Marine Biology

, 163:99 | Cite as

Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod

  • Alistair G. B. Poore
  • Sarah E. Graham
  • Maria Byrne
  • Symon A. Dworjanyn
Original paper


Macroalgae support productive and diverse communities in marine habitats worldwide, but are threatened by changes to ocean conditions and altered interactions with marine herbivores. To better understand how non-calcifying macroalgae can persist in a changing ocean, we investigated the effects of co-occurring warming and ocean acidification on six species of temperate macroalgae, and subsequent change in palatability to a common gastropod herbivore. Algal growth was unaffected by moderate temperate increases of 2 °C, but five of the six species displayed reduced growth at increases of 4 °C. Lowered pH affected the growth of two species, with no interactions between temperature and pH evident. Changes to temperature and pH environment had little effect on the palatability of these algae to the gastropod Phasianotrochus eximius, with lowered pH increasing subsequent palatability for only one species of macroalgae. These results highlight the variation among algal species in their responses to changed ocean conditions and likely interactions with their consumers.


Macroalgae Algal Growth Algal Species Ocean Acidification Head Tank 
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.



This research was supported by grants from the New South Wales Environmental Trust, the Australian Research Council and the Evolution and Ecology Research Centre (UNSW). We thank Pamela Kamya, Katrina Kaposi, Ceiwen Pease, and Hannah Sheppard Brennand for assistance in the laboratory and in the field. The manuscript was improved by comments from the Associate Editor and two anonymous reviewers.

Supplementary material

227_2016_2878_MOESM1_ESM.pdf (47 kb)
Supplementary material 1 (PDF 47 kb)


