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Fish or Germs? Microbial Dynamics Associated with Changing Trophic Structures on Coral Reefs

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Book cover Coral Reefs: An Ecosystem in Transition

Abstract

Overfishing major predators has dramatically changed the trophic structures of coral reefs. Here, we argue that the photosynthate, which would normally support the large predators via trophic transfers, is being used by microbes (Bacteria and Archaea) on degraded reefs. The supply of higher concentrations of photosynthate to the microbes increases their population size and enables heterotrophic microbes to dominate the community. In turn, the heterotrophic microbes detrimentally affect the corals causing disease outbreaks and death, which causes the phase shift from coral to fleshy algae (including macroalgae and turf algae) dominated reefs. To succeed, conservation and restoration efforts need to understand and consider the influence of microbes.

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References

  • Abram N, Gagan M, McCulloch M, Chappell J, Hantoro W (2003) Coral reef death during the 1997 Indian Ocean dipole linked to Indonesian wildfires. Science 301:952–955

    Article  CAS  Google Scholar 

  • Aerts LAM (1998) Sponge/coral interactions in Caribbean reefs: analysis of overgrowth patterns in relation to species identity and cover. Mar Ecol Prog Ser 175:241–249

    Article  Google Scholar 

  • Albert S, Udy J, Tibbetts IR (2008) Responses of algal communities to gradients in herbivore biomass and water quality in Marovo Lagoon, Solomon Islands. Coral Reefs 27:73–82

    Article  Google Scholar 

  • Allers E, Niesner C, Wild C, Pernthaler J (2008) Microbes enriched in seawater after addition of coral mucus. App Environ Microbiol 74:3274–3278

    Article  CAS  Google Scholar 

  • Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean reefs. Hydrobiologia 460:25–38

    Article  Google Scholar 

  • Atkinson JM (2010) Biogeochemical cycles on coral reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs and ecosystem in transition. Springer, Berlin

    Google Scholar 

  • Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694–696

    Article  CAS  Google Scholar 

  • Azam F, Smith DC (1991) Bacterial influence on the variability in the ocean’s biogeochemical state: a mechanistic view. In: Demers S (ed) Particle analysis in oceanography. Springer, Berlin, pp 213–235

    Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Reil LAM, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Bak RPM, Joenje M, de Jong I, Lambrechts DYM, Nieuwand G (1998) Bacterial suspension feeding by coral benthic organisms. Mar Ecol Prog Ser 175:285–288

    Article  Google Scholar 

  • Bell PRF, Lapointe BE, Elmetri I (2007) Reevaluation of ENCORE: support for the eutrophication threshold model for coral reefs. Ambio 36:416–424

    Article  CAS  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  CAS  Google Scholar 

  • Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439

    Article  CAS  Google Scholar 

  • Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. App Environ Microbiol 73:5642–5647

    Article  CAS  Google Scholar 

  • Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174

    Article  CAS  Google Scholar 

  • Boyer JN, Fourqurean JW, Jones RD (1999) Seasonal and long-term trends in the water quality of Florida Bay (1989-1997). Estuaries 22:417–430

    Article  CAS  Google Scholar 

  • Boyer KE, Fong P, Armitage AR, Cohen RA (2004) Elevated nutrient content of tropical fleshy algae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23:530–538

    Google Scholar 

  • Carlson CA (2002) Production and removal processes. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, Amsterdam, pp 91–153

    Chapter  Google Scholar 

  • Carlson CA, Ducklow HW, Sleeters TD (1996) Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep Sea Res II 43:491–515

    Article  CAS  Google Scholar 

  • Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Otero MP, Vergin K, Wheeler BR (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30:19–36

    Article  Google Scholar 

  • Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Vergin K (2004) Interactions between DOC, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol Oceanogr 49:1073–1083

    Article  CAS  Google Scholar 

  • Carpenter SR, Brock WA, Cole JJ, Kitchell JF, Pace ML (2008) Leading indicators of trophic cascades. Ecol Lett 11:128–138

    CAS  Google Scholar 

  • Charpy L, Charpy-Roubaud CJ (1990) Trophic structure and productivity of the lagoonal communities of Tikehau Atoll (Tuamotu Archipelago, French Polynesia). Hydrobiologia 207:43–52

