Abstract
Urea may be an important source of nitrogen in low nutrient coral reef environments because corals and other organisms can assimilate it easily and it is found throughout ocean waters. We measured the distribution and concentrations of urea in seagrass beds, areas of schooling fish, coral formations and bottom sediments in the Upper Florida Keys Reef Tract. The flux of urea from bottom sediments was also measured. Ambient concentrations of urea in the offshore reefs were similar to the concentrations of nitrate and ammonium. Seagrass beds, areas of schooling fish and coral formations had elevated concentrations of urea that were up to eight times higher than nitrate in the system. Numerous ephemeral hotspots of urea that were 8–20 times the ambient urea concentration existed in seagrass beds, areas of schooling fish, and above sediments. Coastal areas and inland canals had high urea concentrations where urban runoff and septic effluents were prevalent, but there was no anthropogenic influence in the offshore habitats. Urea concentrations above bottom sediments were not different from ambient concentrations and benthic flux chamber incubations showed biological activity in carbonaceous sediments but no net urea production. The decrease in urea concentrations from coasts and inland waterways to a consistent ambient concentration in the offshore reef system and ephemeral hotspots of high urea concentration suggest that urea is a dynamic pool of bioavailable nitrogen in the reefs of the Upper Florida Keys.
References
Aluwihare LI, Repeta DJ, Pantoja S, Johnson CG (2005) Two chemically distinct pools of organic nitrogen accumulate in the ocean. Science 308:1007–1010
Barimo J, Serafy J, Frezza P, Walsh P (2007) Habitat use, urea production and spawning in the gulf toadfish Opsanus beta. Mar Biol 150:497–508
Beauregard AY (2004) Biogeochemical cycling of carbon and nitrogen by the coral-zooxanthellae symbiosis. Ph.D. thesis, University of Delaware, p 139
Boyer JN (2011) Water quality monitoring project for the water quality protection program of the Florida Keys National Marine Sanctuary. Data were provided by the SERC-FIU Water Quality Monitoring Network which is supported by SFWMD/SERC Cooperative Agreements #4600000352 as well as EPA Agreement #X994621-94-0 http://www.serc.fiu.edu/wqmnetwork/fknms-cd/datadl.htm Accessed 18 May, 2011
Boyer JN, Briceño HO (2009) 2009 annual report of the water quality monitoring project for the water quality protection program of the florida keys national marine sanctuary. Southeast Environmental Research Center, Florida International University http://serc.fiu.edu/wqmnetwork/ Accessed 18 May, 2011
Bronk DA (2002) Dynamics of DON. In: Dennis AH, Craig AC (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, pp 153–247
Bronk DA, Glibert PM, Ward BB (1994) Nitrogen uptake, dissolved organic nitrogen release, and new production. Science 265:1843–1846
Bronk DA, Glibert PM, Malone TC, Susan Banahan ES (1998) Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux. Aquat Microb Ecol 15:177–189
Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4:283–296
Caperon WAHJ (1976) The rate of utilization of urea, ammonium, and nitrate by natural populations of marine phytoplankton in a eutrophic environment. Pac Sci 30:329–340
Capone DG, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral-reef sediments. Mar Ecol Prog Ser 80:75–88
Cho BC, Park MG, Shim JH, Azam F (1996) Significance of bacteria in urea dynamics in coastal surface waters. Mar Ecol Prog Ser 142:19–26
Conover RJ, Gustavson KR (1999) Sources of urea in arctic seas: zooplankton metabolism. Mar Ecol-Prog Ser 179:41–54
Conover RJ, Mumm N, Bruecker P, MacKenzie S (1999) Sources of urea in arctic seas: seasonal fast ice? Mar Ecol-Prog Ser 179:55–69
