Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change

Ecology and Evolution

Volumn 4, Issue 9, 2014, Pages 1706-1727

  Cardini, Ulisse ^a   Bednarz, Vanessa N ^a   Foster, Rachel A ^b,d   Wild, Christian ^a,c  

^a LEIBNIZ CENTRE FOR TROPICAL MARINE RESEARCH ZMT   (Germany)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c UNIVERSITY OF BREMEN   (Germany)

^d STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Coral reefs; Cyanobacteria; Deoxygenation; Diazotrophs; Dinitrogen fixation; Eutrophication; Global warming; Ocean acidification; Symbiosis; Ultraviolet radiation stress

Indexed keywords

EID: 84899759206     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1050     Document Type: Article

References (270)

1. Albert, S., J. M. O'Neil, J. W. Udy, K. S. Ahern, C. M. O'Sullivan, and W. C. Dennison 2005. Blooms of the cyanobacterium Lyngbya majuscula in coastal Queensland, Australia: disparate sites, common factors. Mar. Pollut. Bull. 51:428-437.
2. Alongi, D. M., and A. D. McKinnon 2005. The cycling and fate of terrestrially-derived sediments and nutrients in the coastal zone of the Great Barrier Reef shelf. Mar. Pollut. Bull. 51:239-252.
3. Andersson, A. J., K. L. Yeakel, N. R. Bates, and S. J. De Putron 2014. Partial offsets in ocean acidification from changing coral reef biogeochemistry. Nat. Clim. Chang. 4:56-61.
4. Anthony, K. R. N., D. I. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl Acad. Sci. USA 105:17442.
5. Arp, D. J. 2000. The nitrogen cycle. Pp. 1-14 in E. W. Triplett, ed. Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham.
6. Arrigo, K. R. 2005. Marine microorganisms and global nutrient cycles. Nature 437:349-355.
7. Ateweberhan, M., D. A. Feary, S. Keshavmurthy, A. Chen, M. H. Schleyer, and C. R. C. Sheppard 2013. Climate change impacts on coral reefs: synergies with local effects, possibilities for acclimation, and management implications. Mar. Pollut. Bull. 74:526-539.
8. Atkinson, M. J. 2011. Biogeochemistry of nutrients. Pp. 199-206 in Z. Dubinsky and N. Stambler, eds. Coral reefs: an ecosystem in transition. Springer, Netherlands.
9. Banaszak, A. T., and M. P. Lesser 2009. Effects of solar ultraviolet radiation on coral reef organisms. Photochem. Photobiol. Sci. 8:1276-1294.
10. Barcelos, E., J. Ramos, H. Biswas, K. G. Schulz, J. Laroche, and U. Riebesell 2007. Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochem. Cycles 21:GB2028.
11. Barott, K. L., and F. L. Rohwer 2012. Unseen players shape benthic competition on coral reefs. Trends Microbiol. 20:621-628.
12. Barott, K., J. Smith, E. Dinsdale, M. Hatay, S. Sandin, and F. Rohwer 2009. Hyperspectral and physiological analyses of coral-algal interactions. PLoS ONE 4:e8043.
13. Barott, K. L., B. Rodriguez-Mueller, M. Youle, K. L. Marhaver, M. J. A. Vermeij, J. E. Smith, et al. 2012. Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae. Proc. Biol. Sci. 279:1655-1664.
14. Bauer, K., B. Díez, C. Lugomela, S. Seppälä, A. J. Borg, and B. Bergman 2008. Variability in benthic diazotrophy and cyanobacterial diversity in a tropical intertidal lagoon. FEMS Microbiol. Ecol. 63:205-221.
15. Bell, P. R. F., I. Elmetri, and P. Uwins 1999. Nitrogen fixation by Trichodesmium spp. in the Central and Northern Great Barrier Reef Lagoon: relative importance of the fixed-nitrogen load. Mar. Ecol. Prog. Ser., 186:119-126.
16. Berman-Frank, I., P. Lundgren, and P. Falkowski 2003. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 154:157-164.
17. Bertics, V. J., J. A. Sohm, T. Treude, C. E. T. Chow, D. G. Capone, J. A. Fuhrman, et al. 2010. Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction. Mar. Ecol. Prog. Ser. 409:1-15.
18. Bertics, V. J., J. A. Sohm, C. Magnabosco, and W. Ziebis 2012. Denitrification and nitrogen fixation dynamics in the area surrounding an individual ghost shrimp (Neotrypaea californiensis) burrow system. Appl. Environ. Microbiol. 78:3864-3872.
19. Bertics, V. J., C. R. Loescher, I. Salonen, A. W. Dale, J. Gier, R. A. Schmitz, et al. 2013. Occurrence of benthic microbial nitrogen fixation coupled to sulfate reduction in the seasonally hypoxic Eckernforde Bay, Baltic Sea. Biogeosciences 10:1243-1258.
20. Blackburn, T., D. Nedwell, and W. Wiebe 1994. Active mineral cycling in a Jamaican seagrass sediment. Mar. Ecol. Prog. Ser. 110:233-239.
21. Bordeleau, L. M., and D. Prévost 1994. Nodulation and nitrogen fixation in extreme environments. Plant Soil 161:115-125.
22. Breitburg, D. L., D. W. Hondorp, L. A. Davias, and R. J. Diaz 2009. Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Ann. Rev. Mar. Sci. 1:329-349.
23. Burris, R. 1976. Nitrogen fixation by blue-green algae of the lizard island area of the great barrier reef. Funct. Plant Biol. 3:41-51.
24. Caldeira, K., and M. Wickett 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. C: Oceans 110:1-12.
25. Canfield, D. E., A. N. Glazer, and P. G. Falkowski 2010. The evolution and future of earth's nitrogen cycle. Science 330:192-196.
26. Capone, D. 1982. Nitrogen fixation (acetylene reduction) by rhizosphere sediments of the eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 10:67-75.
27. Capone, D. G. 1996. Coral reef ecosystems in the context of the marine nitrogen cycle. Pp. 61-76 in M. Bjork, A. K. Semesi, M. Pederson and B. Bergman, eds. Current trends in marine botanical research in the east African region. SIDA, Marine Science Program, SAREC, Uppsala.
