Skip to main content

Advertisement

SpringerLink
Log in

Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates

  • Review Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Feeding is fundamental for all heterotrophic organisms, providing the means to acquire energy for basic life processes. Recent studies have suggested that experimental ocean acidification (OA) can alter the feeding performance of marine calcifying invertebrates, but results have been inconsistent. While several reviews pertaining to the biological effects of OA exist, none provide a synthesis of OA effects on feeding performance. Here, we provide a quantitative analysis of published experiments testing for effects of elevated CO2 on feeding rates of marine calcifying invertebrates. Results revealed that suspension-feeding molluscs and predatory and grazing echinoderms experienced depressed feeding rates under elevated CO2, while arthropods appeared unaffected; larval and juvenile animals were more susceptible to CO2 effects than adults. Feeding strategy did not appear to influence the overall taxonomic trend, nor did habitat, although exposure time did have an effect. AIC model selection revealed that Phylum best predicted effect size; life stage and exposure time were also included in candidate models. Based on these results, we synthesize potential physiological attributes of different taxa that may drive OA sensitivities in feeding rates, which could potentially result in community-level impacts. We also discuss CO2 effects on calcifier feeding in the context of elevated temperature and other global marine change stressors, and highlight other areas for future research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amaral, V., H. N. Cabral & M. J. Bishop, 2012. Effects of estuarine acidification on predator–prey interactions. Marine Ecology Progress Series 445: 117–127.

    Article  Google Scholar 

  • Anderson, D. R., 2007. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York.

    Google Scholar 

  • Appelhans, Y. S., J. Thomsen, C. Pansch, F. Melzner & M. Wahl, 2012. Sour times: seawater acidification effects on growth, feeding behaviour, and acid-base status of Asterias rubens and Carcinus maenas. Marine Ecology Progress Series 459: 85–97.

    Article  CAS  Google Scholar 

  • Appelhans, Y. S., J. Thomsen, S. Opitz, C. Pansch, F. Melzner & M. Wahl, 2014. Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential. Marine Ecology Progress Series 509: 227–239.

    Article  CAS  Google Scholar 

  • Arnberg, M., P. Calosi, J. I. Spicer, A. H. S. Tandberg, M. Nilsen, S. Westerlund & R. K. Bechmann, 2013. Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Marine Biology 160: 2037–2048.

    Article  CAS  Google Scholar 

  • Ashur, M. M., N. K. Johnston & D. L. Dixson, 2017. Impacts of ocean acidification on sensory function in marine organisms. Integrative and Comparative Biology 57: 63–80.

    Article  PubMed  Google Scholar 

  • Asnaghi, V., M. Chiantore, L. Mangialajo, F. Gazeau, P. Francour, S. Alliouane & J.-P. Gattuso, 2013. Cascading effects of ocean acidification in a rocky subtidal community. PLoS ONE 8: e61978.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Axiak, V. & J. J. George, 1987. Effects of exposure to petroleum hydrocarbons in the gill functions and ciliary functions of a marine bivalve. Marine Biology 94: 241–249.

    Article  CAS  Google Scholar 

  • Beniash, E., A. Ivanina, N. S. Lieb, I. Kurochkin & I. M. Sokolova, 2010. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Marine Ecology Progress Series 419: 95–108.

    Article  CAS  Google Scholar 

  • Benítez, S., C. Duarte, J. López, P. H. Manríquez, J. M. Navarro, C. C. Bonta, R. Torres & P. Quijón, 2016. Ontogenetic variability in the feeding behavior of a marine amphipod in response to ocean acidification. Marine Pollution Bulletin 112: 375–379.

    Article  PubMed  CAS  Google Scholar 

  • Breitburg, D. L., N. Steinberg, S. DuBeau, C. Cooksey & E. D. Houde, 1994. Effects of low dissolved oxygen on predation on estuarine fish larvae. Marine Ecology Progress Series 104: 235–246.

    Article  Google Scholar 

  • Breitburg, D. L., J. Salisbury, J. M. Bernhard, et al., 2015. And on top of all that… coping with ocean acidification in the midst of many stressors. Oceanography 28: 48–61.

    Article  Google Scholar 

  • Burnell, O. W., B. D. Russell, A. D. Irving & S. D. Connell, 2013. Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Marine Ecology Progress Series 485: 37–46.

    Article  CAS  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodal Inference: A Practical Information-Theoretic Approach. Springer, New York.

    Google Scholar 

  • Burton-Sanders, M., T. P. Bean, T. H. Hutchinson & W. J. F. Le Quesne, 2013. Juvenile king scallop, Pecten maximus, is potentially tolerant to low levels of ocean acidification when food is unrestricted. PLoS One 8: e74118.

