefGoogle Scholar
  143. Jackson AE, Yellowlees D (1990) Phosphate uptake by zooxanthellae isolated from corals. Proc R Soc B 242:201–204CrossRefGoogle Scholar
  144. Jacobi Y, Yahel G, Shenkar N (2017) Efficient filtration of micron and submicron particles by ascidians from oligotrophic waters. Limnol Oceanogr.  https://doi.org/10.1002/lno.10736
  145. Jaffé R, Boyer JN, Lu X et al (2004) Source characterization of dissolved organic matter in a subtropical mangrove-dominated estuary by fluorescence analysis. Mar Chem 84:195–210CrossRefGoogle Scholar
  146. Jatkar AA, Brown BE, Bythell JC et al (2010) Coral mucus: the properties of its constituent mucins. Biomacromolecules 11:883–888PubMedCrossRefPubMedCentralGoogle Scholar
  147. Johnson AS, Sebens KP (1993) Consequences of a flattened morphology: effects of flow on feeding rates of the scleractinian coral Meandrina meandrites. Mar Ecol Prog Ser 99:99–114CrossRefGoogle Scholar
  148. Jouiaei M, Yanagihara AA, Madio B et al (2015) Ancient venom systems: a review on Cnidaria toxins. Toxins 7:2251–2271PubMedPubMedCentralCrossRefGoogle Scholar
  149. Karl DM, Björkman KM (2015) Dynamics of dissolved organic phosphorus. In: Hansell DA, Carlson CA (eds) Dynamics of dissolved marine organic matter. Academic Press, Burlington, pp 233–334Google Scholar
  150. Kellogg CA (2004) Tropical archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88CrossRefGoogle Scholar
  151. Kopp C, Pernice M, Domart-Coulon I et al (2013) Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. MBio 4:1–9CrossRefGoogle Scholar
  152. Kremien M, Shavit U, Mass T, Genin A (2013) Benefit of pulsation in soft corals. Proc Natl Acad Sci USA 110:8978–8983PubMedCrossRefPubMedCentralGoogle Scholar
  153. Krupp DA (1984) Mucus production by corals exposed during an extreme low tide. Pac Sci 38:1–11Google Scholar
  154. LaBarbara ML (1984) Feeding currents and particle capture mechanisms in suspension feeding animals. Am Zool 24:71–84CrossRefGoogle Scholar
  155. Lang JC (1973) Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull Mar Sci 23:260–279Google Scholar
  156. Lang JC, Chornesky EA (1990) Competition between scleractinian reef corals-a review of mechanisms and effects. In: Dubinsky D (ed) Ecosystems of the world. Coral reefs, vol 25. Elsevier, Amsterdam, pp 209–252Google Scholar
  157. Lasker HR (1981) A comparison of the particulate feeding abilities of three species of gorgonian soft coral. Mar Ecol Prog Ser 5:61–67CrossRefGoogle Scholar
  158. Lasker HR, Gottfried MD, Coffroth MA (1983) Effects of depth on feeding capabilities of two octocorals. Mar Biol 73:73–78CrossRefGoogle Scholar
  159. Laybourn-Parry JEM, Parry JD (2000) Flagellates and the microbial loop. In: Leadbeater SC, Green JC (eds) The flagellates, unity, diversity and evolution. Taylor and Francis, London, pp 216–239Google Scholar
  160. Leal MC, Ferrier-Pagès C, Calado R et al (2014a) Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar Ecol Prog Ser 504:171–179CrossRefGoogle Scholar
  161. Leal MC, Berger SA, Ferrier-Pagès C et al (2014b) Temporal changes in the tropic ecology of the asymbiotic gorgonian Leptogorgia virgulata. Mar Biol 161:2191–2197CrossRefGoogle Scholar
  162. Lee C, Wakeham S, Arnosti C (2004) Particulate organic matter in the sea: the composition conundrum. Ambio 33:565–575PubMedCrossRefPubMedCentralGoogle Scholar
  163. Lee STM, Davy SK, Tang S-L et al (2015) Successive shifts in the microbial community of the surface mucus layer and tissues of the coral Acropora muricata under thermal stress. FEMS Microbiol Ecol 91:fiv142.  https://doi.org/10.1093/femsec/fiv142CrossRefPubMedPubMedCentralGoogle Scholar
  164. Lee STM, Davy SK, Tang S-L, Kench PS (2016) Mucus sugar content shapes the bacterial community structure in thermally stressed Acropora muricata. Front Microbiol 7:371.  https://doi.org/10.3389/fmicb.2016.00371CrossRefPubMedPubMedCentralGoogle Scholar
  165. Legendre L, Demers S, Delesalle B, Harnols C (1988) Biomass and phototrophic picoplankton in coral reef waters (Moorea, French Polynesia). Mar Ecol Prog Ser 47:153–160CrossRefGoogle Scholar
  166. Léger P, Bengtson DA, Sorgeloos P et al (1987) The nutritional value of Artemia: a review. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (eds) The brine shrimp Artemia. Ecology, culturing, use in aquaculture, vol 3. Universa Press, Wetteren, pp 357–372Google Scholar
  167. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000PubMedCrossRefPubMedCentralGoogle Scholar
  168. Lesser MP, Falcón LI, Rodriguez-Román A et al (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152CrossRefGoogle Scholar
  169. Lesser MP, Slattery M Stat M et al (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003PubMedCrossRefPubMedCentralGoogle Scholar
  170. Levy O, Mizrahi L, Chadwick-Furman NE, Achituv Y (2000) Factors controlling the expansion behavior of Favia favus (Cnidaria:Scleractinia): effects of light, flow, and planktonic prey. Biol Bull 200:118–126CrossRefGoogle Scholar