28. Capone, D. G., and E. J. Carpenter 1982. Nitrogen fixation in the marine environment. Science 217:1140-1142.
29. 2 fixation in the rhizosphere of Thalassia testudinum. Can. J. Microbiol. 26:998-1005.
30. Capone, D. G., D. L. Taylor, and B. F. Taylor 1977. Nitrogen-fixation (acetylene reduction) associated with macroalgae in a coral reef community in Bahamas. Mar. Biol. 40:29-32.
31. 2) fixation in a Thalassia testudinum Community. Limnol. Oceanogr. 24:117-125.
32. Capone, D. G., S. E. Dunham, S. G. Horrigan, and L. E. Duguay 1992. Microbial nitrogen transformations in unconsolidated coral-reef sediments. Mar. Ecol. Prog. Ser. 80:75-88.
33. Carpenter, E. J., and D. G. Capone 2008. Nitrogen fixation in the marine environment. Pp. 141-198 in D. G. Capone, D. A. Bronk, M. R. Mulholland and E. J. Carpenter, eds. Nitrogen in the marine environment, 2nd ed. Academic Press, San Diego.
34. Carpenter, E. J., and R. A. Foster 2002. Marine cyanobacterial symbioses. Pp. 11-17 in A. N. Rai, B. Bergman and U. Rasmussen, eds. Cyanobacteria in symbiosis. Springer, Netherlands.
35. Ceh, J., M. R. Kilburn, J. B. Cliff, J.-B. Raina, M. Van Keulen, and D. G. Bourne 2013. Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol. Evol. 3:2393-2400.
36. Charpy, L., R. Alliod, M. Rodier, and S. Golubic 2007. Benthic nitrogen fixation in the SW New Caledonia lagoon. Aquat. Microb. Ecol. 47:73-81.
37. Charpy, L., B. E. Casareto, M. J. Langlade, and Y. Suzuki 2012a. Cyanobacteria in coral reef ecosystems: a review. J. Mar. Biol. 2012:259571.
38. Charpy, L., K. A. Palinska, R. M. M. Abed, M. J. Langlade, and S. Golubic 2012b. Factors influencing microbial mat composition, distribution and dinitrogen fixation in three western Indian Ocean coral reefs. Eur. J. Phycol. 47:51-66.
39. Charpy-Roubaud, C., and A. W. D. Larkum 2005. Dinitrogen fixation by exposed communities on the rim of Tikehau atoll (Tuamotu Archipelago, French Polynesia). Coral Reefs 24:622-628.
40. Charpy-Roubaud, C., L. Charpy, and A. W. D. Larkum 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.
41. Chisholm, J. R., and P. Moulin 2003. Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol. Oceanogr. 48:787-794.
42. Codispoti, L. A. 2007. An oceanic fixed nitrogen sink exceeding 400 Tg Na-1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4:233-253.
43. Codispoti, L. A., J. A. Brandes, J. P. Christensen, A. H. Devol, S. W. A. Naqvi, H. W. Paerl, et al. 2001. The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci. Mar. 65:85-105.
44. Conley, D., J. Carstensen, R. Vaquer-Sunyer, and C. Duarte 2009. Ecosystem thresholds with hypoxia. Pp. 21-29 in J. H. Andersen and D. J. Conley, eds. Eutrophication in coastal ecosystems. Springer, Netherlands.
45. Corredor, J. E., and J. Morell 1985. Inorganic nitrogen in coral reef sediments. Mar. Chem. 16:379-384.
46. Crossland, C. J., and D. J. Barnes 1976. Acetylene reduction by coral skeletons. Limnol. Oceanogr. 21:153-156.
47. Davey, M., G. Holmes, and R. Johnstone 2008. High rates of nitrogen fixation (acetylene reduction) on coral skeletons following bleaching mortality. Coral Reefs 27:227-236.
48. de Oliveira, L. S., G. B. Gregoracci, G. G. Z. Silva, L. T. Salgado, A. Gilberto Filho, M. A. Alves-Ferreira et al. 2012. Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genom. 13:487.
49. De'ath, G., J. Lough, and K. Fabricius 2009. Declining coral calcification on the Great Barrier Reef. Science 323:116-119.
50. Dekas, A. E., and V. Orphan 2011. Methane-stimulated benthic marine nitrogen fixation at deep-sea methane seeps. Proceedings of AGU fall meeting. Abstract #B33I-07, San Francisco, CA.
51. Dekas, A. E., R. S. Poretsky, and V. J. Orphan 2009. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326:422-426.
52. Deutsch, C., J. L. Sarmiento, D. M. Sigman, N. Gruber, and J. P. Dunne 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445:163-167.
53. Diaz, M. C., and B. B. Ward 1997. Sponge-mediated nitrification in tropical benthic communities. Mar. Ecol. Prog. Ser. 156:97-107.
54. Drollet, J., M. Faucon, and P. Martin 1995. Elevated sea-water temperature and solar UV-B flux associated with two successive coral mass bleaching events in Tahiti. Mar. Freshw. Res. 46:1153-1157.
55. Dugdale, R. C., and J. J. Goering 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Limnol. Oceanogr. 12:196-206.
56. Erwin, P. M., L. Pita, S. López-Legentil, and X. Turon 2012. Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl. Environ. Microbiol. 78:7358-7368.
57. Eyre, B. D., R. N. Glud, and N. Patten 2008. Mass coral spawning: a natural large-scale nutrient addition experiment. Limnol. Oceanogr. 53:997-1013.
58. Fabricius, K. E., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. De'ath, et al. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Chang. 1:165-169.
59. Falkowski, P. G., Z. Dubinsky, L. Muscatine, and L. McCloskey 1993. Population control in symbiotic corals. Bioscience 43:606-611.
60. Falkowski, P., R. J. Scholes, E. Boyle, J. Canadell, D. Canfield, J. Elser, et al. 2000. The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291-296.
61. Farnelid, H., A. F. Andersson, S. Bertilsson, W. A. Al-Soud, L. H. Hansen, S. Sørensen, et al. 2011. Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS ONE 6:e19223.
