Thicker Shells Compensate Extensive Dissolution in Brachiopods under Future Ocean Acidification.

Organisms with long generation times require phenotypic plasticity to survive in changing environments until genetic adaptation can be achieved. Marine calcifiers are particularly vulnerable to ocean acidification due to dissolution and a reduction in shell-building carbonate ions. Long-term experiments assess organisms' abilities to acclimatize or even adapt to environmental change. Here we present an unexpected compensatory response to extensive shell dissolution in a highly calcium-carbonate-dependent organism after long-term culture in predicted end-century acidification and warming conditions. Substantial shell dissolution with decreasing pH posed a threat to both a polar ( Liothyrella uva) and a temperate ( Calloria inconspicua) brachiopod after 7 months and 3 months exposure, respectively, with more extensive dissolution in the polar species. This impact was reflected in decreased outer primary layer thickness in the polar brachiopod. A compensatory response of increasing inner secondary layer thickness, and thereby producing a thicker shell, was exhibited by the polar species. Less extensive dissolution in the temperate brachiopod did not affect shell thickness. Increased temperature did not impact shell dissolution or thickness. Brachiopod ability to produce a thicker shell when extensive shell dissolution occurs suggests this marine calcifier has great plasticity in calcification providing insights into how similar species might cope under future environmental change

Ocean acidification does not impact shell growth or repair of the Antarctic brachiopod Liothyrella uva (Broderip, 1833)

Marine calcifiers are amongst the most vulnerable organisms to ocean acidification due to reduction in the availability of carbonate ions for skeletal/shell deposition. However, there are limited long-term studies on the possible impacts of increased pCO2 on these taxa. A 7 month CO2 perturbation experiment was performed on one of the most calcium carbonate dependent species, the Antarctic brachiopod Liothyrella uva, which inhabits the Southern Ocean where carbonate ion saturation levels are amongst the lowest on Earth. The effects of the predicted environmental conditions in 2050 and 2100 on the growth rate and ability to repair shell in L.uva were tested with four treatments; a low temperature control (0°C, pH7.98), a pH control (2°C, pH8.05), mid-century scenario (2°C, pH7.75) and end-century scenario (2°C, pH7.54). Environmental change impacts on shell repair are rarely studied, but here repair was not affected by either acidified conditions or temperature. Growth rate was also not impacted by low pH. Elevated temperature did, however, increase growth rates. The ability of L.uva to continue, and even increase shell production in warmer and acidified seawater suggests that this species can acclimate to these combined stressors and generate suitable conditions for shell growth at the site of calcification.Emma Cross is supported by the NERC PhD Studentship (NE/T/A/2011).This is the accepted manuscript. The final version is available at http://www.sciencedirect.com/science/article/pii/S0022098114002743

A 120-year record of resilience to environmental change in brachiopods

The inability of organisms to cope in changing environments poses a major threat to their survival. Rising carbon dioxide concentrations, recently exceeding 400 μatm, are rapidly warming and acidifying our oceans. Current understanding of organism responses to this environmental phenomenon is based mainly on relatively short‐ to medium‐term laboratory and field experiments, which cannot evaluate the potential for long‐term acclimation and adaptation, the processes identified as most important to confer resistance. Here, we present data from a novel approach that assesses responses over a centennial timescale showing remarkable resilience to change in a species predicted to be vulnerable. Utilising museum collections allows the assessment of how organisms have coped with past environmental change. It also provides a historical reference for future climate change responses. We evaluated a unique specimen collection of a single species of brachiopod (Calloria inconspicua) collected every decade from 1900 to 2014 from one sampling site. The majority of brachiopod shell characteristics remained unchanged over the past century. One response, however, appears to reinforce their shell by constructing narrower punctae (shell perforations) and laying down more shell. This study indicates one of the most calcium‐carbonate‐dependent species globally to be highly resilient to environmental change over the last 120 years and provides a new insight for how similar species might react and possibly adapt to future change

Thicker shells compensate extensive dissolution in brachiopods under future ocean acidification

Organisms with long generation times require phenotypic plasticity to survive in changing environments until genetic adaptation can be achieved. Marine calcifiers are particularly vulnerable to ocean acidification due to dissolution and a reduction in shell-building carbonate ions. Long-term experiments assess organisms’ abilities to acclimatise or even adapt to environmental change. Here we present an unexpected compensatory response to extensive shell dissolution in a highly calcium-carbonate-dependent organism after long-term culture in predicted end-century acidification and warming conditions. Substantial shell dissolution with decreasing pH posed a threat to both a polar (Liothyrella uva) and a temperate (Calloria inconspicua) brachiopod after 7 months and 3 months exposure, respectively, with more extensive dissolution in the polar species. This impact was reflected in decreased outer primary layer thickness in the polar brachiopod. A compensatory response of increasing inner secondary layer thickness, and thereby producing a thicker shell was exhibited by the polar species. Less extensive dissolution in the temperate brachiopod did not affect shell thickness. Increased temperature did not impact shell dissolution or thickness. Brachiopod ability to produce a thicker shell when extensive shell dissolution occurs suggests this marine calcifier has great plasticity in calcification providing insights into how similar species might cope under future environmental change

