Abstract
Nubbins of the coral Acropora aspera were artificially bleached and nitrogen fixation (acetylene reduction) rates were measured on the developing epilithic communities. Seasonal comparisons were made between corals that died in summer of heat stress and corals that died in winter from natural cold stress. Rates of acetylene reduction from artificially bleached corals peaked at 26.66 nmol cm−2 h−1 2 weeks after summer mortality, while rates from natural winter mortality peaked at 18.07 nmol cm−2 h−1 12 days after coral death. Comparative rates of acetylene reduction taken from live corals and coral rubble ranged between 0.56 and 1.16 nmol cm−2 h−1, and 0.15 and 12.77 nmol cm−2 h−1, respectively. N2-fixation rates from dead corals were up to 30 times greater than those measured on live corals. The observed increase in N2-fixation from dead corals may increase the availability of nitrogen for use in trophic processes within the reef for an extended period following the initial mortality event. If the spatial scale over which coral mortality has occurred in past thermal bleaching events is considered the ramifications of such an increase may be substantial.
References
Alongi DM, Pfitzner J, Trott LA (2006) Deposition and cycling of carbon and nitrogen in carbonate mud of the lagoons of Arlington and Sudbury Reefs, Great Barrier Reef. Coral Reefs 25:123–143
Banner AH (1974) Kaneohe Bay, Hawaii: urban pollution and a coral reef ecosystem. Proc 2nd Int Coral Reef Symp 1:685–702
Bianchi TE, Engelhaupt E, Westman P, Andren T, Rolff C, Elmgren W (2000) Cyanobacterial blooms in the Baltic Sea: natural or human induced? Limnol Oceanogr 45:716–726
Breitbarth E, Mills MM, Friedrichs G, LaRoche J (2004) The Bunsen Gas solubility coefficient of ethylene as a function of temperature and salinity and its importance for Nitrogen fixation assays. Limnol Oceanogr Methods 2:282–288
Brodie J, Furnas MJ (1996) Cyclones, river flood plumes and natural water quality extremes in the central Great Barrier Reef. In: Eyles AG, Hunter HM, Rayment GE (eds) Proceeding of the Conference on Downstream Effects of Land Use, Rockhampton. Queensland Department of Primary Industries, Brisbane, pp 367–374
Bunn SE, Loneragan NR, Kempster MA (1995) Effects of acid washing on stable isotope ratios of C and N in Penaeid shrimp and seagrass: implications for food web studies using multiple stable isotopes. Limnol Oceanogr 40:622–625
Capone D, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar Ecol Prog Ser 80:75–88
Charpy-Roubaud C, Charpy L, Sarazin G (1996) Diffusional nutrient fluxes at the sediment-water interface and organic matter mineralization in an atoll lagoon (Tikehau, Tuamotu Archipelago, French Polynesia). Mar Ecol Prog Ser 132:181–190
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 139:991–997
Clapcott JE, Bunn SE (2003) Can C4 plants contribute to aquatic food webs of subtropical streams. Freshw Biol 48:1105–1116
Costa OS, Leao Z, Nimmo M, Attrill MJ (2000) Nutrification impacts on coral reefs from northern Bahia, Brazil. Hydrobiologia 440:307–315
Crossland CJ, Barnes DJ (1976) Acetylene reduction by coral skeletons. Limnol Oceanogr 1:153–156
Davey AM (2006) Changes in bacterial communities, carbon and nitrogen dynamics on coral surfaces following mortality: potential implications for reef systems. Ph.D. thesis, University of Queensland, p 241
Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132
Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116
Furnas MJ, Mitchell M, Skuza M, Brodie J (2005) In the other 90%: phytoplankton response to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar Pollut Bull 51:253–265
