Coastal ecosystems are exposed to changes in physical-chemical properties, such as those occurring in upwelling and freshwater-influenced areas. In these areas, inorganic carbon can influence seawater properties that may affect organisms and populations inhabiting benthic habitats such as the intertidal mussel Perumytilus purpuratus. Feeding and metabolic responses were measured in adult mussels from two geographic regions (central and southern Chile) and two local habitats (river-influenced and non-river-influenced) and three pCO2 levels (380, 750, and 1200 μatm pCO2 in seawater). The feeding rates of mussels tend to increase at high pCO2 levels in seawater; however this response was variable across regions and local habitats. In contrast, there was no difference in the respiratory rate of mussels between geographic areas, but there was a significant reduction of oxygen consumption at intermediate and high levels of pCO2. The results indicate that river-influenced organisms compensate for reductions in metabolic cost at elevated pCO2 levels by having their energy demands met, in contrast with non-river-influenced organisms. The lack of regional-scale variability in the physiological performance of mussels may indicate physiological homogeneity across populations and thus potential for local adaptation. However, the local-scale influences of river- and non-river-influenced habitats may counterbalance this regional response promoting intra-population variability and phenotypic plasticity in P. purpuratus. The plasticity may be an important mechanism that allows mussels to confront the challenges of projected ocean acidification scenarios.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Bamsted, U., D.J. Gifford, X. Irigoien, A. Atkinson, and M. Roman. 2000. Feeding. In ICES Zooplankton Methodology Manual, ed. R. Harris, P.H. Wiebe, J. Lenz, H.R. Skjoldal, and M. Huntley, 297–399. Academic Press.
Beniash, E., A. Ivanina, N.S. Lieb, I. Kurochkin, and I.M. Sokolova. 2010. Elevated levels of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Marine Ecology Progress Series 419: 95–108.
Berge, J.A., B. Bjerkeng, O. Pettersen, M.T. Schaanning, and S. Oxnevad. 2006. Effects of increased sea water concentrations of CO2 on growth of the bivalve Mytilus edulis L. Chemosphere 62: 681–687.
Breitburg, D.L., J. Salisbury, J.M. Bernhard, W.-J. Cai, S. Dupont, S.C. Doney, K.J. Kroeker, L.A. Levin, W.C. Long, L.M. Milke, S.H. Miller, B. Phelan, U. Passow, B.A. Seibel, A.E. Todgham, and A.M. Tarrant. 2015. And on top of all that… coping with ocean acidification in the midst of many stressors. Oceanography 28 (2): 48–61. https://doi.org/10.5670/oceanog.2015.31.
Briones, C., P. Presa, M. Pérez, A. Pita, and R. Guiñez. 2013. Genetic connectivity of the ecosystem engineer Perumytilus purpuratus north to the 32°S southeast Pacific ecological discontinuity. Marine Biology 160: 3143–3156.
Cai, W.J., X. Hu, W.-J. Huang, M.C. Murrell, J.C. Lehrter, S.E. Lohrenz, W-Ch. Chou, W. Zhai, J.T. Hollibaugh, Y. Wang, P. Zhao, X. Guo, K. Gundersen, M. Dai, and G-Ch. Gong. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience 4: 766–770. https://doi.org/10.1038/ngeo1297.
Caldeira, K., and M.E. Wickett. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research 110: C09S04. https://doi.org/10.1029/2004JC002671.
Cao, Long, Shuangjing Wang, Meidi Zheng, and Han Zhang. 2014. Sensitivity of ocean acidification and oxygen to the uncertainty in climate change. Environmental Research Letters 9: 64005 IOP Publishing. https://doi.org/10.1088/1748-9326/9/6/064005.
Clayton, T.D., and R.H. Byrne. 1993. Spectrophotometric seawater pH measurements: Total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep Sea Research Part I: Oceanographic Research Papers 40: 2115–2129. https://doi.org/10.1016/0967-0637(93)90048-8.