The demise of large tropical brachiopods and the Mesozoic Marine Revolution

Changes in predator–prey interactions are often implicated as drivers of major evolutionary change. A prominent example is the dramatic changes in shallow marine assemblages during the Mesozoic Marine Revolution (MMR) when major clades, including rhynchonelliform brachiopods, became restricted and less diverse. Currently, shallow-water temperate and polar brachiopods can be large, but in the tropics, they are small. By contrast, we demonstrate that throughout the Jurassic large brachiopods occurred in shallow sites, from polar to tropical latitudes, but are absent in later periods from tropical areas. These changes occurred in parallel in both major orders (Rhynchonellida and Terebratulida) and also independently within the two sub-ordinal lineages within the Terebratulida (terebratulinids and terebratellinids). Increases in both grazing and predation pressures associated with the MMR might account for this pattern. However, we note that many current environments support both large brachiopods and high densities of grazing species and suggest that the pattern fits more closely to the intensification of durophagous predation in shallow tropical waters

Gradients in marine predation pressure

Aim: There is a general paradigm that marine predation pressure increases towards the tropics and decreases with depth. However, data demonstrating global trends are generally lacking. Rhynchonelliform brachiopods inhabit all the oceans and often survive shell-crushing predator attacks. We investigate shell repair in brachiopods across a range of southern hemisphere and tropical northern hemisphere latitudes and depths. Location: Southern hemisphere and tropical northern hemisphere. Methods: We analysed the frequency of shell repair in 112 bulk samples, over 70 % of which showed traces of shell damage and repair. Results: The pattern of shell repair frequency (RF) was more complicated than the anticipated increase with decreasing latitude, with low levels at both polar and tropical sites but high levels at temperate latitudes. This pattern is evident, however, only in shallow water assemblages; and there is no latitudinal trend in water deeper than 200 m, where shell repair frequency is systematically low. There was a significant logarithmic relationship between RF and depth. Low polar repair rates reflect reduced predation pressure, directly supporting the global paradigm. Low rates in the tropics appears counter to the paradigm. However tropical brachiopods are generally very small (micromorphic) in shallow water and below the minimum size at which damage is recorded anywhere. Main conclusions: Predation pressure decreased logarithmically with depth. At shallow depths (<200m) repair frequency showed highest levels in the mid, temperate latitudes decreasing frequency towards both the tropics and the poles. Low levels of shell repair at high latitudes are likely due to a lack of crushing predators but in the tropics suggest that the low frequency is a result of the small size of tropical brachiopods and hypothesise that micromorphy in this region may be an outcome of high predation pressure.This is the final version of the article. It first appeared from Wiley via https://doi.org/10.1111/geb.1244

Evolutionary conservation and divergence of the transcriptional regulation of bivalve shell secretion across life history stages

Acknowledgements and Funding Information We are grateful to Andrew Gillis for use for paraffin histology and microscopy equipment and enthusiastic support of this work and the Rothera marine team for collecting the adult Laternula elliptica broodstock. This work was supported by UKRI Natural Environment Research Council (NERC) Core Funding to the British Antarctic Survey, a DTG Studentship (Project Reference: NE/J500173/1) and a Junior Research Fellowship to V.A.S. from Wolfson College, University of Cambridge. Review History: https://www.webofscience.com/api/gateway/wos/peer-review/10.1098/rsos.221022/Peer reviewedPublisher PD

Blue mussel shell shape plasticity and natural environments: a quantitative approach

Shape variability represents an important direct response of organisms to selective environments. Here, we use a combination of geometric morphometrics and generalised additive mixed models (GAMMs) to identify spatial patterns of natural shell shape variation in the North Atlantic and Arctic blue mussels, Mytilus edulis and M. trossulus, with environmental gradients of temperature, salinity and food availability across 3980 km of coastlines. New statistical methods and multiple study systems at various geographical scales allowed the uncoupling of the developmental and genetic contributions to shell shape and made it possible to identify general relationships between blue mussel shape variation and environment that are independent of age and species influences. We find salinity had the strongest effect on the latitudinal patterns of Mytilus shape, producing shells that were more elongated, narrower and with more parallel dorsoventral margins at lower salinities. Temperature and food supply, however, were the main drivers of mussel shape heterogeneity. Our findings revealed similar shell shape responses in Mytilus to less favourable environmental conditions across the different geographical scales analysed. Our results show how shell shape plasticity represents a powerful indicator to understand the alterations of blue mussel communities in rapidly changing environments.The work was funded by the European Union Seventh Framework Programme, Marie Curie ITN under grant agreement n° 605051

A century of coping with environmental and ecological changes via compensatory biomineralization in mussels

Accurate biological models are critical to predict biotic responses to climate change and human‐caused disturbances. Current understanding of organismal responses to change stems from studies over relatively short timescales. However, most projections lack long‐term observations incorporating the potential for transgenerational phenotypic plasticity and genetic adaption, the keys to resistance. Here, we describe unexpected temporal compensatory responses in biomineralization as a mechanism for resistance to altered environmental conditions and predation impacts in a calcifying foundation species. We evaluated exceptional archival specimens of the blue mussel Mytilus edulis collected regularly between 1904 and 2016 along 15 km of Belgian coastline, along with records of key environmental descriptors and predators. Contrary to global‐scale predictions, shell production increased over the last century, highlighting a protective capacity of mussels for qualitative and quantitative trade‐offs in biomineralization as compensatory responses to altered environments. We also demonstrated the role of changes in predator communities in stimulating unanticipated biological trends that run contrary to experimental predictive models under future climate scenarios. Analysis of archival records has a key role for anticipating emergent impacts of climate change