    Article  Google Scholar 

  • Chin W-C, Orellana MV, Verdugo V (1998) Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391:568–572

    Article  CAS  Google Scholar 

  • Connell SD (1998) Effects of predators on growth, mortality and abundance of a juvenile reef-fish: evidence from manipulations of predator and prey abundance. Mar Ecol Prog Ser 169:251–261

    Article  Google Scholar 

  • Coppard SE, Campbell AC (2007) Grazing preferences of diadematid echinoids in Fiji. Aquat Bot 86:204–212

    Article  Google Scholar 

  • 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 6:35–42

    Article  CAS  Google Scholar 

  • Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the Staghorn coral Acropora acuminata. Mar Biol 60:81–90

    Article  CAS  Google Scholar 

  • D’Croz L, Del Rosario JB, Gondola P (2005) The effect of fresh water runoff on the distribution of dissolved inorganic nutrients and plankton in the Bocas del Toro archipelago, Caribbean Panama. Caribbean J Sci 41:414–429

    Google Scholar 

  • de Goeij JM, van Duyl FC (2007) Coral cavities are sinks of dissolved organic carbon (DOC). Limnol Oceanogr 52:2608–2617

    Article  Google Scholar 

  • de Goeij JM, Moodley L, Houtekamer M, Carballeira NM, van Duyl FC (2008a) Tracing C-13-enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge Halisarca caerulea: evidence for DOM feeding. Limnol Oceanogr 53:1376–1386

    Article  Google Scholar 

  • de Goeij JM, van den Berg H, van Oostveen MM, Epping EHG, Van Duyl FC (2008b) Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Mar Ecol Prog Ser 357:139–151

    Article  CAS  Google Scholar 

  • DeMartini EE, Friedlander AM, Sandin SA, Sala E (2008) Differences in fish-assemblage structure between fished and unfished atolls in the northern Line Islands, central Pacific. Mar Ecol Prog Ser 365:199–215

    Article  Google Scholar 

  • Dinsdale EA, Pantos O, Smriga S, Edwards RA, Wegley L, Angly F, Brown E, Haynes M, Krause L, Sala E, Sandin SA, Vega TR, Willis BL, Knowlton N, Azam F, Rohwer F (2008) Microbial ecology of four coral atolls in the Northern Line Islands. PLoS ONE 3:e1584

    Article  CAS  Google Scholar 

  • Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132

    Article  Google Scholar 

  • Dubinsky Z, Stambler N (1996) Marine pollution and coral reefs. Glob Change Biol 2:511–526

    Article  Google Scholar 

  • Ducklow HW, Mitchell R (1979a) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725

    Article  Google Scholar 

  • Ducklow HW, Mitchell R (1979b) Composition of mucus released by coral reef coelenterates. Limnol Oceanogr 24:706–714

    Article  CAS  Google Scholar 

  • Ducklow HW, Mitchell R (1979c) Observations on naturally and artificially diseased tropical corals: a scanning electron microscope study. Microb Ecol 5:215–223

    Article  Google Scholar 

  • Essington TE, Beaudreau AH, Wiedenmann J (2006) Fishing through marine food webs. Proc Natl Acad Sci 103:3171–3175

    Article  CAS  Google Scholar 

  • Fabricius K, Wild C, Wolanski E, Abele D (2003) Effects of transparent exopolymer particles (TEP) and muddy terrigenous sediments on the survival of hard coral recruits. Coast Shelf Sci 57:613–621

    Article  CAS  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43:606–611

    Article  Google Scholar 

  • Forocucci D (1994) Population density, recruitment and 1991 mortality event of Diadema antillarum in the Florida Keys. Bull Mar Sci 54:917–928

    Google Scholar 

  • Fox RJ, Bellwood DR (2008) Remote video bioassays reveal the potential feeding impact of the rabbitfish Siganus canaliculatus (f: Siganidae) on an inner-shelf reef of the Great Barrier Reef. Coral Reefs 27:605–615

    Article  Google Scholar 

  • Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the Main Hawaiian Islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264

    Article  Google Scholar 

  • Fuhrman JA, Sleeter TD, Carlson CA, Proctor LM (1989) Dominance of bacterial biomass in the Sargasso Sea and its ecological implications. Mar Ecol Prog Ser 57:207–217