62. Fernandez, C., L. Farías, and O. Ulloa 2011. Nitrogen fixation in denitrified marine waters. PLoS ONE 6:e20539.
63. Ferrer, L., and A. Szmant 1988. Nutrient regeneration by the endolithic community in coral skeletons. Pp. 1-4 in J. H. Choat, D. Barnes, M. A. Borowitzka, J. C. Coll, P. J. Davies, P. Flood, B. G. Hatcher, D. Hopley, P. A. Hutchings, D. Kinsey, G. R. Orme, M. Pichon, P. F. Sale, P. Sammarco, C. C. Wallace, C. Wilkinson, E. Wolanski and O. Bellwood, eds. Proceedings of the 6th International Coral Reef Symposium. Vol. 3: Contributed Papers, Townsville, Australia.
64. Ferrier-Pagès, C., J. Witting, E. Tambutté, and K. P. Sebens 2003. Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229-240.
65. Fine, M., and Y. Loya 2002. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. Biol. Sci. 269:1205-1210.
66. Fine, M., E. Meroz-Fine, and O. Hoegh-Guldberg 2005. Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J. Exp. Biol. 208:75-81.
67. Fiore, C. L., J. K. Jarett, N. D. Olson, and M. P. Lesser 2010. Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol. 18:455-463.
68. Foster, R. A., and G. D. O'Mullan 2008. Nitrogen-fixing and nitrifying symbioses in the marine environment. Pp. 1197-1218 in D. G. Capone, D. A. Bronk, M. R. Mulholland and E. J. Carpenter, eds. Nitrogen in the marine environment, 2nd ed. Academic Press, San Diego.
69. 15N evidence for nitrogen fixation associated with macroalgae from a seagrass-mangrove coral reef system. Mar. Ecol. Prog. Ser. 167:297-299.
70. Frias-Lopez, J., A. L. Zerkle, G. T. Bonheyo, and B. W. Fouke 2002. Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl. Environ. Microbiol. 68:2214-2228.
71. Frieler, K., M. Meinshausen, A. Golly, M. Mengel, K. Lebek, S. D. Donner, et al. 2013. Limiting global warming to 2 degrees C is unlikely to save most coral reefs. Nat. Clim. Chang. 3:165-170.
72. 2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera. Limnol. Oceanogr. 53:2472-2484.
73. Galloway, J. N., W. H. Schlesinger, H. Levy, A. Michaels, and J. L. Schnoor 1995. Nitrogen fixation: anthropogenic enhancement-environmental response. Global Biogeochem. Cycles 9:235-252.
74. Galloway, J. N., J. D. Aber, J. W. Erisman, S. P. Seitzinger, R. W. Howarth, E. B. Cowling, et al. 2003. The nitrogen cascade. Bioscience 53:341-356.
75. Galloway, J. N., F. J. Dentener, D. G. Capone, E. W. Boyer, R. W. Howarth, S. P. Seitzinger, et al. 2004. Nitrogen cycles: past, present, and future. Biogeochemistry 70:153-226.
76. 2 fization in the diazotroph Trichodesmium erythraeum (Cyanobacteria). J. Phycol. 47:1292-1303.
77. 2-fixing cyanobacterium Crocosphaera watsonii from the western tropical Atlantic Ocean. Eur. J. Phycol. 48:128-139.
78. Garrard, S., R. Hunter, A. Frommel, A. Lane, J. Phillips, R. Cooper, et al. 2012. Biological impacts of ocean acidification: a postgraduate perspective on research priorities. Mar. Biol. 160:1789-1805.
79. Garren, M., and F. Azam 2012. New directions in coral reef microbial ecology. Environ. Microbiol. 14:833-844.
80. Gattuso, J. P., M. Frankignoulle, and R. Wollast 1998. Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu. Rev. Ecol. Syst. 29:405-434.
81. Goldshmid, R., R. Holzman, D. Weihs, and A. Genin 2004. Aeration of corals by sleep-swimming fish. Limnol. Oceanogr. 49:1832-1839.
82. Großkopf, T., and J. Laroche 2012. Direct and indirect costs of dinitrogen fixation in Crocosphaera watsonii WH8501 and possible implications for the nitrogen cycle. Philos. Trans. A Math. Phys. Eng. Sci. 3:236.
83. Großkopf, T., W. Mohr, T. Baustian, H. Schunck, D. Gill, M. M. M. Kuypers, et al. 2012. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488:361-364.
84. Grover, R., J.-F. Maguer, S. Reynaud-Vaganay, and C. Ferrier-Pages 2002. Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 47:782-790.
85. Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pages 2003. Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol. Oceanogr. 48:2266-2274.
86. Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pagès 2006. Urea uptake by the scleractinian coral Stylophora pistillata. J. Exp. Mar. Biol. Ecol. 332:216-225.
87. Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pagès 2008. Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J. Exp. Biol. 211:860-865.
88. 2. Pp. 97-148 in T. Oguz and M. Follows, eds. Carbon climate interactions. Kluwer, Dordrecht.
89. Gruber, N. 2005. Oceanography: a bigger nitrogen fix. Nature 436:786-787.
90. Gruber, N. 2008. The marine nitrogen cycle: overview and challenges. Pp. 1-50 in D. G. Capone, D. A. Bronk, M. R. Mulholland and E. J. Carpenter, eds. Nitrogen in the marine environment, 2nd ed. Academic Press, San Diego.
91. Gruber, N. 2011. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos. Trans. A Math. Phys. Eng. Sci. 369:1980-1996.
92. Gruber, N., and J. N. Galloway 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451:293-296.
93. Guzmán, H., J. Cortés, P. Glynn, and R. Richmond 1990. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar. Ecol. Prog. Ser. Oldendorf 60:299-303.
94. Haas, A. F., J. E. Smith, M. Thompson, and D. D. Deheyn 2014. Effects of reduced dissolved oxygen concentrations on physiology and fluorescence of hermatypic corals and benthic algae. PeerJ 2:e235.
95. Hall-Spencer, J. M., R. Rodolfo-Metalpa, S. Martin, E. Ransome, M. Fine, S. M. Turner, et al. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96-99.
96. Hamersley, M. R., K. A. Turk, A. Leinweber, N. Gruber, J. P. Zehr, T. Gunderson, et al. 2011. Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat. Microb. Ecol. 63:193-205.