    Article  CAS  Google Scholar 

  • Cai, W., X. Hu, W. Huang, M. Murrell, J. Lehrter, S. Lohrenz, W. Chou, W. Zhai, J. Hollibaugh, Y. Wang, P. Zhao, X. Guo, K. Gundersen, M. Dai & G. Gong, 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4: 766–770.

    Article  CAS  Google Scholar 

  • Caldeira, K. & M. E. Wickett, 2003. Anthropogenic carbon and ocean pH. Nature 425: 365.

    Article  PubMed  CAS  Google Scholar 

  • Calosi, P., P. DeWit, P. Thor & S. Dupont, 2016. Will life find a way? Evolution of marine species under global change. Evolutionary Applications 9: 1035–1042.

    Article  PubMed  PubMed Central  Google Scholar 

  • Campanati, C., S. Yip, A. Lane & V. Thiyagarajan, 2016. Combined effects of low pH and low oxygen on the early-life stages of the barnacle Balanus amphitrite. ICES Journal of Marine Science 73: 791–802.

    Article  Google Scholar 

  • Carey, N., J. Harionto & M. Byrne, 2016. Sea urchins in a high-CO2 world: partitioned effects of body size, ocean warming and acidification on metabolic rate. Journal of Experimental Biology 219: 1178–1186.

    Article  PubMed  Google Scholar 

  • Chaparro, O. R., Y. A. Montiel, C. J. Segura, V. M. Cubillos, R. J. Thompson & J. M. Navarro, 2008. The effect of salinity on clearance rate in the suspension-feeding estuarine gastropod Crepipatella dilatata under natural and controlled conditions. Estuarine, Coastal and Shelf Science 74: 861–868.

    Article  Google Scholar 

  • Charpentier, C. L. & J. H. Cohen, 2016. Acidification and γ-aminobutyric acid independently alter kairomone-induced behaviour. Royal Society Open Science 3: 160311.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Christmas, A. M. F. 2013. Effects of ocean acidification on dispersal behavior in the larval stage of the Dungeness crab and the Pacific Green Shore crab. MSc thesis, Western Washington University, Bellingham, WA, USA. 72 pp. http://cedar.wwu.edu/cgi/viewcontent.cgi?article=1305&context=wwuet (last accessed 02 August 2017).

  • Clements, J. C. & H. L. Hunt, 2015. Marine animal behaviour in a high CO2 world. Marine Ecology Progress Series 536: 259–279.

    Article  CAS  Google Scholar 

  • Clements, J. C., M. M. Bishop & H. L. Hunt, 2017. Elevated temperature has adverse effects on GABA-mediated avoidance behaviour to sediment acidification in a wide-ranging marine bivalve. Marine Biology 164: 56.

    Article  CAS  Google Scholar 

  • Clemmesen, B. & C. B. Jørgensen, 1987. Energetic costs and efficiencies of ciliary filter feeding. Marine Biology 94: 445–449.

    Article  Google Scholar 

  • Cole, V. J., L. M. Parker, S. J. O’Connor, W. A. O’Connor, E. Scanes, M. Byrne & P. M. Ross, 2016. Effects of multiple climate change stressors: ocean acidification interacts with warming, hyposalinity, and low food supply on the larvae of the brooding flat oyster Ostrea angasi. Marine Biology 163: 125.

    Article  CAS  Google Scholar 

  • Cooper, H. L., D. C. Potts & A. Paytan, 2016. Metabolic responses of the North Pacific krill, Euphausia pacifica, to short- and long-term pCO2 exposure. Marine Biology 163: 207.

    Article  CAS  Google Scholar 

  • Cripps, G., K. J. Flynn & P. K. Lindeque, 2016. Ocean acidification affects the phyto-zoo plankton trophic transfer efficiency. PLoS One 11: e0151739.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dickinson, G. H., A. V. Ivanina, O. B. Matoo, H. O. Pörtner, G. Lannig, C. Bock, E. Beniash & I. M. Sokolova, 2012. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. Journal of Experimental Biology 215: 29–43.

    Article  PubMed  CAS  Google Scholar 

  • Dodd, L. F., J. H. Grabowski, M. F. Piehler, I. Westfield & J. B. Ries, 2015. Ocean acidification impairs crab foraging behaviour. Proceedings of the Royal Society B: Biological Sciences 282: 20150333.

    Article  PubMed  CAS  Google Scholar 

  • Duarte, C., I. Hendriks, T. Moore, Y. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J. Trotter & M. McCulloch, 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36: 221–236.