Gourlay MR, Colleter G (2005) Wave-generated flow on coral reefs – an analysis for two-dimensional horizontal reef-tops with steep faces. Coast Eng 52:353–387
Grigg RW, Polovina JJ, Atkinson MJ (1984) Model of a coral reef ecosystem III. Resource limitation, community regulation, fisheries yield and resource management. Coral Reefs 3:23–27
Gu B, Alexander V (1993) Estimation of N2 fixation based on differences in the natural abundance of 15N among freshwater N2-fixing and non N2-fixing algae. Oecologia 96:43–48
Guppy R, Bythell JC (2006) Environmental effects on the surface mucus layer bacterial diversity of the reef coral Montastraea faveolata. Mar Ecol Prog Ser 328:133–142
Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 48:1185–1207
Heikoop JM, Risk MJ, Lazier AV, Edinger EN, Jompa J, Limmon GV, Dunn JJ, Browne DR, Schwarcz HP (2000) Nitrogen-15 signals of anthropogenic nutrient loading in reef corals. Mar Pollut Bull 40:628–636
Hoegh-Goldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoegh-Guldberg O, Fine M, Skirving W, Johnstone R, Dove S, Strong A (2005) Coral bleaching following wintry weather. Limnol Oceanogr 50:265–271
Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge
Hunter CL, Evans CW (1995) Coral reefs in Kaneohe Bay, Hawaii: two centuries of western influence and two decades of data. Bull Mar Sci 57:501–515
Johannes RE, Alberts J, D’Elia CF, Kinzie RA, Pomeroy LR, Sottile W, Wiebe WJ, Marsh JR, Helfrich P, Maqragos J, Meyer J, Smith S, Crabtree D, Roth A, McCloskey LR, Betzer S, Marshall N, Pilson MEQ, Telek G, Clutter RI, DuPaul WD, Webb KL, Wells JM (1972) The metabolism of some coral reef communities: a team study of nutrient and energy flux at Eniwetok. Bioscience 22:541–543
Johnstone RW, Koop K, Larkum AWD (1989) Fluxes of inorganic nitrogen between sediments and water in a coral reef lagoon. Proceedings Limnological Society of New South Wales 110:219–227
Johnstone RW, Koop K, Larkum AWD (1990) Physical aspects of coral reef lagoon sediments in relation to detritus processing and primary productivity. Mar Ecol Prog Ser 66:273–283
Jones K, Stewart WDP (1969) Nitrogen turnover in marine and brackish habitats. IV. Uptake of the extracellular products of the nitrogen-fixing alga Calothrix scopulorum. J Mar Biol Assoc UK 49:701–716
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 JB, Larkum AWD, O’Neil JO, Steven A, Tentori E, Ward S, Williamson J, Yellowlees D (2001) ENCORE: the effect of nutrient enrichment or coral reefs, synthesis of results and conclusions. Mar Pollut Bull 42:91–120
Larkum AWD (1988) High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci. Mar Biol 97:503–506
Larkum AWD, Kennedy IR, Muller WJ (1988) Nitrogen fixation on a coral reef. Mar Biol 98:143–155
Larsson U, Hagstrom A (1982) Fractionated phytoplankton primary production, exudate release and bacterial production in a Baltic eutrophication gradient. Mar Biol 67:57–70
Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2004) Discovery of symbiotic nitrogen-fixing Cyanobacteria in corals. Science 305:997–1000
Mather P, Bennett I (1984) A coral reef handbook: a guide to the flora, fauna and geology of Heron Island and adjacent reefs and cays. Australian Coral Reef Society, Brisbane
Mitchell R, Cuet I (1975) Bacterial attack of coral in polluted water. Microb Ecol 2:227–233
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioSci 27:454–460
Paerl HW (1998) Structure and function of anthropogenically altered microbial communities on coastal waters. Curr Opin Biotechnol 1:296–302
Paerl HW, Prufert LE (1987) Oxygen-poor microzones as potential sites of microbial N2- fixation in nitrogen-depleted aerobic marine waters. Appl Env Micro 53:1078–1087