  171. Levy O, Dubinsky Z, Achituv Y (2003) Photobehavior of stony corals: responses to light spectra and intensity. J Exp Biol 206:4041–4049PubMedCrossRefPubMedCentralGoogle Scholar
  172. Levy O, Karako-Lampert S, Ben-Asher HW et al (2016) Molecular assessment of the effect of light and heterotrophy in the scleractinian coral Stylophora pistillata. Proc R Soc B 283:20153025PubMedCrossRefGoogle Scholar
  173. Lewis JB (1978) Feeding mechanisms in black corals (Antipatharia). J Zool 186:393–396CrossRefGoogle Scholar
  174. Lewis JB (1982) Feeding behavior and feeding ecology of the Octocorallia (Coelenterata: Anthozoa). J Zool 196:371–384CrossRefGoogle Scholar
  175. Lewis JB, Price WS (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. J Zool 176:527–544CrossRefGoogle Scholar
  176. Lewis JB, Price WS (1976) Patterns of ciliary currents in Atlantic reef corals and their functional significance. J Zool 178:77–89CrossRefGoogle Scholar
  177. Lomas MW, Burke AL, Bell DW et al (2010) Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus. Biogeosciences 7:695–710CrossRefGoogle Scholar
  178. Longhurst A, Pauly D (1987) Ecology of tropical oceans. Academic Press, San DiegoGoogle Scholar
  179. Lorrain A, Houlbrèque F, Benzoni F et al (2017) Seabirds supply nitrogen to reef-building corals on remote Pacific islets. Sci Rep 7:3721.  https://doi.org/10.1038/s41598-017-03781-yCrossRefPubMedPubMedCentralGoogle Scholar
  180. Mariscal RN (1984) Cnidae. In: Bereiter-Hahn J, Matolsky AG, Richards KS (eds) Biology of the integument. Springer, Berlin, pp 57–111CrossRefGoogle Scholar
  181. Mariscal RN, Bigger CH (1977) Possible ecological significance of octocoral epithelia1 ultrastructure. Proc 3rd Intl Coral Reef Symp Miami 1:127–134Google Scholar
  182. Mariscal RN, Lenhoff HM (1968) The chemical control of feeding behavior in Cyphastrea ocellina and in some other Hawaiian corals. J Exp Biol 49:689–699PubMedPubMedCentralGoogle Scholar
  183. Mariscal RN, McLean RB, Hand C (1977) The form and function of cnidarian spirocysts. 3. Ultrastructure of the thread and the function of spirocysts. Cell Tissue Res 178:427–433PubMedCrossRefPubMedCentralGoogle Scholar
  184. Marshall AT, Wright OP (1993) Confocal laser scanning light microscopy of the extra-thecal epithelia of undecalcified scleractinian corals. Cell Tissue Res 272:533–543CrossRefGoogle Scholar
  185. Martin W, Scheibe R, Schnarrenberger C (2000) The Calvin cycle and its regulation. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis. Advances in photosynthesis and respiration, vol 9. Springer, Dordrecht, pp 9–51Google Scholar
  186. Matthai G (1918) On reactions to stimuli in corals. Proc Camb Philos Soc 19:164–162Google Scholar
  187. Mayer FW, Wild C (2010) Coral Mucus release and following particle trapping contribute to rapid nutrient recycling in a northern Red Sea fringing reef. Mar Freshw Res 61:1006–1014CrossRefGoogle Scholar
  188. McKew BA, Dumbrell AJ, Daud SD et al (2012) Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 84:5229–5237CrossRefGoogle Scholar
  189. McMurray SE, Johnson ZI, Hunt DE et al (2016) Selective feeding by the giant barrel sponge enhances foraging efficiency. Limnol Oceanogr 61:1271–1286CrossRefGoogle Scholar
  190. Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from six species of coral. Mar Biol 99:187–193CrossRefGoogle Scholar
  191. Meyer JL, Schultz ET (1985) Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156CrossRefGoogle Scholar
  192. Middleburg JJ, Mueller CE, Veuger B et al (2015) Discovery of symbiotic nitrogen fixation and chemoautotrophy in cold-water corals. Sci Rep 5:17962.  https://doi.org/10.1038/srep17962CrossRefGoogle Scholar
  193. Migne A, Davoult D (2002) Experimental nutrition in the soft coral Alcyonium digitatum (Cnidaria: Octocorallia): removal rate of phytoplankton and zooplankton. Cah Biol Mar 43:9–16Google Scholar
  194. Mills MM, Sebens KP (2004) Ingestion and assimilation of nitrogen from benthic sediments by three species of coral. Mar Biol 145:1097–1106CrossRefGoogle Scholar
  195. Mills MM, Lipschultz F, Sebens KP (2004a) Particulate matter ingestion and associated nitrogen uptake by four species of scleractinian corals. Coral Reefs 23:311–323CrossRefGoogle Scholar
  196. Mills MM, Ridame C, Dave M (2004b) Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292–294PubMedCrossRefPubMedCentralGoogle Scholar
  197. Møller EF, Thjor P, Nielsen TG (2003) Production of DOC by Calanis finmarchicus, C. glacialis and C. hyperboeus through sloppy feeding and leakage from fecal pellets. Mar Ecol Prog Ser 262:185–191CrossRefGoogle Scholar
  198. Moran Y, Genikhovich G, Gordon D et al (2012) Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones. Proc Biol Sci 279:1351–1358PubMedCrossRefPubMedCentralGoogle Scholar