    Article  CAS  Google Scholar 

  • Duarte, C., J. López, S. Benítez, P. H. Manríquez, J. M. Navarro, C. C. Bonta, R. Torres & P. Quijón, 2016. Ocean acidification induces changes in algal palatability and herbivore feeding behavior and performance. Oecologia 180: 453–462.

    Article  PubMed  Google Scholar 

  • Dupont, S., O. Ortega-Martínez & M. Thorndyke, 2010. Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19: 449–462.

    Article  PubMed  CAS  Google Scholar 

  • Dupont, S. T., M. Murcurio, A. A. G. Giacoletti, et al., 2015. Functional consequences of prey acclimation to ocean acidification for the prey and its predator. PeerJ Preprints. https://doi.org/10.7287/peerj.preprints.1438v1.

    Article  Google Scholar 

  • Edmunds, P. J., 2011. Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnology and Oceanography 56: 2402–2410.

    Article  CAS  Google Scholar 

  • Fernández-Rieriz, M. J., P. Range, X. A. Álvarez-Saldago & U. Labarta, 2011. Physiological energetics of juvenile clams Ruditapes decussatus in a high CO2 coastal ocean. Marine Ecology Progress Series 433: 97–105.

    Article  Google Scholar 

  • Fernández-Reiriz, F., P. Range, X. A. Álvarez-Salgado, J. Espinosa & U. Labarta, 2012. Tolerance of juvenile Mytilus galloprovincialis to experimental seawater acidification. Marine Ecology Progress Series 454: 65–74.

    Article  CAS  Google Scholar 

  • Frieder, C. A., S. L. Applebaum, T.-C. F. Pan, D. Hedgecock & D. T. Manahan, 2017. Metabolic cost of calcification in bivalve larvae under experimental ocean acidification. ICES Journal of Marine Science 74: 941–954.

    Article  Google Scholar 

  • Galtsoff, P. S., 1964. The American oyster Crassostrea virginica Gmelin. Fisheries Bulletin of the Fish and Wildlife Service of the US 64: 1–480.

    Google Scholar 

  • Gazeau, F., L. M. Parker, S. Comeau, J.-P. Gattuso, W. A. O’Connor, S. Martin, H.-O. Pörtner & P. M. Ross, 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology 160: 2207–2245.

    Article  CAS  Google Scholar 

  • Glandon, H. L. & T. J. Miller, 2016. No effect of high pCO2 on juvenile blue crab, Callinectes sapidus, growth and consumption despite positive responses to concurrent warming. ICES Journal of Marine Science 74: 1201–1209.

    Google Scholar 

  • Gobler, C. J. & H. Baumann, 2016. Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life. Biology Letters 12: 20150976.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gooding, R., C. Harley & E. Tang, 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences of the USA 106: 9316–9321.

    Article  PubMed  Google Scholar 

  • Harvey, B. P. & P. J. Moore, 2017. Ocean warming and acidification prevent compensatory response in a predator to reduced prey quality. Marine Ecology Progress Series 563: 111–122.

    Article  CAS  Google Scholar 

  • Harvey, B. P., D. Gwynn-Jones & P. J. Moore, 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecology and Evolution 3: 1016–1030.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harvey, B. P., A.-J. Balsam, S. Broszeit, et al., 2014. Evolution of marine organisms under climate change at different levels of biological organisation. Water 6: 1545–1574.

    Article  Google Scholar 

  • Hedges, L. V., J. Gurevitch & P. S. Curtis, 1999. The metaanalysis of response ratios in experimental ecology. Ecology 80: 1150–1156.

    Article  Google Scholar 

  • Hendriks, I. E., C. B. Duarte & M. Álvarez, 2010. Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal, and Shelf Science 86: 157–164.

    Article  CAS  Google Scholar 

  • Hildebrandt, N., F. J. Sartoris, K. G. Schulz, U. Riebsell & B. Niehoff, 2016. Ocean acidification does not alter grazing in the calanoid copepods Calanus finmarchicus and Calanus glacialis. ICES Journal of Marine Science 73: 927–936.

    Article  Google Scholar 

  • Hoegh-Guldberg, O., R. Cai, E. S. Poloczanska, et al. 2014. The ocean. In Barros, V. R., Field, C. B., Dokken, D. J., et al. (eds), Climate Change 2014: Impacts, Adaptation, and Vulnerability. Cambridge University Press, New York: 1655–1731.

  • Hofmann, G. E., J. P. Barry, P. J. Edmunds, R. D. Gates, D. A. Hutchins, T. Klinger & M. A. Sewell, 2010. The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annual Reviews of Ecology, Evolution and Systematics 41: 127–147.

