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Coral Reefs

, Volume 35, Issue 1, pp 357–368 | Cite as

Increased temperature mitigates the effects of ocean acidification in calcified green algae (Halimeda spp.)

  • Justin E. Campbell
  • Jay Fisch
  • Chris Langdon
  • Valerie J. Paul
Report

Abstract

The singular and interactive effects of ocean acidification and temperature on the physiology of calcified green algae (Halimeda incrassata, H. opuntia, and H. simulans) were investigated in a fully factorial, 4-week mesocosm experiment. Individual aquaria replicated treatment combinations of two pH levels (7.6 and 8.0) and two temperatures (28 and 31 °C). Rates of photosynthesis, respiration, and calcification were measured for all species both prior to and after treatment exposure. Pre-treatment measurements revealed that H. incrassata displayed higher biomass-normalized rates of photosynthesis and calcification (by 55 and 81 %, respectively) relative to H. simulans and H. opuntia. Furthermore, prior to treatment exposure, photosynthesis was positively correlated to calcification, suggesting that the latter process may be controlled by photosynthetic activity in this group. After treatment exposure, net photosynthesis was unaltered by pH, yet significantly increased with elevated temperature by 58, 38, and 37 % for H. incrassata, H. simulans, and H. opuntia, respectively. Both pH and temperature influenced calcification, but in opposing directions. On average, calcification declined by 41 % in response to pH reduction, but increased by 49 % in response to elevated temperature. Within each pH treatment, elevated temperature increased calcification by 23 % (at pH 8.0) and 74 % (at pH 7.6). Interactions between pH, temperature, and/or species were not observed. This work demonstrates that, in contrast to prior studies, increased temperature may serve to enhance the metabolic performance (photosynthesis and calcification) of some marine calcifiers, despite elevated carbon dioxide concentrations. Thus, in certain cases, ocean warming may mitigate the negative effects of acidification.

Keywords

Total Alkalinity Ocean Acidification Halimeda Calcify Alga CaCO3 Content 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Lane Johnston for assistance in the laboratory. This work was made possible through support from the Smithsonian Hunterdon Oceanographic Endowment and the Competitive Grants Program for Science. This is contribution no. 1013 from the Smithsonian Marine Station at Fort Pierce, FL.

