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Ecosystems

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Nitrogen Identity Drives Differential Impacts of Nutrients on Coral Bleaching and Mortality

  • Deron E. BurkepileEmail author
  • Andrew A. Shantz
  • Thomas C. Adam
  • Katrina S. Munsterman
  • Kelly E. Speare
  • Mark C. Ladd
  • Mallory M. Rice
  • Leïla Ezzat
  • Shelby McIlroy
  • Jane C. Y. Wong
  • David M. Baker
  • Andrew J. Brooks
  • Russell J. Schmitt
  • Sally J. Holbrook
Article

Abstract

Nitrogen pollution increases the susceptibility of corals to heat-induced bleaching. However, different forms of nitrogen (nitrate vs. ammonium/urea) may have different impacts on thermal tolerance of corals. We used an 18-month field experiment on the oligotrophic fore reef of Moorea, French Polynesia, to test how different forms of nitrogen (nitrate vs. urea) impacted coral bleaching. The experiment spanned two moderate thermal stress events in 2016 and 2017. Nitrate increased bleaching prevalence in Acropora by up to 100% and in Pocillopora by up to 60% compared to control corals. Urea exposure often had intermediate effects on bleaching (not different from either control or nitrate-exposed corals) in both taxa. Importantly, nitrate prolonged bleaching in both Acropora and Pocillopora as nitrate-exposed corals remained bleached even after thermal stress ended, while control and urea-exposed corals had mostly recovered. Nitrate exposure also increased the prevalence of partial mortality in Pocillopora colonies and more than tripled the number of colonies that completely died. Our data are the first to show contrasting effects of different forms of nitrogen on coral bleaching and mortality in a natural reef environment, linking previous patterns from large-scale correlative studies with results from more mechanistic laboratory experiments. Most importantly, we showed that corals exposed to nitrate exhibited more frequent bleaching, bleached for longer duration, and were more likely to die than corals in low nitrogen conditions. Exposure to excess nitrogen, particularly anthropogenic nitrogen, may lower the temperature threshold at which corals bleach, triggering bleaching events on polluted reefs even when typical thermal stress thresholds have not been crossed.

Keywords

nutrient pollution climate change coral reef eutrophication symbiosis anthropocene 

Notes

Acknowledgements

National Science Foundation Grants OCE-1619697 to SJH, DEB, and RJS, OCE-1547952 to DEB, and OCE-1236905 and OCE-1637396 for the Moorea Coral Reef LTER to RJS and SJH, and a Hong Kong Research Grants Council Grant GRF# 17100014 to DMB supported this research. We thank M. Anskog, A. Duran, C. Fuchs, K. Landfield, S. Leung, K. Neumann, E. Schmeltzer, K. Seydel, A. Simoes Correa, A.T.S. Tang, A. Thurber, R. Vega Thurber, R. Welsh, and S. Wise for field and laboratory assistance. Research was completed under permits issued by the Territorial Government of French Polynesia (Délégation à la Recherche) and the Haut-commissariat de la République en Polynésie Francaise (DTRT) (Protocole d’Accueil 2015-2017).

Supplementary material

10021_2019_433_MOESM1_ESM.docx (113 kb)
Supplementary material 1 (DOCX 112 kb)