  199. Mortensen PB (2001) Aquarium observations on the deep-water coral Lophelia pertusa (L., 1758) (Scleractinia) and selected associated invertebrates. Ophelia 54:83–104CrossRefGoogle Scholar
  200. Mueller CE, Larsson AI, Veuger B et al (2014a) Opportunistic feeding on various organic food sources by the cold-water coral Lophelia pertusa. Biogeosciences 11:123–133CrossRefGoogle Scholar
  201. Mueller B, van der Zande RM, van Leent PJM et al (2014b) Effect of light availability on dissolved organic carbon release by Caribbean reef algae and corals. Bull Mar Sci 90:875–893CrossRefGoogle Scholar
  202. Mueller B, de Goeij JM, Vermeij MJA et al (2014c) Natural diet of coral-excavating sponges consists mainly of dissolved organic carbon (DOC). PLoS One 9(2):e90152PubMedPubMedCentralCrossRefGoogle Scholar
  203. Muscatine L (1973) Nutrition of corals. In: Jones OS, Endean R (eds) Biology and geology of coral reefs, vol 2., Biology. Academic Press, New York, pp 77–116CrossRefGoogle Scholar
  204. Muscatine L, D’Elia CF (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734CrossRefGoogle Scholar
  205. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbiosis adapted to nutrient-poor environments. BioScience 27:454–459CrossRefGoogle Scholar
  206. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  207. Muscatine L, Falkowski PG, Porter JW et al (1984) Fate of photosynthetic fixed carbon in light-and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc B Biol Sci 222:181–202CrossRefGoogle Scholar
  208. Muscatine L, Falkowski PG, Dubinsky Z et al (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc B 236:311–324CrossRefGoogle Scholar
  209. Nakajima R, Yoshida T, Azman BAR et al (2009) In situ release of coral mucus by Acropora and its influence on the heterotrophic bacteria. Aquat Ecol 43:815–823CrossRefGoogle Scholar
  210. Nakajima R, Yoshida T, Fujita K et al (2010) Release of particulate and dissolved organic carbon by the scleractinian coral Acropora formosa. Bull Mar Sci 86:861–870CrossRefGoogle Scholar
  211. Nakajima R, Tanaka Y, Yoshida T et al (2015) High inorganic phosphate concentration in coral mucus and its utilization by heterotrophic bacteria in a Malaysian coral reef. Mar Ecol 36:835–841CrossRefGoogle Scholar
  212. Nakajima R, Yamazaki H, Lewis LS et al (2017a) Planktonic trophic structure in a coral reef ecosystem—grazing versus microbial food webs and the production of mesozooplankton. Progr Oceanogr 156:104–120CrossRefGoogle Scholar
  213. Nakajima R, Tanaka Y, Guillemette R, Kurihara H (2017b) Effects of coral-derived organic matter on the growth of bacterioplankton and heterotrophic nanoflagellates. Coral Reefs 36:1171–1179CrossRefGoogle Scholar
  214. 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. Mar Ecol Prog Ser 385:65–76CrossRefGoogle Scholar
  215. Naumann MS, Haas A, Struck U et al (2010) Organic matter release by dominant hermatypic corals of the northern Red Sea. Coral Reefs 29:649–659CrossRefGoogle Scholar
  216. 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. J Exp Biol 214:3570–3576PubMedCrossRefPubMedCentralGoogle Scholar
  217. Naumann MS, Richter C, Mott C et al (2012) Budget of coral-derived organic carbon in a fringing coral reef in the Gulf of Aqaba. J Mar Syst 105–108:20–29CrossRefGoogle Scholar
  218. Naumann MS, Tolosa I, Taviani M (2015) Trophic ecology of two cold-water coral species from the Mediterranean Sea revealed by lipid biomarkers and compound-specific isotope analyses. Coral Reefs 34:1165–1175CrossRefGoogle Scholar
  219. Nelson CE, Goldberg SJ, Kelly LW (2013) Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. ISME J 7:962–979PubMedPubMedCentralCrossRefGoogle Scholar
  220. Nguyen-Kim H, Bouvier T, Bouvier C et al (2014) High occurrence of viruses in the mucus of scleractinian corals. Environ Microbiol Rep 6:675–682PubMedCrossRefPubMedCentralGoogle Scholar
  221. Ocaña O, Opresko DM, Brito A (2006) First record of the black coral Antipathella wollastoni (Anthozoa: Antipatharia) outside of Macaronesian waters. Rev Acad Can Cien 18:125–138Google Scholar
  222. Oku H, Yamashiro H, Onaga K (2003) Lipid biosynthesis from 14C-glucose in the coral Montipora digitata. Fish Sci 69:625–631CrossRefGoogle Scholar
  223. Olson ND, Lesser MP (2013) Diazotrophic diversity in the Caribbean coral, Montastraea cavernosa. Arch Microbiol 195:853–859PubMedCrossRefPubMedCentralGoogle Scholar
  224. Olson ND, Ainsworth TD, Gates M, Takabayashi M (2009) Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J Exp Mar Biol Ecol 371:140–146CrossRefGoogle Scholar
  225. Omori M, Ikeda T (1992) Methods in marine zooplankton ecology. Krieger Publishing, MalabarGoogle Scholar
  226. Orejas C, Gili J-M, Arntz W (2003) Role of small-plankton communities in the diet of two Antarctic octocorals (Primnoisis Antarctica and Primnoella sp.). Mar Ecol Prog Ser 250:105–116CrossRefGoogle Scholar
