Abstract
The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.
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References
Airoldi L (2003) The effects of sedimentation on rocky coast assemblages. Ocean Mar Biol Annu Rev 41:161–263
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 105:17442–17446
Barry JP, Tyrrell T, Hansson L, Plattner GK, Gattuso JP (2010) Atmospheric CO2 targets for ocean acidification perturbation experiments. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, pp 53–66
Boyd PW (2011) Beyond ocean acidification. Nat Geosci 4:273–274
Ciais P, Sabine CL, Bala G, Bopp L, Brovkin V, Canadell J, Chhabra A, DeFries R, Galloway J, Heimann M, Jones C, Le Quêrê RB, Myneni RB, Piao S, Thornton P (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung 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, United Kingdon and New York, NY, USA
Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014) Diel pCO2 oscillations modulate the response of the coral Acropora hycinthus to ocean acidification. Mar Ecol Prog Ser 501:99–111
Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource amongst competitors for ecosystem dominance. Phil Trans R Soc B 368:20120442. doi:10.20121098/rstb.20122012.20120442
Cornwall CE, Hepburn CD, Pritchard DW, McGraw CM, Currie KI, Hunter KA, Hurd CL (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48:137–144
Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, Boyd PW, Hurd CL (2013a) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B 280:20132201. doi:10.1098/rspb.2013.2201
Cornwall CE, Hepburn CD, Pilditch CA, Hurd CL (2013b) Concentration boundary layers around complex assemblages of macroalgae: implications for the effects of ocean acidification on understorey coralline algae. Limnol Oceanogr 58:121–130
Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2011a) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J Phycol 48:32–39
Diaz-Pulido G, Gouzezo M, Tilbrook B, Dove S, Anthony K (2011b) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Let 14:156–162
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for Ocean CO2 measurements. North Pacific Marine Science Organization
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192
Doropoulos C, Ward S, Diaz-Pulido G, Hoegh-Guldberg O, Mumby PJ (2012) Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol Let 15:338–346
Dufault AM, Cumbo VR, Fan TY, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proc R Soc B 279:2951–2958
Dupont S, Pörtner HO (2013) Get ready for ocean acidification. Nature 498:429
Egilsdottir H, Noisette F, Noël LMLJ, Olafsson J, Martin S (2013) Effects of pCO2 on physiology and skeletal mineralogy in a tide pool coralline alga Corallina elongata. Mar Biol 160:2103–2112
Fabricius K, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Climate Change 1:165–169
Flynn KJ, Blackford JC, Baird ME, Raven JA, Clark DR, Beardall J, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nat Climate Change 2:510–513
Foster MS (1975) Algal succession in a Macrocystis pyrifera forest. Mar Biol 32:313–329
Frieder CA, Gonzalez JP, Bockmon EE, Navarro MO, Levin LA (2014) Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae? Glob Change Biol 20:754–764
Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, pp 41–51
Glas MS, Fabricius KE, De Beer D, Uthicke S (2012) The O2, pH and Ca2+ microenvironment of benthic foraminifera in a high CO2 world. PLoS ONE 7:e50010
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 454:96–99
Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064–1078
Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17:2488–2497
Hofmann LC, Straub S, Bischof K (2012a) Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar Ecol Prog Ser 464:89–105
Hofmann LC, Yildiz G, Hanelt D, Bischof K (2012b) Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol 159:783–792
Hunter KA (2007) SWCO2, http://neon.otago.ac.nz/research/mfc/people/keith_hunter/software/swco2/
Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing methods of ocean acidification on algal metabolism: consideration for experimental designs. J Phycol 45:1236–1251
Hurd CL, Cornwall CE, Currie KI, Hepburn CD, McGraw CM, Hunter KA, Boyd P (2011) Metabolically-induced pH fluctuations by some coastal calcifies exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility? Glob Change Biol 17:3254–3262
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 434–435:94–101
Johnson MD, Moriarty VW, Carpenter RC (2014) Acclimation of crustose coralline alga Porolithon onkodes to variable pCO2. PLoS ONE 9:e87678
Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, MacKenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and macroalgae. Glob Change Biol 19:103–132
Kroeker KJ, Gambi MC, Micheli F (2013a) Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc Natl Acad Sci USA 110:12721–12726
Kroeker KJ, Kordas RL, Crim RN, Hendriks IE, Ramajo L, Singh GG, Duarte CM, Gattuso JP (2013b) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896
Kroeker KJ, Micheli F, Gambi MC (2013c) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Climate Change 3:156–159
Kübler JE, Jonston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant, Cell Environ 22:1303–1310
Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, MacKenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117
Lawrence JM (1975) On the relationships between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286
Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100
Martin S, Rodolfo-Metalpa R, Ransome E, Rowley S, Buia MC, Gattuso JP, Hall-Spencer J (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4:689–692
McCoy SJ (2013) Morphology of the crustose coralline algal Pseudolithophyllum muricatum (Corallinales, Rhodophyta) responds to 30 years of ocean acidification in the Northeast Pacific. J Phycol 49:830–837
McCoy SJ, Pfister CA (2014) Historical comparisons reveal altered competitive interactions in a guild of crustose coralline algae. Ecol Let 17(4):475–483
McGraw CM, Cornwall CE, Reid MR, Currie KI, Hepburn CD, Boyd P, Hurd CL, Hunter KA (2010) An automated pH-controlled culture system for laboratory-based ocean acidification experiments. Limnol Oceanogr Methods 8:686–694
McNeil BI, Matear RJ (2008) Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proc Natl Acad Sci USA 105:18860–18864
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 18:897–907
Munguia P, Alenius B (2013) The role of preconditoning in ocean acidification experiments: a test with the intertidal isopod Paradella dianae. Mar Freshw Behav Physiol 46:33–44
Nelson WA (2009) Calcified macroalgae—critical to coastal ecosystems and vulnerable to change: a review. Mar Freshw Res 60:787–801
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 49:746–757
Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspectives on ocean acidification. Trends Ecol Evol 25:332–344
Porizo L, Garrard SL, Buia MC (2013) The effect of ocean acidification on early algal colonization stages at natural CO2 vents. Mar Biol 160:2247–2259
Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217
Ragazzola F, Foster LC, Form A, Anderson PSL, Hansteen TH, Fietzke J (2012) Ocean acidification weakens the structural integrity of coralline algae. Glob Change Biol 18:2804–2812
Rasband WS (1997) ImageJ. National Institutes of Health, Bethesda
Raven JA (2005) Ocean acidification due to increasing atmospheric carbon dioxide, 12/05, London
Raven JA, Giodarno M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296
Ries JB (2011) Skeletal mineralogy in a high-CO2 world. J Exp Mar Biol Ecol 403:54–64
Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134
Roberts RD (2001) A review of settlement cues for larval abalone (Haliotis spp.). J Shell Res 20:571–586
Roberts RD, Revsbech NP, Damgaard LR (2007) Effect of water velocity and benthic diatom morphology on the water chemistry experienced by postlarval abalone. J Shell Res 26:745–750
Rodolfo-Metalpa R, Houlbréque 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 Climate Change 1:308–312
Roleda MY, Hurd CL (2012) Seaweed responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin Heidelberg, pp 407–431
Rowley RJ (1989) Settlement and recruitment of sea urchins (Stronglocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes? Mar Biol 100:485–494
Russell BD, Thompson JI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15:2153–2162
Russell BD, Passarelli CA, Connell SD (2011) Forecasted CO2 modified the influence of light in shaping subtidal habitat. J Phycol 47:744–752
Scheibling RE, Robinson MC (2008) Settlement behaviour and early post-settlement predation of the sea urchin Strongylocentrotus droebachiensis. J Exp Mar Biol Ecol 365:59–66
Schiel DR (1988) Algal interactions on shallow subtidal reefs in northern New Zealand: a review. N Z J Mar Freshw Res 22:481–489
Shears NT, Babcock RC (2007) Quantitative description of mainland New Zealand’s shallow subtidal reef communities. In: Science for Conservation, vol 280. Science & Technical Pub., Department of Conservation
Smith AM, Sutherland JE, Kregting LT, Farr TJ, Winter DJ (2012) Phylomineralogy of the coralline red algae: correlation of skeletal mineralogy with molecular phylogeny. Phytochem 81:97–108
Sousa WP (2001) Natural disturbance and the dynamics of marine benthic communities. In: Bertness MD, Gaines S, Hay M (eds) Marine community ecology. Sinauer Assoc., Sunderland, pp 85–130
Steneck RS (1986) The ecology of coralline algal crusts: convergent patterns and adaptive strategies. Ann Rev Ecol System 17:273–303
Yildiz G, Hofmann LC, Bischof K, Dere S (2013) Ultraviolet radiation modulates the physiological responses of the calcified rhodophyte Corallina officinalis to elevated CO2. Bot Mar 56:161–168
Acknowledgments
The authors would like to thank Derek Richards, Robert Win, and Stewart Bell for all their help in the laboratory and field. We would also like to acknowledge the management committee of the East Otago Taiāpure (customary fishing reserve) within which the field component of this research was conducted. This project was funded by grants to CLH from the Royal Society of New Zealand Marsden Fund (UOO0914), Department of Botany Performance-Based Research (PBRF) Funding and a Foundation for Research, Science and Technology (FRST) subcontract from the National Institute of Water and Atmospheric Research Ltd., Biodiversity and Biosecurity OBI (C01X0502), and a FRST Te Tipu Putaiao Fellowship (UOOX0709) to CDH.
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Communicated by F. Bulleri.
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James, R.K., Hepburn, C.D., Cornwall, C.E. et al. Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification. Mar Biol 161, 1687–1696 (2014). https://doi.org/10.1007/s00227-014-2453-3
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DOI: https://doi.org/10.1007/s00227-014-2453-3