Properties of the shells and byssus filaments secreted by marine mussels are affected by environmental and biotic factors. In this study, we investigated the effects of pH and temperature on shell and byssus in artificially created monospecific and mixed aggregations of the indigenous mussel Mytilus galloprovincialis and the invasive mussel Xenostrobus securis. The variability in the response of the mussels was mainly explained by species-specific interactions derived from the type of aggregation. In the mixed groups, acidic conditions caused a decrease in byssus strength in M. galloprovincialis, but an increase in byssus strength in X. securis. Increased temperature positively affected shell strength in X. securis, but only in mixed aggregations. Interactive effects of acidification and warming were only detected in the organic matter of shells, the strength of which decreased in M. galloprovincialis in mixed aggregations. Although the invasive mussel may be able to take advantage of changed conditions by enhancing byssal attachment, the effects that acidification has on shells may make this species more vulnerable to some predators. The study findings provide some insight into the responses of protective and attachment structures of mussels to biotic and abiotic stressors, highlighting how species interactions may shape the future of mytilid populations.
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Addadi, L., D. Joester, F. Nudelman & S. Weiner, 2006. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry - A European Journal 12: 980–987.
Amaral, V., H. N. Cabral & M. J. Bishop, 2012. Effects of estuarine acidification on predator–prey interactions. Marine Ecology Progress Series 445: 117–127.
Angert, A. L., S. L. LaDeau & R. S. Ostfeld, 2013. Climate change and species interactions: ways forward. Annals of the New York Academy of Sciences 1297: 1–7.
Babarro, J. M. F. & M. J. Abad, 2013. Co-existence of two mytilids in a heterogeneous environment: mortality, growth, and strength of shell and byssus attachment. Marine Ecology Progress Series 476: 115–128.
Babarro, J. M. F. & L. A. Comeau, 2014. Byssus attachment strength of two mytilids in mono-specific and mixed-species mussel beds. Biofouling: The Journal of Bioadhesion and Biofilm Research 30: 975–985.
Babarro, J. M. F. & M. J. Lassudrie, 2011. Ecophysiological responses of invasive and indigenous mytilids in the Ría de Vigo (NW Spain). Aquatic Living Resources 24: 303–315.
Barbosa, M., J. Pestana & A. M. V. M. Soares, 2014. Predation life history responses to increased temperature variability. PLoS ONE 9(9): e107971.
Borthagaray, A. I. & A. Carranza, 2007. Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecologica 31: 243–250.
Chaparro, O. R., J. A. Montory, C. J. Segura & J. A. Pechenik, 2009. Effect of reduced pH on shells of brooded veligers in the estuarine bivalve Ostrea chilensis Philippi 1845. Journal of Experimental Marine Biology and Ecology 377: 107–112.
Conover, W. J., 2012. The rank transformation – an easy and intuitive way to connect many nonparametric methods to their parametric counterparts for seamless teaching introductory statistics courses. WIREs Computational Statistics 4: 432–438.
Dahlhoff, E., B. Buckley & B. Menge, 2001. Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82: 2816–2829.
Doney, S. C., V. J. Fabry, R. A. Feely & J. A. Kleypas, 2009. Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1: 169–192.
Duarte, C., J. M. Navarro, K. Acuña, R. Torres, P. H. Manríquez, M. A. Lardies, C. A. Vargas, N. A. Lagos & V. Aguilera, 2014. Combined effects of temperature and ocean acidification on the juvenile individuals of the mussel Mytilus chilensis. Journal of Sea Research 85: 308–314.
Fabry, V. J., B. A. Seibel, R. A. Feely & J. C. Orr, 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65: 414–432.
Fernández-Reiriz, M. J., 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.
Fitzer, S. C., L. Vittert, A. Bowman, N. A. Kamenos, V. R. Phoenix & M. Cusack, 2015. Ocean acidification and temperature increase impact mussel shell shape and thickness: problematic for protection? Ecology and Evolution 5(21): 4875–4884.
Fitzer, S. C., W. Zhu, K. E. Tanner, V. R. Phoenix, N. A. Kamenos & M. Cusack, 2017. Ocean acidification alters the material properties of Mytilus edulis shells. Journal of the Royal Society Interface 12: 20141227.
Fabricius, K. E., C. Langdon, S. Uthicke, C. Humphrey, S. Noonan, G. Déath, R. Okazaki, N. Muehllehner, M. S. Glas & J. M. Lough, 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change 1: 165–169.
Gabriel, J. M., 1981. Differing resistance of various mollusc shell materials to simulated whelk attack. Journal of Zoology 194: 363–369.