    Article  Google Scholar 

  • Houlbrèque, F., S. Reynaud, C. Godinot, F. Oberhänsli, R. Rodolfo-Metalpa & C. Ferrier-Pagès, 2015. Ocean acidification reduces feeding rates in the scleractinian coral Stylophora pistillata. Limnology and Oceanography 60: 89–99.

    Article  CAS  Google Scholar 

  • Howes, E. L., F. Joos, C. M. Eakin & J.-P. Gattuso, 2015. An updated synthesis of the observed and projected impacts of climate change on the chemical, physical and biological processes in the oceans. Frontiers in Marine Science 2: 36.

    Article  Google Scholar 

  • Isari, S., S. Zervoudaki, E. Siaz, C. Pelejero & J. Peters, 2015. Copepod vital rates under CO2-induced acidification: a calanoid species and a cyclopoid species under short-term exposures. Journal of Plankton Research 37: 912–922.

    Article  CAS  Google Scholar 

  • Isari, S., S. Zervoudaki, J. Peters, G. Papantoniou, C. Pelejero & E. Siaz, 2016. Lack of evidence for elevated CO2-induced bottom-up effects on marine copepods: a dinoflagellate–calanoid prey–predator pair. ICES Journal of Marine Science 73: 650–658.

    Article  Google Scholar 

  • Jager, T., E. Ravagnan & S. Dupont, 2016. Near-future ocean acidification impacts maintenance costs in sea-urchin larvae: identification of stress factors and tipping points using a DEB modelling approach. Journal of Experimental Marine Biology and Ecology 474: 11–17.

    Article  Google Scholar 

  • Jorgensen, C. B., 1990. Bivalve Filter Feeding: Hydrodynamics, Bioenergetics, Physiology, and Ecology. Olsen and Olsen, Fredensborg: 140.

    Google Scholar 

  • Kamya, P. Z., M. Byrne, A. Graba-Landry & S. A. Dworjanyn, 2016. Near-future ocean acidification enhances the feeding rate and development of the herbivorous juveniles of the crown-of-thorns starfish, Acanthaster planci. Coral Reefs 35: 1241–1251.

    Article  Google Scholar 

  • Keppel, E. A., R. A. Scrosati & S. C. Courtenay, 2015. Interactive effects of ocean acidification and warming on subtidal mussels and sea stars from Atlantic Canada. Marine Biology Research 11: 337–348.

    Article  Google Scholar 

  • Ko, W. K. G., B. S. V. Chan, R. Dineshram, K. S. D. Choi, J. A. Li, Z. Yu & V. Thiyagarajan, 2013. Larval and post-larval stages of pacific oyster (Crassostrea gigas) are resistant to elevated CO2. PLoS ONE 8: e64147.

    Article  Google Scholar 

  • Kooijman, S. A. L. M., 2009. Dynamic Energy Budget Theory for Metabolic Organisation. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte & J.-P. Gattuso, 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurihara, H., M. Matsui, H. Furukawa, M. Hayashi & A. Ishimatsu, 2008. Long-term effects of predicted future seawater CO2 conditions on the survival and growth of the marine shrimp Palaemon pacificus. Journal of Experimental Marine Biology and Ecology 367: 41–46.

    Article  CAS  Google Scholar 

  • Lajeunesse, M. J. & M. R. Forbes, 2003. Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecology Letters 6: 448–454.

    Article  Google Scholar 

  • Landes, A. & M. Zimmer, 2012. Acidification and warming affect both a calcifying predator and prey, but not their interaction. Marine Ecology Progress Series 450: 1–10.

    Article  Google Scholar 

  • Lankford Jr., T. E. & T. E. Targett, 1994. Suitability of estuarine nursery zones for juvenile weakfish (Cynoscion regalis): effects of temperature and salinity on feeding, growth and survival. Marine Biology 119: 611–620.

    Article  Google Scholar 

  • Le Moullac, G., C. Soyez, O. Latchere, J. Vidal-Dupio, J. Fremery, D. Saulnier, A. L. Yat, C. Belliard, N. Mazouni-Gaertner & Y. Gueguen, 2016. Pinctada margaritifera responses to temperature and pH: acclimation capabilities and physiological limits. Estuarine, Coastal and Shelf Science 182B: 261–269.

    Article  CAS  Google Scholar 

  • Lefevre, S. J. 2016. Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction. Conservation Physiology 4: cow009. https://doi.org/10.1093/conphys/cow009

  • Li, W. & K. Gao, 2012. A marine secondary producer respires and feeds more in a high CO2 ocean. Marine Pollution Bulletin 64: 699–703.

