Conservation of thermal physiology in tropical intertidal snails following an evolutionary transition to a cooler ecosystem: climate change implications.

Predictions for animal responses to climate warming usually assume that thermal physiology is adapted to present-day environments, and seldom consider the influence of evolutionary background. Little is known about the conservation of warm-adapted physiology following an evolutionary transition to a cooler environment. We used cardiac thermal performance curves (cTPCs) of six neritid gastropod species to study physiological thermal trait variation associated with a lineage transition from warmer rocky shores to cooler mangroves. We distinguished between functional thermal performance traits, related to energy homeostasis (slope gradient, slope curvature, HRmax, maximum cardiac activity and Topt, the temperature that maximizes cardiac activity) and a trait that limits performance (ULT, the upper lethal temperature). Considering the theory of optimal thermal performance, we predicted that the functional traits should be under greater selective pressure to change directionally and in magnitude than the thermal limit, which is redundant in the cooler environment. We found little variation in all traits across species, habitats and ecosystems, despite a ~20°C reduction in maximum habitat temperature in the mangrove species over 50 million years. While slope gradient was significantly lowered in the mangrove species, the effect difference was negated by greater thermal plasticity in the rocky shore species. ULT showed the least variation and suggested thermal specialization in the warmest habitat studied. The observed muted variation of the functional traits among the species may be explained by their limited role in energy acquisition and rather their association with heat tolerance adaptation, which is redundant in the mangrove species. These findings have implications for the conservation of habitat of intertidal gastropods that transition to cooler environments. Furthermore, they highlight the significance of evolutionary history and physiological conservation when predicting species responses to climate change.

Tracking coastal acidification from erosion of gastropod shells: spatial sensitivity and organism size effect.

The rapidly changing marine environmental chemistry associated with growing industrialisation, urban population expansion, and the unabated rise in atmospheric CO2 necessitates monitoring. Traditional approaches using metres, dataloggers, and buoys to monitor marine acidification have limited application in coastal oceans and intertidal zones subjected to direct wave action. The present study trialled a system to biomonitor coastal acidification (carbonate ion and pH) based on the dissolution of living gastropod shells. We extended on an approach that ranked shell erosion (SER) in Nerita chamaeleon (Nc) in environments where such erosion was found to correlate with exposure to acidified water. We assessed the spatial scale at which the Nc-SER marker could detect change in acidification along rocky shores, and whether snail body size affected this marker. We found that proportional and unique Nc-SERs not only varied between acidified and non-acidified reference shores at a coarse spatial scale (10 km), but also in predictable ways at fine scales (metres), vertically and horizontally within a shore. Differences between acidified and reference shores in the relationship for snail size and Nc-SER were accentuated by less weathered shells at reference localities, highlighting the value of including small, juvenile snails in monitoring protocols. Gastropod shells are shown to be useful for assessing point sources of acidification and the spatial area of affected coastal zones. This cost-effective and easy-to-use approach (potentially even by citizen-scientists) offers an early warning system of acidification of rocky shore ecosystems, where the deployment of instruments is precluded.

Biomonitoring acidification using marine gastropods.

Ocean acidification is mainly being monitored using data loggers which currently offer limited coverage of marine ecosystems. Here, we trial the use of gastropod shells to monitor acidification on rocky shores. Animals living in areas with highly variable pH (8.6-5.9) were compared with those from sites with more stable pH (8.6-7.9). Differences in site pH were reflected in size, shape and erosion patterns in Nerita chamaeleon and Planaxis sulcatus. Shells from acidified sites were shorter, more globular and more eroded, with both of these species proving to be good biomonitors. After an assessment of baseline weathering, shell erosion can be used to indicate the level of exposure of organisms to corrosive water, providing a tool for biomonitoring acidification in heterogeneous intertidal systems. A shell erosion ranking system was found to clearly discriminate between acidified and reference sites. Being spatially-extensive, this approach can identify coastal areas of greater or lesser acidification. Cost-effective and simple shell erosion ranking is amenable to citizen science projects and could serve as an early-warning-signal for natural or anthropogenic acidification of coastal waters.

Substantial heat tolerance acclimation capacity in tropical thermophilic snails, but to what benefit?

The theory for thermal acclimation of ectotherms suggests that (1) heat tolerance is traded off for thermal acclimation in thermophilic species and that (2) plasticity is constrained in tropically distributed ectotherms, which commonly experience relatively thermally stable environments. We observed substantial heat tolerance plasticity in a test of this theory using tropical, thermophilic marine intertidal snails that inhabit extremely hot and highly variable thermal environments. The implication of these results is that plasticity selection is largely driven by habitat temperature conditions irrespective of basal heat tolerance or latitude. However, heat tolerance of field-fresh snails was comparable with that of laboratory warm-acclimated snails, suggesting that snails in the field may often be unable to improve heat hardening with further environmental warming. These findings suggest that field referencing is crucial to using laboratory-measured acclimation capacity when inferring climate warming vulnerability in ectotherms, and overall they question how well current thermal biology theory predicts the outcomes of global change in intertidal environments.

Non-reversible and Reversible Heat Tolerance Plasticity in Tropical Intertidal Animals: Responding to Habitat Temperature Heterogeneity.

The theory for thermal plasticity of tropical ectotherms has centered on terrestrial and open-water marine animals which experience reduced variation in diurnal and seasonal temperatures, conditions constraining plasticity selection. Tropical marine intertidal animals, however, experience complex habitat thermal heterogeneity, circumstances encouraging thermal plasticity selection. Using the tropical rocky-intertidal gastropod, Echinolittorina malaccana, we investigated heat tolerance plasticity in terms of laboratory acclimation and natural acclimatization of populations from thermally-dissimilar nearby shorelines. Laboratory treatments yielded similar capacities of snails from either population to acclimate their lethal thermal limit (LT50 variation was ∼2°C). However, the populations differed in the temperature range over which acclimatory adjustments could be made; LT50 plasticity occurred over a higher temperature range in the warm-shore snails compared to the cool-shore snails, giving an overall acclimation capacity for the populations combined of 2.9°C. In addition to confirming significant heat tolerance plasticity in tropical intertidal animals, these findings reveal two plasticity forms, reversible (laboratory acclimation) and non-reversible (population or shoreline specific) plasticity. The plasticity forms should account for different spatiotemporal scales of the environmental temperature variation; reversible plasticity for daily and tidal variations in microhabitat temperature and non-reversible plasticity for lifelong, shoreline temperature conditions. Non-reversible heat tolerance plasticity, likely established after larvae settle on the shore, should be energetically beneficial in preventing heat shock protein overexpression, but also should facilitate widespread colonization of coasts that support thermally-diverse shorelines. This first demonstration of different plasticity forms in benthic intertidal animals supports the hypothesis that habitat heterogeneity (irrespective of latitude) drives thermal plasticity selection. It further suggests that studies not making reference to different spatial scales of thermal heterogeneity, nor seeking how these may drive different thermal plasticity forms, risk misinterpreting ectothermic responses to environmental warming.