Photosynthesis Research

, Volume 124, Issue 2, pp 181–190 | Cite as

High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem

  • Christopher E. Cornwall
  • Andrew T. Revill
  • Catriona L. Hurd
Regular Paper


Productivity of most macroalgae is not currently considered limited by dissolved inorganic carbon (DIC), as the majority of species have CO2-concentrating mechanisms (CCM) allowing the active uptake of DIC. The alternative, diffusive uptake of CO2 (non-CCM), is considered rare (0–9 % of all macroalgal cover in a given ecosystem), and identifying species without CCMs is important in understanding factors controlling inorganic carbon use by eukaryotic algae. CCM activity has higher energetic requirements than diffusive CO2 uptake, therefore when light is low, CCM activity is reduced in favour of diffusive CO2 uptake. We hypothesized that the proportional cover of macroalgae without CCMs (red and green macroalgae) would be low (<10 %) across four sites in Tasmania, southern Australia at two depths (4–5 and 12–14 m); the proportion of species lacking CCMs would increase with decreasing depth; the δ13C values of macroalgae with CCMs would be more depleted with depth. We found the proportion of non-CCM species ranged from 0 to 90 % and included species from all three macroalgal phyla: 81 % of red (59 species), 14 % of brown (three species) and 29 % of green macroalgae (two species). The proportion of non-CCM species increased with depth at three of four sites. 35 % of species tested had significantly depleted δ13C values at deeper depths. Non-CCM macroalgae are more abundant in some temperate reefs than previously thought. If ocean acidification benefits non-CCM species, the ramifications for subtidal macroalgal assemblages could be larger than previously considered.


CCMs Climate change CO2-concentrating mechanisms Inorganic carbon acquisition Irradiance Seaweed 



We thank S. Ling, A. Fowles, F. Scott, D. Britton, E. Flukes, C. Layton, M. Cameron, M. Taksumi, J. Kean and T. Baulch for assistance in the field, laboratory or with identification of species. We also thank E. Flukes and C. Johnson for providing the irradiance estimates for Fortescue Bay. Samples were collected using the Department of Primary Industries, Parks, Water & Environment Tasmania permit number 13120.

Supplementary material

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Supplementary material 1 (DOCX 16 kb)
11120_2015_114_MOESM2_ESM.pdf (235 kb)
Supplementary material 2 (PDF 235 kb)
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Supplementary material 3 (DOCX 26 kb)
11120_2015_114_MOESM4_ESM.eps (1.3 mb)
Supplementary material 4 (EPS 1356 kb)


