Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    CAS  Article  Google Scholar 

  • 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 49:1–42

    Google Scholar 

  • Campbell AH, Harder T, Nielsen S, Kjelleberg S, Steinberg PD (2011) Climate change and disease: bleaching of a chemically defended seaweed. Glob Change Biol 17:2958–2970

    Article  Google Scholar 

  • Clark JS, Poore AGB, Ralph PJ, Doblin MA (2013) Potential for adaptation in response to thermal stress in an intertidal macroalga. J Phycol 49:630–639

    Article  Google Scholar 

  • Climate Change in Australia (2015) Marine Explorer http://www.climatechangeinaustralia.gov.au/en/climate-projections/coastal-marine/marine-explorer/

  • 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 44:897–901

    Article  Google Scholar 

  • 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 277:1409–1415

    Article  Google Scholar 

  • 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 368:20120442

    Article  Google Scholar 

  • Cook CM, Colman B (1987) Some characteristics of photosynthetic inorganic carbon uptake of a marine macrophytic red alga. Plant Cell Environ 10:275–278

    CAS  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • 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, Australia

  • Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286

    Article  Google Scholar 

  • Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony K (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162

    Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3:191

    Google Scholar 

  • 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 4:11–37

    Article  Google Scholar 

  • Falkenberg LJ, Russell BD, Connell SD (2013) Future herbivory: the indirect effects of enriched CO2 may rival its direct effects. Mar Ecol Prog Ser 492:85–95

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Farrant PA, King RJ (1989) The Dictyotales (Algae: Phaeophyta) of New South Wales. Proc Linnean Soc NSW 110:369–405

    Google Scholar 

  • 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 14:1143–1148

    Article  Google Scholar 

  • 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 96:3–15

    Article  Google Scholar 

  • Guiry MD, Guiry GM (2015) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org

  • 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 453:84–90

    CAS  Article  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshw Res 62:1000–1014

    Article  Google Scholar 

  • Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24:415–425

    Article  Google Scholar 

  • Hofmann LC, Bischof K (2014) Ocean acidification effects on calcifying macroalgae. Aquat Biol 22:261–279

    Article  Google Scholar 

  • Huisman JM (2000) Marine plants of Australia. University of Western Australia Press, Nedlands

    Google Scholar 

  • 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, Cambridge

  • Jansen P (1993) The family Trochidae (Mollusca: Gastropoda) in the Sydney metropolitan area and adjacent coast. Aust Zool 29:49–61

    Article  Google Scholar 

  • 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 13:27–36

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19:103–132

    Article  Google Scholar 

  • 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 157:29–47

    Article  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  Google Scholar 

  • 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 370:20130269

    Article  Google Scholar 

  • O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398

    Article  Google Scholar 

  • 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 122:1065–1079

    CAS  Article  Google Scholar 

  • 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 97:450–462

    Article  Google Scholar 

  • Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD (2011) Will variation among genetic individuals influence species responses to global climate change? Oikos 120:675–689

    Article  Google Scholar 

  • Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464

    Google Scholar 

  • 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 15:912–922

    Article  Google Scholar 

  • 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 173:1113–1124

    Article  Google Scholar 

  • Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287

    CAS  Article  Google Scholar 

  • 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 21:2122–2140

    Article  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106

    CAS  Article  Google Scholar 

  • Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99

    CAS  Article  Google Scholar 

  • 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 29:436–459

    Article  Google Scholar 

  • 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 158:1439–1446

    CAS  Article  Google Scholar 

  • Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TBH (2014) Evolution in an acidifying ocean. Trends Ecol Evol 29:117–125

    Article  Google Scholar 

  • 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 78:97–105

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Taylor RB, Steinberg PD (2005) Host use by Australasian seaweed mesograzers in relation to feeding preferences of larger grazers. Ecology 86:2955–2967

    Article  Google Scholar 

  • 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 281:20140846

    Article  Google Scholar 

  • 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 2:11–30

    Article  Google Scholar 

  • Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832

    CAS  Article  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498

    Article  Google Scholar 

  • 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 3:78–82

    Article  Google Scholar 

  • 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 75:734–744

    CAS  Article  Google Scholar 

  • Wright JT, de Nys R, Poore AGB, Steinberg PD (2004) Chemical defense in a marine alga: heritability and potential for selection by herbivores. Ecology 85:2946–2959

    Article  Google Scholar 

  • 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 53:123–129

    CAS  Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alistair G. B. Poore.

Additional information

Responsible Editor: P. Kraufvelin.

Reviewed by Undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 47 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Poore, A.G.B., Graham, S.E., Byrne, M. et al. Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod. Mar Biol 163, 99 (2016). https://doi.org/10.1007/s00227-016-2878-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2878-y

Keywords

  • Macroalgae
  • Algal Growth
  • Algal Species
  • Ocean Acidification
  • Head Tank