97. Hamisi, M. I., T. J. Lyimo, M. H. S. Muruke, and B. Bergman 2009. Nitrogen fixation by epiphytic and epibenthic diazotrophs associated with seagrass meadows along the Tanzanian coast, Western Indian Ocean. Aquat. Microb. Ecol. 57:33-42.
98. Harnik, P. G., H. K. Lotze, S. C. Anderson, Z. V. Finkel, S. Finnegan, D. R. Lindberg, et al. 2012. Extinctions in ancient and modern seas. Trends Ecol. Evol. 27:608-617.
99. Hegglin, M. I., and T. G. Shepherd 2009. Large climate-induced changes in ultraviolet index and stratosphere-to-troposphere ozone flux. Nat. Geosci. 2:687-691.
100. Hewson, I., and J. A. Fuhrman 2006. Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities. Mar. Ecol. Prog. Ser. 306:79-86.
101. Hilting, A., C. Currin, and R. Kosaki 2013. Evidence for benthic primary production support of an apex predator-dominated coral reef food web. Mar. Biol. 160:1681-1695.
102. Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50:839-866.
103. Hoegh-Guldberg, O. 2011. Coral reef ecosystems and anthropogenic climate change. Reg. Environ. Change 11:215-227.
104. Hoegh-Guldberg, O., P. Mumby, A. Hooten, R. Steneck, P. Greenfield, E. Gomez, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742.
105. Hoffmann, F., R. Radax, D. Woebken, M. Holtappels, G. Lavik, H. T. Rapp, et al. 2009. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11:2228-2243.
106. Hofmann, G. E., J. E. Smith, K. S. Johnson, U. Send, L. A. Levin, F. Micheli, et al. 2011. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6:e28983.
107. Holl, C. M., and J. P. Montoya 2005. Interactions between Nitrate uptake and Nitrogen fixation in continuous cultures of the marine diazotroph Trichodesmium (Cyanobacteria). J. Phycol. 41:1178-1183.
108. Howarth, R. W., and R. Marino 2006. Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol. Oceanogr. 51:364-376.
109. Howarth, R. W., R. Marino, and J. J. Cole 1988. Nitrogen-fixation in fresh-water, estuarine and marine ecosystems. 2. Biogeochemical controls. Limnol. Oceanogr. 33:688-701.
110. Howarth, R. W., H. S. Jensen, R. Marino, and H. Postma 1995. Transport to and processing of P in near-shore and oceanic waters. Pp. 323-345, vol. 54. in H. Tiessen, ed. Phosphorus in the global environment. Transfers, cycles and management. Scope. Wiley, New York, NY.
111. Howarth, R. W., G. Billen, D. Swaney, A. Townsend, N. Jaworski, K. Lajtha, et al. 1996. Regional nitrogen budgets and riverine N&P fluxes for the drainages to the North Atlantic Ocean: natural and human influences. Biogeochemistry 35:75-139.
112. Hughes, T. P., M. J. Rodrigues, D. R. Bellwood, D. Ceccarelli, O. Hoegh-Guldberg, L. McCook, et al. 2007. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17:360-365.
113. Hughes, T. P., Graham. NaJ, J. B. C. Jackson, P. J. Mumby, and R. S. Steneck 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25:633-642.
114. 2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52:1293-1304.
115. 2-enriched ocean. Oceanography 22:128-145.
116. Iizumi, H., and M. Yamamuro 2000. Nitrogen fixation activity by periphytic blue-green algae in a seagrass bed on the Great Barrier Reef. Jpn. Agric. Res. Q. 34:69-73.
117. IPCC 2007. Climate change 2007: The physical science basis. Contribution of working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge Univ. Press, Cambridge, U.K. and New York, NY.
118. Jessen, C., C. Roder, J. F. Villa Lizcano, C. R. Voolstra, and C. Wild 2013. In-Situ effects of simulated overfishing and eutrophication on benthic coral reef algae growth, succession, and composition in the central red sea. PLoS ONE 8:e66992.
119. Joint, I., S. C. Doney, and D. M. Karl 2011. Will ocean acidification affect marine microbes? ISME J. 5:1-7.
120. Karl, D., A. Michaels, B. Bergman, D. Capone, E. Carpenter, R. Letelier, et al. 2002. Dinitrogen fixation in the world's oceans. Biogeochemistry 57:47-98.
121. 2 inventory associated with recent global warming. Proc. Natl Acad. Sci. 99:7848-7853.
122. Keeling, R. F., A. Körtzinger, and N. Gruber 2010. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2:199-229.
123. Kerr, J. B., and C. T. McElroy 1993. Evidence for large upward trends of ultraviolet-b radiation linked to ozone depletion. Science 262:1032-1034.
124. Kiers, E. T., T. M. Palmer, A. R. Ives, J. F. Bruno, and J. L. Bronstein 2010. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13:1459-1474.
125. Kinsey, D., and E. Kinsey 1967. Diurnal changes in oxygen content of the water over the coral reef platform at Heron I. Mar. Freshw. Res. 18:23-34.
126. Kleypas, J. A., and K. K. Yates 2009. Coral reefs and ocean acidification. Oceanography 22:108-117.
127. Kneip, C., P. Lockhart, C. Vosz, and U.-G. Maier 2007. Nitrogen fixation in eukaryotes - New models for symbiosis. BMC Evol. Biol. 7:55.
128. Knowlton, N. 2001. The future of coral reefs. Proc. Natl Acad. Sci. 98:5419-5425.
129. Knowlton, N., and J. B. C. Jackson 2008. Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol. 6:e54.
130. Knowlton, N., and F. Rohwer 2003. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am. Nat. 162:S51-S62.
131. Koop, K., D. Booth, A. Broadbent, J. Brodie, D. Bucher, D. Capone, et al. 2001. ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull. 42:91-120.
132. Kopp, C., M. Pernice, I. Domart-Coulon, C. Djediat, J. E. Spangenberg, D. T. L. Alexander, et al. 2013. Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. MBio 4:e00052-13.
133. 2 and diurnal changes. Limnol. Oceanogr. 54:548-559.
134. 2 and light on the N-2-fixing cyanobacterium trichodesmium IMS101: physiological responses. Plant Physiol. 154:334-345.