  227. Orejas C, Gori A, Rad-Menéndez C et al (2016) The effect of flow speed and food size on the capture efficiency and feeding behavior of the cold-water coral Lophelia pertusa. J Exp Mar Biol Ecol 481:34–40CrossRefGoogle Scholar
  228. Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89CrossRefGoogle Scholar
  229. Palardy JE, Grottoli A, Mathews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J Exp Mar Biol Ecol 331:99–107CrossRefGoogle Scholar
  230. Palardy JE, Rodrigues LJ, Grottoli AG (2008) The importance of zooplankton to the daily requirements of healthy and bleached corals. J Exp Mar Biol Ecol 367:180–188CrossRefGoogle Scholar
  231. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127PubMedPubMedCentralGoogle Scholar
  232. Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55:287–333CrossRefGoogle Scholar
  233. Patten N, Wyatt A, Lowe R, Waite A (2011) Uptake of picophytoplankton, bacterioplankton and virioplankton by a fringing coral reef community (Ningaloo Reef, Australia). Coral Reefs 30:555–567CrossRefGoogle Scholar
  234. Patterson MR (1991) The effects of flow on polyp-level prey capture in an octocoral, Alcyonium siderium. Biol Bull 180:93–102PubMedCrossRefPubMedCentralGoogle Scholar
  235. Patton J, Abraham S, Benson AA (1977) Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae. Evidence of a light-driven carbon cycle between symbiont and host. Mar Biol 44:235–247CrossRefGoogle Scholar
  236. Pernice M, Meier H, Van Den Heuvel A et al (2012) A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis. ISME J 6:1314–1324PubMedPubMedCentralCrossRefGoogle Scholar
  237. Picciano M, Ferrier-Pagès C (2007) Ingestion of Pico- and nanoplankton by the Mediterranean red coral Corallium rubrum. Mar Biol 150:733–782CrossRefGoogle Scholar
  238. Piniak GA (2002) Effect of symbiotic status, flow speed, and prey type on prey capture by the facultatively symbiotic temperate coral Oculina arbuscula. Mar Biol 141:449–455CrossRefGoogle Scholar
  239. Piraino S, Ulianich L, Zupo V, Russo GF (1993) Cnidocyst morphology and distribution in Corallium rubrum (L.) (Cnidaria, Anthozoa). Oebalia 19:67–78Google Scholar
  240. Porter JW (1974) Zooplankton feeding by the Caribbean reef- building coral Montastrea cavernosa. In: Cameron AM, Campbell BM, Cribb AB et al (eds) Proceedings of the second international coral reef symposium. The Great Barrier Reef Committee, Brisbane, pp 111–125Google Scholar
  241. Pratt EM (1905) The digestive organs of the Alcyonaria and their relation to the mesogloeal cell plexus. Quart J Micr Sci 49:327–362Google Scholar
  242. Purcell S, Bellwood D (2001) Spatial patterns of epilithic algal and detrital resources on a windward reef. Coral Reefs 20:117–125CrossRefGoogle Scholar
  243. 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. J Exp Mar Biol Ecol 395:55–62CrossRefGoogle Scholar
  244. Rädecker N, Pogoreutz C, Voolstra CR et al (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning. Trends Microbiol 23:490–497PubMedCrossRefPubMedCentralGoogle Scholar
  245. Raz-Bahat M, Douek J, Moiseeva E et al (2017) The digestive system of the stony coral Stylophora pistillata. Cell Tissue Res 368:311–323PubMedCrossRefPubMedCentralGoogle Scholar
  246. Reynard S, Martinez P, Houlbrèque F et al (2009) Effect of light and feeding on the nitrogen isotopic composition of a zooxanthellate coral: role of nitrogen recycling. Mar Ecol Prog Ser 392:103–110CrossRefGoogle Scholar
  247. Ribes M, Coma R, Gili J-M (1998) Heterotrophic feeding by gorgonian corals with symbiotic zooxanthellae. Limnol Oceanogr 43:1170–1179CrossRefGoogle Scholar
  248. Ribes M, Coma R, Gili J-M (1999) Heterogeneous feeding in benthic suspension. feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Mar Ecol Prog Ser 183:125–137CrossRefGoogle Scholar
  249. Ribes M, Coma R, Rossi S (2003) Natural feeding of the temperate asymbiotic octocoral-gorgonian Leptogorgia sarmentosa (Cnidaria: Octocorallia). Mar Ecol Prog Ser 254:141–150CrossRefGoogle Scholar
  250. Ribes M, Coma R, Atkinson MJ, Kinzie RA III (2005) Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr 50:1480–1489CrossRefGoogle Scholar
  251. Rix L, de Goeij JM, Mueller CE et al (2016) Coral mucus fuels the sponge loop in warm- and cold-water reef ecosystems. Sci Rep 6:18715PubMedPubMedCentralCrossRefGoogle Scholar
  252. Roberts MJ, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547PubMedCrossRefPubMedCentralGoogle Scholar
  253. Robertson DR (1982) Fish feces as fish food. Mar Ecol Prog Ser 7:253–265CrossRefGoogle Scholar
  254. Rodolfo-Metalpa R, Periano A, Houlbrèque F et al (2008) Effects of temperature, light and heterotrophy on the growth rate and budding of the temperate coral Cladocora. Coral Reefs 27:17–25CrossRefGoogle Scholar
  255. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  256. Roff G, Dove SG, Dunn SR (2009) Mesenterial filaments make a clean sweep of substrates for coral growth. Coral Reefs 28:79CrossRefGoogle Scholar