    Article  Google Scholar 

  • Furnas M, Mitchell A, Skuza M, Brodie J (2005) In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrierr Reef Lagoon. Mar Pollut Bull 51:253–265

    Article  CAS  Google Scholar 

  • Green EP, Bruckner AW (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96:347–361

    Article  Google Scholar 

  • Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2003) Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–2274

    Article  CAS  Google Scholar 

  • Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 332:216–225

    Article  CAS  Google Scholar 

  • Hairston NG Jr, Hairston NG Sr (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. Am Natl 142:379–411

    Article  Google Scholar 

  • Hairston NGJ, Hairston NGS (1997) Does food web complexity eliminate trophic-level dynamics? Am Nat 149:1001–1007

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  CAS  Google Scholar 

  • Harvell CD, Kim K, Burkholder J, Colwell RR, Epstein PR, Grimes J, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet R, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases – climate links and anthropogenic factors. Science 285:1505–1510

    Article  CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risk for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  Google Scholar 

  • Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith GJ, Weil E, Willis BL (2007) Coral disease, environmental drivers and the balance between coral and microbial associates. Oceanography 20:172–195

    Google Scholar 

  • Hata H, Kudo S, Yamano H, Kurano N, Kayanne H (2002) Organic carbon flux in Shiraho coral reef (Ishigaki Island, Japan). Mar Ecol Prog Ser 232:129–140

    Article  Google Scholar 

  • Haynes D (2001) Great Barrier Reef water quality: current issues. Great Barrier Reef Marine Park Authority, Townsville, p 90

    Google Scholar 

  • Hodgson G (1990) Tetracycline reduces sedimentation damage to corals. Mar Biol 104:493–496

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) Influence of the population-density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57:173–186

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Muscatine L, Goiran C, Siggaard D, Marion G (2004) Nutrient-induced perturbations to delta C-13 and delta N-15 in symbiotic dinoflagellates and their coral hosts. Mar Ecol Prog Ser 280:105–114

    Article  Google Scholar 

  • Hughes TP (1994) Catastrophes, phase shift, and large-scale degradation of a Caribbean reef. Science 265:1547–1551

    Article  CAS  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis BL (2007) Phase shifts, herbivory, and resilience of coral reefs to climate change. Curr Biol 17:1–6

    Article  CAS  Google Scholar 

  • Jackson JBC (2008) Ecological extinction and evolution in the brave new ocean. Proc Natl Acad Sci 105:11458–11465

    Article  CAS  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  CAS  Google Scholar 

  • Johnston IS, Rohwer F (2007) Microbial landscapes on the outer tissue surfaces of the reef-building coral Porites compressa. Coral Reefs 26:375–383

    Article  Google Scholar 

  • Klaus JS, Janse I, Heikoop JM, Sanford RA, Fouke BW (2007) Coral microbial communities, zooxanthellae and mucus along gradients of seawater depth and coastal pollution. Environ Microbiol 9:1291–1305

    Article  CAS  Google Scholar 

  • Kline DL, Kuntz NM, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314:119–125

    Article  CAS  Google Scholar 

  • Knowlton N (1992) Thresholds and multiple stable states in coral reef community dynamics. Am Zoo 32:674–682

    Google Scholar 

  • Knowlton NK, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:215–220

    Article  CAS  Google Scholar 

  • Koop K, Booth D, Broadbent A, Brodie J, Bucher D, Capone D, Coll J, Dennison W, Erdmann M, Harrison P, Hoegh-Guldberg O, Hutchings P, Jones GB, Larkum AWD, O’Neil J, Steven A, Tentori E, Ward S, Williamson J, Yellowlees D (2001) ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar Pollut Bull 42:91–120

    Article  CAS  Google Scholar 

  • Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259

    Article  CAS  Google Scholar 

  • Kramer KL, Heck KL (2007) Top-down trophic shifts in Florida keys patch reef marine protected areas. Mar Ecol Prog Ser 349:111–123

    Article  Google Scholar 

  • Kuntz NM, Kline DL, Sandin SA, Rohwer F (2005) Pathologies and mortality rates caused by organic carbon and nutrient stressors in three Caribbean coral species. Mar Ecol Prog Ser 294:173–180

