Coral Reefs

, Volume 32, Issue 3, pp 727–735 | Cite as

Calcification by juvenile corals under heterotrophy and elevated CO2

Report

Abstract

Ocean acidification (OA) threatens the existence of coral reefs by slowing the rate of calcium carbonate (CaCO3) production of framework-building corals thus reducing the amount of CaCO3 the reef can produce to counteract natural dissolution. Some evidence exists to suggest that elevated levels of dissolved inorganic nutrients can reduce the impact of OA on coral calcification. Here, we investigated the potential for enhanced energetic status of juvenile corals, achieved via heterotrophic feeding, to modulate the negative impact of OA on calcification. Larvae of the common Atlantic golf ball coral, Favia fragum, were collected and reared for 3 weeks under ambient (421 μatm) or significantly elevated (1,311 μatm) CO2 conditions. The metamorphosed, zooxanthellate spat were either fed brine shrimp (i.e., received nutrition from photosynthesis plus heterotrophy) or not fed (i.e., primarily autotrophic). Regardless of CO2 condition, the skeletons of fed corals exhibited accelerated development of septal cycles and were larger than those of unfed corals. At each CO2 level, fed corals accreted more CaCO3 than unfed corals, and fed corals reared under 1,311 μatm CO2 accreted as much CaCO3 as unfed corals reared under ambient CO2. However, feeding did not alter the sensitivity of calcification to increased CO2; ∆ calcification/∆Ω was comparable for fed and unfed corals. Our results suggest that calcification rates of nutritionally replete juvenile corals will decline as OA intensifies over the course of this century. Critically, however, such corals could maintain higher rates of skeletal growth and CaCO3 production under OA than those in nutritionally limited environments.

Keywords

Climate change Ocean acidification Coral reefs Coral calcification Heterotrophy Energetics 

Supplementary material

338_2013_1021_MOESM1_ESM.docx (122 kb)
Supplementary material 1 (DOCX 121 kb)

