Skip to main content

Biological impacts of ocean acidification: a postgraduate perspective on research priorities

Abstract

Research into the effects of ocean acidification (OA) on marine organisms has greatly increased during the past decade, as realization of the potential dramatic impacts has grown. Studies have revealed the multifarious responses of organisms to OA conditions, indicating a high level of intra- and interspecific variation in species’ ability to accommodate these alterations. If we are to provide policy makers with sound, scientific input regarding the expected consequences of OA, we need a broader understanding of these predicted changes. As a group of 20 multi-disciplinary postgraduate students from around the globe, with a study focus on OA, we are a strong representation of ‘next generation’ scientists in this field. In this unique cumulative paper, we review knowledge gaps in terms of assessing the biological impacts of OA, outlining directions for future research.

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

References

  • Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–490

    Article  Google Scholar 

  • Allen HE (1993) The significance of trace metal speciation for water, sediment and soil quality criteria and standards. Sci Total Environ 134(Supplement 1):23–45

    Article  Google Scholar 

  • Allgaier M, Riebesell U, Vogt M, Thyrhaug R, Grossart HP (2008) Coupling of heterotrophic bacteria to phytoplankton bloom development at different pCO(2) levels: a mesocosm study. Biogeosciences 5:1007–1022

    CAS  Article  Google Scholar 

  • Andersson AJ, Kuffner IB, Mackenzie FT, Jokiel PL, Rodgers KS, Tan A (2009) Net Loss of CaCO3 from a subtropical calcifying community due to seawater acidification: mesocosm-scale experimental evidence. Biogeosciences 6:1811–1823

    CAS  Article  Google Scholar 

  • Ardelan MV, Steinnes E (2010) Changes in mobility and solubility of the redox sensitive metals Fe, Mn and Co at the seawater-sediment interface following CO2 seepage. Biogeosciences 7:569–583

    CAS  Article  Google Scholar 

  • Arnold KE, Findlay HS, Spicer JI, Daniels CL, Boothroyd D (2009) Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences 6:1747–1754

    CAS  Article  Google Scholar 

  • Barnes JH (1966) The crown-of-thorns starfish as a destroyer of corals. Aust Natural History 15:257–261

    Google Scholar 

  • Barry JP, Buck KR, Lovera CF, Kuhnz L, Whaling PJ, Peltzer ET, Walz P, Brewer PG (2004) Effects of direct ocean CO(2) injection on deep-sea meiofauna. J Oceanogr 60:759–766

    CAS  Article  Google Scholar 

  • Barry JP, Hall-Spencer J, Tyrrell T (2010) In situ perturbation experiments: natural venting sites, spatial/temporal gradients in ocean pH, manipulative in situ p(CO2) perturbations. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting, Luxembourg, pp 123–136

  • Becker WA (1984) Manual of quantitative genetics. Academic Enterprises, Pullman, Washington

    Google Scholar 

  • Bellerby RGJ, Schulz KG, Riebesell U, Neill C, Nondal G, Heegaard E, Johannessen T, Brown KR (2008) Marine ecosystem community carbon and nutrient uptake stoichiometry under varying ocean acidification during the PeECE III experiment. Biogeosciences 5:1517–1527

    CAS  Article  Google Scholar 

  • Bertness MD, Hacker SD (1994) Physical stress and positive associations among marsh plants. Am Natur 144:363–372

    Article  Google Scholar 

  • Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J (2007) Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol Lett 3:699–701

    Article  Google Scholar 

  • Bijlsma R, Loeschcke V (2005) Environmental stress, adaptation and evolution: an overview. J Evol Biol 18:744–749

    CAS  Article  Google Scholar 

  • Blackford JC, Gilbert FJ (2007) pH variability and CO(2) induced acidification in the North Sea. J Mar Syst 64:229–241

    Article  Google Scholar 

  • Brand LE, Sunda WG, Guillard RRL (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. J Exp Mar Biol Ecol 96:225–250

    CAS  Article  Google Scholar 

  • Breitbarth E, Achterberg EP, Ardelan MV, Baker AR, Bucciarelli E, Chever F, Croot P, Duggen S, Gledhill M, HassellÃv M, Hassler C, Hoffmann LJ, Hunter KA, Hutchins DA, Ingri J, Jickells T, Lohan MC, Nielsdóttir MC, Sarthou G, Schoemann V, Trapp JM, Turner DR, Ye Y (2010) Iron biogeochemistry across marine systems—progress from the past decade. Biogeosciences 7:1075–1097