  257. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  258. Rosenberg E, Koren O, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362PubMedCrossRefPubMedCentralGoogle Scholar
  259. Roshan S, DeVries T (2017) Efficient dissolved organic carbon production and export in the oligotrophic ocean. Nat Commun 8:2036.  https://doi.org/10.1038/s41467-017-02227-3CrossRefPubMedPubMedCentralGoogle Scholar
  260. Rosset S, D’Angelo C, Wiedenmann J (2015) Ultrastructural biomarkers in symbiotic algae reflect the availability of dissolved inorganic nutrients and particulate food to the reef coral holobiont. Front Mar Sci 2:103.  https://doi.org/10.3389/fmars.2015.00103CrossRefGoogle Scholar
  261. Rosset S, Wiedenmann J, Reed AJ, D’Angelo C (2017) Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar Pollut Bull 118:180–187PubMedPubMedCentralCrossRefGoogle Scholar
  262. Rossi S, Ribes M, Coma R, Gili J-M (2004) Temporal variability in zooplankton prey capture rate of the passive suspension feeder Leptogorgia sarmentosa (Cnidaria: Octocorallia), a case study. Mar Biol 144:89–99CrossRefGoogle Scholar
  263. Rubio-Portillo E, Kersting DK, Linares C et al (2018) Biogeographic differences in the microbiome and pathobiome of the coral Cladocora caespitosa in the western Mediterranean Sea. Front Microbiol 9:22.  https://doi.org/10.3389/fmicb.2018.00022CrossRefPubMedPubMedCentralGoogle Scholar
  264. Rusch A, Hannides AK, Gaidos E (2009) Diverse communities of active bacteria and archaea along oxygen gradients in coral reef sediments. Coral Reefs 28:15–26CrossRefGoogle Scholar
  265. Sammarco PW, Coll JC (1992) Chemical adaptations in the Octocorallia—evolutionary considerations. Mar Ecol Prog Ser 88:93–104CrossRefGoogle Scholar
  266. Sammarco PW, Risk MJ, Schwarcz HP, Heikoop JM (1999) Cross-continental shelf trends in coral δ15N on the Great Barrier Reef: further consideration of the reef nutrient paradox. Mar Ecol Prog Ser 180:131–138Google Scholar
  267. Sato Y, Willis BL, Bourne DG (2009) Successional changes in bacterial communities during the development of black band disease on the reef coral, Montipora hispida. ISME J 24:203–214Google Scholar
  268. Schantz AA, Ladd MC, Schrack E, Burkepile DE (2017) Fish-derived nutrient hotspots shape coral reef benthic communities. Ecol Appl 25:2142–2152CrossRefGoogle Scholar
  269. Scheffers SR, Nieuwland G, Bak RPM, Van Duyl FC (2004) Removal of bacteria and nutrient dynamics within the coral reef framework of Curacao (Netherlands Antilles). Coral Reefs 23:413–422CrossRefGoogle Scholar
  270. Schlichter D (1982) Epidermal nutrition of the alcyonarian Heteroxenia fuscescens (Ehrib): absorption of dissolved organic material and lost endogenous photosynthates. Oecologia 53:40–49PubMedCrossRefPubMedCentralGoogle Scholar
  271. Schlichter D, Brendelberger H (1998) Plasticity of the scleractinian body plan: functional morphology and trophic specialization of Mycedium elephantotus (Pallas, 1766). Facies 39:227–241CrossRefGoogle Scholar
  272. Schlichter D, Fricke HW, Weber W (1986) Light harvesting by wavelength transformation in a symbiotic coral of the Red Sea twilight zone. Mar Biol 91:403–407CrossRefGoogle Scholar
  273. Schmidt H, Moraw B (1982) The cnidogenesis of the Octocorallia (Anthozoa, Cnidaria) 2. maturation, migration and degeneration of cnidoblast and nematocyst. Helgol Meeresunters 35:97–118CrossRefGoogle Scholar
  274. Schöttner SI, Pfitzner B, Grünke S (2011) Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environ Microbiol 13:1815–1826PubMedPubMedCentralCrossRefGoogle Scholar
  275. Sebens KP (1984) Water flow and coral colony size: interhabitat comparisons of the octocoral Alcyonium siderium. Proc Natl Acad Sci USA 81:5473–5477PubMedCrossRefPubMedCentralGoogle Scholar
  276. Sebens KP, Johnson AS (1991) Effect of water movement on prey capture and distribution of reef coral. Hydrobiologia 226:91–101CrossRefGoogle Scholar
  277. Sebens KP, Koehl MAR (1984) Predation on zooplankton by the benthic anthozoans Alcyonium siderium (Alcyonacea) and Metridium senile (Actiniaria) in the New England subtidal. Mar Biol 81:255–271CrossRefGoogle Scholar
  278. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastraea cavernosa, in a field enclosure. Mar Biol 127:303–317CrossRefGoogle Scholar
  279. Sebens KP, Grace SP, Helmuth B et al (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastraea cavernosa and Porites porites, in a field enclosure. Mar Biol 131:347–360CrossRefGoogle Scholar
  280. Seeman J (2013) The use of 13C and 15N isotope labeling techniques to assess heterotrophy of corals. J Exp Mar Biol Ecol 442:88–95CrossRefGoogle Scholar
  281. Servetto N, Rossi S, Fuentes V et al (2017) Seasonal trophic ecology of the dominant Antarctic coral Malacobelemnon daytoni (Octocorallia, Pennatulacea, Kophobelemnidae). Mar Environ Res 130:264–274PubMedCrossRefPubMedCentralGoogle Scholar
  282. Shapiro OH, Fernandez VI, Garren M et al (2014) Vortical ciliary flows actively enhance mass transport in reef corals. Proc Natl Acad Sci USA 111:13391–13396PubMedCrossRefPubMedCentralGoogle Scholar