135. Krediet, C. J., K. B. Ritchie, V. J. Paul, and M. Teplitski 2013. Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc. Biol. Sci., 280:20122328.
136. Kuffner, I. B., and V. J. Paul 2004. Effects of the benthic cyanobacterium Lyngbya majuscula on larval recruitment of the reef corals Acropora surculosa and Pocillopora damicornis. Coral Reefs 23:455-458.
137. Kuffner, I., L. Walters, M. Becerro, V. Paul, R. Ritson-Williams, and K. Beach 2006. Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar. Ecol. Prog. Ser. 323:107-117.
138. 2, pH and light. Mar. Ecol. Prog. Ser. 117:159-172.
139. Kumar, A., M. B. Tyagi, P. N. Jha, G. Srinivas, and A. Singh 2003. Inactivation of cyanobacterial nitrogenase after exposure to ultraviolet-b radiation. Curr. Microbiol. 46:0380-0384.
140. Kustka, A., E. J. Carpenter, and S. A. Sañudo-Wilhelmy 2002. Iron and marine nitrogen fixation: progress and future directions. Res. Microbiol. 153:255-262.
141. Kvennefors, E. C. E., and G. Roff 2009. Evidence of cyanobacteria-like endosymbionts in Acroporid corals from the Great Barrier Reef. Coral Reefs 28:547.
142. Lapointe, B. E., P. J. Barile, and W. R. Matzie 2004. Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources. J. Exp. Mar. Biol. Ecol. 308:23-58.
143. Larkum, A. W. D. 1988. High rates of nitrogen fixation on coral skeletons after predation by the crown of thorns starfish Acanthaster planci. Mar. Biol. 97:503-506.
144. Larkum, A. W. D., I. R. Kennedy, and W. J. Muller 1988. Nitrogen fixation on a coral reef. Mar. Biol. 98:143-155.
145. 2 in the South Pacific. Glob. Change Biol. 18:3004-3014.
146. Le Campion-Alsumard, T., S. Golubic, and P. Hutchings 1995. Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar. Ecol. Prog. Ser. 117:149-157.
147. Lema, K. A., B. L. Willis, and D. G. Bourne 2012. Corals form characteristic associations with symbiotic nitrogen-fixing bacteria. Appl. Environ. Microbiol. 78:3136-3144.
148. Lema, K. A., B. L. Willis, and D. G. Bourne 2014. Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ. Microbiol. Early View. doi:10.1111/1462-2920.12366.
149. Lesser, M. P. 2008. Effects of ultraviolet radiation on productivity and nitrogen fixation in the Cyanobacterium, Anabaena sp. (Newton's strain). Hydrobiologia 598:1-9.
150. Lesser, M. P., C. H. Mazel, M. Y. Gorbunov, and P. G. Falkowski 2004. Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:997-1000.
151. Lesser, M. P., L. I. Falcon, A. Rodriguez-Roman, S. Enriquez, O. Hoegh-Guldberg, and R. Iglesias-Prieto 2007. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346:143-152.
152. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob. Change Biol. 13:531-538.
153. 2 concentrations. Environ. Microbiol. 12:1899-1912.
154. 2 and light on the N-2-fixing cyanobacterium trichodesmium IMS101: a mechanistic view. Plant Physiol. 154:346-356.
155. Liu, J., M. G. Weinbauer, C. Maier, M. Dai, and J. P. Gattuso 2010. Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquat. Microb. Ecol. 61:291-305.
156. Lomas, M. W., B. M. Hopkinson, J. L. Losh, D. E. Ryan, D. L. Shi, Y. Xu, et al. 2012. Effect of ocean acidification on cyanobacteria in the subtropical North Atlantic. Aquat. Microb. Ecol. 66:211-222.
157. Madronich, S., R. L. McKenzie, L. O. Björn, and M. M. Caldwell 1998. Changes in biologically active ultraviolet radiation reaching the Earth's surface. J. Photochem. Photobiol., B 46:5-19.
158. 2 fixation. Am. J. Sci. 305:546-595.
159. 2 exchange between the ocean and atmosphere in a tropical coral reef environment. Aquat. Geochem. 18:357-386.
160. Mazard, S. L., N. J. Fuller, K. M. Orcutt, O. Bridle, and D. J. Scanlan 2004. PCR analysis of the distribution of unicellular cyanobacterial diazotrophs in the Arabian sea. Appl. Environ. Microbiol. 70:7355-7364.
161. McFall-Ngai, M., M. G. Hadfield, T. C. G. Bosch, H. V. Carey, T. Domazet-Lošo, A. E. Douglas, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. 110:3229-3236.
162. McGlathery, K. J., N. Risgaard-Petersen, and P. B. Christensen 1998. Temporal and spatial variation in nitrogen fixation activity in the eelgrass Zostera marina rhizosphere. Mar. Ecol. Prog. Ser. 168:245-258.
163. McRoy, C. P., J. J. Goering, and B. Chaney 1973. Nitrogen fixation associated with seagrasses. Limnol. Oceanogr. 18:998-1002.
164. Mehta, M. P., and J. A. Baross 2006. Nitrogen fixation at 92°C by a hydrothermal vent archaeon. Science 314:1783-1786.
165. Mehta, M. P., D. A. Butterfield, and J. A. Baross 2003. Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the juan de fuca ridge. Appl. Environ. Microbiol. 69:960-970.
166. Meron, D., E. Atias, L. I. Kruh, H. Elifantz, D. Minz, M. Fine, et al. 2011. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5:51-60.
167. Mills, M., F. Lipschultz, and K. Sebens 2004a. Particulate matter ingestion and associated nitrogen uptake by four species of scleractinian corals. Coral Reefs 23:311-323.
168. Mills, M. M., C. Ridame, M. Davey, J. La Roche, and R. J. Geider 2004b. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292-294.
169. Miyajima, T., M. Suzumura, Y. Umezawa, and I. Koike 2001. Microbiological nitrogen transformation in carbonate sediments of a coral-reef lagoon and associated seagrass beds. Mar. Ecol. Prog. Ser. 217:273-286.