    CAS  Article  Google Scholar 

  • Brennan ST, Lowenstein TK, Horita J (2004) Seawater chemistry and the advent of biocalcification. Geology 32:473–476

    CAS  Article  Google Scholar 

  • Brennand HS, Soars N, 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(6):e11372. doi:10.1371/journal.pone.0011372

    Article  CAS  Google Scholar 

  • Byrne RH (2002) Inorganic speciation of dissolved elements in seawater: the influence of pH on concentration ratios. Geochem Trans 3:11–16

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    CAS  Article  Google Scholar 

  • Carroll SP, Hendry AP, Reznick DN, Fox CW (2007) Evolution on ecological time-scales. Funct Ecol 21:387–393

    Article  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 (Berlin) 157:2489–2502

    Article  Google Scholar 

  • Comeau S, Gorsky G, Alliouane S, Gattuso JP (2010) Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Mar Biol 157:2341–2345

    CAS  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 B Biol Sci 277:1409–1415

    Article  Google Scholar 

  • Cooke IR, Queenborough SA, Mattison EHA, Bailey AP, Sandars DL, Graves AR, Morris J, Atkinson PW, Trawick P, Freckleton RP, Watkinson AR, Sutherland WJ (2009) Integrating socio-economics and ecology: a taxonomy of quantitative methods and a review of their use in agro-ecology. J Appl Ecol 46:269–277

    Article  Google Scholar 

  • Costanza R, d’Arge R, deGroot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, Oneill RV, Paruelo J, Raskin RG, Sutton P, vandenBelt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    CAS  Article  Google Scholar 

  • Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16:851–863

    Article  Google Scholar 

  • Cripps IL, Munday PL, McCormick MI (2011) Ocean acidification affects prey detection by a predatory reef fish. PLoS One 6

  • Crook E, Potts D, Rebolledo-Vieyra M, Hernandez L, Paytan A (2012) Calcifying coral abundance near low-pH springs: implications for future ocean acidification. Coral Reefs 31:239–245

    Article  Google Scholar 

  • Czerny J, Ramos JBE, Riebesell U (2009) Influence of elevated CO(2) concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosciences 6:1865–1875

    CAS  Article  Google Scholar 

  • Dahms HU, Dobretsov S, Qian PY (2004) The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J Exp Mar Biol Ecol 313:191–209

    Article  Google Scholar 

  • Dale AW, Prego R (2002) Physico-biogeochemical controls on benthic-pelagic coupling of nutrient fluxes and recycling in a coastal upwelling system. Mar Ecol Prog Ser 235:15–28

    Article  Google Scholar 

  • Danovaro R, Dell’Anno A, Corinaldesi C, Magagnini M, Noble R, Tamburini C, Weinbauer M (2008) Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454:1084–1087

    CAS  Article  Google Scholar 

  • Dayton PK (1971) Competition, disturbance, and community organization—provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Article  Google Scholar 

  • De Bodt C, Van Oostende N, Harlay J, Sabbe K, Chou L (2010) Individual and interacting effects of pCO(2) and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size. Biogeosciences 7:1401–1412

    Article  CAS  Google Scholar 

  • de Groot RS, Wilson MA, Boumans RMJ (2002) A typology for the classification, description and valuation of ecosystem functions, goods and services. Ecol Econ 41:393–408

    Article  Google Scholar 

  • Dissard D, Nehrke G, Reichart GJ, Bijma J (2010) Impact of seawater pCO(2) on calcification and Mg/Ca and Sr/Ca ratios in benthic foraminifera calcite: results from culturing experiments with Ammonia tepida. Biogeosciences 7:81–93

    CAS  Article  Google Scholar 

  • Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75

    Article  Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pitcher CR (2011) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Clim Change. doi:10.1038/nclimate1323

    Google Scholar 

  • Doney SC, Balch WM, Fabry VJ, Feely RA (2009) Ocean acidification: a critical emerging problem for the ocean sciences. Oceanography 22:16–25

    Article  Google Scholar 

  • Dupont S, Thorndyke M (2009) Impact of CO2-driven ocean acidification on invertebrates early life-history—what we know, what we need to know and what we can do. Biogeosciences 6:3109–3131 (discussions)