Cornell SE, Jickells TD, Cape JN, Rowland AP, Duce RA (2003) Organic nitrogen deposition on land and coastal environments: a review of methods and data. Atmos Environ 37:2173–2191
Eyre BD, Ferguson AJP (2002) Comparison of carbon production and decomposition, benthic nutrient fluxes and denitrification in seagrass, phytoplankton, benthic microalgae- and macroalgae-dominated warm-temperate Australian lagoons. Mar Ecol-Prog Ser 229:43–59
Glibert PM, Heil CA, Hollander D, Revilla M, Hoare A, Alexander J, Murasko S (2004) Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar Ecol Prog Ser 280:73–83
Glibert PM, Trice TM, Michael B, Lane L (2005) Urea in the tributaries of the Chesapeake and coastal bays of Maryland. Water Air Soil Pollut 160:229–243
Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea - a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463
Glibert PM, Wazniak CE, Hall MR, Sturgis B (2007) Seasonal and interannual trends in nitrogen and brown tide in Maryland’s coastal bays. Ecol Appl 17:S79–S87
Glibert PM, Kelly V, Alexander J, Codispoti LA, Boicourt WC, Trice TM, Michael B (2008) In Situ nutrient monitoring: A tool for capturing nutrient variability and the antecedent conditions that support algal blooms. Harmful Algae 8:175–181
Goeyens L, Kindermans N, Abu Yusuf M, Elskens M (1998) A room temperature procedure for the manual determination of urea in seawater. Estuar Coast Shelf Sci 47:415–418
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
Grover R, Maguer JF, Allemand D, Ferrier-Pages C (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865
Hammond DE, Cummins KM, McManus J, Berelson WM, Smith G, Spagnoli F (2004) Methods for measuring benthic nutrient flux on the California Margin: comparing shipboard incubations to in situ lander results. Limnol Oceanogr: Methods 2:146–159
Hansen JW, Udy JW, Perry CJ, Dennison WC, Lomstein BA (2000) Effect of the seagrass Zostera capricorni on sediment microbial processes. Mar Ecol Prog Ser 199:83–96
Holbrook SJ, Brooks AJ, Schmitt RJ, Stewart HL (2008) Effects of sheltering fish on growth of their host corals. Mar Biol 155:521–530
Jørgensen NOG, Tranvik LJ, Berg GM (1999) Occurrence and bacterial cycling of dissolved nitrogen in the Gulf of Riga, the Baltic Sea. Mar Ecol Prog Ser 191:1–18
Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407
Lomas MW, Trice TM, Glibert PM, Bronk DA, McCarthy JJ (2002) Temporal and spatial dynamics of urea uptake and regeneration rates and concentrations in Chesapeake Bay. Estuaries 25:469–482
Lomstein BA, Blackburn TH, Henriksen K (1989) Aspects of nitrogen and carbon cycling in the Northern Bering Shelf sediment. I. The significance of urea turnover in the mineralization of NH4+. Mar Ecol-Prog Ser 57:237–247
Lund BA, Blackburn TH (1989) Urea turnover in a coastal marine sediment measured by a C-14-urea short-term incubation. J Microbiol Meth 9:297–308
McCarthy JJ (1972) The uptake of urea by natural populations of marine phytoplankton. Limnol Oceanogr 17:738–748
McCarthy JJ, Whitledge TE (1972) Nitrogen excretion by anchovy (Engraulis mordax) and jack mackerel (Trachurus symmetricus). Fish Bull 70:395–401
McCarthy M, Pratum T, Hedges J, Benner R (1997) Chemical composition of dissolved organic nitrogen in the ocean. Nature 390:150–154
McDonald MD, Smith CP, Walsh PJ (2006) The physiology and evolution of urea transport in fishes. J Membr Biol 212:93–107
Meyer JL, Schultz ET (1985) Migration haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156
Miller CA, Glibert PM (1998) Nitrogen excretion by the calanoid copepod Acartia tonsa: results of mesocosm experiments. J Plankton Res 20:1767–1780
Mulvenna PF, Savidge G (1992) A modified manual method for the determination of urea in seawater using diacetylmonoxime reagent. Estuar Coast Shelf Sci 34:429–438