170. Mohamed, N. M., A. S. Colman, Y. Tal, and R. T. Hill 2008. Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ. Microbiol. 10:2910-2921.
171. Mohamed, N. M., K. Saito, Y. Tal, and R. T. Hill 2009. Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J. 4:38-48.
172. Mohr, W., T. Großkopf, D. W. R. Wallace, and J. Laroche 2010. Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE 5:e12583.
173. 2 fixation domain. Science 327:1512-1514.
174. 2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430:1027-1032.
175. Moriarty, D., and M. O'Donohue 1993. Nitrogen fixation in seagrass communities during summer in the Gulf of Carpentaria, Australia. Mar. Freshw. Res. 44:117-127.
176. Moutin, T., N. V. D. Broeck, B. Beker, C. Dupouy, P. Rimmelin, and A. L. Bouteiller 2005. Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean. Mar. Ecol. Prog. Ser. 297:15-21.
177. Mulholland, M. R., K. Ohki, and D. G. Capone 2001. Nutrient controls on Nitrogen uptake and metabolism by natural populations and cultures of Trichodesmium (Cyanobacteria). J. Phycol. 37:1001-1009.
178. Needoba, J. A., R. A. Foster, C. Sakamoto, J. P. Zehr, and K. S. Johnson 2007. Nitrogen fixation by unicellular diazotrophic cyanobacteria in the temperate oligotrophic North Pacific Ocean. Limnol. Oceanogr. 52:1317-1327.
179. Nielsen, L. B., K. Finster, D. T. Welsh, A. Donelly, R. A. Herbert, R. De Wit, et al. 2001. Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environ. Microbiol. 3:63-71.
180. O'Donohue, M. J., D. J. W. Moriarty, and I. C. M. Rae 1991. Nitrogen fixation in sediments and the rhizosphere of the seagrass Zostera capricorni. Microb. Ecol. 22:53-64.
181. Olson, N. D., T. D. Ainsworth, R. D. Gates, and M. Takabayashi 2009. Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J. Exp. Mar. Biol. Ecol. 371:140-146.
182. O'Neil, J. M., and D. Capone 1989. Nitrogenase activity in tropical carbonate marine sediments. Mar. Ecol. Prog. Ser. 56:145-156.
183. O'Neil, J. M., and D. G. Capone 2008. Nitrogen cycling in coral reef environments. Pp. 949-989 in D. G. Capone, D. A. Bronk, M. R. Mulholland and E. J. Carpenter, eds. Nitrogen in the marine environment, 2nd ed. Academic Press, San Diego.
184. O'Neil, J. M., T. W. Davis, M. A. Burford, and C. J. Gobler 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313-334.
185. Paerl, H. W. 1997. Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnol. Oceanogr. 42:1154-1165.
186. Paerl, H. W., and J. Huisman 2008. Climate - Blooms like it hot. Science 320:57-58.
187. Paerl, H. W., and J. Huisman 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1:27-37.
188. Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418-422.
189. Pastorok, R. A., and G. R. Bilyard 1985. Effects of sewage pollution on coral-reef communities. Mar. Ecol. Prog. Ser. Oldendorf 21:175-189.
190. Patriquin, D., and R. Knowles 1972. Nitrogen fixation in the rhizosphere of marine angiosperms. Mar. Biol. 16:49-58.
191. Paul, V. J., R. W. Thacker, K. Banks, and S. Golubic 2005. Benthic cyanobacterial bloom impacts the reefs of South Florida (Broward County, USA). Coral Reefs 24:693-697.
192. Pernice, M., A. Meibom, A. Van Den Heuvel, C. Kopp, I. Domart-Coulon, O. Hoegh-Guldberg, et al. 2012. A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J. 6:1314-1324.
193. Porzio, L., M. C. Buia, and J. M. Hall-Spencer 2011. Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400:278-287.
194. Ralph, P., A. Larkum, and M. Kühl 2007. Photobiology of endolithic microorganisms in living coral skeletons: 1. Pigmentation, spectral reflectance and variable chlorophyll fluorescence analysis of endoliths in the massive corals Cyphastrea serailia, Porites lutea and Goniastrea australensis. Mar. Biol. 152:395-404.
195. Rao, A. M. F., and M. A. Charette 2012. Benthic nitrogen fixation in an eutrophic estuary affected by groundwater discharge. J. Coastal Res. 28:477-485.
196. Rees, A. P. 2012. Pressures on the marine environment and the changing climate of ocean biogeochemistry. Philos. Trans. A Math. Phys. Eng. Sci. 370:5613-5635.
197. Riemann, L., H. Farnelid, and G. F. Steward 2010. Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat. Microb. Ecol. 61:225-237.
198. Rijkenberg, M. J. A., R. J. Langlois, M. M. Mills, M. D. Patey, P. G. Hill, M. C. Nielsdóttir, et al. 2011. Environmental forcing of nitrogen fixation in the eastern tropical and sub-tropical North Atlantic Ocean. PLoS ONE 6:e28989.
199. Robson, R. L., and J. R. Postgate 1980. Oxygen and hydrogen in biological nitrogen fixation. Annu. Rev. Microbiol. 34:183-207.
200. Rohwer, F., M. Breitbart, J. Jara, F. Azam, and N. Knowlton 2001. Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85-91.
201. Rohwer, F., V. Seguritan, F. Azam, and N. Knowlton 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1-10.
202. Rosenberg, E., and Y. Loya 2004. Coral health and disease. Springer, Berlin.
203. Rosenberg, G., and H. W. Paerl 1981. Nitrogen fixation by blue-green algae associated with the siphonous green seaweed Codium decorticatum: effects on ammonium uptake. Mar. Biol. 61:151-158.
204. Salihoglu, B., S. Neuer, S. Painting, R. Murtugudde, E. E. Hofmann, J. H. Steele, et al. 2012. Bridging marine ecosystem and biogeochemistry research: lessons and recommendations from comparative studies. J. Mar. Syst. 109-110:161-175.
205. Sarmiento, J. L., T. M. C. Hughes, R. J. Stouffer, and S. Manabe 1998. Simulated response of the ocean carbon cycle to anthropogenic climate warming. Nature 393:245-249.
206. Schläppy, M.-L., S. Schöttner, G. Lavik, M. M. Kuypers, D. Beer, and F. Hoffmann 2010. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar. Biol. 157:593-602.