    Google Scholar 

  • Dupont S, Thorndyke MC (2012) Relationship between CO2-driven changes in extracellular acid–base balance and cellular immune response in two polar echinoderm species. J Exp Mar Biol Ecol 424–425:32–37

    Article  CAS  Google Scholar 

  • Dupont S, Dorey N, Thorndyke M (2010a) What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar Coast Shelf Sci 89:182–185

    Article  Google Scholar 

  • Dupont S, Lundve B, Thorndyke M (2010b) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J Exp Zool B Mol Dev Evol 314B:382–389

    Article  Google Scholar 

  • Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke MC (2012a) Long term and trans life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol. doi:10.1007/s00227-012-1921-x

    Google Scholar 

  • Dupont S, Moya A, Bailly X (2012b) Stable photosymbiotic relationship under CO2-induced acidification in the acoel worm Symsagittifera Roscoffensis. PLoS ONE 7:e29568. doi:29510.21371/journal.pone.0029568

    CAS  Article  Google Scholar 

  • E Ramos JB, Biswas H, Schulz KG, LaRoche J, Riebesell U (2007) Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeocheml Cycles 21:GB2028. doi:10.1029/2006GB002898

  • Engel A (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. J Plankton Res 24:49–53

    CAS  Article  Google Scholar 

  • Engel A, Schulz KG, Riebesell U, Bellerby R, Delille B, Schartau M (2008) Effects of CO(2) on particle size distribution and phytoplankton abundance during a mesocosm bloom experiment (PeECE II). Biogeosciences 5:509–521

    CAS  Article  Google Scholar 

  • Engel A, e’Ramos JB, Geider RJ, Hutchins DA, Lee C, Rost B, Rottgers R, Thingstad F (2010) Chapter 11 Production and export of organic matter. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim Change 1:165–169

    CAS  Article  Google Scholar 

  • Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432

    CAS  Article  Google Scholar 

  • Fabry VJ, McClintock JB, Mathis JT, Grebmeier JM (2009) Ocean acidification at high latitudes: the bell weather. Oceanography 22:160–171

    Article  Google Scholar 

  • Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1490–1492

    CAS  Article  Google Scholar 

  • Feely RA, Alin SR, Newton J, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci 88:442–449

    CAS  Article  Google Scholar 

  • Ferrari MCO, Dixson DL, Munday PL, McCormick MI, Meekan MG, Sih A, Chivers DP (2011a) Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities. Global Change Biol 17:2980–2986

    Article  Google Scholar 

  • Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, Lonnstedt O, Chivers DP (2011b) Putting prey and predator into the CO(2) equation—qualitative and quantitative effects of ocean acidification on predator-prey interactions. Ecol Lett 14:1143–1148

    Article  Google Scholar 

  • Findlay HS, Kendall MA, Spicer JI, Turley C, Widdicombe S (2008) Novel microcosm system for investigating the effects of elevated carbon dioxide and temperature on intertidal organisms. Aqua Biol 3:51–62

    Article  Google Scholar 

  • Findlay HS, Kendall MA, Spicer J, Widdicombe S (2010) Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution. Estuar Coast Shelf Sci 86:675–682

    CAS  Article  Google Scholar 

  • Fowler SW, Knauer GA (1986) Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog Oceanogr 16:147–194

    Article  Google Scholar 

  • Francois R, Honjo S, Krishfield R, Manganini S (2002) Factors controlling the flux of organic carbon to the bathypelagic zone of the ocean. Global Biogeochem Cycles 16:1087–2006

    Article  CAS  Google Scholar 

  • Frommel AY, Schubert A, Piatkowski U, Clemmesen C (2012) Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification. Mar Biol. doi:10.1007/s00227-011-1876-3

  • Fuhrman JA, Schwalbach MS, Stingl U (2008) Opinion—Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol 6:488–494

    CAS  Google Scholar 

  • Gagné F, Blaise C, Andre C (2006) Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicol Environ Saf 64:329–336

    Article  CAS  Google Scholar 

  • Gardner WD (2000) Sediment trap sampling in surface waters. In: Hanson RB, Ducklow HW, G FJ (eds) The changing carbon cycle: a midterm synthesis of joint ocean flux study. Cambridge University Press, Cambridge, pp 240–281

    Google Scholar 

  • Garren M, Azam F (2011) Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment. ISME J. doi:10.1038/ismej.2011.1180