Paerl HW, Crocker KM, Prufert LME (1987) Limitation of N2-fixation in coastal marine waters: relative importance of molybdenum, iron, phosphorus, and organic matter availability. Limnol Oceanogr 32:525–536
Postgate JR (1982) The fundamentals of Nitrogen fixation. Cambridge University Press, Cambridge
Ritchie KB, Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, New York, pp 259–263
Ryther JH (1969) Photosynthesis and fish production in the sea. Science 166:72–76
Schaffelke B (1999) Short-term nutrient pulses as tools to assess responses of coral reef macroalgae to enhanced nutrient availability. Mar Ecol Prog Ser 182:305–310
Schaffelke B, Klump DW (1998) Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar Ecol Prog Ser 170:96–105
Shashar N, Cohen Y, Loya Y, Sar N (1994a) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral-bacteria interactions. Mar Ecol Prog Ser 111:259–264
Shashar N, Feldstein T, Cohen Y, Loya Y (1994b) Nitrogen fixation (Acetylene-Reduction) on a coral reef. Coral Reefs 13:171–174
Stewart WDP, Fitzgerald GP, Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proc Natl Acad Sci USA 58:2017–2078
Webb KL, DuPaul WD, Wiebe WJ, Sottile W, Johannes RE (1975) Enewetok Atoll: aspects of the nitrogen cycle on a coral reef. Limnol Oceanogr 20:198–210
Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jorgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70
Wilkinson CR (ed) (2000) Status of the coral reefs of the world: 2000. Australian Institute of Marine Sciences, Townsville
Wilkinson CR (ed) (2002) Status of the coral reefs of the world: 2002. Australian Institute of Marine Sciences, Townsville
Wilkinson CR (ed) (2004) Status of the coral reefs of the world: 2004. Australian Institute of Marine Sciences, Townsville
Wilkinson CR, Williams DM, Sammarco PW, Hogg RW, Trott LA (1984) Rates of nitrogen fixation on coral reefs across the continental shelf of the central Great Barrier Reef. Mar Biol 80:255–262
Wilkinson CR, Linden O, Cesar H, Hodgson G, Rubens J, Strong AE (1999) Ecological and socioeconomic impacts of the 1998 coral mortality in the Indian Ocean: an ENSO impact and a warning of future change. Ambio 28:188–196
Williams SL, Carpenter RC (1988) Nitrogen-limited primary productivity of coral reef algal turfs: potential contribution of ammonium excreted by Diadema antillarum. Mar Ecol Prog Ser 47:145–152
Williams SL, Carpenter RC (1997) Grazing effects on nitrogen fixation in coral reef algal turfs. Mar Biol 130:223–231
Williams SL, Carpenter RC (1998) Effects of unidirectional and oscillatory water flow on nitrogen fixation (acetylene reduction) in coral reef algal turfs, Kaneohe Bay, Hawaii. J Exp Mar Biol Ecol 226:293–316
Yamamuro M, Kayanne H (1995) Rapid direct determination of organic carbon and nitrogen in carbonate-bearing sediments with a Yanaco MT-5 CHN analyser. Limnol Oceanogr 40:1001–1005
Acknowledgments
MD would like to thank J. Davy, P. Fisher. A. Grinham and the management and staff of Heron Island Research Station for their assistance during the project. MD especially thanks G. Kerven and R. Diocares for analytical assistance, as well as O. Hoegh-Guldberg, S.K. Davy, I. Tibbetts and O. Pantos for reviewing the manuscript. The authors would also like to acknowledge the financial assistance of the Cooperative Research Centre for Reef Research and the Global Education Fund-World Bank Coral Bleaching Program.
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Davey, M., Holmes, G. & Johnstone, R. High rates of nitrogen fixation (acetylene reduction) on coral skeletons following bleaching mortality. Coral Reefs 27, 227–236 (2008). https://doi.org/10.1007/s00338-007-0316-9
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DOI: https://doi.org/10.1007/s00338-007-0316-9