  1. Axelsson L (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar Biol 97:287–294CrossRefGoogle Scholar
  2. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  3. 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 et al (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, CambridgeGoogle Scholar
  4. Clementson LA, Parslow JS, Turnbull AR, Bonham PI (2004) Properties of light absorption in a highly coloured estuarine system in south-east Australia which is prone to blooms of the toxic dinoflagellate Gymondinium catenatum. Estuar Coast Shelf Sci 60:101–112CrossRefGoogle Scholar
  5. 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.
  6. Cornelisen CD, Wing SR, Clark KL, Bowman MH, Frew RD, Hurd CL (2007) Patterns in the δ13C and δ15N signature of Ulva pertusa: interaction between physical gradients and nutrient source pools. Limnol Oceanogr 52:820–832CrossRefGoogle Scholar
  7. 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 48:137–144CrossRefGoogle Scholar
  8. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for Ocean CO2 measurements. North Pacific Marine Science Organization, SidneyGoogle Scholar
  9. Dunton KH (2001) δ15N and δ13C measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41(1):99–112CrossRefGoogle Scholar
  10. Fischer G, Wiencke C (1992) Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region. Polar Biol 12:341–348CrossRefGoogle Scholar
  11. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131CrossRefPubMedGoogle Scholar
  12. 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
  13. 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 17:2488–2497CrossRefGoogle Scholar
  14. Kevekordes K, Holland D, Häbner N, Jenkins S, Kos R, Roberts S, Raven JA, Scrimgeour CM, Shelly K, Stojkovic S, Beardall J (2006) Inorganic carbon acquisition by eight species of Caulerpa (Caulerpaceae, Chlorophyta). Phycologia 45:442–449CrossRefGoogle Scholar
  15. Korb RE, Raven JA, Johnston AM, Leftley JW (1996) Effects of cell size and specific growth rate on stable carbon isotope discrimination by two species of marine diatom. Mar Ecol Prog Ser 143:283–288CrossRefGoogle Scholar
  16. Kroeker KJ, Kordas RL, Crim RN, Hendriks IE, Ramajo L, Singh GG, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19(6):1884–1896CrossRefGoogle Scholar
  17. Kübler JE, Raven JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Mar Ecol Prog Ser 110:203–209CrossRefGoogle Scholar
  18. Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant, Cell Environ 22:1303–1310CrossRefGoogle Scholar
  19. Lee D, Carpenter SJ (2001) Isotopic disequilibrium in marine calcareous algae. Chem Geol 172:307–329CrossRefGoogle Scholar
  20. Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513–518CrossRefGoogle Scholar
  21. Lüning K, Dring MJ (1979) Continuous underwater light measurements near Helgoland (North Sea) and its significance for characteristic light limits in the sublittoral region. Helgol Mar Res 32:403–424Google Scholar
  22. Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. Phycologia 26:439–449CrossRefGoogle Scholar
  23. Maberly SC, Madsen TV (1998) Affinity for CO2 in relation to the ability go freshwater macrophytes to use HCO3 . Funct Ecol 12:99–106CrossRefGoogle Scholar
  24. Maberly SC, Berthelot SA, Stott AW, Gontero B (2014) Adaptation by macrophytes to inorganic carbon down river with naturally variable concentrations of CO2. J Plant Phys 172:120–127CrossRefGoogle Scholar
  25. Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography, and depth on δ13C and δ15N variation in a large collection of macroalgae. J Phycol 47:1023–1035CrossRefGoogle Scholar
  26. 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 40:837–845CrossRefGoogle Scholar
  27. Nelson W, Neill K, D’Archino R, Anderson T, Beaumont J, Dalen J (2014) Beyond diving depths: deepwater macroalgae in the New Zealand region. Mar Biodiv. doi: 10.1007/s1256-014-0293-5 Google Scholar
  28. R Core Development Team (2008) R: a language and environment for statistical computing. 2.7.0 edn. R Foundation for Statistical Computing, ViennaGoogle Scholar
  29. Raven JA (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant, Cell Environ 14:779–794CrossRefGoogle Scholar
  30. Raven JA (1997) Putting the C in phycology. Eur J Phycol 32:319–333CrossRefGoogle Scholar
  31. Raven JA (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynth Res 106:123–134CrossRefPubMedGoogle Scholar
  32. Raven JA, Beardall J (2014) CO2 concentrating mechanisms and environmental change. Aquat Bot 118:24–37CrossRefGoogle Scholar
  33. Raven JA, Johnston AM, Kübler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Clayton MN, Vanderklift MA, Fredriksen S, Dunton KH (2002a) Seaweeds in cold seas: evolution and carbon acquisition. Ann Bot 90:525–536CrossRefPubMedCentralPubMedGoogle Scholar
  34. Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift MA, Fredriksen S, Dunton KH (2002b) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378CrossRefGoogle Scholar
  35. Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005a) Algae lacking carbon-concentrating mechanisms. Can J Bot 83:879–890CrossRefGoogle Scholar
  36. Raven JA, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005b) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society, LondonGoogle Scholar
  37. Raven JA, Giodarno M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296CrossRefPubMedGoogle Scholar
  38. Raven JA, Beardall J, Giordano M (2014) Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121:111–124CrossRefPubMedGoogle Scholar
  39. Runcie JW, Gurgel CFD, McDermid KJ (2008) In situ photosynthetic rates of tropical marine macroalgae at their lower depth limit. Eur J Phycol 43(4):377–388CrossRefGoogle Scholar
  40. Scott FJ (2012) Rare marine macroalgae of southern Australia. University of Tasmania, HobartGoogle Scholar
  41. Silberfeld T, Leight JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”. Mol Phylogenet Evol 56:659–674CrossRefPubMedGoogle Scholar
  42. Steneck RS, Graham MH, Bourque BJ, Corbett P, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  43. Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci 57:579–589CrossRefGoogle Scholar
  44. Wiencke C, Fischer G (1990) Growth and stable carbon isotop composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65:283–292CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Christopher E. Cornwall
    • 1
    • 2
  • Andrew T. Revill
    • 3
  • Catriona L. Hurd
    • 1
  1. 1.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  2. 2.School of Earth and Environment and Oceans Institute, ARC Centre of Excellence for Coral Reef StudiesUniversity of Western AustraliaCrawleyAustralia
  3. 3.CSIRO Oceans and AtmosphereHobartAustralia

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