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Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction

  • Global change ecology - Original research
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Abstract

The impacts of climatic change on organisms depend on the interaction of multiple stressors and how these may affect the interactions among species. Consumer–prey relationships may be altered by changes to the abundance of either species, or by changes to the per capita interaction strength among species. To examine the effects of multiple stressors on a species interaction, we test the direct, interactive effects of ocean warming and lowered pH on an abundant marine herbivore (the amphipod Peramphithoe parmerong), and whether this herbivore is affected indirectly by these stressors altering the palatability of its algal food (Sargassum linearifolium). Both increased temperature and lowered pH independently reduced amphipod survival and growth, with the impacts of temperature outweighing those associated with reduced pH. Amphipods were further affected indirectly by changes to the palatability of their food source. The temperature and pH conditions in which algae were grown interacted to affect algal palatability, with acidified conditions only affecting feeding rates when algae were also grown at elevated temperatures. Feeding rates were largely unaffected by the conditions faced by the herbivore while feeding. These results indicate that, in addition to the direct effects on herbivore abundance, climatic stressors will affect the strength of plant–herbivore interactions by changes to the susceptibility of plant tissues to herbivory.

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References

  • Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91

    Article  CAS  Google Scholar 

  • Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford

    Book  Google Scholar 

  • Arnold T, Mealey C, Leahey H, Miller AW, Hall-Spencer JM, Milazzo M, Maers K (2012) Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE 7:e35107

    Article  PubMed  CAS  Google Scholar 

  • Burgess SC, Marshall DJ (2011) Temperature-induced maternal effects and environmental predictability. J Exp Biol 214:2329–2336

    Article  PubMed  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. Ocean Mar Biol Ann Rev 49:1–42

    Google Scholar 

  • Byrne M et al (2011) Unshelled abalone and corrupted urchins: development of marine calcifies in a changing ocean. Proc R Soc Lond B 278:2376–2383

    Article  Google Scholar 

  • Caldeira K, Wicket ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    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 

  • Cebrian J, Shurin JB, Borer ET, Cardinale BJ, Ngai JT, Smith MD, Fagan WF (2009) Producer nutritional quality controls ecosystem trophic structure. PLoS ONE 4:e4929

    Article  PubMed  Google Scholar 

  • Cigliano M, Gambi MC, Rodolfo-Metalpa R, Patti FP, Hall-Spencer JM (2010) Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar Biol 157:2489–2502

    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 277:1409–1415

    Article  Google Scholar 

  • Connell SD, Russell BD, Irving AD (2011) Can strong consumer and producer effects be reconciled to better forecast ‘catastrophic’ phase-shifts in marine ecosystems? J Exp Mar Biol Ecol 400:296–301

    Article  Google Scholar 

  • Cook K, Vanderklift MA, Poore AGB (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269

    Article  Google Scholar 

  • Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37

    Article  Google Scholar 

  • Egilsdottir H, Spicer JI, Rundle SD (2009) The effect of CO2 acidified sea water and reduced salinity on aspects of the embryonic development of the amphipod Echinogammarus marinus (Leach). Mar Poll Bull 58:1187–1191

    Article  CAS  Google Scholar 

  • Englund G, Öhlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921

    Article  PubMed  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  PubMed  Google Scholar 

  • Foo SA, SA Dworjanyn, AGB Poore, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS ONE 7:e42497

  • Hale R, Calosi P, Mcneill L, Mieszkowska N, Widdicombe S (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674

    Article  Google Scholar 

  • Harley CD, 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

    Article  CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  PubMed  CAS  Google Scholar 

  • Hauton C, Tyrrell T, Williams J (2009) The subtle effects of sea water acidification on the amphipod Gammarus locusta. Biogeosciences 6:1479–1489

    Article  CAS  Google Scholar 

  • Hays WL (1994) Statistics, 5th edn). Wadsworth, Belmont

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • IPCC (2007) Climate change 2007: the fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, Cambridge

    Google Scholar 

  • Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of macroalgae grown under current and elevated seawater CO2 conditions. Glob Change Biol 8:831–840

    Article  Google Scholar 

  • Jiang ZJ, Huang X-P, Zhang J-P (2010) Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J Integ Plant Biol 52:904–913

    Article  CAS  Google Scholar 

  • Johnson VR, Russell BD, Fabricus KE, Brownless C, Hall-Spencer JM (2012) Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob Change Biol 18:2792–2803

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang X-H (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19(1):103–132. doi:10.1111/j.1365-2486.2012.02791.x

    Article  Google Scholar 

  • Kordas RL, Harley CDG, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226

    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  PubMed  Google Scholar 

  • Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011) Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc Natl Acad Sci USA 108:14515–14520

    Article  PubMed  CAS  Google Scholar 

  • Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:704

    Article  PubMed  Google Scholar 

  • Lindroth RL (2012) Atmospheric change, plant secondary metabolites and ecological interactions. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 120–153

    Chapter  Google Scholar 

  • Liu L, Heinrich M, Myers S, Dworjanyn SA (2012) Towards a better understanding of medicinal uses of the brown seaweed Sargassum in traditional Chinese medicine: a phytochemical and pharmacological review. J Ethnopharmacol 142:591–619

    Article  PubMed  Google Scholar 

  • Macnab VL, Barber I (2012) Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Glob Change Biol 18:1540–1548

