Glycogen, not dehydration or lipids, limits winter survival of side-blotched lizards (Uta stansburiana)

Abstract

SUMMARYClimate change is causing winters to become milder (less cold and shorter). Recent studies of overwintering ectotherms have suggested that warmer winters increase metabolism and decrease winter survival and subsequent fecundity. Energetic constraints (insufficient energy stores) have been hypothesized as the cause of winter mortality but have not been tested explicitly. Thus, alternative sources of mortality, such as winter dehydration, cannot be ruled out. By employing an experimental design that compared the energetics and water content of lizards that died naturally during laboratory winter with those that survived up to the same point but were then sacrificed, we attempt to distinguish among multiple possible causes of mortality. We test the hypothesis that mortality is caused by insufficient energy stores in the liver, abdominal fat bodies, tail or carcass or through excessive water loss. We found that lizards that died naturally had marginally greater mass loss, lower water content, and less liver glycogen remaining than living animals sampled at the same time. Periodically moistening air during winter reduced water loss, but this did not affect survival, calling into question dehydration as a cause of death. Rather, our results implicate energy limitations in the form of liver glycogen, but not lipids, as the primary cause of mortality in overwintering lizards. When viewed through a lens of changing climates, our results suggest that if milder winters increase the metabolic rate of overwintering ectotherms, individuals may experience greater energetic demands. Increased energy use during winter may subsequently limit individual survival and possibly even impact population persistence.

Long‐term changes in abundances of Sonoran Desert lizards reveal complex responses to climatic variation

“…Rising T min and T e can increase energetic costs of maintenance metabolism if inactive, nonforaging individuals experience physiologically costly body temperatures (Brischoux, Dupou e, Lourdais, & Angelier, 2016;Clarke & Zani, 2012;Patterson & Davies, 1978;Zani, 2008;Zani et al, 2012). Despite the relative novelty of these patterns, core aspects of lizard behavior and thermal biology suggest a mechanism we proposed is plausible.…”

“…In arid environments, P often drives rapid increases in plant biomass, seed production, and insect abundance, which bolsters food availability for small vertebrates, increasing their abundance at short lag times and predator abundance at longer lag times (Beatley, 1969;Holmgren et al, 2006). Alternatively, high T min could reduce the quality of low-temperature thermoregulatory refugia and increase energetic costs of maintenance metabolism during dormancy or nocturnal inactivity in ways that diminish energy reserves for reproduction and hence abundance the following year (Zani, 2008;Zani et al, 2012). Similarly, the predation hypothesis predicts lizard abundance in year t decreases with P at longer lag times or is highest at moderate P but declines at low and high P. High average maximum daily temperatures (T max ) during the warm season could restrict foraging and other lizard activities thereby reducing reproduction or survival, and hence abundance the following year (Kearney et al, 2009;Sinervo et al, 2010).…”

“…Low T min , for example, could restrict emergence from winter dormancy, foraging, and ovarian processes in ways that reduce body condition, growth, reproduction, or survival, and hence abundance at lag times of %1-1.5 years, especially for winter-active species (Asplund & Lowe, 1964). Alternatively, high T min could reduce the quality of low-temperature thermoregulatory refugia and increase energetic costs of maintenance metabolism during dormancy or nocturnal inactivity in ways that diminish energy reserves for reproduction and hence abundance the following year (Zani, 2008;Zani et al, 2012).…”

“…Despite the relative novelty of these patterns, core aspects of lizard behavior and thermal biology suggest a mechanism we proposed is plausible. Rising T min and T e can increase energetic costs of maintenance metabolism if inactive, nonforaging individuals experience physiologically costly body temperatures (Brischoux, Dupou e, Lourdais, & Angelier, 2016;Clarke & Zani, 2012;Patterson & Davies, 1978;Zani, 2008;Zani et al, 2012). In ectotherms, metabolic activity rises exponentially with temperature and consumes energy important for growth, reproduction, and other processes, thereby requiring additional activity and risk to acquire lost energy (Adolph & Porter, 1993;Bennett & Dawson, 1976;Huey & Slatkin, 1976).…”

Comparative physiological, biochemical, and molecular thermal stress response profiles for two Unionid freshwater mussel species

“…This build up of glycogen could represent a decline in metabolism, as glycogen is not being broken down via glycolysis. This glycogen could then be allocated toward maintaining reproductive function over growth or performance (Guderley, 2004;Zani et al, 2012). This is a clear advantage as these two species of unionid freshwater mussel are long-term brooders of developing glochidia from autumn to spring, and long-term environmental stress such as temperature and oxygen limitations could lead to premature evacuation of glochidia (Aldridge and McIvor, 2003).…”