    Article  CAS  Google Scholar 

  • Lampert Y, Kelman D, Nitzan Y, Dubinsky Z, Behar A, Hill RT (2008) Phylogenetic diversity of bacteria associated with the mucus of Red Sea corals. FEMS Microbiol Ecol 64:187–198

    Article  CAS  Google Scholar 

  • Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131

    Article  CAS  Google Scholar 

  • Ledlie MH, Graham NAJ, Bythell JC, Wilson SK, Jennings S, Polunin NVC, Hardcastle J (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641–653

    Article  Google Scholar 

  • Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997–1000

    Article  CAS  Google Scholar 

  • Lesser MP, Falcón LI, Rodríguez-Román A, Enríquez S, Hoegh-Guldberg O, Roberto Iglesias-Prieto R (2007) Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar Ecol Prog Ser 346:143–152

    Article  CAS  Google Scholar 

  • Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Ann Rev Ecol Syst 19:371–393

    Google Scholar 

  • Lessios HA (2005) Diadema antillarum populations in Panama twenty years following mass mortality. Coral Reefs 24:125–127

    Article  Google Scholar 

  • Littler MM, Littler DS, Titlyanov EA (1991) Comparisons of N- and P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles Archipelago: a test of the relative-dominance paradigm. Coral Reefs 10:199–209

    Article  Google Scholar 

  • Littler MM, Littler DS, Brooks BL, Lapointe BE (2006) Nutrient manipulation methods for coral reef studies: a critical review and experimental field data. J Exp Mar Biol Ecol 336:242–253

    Article  Google Scholar 

  • Littman RA, Willis BL, Pfeffer C, Bourne DG (2009) Diversity of coral-associated bacteria differ with location, but not species for three Acroporids on the Great Barrier Reef. FEMS Microbiol Ecol 68:152–156

    Article  CAS  Google Scholar 

  • Lokrantz J, Nystrom M, Thyresson M, Johansson C (2008) The non-linear relationship between body size and function in parrotfishes. Coral Reefs 27:967–974

    Article  Google Scholar 

  • Marhaver KL, Edwards RA, Rohwer F (2008) Viral communities associated with healthy and bleaching corals. Environ Microbiol 10:2277–2286

    Article  CAS  Google Scholar 

  • McClanahan T, Sala E, Stickels P, Cokos B, Baker A, Starger C (2003) Interaction between nutrients and herbivory in controlling algal communities and coral condition on Glover’s Reef, Belize. Mar Ecol Prog Ser 261:135–147

    Article  Google Scholar 

  • McClenachan L, Cooper AB (2008) Extinction rate, historical population structure and ecological role of the Caribbean monk seal. Proc R Soc Lond B 275:1351–1358

    Article  Google Scholar 

  • McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417

    Article  Google Scholar 

  • McDole T, Edwards RA, Dinsdale EA, Walsh S, Donovan M, Rohwer F (2008) Microbial dynamics of Kiritimati Atoll. 11th Int. Coral Reef Symp. Fort Lauderdale

    Google Scholar 

  • Mora C, Andrefoutet S, Costello MJ, Kranenburg C, Rollo A, Veron J, Gaston KJ, Myers RA (2006) Coral reefs and the global network of marine protected areas. Science 312:1750–1751

    Article  CAS  Google Scholar 

  • Mora C (2008) A clear human footprint in the coral reefs of the Caribbean. Proc R Soc B 275:767–773

    Article  CAS  Google Scholar 

  • Mullen K, Peters E, Harvell CD (2004) Coral resistance to disease. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 377–399

    Google Scholar 

  • Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101

    Article  CAS  Google Scholar 

  • Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci 104:8362–8367

    Article  CAS  Google Scholar 

  • Munro JL (1983) Caribbean coral reef fisheries, 2nd edn. ICLARM Stud. Rev. ICLARM, Makati, pp 1–276

    Google Scholar 

  • Muscatine L, D’elia CF (1978) Uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734

    Article  CAS  Google Scholar 

  • Newman MJH, Paredes GA, Sala E, Jackson JBC (2006) Structure of Caribbean coral reef communities across a large gradient of fish biomass. Ecol Letters 9:1216–1227