References

  1. Anthony KR, 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 23:539–550CrossRefGoogle Scholar
  2. Atkinson MJ, Cuet P (2008) Possible effects of ocean acidification on coral reef biogeochemistry: topics for research. Mar Ecol Prog Ser 373:249–256CrossRefGoogle Scholar
  3. Atkinson MJ, Carlson B, Crowe JB (1995) Coral growth in high-nutrient, low pH seawater: a case study in coral growth at the Waikiki aquarium. Coral Reefs 14:215–233Google Scholar
  4. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  5. Cantin NE, Negri AP, Willis BL (2007) Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals. Mar Ecol Prog Ser 344:81–93CrossRefGoogle Scholar
  6. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325PubMedCrossRefGoogle Scholar
  7. Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127CrossRefGoogle Scholar
  8. Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: Insights into the biomineralization response to ocean acidification. Geochem Geophys Geosy 10:Q07005Google Scholar
  9. Cooper TF, De’ath G, Fabricius KE, Lough JM (2008) Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Global Change Biol 14:529–538CrossRefGoogle Scholar
  10. de Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2011) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs 30:321–328CrossRefGoogle Scholar
  11. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743CrossRefGoogle Scholar
  12. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: The other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  13. Edmunds PJ (2011) Zooplanktivory ameliorates the affects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410CrossRefGoogle Scholar
  14. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432CrossRefGoogle Scholar
  15. Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 42:606–611CrossRefGoogle Scholar
  16. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366PubMedCrossRefGoogle Scholar
  17. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509PubMedGoogle Scholar
  18. Goodbody-Gringley G, de Putron SJ (2009) Planulation patterns of the brooding coral, Favia fragum, in Bermuda. Coral Reefs 28:959–963CrossRefGoogle Scholar
  19. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  20. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  21. Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386:27–33CrossRefGoogle Scholar
  22. Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc 84:1–17PubMedCrossRefGoogle Scholar
  23. Houlbrèque F, Tambutte E, Ferrier-Pages C (2003) Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166CrossRefGoogle Scholar
  24. Houlbrèque F, Tambutte E, Allemand D, Ferrier-Pages C (2004) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. 207: 1461-1469Google Scholar
  25. Hughes TP, Jackson JBC (1985) Population-dynamics and life histories of foliaceous corals. Ecol Monogr 55:141–166CrossRefGoogle Scholar
  26. Kleypas J, Buddemeier R, Archer D, Gattuso J, Langdon C, Opdyke B (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120PubMedCrossRefGoogle Scholar
  27. Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res-Oceans 110:1–54CrossRefGoogle Scholar
  28. Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639–654CrossRefGoogle Scholar
  29. Lewis JB, Price WS (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. J Zool 176:527–544CrossRefGoogle Scholar
  30. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center Oak Ridge Natl Lab. US Dept of Energy, Oak Ridge, TNGoogle Scholar
  31. Marubini F, Atkinson MJ (1999) Effects of lowered pH and elevated nitrate on coral calcification. Mar Ecol Prog Ser 188:117–121CrossRefGoogle Scholar
  32. Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328CrossRefGoogle Scholar
  33. Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102CrossRefGoogle Scholar
  34. Mehrbach C, Culberso CH, Hawley JE, Pytkowic RM (1973) Measurement of apparent dissociation-constants of carbonic-acid in seawater at atmospheric-pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  35. Mucci A (1983) The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. Am J Sci 283:780–799CrossRefGoogle Scholar
  36. Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population-dynamics of zooxanthellae in a reef coral. Proc R Soc B-Biol Sci 236:311–324CrossRefGoogle Scholar
  37. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686PubMedCrossRefGoogle Scholar
  38. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422PubMedCrossRefGoogle Scholar
  39. Pelletier G, Lewis E, Wallace D (2007) CO2sys.xls: A Calculator for the CO2 System in Seawater for Microsoft Excel/VBA. Washington State Department of Ecology/Brookhaven National Laboratory, Olympia, WA/Upton, NY, USAGoogle Scholar
  40. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064CrossRefGoogle Scholar
  41. Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674CrossRefGoogle Scholar
  42. Rodrigues LJ, Grottoli AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim Cosmochim Acta 70:2781–2789CrossRefGoogle Scholar
  43. Rodrigues LJ, Grottoli A (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  44. Rylaarsdam KW (1983) Life histories and abundance patterns of colonial corals on Jamaican reefs. Mar Ecol Prog Ser 13:249–260CrossRefGoogle Scholar
  45. Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75CrossRefGoogle Scholar
  46. Silverman J, Lazar B, Erez J (2007) Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads. Biogeochemistry 84:67–82CrossRefGoogle Scholar
  47. Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 26:1–5Google Scholar
  48. Steinacher M, Joos F, Frölicher TL, Plattner G-K, Doney SC (2009) Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6:515–533. doi:10.5194/bg-6-515-2009 CrossRefGoogle Scholar
  49. Titlyanov EA, Tsukahara J, Titlyanova TV, Leletkin VA, van Woesik R, Yamazato K (2000a) Zooxanthellae population density and physiological state of the coral Stylophora pistillata during starvation and osmotic shock. Symbiosis 28:303–322Google Scholar
  50. Titlyanov E, Bil’ K, Fomina I, Titlyanova T, Leletkin V, Eden N, Malkin A, Dubinsky Z (2000b) Effects of dissolved ammonium addition and host feeding with Artemia salina on photoacclimation of the hermatypic coral Stylophora pistillata. Mar Biol 127:319–328Google Scholar
  51. Titlyanov EA, Titlyanova TV, Yamazato K, van Woesik R (2001) Photo-acclimation of the hermatypic coral Stylophora pistillata while subjected to either starvation or food provisioning. J Exp Mar Biol Ecol 257:163–181PubMedCrossRefGoogle Scholar
  52. Vermeij MJA, Sandin SA (2008) Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89:1994–2004PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • E. J. Drenkard
    • 1
    • 5
  • A. L. Cohen
    • 2
    • 6
  • D. C. McCorkle
    • 2
  • S. J. de Putron
    • 3
  • V. R. Starczak
    • 2
  • A. E. Zicht
    • 4
    • 7
  1. 1.Woods Hole Oceanographic Institution Joint Program in OceanographyMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Woods Hole Oceanographic InstitutionWoods HoleUSA
  3. 3.Bermuda Institute of Ocean SciencesSt. George’sBermuda
  4. 4.Oberlin CollegeOberlinUSA
  5. 5.Woods HoleUSA
  6. 6.Woods HoleUSA
  7. 7.Rutgers University Institute of Marine and Coastal SciencesNew BrunswickUSA

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