    Article  PubMed  CAS  Google Scholar 

  • Li, W., G. Han, Y. Dong, A. Ishimatsu, B. D. Russell & K. Gao, 2015. Combined effects of short-term ocean acidification and heat shock in a benthic copepod Tigriopus japonicus Mori. Marine Biology 162: 1901–1912.

    Article  CAS  Google Scholar 

  • Liu, W. & M. He, 2012. Effects of ocean acidification on the metabolic rates of three species of bivalve from southern coast of China. Chinese Journal of Oceanology and Limnology 30: 206–211.

    Article  CAS  Google Scholar 

  • Mathieu, S., D. Sylvain, F. Walden, E. Catapane, and M. Carroll. 2014. GABA is an inhibitory neurotransmitter in ganglia of the bivalve mollusc, Crassostrea virginica. The FASEB Journal 28: Supplement 1059.4.

  • Mazerolle, M. J. 2017. Model selection and multimodel inference based on (Q)AIC(c). https://cran.r-project.org/web/packages/AICcmodavg/index.html (last accessed 30 July 2017)

  • Melzner, F., M. A. Gutowska, M. Langenbuch, S. Dupont, M. Lucassen, M. C. Thorndyke, M. Bleich & H.-O. Pörtner, 2009. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6: 2313–2331.

    Article  CAS  Google Scholar 

  • Michaelidis, B., C. Ouzounis, A. Paleras & H.-O. Pörtner, 2005. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293: 109–118.

    Article  Google Scholar 

  • Miles, H., S. Widdicombe & J. I. Spicer, 2007. Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin Psammechinus miliaris. Marine Pollution Bulletin 54: 89–96.

    Article  PubMed  CAS  Google Scholar 

  • Morley, S. A., C. C. Suckling, M. S. Clark, E. L. Cross & L. S. Peck, 2016. Long-term effects of altered pH and temperature on the feeding energetics of the Antarctic sea urchin, Sterechinus neumayeri. Biodiversity 17: 34–45.

    Article  Google Scholar 

  • Navarro, J. M., R. Torres, K. Acuña, C. Duarte, P. H. Manríquez, M. Lardies, N. A. Lagos, C. Vargas & V. Aguilera, 2013. Impact of medium-term exposure to elevated pCO2 levels on the physiological energetics of the mussel Mytilus chilensis. Chemosphere 90: 1242–1248.

    Article  PubMed  CAS  Google Scholar 

  • Navarro, J. M., C. Duarte, P. H. Manríquez, M. A. Lardies, R. Torres, K. Acuña, C. A. Vargas & N. A. Lagos, 2016. Ocean warming and elevated carbon dioxide: multiple stressor impacts on juvenile mussels from southern Chile. ICES Journal of Marine Science 73: 764–771.

    Article  Google Scholar 

  • Noisette, F., F. Bordeyne, D. Davoult & S. Martin, 2016. Assessing the physiological responses of the gastropod Crepidula fornicata to predicted ocean acidification and warming. Limnology and Oceanography 61: 430–444.

    Article  CAS  Google Scholar 

  • Norman, S. 2012. The temperature dependence of ectotherm consumption. MSc thesis, Umeå Universitet, Umeå, Sweden. 13 pp. http://www.diva-portal.org/smash/get/diva2:588173/FULLTEXT01.pdf (last accessed 08 August 2017).

  • Orr, J. C., V. J. Fabry, O. Aumont, et al., 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681–686.

    Article  PubMed  CAS  Google Scholar 

  • Palmer, A. R., 1992. Calcification in marine molluscs: how costly is it? Proceedings of the National Academy of Sciences of the USA 89: 1379–1382.

    Article  PubMed  CAS  Google Scholar 

  • Pan, T. C. F., S. L. Applebaum & D. T. Manahan, 2015. Experimental ocean acidification alters the allocation of metabolic energy. Proceedings of the National Academy of Sciences of the USA 112: 4696–4701.

    Article  PubMed  CAS  Google Scholar 

  • Pedersen, S. A., O. J. Håkedal, I. Salaberria, et al., 2014. Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environmental Science and Technology 48: 12275–12284.

    Article  PubMed  CAS  Google Scholar 

  • Pepin, P., D. Robert, C. Bouchard, J. F. Dower, M. Falardeau, L. Fortier, G. P. Jenkins, V. Leclerc, K. Levesque, J. K. Llopiz, M. G. Meekan, H. M. Murphy, M. Ringuette, P. Sirois & S. Sponaugle, 2014. Once upon a larva: revisiting the relationship between feeding success and growth in fish larvae. ICES Journal of Marine Science 72: 359–373.

    Article  Google Scholar 

  • Pihl, L., S. P. Baden, R. J. Diaz & L. C. Schaffher, 1992. Effects of periodic hypoxia on distribution of demersal fish and crustaceans. Marine Biology 108: 349–360.