  283. Sharon G, Rosenberg E (2008) Bacterial growth on coral mucus. Curr Microbiol 56:481–488PubMedCrossRefPubMedCentralGoogle Scholar
  284. Sharoni S, Trainic M, Schatz D et al (2015) Infection of phytoplankton by aerosolized marine viruses. Proc Natl Acad Sci USA 112:6643–6647PubMedCrossRefPubMedCentralGoogle Scholar
  285. Sherwood OA, Jamieson RE, Edinger EN et al (2008) Stable C and N isotopic composition of cold-water corals from Newfoundland and Labrador continental slope: examination of trophic, depth and spatial effects. Deep-Sea Res 55:1392–1402CrossRefGoogle Scholar
  286. Shick JM (1991) A functional biology of sea anemones. Springer Science+Business Media, DordrechtCrossRefGoogle Scholar
  287. Sieburth JM, Smetacek V, Lenz J (1978) Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol Oceanogr 23:1256–1263CrossRefGoogle Scholar
  288. Silveira CB, Cavalcanti GS, Walter JM et al (2017) Microbial processes driving coral reef organic carbon flow. FEMS Microbiol Rev 41:575–595PubMedCrossRefPubMedCentralGoogle Scholar
  289. Slattery M, McClintock JB, Bowser SS (1997) Deposit feeding: a novel mode of nutrition in the Antarctic colonial soft coral Gersemia antarctica. Mar Ecol Prog Ser 149:299–304CrossRefGoogle Scholar
  290. Smriga S, Sandin SA, Azam F (2010) Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol Ecol 73:31–42PubMedPubMedCentralGoogle Scholar
  291. Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9:499–508PubMedCrossRefPubMedCentralGoogle Scholar
  292. Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Organ 87:5–18PubMedCrossRefPubMedCentralGoogle Scholar
  293. Sorokin Y (1973) On the feeding of some scleractinian corals with bacteria and dissolved organic matter. Limnol Oceanogr 18:380–385CrossRefGoogle Scholar
  294. Sorokin Y (1991) Biomass, metabolic rates and feeding of some common reef zoantharians and octocorals. Aust J Mar Freshwater Res 42:729–741CrossRefGoogle Scholar
  295. Sorokin YI (1992) Phosphorus metabolism in coral reef communities: Exchange between the water column and bottom biotopes. Hydrobiologia 242:105–114CrossRefGoogle Scholar
  296. Sorokin Y (1995) Coral reef ecology. Springer, BerlinGoogle Scholar
  297. Sorokin YI, Sorokin PY (2010) Plankton of the central Great Barrier Reef: abundance, production and trophodynamic roles. J Mar Biol Assoc UK 90:1173–1187CrossRefGoogle Scholar
  298. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904Google Scholar
  299. Stocker JG (1988) Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol Oceanogr 33:765–775Google Scholar
  300. Stocker JG (2012) Marine microbes see a sea of gradients. Science 338:628–633PubMedCrossRefPubMedCentralGoogle Scholar
  301. Strömberg SM, Östman C (2017) The cnidome and internal morphology of Lophelia pertusa (Linnaeus, 1758) (Cnidaria, Anthozoa). Acta Zool 98:191–213PubMedCrossRefPubMedCentralGoogle Scholar
  302. Suttle CA (2005) Viruses in the sea. Nature 437:356–361PubMedCrossRefPubMedCentralGoogle Scholar
  303. Suzuki Y, Casareto BE (2011) The role of dissolved organic nitrogen (DON) in coral biology and reef ecology. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer Sci Business Media BV, Dordrecht, pp 207–214Google Scholar
  304. Sweet M, Bythell J (2016) The role of viruses in coral health and disease. J Invertebr Pathol 147:136–144PubMedCrossRefPubMedCentralGoogle Scholar
  305. Tada K, Sakai K, Nakano Y et al (2003) Size-fractionated phytoplankton biomass in coral reef waters off Sesoko Island, Okinawa, Japan. J Plankton Res 25:991–997CrossRefGoogle Scholar
  306. Tagliafico A, Rudd D, Rangel MS et al (2017a) Lipid-enriched diets reduce the impacts of thermal stress in corals. Mar Ecol Prog Ser 573:129–141CrossRefGoogle Scholar
  307. Tagliafico A, Rangel S, Kelaher B, Christidis L (2017b) Optimizing heterotrophic feeding rates of three commercially important scleractinian corals. Aquaculture 483:96–101CrossRefGoogle Scholar
  308. Tanaka Y, Miyajima T, Isao K et al (2008) Production of dissolved and particulate organic matter by the reef-building corals Porites cylindrica and Acropora pulchra. Bull Mar Sci 82:237–245Google Scholar
  309. Tanaka Y, Miyajima T, Umezawa Y (2009) Net release of dissolved organic matter by the scleractinian coral Acropora pulchra. J Exp Mar Biol Ecol 377:101–106CrossRefGoogle Scholar
  310. Tanaka Y, Ogawa H, Miyajima T (2011) Bacterial decomposition of coral mucus as evaluated by long-term and quantitative observation. Coral Reefs 30:443–449CrossRefGoogle Scholar
  311. Tanaka Y, Grottoli AG, Matsui Y et al (2015) Partitioning of nitrogen sources to algal endosymbionts of corals with long-term 15N-labelling and a mixing model. Ecol Model 309–310:163–169CrossRefGoogle Scholar
  312. Taniguchi A, Yoshida T, Eguchi M (2014) Bacterial production is enhanced by coral mucus in reef systems. J Exp Mar Biol Ecol 461:331–336CrossRefGoogle Scholar