References

  1. Alldredge A. 2019. MCR LTER: Coral Reef: water column: nutrients, ongoing since 2005. knb-lter-mcr.1034.9.  https://doi.org/10.6073/pasta/9328a024f2bf16ecc66024f07dbcc574.
  2. Allgeier JE, Burkepile DE, Layman CA. 2017. Animal pee in the sea: consumer-mediated nutrient dynamics in the world’s changing oceans. Glob Change Biol 23:2166–78.CrossRefGoogle Scholar
  3. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R. 2009. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–50.CrossRefGoogle Scholar
  4. Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N. 2018. Climate change promotes parasitism in a coral symbiosis. ISME J 31:1–10.Google Scholar
  5. Bennett EM, Carpenter SR, Caraco NF. 2001. Human impact on erodable phosphorus and eutrophication: a global perspective: increasing accumulation of phosphorus in soil threatens rivers, lakes, and coastal oceans with eutrophication. Bioscience 51:227–34.CrossRefGoogle Scholar
  6. Béraud E, Gevaert F, Rottier C, Ferrier-Pagès C. 2013. The response of the scleractinian coral Turbinaria reniformis to thermal stress depends on the nitrogen status of the coral holobiont. J Exp Biol 216:2665–74.CrossRefGoogle Scholar
  7. Biscéré T, Ferrier-Pagès C, Grover R, Gilbert A, Wright A, Payri C, Holulbrèque F. 2018. Enhancement of coral calcification via the interplay of nickel and urease. Aquat Toxicol 200:247–56.CrossRefGoogle Scholar
  8. Bruno JF, Petes LE, Harvell CD, Hettinger A. 2003. Nutrient enrichment can increase the severity of coral diseases. Ecol Lett 6:1056–61.CrossRefGoogle Scholar
  9. Cacciapaglia C, Van Woesik R. 2015. Climate-change refugia: shading reef corals by turbidity. Glob Change Biol 22:1145–54.CrossRefGoogle Scholar
  10. Crandall JB, Teece MA. 2012. Urea is a dynamic pool of bioavailable nitrogen in coral reefs. Coral Reefs 31:207–14.CrossRefGoogle Scholar
  11. Cunning R, Baker AC. 2013. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Climate Change 3:259–62.CrossRefGoogle Scholar
  12. D’Angelo C, Wiedenmann J. 2014. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93.CrossRefGoogle Scholar
  13. Dagenais-Bellefeuille S, Morse D. 2013. Putting the N in dinoflagellates. Front Microbiol 4:369.CrossRefGoogle Scholar
  14. Ezzat L, Maguer J-F, Grover R, Ferrier-Pagès C. 2015. New insights into carbon acquisition and exchanges within the coral–dinoflagellate symbiosis under NH4 + and NO3 supply. Proc R Soc B Biol Sci 282:20150610.CrossRefGoogle Scholar
  15. Ezzat L, Maguer J-F, Grover R, Ferrier-Pagès C. 2016a. Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean. Sci Rep 6:1–11.CrossRefGoogle Scholar
  16. Ezzat L, Towle E, Irisson JO, Langdon C, Ferrier-Pagès C. 2016b. The relationship between heterotrophic feeding and inorganic nutrient availability in the scleractinian coral T. reniformis under a short-term temperature increase. Limnol Oceanogr 61:89–102.CrossRefGoogle Scholar
  17. Ferdie M, Fourqurean JW. 2004. Responses of seagrass communities to fertlization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnol Oceanogr 49:2082–94.CrossRefGoogle Scholar
  18. Fitt WK, McFarland FK, Warner ME, Chilcoat GC. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–85.CrossRefGoogle Scholar
  19. Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O. 2013. Limiting global warming to 2°C is unlikely to save most coral reefs. Nat Clim Change 3:165–70.CrossRefGoogle Scholar
  20. Godinot C, Houlbrèque F, Grover R, Ferrier-Pagès C. 2011. Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous change in temperature and pH. PLoS ONE 6:e25024.CrossRefGoogle Scholar
  21. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y. 2014. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Change Biol 20:3823–33.CrossRefGoogle Scholar
  22. Grover R, Maguer J-F, Raynaud-Vaganay S, Ferrier-Pagès C. 2002. Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–90.CrossRefGoogle Scholar
  23. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C. 2003. Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48:2266–74.CrossRefGoogle Scholar
  24. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C. 2006. Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 332:216–25.CrossRefGoogle Scholar
  25. Heron SF, Maynard JA, van Hooidonk R, Eakin CM. 2016. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci Rep 6:38402.CrossRefGoogle Scholar
  26. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–3.CrossRefGoogle Scholar
  27. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, Kuo C-y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK. 2017. Global warming and recurrent mass bleaching of corals. Nature 543:373–7.CrossRefGoogle Scholar
  28. Kendall C, Elliott EM, Wankel SD. 2007. Tracing anthropogenic inputs of nitrogen to ecosystems. In: Michener RH, Lajtha K, Eds. Stable Isotopes in Ecology and Environmental Science. 2nd edn. Hoboken: Blackwell. p 375–449.CrossRefGoogle Scholar
  29. Lesser MP. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–78.CrossRefGoogle Scholar