207. Schlesinger, W. H. 2009. On the fate of anthropogenic nitrogen. Proc. Natl Acad. Sci. 106:203-208.
208. Shashar, N., Y. Cohen, and Y. Loya 1993. Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol. Bull. 185:455-461.
209. Shashar, N., Y. Cohen, Y. Loya, and N. Sar 1994a. Nitrogen-fixation (acetylene reduction) in stony corals - evidence for coral-bacteria interactions. Mar. Ecol. Prog. Ser. 111:259-264.
210. Shashar, N., T. Feldstein, Y. Cohen, and Y. Loya 1994b. Nitrogen-fixation (acetylene reduction) on a coral reef. Coral Reefs 13:171-174.
211. Shi, D. L., Y. Xu, B. M. Hopkinson, and F. M. M. Morel 2010. Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676-679.
212. Shi, D., S. A. Kranz, J.-M. Kim, and F. M. M. Morel 2012. Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions. Proc. Natl Acad. Sci. 109:E3094-E3100.
213. Shick, J. M., M. P. Lesser, and P. L. Jokiel 1996. Effects of ultraviolet radiation on corals and other coral reef organisms. Glob. Change Biol. 2:527-545.
214. Short, F., W. Dennison, and D. Capone 1990. Phosphorus-limited growth of the tropical seagrass Syringodium filiforme in carbonate sediments. Mar. Ecol. Prog. Ser. Oldendorf 62:169-174.
215. Simpson, C. J., J. L. Cary, and R. J. Masini 1993. Destruction of corals and other reef animals by coral spawn slicks on Ningaloo Reef, Western Australia. Coral Reefs 12:185-191.
216. Singh, S. P., D.-P. Häder, and R. P. Sinha 2010. Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res. Rev. 9:79-90.
217. Smith, S. V. 1984. Phosphorus versus nitrogen limitation in the marine environment. Limnol. Oceanogr. 29:1149-1160.
218. Smith, J. E., M. Shaw, R. A. Edwards, D. Obura, O. Pantos, E. Sala, et al. 2006. Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol. Lett. 9:835-845.
219. Sohm, J. A., J. A. Hilton, A. E. Noble, J. P. Zehr, M. A. Saito, and E. A. Webb 2011a. Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System. Geophys. Res. Lett. 38:L16608.
220. Sohm, J. A., E. A. Webb, and D. G. Capone 2011b. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9:499-508.
221. Stal, L. J. 2009. Is the distribution of nitrogen-fixing cyanobacteria in the oceans related to temperature? Environ. Microbiol. 11:1632-1645.
222. Stambler, N. 2011. Zooxanthellae: the yellow symbionts inside animals. Pp. 87-106 in Z. Dubinsky and N. Stambler, eds. Coral reefs: an ecosystem in transition. Springer, Netherlands.
223. Steckbauer, A., C. M. Duarte, J. Carstensen, R. Vaquer-Sunyer, and D. J. Conley 2011. Ecosystem impacts of hypoxia: thresholds of hypoxia and pathways to recovery. Environ. Res. Lett. 6:25003-25014.
224. 2 fixation by sulfate-reducing bacteria in a marine intertidal microbial mat. Aquat. Microb. Ecol. 28:1-12.
225. Steppe, T. F., J. L. Pinckney, J. Dyble, and H. W. Paerl 2001. Diazotrophy in modern marine bahamian stromatolites. Microb. Ecol. 41:36-44.
226. Stolarski, R., R. Bojkov, L. Bishop, C. Zerefos, J. Staehelin, and J. Zawodny 1992. Measured trends in stratospheric ozone. Science 256:342-349.
227. Suzuki, Y., and B. Casareto 2011. The role of Dissolved Organic Nitrogen (DON) in coral biology and reef ecology. Pp. 207-214 in Z. Dubinsky and N. Stambler, eds. Coral reefs: an ecosystem in transition. Springer, Netherlands.
228. 2 in coral reefs. Energy Convers. Manage. 36:737-740.
229. Szmant-Froelich, A. 1983. Functional aspects of nutrient cycling on coral reefs. Pp. 133-139 in M. L. Reaka, ed. The ecology of deep and shallow coral reefs. NOAA Symposium Series Undersea Research, Rockville, Maryland.
230. Tedetti, M., and R. Sempéré 2006. Penetration of ultraviolet radiation in the marine environment. A Review. Photochem. Photobiol. 82:389-397.
231. Thacker, R. W. 2005. Impacts of shading on sponge-cyanobacteria symbioses: a comparison between host-specific and generalist associations. Integr. Comp. Biol. 45:369-376.
232. Tyagi, R., G. Srinivas, D. Vyas, A. Kumar, and H. D. Kumar 1992. Differential effect of ultraviolet-B radiation on certain metabolic processes in a chromatically adapting Nostoc. Photochem. Photobiol. 55:401-407.
233. Vega Thurber, R., D. Willner-Hall, B. Rodriguez-Mueller, C. Desnues, R. A. Edwards, F. Angly, et al. 2009. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11:2148-2163.
234. Vega Thurber, R., D. E. Burkepile, A. M. S. Correa, A. R. Thurber, A. A. Shantz, R. Welsh, et al. 2012. Macroalgae decrease growth and alter microbial community structure of the reef-building coral, Porites astreoides. PLoS ONE 7:e44246.
235. Vega Thurber, R. L., D. E. Burkepile, C. Fuchs, A. A. Shantz, R. McMinds, and J. R. Zaneveld 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Change Biol. 20:544-554.
236. Vincent, W. F., and S. Roy 1993. Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery. Environ. Rev. 1:1-12.
237. Voss, M., P. Croot, K. Lochte, M. Mills, and I. Peeken 2004. Patterns of nitrogen fixation along 10 N in the tropical Atlantic. Geophys. Res. Lett., 31:L23S09.
238. Wahl, M., F. Goecke, A. Labes, S. Dobretsov, and F. Weinberger 2012. The second skin: ecological role of epibiotic biofilms on marine organisms. Front. Microbiol. 3:292.