Painter SC, Sanders R, Waldron HN, Lucas MI, Torres-Valdes S (2008) Urea distribution and uptake in the Atlantic Ocean between 50 degrees N and 50 degrees S. Mar Ecol Prog Ser 368:53–63
Pedersen H, Lomstein BA, Blackburn TH (1993) Evidence for bacterial urea production in marine sediments. FEMS Microbiol Ecol 12:51–59
Rysgaard S, Thamdrup B, Risgaard-Petersen N, Fossing H, Berg P, Christensen PB, Dalsgaard T (1998) Seasonal carbon and nutrient mineralization in a high-Arctic coastal marine sediment, Young Sound, Northeast Greenland. Mar Ecol Prog Ser 175:261–276
Satoh Y (1980) Production of urea by bacterial decomposition of organic matter including phytoplankton. Int Rev Gesamten Hydrobiol Hydrogr 65:295–301
Sharp JH, Beuregard AY, Burdige D, Cauwet G, Curless SE, Lauck R, Nagel K, Ogawa H, Parker AE, Primm O, Pujo-Pay A, Savidge WB, Seitzinger S, Spyres G, Styles R (2004) A direct instrument comparison for measurement of total dissolved nitrogen in seawater. Mar Chem 84:181–193
Szmant AM (2002) Nutrient enrichment on coral reefs: is it a major cause of coral reef decline? Estuaries 25:743–766
Tanaka Y, Miyajima T, Watanabe A, Nadaoka K, Yamamoto T, Ogawa H (2011) Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs 30(2):533–541
Therkildsen MS, Lomstein BA (1994) Seasonal-variation in sediment urea turnover in a shallow estuary. Mar Ecol Prog Ser 109:77–82
Turley CM (1985) Biological studies in the vicinity of a shallow-sea tidal mixing front. 4. seasonal and spatial-distribution of urea and its uptake by phytoplankton. Philos Trans R Soc B 310:471–500
Vonk JA, Middelburg JJ, Stapel J, Bouma TJ (2008) Dissolved organic nitrogen uptake by seagrasses. Limnol Oceanogr 53:542–548
Wafar MVM, Wafar S, Devassy VP (1986) Nitrogenous nutrients and primary production in a tropical oceanic environment. Bull Mar Sci 38:273–284
Wafar MVM, Wafar S, Kumar RR (1993) Nitrogen uptake kinetics of freshly isolated zooxanthellae. Indian J Mar Sci 22:83–88
Walsh PJ, Wang Y, Campbell CE, Boeck GD, Wood CM (2001) Patterns of nitrogenous waste excretion and gill urea transporter mRNA expression in several species of marine fish. Mar Biol 139:839–844
Wild C, Naumann MS, Haas A, Struck U, Mayer FW, Rasheed MY, Huettel M (2009) Coral sand O2 uptake and pelagic-benthic coupling in a subtropical fringing reef, Aqaba, Red Sea. Aquat Biol 6:133–142
Williams SL, Yarish SM, Gill IP (1985) Ammonium distributions, production and efflux from backreef sediments, St. Croix, US Virgin Islands. Mar Ecol Prog Ser 24:57–64
Wood CM, Gilmour KM, Perry SF, Part P, Laurent P, Walsh PJ (1998) Pulsatile urea excretion in gulf toadfish (Opsanus beta): Evidence for activation of a specific facilitated diffusion transport system. J Exp Biol 201:805–817
Acknowledgments
We thank the staff at the National Undersea Research Center for help with sample collection. The comments of Deborah Bronk and three anonymous reviewers greatly improved the manuscript and feedback from Ruth Yanai was invaluable throughout the writing process. This material is based on work supported by a grant from the National Undersea Research Program of the National Oceanic and Atmospheric Administration (NOAA), and the NOAA Coral Reef Conservation Program. These statements, findings, conclusions, views, and recommendations are those of the authors and do not necessarily reflect the views of any of those organizations.
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Crandall, J.B., Teece, M.A. Urea is a dynamic pool of bioavailable nitrogen in coral reefs. Coral Reefs 31, 207–214 (2012). https://doi.org/10.1007/s00338-011-0836-1
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DOI: https://doi.org/10.1007/s00338-011-0836-1