  30. Loya S, Sakai K, Yamazato K, Nakano Y, Sambali W, van Woesik R. 2001. Coral bleaching: the winners and the losers. Ecol Lett 4:122–31.CrossRefGoogle Scholar
  31. Luke SG. 2017. Evaluating significance in linear mixed-effects models in R. Behav Res Methods 49:1494–502.CrossRefGoogle Scholar
  32. MacNeil MA, Mellin C, Matthews S, Wolff NH, McClanahan TR, Devlin M, Drovandi C, Mengersen K, Graham NAJ. 2019. Water quality mediates resilience on the Great Barrier Reef. Nat Ecol Evolution 3:620–7.CrossRefGoogle Scholar
  33. Pogoreutz C, Rädecker N, Cárdenas A, Gärdes A, Wild C, Voolstra CR. 2018. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol Evol 8:2240–52.Google Scholar
  34. Pratchett MS, McCowan D, Maynard JA, Heron SF. 2013. Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia. PLoS ONE 8:e70443.CrossRefGoogle Scholar
  35. R Core Team. 2018. R: A Language and Environment for Statisical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  36. Revilla M, Alexander J, Glibert PM. 2005. Urea analysis in coastal waters: comparison of enzymatic and direct methods. Limnol Oceanogr Methods 3:290–9.CrossRefGoogle Scholar
  37. Rodrigues LJ, Grottoli AG. 2007. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–82.CrossRefGoogle Scholar
  38. Rosset S, Wiedenmann J, Reed AJ, D’Angelo C. 2017. Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar Pollut Bull 118:180–7.CrossRefGoogle Scholar
  39. Schaus MH, Vanni MJ, Wissing TE, Bremigan MT, Garvey JE, Stein RA. 1997. Nitrogen and phosphorus excretion by detritivorous gizzard shad in a reservoir ecosystem. Limnol Oceanogr 42:1386–97.CrossRefGoogle Scholar
  40. Shantz AA, Burkepile DE. 2014. Context-dependent effects of nutrient loading on the coral-algal mutualism. Ecology 95:1995–2005.CrossRefGoogle Scholar
  41. Sinha E, Michalak AM, Balaji V. 2017. Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357:405–8.CrossRefGoogle Scholar
  42. Sully S, Burkepile DE, Donvan MK, Hodgson G, van Woesik R. 2019. A global analysis of coral bleaching over the past two decades. Nat Commun 10:1264.CrossRefGoogle Scholar
  43. van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S. 2016. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci Rep 6:1–8.CrossRefGoogle Scholar
  44. Vega Thurber R, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld J. 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob Change Biol 20:544–54.CrossRefGoogle Scholar
  45. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997. Human domination of Earth’s ecosystems. Science 277:494–9.CrossRefGoogle Scholar
  46. Wagner DE, Kramer P, van Woesik R. 2010. Species composition, habitat, and water quality influence coral bleaching in southern Florida. Mar Ecol Prog Ser 408:65–78.CrossRefGoogle Scholar
  47. Wang L, Shantz AA, Payet JP, Sharpton TJ, Foster A, Burkepile DE, Vega Thurber R. 2018. Corals and their microbiomes are differentially affected by exposure to elevated nutrients and a natural thermal anomaly. Front Mar Sci 5:101.CrossRefGoogle Scholar
  48. Whiles MR, Huryn AD, Taylor BW, Reeve JD. 2009. Influence of handling stress and fasting on estimates of ammonium excretion by tadpoles and fish: recommendations for designing excretion experiments. Limnol Oceanogr Methods 7:1–7.CrossRefGoogle Scholar
  49. Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP. 2013. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Change 3:160–4.CrossRefGoogle Scholar
  50. Wooldridge SA. 2009. A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis. Mar Freshw Res 60:483–96.CrossRefGoogle Scholar
  51. Wooldridge SA. 2016. Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1. Identifying thresholds of concern for the Great Barrier Reef, Australia. Mar Pollut Bull .  https://doi.org/10.1016/j.marpolbul.2016.04.054.Google Scholar
  52. Wooldridge SA, Done TJ. 2009. Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19:1492–9.CrossRefGoogle Scholar
  53. Zaneveld J, Burkepile DE, Shantz AA, Pritchard C, McMinds R, Payet J, Welsh R, Correa AMS, Lemoine NP, Rosales S, Fuchs C, Vega Thurber R. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat Commun 7:11833.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Deron E. Burkepile
    • 1
    • 2
    Email author
  • Andrew A. Shantz
    • 1
  • Thomas C. Adam
    • 2
  • Katrina S. Munsterman
    • 1
  • Kelly E. Speare
    • 1
  • Mark C. Ladd
    • 1
  • Mallory M. Rice
    • 1
  • Leïla Ezzat
    • 1
  • Shelby McIlroy
    • 3
  • Jane C. Y. Wong
    • 3
  • David M. Baker
    • 3
  • Andrew J. Brooks
    • 2
  • Russell J. Schmitt
    • 1
    • 2
  • Sally J. Holbrook
    • 1
    • 2
  1. 1.Department of Ecology, Evolution, and Marine BiologyUniversity of California, Santa BarbaraSanta BarbaraUSA
  2. 2.Marine Science InstituteUniversity of California, Santa BarbaraSanta BarbaraUSA
  3. 3.The Swire Institute of Marine Science and School of Biological SciencesThe University of Hong KongHong KongPeople’s Republic of China

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