    Article  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar. 2017. nlme: linear and nonlinear mixed effects models. https://CRAN.R-project.org/package=nlme (last accessed 30 July 2017)

  • Poore, A. G., A. Graba-Landry, M. Favret, H. S. Brennand, M. Byrne & S. A. Dworjanyn, 2013. Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia 173: 1113–1124.

    Article  PubMed  Google Scholar 

  • Pörtner, H.-O., 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology Progress Series 373: 203–218.

    Article  CAS  Google Scholar 

  • R Development Core Team, 2016. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Ramajo, L., N. Marbà, L. Prado, S. Peron, M. A. Lardies, A. B. Rodriguez-Navarro, C. A. Vargas, N. A. Lagos & C. M. Duarte, 2016a. Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification. Global Change Biology 22: 2025–2037.

    Article  PubMed  Google Scholar 

  • Ramajo, L., E. Pérez-Léon, I. E. Hendriks, N. Marbà, D. Krause-Jensen, M. K. Sejr, M. E. Bilcher, N. A. Lagos, Y. S. Olsen & C. M. Duarte, 2016b. Food supply confers calcifiers resistance to ocean acidification. Scientific Reports 6: 19374.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ries, J. B., A. L. Cohen & D. C. McCorkle, 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: 1131–1134.

    Article  CAS  Google Scholar 

  • Rossoll, D., R. Bermúdez, H. Hauss, K. G. Schula, U. Riebesell, U. Sommer & M. Winder, 2012. Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7: e34737.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Runge, J. A., D. M. Fields, C. R. S. Thompson, S. D. Shema, R. M. Bjelland, C. M. F. Durif, A. B. Skiftesvik & H. I. Browman, 2016. End of the century CO2 concentrations do not have a negative effect on vital rates of Calanus finmarchicus, an ecologically critical planktonic species in North Atlantic ecosystems. ICES Journal of Marine Science 73: 937–950.

    Article  Google Scholar 

  • Russell, B. D., S. D. Connell, H. S. Findlay, K. Tait, S. Widdicombe & N. Mieszkowska, 2013. Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Philosophical Transactions of the Royal Society B 368: 20120438.

    Article  CAS  Google Scholar 

  • Saba, G. K., O. Schofield, J. J. Torres, E. H. Ombres & D. K. Steinberg, 2012. Increased feeding and nutrient excretion of adult Antarctic krill, Euphausia superba, exposed to enhanced carbon dioxide (CO2). PLoS ONE 7: e52224.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanford, E., 2002. Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integrative and Comparative Biology 42: 881–891.

    Article  PubMed  Google Scholar 

  • Sanford, E., B. Gaylord, A. Hettinger, E. A. Lenz, E. Meyer & T. M. Hill, 2014. Ocean acidification increases the vulnerability of native oysters to predation by invasive snails. Proceedings of the Royal Society B: Biological Sciences 281: 20132681.

    Article  PubMed  Google Scholar 

  • Schoepf, V., A. G. Grottoli, M. E. Warner, W. J. Cai, T. F. Melman, K. D. Hoadley, D. T. Pettay, X. Hu, Q. Li, H. Xu & Y. Wang, 2013. Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS ONE 8: e75049.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Secretariat of the Convention on Biological Diversity. 2009. Scientific synthesis of the impacts of ocean acidification on marine biodiversity, Technical Series No. 46. Montreal, Canada. https://www.cbd.int/doc/publications/cbd-ts-46-en.pdf (last accessed 02 August 2017).

  • Shumway, S. W., 1977. Effect of salinity fluctuation on the osmotic pressure and Na + , Ca2 + and Mg2 + ion concentrations in the hemolymph of bivalve molluscs. Marine Biology 41: 153–177.

    Article  CAS  Google Scholar 

  • Small, D. P., P. Calosi, D. Boothroyd, S. Widdicombe & J. I. Spicer, 2016. The sensitivity of the early benthic juvenile stage of the European lobster Homarus gammarus (L.) to elevated pCO2 and temperature. Marine Biology 163: 53.

    Article  CAS  Google Scholar 

  • Smith, J. N., G. De’ath, C. Richter, A. Cornils, J. M. Hall-Spencer & K. E. Fabricius, 2016. Ocean acidification reduces demersal zooplankton that reside in tropical coral reefs. Nature Climate Change 6: 1124–1129.

    Article  CAS  Google Scholar 

  • Stapp, L. S., J. Thomsen, H. Schade, C. Bock, F. Melzner, H. O. Pörtner & G. Lannig, 2017. Intra-population variability of ocean acidification impacts on the physiology of Baltic blue mussels (Mytilus edulis): integrating tissue and organism response. Journal of Comparative Physiology B 187: 529–543.

