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Controls on the nitrogen isotopic composition of shallow water corals across a tropical reef flat transect

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Abstract

We tested the hypothesis that the nitrogen (N) isotopic signature (δ15N) of coral skeletal organic material (CS-δ15N) matches that of the coral tissue and also reflects the δ15N of water column fixed N, such that CS-δ15N can be used as a proxy for spatio-temporal oceanic N isotope distributions. Strong correlations between the δ15N of skeletal organic material and that of coral tissue in two scleractinian corals (Porites lutea and Favia stelligera) across a tropical coral reef flat support the use of CS-δ15N in reconstructing coral biomass δ15N changes. However, we observed a consistent and species-specific offset between the coral tissue δ15N and the skeletal CS-δ15N. As such, the CS-δ15N is not an absolute measure of tissue δ15N. The CS-δ15N of both coral species and three species of macroalgae increased across the reef flat in response to a natural gradient in water column δ15N. There was an apparent dampening of the water column δ15N gradient recorded in the coral tissue δ15N and the CS-δ15N, possibly caused by shifting trophic status of corals across the reef flat. The CS-δ15N therefore appears to robustly reflect the δ15N of the coral tissue, and the coral system is responsive to the δ15N of the water column N pools. The distortion of the true water column δ15N by corals requires further investigation and is an important consideration for the use of coral skeletons in temporal reconstructions of water column δ15N.

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References

  • Allemand D, Tambutte E, Girard J-P, Jaubert J (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tributyltin. J Exp Biol 201:2001–2009

    CAS  PubMed  Google Scholar 

  • Altabet MA, François R (1994) Sedimentary nitrogen isotopic ratio as a recorder for surface ocean nitrate utilization. Global Biogeochem Cycles 8:103–116

    Article  CAS  Google Scholar 

  • Aravena R, Robertson WD (1998) Use of multiple isotope tracers to evaluate denitrification in ground water: Study of nitrate from a large-flux septic system plume. Ground Water 36:975–982

    Article  CAS  Google Scholar 

  • Braman RS, Hendrix SA (1989) Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal Chem 61:2715–2718

    Article  CAS  PubMed  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  CAS  Google Scholar 

  • Costanzo SD, Udy J, Longstaff B, Jones A (2005) Using nitrogen stable isotope ratios (delta N-15) of macroalgae to determine the effectiveness of sewage upgrades: changes in the extent of sewage plumes over four years in Moreton Bay, Australia. Mar Pollut Bull 51:212–217

    Article  CAS  PubMed  Google Scholar 

  • Costanzo SD, O’Donohue MJ, Dennison WC, Loneragan NR, Thomas M (2001) A new approach for detecting and mapping sewage impacts. Mar Pollut Bull 42:149–156

    Article  CAS  PubMed  Google Scholar 

  • D’Elia C, Webb K, Porter J (1981) Nitrate-rich groundwater inputs to Discovery Bay, Jamaica: a significant source of N to local coral reefs? Bull Mar Sci 31:903–910

    Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Drake JL, Mass T, Haramaty L, Zelzion E, Bhattacharya D, Falkowski PG (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci U S A 110:3788–3793

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Druffel ERM (1997) Geochemistry of corals: Proxies of past ocean chemistry, ocean circulation, and climate. Proc Natl Acad Sci U S A 94:8354–8361

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans Roy Soc Lond B Biol Sci 368:20130164

    Article  Google Scholar 

  • Gagan MK, Ayliffe LK, Beck JW, Cole JE, Druffel ERM, Dunbar RB, Schrag DP (2000) New views of tropical paleoclimates from corals. Quart Sci Rev 19:45–64

    Article  Google Scholar 

  • Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull 116:59–75

    Article  CAS  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 Bio Ecol 332:216–225

    Article  CAS  Google Scholar 

  • Heikoop JM, Dunn JJ, Risk MJ, Sandeman IM, Schwarcz HP, Waltho N (1998) Relationship between light and the δ15 N of coral tissue: examples from Jamaica and Zanzibar. Limnol Oceanogr 43:909–920

    Article  CAS  Google Scholar 

  • Higgins MB, Wolfe-Simon F, Robinson RS, Qin Y, Saito MA, Pearson A (2011) Paleoenvironmental implications of taxonomic variation among delta N-15 values of chloropigments. Geochim Cosmochim Acta 75:7351–7363

    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 

  • Houlbreque F, Ferrier-Pages C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • Ingalls AE, Lee C, Druffel ERM (2003) Preservation of organic matter in mound-forming coral skeletons. Geochim Cosmochim Acta 67:2827–2841

