Abstract
Projected ocean acidification will have a detrimental impact on coral reef ecosystems, where fleshy algae are expected to replace corals. Of particular importance to reef ecosystems are fleshy turf algal communities, which have the potential to overgrow corals; few studies have investigated the community structure and diversity of turfs to climate change. Here, we assessed the response of reef-associated turf algal communities from the Great Barrier Reef, Australia to three levels of ocean acidification. Biomass of turf communities was positively affected by increases in carbon dioxide (CO2), where turf communities grown under high CO2 had the greatest biomass. No effect of CO2 was found on mean turf organic content or genus richness. By contrast, turf community evenness and diversity (H′) increased under medium and high CO2 treatments. Our results indicate that increased turf growth under high CO2 will aid the overall expansion and growth of fleshy macroalgae in coral reef ecosystems, as opportunistic algae may have an advantage over other reef-associated species. Changes in turf community diversity will help provide insight into how macroalgal communities may be structured in the future, highlighting genera primed to take advantage of the changes in ocean chemistry associated with ocean acidification.
Similar content being viewed by others
References
Airoldi L, Rindi F, Cinelli F (1995) Structure, seasonal dynamics and reproductive phenology of a filamentous turf assemblage on a sediment influenced, rocky subtidal shore. Bot Mar 38:227–238
Alsterberg C, Eklöf JS, Gamfeldt L et al (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. PNAS 110:8603–8608. doi:10.1073/pnas.1303797110
Anthony KR, Kline DI, Diaz-Pulido G et al (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci 105:17442–17446
Anthony K, Maynard JA, Diaz-Pulido G et al (2011) Ocean acidification and warming will lower coral reef resilience. Glob Change Biol 17:1798–1808
Baggini C, Issaris Y, Salomidi M, Hall-Spencer J (2015) Herbivore diversity improves benthic community resilience to ocean acidification. J Exp Mar Biol Ecol 469:98–104. doi:10.1016/j.jembe.2015.04.019
Bender D, Diaz-Pulido G, Dove S (2014) Warming and acidification promote cyanobacterial dominance in turf algal assemblages. Mar Ecol Prog Ser 517:271–284
Bender D, Champ CM, Kline D et al (2015) Effects of “reduced” and “business-as-usual” CO2 emission scenarios on the algal territories of the damselfish Pomacentrus wardi (Pomacentridae). PLoS ONE 10:e0131442
Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414
Carilli JE, Norris RD, Black BA et al (2009) Local stressors reduce coral resilience to bleaching. PLoS ONE 4:e6324
Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–364
Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. In: Proceedings of the Royal Society of London B: Biological Sciences rspb20092069
Connell SD, Kroeker KJ, Fabricius KE et al (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc B Biol Sci 368:20120442
Connell SD, Foster MS, Airoldi L (2014) What are algal turfs? Towards a better description of turfs. Mar Ecol Prog Ser 495:299–307
Cornwall CE, Hepburn CD, Pritchard D et al (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48:137–144
Diaz-Pulido G, McCook LJ (2002) The fate of bleached corals: patterns and dynamics of algal recruitment. Mar Ecol Prog Ser 232:115–128
Diaz-Pulido G, Gouezo M, Tilbrook B et al (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci Journal du Conseil 65:414–432
Falkenberg LJ, Connell SD, Russell BD (2014) Herbivory mediates the expansion of an algal habitat under nutrient and CO2 enrichment. Mar Ecol Prog Ser 497:87–92
Feely RA, Sabine CL, Lee K et al (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366
Fricke A, Teichberg M, Nugues MM et al (2014) Effects of depth and ultraviolet radiation on coral reef turf algae. J Exp Mar Biol Ecol 461:73–84
Gao K, Aruga Y, Asada K et al (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. J Appl Phycol 3:355–362
Ghedini G, Russell BD, Connell SD (2015) Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecol Lett 18:182–187. doi:10.1111/ele.12405
Gil MA, Jiao J, Osenberg CW (2015) Enrichment scale determines herbivore control of primary producers. Oecologia 180:833–840. doi:10.1007/s00442-015-3505-1
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
Gutow L, Rahman MM, Bartl K et al (2014) Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90
Hall-Spencer JM, Rodolfo-Metalpa R, Martin S et al (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99
Harley CD, Randall Hughes A, Hultgren KM et al (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241
Hepburn CD, Pritchard DW, Cornwall CE et al (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17:2488–2497
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528
Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hofmann GE, Smith JE, Johnson KS et al (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6:e28983
Hurd CL, Hepburn CD, Currie KI et al (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J Phycol 45:1236–1251
Johnston AM (1991) The acquisition of inorganic carbon by marine macroalgae. Can J Bot 69:1123–1132
Johnson MD, Price NN, Smith JE (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411
Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2005) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. In: Report of a workshop held 18–20 April 2005, St. Petersburg, FL, USA, p 88
Klumpp DD, McKinnon DA, Daniel PP (1987) Damselfish territories: zones of high productivity on coral reefs. Mar Ecol Progres Ser 40:41–51
Klumpp DD, McKinnon DA (1992) Community structure, biomass and productivity of epilithic algal communities on the Great Barrier Reef: dynamics at different spatial scales. Mar Ecol Progres Ser 86:77–89
Kroeker KJ, Micheli F, Gambi MC (2013) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Change 3:156–159
Kübler JE, Johnston 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 et al (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117
Magnusson G, Larsson C, Axelsson L (1996) Effects of high CO2 treatment on Nitrate and ammonium uptake by Ulva lactuca grown in different nutrient regimes. Sci Mar 60:179–189
McSkimming C, Tanner JE, Russell BD, Connell SD (2015) Compensation of nutrient pollution by herbivores in seagrass meadows. J Exp Mar Biol Ecol 471:112–118. doi:10.1016/j.jembe.2015.05.018
Meinshausen M, Smith SJ, Calvin K et al (2011) The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim Change 109:213–241
Menge BA (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–289
Morrison D (1988) Comparing fish and urchin grazing in shallow and deeper coral reef algal communities. Ecology 69:1367–1382
Moss RH, Edmonds JA, Hibbard KA et al (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756
Nagelkerken I, Russell BD, Gillanders BM, Connell SD (2015) Ocean acidification alters fish populations indirectly through habitat modification. Nat Clim Change. doi:10.1038/nclimate2757
Olischläger M, Wiencke C (2013) Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J Exp Bot 64:5587–5597. doi:10.1093/jxb/ert329
Orr JC, Fabry VJ, Aumont O et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Pachauri RK, Allen MR, Barros VR et al (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, Switzerland
Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326. doi:10.1038/307321a0
Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287
Porzio 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
Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746
Raven J (1997) Putting the C in phycology. Eur J Phycol 32:319–333
Raven JA, Beardall J (2003) Carbon acquisition mechanisms of algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwar Academic Publishers, Dordrect, pp 225–244
Raven JA, Johnston AM, Kübler JE et al (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378
Raven JA, Ball LA, Beardall J et al (2005) Algae lacking carbon-concentrating mechanisms. Can J Bot 83:879–890
Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134
Russell BD, Thompson J-AI, 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
Sabine CL, Feely RA, Gruber N et al (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371
Schram JB, Amsler MO, Amsler CD et al (2016) Antarctic crustacean grazer assemblages exhibit resistance following exposure to decreased pH. Mar Biol 163:106. doi:10.1007/s00227-016-2894-y
Swanson AK, Fox CH (2007) Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal food webs. Glob Change Biol 13:1696–1709
Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76
Venera-Ponton DE, Diaz-Pulido G, McCook LJ, Rangel-Campo A (2011) Macroalgae reduce growth of juvenile corals but protect them from parrotfish damage. Mar Ecol Prog Ser 421:109–115
Vermeij MJ, Van Moorselaar I, Engelhard S et al (2010) The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS ONE 5:e14312
Waldbusser GG, Hales B, Langdon CJ et al (2015) Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nat Clim Change 5:273–280
Westphalen G, Cheshire AC (1997) Quantum efficiency and photosynthetic production of a temperate turf algal community. Aust J Bot 45:343–349
Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. In: Elsevier oceanography series, 65. Elsevier, Amsterdam, London, New York.
Acknowledgments
We thank Patrick Gartrell, Carlos del Mónaco, Alexandra Ordoñez Alvarez, and Bonnie Lewis for their support throughout the project. This material is based on work supported by the National Science Foundation under Grant No. OISE-1209497. This material is based upon work supported in part by the National Science Foundation EPSCoR Cooperative Agreement #EPS-1004057. Support was provided by an Australian Research Council Grant (ARC DP120101778) awarded to Dr. Guillermo Diaz-Pulido.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Gordon Ober, Dr. Guillermo Diaz-Pulido, and Dr. Carol Thornber declare that they have no conflict of interest.
Ethical standard
This study was funded by the National Science Foundation under Grant No. OISE-1209497 (awarded to Gordon Ober), the National Science Foundation EPSCoR Cooperative Agreement #EPS-1004057 (awarded to Gordon Ober), and Australian Research Council Grant (ARC DP120101778) awarded to Dr. Guillermo Diaz-Pulido. This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Responsible Editor: S. Connell.
Reviewed by undisclosed experts.
Rights and permissions
About this article
Cite this article
Ober, G.T., Diaz-Pulido, G. & Thornber, C. Ocean acidification influences the biomass and diversity of reef-associated turf algal communities. Mar Biol 163, 204 (2016). https://doi.org/10.1007/s00227-016-2978-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2978-8