  313. Tazoli S, Bo M, Boyer M et al (2007) Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia). Zool Stud 46:227–241Google Scholar
  314. Tchernov D, Gorbunov MY, de Vargas C et al (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching. Proc Natl Acad Sci USA 101:13531–13535PubMedCrossRefPubMedCentralGoogle Scholar
  315. Tezcan ÖD (2016) Unusual cnidarian envenomations. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. The world of medusa and her sisters. Springer, Switzerland, pp 609–622CrossRefGoogle Scholar
  316. Thorington GU, Hessinger DA (1996) Efferent mechanisms of discharging cnidae: I. Measurements of intrinsic adherence of cnidae discharged from tentacles of the sea anemone, Aiptasia pallida. Biol Bull 190:125–138PubMedCrossRefPubMedCentralGoogle Scholar
  317. Thorington GU, Hessinger DA (1998) Efferent mechanisms of discharging cnidae: II. A nematocyst release response in the sea anemone tentacle. Biol Bull 195:145–155PubMedCrossRefPubMedCentralGoogle Scholar
  318. Thorington GU, McAuley V, Hessinger DA (2010) Effects of satiation and starvation on nematocyst discharge, prey killing and ingestion in two species of sea anemone. Biol Bull 219:122–131PubMedCrossRefPubMedCentralGoogle Scholar
  319. Thurber RV, Payet JP, Thurber AR, Correa AMS (2017) Virus-host interactions and their roles in coral reef health and disease. Nat Rev Microbiol 15:205–216PubMedCrossRefPubMedCentralGoogle Scholar
  320. Treignier C, Grover R, Ferrier-Pagès C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53:2702–2710CrossRefGoogle Scholar
  321. Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species. Mar Ecol Prog Ser 422:165–177CrossRefGoogle Scholar
  322. Tremblay P, Grover G, Maguer J-F et al (2012a) Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393PubMedCrossRefPubMedCentralGoogle Scholar
  323. Tremblay P, Ferrier-Pagès C, Maguer JF et al (2012b) Controlling effects of irradiance and heterotrophy on carbon translocation in the temperate coral Cladocora caespitosa. PLoS One 7(9):e44672PubMedPubMedCentralCrossRefGoogle Scholar
  324. Tremblay P, Grover R, Maguer JF (2014) Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata. Coral Reefs 33:1–13CrossRefGoogle Scholar
  325. Tremblay P, Maguer JF, Grover R, Ferrier-Pagès C (2015) Trophic dynamics of scleractinian corals: stable isotope evidence. J Exp Biol 218:1223–1243PubMedCrossRefPubMedCentralGoogle Scholar
  326. Tseng LC, Dahma HU, Hsu NJ, Hwang JS (2011) Effects of sedimentation on the gorgonian Subergorgia suberosa (Pallas, 1766). Mar Biol 158:1301–1310CrossRefGoogle Scholar
  327. Tsounis G, Rossi S, Laudien J et al (2006) Diet and seasonal prey capture rates in the Mediterranean red coral (Corallium rubrum L.). Mar Biol 149:313–325CrossRefGoogle Scholar
  328. Turner JT (2002) Zooplankton fecal pellets, marine snow and sinking plankton blooms. Aquat Microb Ecol 27:57–102CrossRefGoogle Scholar
  329. Turner JT (2015) Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr 130:205–248CrossRefGoogle Scholar
  330. Ulstrup KE, van Oppen MJH, Kühl M, Ralph J (2007) Inter-polyp genetic and physiological characterization of Symbiodinium in an Acropora valida colony. Mar Biol 153:225–234CrossRefGoogle Scholar
  331. van Oevelen D, Mueller CE, Lundälv T, Middleberg JJ (2016) Food selectivity and processing by the cold-water coral Lophelia pertusa. Biogeosciences 13:5789–5798CrossRefGoogle Scholar
  332. Vanhaecke P, Sorgeloos P (1980) The biometrics of Artemia strains from different geographical origin. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (eds) The brine shrimp Artemia, vol 3 Ecology, culturing, use in aquaculture. Universa Press, Wetteren, pp 393–405Google Scholar
  333. Van-Praët M (1985) Nutrition of sea anemones. Adv Mar Biol 22:65–99CrossRefGoogle Scholar
  334. Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria:Anthozoa: Hexacorallia: Antipatharia). Adv Mar Biol 63:67–132PubMedCrossRefPubMedCentralGoogle Scholar
  335. Wainwright SA, Dillon JR (1969) On the orientation of sea fans (genus Gorgonia). Bull Mar Sci 136:130–139Google Scholar
  336. Waite AM, Safi K, Hall JA, Nodder SD (2000) Mass sedimentation of picoplankton embedded in organic aggregates. Limnol Oceanogr 45:87–97CrossRefGoogle Scholar
  337. Walsh K, Haggerty JM, Doane MP et al (2017) Aura-biomes are present in the water layer above coral reef macro-organisms. Peer J 5:e3666PubMedCrossRefPubMedCentralGoogle Scholar
  338. Warner GF (1981) Species descriptions and ecological observations of black corals (Antipatharia) from Trinidad. Bull Mar Sci 31:147–163Google Scholar
  339. Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897CrossRefGoogle Scholar
  340. Watson GM, Mariscal RN (1983) The development of a sea anemone tentacle specialized for aggression: morphogenesis and regression of the catch tentacle of Haliplanella luciae (Cnidaria:Anthozoa). Biol Bull 164:506–517CrossRefGoogle Scholar