    Article  CAS  Google Scholar 

  • Jones PD, Briffa KR, Osborn TJ, Lough JM, van Ommen TD, Vinther BM, Luterbacher J, Wahl ER, Zwiers FW, Mann ME, Schmidt GA, Ammann CM, Buckley BM, Cobb KM, Esper J, Goosse H, Graham N, Jansen E, Kiefer T, Kull C, Kuettel M, Mosley-Thompson E, Overpeck JT, Riedwyl N, Schulz M, Tudhope AW, Villalba R, Wanner H, Wolff E, Xoplaki E (2009) High-resolution palaeoclimatology of the last millennium: a review of current status and future prospects. Holocene 19:3–49

    Article  Google Scholar 

  • Jupiter S, Roff G, Marion G, Henderson M, Schrameyer V, McCulloch M, Hoegh-Guldberg O (2008) Linkages between coral assemblages and coral proxies of terrestrial exposure along a cross-shelf gradient on the southern Great Barrier Reef. Coral Reefs 27:887–903

    Article  Google Scholar 

  • Knapp AN, Sigman DM, Lipschultz F (2005) N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic time-series study site. Global Biogeochem Cycles 19:GB1018

  • Lewis SE, Brodie JE, McCulloch MT, Mallela J, Jupiter SD, Stuart Williams H, Lough JM, Matson EG (2012) An assessment of an environmental gradient using coral geochemical records, Whitsunday Islands, Great Barrier Reef, Australia. Mar Pollut Bull 65:306–319

    Article  CAS  PubMed  Google Scholar 

  • Marion GS, Dunbar RB, Mucciarone DA, Kremer JN, Lansing JS, Arthawiguna A (2005) Coral skeletal δ15N reveals isotopic traces of an agricultural revolution. Mar Pollut Bull 50:931–944

    Article  CAS  PubMed  Google Scholar 

  • McIlvin MR, Altabet MA (2005) Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal Chem 77:5589–5595

    Article  CAS  PubMed  Google Scholar 

  • Montagna P, McCulloch M, Taviani M, Mazzoli C, Vendrell B (2006) Phosphorus in cold-water corals as a proxy for seawater nutrient chemistry. Science 312:1788–1791

    Article  CAS  PubMed  Google Scholar 

  • Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D (2005) Stable isotopes (delta C-13 and delta N-15) of organic matrix from coral skeleton. Proc Natl Acad Sci U S A 102:1525–1530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pearse VB, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull 141:350–363

    Article  CAS  Google Scholar 

  • Puverel S, Houlbreque F, Tambutte E, Zoccola D, Payan P, Caminiti N, Tambutte S, Allemand D (2007) Evidence of low molecular weight components in the organic matrix of the reef building coral, Stylophora pistillata. Comp Biochem Physiol A Mol Integr Physiol 147:850–856

    Article  CAS  PubMed  Google Scholar 

  • Ren H, Sigman DM, Meckler AN, Plessen B, Robinson RS, Rosenthal Y, Haug GH (2009) Foraminiferal isotope evidence of reduced nitrogen fixation in the ice age Atlantic Ocean. Science 323:244–248

    Article  CAS  PubMed  Google Scholar 

  • Ren H, Sigman DM, Thunell RC, Prokopenko MG (2012) Nitrogen isotopic composition of planktonic foraminifera from the modern ocean and recent sediments. Limnol Oceanogr 57:1011–1024

    Article  CAS  Google Scholar 

  • Reynaud S, Martinez P, Houlbreque F, Billy I, Allemand D, Ferrier-Pages C (2009) Effect of light and feeding on the nitrogen isotopic composition of a zooxanthellate coral: role of nitrogen recycling. Mar Ecol Prog Ser 392:103–110

    Article  CAS  Google Scholar 

  • Risk MJ, Lapointe BE, Sherwood OA, Bedford BJ (2009) The use of delta N-15 in assessing sewage stress on coral reefs. Mar Pollut Bull 58:793–802

    Article  CAS  PubMed  Google Scholar 

  • Robinson RS, Brunelle BG, Sigman DM (2004) Revisiting nutrient utilization in the glacial Antarctic: Evidence from a new method for diatom-bound N isotopic analysis. Paleoceanography. doi:10.1029/2003PA000996

    Google Scholar 

  • Santos IR, Erler DV, Tait D, Eyre BD (2010) Breathing of a coral cay: Tracing tidally-driven seawater recirculation in permeable coral reef sediments. J Geophys Res 115(C12):12010