    Article  Google Scholar 

  • Nordemar I, Sjoo GL, Mork E, McClanahan TR (2007) Effects of estimated herbivory on the reproductive potential of four East African algal species – a mechanism behind ecosystem shifts on coral reefs? Hydrobiologia 575:57–68

    Article  Google Scholar 

  • Nugues MM, Smith GW, van Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923

    Article  Google Scholar 

  • Opsahl S, Benner R (1997) Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386:480–482

    Article  CAS  Google Scholar 

  • Pages J, Torreton J, Sempere R (1997) Dissolved organic carbon in coral-reef lagoons by high temperature catalytic oxidation and UV spectrometry. C R Acad Sci Ser II A Sci Terre Planetes 324:915–922

    CAS  Google Scholar 

  • Pandolfi JM, Jackson JBC, Baron N, Bradbury RH, Guzman HM, Hughes TP, Kappel CV, Micheli F, Ogden CJ, Possingham HP, Sala E (2005) Are U. S. coral reefs on the slippery slope to slime? Science 307:1725–1726

    Article  CAS  Google Scholar 

  • Pascal H, Vacelet V (1981) Bacterial utilization of mucus on the coral reef of Aquaba (Red Sea). Proc 4th Int Coral Reef Symp 1:669–677

    Google Scholar 

  • Patten NL, Harrison PL, Mitchell JG (2008a) Prevalence of virus-like particles within a staghorn scleractinian coral (Acropora muricata) from the Great Barrier Reef. Coral Reefs 27:569–580

    Article  Google Scholar 

  • Patten NL, Mitchell JG, Middelboe M, Eyre BD, Seuront L, Harrison PL, Glud RN (2008b) Bacterial and viral dynamics during a mass coral spawning period on the Great Barrier Reef. Aquat Microb Ecol 50:209–220

    Article  Google Scholar 

  • Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2068–2073

    Article  CAS  Google Scholar 

  • Rohwer F, Kelley S (2004) Culture-independent analyses of coral-associated microbes. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 265–277

    Google Scholar 

  • Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of Bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91

    Article  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Rosenberg, Kurshmaro EA (2010) Microbial diseases of corals: pathology and ecology. In: Dubinsky Z, Stambler N (eds) Coral reefs and ecosystem in transition. Springer, Berlin

    Google Scholar 

  • Rosenberg E, Loya Y (2004) Coral health and disease. Springer, Berlin

    Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  Google Scholar 

  • Sakka A, Legendre L, Gosselin M, Niquil N, Delesalle B (2002) Carbon budget of the planktonic food web in an atoll lagoon (Takapoto, French Polynesia). J Plankton Res 24:301–320

    Article  Google Scholar 

  • Sandin S, Smith JE, DeMartini E, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos J, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the northern Line Islands. PLoS ONE 3:e1548

    Article  CAS  Google Scholar 

  • Schaffelke B, Klumpp DW (1998) Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar Ecol Prog Ser 170:95–105

    Article  Google Scholar 

  • Schaffelke B, Mellors J, Duke NC (2005) Water quality in the Great Barrier Reef region: responses of mangrove, seagrass and macroalgal communities. Mar Pollut Bull 51:279–296

    Article  CAS  Google Scholar 

  • Siboni N, Ben-Dov E, Sivan A, Kushmaro A (2008) Global distribution and diversity of coral-associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ Microbiol 10:2979–2990

    Article  CAS  Google Scholar 

  • Smith TB (2008) Temperature effects on herbivory for an Indo-Pacific parrotfish in Panama: implications for coral-algal competition. Coral Reefs 27:397–405

    Article  Google Scholar 

  • Smith JE, D SC, Hunter CL (2001) An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332–342

    Google Scholar 

  • Smith JE, Shaw M, Edwards RA, Obura DO, Pantos O, Sala E, Sandin SA, Rohwer F (2006) Indirect effects of algae on coral:algae-mediated, microbe-induced coral mortality. Ecol Letters 9:835–345

    Article  Google Scholar 

  • Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  Google Scholar 

  • Tanaka Y, Miyajima T, Koike I, Hayashibara T, Ogawa H (2006) Translocation and conservation of organic nitrogen within the coral-zooxanthellae symbiotic system of Acropora pulchra, as demonstrated by dual isotope-labeling techniques. J Exp Mar Biol Ecol 336:110–119