    Article  CAS  Google Scholar 

  • Stevens, P. M., 1987. Response of excised gill tissue from the New England scallop Pecten novaezelandiae to suspended silt. New Zealand Journal of Marine and Freshwater Research 21: 605–614.

    Article  CAS  Google Scholar 

  • Stumpp, M., J. Wren, F. Melzner, M. C. Thorndyke & S. T. Dupont, 2011. CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comparative and Biochemical Physiology Part A: Molecular and Integrative Physiology 160: 331–340.

    Article  CAS  Google Scholar 

  • Stumpp, M., M. Hu, I. Casties, R. Saborowski, M. Bleich, F. Melzner & S. Dupont, 2013. Digestion in sea urchin larvae impaired under ocean acidification. Nature Climate Change 3: 1044–1049.

    Article  CAS  Google Scholar 

  • Sui, Y., H. Kong, X. Huang, et al., 2016. Combined effects of short-term exposure to elevated CO2 and decreased O2 on the physiology and energy budget of the thick shell mussel Mytilus coruscus. Chemosphere 155: 207–216.

    Article  PubMed  CAS  Google Scholar 

  • Sunday, J. M., P. Calosi, S. Dupont, P. L. Munday, J. H. Stillmon & T. B. H. Reusch, 2014. Evolution in an acidifying ocean. Trends in Ecology and Evolution 29: 117–125.

    Article  PubMed  Google Scholar 

  • Talmage, S. C. & C. J. Gobler, 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proceedings of the National Academy of Sciences of the USA 107: 17246–17251.

    Article  PubMed  Google Scholar 

  • Tate, R. D., K. Bekendorff, R. Ab Lah & B. P. Kelaher, 2017. Ocean acidification and warming impacts the nutritional properties of the predatory whelk, Dicathais orbita. Journal of Experimental Marine Biology and Ecology 493: 7–13.

    Article  CAS  Google Scholar 

  • Thomsen, J., I. Casties, C. Pansch, A. Körtzinger & F. Melzner, 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Global Change Biology 19: 1017–1027.

    Article  PubMed  Google Scholar 

  • Thor, P. & E. O. Oliva, 2015. Ocean acidification elicits different energetic responses in an Arctic and a boreal population of the copepod Pseudocalanus acuspes. Marine Biology 162: 799–807.

    Article  CAS  Google Scholar 

  • Towle, E. K., I. C. Enochs & C. Langdon, 2015. Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE 10: e0123394.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tresguerres, M. & T. J. Hamilton, 2017. Acid-base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. Journal of Experimental Biology 220: 2136–2148.

    Article  PubMed  Google Scholar 

  • Vargas, C. A., M. de la Hoz, V. Aguilera, et al., 2013. CO2-driven ocean acidification reduces larval feeding efficiency and changes food selectivity in the mollusk Concholepas concholepas. Journal of Plankton Research 35: 1059–1068.

    Article  CAS  Google Scholar 

  • Vargas, C. A., V. M. Aguilera, V. San Martín, P. H. Manríquez, J. M. Navarro, C. Duarte, R. Torres, M. A. Lardies & N. A. Lagos, 2015. CO2-driven ocean acidification disrupts the filter feeding behavior in Chilean gastropod and bivalve species from different geographic localities. Estuaries and Coasts 38: 1163–1177.

    Article  CAS  Google Scholar 

  • Ventura, A., S. Schulz & S. Dupont, 2016. Maintained larval growth in mussel larvae exposed to acidified undersaturated seawater. Scientific Reports 6: 23728.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Viechtbauer, W., 2010. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36: 1–48.

    Article  Google Scholar 

  • Waldbusser, G. G., B. Hales, C. J. Langdon, B. A. Haley, P. Schrader, E. L. Brunner, M. W. Gray, C. A. Miller, I. Giminez & G. Hutchinson, 2015. Ocean acidification has multiple modes of action on bivalve larvae. PLoS ONE 10: e0128376.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wallace, R. B., H. Baumann, J. S. Grear, R. C. Aller & C. J. Gobler, 2014. Coastal ocean acidification: the other eutrophication problem. Estuarine, Coastal and Shelf Science 148: 1–13.

    Article  CAS  Google Scholar 

  • Waller, J. D., R. A. Wahle, H. McVeigh & D. M. Fields, 2016. Linking rising pCO2 and temperature to the larval development and physiology of the American lobster (Homarus americanus). ICES Journal of Marine Science 74: 1210–1219.

