Advertisement

Oecologia

, Volume 173, Issue 3, pp 1113–1124 | Cite as

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

  • Alistair G. B. PooreEmail author
  • Alexia Graba-Landry
  • Margaux Favret
  • Hannah Sheppard Brennand
  • Maria Byrne
  • Symon A. Dworjanyn
Global change ecology - Original research

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.

Keywords

Acidification Warming Herbivory Multiple stressors Macroalgae 

Notes

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.

Supplementary material

442_2013_2683_MOESM1_ESM.pdf (128 kb)
Supplementary material 1 (PDF 128 kb)

References

  1. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91CrossRefGoogle Scholar
  2. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  3. 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:e35107PubMedCrossRefGoogle Scholar
  4. Burgess SC, Marshall DJ (2011) Temperature-induced maternal effects and environmental predictability. J Exp Biol 214:2329–2336PubMedCrossRefGoogle Scholar
  5. 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 49:1–42Google Scholar
  6. Byrne M et al (2011) Unshelled abalone and corrupted urchins: development of marine calcifies in a changing ocean. Proc R Soc Lond B 278:2376–2383CrossRefGoogle Scholar
  7. Caldeira K, Wicket ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04Google Scholar
  8. 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
  9. 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:e4929PubMedCrossRefGoogle Scholar
  10. 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 157:2489–2502CrossRefGoogle Scholar
  11. 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 277:1409–1415CrossRefGoogle Scholar
  12. 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 400:296–301CrossRefGoogle Scholar
  13. Cook K, Vanderklift MA, Poore AGB (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269CrossRefGoogle Scholar
  14. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315PubMedCrossRefGoogle Scholar
  15. Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286PubMedCrossRefGoogle Scholar
  16. Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN (2011) High CO2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162PubMedCrossRefGoogle Scholar
  17. 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
  18. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  19. 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 4:11–37CrossRefGoogle Scholar
  20. 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 58:1187–1191CrossRefGoogle Scholar
  21. Englund G, Öhlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921PubMedCrossRefGoogle Scholar
  22. 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 14:1143–1148PubMedCrossRefGoogle Scholar
  23. 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:e42497Google Scholar
  24. 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 120:661–674CrossRefGoogle Scholar
  25. 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 48:1064–1078CrossRefGoogle Scholar
  26. 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 296:2158–2162PubMedCrossRefGoogle Scholar
  27. Hauton C, Tyrrell T, Williams J (2009) The subtle effects of sea water acidification on the amphipod Gammarus locusta. Biogeosciences 6:1479–1489CrossRefGoogle Scholar
  28. Hays WL (1994) Statistics, 5th edn). Wadsworth, BelmontGoogle Scholar
  29. 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
  30. Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshw Res 62:1000–1014CrossRefGoogle Scholar
  31. 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 45:1236–1251CrossRefGoogle Scholar
  32. IPCC (2007) Climate change 2007: the fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, CambridgeGoogle Scholar
  33. 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 8:831–840CrossRefGoogle Scholar
  34. 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 52:904–913CrossRefGoogle Scholar
  35. 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 18:2792–2803CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 400:218–226CrossRefGoogle Scholar
  38. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434PubMedCrossRefGoogle Scholar
  39. 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 108:14515–14520PubMedCrossRefGoogle Scholar
  40. Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat Commun 3:704PubMedCrossRefGoogle Scholar
  41. 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 120–153CrossRefGoogle Scholar
  42. 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 142:591–619PubMedCrossRefGoogle Scholar
  43. 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 18:1540–1548CrossRefGoogle Scholar
  44. 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 18:897–907CrossRefGoogle Scholar
  45. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs: patterns and importance. Ecol Monogr 65:21–74CrossRefGoogle Scholar
  46. 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 348:162–173CrossRefGoogle Scholar
  47. 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 18:2466–2476CrossRefGoogle Scholar
  48. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398PubMedCrossRefGoogle Scholar
  49. Pease C, Johnston EL, Poore AGB (2010) Genetic variability in tolerance to copper contamination in a herbivorous marine invertebrate. Aquat Toxicol 99:10–16PubMedCrossRefGoogle Scholar
  50. Pennings SC, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619CrossRefGoogle Scholar
  51. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86Google Scholar
  52. 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
  53. Poore AGB, Lowry JK (1997) New ampithoid amphipods from Port Jackson, New South Wales, Australia (Crustacea: Amphipoda: Ampithoidae). Invert Taxon 11:897–941CrossRefGoogle Scholar
  54. 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
  55. Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62:21–38PubMedGoogle Scholar
  56. 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 97:164–175CrossRefGoogle Scholar
  57. 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 15:912–922PubMedCrossRefGoogle Scholar
  58. Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461CrossRefGoogle Scholar
  59. Ridgway KR (2007) Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett 34:L13613CrossRefGoogle Scholar
  60. Ridgway KR, Dunn JR, Wilkin JL (2002) Ocean interpolation by four-dimensional least squares -application to the waters around Australia. J Atmos Ocean Technol 19:1357–1375CrossRefGoogle Scholar
  61. 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 UnionGoogle Scholar
  62. 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 194:321–336PubMedCrossRefGoogle Scholar
  63. 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:e34737PubMedCrossRefGoogle Scholar
  64. 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:e11372PubMedCrossRefGoogle Scholar
  65. Sotka EE, Giddens H (2009) Seawater temperature alters feeding discrimination by cold-temperate but not subtropical individuals of an ectothermic herbivore. Biol Bull 216:75–84PubMedGoogle Scholar
  66. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99CrossRefGoogle Scholar
  67. Steinberg PD, Van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222CrossRefGoogle Scholar
  68. 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
  69. Suttle KB, Thomsen MA, Power ME (2007) Species interactions reverse grassland responses to changing climate. Science 315:640–642PubMedCrossRefGoogle Scholar
  70. 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
  71. Trenberth K (2012) Framing the way to relate climate extremes to climate change. Clim Change 115:283–290CrossRefGoogle Scholar
  72. Urabe J, Waki N (2009) Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets. Glob Change Biol 15:523–531CrossRefGoogle Scholar
  73. 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 417:159–170CrossRefGoogle Scholar
  74. 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 400:7–16CrossRefGoogle Scholar
  75. Wernberg T, Smale DA, Thomsen MS (2012a) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498CrossRefGoogle Scholar
  76. 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 3:78–82CrossRefGoogle Scholar
  77. Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271CrossRefGoogle Scholar
  78. 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 53:123–129CrossRefGoogle Scholar
  79. 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 145:895–903CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Alistair G. B. Poore
    • 1
    Email author
  • Alexia Graba-Landry
    • 2
  • Margaux Favret
    • 3
  • Hannah Sheppard Brennand
    • 2
  • Maria Byrne
    • 4
  • Symon A. Dworjanyn
    • 2
  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.National Marine Science CentreSouthern Cross UniversityCoffs HarbourAustralia
  3. 3.Agro Campus OuestPôle HalieutiqueRennes cedexFrance
  4. 4.Schools of Medical and Biological SciencesUniversity of SydneySydneyAustralia

Personalised recommendations