  341. Wheeler AJ, Beyer A, Freiwald A et al (2007) Morphology and environment of cold-water coral carbonate mounds on the NW European margin. Int J Earth Sci 96:37–56CrossRefGoogle Scholar
  342. Widdig A, Schlichter D (2001) Phytoplankton: a significant trophic source for soft corals? Helgoland Mar Res 55:198–211CrossRefGoogle Scholar
  343. Wiedenmann J, D’Angelo CD, Smith EG et al (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:160–164CrossRefGoogle Scholar
  344. Wijgerde T, Diantari R, Lewaru MW et al (2011) Extracoelenteric zooplankton feeding is the key mechanism of nutrient acquisition for the scleractinian coral Galaxea fascicularis. J Exp Biol 214:3351–3357PubMedCrossRefPubMedCentralGoogle Scholar
  345. Wijgerde T, Spijkers P, Karruppannan E et al (2012) Water flow affects zooplankton feeding by the scleractinian coral Galaxea fascicularis on a polyp and colony level. J Mar Biol 854489  https://doi.org/10.1155/2012/854849
  346. Wild C, Huettel M, Klueter A et al (2004a) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70PubMedCrossRefPubMedCentralGoogle Scholar
  347. Wild C, Rasheed MY, Werner U et al (2004b) Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267:159–171CrossRefGoogle Scholar
  348. Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87–98CrossRefGoogle Scholar
  349. Wild C, Mayr C, Wehrmann L et al (2008) Organic matter release by cold-water corals and its implications for fauna-microbe interaction. Mar Ecol Prog Ser 272:67–75CrossRefGoogle Scholar
  350. Wild C, Naumann MS, Haas A (2010a) Organic matter release by Red Sea coral reef organisms- potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411:61–71CrossRefGoogle Scholar
  351. Wild C, Naumann M, Niggl W, Haas A (2010b) Composition of mucus released by scleractinian warm- and cold-water reef corals. Aquat Biol 10:41–45CrossRefGoogle Scholar
  352. Williams B, Grottoli AG (2010) Stable nitrogen and carbon isotope (δ15N and δ13C) variability in shallow tropical Pacific soft coral and black coral taxa and implications for paleoceanographic reconstructions. Geochim Cosmochim Acta 74:5280–5288Google Scholar
  353. Wilson SK, Bellwood DR, Choat HJ, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol Annu Rev 41:279–309Google Scholar
  354. Wooldridge SA (2017) Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1. Identifying thresholds of concern for the Great Barrier Reef, Australia. Mar Pollut Bull 114:343–354PubMedCrossRefPubMedCentralGoogle Scholar
  355. Work T, Meteyer C (2014) To understand coral disease, look at coral cells. Ecohealth 11:610–618PubMedCrossRefPubMedCentralGoogle Scholar
  356. Wotton RS, Malmqvist B (2001) Feces in aquatic ecosystems: feeding animals transform organic matter into fecal pellets, which sink or are transported horizontally by currents; these fluxes relocate organic matter in aquatic ecosystems. BioScience 51:537–544CrossRefGoogle Scholar
  357. Wyatt ASJ, Lowe RJ, Humphries S, Waite AM (2010) Particulate nutrient fluxes over a fringing coral reef: relevant scales of phytoplankton production and mechanisms of supply. Mar Ecol Prog Ser 405:113–130CrossRefGoogle Scholar
  358. Wyatt ASJ, Lowe RJ, Humphries S, Waite AM (2013) Particulate nutrient fluxes over a fringing reef: source-sink dynamics inferred from carbon to nitrogen ratios and stable isotopes. Limnol Oceanogr 58:409–427CrossRefGoogle Scholar
  359. Yahel R, Yahel G, Genin A (2005) Near-bottom depletion of zooplankton over coral reefs: I: diurnal dynamics and size distribution. Coral Reefs 24:75–85CrossRefGoogle Scholar
  360. Yamamuro M, Kayanne H, Minagawa M (1995) Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol Oceanogr 40:617–621CrossRefGoogle Scholar
  361. Yamashiro H, Oku H, Higa H et al (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physiol B 122:397–407CrossRefGoogle Scholar
  362. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694PubMedCrossRefPubMedCentralGoogle Scholar
  363. Yoffe C, Lotan Y, Benayahu Y (2012) A modified view on octocorals: Heteroxenia fuscesans nematocysts are diverse, featuring both an ancestral and a novel type. PLoS One 7(2):e31902PubMedPubMedCentralCrossRefGoogle Scholar
  364. Yonge CM (1930a) Studies on the physiology of corals 3. Assimilation and excretion. British Mus Nat Hist Gt Barrier Reef Exped 1928–1929 Sci Repts 1:83–92Google Scholar
  365. Yonge CM (1930b) Studies on the physiology of corals 1. Feeding mechanisms and food. British Mus Nat Hist Gt Barrier Reef Exped 1928–1929 Sci Repts 1:13–57Google Scholar
  366. Zetsche E-M, Baussant T, Meysman FJR, van Oevelen D (2016) Direct visualization of mucus production by the cold-water coral Lophelia pertusa with digital holographic microscopy. PLoS One 11:e0146766.  https://doi.org/10.1371/journal.pone.0146766CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesFlorida International UniversityMiamiUSA

Personalised recommendations