in

Plasticity in organic composition maintains biomechanical performance in shells of juvenile scallops exposed to altered temperature and pH conditions

  • 1.

    Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320, 1490–1492 (2008).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 2.

    Hofmann, G. E. et al. High-frequency dynamics of ocean ph: A multi-ecosystem comparison. PLoS ONE 6(12), e28983 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 3.

    Kroeker, K. J. et al. Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. Ecol. Lett. 19, 771–779 (2016).

    PubMed 

    Google Scholar 

  • 4.

    Gutiérrez, D. et al. Coastal cooling and increased productivity in the main upwelling zone off Peru since the mid-twentieth century. Geophys. Res. Lett. 38, L07603. https://doi.org/10.1029/2010GL046324 (2011).

    ADS 
    Article 

    Google Scholar 

  • 5.

    Aiken, C. M., Navarrete, S. A. & Pelegrí, J. L. Potential changes in larval dispersal and alongshore connectivity on the central Chilean coast due to an altered wind climate. J. Geophys. Res. 116, G04026. https://doi.org/10.1029/2011JG001731 (2011).

    ADS 
    Article 

    Google Scholar 

  • 6.

    Lagos, N. A., Castilla, J. C. & Broitman, B. Spatial Environmental correlates of intertidal recruitment: A test using barnacles in northern Chile. Ecol. Monogr. 78, 245–261 (2008).

    Google Scholar 

  • 7.

    Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 84. https://doi.org/10.1038/s41559-017-0084 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 8.

    Broitman, B. R. et al. Phenotypic plasticity is not a cline: Thermal physiology of an intertidal barnacle over 20° of latitude. J. Anim. Ecol. 00, 1–12. https://doi.org/10.1111/1365-2656.13514 (2021).

    Article 

    Google Scholar 

  • 9.

    Ramajo, L. et al. Physiological responses of juvenile Chilean scallops (Argopecten purpuratus) to isolated and combined environmental drivers of coastal upwelling. ICES J. Mar. Sci. 76, 1836e1849 (2019).

    Google Scholar 

  • 10.

    Saavedra, L. M., Saldías, G., Broitman, B. & Vargas, C. Carbonate chemistry dynamics in shellfish farming areas along the Chilean coast: Natural ranges and biological implications. ICES J. Mar. Sci. 78, 323–339 (2021).

    Google Scholar 

  • 11.

    Lardies, M. A. et al. Physiological and histopathological impacts of increased carbon dioxide and temperature on the scallops Argopecten purpuratus cultured under upwelling influences in northern Chile. Aquaculture 479, 455–466 (2017).

    Google Scholar 

  • 12.

    Ramajo, L. et al. Upwelling intensity modulates the fitness and physiological performance of coastal species: Implications for the aquaculture of the scallop Argopecten purpuratus in the Humboldt Current System. Sci. Total Environ. 745, 140949 (2020).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 13.

    Bakun, A. Global climate change and intensification of coastal ocean upwelling. Science 247, 198–201 (1990).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 14.

    Wang, D. et al. Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518, 390–394 (2015).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 15.

    Kim, T. W., Barry, J. P. & Micheli, F. The effects of intermittent exposure to low-pH and low-oxygen conditions on survival and growth of juvenile red abalone. Biogeosciences 10, 7255–7262 (2013).

    ADS 

    Google Scholar 

  • 16.

    Ramajo, L. et al. Plasticity and trade-offs in physiological traits of intertidal mussels subjected to freshwater-induced environmental variation. Mar. Ecol. Prog. Ser. 553, 93–109 (2016).

    ADS 

    Google Scholar 

  • 17.

    Leung, J. Y., Connell, S. D., Nagelkerken, I. & Russell, B. D. Impacts of near-future ocean acidification and warming on the shell mechanical and geochemical properties of gastropods from intertidal to subtidal zones. Environ. Sci. Technol. 51, 12097–12103 (2017).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 18.

    Findlay, H. et al. Calcification, a physiological process to be considered in the context of the whole organism. Biogeosciences Discuss. 6, 2267–2284 (2009).

    ADS 

    Google Scholar 

  • 19.

    Waldbusser, G. et al. Saturation-state sensitivity of marine bivalves larvae to ocean acidification. Nat. Clim. Change 5, 273–280 (2015).

    ADS 
    CAS 

    Google Scholar 

  • 20.

    Tunnicliffe, V. et al. Survival of mussels in extremely acidic waters on a submarine volcano. Nat. Geosci. 2, 344–348 (2009).

    ADS 
    CAS 

    Google Scholar 

  • 21.

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

    ADS 
    CAS 

    Google Scholar 

  • 22.

    Leung, J. Y., Russell, B. D. & Connell, S. D. Mineralogical plasticity acts as a compensatory mechanism to the impacts of ocean acidification. Environ. Sci. Technol. 51, 2652–2659 (2017).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 23.

