Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits

Abstract

Species’ tolerance limits determine their capacity to tolerate climatic extremes and limit their potential distributions. Interspecific variation in thermal tolerances is often proposed to indicate climatic vulnerability and is, therefore, the subject of many recent meta-studies on differential capacities of species from climatically different habitats to deal with climate change. Most studies on thermal tolerances do not acclimate animals or use inconsistent, and insufficient, acclimation times, limiting our knowledge of the shape, duration and extent of acclimation responses. Consequently patterns in thermal tolerances observed in meta-analyses, based on data from the literature are based on inconsistent, partial acclimation and true trends may be obscured. In this study we describe time-course of complete acclimation of critical thermal minima in the tropical ectotherm Carlia longipes and compare it to the average acclimation response of other reptiles, estimated from published data, to assess how much acclimation time may contribute to observed differences in thermal limits. Carlia longipes decreased their lower critical thermal limits by 2.4°C and completed 95% of acclimation in 17 weeks. Wild populations did not mirror this acclimation process over the winter. Other reptiles appear to decrease cold tolerance more quickly (95% in 7 weeks) and to a greater extent, with an estimated average acclimation response of 6.1°C. However, without data on tolerances after longer acclimation times available, our capacity to estimate final acclimation state is very limited. Based on the subset of data available for meta-analysis, much of the variation in cold tolerance observed in the literature can be attributed to acclimation time. Our results indicate that (i) acclimation responses can be slow and substantial, even in tropical species, and (ii) interspecific differences in acclimation speed and extent may obscure trends assessed in some meta-studies. Cold tolerances of wild animals are representative of cumulative responses to recent environments, while lengthy acclimation is necessary for controlled comparisons of physiological tolerances. Measures of inconsistent, intermediate acclimation states, as reported by many studies, represent neither the realised nor the potential tolerance in that population, are very likely underestimates of species’ physiological capacities and may consequently be of limited value.

Basking behavior predicts the evolution of heat tolerance in Australian rainforest lizards

“…) and broader meta‐analyses of acclimation (Gunderson and Stillman ) all find that physiological traits typically only shift by 1–2°C in response to acute or sustained environmental shifts (but see meta‐analysis of CT min acclimation in Pintor et al. ), whereas our measurements often differed by up to 12°C (Fig. ).…”

“…; Pintor et al. ), we estimated environmental temperature as the mean of the maximum daily temperature for the month preceding capture for T opt and CT max . For CT min and B95 , we used the mean of the minimum daily temperature for the month preceding capture (see “Phylogenetic Analyses” next for explanation).…”

“…For estimates of thermal environment to be most ecologically relevant, mean temperature on a temporal scale appropriate to the conditions influencing physiology at time of capture should be used. Given that most physiological acclimation in lizards occurs within four weeks (Kolbe et al 2012;Pintor et al 2016), we estimated environmental temperature as the mean of the maximum daily temperature for the month preceding capture for T opt and CT max . For CT min and B95, we used the mean of the minimum daily temperature for the month preceding capture (see "Phylogenetic Analyses" next for explanation).…”

Thermoregulatory behaviour explains countergradient variation in the upper thermal limit of a rainforest skink

“…Why was the effect size not larger, given the substantial difference in mean temperature between the two incubation treatments? Perhaps the acclimation experiment only produced a small shift in CT max because the acclimation period was too short: Pintor et al (), for example, demonstrate acclimation occuring over more than five months in other species from northern Australia. Another possible explanation for the small shift is that the sunskinks’ upper thermal limits may not have been challenged sufficiently during acclimation (Otto ).…”

Ecophysiological variation across a forest‐ecotone gradient produces divergent climate change vulnerability within species

“…Plasticity could potentially play an even greater role in mitigating the consequences of warming (Chown et al 2010, Urban et al 2014, Llewelyn et al 2016. For example, in this study, it is possible that the magnitude of the impact we have estimated for both habitat groups would have been less severe if we acclimated the lizards at a warmer temperature before running our experiments (Pintor et al 2016). This is would be driven by the capacity for rapid short-term acclimation in CTmax to warmer temperatures, termed heat-hardening, which has been observed in ectotherms in previous studies (Overgaard et al 2011, Phillips et al 2015.…”