Gazeau, F., C. Quiblier, J. M. Jansen, J.-P. Gattuso, J. J. Middleburg & C. H. R. Heip, 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34: L07603.
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.
Gestoso, I., C. Olabarria & F. Arenas, 2012. The invasive mussel Xenostrobus securis along the Galician Rias Baixas (NW of Spain): status of invasion. Cahiers de Biologie Marine 53: 391–396.
Gestoso, I., F. Arenas & C. Olabarria, 2015. Feeding behaviour of an intertidal snail: does past environmental stress affect predator choices and prey vulnerability? Journal of Sea Research 97: 66–74.
Gestoso, I., C. Olabarria & F. Arenas, 2016. Ecological interactions modulate responses of two intertidal mussel species to changes in temperature and pH. Journal of Experimental Marine Biology and Ecology 474: 116–125.
Hale, R., P. Calosi, L. McNeill, N. Mieszkowska & S. Widdicombe, 2011. Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120: 661–674.
Harrington, M. J. & J. H. Waite, 2007. Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads. Journal of Experimental Biology 210: 4307–4318.
Hiebenthal, C., E. E. R. Philipp, A. Eisenhauer & M. Wahl, 2013. Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.). Marine Biology 160: 2073–2087.
Hughes, L., 2012. Climate change impacts on species interactions: assessing the threat of cascading extinctions. In Hannath, L. (ed.), Saving a million species. Extinction risk from climate change. Island Press, Washington, DC.
IPCC, 2013. Climate change 2013. The Physical Science Basis. Summary for Policymakers. Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
Ivanina, A. V., G. H. Dickinson, O. B. Matoo, R. Bagwe, A. Dickinson, E. Beniash & I. M. Sokolova, 2013. Interactive effects of elevated temperature and CO2 levels on energy metabolism and biomineralization of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Comparative Biochemistry and Physiology, Part A 166: 101–111.
Jurgens, L. J. & B. Gaylord, 2016. Edge effects reverse facilitation by a widespread foundation species. Scientific Reports 6: 37573.
Kimura, T. & H. Sekiguchi, 2009. Spatial and temporal patterns of abundance of the exotic mytilid Xenostrobus securis and the native mytilid Musculista senhousia in the Lake Hamana, Japan. Marine Biodiversity Records 2: e89.
Kroeker, K. J., F. Micheli, M. C. Gambi & T. R. Martz, 2011. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proceedings of the National Academy of Sciences of the United States of America 108: 14515–14520.
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.
Kroeker, K. J., B. Gaylord, T. M. Hill, J. D. Hosfelt, S. H. Miller & E. Sanford, 2014. The role of temperature in determining species´ vulnerability to ocean acidification: a case study using Mytilus galloprovincialis. PLoS ONE 9(7): e100353.
Lamarck, J.-B. M., 1819. Histoire naturelle des animaux sans vertèbres. Tome sixième, 1re partie. Paris: vi + 343 pp.
Li, S., C. Liu, J. Huang, Y. Liu, G. Zheng, L. Xie & R. Zhang, 2015. Interactive effects of seawater acidification and elevated temperature on biomineralization and amino acid metabolism in the mussel Mytilus edulis. Journal of Experimental Biology 218: 3623–3631.
Mackenzie, C. L., G. A. Ormondroyd, S. F. Curling, R. J. Ball, N. M. Whiteley & S. K. Malham, 2014. Ocean warming, more than acidification, reduces shell strength in a commercial shellfish species during food limitation. PLoS One 9: e86764.
Marin, F., G. Luquet, B. Marie & D. Medakovic, 2008. Molluscan shell proteins: primary structure, origin, and evolution. Current Topics in Developmental Biology 80: 209–276.
Meehl, G. A., T. F. Stocker, W. D. Collins, P. Friedlingstein, A. T. Gaye, J. M. Gregory, et al., 2007. Global climate projections. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis & K. B. Averyt (eds), Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
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. Marine Ecology Progress Series 293: 109–118.
Milano, S., G. Nehrke, A. D. Wanamaker Jr., I. Ballesta-Artero, T. Brey & B. R. Schöne, 2017. The effects of environment on Arctica islandica shell formation and architecture. Biogeosciences 14: 1577–1591.
Montoya, J. M. & D. Raffaelli, 2010. Climate change, biotic interactions and ecosystem services. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 2013–2018.
Morse, J. W., A. Mucci & F. J. Millero, 1980. The solubility of calcite and aragonite in seawater of 35‰ salinity at 25 & #xB0;C and atmospheric pressure. Geochimica et Cosmochimica Acta 44: 85–94.