    Duarte, C. et al. The energetic physiology of juvenile mussels, Mytilus chilensis (Hupe): The prevalent role of salinity under current and predicted pCO2 scenarios. Environ. Pollut. 242, 156–163 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 24.

    Rodolfo-Metalpa, R. et al. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat. Clim. Change. 1, 308–312 (2011).

    ADS 
    CAS 

    Google Scholar 

  • 25.

    Waldbusser, G. et al. Slow shell building, a possible trait for resistance to the effects of acute ocean acidification. Limnol. Oceanogr. 61, 1969–1983 (2016).

    ADS 

    Google Scholar 

  • 26.

    Fitzer, S. C. et al. Ocean acidification and temperature increase impact mussel shell shape and thickness: Problematic for protection?. Ecol. Evol. 5, 4875–4884 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 27.

    Fitzer, S. C., Phoenix, V. R., Cusack, M. & Kamenos, N. A. Ocean acidification impacts mussel control on biomineralization. Sci. Rep. 28, 6218 (2014).

    Google Scholar 

  • 28.

    Fitzer, S. C., Cusack, M., Phoenix, V. R. & Kamenos, N. A. Ocean acidification reduces the crystallographic control in juvenile mussel shells. J. Struct. Biol. 188, 39–45 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • 29.

    Fitzer, S. C. et al. Biomineral shell formation under ocean acidification: A shift from order to chaos. Sci. Rep. 6, 21076 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Lagos, N. A. et al. Effects of temperature and ocean acidification on shell characteristics of Argopecten purpuratus: Implications for scallop aquaculture in an upwelling-influenced area. Aquac. Environ. Interact. 8, 357–370 (2016).

    Google Scholar 

  • 31.

    Ramajo, L. et al. Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification. Glob. Chang. Biol. 22, 2025–2203 (2016).

    ADS 
    PubMed 

    Google Scholar 

  • 32.

    Osores, S. J. et al. Plasticity and inter-population variability in physiological and life-history traits of the mussel Mytilus chilensis: A reciprocal transplant experiment. J. Exp. Mar. Biol. Ecol. 490, 1–12 (2017).

    Google Scholar 

  • 33.

    Telesca, L. et al. Plasticity and environmental heterogeneity predict geographic resilience patterns of foundation species to future change. Glob. Chang. Biol. https://doi.org/10.1111/gcb.14758 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Grenier, C. et al. The combined effects of salinity and pH on shell biomineralization of the edible mussel Mytilus chilensis. Environ. Pollut. 263, 114555 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • 35.

    Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: Quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

    ADS 

    Google Scholar 

  • 36.

    Mackenzie, C. L. et al. Ocean warming, more than acidification, reduces shell strength in a commercial shellfish species during food limitation. PLoS ONE 9(1), e86764 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 37.

    Rykaczewski, R. R. et al. Poleward displacement of coastal upwelling-favorable winds in the ocean’s eastern boundary currents through the 21st century. Geophys. Res. Lett. 42, 6424–6431 (2015).

    ADS 

    Google Scholar 

  • 38.

    Rodríguez-Navarro, A. B. Rapid quantification of avian eggshell microstructure and crystallographic-texture using two-dimensional X-ray diffraction. Br. Poult. Sci. 48, 133–144 (2007).

    PubMed 

    Google Scholar 

  • 39.

    Rodríguez-Navarro, A. B. XRD2DScan: New software for polycrystalline materials characterization using two-dimensional X-ray diffraction. J. Appl. Cryst. 39, 905–909 (2006).

    Google Scholar 

  • 40.

    Li, S. et al. Interactive effects of seawater acidification and elevated temperature on biomineralization and amino acid metabolism in the mussel Mytilus edulis. J. Exp. Biol. 218, 3623–3631 (2015).

    PubMed 

    Google Scholar 

  • 41.

    Li, S. et al. Interactive effects of seawater acidification and elevated temperature on the transcriptome and biomineralization in the pearl oyster Pinctada fucata. Environ. Sci. Technol. 50, 1157–1165 (2016).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 42.

    Gestoso, I., Arenas, F. & Olabarria, C. Ecological interactions modulate responses of two intertidal mussel species to changes in temperature and pH. J. Exp. Mar. Biol. 474, 116–125 (2016).

    Google Scholar 

  • 43.

    Babarro, J. M., Abad, M. J., Gestoso, I., Silva, E. & Olabarria, C. Susceptibility of two co-existing mytilid species to simulated predation under projected climate change conditions. Hydrobiologia 807, 247–261 (2018).

    Google Scholar 

  • 44.

    Barthelat, F., Rim, J. E. & Espinosa, H. D. A review on the structure and mechanical properties of mollusk shells: Perspectives on synthetic biomimetic materials. In Applied Scanning Probe Methods XIII (eds Bhushan, B. & Fuchs, H.) 17–44 (Springer, 2009).

    Google Scholar 

  • 45.

