Predicting organismal response to marine heatwaves using dynamic thermal tolerance landscape models.

Marine heatwaves (MHWs) can cause thermal stress in marine organisms, experienced as extreme 'pulses' against the gradual trend of anthropogenic warming. When thermal stress exceeds organismal capacity to maintain homeostasis, organism survival becomes time-limited and can result in mass mortality events. Current methods of detecting and categorizing MHWs rely on statistical analysis of historic climatology and do not consider biological effects as a basis of MHW severity. The re-emergence of ectotherm thermal tolerance landscape models provides a physiological framework for assessing the lethal effects of MHWs by accounting for both the magnitude and duration of extreme heat events. Here, we used a simulation approach to understand the effects of a suite of MHW profiles on organism survival probability across (1) three thermal tolerance adaptive strategies, (2) interannual temperature variation and (3) seasonal timing of MHWs. We identified survival isoclines across MHW magnitude and duration where acute (short duration-high magnitude) and chronic (long duration-low magnitude) events had equivalent lethal effects on marine organisms. While most research attention has focused on chronic MHW events, we show similar lethal effects can be experienced by more common but neglected acute marine heat spikes. Critically, a statistical definition of MHWs does not accurately categorize biological mortality. By letting organism responses define the extremeness of a MHW event, we can build a mechanistic understanding of MHW effects from a physiological basis. Organism responses can then be transferred across scales of ecological organization and better predict marine ecosystem shifts to MHWs.

Environment and phenology shape local adaptation in thermal performance.

Populations within species often exhibit variation in traits that reflect local adaptation and further shape existing adaptive potential for species to respond to climate change. However, our mechanistic understanding of how the environment shapes trait variation remains poor. Here, we used common garden experiments to quantify thermal performance in eight populations of the marine snail Urosalpinx cinerea across thermal gradients on the Atlantic and the Pacific coasts of North America. We then evaluated the relationship between thermal performance and environmental metrics derived from time-series data. Our results reveal a novel pattern of 'mixed' trait performance adaptation, where thermal optima were positively correlated with spawning temperature (cogradient variation), while maximum trait performance was negatively correlated with season length (countergradient variation). This counterintuitive pattern probably arises because of phenological shifts in the spawning season, whereby 'cold' populations delay spawning until later in the year when temperatures are warmer compared to 'warm' populations that spawn earlier in the year when temperatures are cooler. Our results show that variation in thermal performance can be shaped by multiple facets of the environment and are linked to organismal phenology and natural history. Understanding the impacts of climate change on organisms, therefore, requires the knowledge of how climate change will alter different aspects of the thermal environment.

Limited plasticity in thermally tolerant ectotherm populations: evidence for a trade-off.

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming.

Diminished warming tolerance and plasticity in low-latitude populations of a marine gastropod.

Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from native Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance - habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations.