Calcifiers can Adjust Shell Building at the Nanoscale to Resist Ocean Acidification

Abstract

Ocean acidification is considered detrimental to marine calcifiers based on laboratory studies showing that increased seawater acidity weakens their ability to build calcareous shells needed for growth and protection. In the natural environment, however, the effects of ocean acidification are subject to ecological and evolutionary processes that may allow calcifiers to buffer or reverse these short‐term negative effects through adaptive mechanisms. Using marine snails inhabiting a naturally CO2‐enriched environment over multiple generations, it is discovered herein that they build more durable shells (i.e., mechanically more resilient) by adjusting the building blocks of their shells (i.e., calcium carbonate crystals), such as atomic rearrangement to reduce nanotwin thickness and increased incorporation of organic matter. However, these adaptive adjustments to future levels of ocean acidification (year 2100) are eroded at extreme CO2 concentrations, leading to construction of more fragile shells. The discovery of adaptive mechanisms of shell building at the nanoscale provides a new perspective on why some calcifiers may thrive and others collapse in acidifying oceans, and highlights the inherent adaptability that some species possess in adjusting to human‐caused environmental change.

How the Pacific Oyster Responds to Ocean Acidification: Development and Application of a Meta-Analysis Based Adverse Outcome Pathway

“…Such impacts are of concern given that mollusks fulfill numerous ecological roles (Gazeau et al, 2013), provide an abundance of ecosystem services (Lemasson et al, 2017), and represent an aquaculture industry that was worth US $19 billion globally in 2016 (FAO, 2016). The effects of ocean acidification on calcifying mollusks have been suggested to result largely from impacts on the development of calcified structures, as well as their maintenance via enhanced erosion and dissolution due to the increased porosity of the shells' internal microstructure (e.g., Marshall et al, 2008;Nienhuis et al, 2010;Rodolfo-Metalpa et al, 2011;Fitzer et al, 2015Fitzer et al, , 2016Fitzer et al, , 2019Meng et al, 2018;Byrne and Fitzer, 2019;Leung et al, 2020a). Although calcification represents one of the physiological processes most susceptible to ocean acidification (Kroeker et al, 2010), studies have only relatively recently started to unravel the complex drivers of such effects (e.g., Meng et al, 2018;Clark et al, 2020;Leung et al, 2020b).…”

“…The required reallocation of metabolic resources to maintain calcified structures appears to occur at the detriment of other physiological processes including growth, reproduction, and immune system function (Wood et al, 2008;Scanes et al, 2014;Garilli et al, 2015;Harvey and Moore, 2017;Leung et al, 2017;Telesca et la., 2019). Promisingly, some calcifying mollusks can buffer the effects of acidification through energy reallocation (Leung et al, 2020b), adjusting internal pH (Zhao et al, 2018), and adjusting the mineralogical composition of their shells (Leung et al, 2017(Leung et al, , 2020a. It is important to note, however, that such adaptive capacities may be considerably reduced when acidity is modified to more extreme levels, indicating that processes associated with calcification may lack the capacity to overcome the challenges of future acidification (Leung et al, 2020a).…”

“…Promisingly, some calcifying mollusks can buffer the effects of acidification through energy reallocation (Leung et al, 2020b), adjusting internal pH (Zhao et al, 2018), and adjusting the mineralogical composition of their shells (Leung et al, 2017(Leung et al, , 2020a. It is important to note, however, that such adaptive capacities may be considerably reduced when acidity is modified to more extreme levels, indicating that processes associated with calcification may lack the capacity to overcome the challenges of future acidification (Leung et al, 2020a). Of particular concern are changes occurring in oysters, which are a group of considerable economic and ecological importance (see Lemasson et al, 2017 and references therein).…”

Morphological Properties of Gastropod Shells in a Warmer and More Acidic Future Ocean Using 3D Micro-Computed Tomography

“…Three different polymorphs of biogenic CaCO 3 structures have been found in marine shells (aragonite, calcite and vaterite) that represent complex composites of one or more mineral phases and organic molecules (Nehrke et al, 2012). Calcifiers can adjust their shell strength and properties, which depend on the thickness and packing (i.e., porosity) of calcium carbonate crystals, in order to build more durable shells under ocean acidification conditions (Leung et al, 2020). Ocean acidification might be causing a shift to a more disorganized crystallographic structure in shells, thus reducing their structural integrity and the ability of marine calcifiers to biomineralise (Fitzer et al, 2015).…”

“…Thicker and architecturally more diverse shells are a fitness advantage for molluscs as an adaptation to predators (Fisher et al, 2009). Ocean acidification may not only lead to increased fragility of shells but may also elevate energetic costs for shell formation or repairing (Leung et al, 2020). The capacity of molluscs to maintain their shell calcification mechanisms under altered environmental conditions will regulate their successful adaptation and persistence in the future.…”