    Leung, J. Y. et al. Calcifiers can adjust shell building at the nanoscale to resist ocean acidification. Small 16, 2003186 (2020).

    CAS 

    Google Scholar 

  • 46.

    Chatzinikolaou, E., Grigoriou, P., Keklikoglou, K., Faulwetter, S. & Papageorgiou, N. The combined effects of reduced pH and elevated temperature on the shell density of two gastropod species measured using micro-CT imaging. ICES J. Mar. Sci. 74, 1135–1149 (2017).

    Google Scholar 

  • 47.

    Nienhuis, S., Palmer, R. & Harley, C. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proc. R. Soc. Lond. B Biol. Sci. 277, 2553–2558 (2010).

    CAS 

    Google Scholar 

  • 48.

    Bourdeau, P. E. Prioritized phenotypic responses to combined predators in a marine snail. Ecology 90, 1659–1669 (2009).

    PubMed 

    Google Scholar 

  • 49.

    Weiner, S. & Addadi, L. Crystallization pathways in biomineralization. Annu. Rev. Mater. Sci. 41, 21–40 (2011).

    ADS 
    CAS 

    Google Scholar 

  • 50.

    Nudelman, F. Nacre biomineralisation: A review on the mechanisms of crystal nucleation (In Seminars in cell & developmental biology), 2–10 (Academic Press, 2015).

  • 51.

    Harper, E. M., Checa, A. G. & Rodríguez-Navarro, A. B. Organization and mode of secretion of the granular prismatic microstructure of Entodesma navicular (Bivalvia: Mollusca). Acta Zool. 90, 132e141 (2009).

    Google Scholar 

  • 52.

    Pennington, B. J. & Currey, J. D. A mathematical model for the mechanical properties of scallop shells. J. Zool. 202, 239–263 (1984).

    Google Scholar 

  • 53.

    Yevenes, M. A., Lagos, N. A., Farías, L. & Vargas, C. A. Greenhouse gases, nutrients and the carbonate system in the Reloncaví Fjord (Northern Chilean Patagonia): Implications on aquaculture of the mussel, Mytilus chilensis, during an episodic volcanic eruption. Sci. Total Environ. 669, 49–61 (2019).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 54.

    Dickinson, G. H. et al. Interactive effects of salinity and elevated CO2 levels on juvenile eastern oysters, Crassostrea virginica. J. Exp. Biol. 215, 29–43 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • 55.

    Gaylord, B. et al. Functional impacts of ocean acidification in an ecologically critical foundation species. J. Exp. Biol. 214, 2586–2594 (2011).

    CAS 
    PubMed 

    Google Scholar 

  • 56.

    O’Toole-Howes, M. et al. Deconvolution of the elastic properties of bivalve shell nanocomposites from direct measurement and finite element analysis. J. Mater. Res. 34, 2869–2880 (2019).

    ADS 

    Google Scholar 

  • 57.

    Auzoux-Bordenave, S. et al. Ocean acidification impacts growth and shell mineralization in juvenile abalone (Haliotis tuberculata). Mar. Biol. 167, 11 (2020).

    CAS 

    Google Scholar 

  • 58.

    Torres, R. et al. Evaluation of a semiautomatic system for long-term seawater carbonate chemistry manipulation. Rev. Chil. Hist. Nat. 86, 443–451 (2013).

    Google Scholar 

  • 59.

    IPCC. Climate Change 2021. The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Eds. Masson-Delmotte, V., P. Zhai, A. Pirani, S.L. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M.I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J.B.R. Matthews, T.K. Maycock, T. Waterfield, O. Yelekçi, R. Yu, and B. Zhou). Cambridge University Press. In Press. (2021).

  • 60.

    DOE. Handbook of methods for the analysis of the various parameters of the carbon dioxide system in seawater; version 2 (eds. Dickson, A.G. & Goyet, C.), (ORNL/CDIAC, 74, 1994).

  • 61.

    Meinshausen, M. et al. The RPC greenhouse gas concentrations and their extensions from 1765 to 2300. Clim. Change. 109, 213–241 (2011).

    ADS 
    CAS 

    Google Scholar 

  • 62.

    Rahn, D. A., Rosenblüth, B. & Rutllant, J. A. Detecting subtle seasonal transitions of upwelling in North-Central Chile. J. Phys. Oceanogr. 45, 854–867 (2015).

    ADS 

    Google Scholar 

  • 63.

    Meng, Y., Guo, Z., Yao, H., Yeung, K. W. & Thiyagarajan, V. Calcium carbonate unit realignment under acidification: A potential compensatory mechanism in an edible estuarine oyster. Mar. Pollut. Bull. 139, 141–149 (2019).

    CAS 
    PubMed 

    Google Scholar 

  • 64.

    Rasband, W. S. ImageJ U.S. National Institute of Health, Maryland, USA (1997–2020).


  • Source: Ecology - nature.com

    The power of economics to explain and shape the world

    Expanding the conversation about sustainability