    Article  Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74

    Article  Google Scholar 

  • Morelissen B, Harley CDG (2007) The effects of temperature on producers, consumers, and plant–herbivore interactions in an intertidal community. J Exp Mar Biol Ecol 348:162–173

    Article  Google Scholar 

  • Nguyen HD, Doo SS, Soars NA, Byrne M (2012) Noncalcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star Meridiastra calcar. Glob Change Biol 18:2466–2476

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Pease C, Johnston EL, Poore AGB (2010) Genetic variability in tolerance to copper contamination in a herbivorous marine invertebrate. Aquat Toxicol 99:10–16

    Article  PubMed  CAS  Google Scholar 

  • Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619

    Article  Google Scholar 

  • Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86

    Google Scholar 

  • Pierrot D, Lewis E, Wallace WR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a., Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee. doi:10.3334/CDIAC/otg.CO2SYS_XLS_CDIAC105a, Carbon Dioxide Information Analysis Center

  • Poore AGB, Lowry JK (1997) New ampithoid amphipods from Port Jackson, New South Wales, Australia (Crustacea: Amphipoda: Ampithoidae). Invert Taxon 11:897–941

    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, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62:21–38

    PubMed  Google Scholar 

  • Poore AGB, Campbell AH, Steinberg PD (2009) Natural densities of mesograzers fail to limit the growth of macroalgae or their epiphytes in a temperate algal bed. J Ecol 97:164–175

    Article  Google Scholar 

  • Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA, Duffy JE (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922

    Article  PubMed  Google Scholar 

  • Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461

    Article  CAS  Google Scholar 

  • Ridgway KR (2007) Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett 34:L13613

    Article  Google Scholar 

  • Ridgway KR, Dunn JR, Wilkin JL (2002) Ocean interpolation by four-dimensional least squares -application to the waters around Australia. J Atmos Ocean Technol 19:1357–1375

    Article  Google Scholar 

  • Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) (2010) Guide to best practices for ocean acidification research and data reporting. Luxembourg Publications Office of the European Union

  • Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336

    Article  PubMed  CAS  Google Scholar 

  • Rossoll D, Bermúdez R, Hauss H, Schulz KG, Riebesell U, Sommer U, Winder M (2012) Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7:e34737

    Article  PubMed  CAS  Google Scholar 

  • Sheppard Brennand H, Dworjanyn SA, Davis AR, Byrne M (2010) Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5:e11372

    Article  PubMed  Google Scholar 

  • Sotka EE, Giddens H (2009) Seawater temperature alters feeding discrimination by cold-temperate but not subtropical individuals of an ectothermic herbivore. Biol Bull 216:75–84

    PubMed  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

    Article  CAS  Google Scholar 

  • Steinberg PD, Van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    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

    Article  CAS  Google Scholar 

  • Suttle KB, Thomsen MA, Power ME (2007) Species interactions reverse grassland responses to changing climate. Science 315:640–642

    Article  PubMed  CAS  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 

  • Trenberth K (2012) Framing the way to relate climate extremes to climate change. Clim Change 115:283–290

    Article  Google Scholar 

  • Urabe J, Waki N (2009) Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets. Glob Change Biol 15:523–531

    Article  Google Scholar 

  • Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N). Mar Ecol Prog Ser 417:159–170

    Article  Google Scholar 

  • Wernberg T, Russell BD, Moore PJ et al (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400:7–16

    Article  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012a) 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 (2012b) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78–82

    Article  Google Scholar 

  • Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271

    Article  CAS  Google Scholar 

  • Xu ZG, Zou DH, Gao KS (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

    Article  CAS  Google Scholar 

  • Yee EH, Murray SN (2004) Effects of temperature on activity, food consumption rates, and gut passage times of seaweed-eating Tegula species (Trochidae) from California. Mar Biol 145:895–903

    Article  Google Scholar 

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Acknowledgments

This research was supported by grants from the New South Wales Environmental Trust and the Australian Research Council. A. Graba-Landry was supported by a scholarship from the Centre for Coastal Biogeochemistry, Southern Cross University. We thank Matheus Carvalho for assistance with carbon and nitrogen measurements, and Keryn Bain for assistance with phlorotannin measurements. This manuscript was improved by comments from Craig Osenberg, Steve Swearer, Thomas Wernberg and an anonymous reviewer.

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Authors and Affiliations

  1. Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

    Alistair G. B. Poore

  2. National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW, 2450, Australia

    Alexia Graba-Landry, Hannah Sheppard Brennand & Symon A. Dworjanyn

  3. Agro Campus Ouest, Pôle Halieutique, 65 rue de St-Brieuc, CS 84 215, 35042, Rennes cedex, France

    Margaux Favret

  4. Schools of Medical and Biological Sciences, University of Sydney, Sydney, NSW, 2006, Australia

    Maria Byrne

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  1. Alistair G. B. Poore
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  2. Alexia Graba-Landry
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  3. Margaux Favret
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  4. Hannah Sheppard Brennand
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  5. Maria Byrne
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  6. Symon A. Dworjanyn
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Correspondence to Alistair G. B. Poore.

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Communicated by Steve Swearer.

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Poore, A.G.B., Graba-Landry, A., Favret, M. et al. Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction. Oecologia 173, 1113–1124 (2013). https://doi.org/10.1007/s00442-013-2683-y

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