Ecologically relevant measures of tolerance to potentially lethal temperatures

Abstract

SummaryThe acute thermal tolerance of ectotherms has been measured in a variety of ways; these include assays where organisms are shifted abruptly to stressful temperatures and assays where organisms experience temperatures that are ramped more slowly to stressful levels. Ramping assays are thought to be more relevant to natural conditions where sudden abrupt shifts are unlikely to occur often, but it has been argued that thermal limits established under ramping conditions are underestimates of true thermal limits because stresses due to starvation and/or desiccation can arise under ramping. These confounding effects might also impact the variance and heritability of thermal tolerance. We argue here that ramping assays are useful in capturing aspects of ecological relevance even though there is potential for confounding effects of other stresses that can also influence thermal limits in nature. Moreover, we show that the levels of desiccation and starvation experienced by ectotherms in ramping assays will often be minor unless the assays involve small animals and last for many hours. Empirical data illustrate that the combined effects of food and humidity on thermal limits under ramping and sudden shifts to stressful conditions are unpredictable; in Drosophila melanogaster the presence of food decreased rather than increased thermal limits, whereas in Ceratitis capitata they had little impact. The literature provides examples where thermal limits are increased under ramping presumably because of the potential for physiological changes leading to acclimation. It is unclear whether heritabilities and population differentiation will necessarily be lower under ramping because of confounding effects. Although it is important to clearly define experimental methods, particularly when undertaking comparative assessments, and to understand potential confounding effects, thermotolerance assays based on ramping remain an important tool for understanding and predicting species responses to environmental change. An important area for further development is to identify the impact of rates of temperature change under field and laboratory conditions.

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

“…Nevertheless, in our opinion these confounding effects will be minor relative to heat resistance variation found between species. CT max as estimated in the present study may be confounded by effects of desiccation and starvation (assays are performed without food or moisture for ∼3 h) as discussed recently in the literature (43,44). This might inflate estimates of CT max particularly for highly desiccation/starvation-resistant species, but recent experiments on Drosophila melanogaster have found the impact of desiccation and starvation stress to be negligible with respect to CT max when using heat exposures similar to the one used here (45).…”

Physiology and Biogeography: The Response of European Mussels (Mytilusspp.) to Climate Change*

“…The tolerance of species to cold temperatures depends on a variety of factors, including the thermal regimes and acclimation times experienced (Renault et al 2004, Terblanche et al 2011. Jansen et al (2007) found that Mytilus galloprovincialis populations were much more sensitive to cold shock than M. edulis populations.…”

An invitation to measure insect cold tolerance: Methods, approaches, and workflow

“…It is clear that the rate of temperature change does affect the response of the insect (this has also been vigorously discussed in the context of high temperature tolerances, e.g. Santos et al, 2011;Terblanche et al, 2007;Terblanche et al, 2011). Thus, it is important to maintain consistent cooling rates among sites or species for comparisons, and to be cognizant of the assumptions inherent in comparing thermal limits among studies that used different exposure conditions.…”

“…Kleynhans et al, 2014;MacMillan and Sinclair, 2011b;Terblanche et al, 2006). Note that there has been considerable recent debate on the 'correct' rate for measuring high temperature tolerances Santos et al, 2011;Terblanche et al, 2007;Terblanche et al, 2011), and it is therefore imperative to clearly report the conditions when describing CT min experiments. To expedite measurements, it should be possible to rapidly reduce the temperature from the rearing temperature to an intermediate temperature (e.g.…”