Coughlan, J. 1969. The estimation of filtering rate from the clearance of suspensions. Marine Biology 2: 356–358.
Cummings, V., J. Hewitt, A. Van Rooyen, K. Currie, S. Beard, S. Thrush, J. Norkko, N.L. Barr, P. Heath, N.J. Halliday, R. Sedcole, A. Gomez, C.H. McGraw, and V. Metcalf. 2011. Ocean acidification at high latitudes: Potential effects on functioning of the Antarctic bivalve Laternula elliptica. PLoS One 6 (1): e16069. https://doi.org/10.1371/journal.pone.0016069.
DOE. 1992. Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water. DOE Handbook 1994: 22. Doi:ORNL/CDIAC-74.
Doney, S.C., M. Ruckelshaus, J.E. Duffy, J.P. Barry, F. Chan, Ch.A. English, H.M. Galindo, J.M. Grebmeier, A.B. Hollowed, N. Knowlton, J. Polovina, N.N. Rabalais, W.J. Sydeman, and L.D. Talley. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science Annual Reviews 4: 11–37. https://doi.org/10.1146/annurev-marine-041911-111611.
Duarte, C.M., I.E. Hendriks, T.S. Moore, Y.S. Olsen, A. Steckbauer, L. Ramajo, J. Carstensen, J.A. Trotter, and M. McCulloch. 2013. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36: 221–236. https://doi.org/10.1007/s12237-013-9594-3.
Duarte, C., J.M. Navarro, K. Acuña, R. Torres, P.H. Manríquez, M.A. Lardies, C.A. Vargas, N.A. Lagos, and V. Aguilera. 2014. Intraspecific variability in the response of the edible mussel Mytilus chilensis (Hupe) to ocean acidification. Estuaries and Coasts 38: 590–598. https://doi.org/10.1007/s12237-014-9845-y.
Fabry, V., B.A. Seibel, R.A. Feely, and J.C. Orr. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65 (3): 414–432. https://doi.org/10.1093/icesjms/fsn048.
Feely, R., Ch.L. Sabine, J.M. Hernandez-Ayon, D. Ianson, and B. Hales. 2008. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320: 1490–1492. https://doi.org/10.1126/science.1155676.
Fernández-Reiriz, M.J., P. Range, X.A. Álvarez-Salgado, and U. Labarta. 2011. Physiological energetics of juvenile clams Ruditapes decussatus in a high CO2 coastal ocean. Marine Ecology Progress Series 433: 97–105. https://doi.org/10.3354/meps09062.
Gattuso, J.P., A. Magnan, R. Bille, W.W.L. Cheung, E.L. Howes, F. Joos, D. Allemand, L. Bopp, S.R. Cooley, C.M. Eakin, O. Hoegh-Guldberg, R.P. Kelly, H.O. Pörtner, A.D. Rogers, J.M. Baxter, D. Laffoley, D. Osborn, A. Rankovic, J. Rochette, U.R. Sumaila, S. Treyer, and C. Turley. 2015. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349: aac4722-1–aac4722-10. https://doi.org/10.1126/science.aac4722.
Gazeau, F., L.M. Parker, S. Comeau, J.P. Gattuso, W.A. O’Connor, S. Martin, H.O. Pörtner, and P.M. Ross. 2013. Impacts of ocean acidification on marine shelled molluscs. Marine Biology 160: 2207–2245. https://doi.org/10.1007/s00227-013-2219-3.
Godbold, J., and P. Calosi. 2013. Ocean acidification and climate change: Advances in ecology and evolution. Philosophical Transactions of the Royal Society B 368 (1627): 20120448. https://doi.org/10.1098/rstb.2012.0448.
Kroeker, K.J., R.L. Kordas, R.N. Crim, and G.G. Singh. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13: 1419–1434 Blackwell Publishing Ltd. https://doi.org/10.1111/j.1461-0248.2010.01518.x.