References

  1. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446PubMedCentralCrossRefPubMedGoogle Scholar
  2. Atkinson MJ, Carlson B, Crow GL (1995) Coral growth in high-nutrient, low-pH seawater: a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14:215–223CrossRefGoogle Scholar
  3. Beach K, Walters L, Vroom P, Smith C, Coyer J, Hunter C (2003) Variability in the ecophysiology of Halimeda spp. (Chlorophyta, Bryopsidales) on Conch Reef, Florida Keys, USA. J Phycol 39:633–643CrossRefGoogle Scholar
  4. Borowitzka MA, Larkum AWD (1977) Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development. J Phycol 13:6–16Google Scholar
  5. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  6. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res Oceans 110:C09S04CrossRefGoogle Scholar
  7. Campbell J, Craft J, Muehllehner N, Langdon C, Paul V (2014) Responses of calcifying algae (Halimeda spp.) to ocean acidification: implications for herbivores. Mar Ecol Prog Ser 514:43–56CrossRefGoogle Scholar
  8. Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325CrossRefPubMedGoogle Scholar
  9. Castillo KD, Ries JB, Weiss JM, Lima FP (2012) Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat Clim Chang 2:756–760CrossRefGoogle Scholar
  10. Castillo KD, Ries JB, Bruno JF, Westfield IT (2014) The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming. Proc R Soc Lond B Biol Sci 281:20141856CrossRefGoogle Scholar
  11. Collins M, Knutti R, Arblaster J, Dufresne JL, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term climate change: projections, commitments and irreversibility In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Doschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds), Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UKGoogle Scholar
  12. Comeau S, Carpenter RC, Edmunds PJ (2012) Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate. Proc R Soc Lond B Biol Sci 280:20122374CrossRefGoogle Scholar
  13. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnol Oceanogr 58:388–398CrossRefGoogle Scholar
  14. Comeau S, Edmunds PJ, Lantz CA, Carpenter RC (2014) Water flow modulates the response of coral reef communities to ocean acidification. Sci Rep 4:6681PubMedCentralCrossRefPubMedGoogle Scholar
  15. 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. Glob Chang Biol 14:529–538CrossRefGoogle Scholar
  16. Cornwall CE, Hurd CL (2015) Experimental design in ocean acidification research: problems and solutions. ICES J Mar Sci. doi: 10.1093/icesjms/fsv118 Google Scholar
  17. Davies PS (1989) Short term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  18. De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119CrossRefPubMedGoogle Scholar
  19. De Beer D, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24:1209–1217CrossRefGoogle Scholar
  20. Deser C, Phillips AS, Alexander MA (2010) Twentieth century tropical sea surface temperature trends revisited. Geophys Res Lett 37:L10701CrossRefGoogle Scholar
  21. Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2012) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J Phycol 48:32–39CrossRefGoogle Scholar
  22. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part 1 Oceanogr Res Pap 34:1733–1743CrossRefGoogle Scholar
  23. Dove SG, Kline DI, Pantos O, Angly FE, Tyson GW, Hoegh-Guldberg O (2013) Future reef decalcification under a business-as-usual CO2 emission scenario. Proc Natl Acad Sci U S A 110:15342–15347PubMedCentralCrossRefPubMedGoogle Scholar
  24. Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Glob Chang Biol 18:2173–2183CrossRefGoogle Scholar
  25. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99CrossRefPubMedGoogle Scholar
  26. Hay ME, Paul VJ, Lewis SM, Gustafson K, Tucker J, Trindell RN (1988) Can tropical seaweeds reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia 75:233–245CrossRefGoogle Scholar
  27. Hofmann LC, Heiden J, Bischof K, Teichberg M (2014) Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) JV Lamouroux to low pH. Planta 239:231–242CrossRefPubMedGoogle Scholar
  28. Hofmann LC, Bischof K, Baggini C, Johnson A, Koop-Jakobsen K, Teichberg M (2015) CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte. Oecologia 177:1157–1169CrossRefPubMedGoogle Scholar
  29. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  30. Jensen PR, Gibson RA, Littler MM, Littler DS (1985) Photosynthesis and calcification in four deep water Halimeda species (Chlorophyceae, Caulerpales). Deep Sea Res Part 1 Oceanogr Res Pap 32:451–464CrossRefGoogle Scholar
  31. Johnson MD, Carpenter RC (2012) Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J Exp Mar Biol Ecol 434:94–101CrossRefGoogle Scholar
  32. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefPubMedGoogle Scholar
  33. Langdon C (2010) Determination of dissolved oxygen in seawater by Winkler titration using the amperometric technique. In: Hood EM, Sabine CL, Sloyan BM (eds). The GO-SHIP repeat hydrography manual: a collection of expert reports and guidelines. IOCCP Report Number 14, ICPO Publication Series Number 134, pp 1–18Google Scholar
  34. Lapointe BE, Littler MM, Littler DS (1987) A comparison of nutrient limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem. Aquat Bot 28:243–255CrossRefGoogle Scholar
  35. Larkum AWD, Salih A, Kühl M (2011) Rapid mass movement of chloroplasts during segment formation of the calcifying siphonalean green alga, Halimeda macroloba. PLoS One 6:e20841PubMedCentralCrossRefPubMedGoogle Scholar
  36. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TNGoogle Scholar
