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Urea is a dynamic pool of bioavailable nitrogen in coral reefs

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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.

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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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Bronk DA, Glibert PM, Ward BB (1994) Nitrogen uptake, dissolved organic nitrogen release, and new production. Science 265:1843–1846

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4:283–296

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Capone DG, Dunham SE, Horrigan SG, Duguay LE (1992) Microbial nitrogen transformations in unconsolidated coral-reef sediments. Mar Ecol Prog Ser 80:75–88

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Conover RJ, Gustavson KR (1999) Sources of urea in arctic seas: zooplankton metabolism. Mar Ecol-Prog Ser 179:41–54

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Holbrook SJ, Brooks AJ, Schmitt RJ, Stewart HL (2008) Effects of sheltering fish on growth of their host corals. Mar Biol 155:521–530

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McCarthy JJ (1972) The uptake of urea by natural populations of marine phytoplankton. Limnol Oceanogr 17:738–748

    Article  Google Scholar 

  • McCarthy JJ, Whitledge TE (1972) Nitrogen excretion by anchovy (Engraulis mordax) and jack mackerel (Trachurus symmetricus). Fish Bull 70:395–401

    Google Scholar 

  • McCarthy M, Pratum T, Hedges J, Benner R (1997) Chemical composition of dissolved organic nitrogen in the ocean. Nature 390:150–154

    Article  CAS  Google Scholar 

  • McDonald MD, Smith CP, Walsh PJ (2006) The physiology and evolution of urea transport in fishes. J Membr Biol 212:93–107

    Article  PubMed  CAS  Google Scholar 

  • Meyer JL, Schultz ET (1985) Migration haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol Oceanogr 30:146–156

    Article  Google Scholar 

  • Miller CA, Glibert PM (1998) Nitrogen excretion by the calanoid copepod Acartia tonsa: results of mesocosm experiments. J Plankton Res 20:1767–1780

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pedersen H, Lomstein BA, Blackburn TH (1993) Evidence for bacterial urea production in marine sediments. FEMS Microbiol Ecol 12:51–59

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Satoh Y (1980) Production of urea by bacterial decomposition of organic matter including phytoplankton. Int Rev Gesamten Hydrobiol Hydrogr 65:295–301

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Szmant AM (2002) Nutrient enrichment on coral reefs: is it a major cause of coral reef decline? Estuaries 25:743–766

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Therkildsen MS, Lomstein BA (1994) Seasonal-variation in sediment urea turnover in a shallow estuary. Mar Ecol Prog Ser 109:77–82

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vonk JA, Middelburg JJ, Stapel J, Bouma TJ (2008) Dissolved organic nitrogen uptake by seagrasses. Limnol Oceanogr 53:542–548

    Article  CAS  Google Scholar 

  • Wafar MVM, Wafar S, Devassy VP (1986) Nitrogenous nutrients and primary production in a tropical oceanic environment. Bull Mar Sci 38:273–284

    Google Scholar 

  • Wafar MVM, Wafar S, Kumar RR (1993) Nitrogen uptake kinetics of freshly isolated zooxanthellae. Indian J Mar Sci 22:83–88

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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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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Correspondence to J. B. Crandall.

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Communicated by Geology Editor Prof. Bernhard Riegl

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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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