Environmental change impacts on shell formation in the muricid Nucella lapillus

Environmental change is a significant threat to marine ecosystems worldwide. Ocean acidification, global warming and long-term emissions of anthropogenic effluents are all negatively impacting aquatic life. Marine calcifying organisms, in particular, are expected to be severely affected by decreasing seawater pH, resulting in shell dissolution and retardations during the formation and repair of shells. Understanding the underlying biological and environmental factors driving species vulnerabilities to habitat alterations is thus crucial to our ability to faithfully predict impacts on marine ecosystems under an array of environmental change scenarios. So far, existing knowledge about organism responses mainly stems from short to medium term laboratory experiments of single species or over- simplified communities. Although these studies have provided important insights, results may not translate to organism responses in a complex natural system requiring a more holistic experimental approach. In this thesis, I investigated shell formation mechanisms and shape and elemental composition responses in the shell of the important intertidal predatory muricid Nucella lapillus both in situ and across heterogeneous environmental gradients. The aim was to identify potential coping mechanisms of N. lapillus to environmental change and provide a more coherent picture of shell formation responses along large ecological gradients in the spatial and temporal domain. To investigate shell formation mechanisms, I tested for the possibility of shell recycling as a function to reduce calcification costs during times of exceptional demand using a multi-treatment shell labelling experiment. Reports on calcification costs vary largely in the literature. Still, recent discoveries showed that costs might increase as a function of decreasing calcification substrate abundance, suggesting that shell formation becomes increasingly more costly under future environmental change scenarios. However, despite the anticipated costs, no evidence was found that would indicate the use of functional dissolution as a means to recycle shell material for a more cost-efficient shell formation in N. lapillus. To investigate shell formation responses, I combined morphometric and shell thickness analyses with novel statistical methods to identify natural shape and thickness response of N. lapillus to large scale variability in temperature, salinity, wind speed and the carbonate system across a wide geographic range (from Portugal to Iceland) and through time (over 130 years). I found that along geographical gradients, the state of the carbonate system and, more specifically, the substrate inhibitor ratio ([HCO3−][H+]−1) (SIR) was the main predictor for shape variations in N. lapillus. Populations in regions with a lower SIR tend to form narrower shells with a higher spire to body whorl ratio. In contrast, populations in regions with a higher SIR form wider shells with a much lower spire to body whorl ratio. The results suggest a widespread phenotypic response of N. lapillus to continuing ocean acidification could be expected, affecting its phenotypic response patterns to predator or wave exposure regimes with profound implications for North Atlantic rocky shore communities. On the contrary, investigations of shell shape and thickness changes over the last 130 years from adjacent sampling regions on the Southern North Sea coast revealed that contrary to global predictions, N. lapillus built continuously thicker shells while maintaining a consistent shell shape throughout the last century. Systematic modelling efforts suggested that the observed shell thickening resulted from higher annual temperatures, longer yearly calcification windows, nearshore eutrophication, and enhanced prey abundance, which mitigated the impact of other climate change factors. An investigation into the trace elemental composition of common pollutant metals in the same archival N. lapillus specimens revealed that shell Cu/Ca and Zn/Ca concentration ratios remained remarkably constant throughout the last 130 years despite substantial shifts in the environmental concentration. However, Pb/Ca concentration ratios showed a definite trend closely aligned with leaded petrol emissions in Europe over the same period. Discussing physiological and environmental drivers for the observed shell bound heavy metal patterns, I argue that, unlike for Pb, constraints on environmental dissolved Cu species abundance and biologically mediated control on internal Zn levels were likely responsible for a decoupling of shell-bound to total ambient Cu and Zn concentrations. The results highlight the complexity of internal and external pathways that govern the uptake of heavy metals into the molluscan shell and suggest that the shell of N. lapillus could be a suitable archive for a targeted investigation of Pb pollution in the intertidal zone.

Mayk D., 2022. Environmental change impacts on shell formation in the muricid Nucella lapillus. PhD thesis, University of Cambridge. Thesis (restricted access).

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