239. Wangpraseurt, D., M. Weber, H. Røy, L. Polerecky, D. de Beer, and M. M. Nugues 2012. In Situ oxygen dynamics in coral-algal interactions. PLoS ONE 7:e31192.
240. 2 - Part 1: growth, production and nitrogen cycling. Biogeosciences 9:2973-2988.
241. Webb, K. L., W. D. Dupaul, W. Wiebe, W. Sottile, and R. E. Johannes 1975. Enewetak (Eniwetok) atoll: aspects of the nitrogen cycle on a coral reef. Limnol. Oceanogr. 20:198-210.
242. Webster, N. S., and M. W. Taylor 2012. Marine sponges and their microbial symbionts: love and other relationships. Environ. Microbiol. 14:335-346.
243. Webster, N. S., A. P. Negri, F. Flores, C. Humphrey, R. Soo, E. S. Botté, et al. 2012. Near-future ocean acidification causes differences in microbial associations within diverse coral reef taxa. Environ. Microbiol. Rep. 5:243-251.
244. Weisz, J., U. Hentschel, N. Lindquist, and C. Martens 2007. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar. Biol. 152:475-483.
245. Weisz, J. B., A. J. Massaro, B. D. Ramsby, and M. S. Hill 2010. Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biol. Bull. 219:189-197.
246. Welsh, D. T. 2000. Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity. Ecol. Lett. 3:58-71.
247. Welsh, D., S. Bourgues, R. De Wit, and R. Herbert 1996a. Seasonal variations in nitrogen-fixation (acetylene reduction) and sulphate-reduction rates in the rhizosphere of Zostera noltii: nitrogen fixation by sulphate-reducing bacteria. Mar. Biol. 125:619-628.
248. Welsh, D. T., S. Bourguès, R. De Wit, R. A. Herbert 1996b. Seasonal variation in rates of heterotrophic nitrogen fixation (acetylene reduction) in Zostera noltii meadows and uncolonised sediments of the Bassin d'Arcachon, south-west France. Hydrobiologia 329:161-174.
249. Welsh, DT, P. Wellsbury, S. Bourguès, R. De Wit, and R. A. Herbert 1996c. Relationship between porewater organic carbon content, sulphate reduction and nitrogen fixation (acetylene reduction) in the rhizosphere of Zostera noltii. Pp 175-183 in P. Caumette, J. Castel and R. Herbert, eds. Coastal Lagoon Eutrophication and ANaerobic Processes (C.L.E.AN.). Springer, Dordrecht, Netherlands.
250. Werner, U., A. Blazejak, P. Bird, G. Eickert, R. Schoon, R. M. M. Abed, et al. 2008. Microbial photosynthesis in coral reef sediments (Heron Reef, Australia). Estuar. Coast. Shelf Sci. 76:876-888.
251. Wiedenmann, J., C. D'Angelo, E. G. Smith, A. N. Hunt, F.-E. Legiret, A. D. Postle, et al. 2013. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Chang. 3:160-164.
252. Wild, C., M. Huettel, A. Klueter, S. G. Kremb, M. Y. M. Rasheed, and B. B. Jorgensen 2004. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66-70.
253. Wild, C., O. Hoegh-Guldberg, M. S. Naumann, M. F. Colombo-Pallotta, M. Ateweberhan, W. K. Fitt, et al. 2011. Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar. Freshw. Res. 62:205-215.
254. Wilkinson, C. R. 1999. Nitrogen fixation is symbiotic marine sponges; ecological significance and difficulties in detection. Mem. Queensl. Mus. 44:667-673.
255. Wilkinson, C. R., and P. Fay 1979. Nitrogen-fixation in coral reef sponges with symbiotic cyanobacteria. Nature 279:527-529.
256. Wilkinson, C. R., D. M. Williams, P. W. Sammarco, R. W. Hogg, and L. A. Trott 1984. Rates of nitrogen-fixation on coral reefs across the continental-shelf of the central Great Barrier Reef. Mar. Biol. 80:255-262.
257. Williams, S. L., and R. C. Carpenter 1997. Grazing effects on nitrogen fixation in coral reef algal turfs. Mar. Biol. 130:223-231.
258. Williams, S. L., and R. C. Carpenter 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.
259. Williams, S, I. Gill, and S. Yarish 1985. Nitrogen cycling in backreef sediments (St. Croix, US Virgin Islands). Pp 389-394 in C. Gabrie, J. L. Toffart and B. Salvat, eds. Proceedings of the fifth international coral reef congress. Vol. 3: Symposia and Seminars (A), Tahiti.
260. Williams, W., A. Viner, and W. Broughton 1987. Nitrogen fixation (acetylene reduction) associated with the living coral Acropora variabilis. Mar. Biol. 94:531-535.
261. Wilson, S. T., D. Böttjer, M. J. Church, and D. M. Karl 2012. Comparative assessment of nitrogen fixation methodologies, conducted in the Oligotrophic North Pacific Ocean. Appl. Environ. Microbiol. 78:6516-6523.
262. Witt, V., C. Wild, K. R. N. Anthony, G. Diaz-Pulido, and S. Uthicke 2011. Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ. Microbiol. 13:2976-2989.
263. Wittenberg, J. B., F. J. Bergersen, C. A. Appleby, and G. L. Turner 1974. Facilitated Oxygen Diffusion: the role of leghemoglobin in Nitrogen fixation by bacteroids isolated from soybean root nodules. J. Biol. Chem. 249:4057-4066.
264. Wooldridge, S. A. 2009. Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar. Pollut. Bull. 58:745-751.
265. Wu, J., W. Sunda, E. A. Boyle, and D. M. Karl 2000. Phosphate depletion in the western north atlantic ocean. Science 289:759-762.
266. Yamamuro, M., H. Kayanne, and M. Minagawa 1995. Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol. Oceanogr. 40:617-621.
267. Yellowlees, D., Rees. TaV, and W. Leggat 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell Environ. 31:679-694.
268. Zehr, J. P. 2011. Nitrogen fixation by marine cyanobacteria. Trends Microbiol. 19:162-173.
269. 2 in the subtropical North Pacific Ocean. Nature 412:635-638.
270. Zehr, J. P., B. D. Jenkins, S. M. Short, and G. F. Steward 2003. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5:539-554.