    Google Scholar 

  • Wang, Y., L. Li, M. Hu & W. Lu, 2015. Physiological energetics of the thick shell mussel Mytilus coruscus exposed to seawater acidification and thermal stress. Science of the Total Environment 514: 261–272.

    Article  PubMed  CAS  Google Scholar 

  • Watson, S.-A., S. Lefevre, M. I. McCormick, P. Domenici, G. E. Nilsson & P. L. Munday, 2014. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proceedings of the Royal Society B 281: 20132377.

    Article  PubMed  CAS  Google Scholar 

  • Watson, S.-A., J. B. Fields & P. L. Munday, 2017. Ocean acidification alters predator behaviour and reduces predation rate. Biology Letters 13: 20160797.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wittman, A. C. & H.-O. Pörtner, 2013. Sensitivities of extant animal taxa to ocean acidification. Nature Climate Change 3: 995–1001.

    Article  CAS  Google Scholar 

  • Wood, H. L., J. I. Spicer & S. Widdicombe, 2008. Ocean acidification may increase calcification rates, but at a cost. Proceedings of the Royal Society B: Biological Sciences 275: 1767–1773.

    Article  PubMed  Google Scholar 

  • Wong, W. H. & S. G. Cheung, 2001. Feeding rates and scope for growth of green mussels, Perna viridis (L.) and their relationship with food availability in Kat O. Hong Kong. Aquaculture 193: 123–137.

    Google Scholar 

  • Wu, F., T. Wang, S. Cui, Z. Xie, S. Dupont, J. Zeng, H. Gu, H. Kong, M. Hu, W. Lu & Y. Wang, 2017. Effects of seawater pH and temperature on foraging behavior of the Japanese stone crab Charybdis japonica. Marine Pollution Bulletin 120: 99–108.

    Article  PubMed  CAS  Google Scholar 

  • Xu, X., F. Yang, L. Zhao & X. Yan, 2016. Seawater acidification affects the physiological energetics and spawning capacity of the Manila clam Ruditapes philippinarum during gonadal maturation. Comparative and Biochemical Physiology Part A: Molecular and Integrative Physiology 196: 20–29.

    Article  CAS  Google Scholar 

  • Yuan, X., S. Shao, X. Yang, D. Yang, Q. Xu, H. Zong & S. Liu, 2016. Bioenergetic trade-offs in the sea cucumber Apostichopus japonicus (Echinodermata: Holothuroidea) in response to CO2-driven ocean acidification. Environmental Science and Pollution Research 23: 8453–8461.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, H., P. K. S. Shin & S. G. Cheung, 2015. Physiological responses and scope for growth upon medium-term exposure to the combined effects of ocean acidification and temperature in a subtidal scavenger Nassarius conoidalis. Marine Environmental Research 106: 51–60.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We wish to thank Dr. Benjamin Harvey for his assistance and guidance with the meta-analysis component of this study. We also thank Dr. Robert Condon, Dr. Luc Comeau, Dr. Remi Sonier, and three anonymous reviewers for constructive feedback which helped improve the original manuscript. This study was funded by a NSERC Visiting Postdoctoral Fellowship to JCC (Grant #501540-2016).

Author information

Authors and Affiliations

  1. Aquaculture and Coastal Ecosystems Section, Fisheries and Oceans Canada, Gulf Fisheries Centre, 343 Université Avenue, Moncton, NB, E1C 9B6, Canada

    Jeff C. Clements

  2. Department of Biology and Marine Biology, Center for Marine Science, University of North Carolina Wilmington, 5600 Marvin K. Moss Lane, Wilmington, NC, 28409, USA

    Elizabeth S. Darrow

Authors
  1. Jeff C. Clements
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth S. Darrow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeff C. Clements.

Additional information

Handling editor: Iacopo Bertocci

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1. Raw data for literature search. Supplementary material 1 (XLSX 26 kb)

10750_2018_3665_MOESM2_ESM.xlsx

Table S2. Correlation matrix for predictor variables used to build additive linear mixed effects models in AIC model selection analysis. Supplementary material 2 (XLSX 8 kb)

Table S3. Raw data for effect size analysis. Supplementary material 3 (XLSX 30 kb)

10750_2018_3665_MOESM4_ESM.xlsx

Table S4. Weighted mean effect sizes, bootstrapped 95% confidence intervals, and Q-test results from effect size analysis. Supplementary material 4 (XLSX 18 kb)

Table S5. AIC model selection results. Supplementary material 5 (XLSX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Clements, J.C., Darrow, E.S. Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia 820, 1–21 (2018). https://doi.org/10.1007/s10750-018-3665-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3665-1

Keywords

Search

Navigation