    Google Scholar 

  • Gattuso JP, Lavigne H (2009) Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121–2133

    CAS  Article  Google Scholar 

  • Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: U R, VJ F, L H, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg

  • Gaylord B, Hill TM, Sanford E, Lenz EA, Jacobs LA, Sato KN, Russell AD, Hettinger A (2011) Functional impacts of ocean acidification in an ecologically critical foundation species. J Exp Biol 214:2586–2594

    CAS  Article  Google Scholar 

  • Gazeau F, Quiblier C, Jansen JM, Gattuso JP, Middelburg JJ, Heip CHR (2007) Impact of elevated CO2 on shellfish calcification. Geophys Res Lett 34

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    CAS  Article  Google Scholar 

  • Gooding RA, Harley CDG, Tang E (2009) Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proc Nat Acad Sci USA 106:9316–9321

    CAS  Article  Google Scholar 

  • Gracey AY (2007) Interpreting physiological responses to environmental change through gene expression profiling. J Exp Biol 210:1584–1592

    CAS  Article  Google Scholar 

  • Grime JP (1997) Biodiversity and ecosystem function: the debate deepens. Science 277:1260–1261

    CAS  Article  Google Scholar 

  • Grossart HP, Allgaier M, Passow U, Riebesell U (2006) Testing the effect of CO2 concentration on the dynamics of marine heterotrophic bacterioplankton. Limnol Oceanogr 51:1–11

    CAS  Article  Google Scholar 

  • Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems year in ecology and conservation biology 2008. Blackwell, Oxford, pp 320–342

    Google Scholar 

  • Gutierrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90

    Article  Google Scholar 

  • Gutowska MA, Melzner F, Portner HO, Meier S (2010) Cuttlebone calcification increases during exposure to elevated seawater pCO(2) in the cephalopod Sepia officinalis. Mar Biol 157:1653–1663

    CAS  Article  Google Scholar 

  • 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 

  • 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 454:96–99

    CAS  Article  Google Scholar 

  • Havenhand JN, Buttler FR, Thorndyke MC, Williamson JE (2008) Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr Biol 18:R651–R652

    CAS  Article  Google Scholar 

  • Hewson I, Brown JM, Burge CA, Couch CS, LaBarre BA, Mouchka ME, Naito M, Harvell CD (2011) Description of viral assemblages associated with the Gorgonia ventalina holobiont. Coral Reefs: 1–5

  • Hilmi N, Allemand D, Dupont S, Safa A, Haraldsson G, Nunes PALD, Moore C, Hattam C, Reynaud S, Hall-Spencer JM, Fine M, Turley C, Jeffree R, Orr J, Munday PL, Cooley SR (2012) Towards improved socio-economic assessments of ocean acidification’s impacts. Mar Biol. doi:10.1007/s00227-012-2031-5

  • Hiscock K, Southward A, Tittley I, Hawkins S (2004) Effects of changing temperature on benthic marine life in Britain and Ireland. Aquat Conserv 14:333–362

    Article  Google Scholar 

  • Hofmann M, Schellnhuber HJ (2009) Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes. Proc Nat Acad Sci USA 106:3017–3022

    CAS  Article  Google Scholar 

  • Hofmann GE, Smith2 JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson BJ, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6:e28983

  • Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386:27–33

    Article  Google Scholar 

  • Honisch B, Hemming NG, Archer D, Siddall M, McManus JF (2009) Atmospheric carbon dioxide concentration across the mid-pleistocene transition. Science 324:1551–1554

    Article  CAS  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 design. J Phycol 45:1236–1251

    CAS  Article  Google Scholar 

  • Hutchins DA, Fu FX, Zhang Y, Warner ME, Feng Y, Portune K, Bernhardt PW, Mulholland MR (2007) CO2 control of Trichodesmium N-2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 52:1293–1304

    CAS  Article  Google Scholar 

  • Iglesias-Rodriguez MD, Halloran PR, Rickaby REM, Hall IR, Colmenero-Hidalgo E, Gittins JR, Green DRH, Tyrrell T, Gibbs SJ, von Dassow P, Rehm E, Armbrust EV, Boessenkool KP (2008) Phytoplankton calcification in a high-CO2 world. Science 320:336–340

    CAS  Article  Google Scholar 

  • Joint I, Doney SC, Karl DM (2011) Will ocean acidification affect marine microbes? ISME J 5:1–7

