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Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals?

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Abstract

Annual coral bleaching events due to increasing sea surface temperatures are predicted to occur globally by the mid-century and as early as 2025 in the Caribbean, and severely impact coral reefs. We hypothesize that heterotrophic carbon (C) in the form of zooplankton and dissolved organic carbon (DOC) is a significant source of C to bleached corals. Thus, the ability to utilize multiple pools of fixed carbon and/or increase the amount of fixed carbon acquired from one or more pools of fixed carbon (defined here as heterotrophic plasticity) could underlie coral acclimatization and persistence under future ocean-warming scenarios. Here, three species of Caribbean coral—Porites divaricata, P. astreoides, and Orbicella faveolata—were experimentally bleached for 2.5 weeks in two successive years and allowed to recover in the field. Zooplankton feeding was assessed after single and repeat bleaching, while DOC fluxes and the contribution of DOC to the total C budget were determined after single bleaching, 11 months on the reef, and repeat bleaching. Zooplankton was a large C source for P. astreoides, but only following single bleaching. DOC was a source of C for single-bleached corals and accounted for 11–36 % of daily metabolic demand (CHARDOC), but represented a net loss of C in repeat-bleached corals. In repeat-bleached corals, DOC loss exacerbated the negative C budgets in all three species. Thus, the capacity for heterotrophic plasticity in corals is compromised under annual bleaching, and heterotrophic uptake of DOC and zooplankton does not mitigate C budget deficits in annually bleached corals. Overall, these findings suggest that some Caribbean corals may be more susceptible to repeat bleaching than to single bleaching due to a lack of heterotrophic plasticity, and coral persistence under increasing bleaching frequency may ultimately depend on other factors such as energy reserves and symbiont shuffling.

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References

  • Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Bio Ecol 232:85–106

    Article  Google Scholar 

  • Anthony KRN (2000) Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs 19:59–67

    Article  Google Scholar 

  • 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 23:539–550

    Article  Google Scholar 

  • Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proc Roy Soc Lond B Biol Sci 279:1100–1107

    Article  CAS  Google Scholar 

  • Brocke HJ, Wenzhoefer F, de Beer D, Mueller B, van Duyl FC, Nugues MM (2015) High dissolved organic carbon release by benthic cyanobacterial mats in a Caribbean reef ecosystem. Sci Rep 5:8852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Bythell JC (1988) A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck). Proc 6th Int Coral Reef Symp 2:535–540

  • Cox EF (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724

    Article  Google Scholar 

  • Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42

    Article  CAS  Google Scholar 

  • Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol 60:81–90

    Article  CAS  Google Scholar 

  • D’Croz L, Mate JL, Oke JE (2001) Responses to elevated seawater temperature and UV radiation in the coral Porites lobata from upwelling and non-upwelling environments on the Pacific coast of Panama. Bull Mar Sci 69:203–214

    Google Scholar 

  • Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci USA 104:5483–5488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edmunds PJ, Davies PS (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ferrier-Pages C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    Article  CAS  Google Scholar 

  • Ferrier-Pages C, Peirano A, Abbate M, Cocito S, Negri A, Rottier C, Riera P, Rodolfo-Metalpa R, Reynaud S (2011) Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol Oceanogr 56:1429–1438

    Article  Google Scholar 

  • 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 Chang 3:165–170

    Article  Google Scholar 

  • Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509

    Article  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • 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 Chang Biol 20:3823–3833

    Article  PubMed  Google Scholar 

  • Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas AF, Jantzen C, Naumann MS, Iglesias-Prieto R, Wild C (2010) Organic matter release by the dominant primary producers in a Caribbean reef lagoon: implication for in situ O2 availability. Mar Ecol Prog Ser 409:27–39

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162

    Article  Google Scholar 

  • LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc R Soc Lond B Biol Sci 276:4139–4148

    Article  Google Scholar 

  • Leal MC, Ferrier-Pages C, Calado R, Brandes JA, Frischer ME, Nejstgaard JC (2014) Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar Ecol Prog Ser 504:171–179

    Article  Google Scholar 

  • Levas SJ, Grottoli AG, Hughes A, Osburn CL, Matsui Y (2013) Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS One 8:e63267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levas S, Grottoli AG, Warner ME, Cai WJ, Bauer J, Schoepf V, Baumann JH, Matsui Y, Gearing C, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y (2015) Organic carbon fluxes mediated by corals at elevated pCO2 and temperature. Mar Ecol Prog Ser 519:153–164

    Article  CAS  Google Scholar 

  • Marsh JA (1970) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263

    Article  Google Scholar 

  • Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182

    Article  Google Scholar 

  • McClanahan TR, Muthiga NA (2014) Community change and evidence for variable warm-water temperature adaptation of corals in northern Male Atoll, Maldives. Mar Pollut Bull 80:107–113

    Article  CAS  PubMed  Google Scholar 

  • Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056

    Article  PubMed  Google Scholar 

  • Muscatine L, Mccloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    Article  CAS  Google Scholar 

  • Naumann MS, Haas A, Struck U, Mayr C, El-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the northern Red Sea. Coral Reefs 29:649–659

    Article  Google Scholar 

  • Naumann MS, Richter C, Mott C, el-Zibdah M, Manasrah R, Wild C (2012) Budget of coral-derived organic carbon in a fringing coral reef of the Gulf of Aqaba, Red Sea. J Mar Syst 105:20–29