  1. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550CrossRefGoogle Scholar
  2. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol Annu Rev 49:1–42Google Scholar
  3. Campbell AH, Harder T, Nielsen S, Kjelleberg S, Steinberg PD (2011) Climate change and disease: bleaching of a chemically defended seaweed. Glob Change Biol 17:2958–2970CrossRefGoogle Scholar
  4. Clark JS, Poore AGB, Ralph PJ, Doblin MA (2013) Potential for adaptation in response to thermal stress in an intertidal macroalga. J Phycol 49:630–639CrossRefGoogle Scholar
  5. Coleman MA, Kelaher BP, Steinberg PD, Millar AJK (2008) Absence of a large brown macroalga on urbanized rocky reefs around Sydney, Australia, and evidence for historical decline. J Phycol 44:897–901CrossRefGoogle Scholar
  6. 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. Proc R Soc Lond B Biol Sci 277:1409–1415CrossRefGoogle Scholar
  7. 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 B Biol Scie 368:20120442CrossRefGoogle Scholar
  8. Cook CM, Colman B (1987) Some characteristics of photosynthetic inorganic carbon uptake of a marine macrophytic red alga. Plant Cell Environ 10:275–278Google Scholar
  9. Cornwall CE, Revill AT, Hurd CL (2015) High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem. Photosynth Res 124:181–190CrossRefGoogle Scholar
  10. CSIRO and Bureau of Meteorology (2015) Climate change in Australia. Information for Australia’s natural resource management regions: Technical Report, CSIRO and Bureau of Meteorology, AustraliaGoogle Scholar
  11. Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286CrossRefGoogle Scholar
  12. Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony K (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162CrossRefGoogle Scholar
  13. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res 34:1733–1743CrossRefGoogle Scholar
  14. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:191Google Scholar
  15. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37CrossRefGoogle Scholar
  16. Falkenberg LJ, Russell BD, Connell SD (2013) Future herbivory: the indirect effects of enriched CO2 may rival its direct effects. Mar Ecol Prog Ser 492:85–95CrossRefGoogle Scholar
  17. Falkenberg LJ, Connell SD, Russell BD (2014) Herbivory mediates the expansion of an algal habitat under nutrient and CO2 enrichment. Mar Ecol Prog Ser 497:87–92CrossRefGoogle Scholar
  18. Farrant PA, King RJ (1989) The Dictyotales (Algae: Phaeophyta) of New South Wales. Proc Linnean Soc NSW 110:369–405Google Scholar
  19. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, Lonnstedt O, Chivers DP (2011) Putting prey and predator into the CO2 equation–qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecol Lett 14:1143–1148CrossRefGoogle Scholar
  20. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Dupont S, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Ruyssell BD, Sanford E, Schreiber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15CrossRefGoogle Scholar
  21. Guiry MD, Guiry GM (2015) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway.
  22. Gutow L, Rahman MM, Bartl K, Saborowski R, Bartsch I, Wiencke C (2014) Ocean acidification affects growth but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90CrossRefGoogle Scholar
  23. 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 48:1064–1078CrossRefGoogle Scholar
  24. 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
  25. Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshw Res 62:1000–1014CrossRefGoogle Scholar
  26. Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24:415–425CrossRefGoogle Scholar
  27. Hofmann LC, Bischof K (2014) Ocean acidification effects on calcifying macroalgae. Aquat Biol 22:261–279CrossRefGoogle Scholar
  28. Huisman JM (2000) Marine plants of Australia. University of Western Australia Press, NedlandsGoogle Scholar
  29. IPCC (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change (IPCC), United Kingdom and New York, USA, CambridgeGoogle Scholar
  30. Jansen P (1993) The family Trochidae (Mollusca: Gastropoda) in the Sydney metropolitan area and adjacent coast. Aust Zool 29:49–61CrossRefGoogle Scholar
  31. Jueterbock A, Kollias S, Smolina I, Fernandes JMO, Coyer JA, Olsen JL, Hoarau G (2014) Thermal stress resistance of the brown alga Fucus serratus along the North-Atlantic coast: acclimatization potential to climate change. Mar Genomics 13:27–36CrossRefGoogle Scholar
  32. Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19:103–132CrossRefGoogle Scholar
  33. Kraufvelin P, Lindholm A, Pedersen MF, Kirkerud LA, Bonsdorff E (2010) Biomass, diversity and production of rocky shore macroalgae at two nutrient enrichment and wave action levels. Mar Biol 157:29–47CrossRefGoogle Scholar
  34. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefGoogle Scholar
  35. Ling SD, Scheibling RE, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Pérez-Matus A, Hernández JC (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc Lond B Biol Sci 370:20130269CrossRefGoogle Scholar
  36. O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398CrossRefGoogle Scholar
  37. Olabarria C, Arenas F, Viejo RM, Gestoso I, Vaz-Pinto F, Incera M, Rubal M, Cacabelos E, Veiga P, Sobrino C (2013) Response of macroalgal assemblages from rockpools to climate change: effects of persistent increase in temperature and CO2. Oikos 122:1065–1079CrossRefGoogle Scholar
  38. Pearson GA, Lago-Leston A, Mota C (2009) Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populations. J Ecol 97:450–462CrossRefGoogle Scholar
  39. Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD (2011) Will variation among genetic individuals influence species responses to global climate change? Oikos 120:675–689CrossRefGoogle Scholar
  40. Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464Google Scholar
  41. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922CrossRefGoogle Scholar
  42. Poore AGB, Graba-Landry A, Favret M, Sheppard Brennand H, Byrne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction. Oecologia 173:1113–1124CrossRefGoogle Scholar
  43. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287CrossRefGoogle Scholar
  44. Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Change Biol 21:2122–2140CrossRefGoogle Scholar
  45. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106CrossRefGoogle Scholar
  46. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99CrossRefGoogle Scholar
  47. Steneck RS, Graham MH, Borque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  48. Sudatti DB, Fujii MT, Rodrigues SV, Turra A, Pereira RC (2011) Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Mar Biol 158:1439–1446CrossRefGoogle Scholar
  49. Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TBH (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125CrossRefGoogle Scholar
  50. Surif MB, Raven JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78:97–105CrossRefGoogle Scholar
  51. 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 13:1696–1709CrossRefGoogle Scholar
  52. Taylor RB, Steinberg PD (2005) Host use by Australasian seaweed mesograzers in relation to feeding preferences of larger grazers. Ecology 86:2955–2967CrossRefGoogle Scholar
  53. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira F, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Sen Gupta A, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc Lond B Biol Sci 281:20140846CrossRefGoogle Scholar
  54. Wahl M, Molis M, Hobday AJ, Dudgeon S, Neumann R, Steinberg PD, Campbell AH, Marzinelli E, Connell S (2015) The responses of brown macroalgae to environmental change from local to global scales: direct versus ecologically mediated effects. Perspect Phycol 2:11–30CrossRefGoogle Scholar
  55. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832CrossRefGoogle Scholar
  56. Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498CrossRefGoogle Scholar
  57. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3:78–82CrossRefGoogle Scholar
  58. Wirth D, Fischer-Lui I, Boland W, Icheln D, Runge T, König WA, Phillips J, Clayton M (1992) Unusual and novel C11H16 hydrocarbons from the southern Australian brown alga Dictyopteris acrostichoides (Phaeophyceae). Helv Chim Acta 75:734–744CrossRefGoogle Scholar
  59. Wright JT, de Nys R, Poore AGB, Steinberg PD (2004) Chemical defense in a marine alga: heritability and potential for selection by herbivores. Ecology 85:2946–2959CrossRefGoogle Scholar
  60. Xu Z, Zou D, Gao K (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–129CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alistair G. B. Poore
    • 1
  • Sarah E. Graham
    • 1
  • Maria Byrne
    • 2
  • Symon A. Dworjanyn
    • 3
  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Schools of Medical and Biological SciencesUniversity of SydneySydneyAustralia
  3. 3.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia

Personalised recommendations