    Article  Google Scholar 

  • Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483

    Article  Google Scholar 

  • Kerrison P, Hall-Spencer JM, Suggett DJ, Hepburn LJ, Steinke M (2011) Assessment of pH variability at a coastal CO(2) vent for ocean acidification studies. Estuar Coast Shelf Sci 94:129–137

    CAS  Article  Google Scholar 

  • Kranz SA, Sultemeyer D, Richter KU, Rost B (2009) Carbon acquisition by Trichodesmium: the effect of pCO(2) and diurnal changes. Limnol Oceanogr 54:548–559

    CAS  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 

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

    CAS  Article  Google Scholar 

  • Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117

    CAS  Article  Google Scholar 

  • Kurihara H, Ishimatsu A (2008) Effects of high CO2 seawater on the copepod (Acartia tsuensis) through all life stages and subsequent generations. Mar Pollut Bull 56:1086–1090

    CAS  Article  Google Scholar 

  • Kurihara H, Ishimatsu A, Shirayama Y (2007) Effects of elevated seawater CO2 concentration on the meiofauna. J Mar Sci Technol 15:17–22

    Google Scholar 

  • Lacoue-Labarthe T, Martin S, Oberhansli F, Teyssie JL, Markich S, Ross J, Bustamante P (2009) Effects of increased pCO(2) and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences 6:2561–2573

    CAS  Article  Google Scholar 

  • Lacoue-Labarthe T, Reveillac E, Oberhansli F, Teyssie JL, Jeffree R, Gattuso JP (2011) Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris. Aqu Toxicol 105:166–176

    CAS  Article  Google Scholar 

  • Larsen JB, Larsen A, Thyrhaug R, Bratbak G, Sandaa RA (2008) Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO(2) levels. Biogeosciences 5:523–533

    Article  Google Scholar 

  • Lau JA, Shaw RG, Reich PB, Shaw FH, Tiffin P (2007) Strong ecological but weak evolutionary effects of elevated CO2 on a recombinant inbred population of Arabidopsis thaliana. New Phytol 175:351–362

    CAS  Article  Google Scholar 

  • Lehman CL, Tilman D (2000) Biodiversity, stability, and productivity in competitive communities. Am Nat 156:534–552

    Article  Google Scholar 

  • Lischka S, Budenbender J, Boxhammer T, Riebesell U (2011) Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth. Biogeosciences 8:919–932

    CAS  Article  Google Scholar 

  • Liu JW, Weinbauer MG, Maier C, Dai MH, Gattuso JP (2010) Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aqu Micro Ecol 61:291–305

    Article  Google Scholar 

  • Low-Decarie E, Fussmann GF, Bell G (2011) The effect of elevated CO(2) on growth and competition in experimental phytoplankton communities. Global Change Biol 17:2525–2535

    Article  Google Scholar 

  • Marshall DJ (2006) Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners. Mar Pollu Bull 52:734–738

    CAS  Article  Google Scholar 

  • Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the Northeast Pacific Subarctic. Nature 331:341–343

    CAS  Article  Google Scholar 

  • Martin S, Richier S, Pedrotti ML, Dupont S, Castejon C, Gerakis Y, Kerros ME, Oberhansli F, Teyssie JL, Jeffree R, Gattuso JP (2011) Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J Exp Biol 214:1357–1368

    CAS  Article  Google Scholar 

  • Martín-Díaz M, Blasco J, Sales D, DelValls T (2004) Biomarkers as tools to assess sediment quality: laboratory and field surveys. Trends Analyt Chem 23:807–818

    Article  CAS  Google Scholar 

  • McDonald MR, McClintock JB, Amsler CD, Rittschof D, Angus RA, Orihuela B, Lutostanski K (2009) Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite. Mar Ecol Prog Ser 385:179–187

    CAS  Article  Google Scholar 

  • McFarland V, Inouye L, Lutz C, Jarvis A, Clarke J, McCant D (1999) Biomarkers of oxidative stress and genotoxicity in livers of field-collected brown bullhead, Ameiurus nebulosus. Arch Environ Contam Toxicol 37:236–241

    CAS  Article  Google Scholar 

  • McNeil BI, Matear RJ (2008) Southern ocean acidification: a tipping point at 450-ppm atmospheric CO(2). Proc Nat Acad Sci USA 105:18860–18864