Kroeker, Kristy J., Rebecca L. Kordas, Ryan Crim, Iris E. Hendriks, Laura Ramajo, Gerald S. Singh, Carlos M. Duarte, and Jean Pierre Gattuso. 2013. Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Global Change Biology 19: 1884–1896. https://doi.org/10.1111/gcb.12179.
Lagos, N.A., F.J. Tapia, S.A. Navarrete, and J.C. Castilla. 2007. Spatial synchrony in the recruitment of intertidal invertebrates along the coast of central Chile. Marine Ecology Progress Series 350: 29–39.
Lardies, M.A., J.L. Muñoz, K.A. Paschke, and F. Bozinovic. 2011. Latitudinal variation in the aerial/aquatic ratio of oxygen consumption of a supratidal high rocky-shore crab. Marine Ecology 32: 42–51. https://doi.org/10.1111/j.1439-0485.2010.00408.x.
Lardies, M.A., M. Belén, M. Jose, P.H. Manríquez, R. Torres, C.A. Vargas, J.M. Navarro, and N.A. Lagos. 2014. Differential response to ocean acidification in physiological traits of Concholepas concholepas populations. Journal of Sea Research 90: 127–134. https://doi.org/10.1016/j.seares.2014.03.010.
Lewis, C.N., K.A. Brown, L.A. Edwards, G. Cooper, and H.S. Findlay. 2013. Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice. Proceedings of the National Academy of Sciences of the United States of America 110: E4960–E4967. https://doi.org/10.1073/pnas.1315162110.
Liu, W., and 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. https://doi.org/10.1007/s00343-012-1067-1.
Magnan, A.K., M. Colombier, R. Billé, F. Joos, O. Hoegh-Guldberg, H.O. Pörtner, H. Waisman, T. Spencer, and J.P. Gattuso. 2016. Implications of the Paris agreement for the ocean. Nature Climate Change 6: 732–735. https://doi.org/10.1038/nclimate3038.
Melzner, F., P. Stange, K. Trübenbach, J. Thomsen, I. Casties, U. Panknin, S. Gorb, and M. Gutowska. 2011. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS One 6 (9): e24223. https://doi.org/10.1371/journal.pone.0024223.
Michaelidis, B., C. Ouzounis, A. Paleras, and 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. https://doi.org/10.3354/meps293109.
Navarro, J.M., R. Torres, K. Acuña, C. Duarte, P.H. Manriquez, M.A. Lardies, N.A. Lagos, C.A. Vargas, and 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. https://doi.org/10.1016/j.chemosphere.2012.09.063.
O’Connor, M.I., J.F. Bruno, S.D. Gaines, B.S. Halpern, S.E. Lester, B.P. Kinlan, and J.M. Weiss. 2007. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proceedings of the National Academy of Sciences USA 104: 1266–1271.
Palmer, A.R. 1982. Growth in marine gastropods: A non-destructive technique for independently measuring shell and body weight. Malacologia 23: 63–73.
Pérez, C.A., M.D. DeGrandpre, N.A. Lagos, G.S. Saldías, E.K. Cascales, and C.A. Vargas. 2015. Influence of climate and land use in carbon biogeochemistry in lower reaches of rives in central southern Chile: Implications for the carbonate system in river-influenced rocky shore environments. Journal of Geophysical Research: Biogeosciences 120 (4): 673–692. https://doi.org/10.1002/2014JG002699.
Pérez, C.A., N.A. Lagos, G.S. Saldías, G. Waldbusser, and C.A. Vargas. 2016. Riverine discharges impact physiological traits and carbon sources for shell carbonate in the marine intertidal mussel Perumytilus purpuratus. Limnology and Oceanography 61: 969–983. https://doi.org/10.1002/lno.10265.
Ramajo, L., N. Marbà, L. Prado, S. Peron, M.A. Lardies, A.B. Rodriguez-Navarro, C.A. Vargas, N.A. Lagos, and C.M. Duarte. 2016a. Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification. Global Change Biology 22: 2025–2037. https://doi.org/10.1111/gcb.13179.