  37. Littler MM, Littler DS, Lapointe BE (1988) A comparison of nutrient-limited and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda (Caulerpales, Halimedaceae) from the Bahamas. Coral Reefs 6:219–225CrossRefGoogle Scholar
  38. Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243CrossRefPubMedGoogle Scholar
  39. Manzello DP, Enochs IC, Melo N, Gledhill DK, Johns EM (2012) Ocean acidification refugia of the Florida Reef Tract. PLoS One 7:e41715PubMedCentralCrossRefPubMedGoogle Scholar
  40. Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Chang Biol 15:2089–2100CrossRefGoogle Scholar
  41. Martin S, Castets MD, Clavier J (2006) Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquat Bot 85:121–128CrossRefGoogle Scholar
  42. Martin S, Clavier J, Chauvaud L, Thouzeau G (2007) Community metabolism in temperate maerl beds. I. Carbon and carbonate fluxes. Mar Ecol Prog Ser 335:19–29CrossRefGoogle Scholar
  43. Martin S, Cohu S, Vignot C, Zimmerman G, Gattuso JP (2013) One-year experiment on the physiological response of the Mediterranean crustose coralline alga, Lithophyllum cabiochae, to elevated pCO2 and temperature. Ecol Evol 3:676–693PubMedCentralCrossRefPubMedGoogle Scholar
  44. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  45. Meyer FW, Vogel N, Teichberg M, Uthicke S, Wild C (2015) The physiological response of two green calcifying algae from the Great Barrier Reef towards high dissolved inorganic and organic carbon (DIC and DOC) availability. PLoS One 10:e0133596PubMedCentralCrossRefPubMedGoogle Scholar
  46. Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T, Meehl GA, Mitchell JFB, Nakicenovic N, Riahi K, Smith SJ, Stouffer RJ, Thomson AM, Weyant JP, Wilbanks TJ (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756CrossRefPubMedGoogle Scholar
  47. Muehllehner N, Edmunds PJ (2008) Effects of ocean acidification and increased temperature on skeletal growth of two scleractinian corals, Pocillopora meandrina and Porites rus. Proc 11th Int Coral Reef Symp 1:57–61Google Scholar
  48. Noisette F, Duong G, Six C, Davoult D, Martin S (2013) Effects of elevated pCO2 on the metabolism of a temperate rhodolith Lithothamnion corallioides grown under different temperatures. J Phycol 49:746–757CrossRefGoogle Scholar
  49. 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 437:681–686CrossRefPubMedGoogle Scholar
  50. Payri CE (1988) Halimeda contribution to organic and inorganic production in a Tahitian reef system. Coral Reefs 6:251–262CrossRefGoogle Scholar
  51. Potin P, Floch JY, Augris C, Cabioch J (1990) Annual growth rate of the calcareous red alga Lithothamnion corallioides (Corallinales, Rhodophyta) in the Bay of Brest, France. Hydrobiologia 204:263–267CrossRefGoogle Scholar
  52. Price NN, Hamilton SL, Tootell JS, Smith JE (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440:67–78CrossRefGoogle Scholar
  53. Rees SA, Opdyke BN, Wilson PA, Henstock TJ (2007) Significance of Halimeda bioherms to the global carbonate budget based on a geological sediment budget for the northern Great Barrier Reef, Australia. Coral Reefs 26:177–188CrossRefGoogle Scholar
  54. Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagés C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668CrossRefGoogle Scholar
  55. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  56. Rodolfo-Metalpa R, Houlbreque F, Tambutte E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1:308–312CrossRefGoogle Scholar
  57. Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293CrossRefGoogle Scholar
  58. Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56:1200–1212CrossRefGoogle Scholar
  59. Sinutok S, Hill R, Doblin MA, Kuhl M, Ralph PJ (2012) Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming. Coral Reefs 31:1201–1213CrossRefGoogle Scholar
  60. Suggett DJ, Dong LF, Lawson T, Lawrenz E, Torres L, Smith DJ (2013) Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32:327–337CrossRefGoogle Scholar
  61. Van Tussenbroek BI, van Dijk JK (2007) Spatial and temporal variability in biomass and production of psammophytic Halimeda incrassata (Bryopsidales, Chlorophyta) in a Caribbean reef lagoon. J Phycol 43:69–77CrossRefGoogle Scholar
  62. Verbruggen H, Kooistra W (2004) Morphological characterization of lineages within the calcified tropical seaweed genus Halimeda (Bryopsidales, Chlorophyta). Eur J Phycol 39:213–228CrossRefGoogle Scholar
  63. Vogel N, Meyer F, Wild C, Uthicke S (2015a) Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms. Mar Ecol Prog Ser 521:49–61CrossRefGoogle Scholar
  64. Vogel N, Fabricius KE, Strahl J, Noonan SHC, Wild C, Uthicke S (2015b) Calcareous green alga Halimeda tolerates ocean acidification conditions at tropical carbon dioxide seeps. Limnol Oceanogr 60:263–275CrossRefGoogle Scholar
  65. Vroom P, Smith C, Coyer J, Walters L, Hunter C, Beach K, Smith J (2003) Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: comparative growth, survivorship, recruitment, and reproduction. Hydrobiologia 501:149–166CrossRefGoogle Scholar
  66. Wizemann A, Meyer FW, Westphal H (2014) A new model for the calcification of the green macro-alga Halimeda opuntia (Lamouroux). Coral Reefs 33:951–964CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Justin E. Campbell
    • 1
  • Jay Fisch
    • 2
  • Chris Langdon
    • 2
  • Valerie J. Paul
    • 1
  1. 1.Smithsonian Marine StationFort PierceUSA
  2. 2.Corals and Climate Change Laboratory, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA

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