    CAS  Article  Google Scholar 

  • Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Portner HO (2009) Physiological basis for high CO(2) tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331

    CAS  Article  Google Scholar 

  • Meron D, Atias E, Kruh LI, Elifantz H, Minz D, Fine M, Banin E (2011) The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J 5:51–60

    Article  Google Scholar 

  • Millero FJ, Woosley R, Ditrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85

    Article  Google Scholar 

  • Mouchka ME, Hewson I, Harvell CD (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50:662–674

    Article  Google Scholar 

  • Müller MN, Schulz KG, Riebesell U (2010) Effects of long-term high CO2 exposure on two species of coccolithophores. Biogeosciences 7:1109–1116

    Article  Google Scholar 

  • Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Nat Acad Sci USA 106:1848–1852

    CAS  Article  Google Scholar 

  • Novak M, Wootton JT (2010) Using experimental indices to quantify the strength of species interactions. Oikos 119:1057–1063

    Article  Google Scholar 

  • Odum EP (1985) Trends expected in stressed ecosystems. Bioscience 35:419–422

    Article  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    CAS  Article  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Paine RT (1992) Food-web analysis through field measurement of per-capita interaction strength. Nature 355:73–75

    Article  Google Scholar 

  • Parker LM, Ross PM, O’Connor WA (2009) The effect of ocean acidification and temperature on the fertilization and embryonic development of the Sydney rock oyster Saccostrea glomerata (Gould 1850). Global Change Biol 15:2123–2136

    Article  Google Scholar 

  • Parker LM, Ross PM, O’Connor WA (2011) Populations of the Sydney rock oyster, Saccostrea glomerata, vary in response to ocean acidification. Marine Biol 158:689–697

    Article  Google Scholar 

  • Pascal P-Y, Fleeger JW, Galvez F, Carman KR (2010) The toxicological interaction between ocean acidity and metals in coastal meiobenthic copepods. Mar Pollu Bull 60:2201–2208

    CAS  Article  Google Scholar 

  • Passow U (2002) Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanog 55:287–333

    Article  Google Scholar 

  • Peakall D, Walker C (1994) The role of biomarkers in environmental assessment (3), Vertebrates. Ecotoxicology 3:173–179

    Article  Google Scholar 

  • Pfister CA, McCoy SJ, Wootton JT, Martin PA, Colman AS, Archer D (2011) Rapid environmental change over the past decade revealed by isotopic analysis of the california mussel in the Northeast Pacific. PLoS One 6

  • Piazzi L, Ceccherelli G, Cinelli F (2001) Threat to macroalgal diversity: Effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol Prog Ser 149–159

  • Piontek J, Lunau M, Handel N, Borchard C, Wurst M, Engel A (2010) Acidification increases microbial polysaccharide degradation in the ocean. Biogeosciences 7:1615–1624

    CAS  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 

  • Portner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar Ecol Prog Ser 373:203–217

    Article  CAS  Google Scholar 

  • Portner HO, Langenbuch M, Reipschlager A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. J Oceanogr 60:705–718

    Article  Google Scholar 

  • Reuter KE, Lotterhos KE, Crim RN, Thompson CA, Harley CDG (2011) Elevated pCO(2) increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus. Global Change Biol 17:163–171

    Article  Google Scholar 

  • Riba I, Kalman J, Vale C, Blasco J (2010) Influence of sediment acidification on the bioaccumulation of metals in Ruditapes philippinarum. Environ Sci Pollu Res 17:1519–1528

    Article  CAS  Google Scholar 

  • Riebesell U, Wolfgladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361:249–251

    CAS  Article  Google Scholar 

  • Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, Meyerhofer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zollner E (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450:548–549

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    CAS  Article  Google Scholar 

  • Rodolfo-Metalpa R, Houlbrèque F, Tambutté E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer J (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Change 1:308–312

    CAS  Article  Google Scholar 

  • Rosa R, Seibel BA (2008) Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. Proc Nat Acad Sci USA 105:20776–20780

    CAS  Article  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    CAS  Article  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(4):e34737. doi:10.1371/journal.pone.0034737

  • Rost B, Zondervan I, Wolf-Gladrow D (2008) Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar Ecol Prog Ser 373:227–237