Ramajo, L., L. Prado, A.B. Rodriguez-Navarro, M.A. Lardies, C.M. Duarte, and N.A. Lagos. 2016b. Plasticity and trade-offs in physiological traits of intertidal mussels subjected to freshwater-induced environmental variation. Marine Ecology Progress Series 553: 93–109. https://doi.org/10.3354/meps11764.
Range, P., D. Piló, R. Ben-Hamadou, M.A. Chícharo, D. Matias, S. Joaquim, A.P. Oliveira, and L. Chícharo. 2012. Seawater acidification by CO2 in a coastal lagoon environment: Effects on life history traits of juvenile mussels Mytilus galloprovincialis. Journal of Experimental Marine Biology and Ecology 424: 89–98. https://doi.org/10.1016/j.jembe.2012.05.010.
Range, P., M.A. Chícharo, R. Ben-Hamadou, D. Piló, M.J. Fernandez-Reiriz, U. Labarta, M.G. Marin, M. Bressan, V. Matozzo, A. Chinellato, M. Munari, N.T. El Menif, M. Dellali, and L. Chícharo. 2014. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Regional Environmental Change 14: 19–30. https://doi.org/10.1007/s10113-013-0478-7.
Sobarzo, M., L. Bravo, D. Donoso, J. Garcés-Vargas, and W. Schneider. 2007. Coastal upwelling and seasonal cycles that influence the water column over the continental shelf off central Chile. Progress in Oceanography 75: 363–382. https://doi.org/10.1016/j.pocean.2007.08.022.
Sokolova, I.M., O.B. Matoo, G.H. Dickinson, and E. Beniash. 2016. Physiological effects of ocean acidification on animal calcifiers. In Stressors in the Marine Environment, 36–55. Oxford University Press. Doi:https://doi.org/10.1093/acprof:oso/9780198718826.003.0003.
Stillman, J.H., and A.W. Paganini. 2015. Biochemical adaptation to ocean acidification. Journal of Experimental Biology 218: 1946–1955. https://doi.org/10.1242/jeb.115584.
Stillman, J.H., and G.N. Somero. 2000. A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: Influences of latitude, vertical zonation, acclimation, and phylogeny. Physiological and Biochemical Zoology 73: 200–208. https://doi.org/10.1086/316738.
Storch, D., M. Fernández, S.A. Navarrete, and H.O. Pörtner. 2011. Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus. Marine Ecology Progress Series 429: 157–167. https://doi.org/10.3354/meps09059.
Strickland, J.D.H., and T.R. Parsons. 1968. Determination of reactive phosphorus. A practical handbook of seawater analysis. Fisheries Research Board of Canada, Bulletin 167: 49–56.
Stumpp, M., S. Dupont, M.C. Thorndyke, and F. Melzner. 2011. CO2 induced seawater acidification impacts sea urchin larval development II: gene expression patterns in pluteus larvae. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 160: 320–330. Doi:https://doi.org/10.1016/j.cbpa.2011.06.023.
Sui, Yanming, Hui Kong, Xizhi Huang, Sam Dupont, Menghong Hu, Daniela Storch, Hans-Otto Pörtner, Weiqun Lu, and Youji Wang. 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. https://doi.org/10.1016/j.chemosphere.2016.04.054.
Sui, Yanming, Yimeng Liu, Xin Zhao, Sam Dupont, Menghong Hu, Fangli Wu, Xizhi Huang, Jiale Li, Weiqun Lu, and Youji Wang. 2017. Defense responses to short-term hypoxia and seawater acidification in the thick shell mussel Mytilus coruscus. Frontiers in physiology 8. Frontiers Media SA: 145. doi:https://doi.org/10.3389/fphys.2017.00145.
Thomsen, J., I. Casties, Ch. Pansch, A. Körtzinger, and F. Melzner. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: Laboratory and field experiments. Global Change Biology 19: 1017–1027. https://doi.org/10.1111/gcb.12109.