    Article  Google Scholar 

  • Niggl W, Glas M, Laforsch C, Mayr C, Wild C (2009) First evidence of coral bleaching stimulating organic matter release by reef corals. Proc 11th Int Coral Reef Symp, pp 905–911

  • Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89

    Article  Google Scholar 

  • Palardy JE, Grottoli AG, Matthews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the eastern Pacific. J Exp Mar Bio Ecol 331:99–107

    Article  Google Scholar 

  • Palardy JE, Rodrigues LJ, Grottoli AG (2008) The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J Exp Mar Bio Ecol 367:180–188

    Article  CAS  Google Scholar 

  • Piontkovski SA, Castellani C (2009) Long-term declining trend of zooplankton biomass in the tropical Atlantic. Hydrobiologia 632:365–370

    Article  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • Schoepf V, McCulloch MT, Warner ME, Levas SJ, Matsui Y, Aschaffenburg MD, Grottoli AG (2014) Short-term coral bleaching is not recorded by skeletal boron isotopes. PLoS One 9:e112011

    Article  PubMed  PubMed Central  Google Scholar 

  • Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317

    Article  Google Scholar 

  • Tada K, Sakai K, Nakano Y, Takemura A, Montani S (2003) Size-fractionated phytoplankton biomass in coral reef waters off Sesoko Island, Okinawa, Japan. J Plankton Res 25:991–997

    Article  CAS  Google Scholar 

  • Tanaka Y, Miyajima T, Koike I, Hayashibara T, Ogawa H (2008) Production of dissolved and particulate organic matter by the reef-building corals Porites cylindrica and Acropora pulchra. Bull Mar Sci 82:237–245

    Google Scholar 

  • Tanaka Y, Miyajima T, Umezawa Y, Hayashibara T, Ogawa H, Koike I (2009) Net release of dissolved organic matter by the scleractinian coral Acropora pulchra. J Exp Mar Bio Ecol 377:101–106

    Article  CAS  Google Scholar 

  • Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722

    Article  Google Scholar 

  • Tremblay P, Naumann MS, Sikorski S, Grover R, Ferrier-Pages C (2012) Experimental assessment of organic carbon fluxes in the scleractinian coral Stylophora pistillata during a thermal and photo stress event. Mar Ecol Prog Ser 453:63–77

    Article  CAS  Google Scholar 

  • van Hooidonk R, Maynard JA, Liu Y, Lee SK (2015) Downscaled projections of Caribbean coral bleaching that can inform conservation planning. Glob Chang Biol 21:3389–3401

    Article  PubMed  Google Scholar 

  • Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87–98

    Article  CAS  Google Scholar 

  • Wild C, Naumann M, Niggl W, Haas A (2010a) Carbohydrate composition of mucus released by scleractinian warm- and cold-water reef corals. Aquat Biol 10:41–45

    Article  Google Scholar 

  • Wild C, Niggl W, Naumann MS, Haas AF (2010b) Organic matter release by Red Sea coral reef organisms-potential effects on microbial activity and in situ O2 availability. Mar Ecol Prog Ser 411:61–71

    Article  CAS  Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MY, Jorgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  CAS  PubMed  Google Scholar 

  • Wild C, Mayr C, Wehrmann L, Schottner S, Naumann M, Hoffmann F, Rapp HT (2008) Organic matter release by cold water corals and its implication for fauna-microbe interaction. Mar Ecol Prog Ser 372:67–75

    Article  CAS  Google Scholar 

  • Wilkinson C (2008) Status of coral reefs of the world 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville

    Google Scholar 

Download references

Acknowledgments

We thank Roberto Iglesias-Prieto, Ania Banaszak, Susana Enriquez, Robin Smith, and the staff of the Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autonoma de Mexico for their generous time and logistical support. We also thank Yohei Matsui, Teresa Huey, Dana Borg, and Amy Barrett for field and laboratory assistance. This research was funded by the National Science Foundation division of Biological Oceanography grants OCE-0825490 to AG and OCE-0825413 to MW. We also thank the Ford Foundation. Data archived at http://www.bco-dmo.org/project/516103. All work undertaken in this study complied with the current laws of Mexico and the USA.

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Author notes

  1. Stephen Levas

    Present address: Department of Geography and the Environment, Villanova University, Villanova, PA, 19460, USA

  2. Verena Schoepf

    Present address: ARC Centre of Excellence for Coral Reef Studies, School of Earth and Environment, and UWA Oceans Institute, The University of Western Australia, Crawley, WA, 6009, Australia

  3. Justin Baumann

    Present address: Department of Marine Sciences, University of North Carolina, Chapel Hill, NC, 27599, USA

Authors and Affiliations

  1. School of Earth Sciences, The Ohio State University, Columbus, OH, 43210, USA

    Stephen Levas, Andréa G. Grottoli, Verena Schoepf & Justin Baumann

  2. School of Marine Sciences and Policy, University of Delaware, Lewes, DE, 19716, USA

    Matthew Aschaffenburg & Mark E. Warner

  3. Aquatic Biogeochemistry Laboratory, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, Columbus, OH, 43210, USA

    James E. Bauer

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  1. Stephen Levas
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Correspondence to Stephen Levas.

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Communicated by Biology Editor Dr. Anastazia Banaszak

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Levas, S., Grottoli, A.G., Schoepf, V. et al. Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals?. Coral Reefs 35, 495–506 (2016). https://doi.org/10.1007/s00338-015-1390-z

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  • DOI: https://doi.org/10.1007/s00338-015-1390-z

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