    CAS  Article  Google Scholar 

  • Russell BD, Harley CD, Wernberg T, Mieszkowska N, Widdicombe S, Hall-Spencer JM, Connell SD (2011) Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems. Biol Lett 8(2):164–166

    Google Scholar 

  • Sabine CL, Feely RA (2007) The oceanic sink for carbon dioxide. In: Reay D, Hewitt N, Grace J, Smith J (eds) Greenhouse gas sinks. CABI Publishing, Oxfordshire

    Google Scholar 

  • Sala E, Dayton PK (2011) Predicting strong community impacts using experimental estimates of per capita interaction strength: benthic herbivores and giant kelp recruitment. Mar Ecol Evol Perspec 32:300–312

    Article  Google Scholar 

  • Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298:1987–1990

    CAS  Article  Google Scholar 

  • Shi DL, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science 327:676–679

    CAS  Article  Google Scholar 

  • Soetaert K, Hofmann AF, Middelburg JJ, Meysman FJR, Greenwood J (2007) The effect of biogeochemical processes on pH (Reprinted from Marine Chemistry, vol 105, p 30–51, 2007). Mar Chem 106:380–401

    CAS  Article  Google Scholar 

  • Solé M, Porte C, Albaiges J (1995) Seasonal variation in the mixed-function oxygenase system and antioxidant enzymes of the mussel Mytilus galloprovincialis. Environ Toxicol Chem 14:157–164

    Google Scholar 

  • Steinacher M, Joos F, Frolicher TL, Plattner GK, Doney SC (2009) Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6:515–533

    CAS  Article  Google Scholar 

  • Striegl RG, Dornblaser MM, Aiken GR, Wickland KP, Raymond PA (2007) Carbon export and cycling by the Yukon, Tanana, and Porcupine rivers, Alaska, 2001–2005. Water Resour Res 43

  • Stumpp M, Dupont S, Thorndyke MC, Melzner F (2011) CO(2) induced seawater acidification impacts sea urchin larval development II: gene expression patterns in pluteus larvae. Comp Biochem Physiol A: Mol Integr Physiol 160:320–330

    CAS  Article  Google Scholar 

  • Stumpp M, Trübenbacha K, Brenneckea D, Hua MY, Melznera F (2012) Resource allocation and extracellular acid–base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquatic Toxicol 110–111:194–207

    Article  CAS  Google Scholar 

  • Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6

  • Talmage SC, Gobler CJ (2010) Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc Nat Acad Sci USA 107:17246–17251

    CAS  Article  Google Scholar 

  • Tanaka T, Thingstad TF, Lovdal T, Grossart HP, Larsen A, Allgaier M, Meyerhofer M, Schulz KG, Wohlers J, Zollner E, Riebesell U (2008) Availability of phosphate for phytoplankton and bacteria and of glucose for bacteria at different pCO(2) levels in a mesocosm study. Biogeosciences 5:669–678

    CAS  Article  Google Scholar 

  • Thompson JB, Paloczi GT, Kindt JH, Michenfelder M, Smith BL, Stucky G, Morse DE, Hansma PK (2000) Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins. Biophys J 79:3307–3312

    CAS  Article  Google Scholar 

  • Tilman D (1996) Biodiversity: population versus ecosystem stability. Ecology 77:350–363

    Article  Google Scholar 

  • Tortell PD, Payne CD, Li YY, Trimborn S, Rost B, Smith WO, Riesselman C, Dunbar RB, Sedwick P, DiTullio GR (2008) CO(2) sensitivity of southern Ocean phytoplankton. Geophys Res Lett 35

  • Tunnicliffe V, Davies KTA, Butterfield DA, Embley RW, Rose JM, Chadwick WW (2009) Survival of mussels in extremely acidic waters on a submarine volcano. Nat Geosci 2:344–348

    CAS  Article  Google Scholar 

  • Tuominen L, Makela K, Lehtonen KK, Haahti H, Hietanen S, Kuparinen J (1999) Nutrient fluxes, porewater profiles and denitrification in sediment influenced by algal sedimentation and bioturbation by Monoporeia affinis. Estuar Coast Shelf Sci 49:83–97

    CAS  Article  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Vasseur P, Cossu-Leguille C (2003) Biomarkers and community indices as complementary tools for environmental safety. Environ Int 28:711–717

    CAS  Article  Google Scholar 

  • Vasseur P, Leguille C (2004) Defense systems of benthic invertebrates in response to environmental stressors. Environ Toxicol 19:433–436

