Abstract
Macroalgae are generally used as indicators of coral reef status; thus, understanding the drivers and mechanisms leading to increased macroalgal abundance are of critical importance. Ocean acidification (OA) due to elevated carbon dioxide (CO2) concentrations has been suggested to stimulate macroalgal growth and abundance on reefs. However, little is known about the physiological mechanisms by which reef macroalgae use CO2 from the bulk seawater for photosynthesis [i.e., (1) direct uptake of bicarbonate (HCO3 −) and/or CO2 by means of carbon concentrating mechanisms (CCM) and (2) the diffusive uptake of CO2], which species could benefit from increased CO2 or which habitats may be more susceptible to acidification-induced algal proliferations. Here, we provide the first quantitative examination of CO2-use strategies in coral reef macroalgae and provide information on how the proportion of species and the proportional abundance of species utilising each of the carbon acquisition strategies varies across a gradient of terrestrial influence (from inshore to offshore reefs) in the Great Barrier Reef (GBR). Four macroalgal groups were identified based on their carbon uptake strategies: (1) CCM-only (HCO3 − only users); (2) CCM-HCO3 −/CO2 (active uptake HCO3 − and/or CO2 use); (3) Non-CCM species (those relying on diffusive CO2 uptake); and (4) Calcifiers. δ13C values of macroalgae, confirmed by pH drift assays, show that diffusive CO2 use is more prevalent in deeper waters, possibly due to low light availability that limits activity of CCMs. Inshore shallow reefs had a higher proportion of CCM-only species, while reefs further away from terrestrial influence and exposed to better water quality had a higher number of non-CCM species than inshore and mid-shelf reefs. As non-CCM macroalgae are more responsive to increased seawater CO2 and OA, reef slopes of the outer reefs are probably the habitats most vulnerable to the impacts of OA. Our results suggest a potentially important role of carbon physiology in structuring macroalgal communities in the GBR.
This is a preview of subscription content, access via your institution.







References
Anthony KRN, Diaz-Pulido G, Verlinden N, Tilbrook B, Andersson AJ (2013) Benthic buffers and boosters of ocean acidification on coral reefs. Biogeosciences 10:4897–4909
Bender D, Diaz-Pulido G, Dove SG (2014) The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects. J Phycol 50:203–215
Black CC, Bender MM (1976) δ13C values in marine organisms from the Great Barrier Reef. Aust J Plant Physiol 3:25–32
Brodie JE, Devlin M, Haynes D, Waterhouse J (2011) Assessment of the eutrophication status of the Great Barrier Reef Lagoon (Australia). Biogeochemistry 106:281–302
Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484
Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc Lond 368:20120442
Cornwall CE, Revill AT, Hurd CL (2015) High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem. Photosynth Res 124:181–190
Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, 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
De’ath G, Fabricius KE (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850
Diaz-Pulido G, Harii S, McCook LJ, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203–208
Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162
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 48:32–39
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. North Pacific Marine Science Organization (PICES Special Publication, 3), Sidney, British Columbia
Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar Coast 36:221–236
Enochs IC, Manzello DP, Donham EM, Kolodziej G, Okano R, Johnston L, Young C, Iguel J, Edwards CB, Fox MD, Valentino L, Johnson S, Benavente D, Clark SJ, Carlton R, Burton T, Eynaud Y, Price NN (2015) Shift from coral to macroalgae dominance on a volcanically acidified reef. Nature Clim Chang 5:1083–1088
Fabricius KE, De’ath G, McCook LJ, Turak E, Williams DM (2005) Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Mar Pollut Bull 51:384–398
Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner NGMS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim Chang 1:165–169
Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, Legrand H, Thompson A, Schaffelke B (2012) A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Pollut Bull 65:320–332
Fernandez PA, Hurd CL, Roleda MY (2014) Bicarbonate uptake via the anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. J Phycol 50:998–1008
Fry B, Lutes R, Northam M, Parker PL, Ogden JC (1982) A 13C/12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389–398
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
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
Hay ME (1981) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118:520–540
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
Hopkinson BM, Dupont CL, Allen AE, Morel FMM (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proc Natl Acad Sci USA 108:3830–3837
Hughes TP (1994) Catastrophes, phase-shifts and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: Considerations for experimental designs. J Phycol 45:1236–1251
Johnson MD, Price NN, Smith JE (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132
Kram SL, Price NN, Donham EM, Johnson MD, Kelly ELA, Hamilton SL, Smith JE (2016) Variable responses of temperate calcified and fleshy macroalgae to elevated pCO2 and warming. ICES J Mar Sci 73:693–703
Kübler JE, Dudgeon SR (2015) Predicting effects of ocean acidification and warming on algae lacking carbon concentrating mechanisms. PLoS One 10:e0132806
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
Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee
Linares C, Vidal M, Canals M, Kersting DK, Amblas D, Aspillaga E, Cebriįn E, Delgado-Huertas A, Dķaz D, Garrabou J, Hereu B, Navarro L, Teixidó N, Ballesteros E (2015) Persistent natural acidification drives major distribution shifts in marine benthic ecosystems. Proc R Soc B 282:20150587
Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492
Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography, and depth on delta C-13 and delta N-15 variation in a large collection of macroalgae. J Phycol 47:1023–1035
McCook LJ (1996) Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: cross-shelf transplants. Mar Ecol Prog Ser 139:179–192
McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367
McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563
Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845
Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923
Olischlager 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
Raven JA, Beardall J (2014) CO2 concentrating mechanisms and environmental change. Aquat Bot 118:24–37
Raven JA, Giordano M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296
Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005) Algae lacking carbon-concentrating mechanisms. Can J Bot 83:879–890
Raven JA, Johnston AM, Kübler JE, Korb R, Mcinroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378
Schaffelke B, Mellors J, Duke NC (2005) Water quality in the Great Barrier Reef region: responses of mangrove, seagrass and macroalgal communities. Mar Pollut Bull 51:279–296
Smith JE, Price NN, Nelson CE, Haas AF (2013) Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Mar Biol 160:2437–2447
Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe induced coral mortality. Ecol Lett 9:835–845
Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498
Stepien CC (2015) Impacts of geography, taxonomy and functional group on inorganic carbon use patterns in marine macrophytes. J Ecol 103:1372–1383
Uthicke S, Furnas MJ, Lųnborg C (2014) Coral reefs on the edge? Carbon chemistry on inshore reefs of the Great Barrier Reef. PLoS One 9:e109092
Wismer S, Hoey AS, Bellwood DR (2009) Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54
Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97
Acknowledgments
We are grateful for help in the field from A. Hoey and C.P. Arango. A. Ordoñez, and C. Barrón assisted with the carbonate chemistry analyses. To B. Fry for comments on the manuscript. support was provided by an ARC Grant (DP120101778) awarded to GDP. This research was conducted under permit G11/34560 from the Great Barrier Reef Marine Park Authority.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Anastazia Banaszak
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Diaz-Pulido, G., Cornwall, C., Gartrell, P. et al. Strategies of dissolved inorganic carbon use in macroalgae across a gradient of terrestrial influence: implications for the Great Barrier Reef in the context of ocean acidification. Coral Reefs 35, 1327–1341 (2016). https://doi.org/10.1007/s00338-016-1481-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-016-1481-5
Keywords
- Seaweeds
- Carbon dioxide
- Carbon concentrating mechanisms
- Ocean acidification
- Terrestrial runoff
- Great Barrier Reef