    Article  Google Scholar 

  • Schmidt S, Dennison WC, Moss GJ, Stewart GR (2004) Nitrogen ecophysiology of Heron Island, a subtropical coral cay of the Great Barrier Reef, Australia. Funct Plant Biol 31:517–528

    Article  CAS  Google Scholar 

  • Sherwood OA, Heikoop JM, Scott DB, Risk MJ, Guilderson TP, McKinney RA (2005) Stable isotopic composition of deep-sea gorgonian corals Primnoa spp.: a new archive of surface processes. Mar Ecol Prog Ser 301:135–148

    Article  CAS  Google Scholar 

  • Sigman DM, Altabet MA, Francois R, McCorkle DC, Gaillard JF (1999) The isotopic composition of diatom-bound nitrogen in Southern Ocean sediments. Paleoceanography 14:118–134

    Article  Google Scholar 

  • Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Bohlke JK (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–4153

    Article  CAS  PubMed  Google Scholar 

  • Smith JS, Johnson CR (1995) Nutrient inputs form seabirds and humans on a populated coral cay. Mar Ecol Prog Ser 124:189–200

    Article  Google Scholar 

  • Smith RL, Howes BL, Duff JH (1991) Denitrification in nitrate contaminated groundwater - occurrence in steep vertical geochemical gradients. Geochim Cosmochim Acta 55:1815–1825

    Article  CAS  Google Scholar 

  • Tanaka Y, Ogawa H, Miyajima T (2011a) Production and bacterial decomposition of dissolved organic matter in a fringing coral reef. J Oceanogr 67:427–437

    Article  CAS  Google Scholar 

  • Tanaka Y, Miyajima T, Watanabe A, Nadaoka K, Yamamoto T, Ogawa H (2011b) Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs 30:533–541

    Article  Google Scholar 

  • Tsunogai U, Kido T, Hirota A, Ohkuboy SB, Komatsu DD, Nakagawa F (2008) Sensitive determinations of stable nitrogen isotopic composition of organic nitrogen through chemical conversion into N2O. Rapid Commun Mass Spectrom 22:345–354

    Article  CAS  PubMed  Google Scholar 

  • Uchida A, Nishizawa M, Shirai K, Iijima H, Kayanne H, Takahata N, Sano Y (2008) High sensitivity measurements of nitrogen isotopic ratios in coral skeletons from Palau, western Pacific: Temporal resolution and seasonal variation of nitrogen sources. Geochem J 42:255–262

    Article  Google Scholar 

  • Uhle M, Macko S, Spero H, Engel M, Lea D (1997) Sources of carbon and nitrogen in modern planktonic foraminifera: the role of algal symbionts as determined by bulk and compound specific stable isotopic analyses. Org Geochem 27:103–113

    Article  CAS  Google Scholar 

  • Wang XT, Sigman DM, Cohen AL, Sinclair DJ, Sherrell RM, Weigand MA, Erler DV, Ren H (2014) Isotopic composition of skeleton-bound organic nitrogen in reef-building symbiotic corals: a new method and proxy evaluation at Bermuda. Geochim Cosmochim Acta. doi:10.1016/j.gca.2014.09.017

  • Ward-Paige CA, Risk MJ, Sherwood OA (2005) Reconstruction of nitrogen sources on coral reefs: delta N-15 and delta C-13 in gorgonians from Florida Reef Tract. Mar Ecol Prog Ser 296:155–163

    Article  CAS  Google Scholar 

  • Yamazaki A, Watanabe T, Tsunogai U (2011) Nitrogen isotopes of organic nitrogen in reef coral skeletons as a proxy of tropical nutrient dynamics. Geophys Res Lett 38:L19605

  • Young SD (1971) Organic material from scleractinian coral skeletons—I. Variation in composition between several species. Comp Biochem Physiol B Biochem Mol Biol 40:113–120

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by Southern Cross University (Special Studies Leave program), the Australian Research Council (LP100200732, DP0878683), US NSF grants OCE-1234664 and OCE-1060947 (to D.M.S), and the Grand Challenges Program at Princeton University. We thank I. Alexander and M. Carvalho de Carvalho from SCU, and A. M. Weigand from Princeton University for technical assistance. We also thank I. Santos for assistance with Heron Island sample collection.

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Correspondence to Dirk V. Erler.

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Erler, D.V., Wang, X.T., Sigman, D.M. et al. Controls on the nitrogen isotopic composition of shallow water corals across a tropical reef flat transect. Coral Reefs 34, 329–338 (2015). https://doi.org/10.1007/s00338-014-1215-5

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