    CAS  Article  Google Scholar 

  • Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163

    Article  CAS  Google Scholar 

  • Vinebrooke RD, Schindler DW, Findlay DL, Turner MA, Paterson M, Milis KH (2003) Trophic dependence of ecosystem resistance and species compensation in experimentally acidified lake 302S (Canada). Ecosystems 6:101–113

    Article  Google Scholar 

  • Vizzini S, Tomasello A, Maida GD, Pirrotta M, Mazzola A, Calvo S (2010) Effect of explosive shallow hydrothermal vents on δ13C and growth performance in the seagrass Posidonia oceanica. J Ecol 98:1284–1291

    Article  Google Scholar 

  • Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346

    CAS  Article  Google Scholar 

  • Weinbauer MG, Mari X, Gattuso JP (2011) Effect of ocean acidification on the diversity and activity of heterotrophic marine microorganisms. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 83–98

  • Whitman JD, Roy K (2009) Marine macroecology. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Widdicombe S, Austen MC (1998) Experimental evidence for the role of Brissopsis lyrifera (Forbes, 1841) as a critical species in the maintenance of benthic diversity and the modification of sediment chemistry. J Exp Mar Biol Ecol 228:241–255

    CAS  Article  Google Scholar 

  • Widdicombe S, Needham HR (2007) Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar Ecol Prog Ser 341:111–122

    Article  Google Scholar 

  • Widdicombe S, Dashfield SL, McNeill CL, Needham HR, Beesley A, McEvoy A, Oxnevad S, Clarke KR, Berge JA (2009) Effects of CO2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar Ecol Prog Ser 379:59–75

    CAS  Article  Google Scholar 

  • Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aqu Toxicol 19:137–161

    CAS  Article  Google Scholar 

  • Witt V, Wild C, Anthony K, Diaz-Pulido G, Uthicke S (2011) Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef. Environ Microbiol 13:2976–2989

    CAS  Article  Google Scholar 

  • Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Nat Acad Sci USA 105:18848–18853

    CAS  Article  Google Scholar 

  • Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

    CAS  Article  Google Scholar 

  • Wright DA, Welbourn P (2002) Environmental toxicology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Wu Y, Gao K, Riebesell U (2010) CO(2)-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7:2915–2923

    CAS  Article  Google Scholar 

  • Yamada N, Suzumura M (2010) Effects of seawater acidification on hydrolytic enzyme activities. J Oceanogr 66:233–241

    CAS  Article  Google Scholar 

  • Yamamoto-Kawai M, McLaughlin FA, Carmack EC, Nishino S, Shimada K (2009) Aragonite undersaturation in the Arctic Ocean: effects of ocean acidification and sea ice melt. Science 326:1098–1100

    CAS  Article  Google Scholar 

  • Zhu QZ, Aller RC, Fan YZ (2006) Two-dimensional pH distributions and dynamics in bioturbated marine sediments. Geochim Cosmochim Acta 70:4933–4949

    CAS  Article  Google Scholar 

  • Zippay ML, Hofmann GE (2010) Effect of pH on gene expression and thermal tolerance of early life history stages of red abalone (Haliotis rufescens). J Shellfish Res 29:429–439

    Article  Google Scholar 

Download references

Acknowledgments

The ‘acidification in aquatic environments’ workshop was sponsored by the Fram Centre, the Norwegian Polar Institute, the Institute of Marine Research, the Bjerknes Centre, the Norwegian Institute for Water Research, Avkaplan-NIVA, NOFIMA Marin, the University of Tromsø and the Association of Polar Early Career Scientists. We would like to give special acknowledgements to the organizing committee; Howard Browman, Clara Manno, Richard Bellerby, JoLynn Carroll, Kai Sorensen and Helge Tveiten and finally thank Sam Dupont and two anonymous reviewers for their comments on this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Samantha L. Garrard.

Additional information

Communicated by S. Dupont.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Garrard, S.L., Hunter, R.C., Frommel, A.Y. et al. Biological impacts of ocean acidification: a postgraduate perspective on research priorities. Mar Biol 160, 1789–1805 (2013). https://doi.org/10.1007/s00227-012-2033-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2033-3

Keywords

  • Phytoplankton
  • Meiofauna
  • Ocean Acidification
  • Carbonate Chemistry
  • High pCO2