Torres, R., P.H. Manriquez, C. Duarte, J.M. Navarro, N.A. Lagos, C.A. Vargas, and M.A. Lardies. 2013. Evaluation of a semi-automatic system for long-term seawater carbonate chemistry manipulation. Revista Chilena de Historia Natural 86: 443–451. https://doi.org/10.4067/S0716-078X2013000400006.
Turley, C., and K. Boot. 2010. Environmental consequences of ocean acidification: A threat to food security. UNEP Emerging Issues Bulletin 12.
Vargas, C.A., M. de la Hoz, V. Aguilera, V.S. Martin, P.H. Manriquez, J.M. Navarro, R. Torres, M.A. Lardies, and N.A. Lagos. 2013. CO2-driven ocean acidification reduces larval feeding efficiency and changes food selectivity in the mollusk Concholepas concholepas. Journal of Plankton Research 35 (5): 1059–1068.
Vargas, C.A., V.M. Aguilera, V. San Martín, P.H. Manríquez, J.M. Navarro, C. Duarte, R. Torres, M.A. Lardies, and 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. https://doi.org/10.1007/s12237-014-9873-7.
Vargas, C.A., P.Y. Contreras, C.A. Pérez, M. Sobarzo, G.S. Saldías, and J. Salisbury. 2016. Influences of riverine and upwelling waters on the coastal carbonate system off Central Chile and their ocean acidification implications. Journal of Geophysical Research G: Biogeosciences 121: 1468–1483. https://doi.org/10.1002/2015JG003213.
Vargas, C.A., N.A. Lagos, M.A. Lardies, C. Duarte, P.H. Manríquez, V.M. Aguilera, B. Broitman, S. Widdicombe, and S. Dupont. 2017. Species-specific responses to ocean acidification should account for local adaptation and adaptative plasticity. Nature ecology and evolution 1: 0084. https://doi.org/10.1038/s41559-017-0084.
Waldbusser, G.G., and J.E. Salisbury. 2014. Ocean acidification in the coastal zone from an organism’s perspective: Multiple system parameters, frequency domains, and habitats. Annual Review of Marine Science 6: 221–247. https://doi.org/10.1146/annurev-marine-121211-172238.
Wang, Youji, Lisha Li, Menghong Hu, and Lu. Weiqun. 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. https://doi.org/10.1016/j.scitotenv.2015.01.092.
Zhen, Yu, Jiang Aili, and Changhai Wang. 2010. Oxygen consumption, ammonia excretion, and filtration rate of the marine bivalve Mytilus edulis exposed to methamidophos and omethoate. PLoS One 43: 243–255. https://doi.org/10.1080/10236244.2010.498124.
Technical support received from the laboratory LAFE is greatly appreciated.
This work was supported by the FONDECYT grants 1090624 and 1140938 (TOA-SPACE Projects) to N. Lagos and C. Vargas, with additional support from the Millennium Nucleus “Center for the Study of Multiple-drivers on Marine Socio-Ecological Systems (MSELS),” funded by MINECON NC120086, and the Millennium Institute of Oceanography (IMO) funded by MINECON IC120019. Additional support from FONDECYT 1130254 to C. Vargas, and the Post-Doctoral FONDECYT Project 3150392 to L. Saavedra, is also acknowledged. Any data used in this paper can be obtained by contacting the corresponding author.
Conflict of Interest
The authors declare that they have no conflicts of interest.
Communicated by Marianne Holmer
Rights and permissions
About this article
Cite this article
Saavedra, L.M., Parra, D., Martin, V.S. et al. Local Habitat Influences on Feeding and Respiration of the Intertidal Mussels Perumytilus purpuratus Exposed to Increased pCO2 Levels. Estuaries and Coasts 41, 1118–1129 (2018). https://doi.org/10.1007/s12237-017-0333-z
- Ocean acidification
- Perumytilus purpuratus
- Phenotypic plasticity