Morton, B., 2008. Attack responses of the southern Australian whelk, Lepsiella vinosa (Lamarck, 1822) (Gastropoda: Muricidae), to novel bivalve prey: an experimental approach. Biological Invasions 10: 1265–1275.
Nienhuis, S., A. R. Palmer & C. D. G. Harley, 2010. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proceedings of the Royal Society B: Biological Sciences 277(1693): 2553–2558.
O’Donnell, M. J., M. N. George & E. Carrington, 2013. Mussel byssus attachment weakened by ocean acidification. Nature Climate Change 3: e587–e590.
Olabarria, C., I. Gestoso, F. P. Lima, E. Vázquez, L. A. Comeau, F. Gomes, R. Seabra & J. M. F. Babarro, 2016. Response of two mytilids to a heatwave: the complex interplay of physiology, behaviour and ecological interactions. PLoS ONE 11(10): e0164330.
Pilson, M. E., 2013. An Introduction to the Chemistry of the Sea. Cambridge University Press, Cambridge.
Pörtner, H. O., 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology Progress Series 373: 203–217.
Pörtner, H. O. & A. P. Farrel, 2008. Physiology and climate change. Science 322: 690–692.
Pörtner, H. O., M. Langenbuch & B. Michaelidis, 2005. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. Journal of Geophysical Research 110: 1–15.
Queirós, A. M., J. A. Fernandes, S. Faulwetter, J. Nunes, A. P. S. Rastrick, N. Mieszkowska, Y. Artioli, A. Yool, P. Calosi, C. Arvanitidis, H. S. Findlay, M. Barange, W. W. L. Cheung & S. Widdicombe, 2015. Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Global Change Biology 21: 130–143.
Range, P., D. Piló, R. Ben-Hamadou, M. A. Chícharo, D. Matias, S. Joaquim, A. P. Oliveira & 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 424–425: 89–98.
Range, P., M. A. Chícharo, R. Ben-Hamadou, D. Piló, M. J. Fernández-Reiriz, U. Labarta, M. G. Marin, M. Bressan, V. Matozzo, A. Chinellato, M. Munari, E. T. El Menif, M. Dellali & L. Chícharo, 2014. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Regional Environmental Change 14(Suppl 1): S19–S30.
Raven, J., K. Caldeira, H. Elderfield, O. Hoegh-Guldberg, P. S. Liss, U. Riebesell, J. Sheperd, C. Turley & A. Watson, 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Royal Society, London: 57.
Ries, J. B., A. L. Cohen & D. C. McCorkle, 2009. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: 1131–1134.
Scanes, E., L. M. Parker, W. A. ÓConnor, L. S. Stapp & P. M. Ross, 2017. Intertidal oysters reach their physiological limit in a future high-CO2 world. Journal of Experimental Biology 220: 765–774.
Sui, Y., M. Hu, X. Huang, Y. Wang & W. Lu, 2015. Anti-predatory responses of the thick shell mussel Mytilus coruscus exposed to seawater acidification and hypoxia. Marine Environmental Research 109: 159–167.
Waite, J. H., 2002. Adhesion à la Moule. Intregrative and Comparative Biology 42: 1172–1180.
Walther, G.-R., 2010. Community and ecosystem responses to recent climate change. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 2019–2024.
Welladsen, H. M., P. C. Southgate & K. Heimann, 2010. The effects of exposure to near-future levels of ocean acidification on shell characteristics of Pinctada fucata (Bivalvia: Pteriidae). Molluscan Research 30(3): 125–130.
Zeebe, R. E. & D. Wolf-Gladrow, 2001. CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier, Amsterdam.
Zhao, X., C. Guo, Y. Han, Z. Che, Y. Wang, X. Wang, X. Chai, H. Wu & G. Liu, 2017. Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses. Marine Ecology Progress Series 565: 67–77.
This study was funded by the Spanish government through the Ministerio de Economía y Competitividad (projects AGL2013-45945-R and CTM2016-76146-C3-2-R) and the Autonomic government Xunta de Galicia-FEDER (project GRC2013-004). We thank three anonymous reviewers who provided helpful comments on the original manuscript.
Handling editor: Iacopo Bertocci
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Babarro, J.M.F., Abad, M.J., Gestoso, I. et al. Susceptibility of two co-existing mytilid species to simulated predation under projected climate change conditions. Hydrobiologia 807, 247–261 (2018). https://doi.org/10.1007/s10750-017-3397-7
- Mytilus galloprovincialis
- Xenostrobus securis
- Protective structure
- Byssus attachment
- Climate change