    Article  CAS  Google Scholar 

  • Tanner J, Hughes T, Connell J (1994) Species coexistence, keystone species, and succession – a sensitivity analysis. Ecology 75: 2204–2219

    Article  Google Scholar 

  • Thacker R, Ginsburg D, Paul V (2001) Effects of herbivore exclusion and nutrient enrichment on coral reef fleshy algae and cyanobacteria. Coral Reefs 19:318–329

    Article  Google Scholar 

  • Toledo-Hernandez C, Zuluaga-Montero A, Bones-Gonzalez A, Rodriguez JA, Sabat AM, Bayman P (2008) Fungi in healthy and diseased sea fans (Gorgonia ventalina): is Aspergillus sydowii always the pathogen? Coral Reefs 27:707–714

    Article  Google Scholar 

  • Torreton J-P, Pages J, Dufour P, Cauwet G (1997) Bacterioplankton carbon growth yield and DOC turnover in some coral reef lagoons. Proc 8th Int Coral Reef Symp 1:947–952

    CAS  Google Scholar 

  • UNESCO (1994) Protocols for the Joint Global Ocean Flux study (JGOFS) Core Measurements. IOC report Manuals and Guidelines 170

    Google Scholar 

  • van Duyl FC, Gast GJ (2001) Linkage of small-scale spatial variations in DOC, inorganic nutrients and bacterioplankton growth with different coral reef water types. Aquat Microb Ecol 24:17–26

    Article  Google Scholar 

  • van Duyl FC, Scheffers SR, Thomas FIM, Driscoll M (2006) The effect of water exchange on bacterioplankton depletion and inorganic nutrient dynamics in coral reef cavities. Coral Reefs 25:23–36

    Article  Google Scholar 

  • Verdugo V, Alldredge AL, Azam F, Kirchman DI, Passow U, Santschi PH (2004) The oceanic gel phase: a bridge in the DOM-POM continuum. Mar Chem 92:67–85

    Article  CAS  Google Scholar 

  • Vermeij MJA, Smith JE, Smith CM, Vega TR, Sandin SA (2008) Survival and settlement success of coral planulae independent and synergistic effects of fleshy algae and microbes. Oecologia 159:325–336

    Article  Google Scholar 

  • Voss JD, Richardson LL (2006) Nutrient enrichment enhances black band disease progression in corals. Coral Reefs 25:569–576

    Article  Google Scholar 

  • Wegley L, Yu Y, Breitbart M, Casas V, Kline DL, Rohwer F (2004) Coral-associated Archaea. Mar Ecol Prog Ser 273:89–96

    Article  CAS  Google Scholar 

  • Wegley L, Edwards RA, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719

    Article  CAS  Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MY, Jorgensen BB (2004a) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  CAS  Google Scholar 

  • Wild C, Rasheed MY, Werner U, Franke U, Johnson R, Huettel M (2004b) Degradation and mineralization of coral mucus in reef environments. Mar Ecol Prog Ser 267:169–171

    Article  Google Scholar 

  • Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87–98

    Article  CAS  Google Scholar 

  • Wild C, Jantzen C, Struck U, Hoegh-Guldberg O, Huettel M (2008) Biogeochemical responses following coral mass spawning on the Great Barrier Reef: pelagic-benthic coupling. Coral Reefs 27:123–132

    Article  Google Scholar 

  • Willis BL, Page C, Dinsdale EA (2004) Coral disease on the Great Barrier Reef. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Berlin, pp 69–104

    Google Scholar 

  • Yahel G, Sharp JH, Marie D, Hase C, Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: bulk DOC is the major source for carbon. Limnol Oceanogr 48:141–149

    Article  Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank the participants of the Line Islands Expedition and the San Diego Coral Club for their helpful discussions, criticisms, and insights.

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Correspondence to Elizabeth A. Dinsdale .

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Dinsdale, E.A., Rohwer, F. (2011). Fish or Germs? Microbial Dynamics Associated with Changing Trophic Structures on Coral Reefs. In: Dubinsky, Z., Stambler, N. (eds) Coral Reefs: An Ecosystem in Transition. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0114-4_16

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