Physiological acclimation and persistence of ectothermic species under extreme heat events

Abstract

Aim To test if physiological acclimation can buffer species against increasing extreme heat due to climate change. Location Global. Time period 1960 to 2015. Major taxa studied Amphibians, arthropods, brachiopods, cnidarians, echinoderms, fishes, molluscs, reptiles. Methods We draw together new and existing data quantifying the warm acclimation response in 319 species as the acclimation response ratio (ARR): the increase in upper thermal limit per degree increase in experimental temperature. We develop worst‐case scenario climate projections to calculate the number of years and generations gained by ARR until loss of thermal safety. We further compute a vulnerability score that integrates across variables estimating exposure to climate change and species‐specific tolerance through traits, including physiological plasticity, generation time and latitudinal range extent. Results ARR is highly variable, but with marked differences across taxa, habitats and latitude. Polar terrestrial arthropods show high ARRs [95% upper confidence limit (UCL95%) = 0.68], as do some polar aquatic invertebrates that were acclimated for extended durations (ARR > 0.4). While this physiological plasticity buys 100s of years until thermal safety is lost, combination with long generation times leads to decreased potential for evolutionary adaptation. Additionally, 27% of marine polar invertebrates have no capacity for acclimation and reptiles and amphibians have minimal ARR (UCL95% = 0.16). Low physiological plasticity, long generations times and restricted latitudinal ranges combine to distinguish reptiles, amphibians and polar invertebrates as being highly vulnerable amongst ectotherms. Main conclusions In some taxa the combined effects of acclimation capacity and generation time can provide 100s of years and generations before thermal safety is lost. The accuracy of assessments of vulnerability to climate change will be improved by considering multiple aspects of species’ biology that, in combination may increase persistence under extreme heat events, and increase the probability for evolutionary rescue.

Egg incubation temperature does not influence adult heat tolerance in the lizard Anolis sagrei

“…Global warming is driving an increase in the frequency of extreme heat events that induce physiological stress [33], cause mass die-offs [34] and increase extinction risk [8]. Developmental plasticity has the potential to reduce the negative effects of extreme temperatures by increasing heat tolerance, especially given that nest temperatures are projected to rise along with body temperatures of free-ranging animals [35].…”

Climate change and ageing in ectotherms

“…The study of telomere dynamics in populations inhabiting divergent temperature conditions might allow us to evaluate the effects of human‐induced thermal stress on ageing rates. This would be particularly relevant for populations of ectotherms living in regions of rapid thermal change, especially if they have long generation times that slow the potential rate of adaptation to changing environments (Morley, Peck, Sunday, Heiser, & Bates, 2019). Species with shorter generation time and larger populations are predicted to evolve quickly while maintaining genetic variation (Hoffmann & Sgrò, 2011).…”

“…Metabolic rates of terrestrial, freshwater, and marine ectothermic species are predicted to keep increasing in the coming decades (Seebacher et al., 2015). Plasticity is, on average, higher in aquatic than terrestrial ectotherms (Gunderson & Stillman, 2015; Huey et al., 2012; Morley et al., 2019), and it may buffer the negative impact of warming on ectotherm physiology. However, plasticity alone cannot fully protect aquatic ectotherms from overheating (Gunderson et al., 2017).…”

Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus

“…The extents to which these effects have occurred, and will continue to occur, depend largely on the adaptive and plastic capacities of organisms to adjust key physiological traits, such as thermal tolerance limits (especially in aquatic ectotherms; Sunday et al, 2012;Pinsky et al, 2019), in response to increased temperatures (e.g., Crain et al, 2008;Somero, 2010;Bay et al, 2017;Kellermann and van Heerwaarden, 2019). In particular, given that rapid phenotypic changes are necessary due to high rates of environmental change (e.g., Barrett and Hendry, 2012;Fox et al, 2019), phenotypic plasticity may play a critical role in the resilience of populations and species to the effects of climate change (Merilä and Hendry, 2014;Donelson et al, 2019;Morley et al, 2019).…”