Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum.

Subterranean rodents inhabit closed tunnel systems that are hypoxic and hypercapnic and buffer aboveground ambient temperature. In contrast to other strictly subterranean rodents, Ctenomys talarum exhibits activity on the surface during foraging and dispersion and hence, is exposed also to the aboveground environment. In this context, this species is a valuable model to explore how the interplay between underground and aboveground use affects the relationship among basal metabolic rate (BMR), cold-induced maximum metabolic rate (MMR), shivering (ST), and non-shivering thermogenesis (NST). In this work, we provide the first evidence of the presence of NST, including the expression of uncoupling proteins in brown adipose tissue (BAT), and shivering thermogenesis in Ctenomys talarum, a species belonging to the most numerous subterranean genus, endemic to South America. Our results show no differences in BMR, cold-induced MMR, and NST between cold- (15 °C) and warm- (25 °C) acclimated individuals. Furthermore, thermal acclimation had no effect on the expression of mitochondrial uncoupling protein 1 (UCP1) in BAT. Only cytochrome c oxidase (COX) content and activity increased during cold acclimation. When interscapular BAT was removed, NST decreased more than 30%, whereas cold-induced MMR remained unchanged. All together, these data suggest that cold-induced MMR reaches a maximum in warm-acclimated individuals and so a probable ceiling in NST and UCP1 expression in BAT. Possible thermogenic mechanisms explaining the increase in the oxidative capacity, mediated by COX in BAT of cold-acclimated individuals and the role of ST in subterranean life habits are proposed.

Cortisol and corticosterone exhibit different seasonal variation and responses to acute stress and captivity in tuco-tucos (Ctenomys talarum).

In this work we aimed to evaluate variations in plasma glucocorticoids (GCs, cortisol and corticosterone) levels throughout an annual cycle in free-living male tuco-tucos (Ctenomys talarum) and compare their responses to acute and chronic stressors (trapping, manipulation, immobilization, confinement in a novel environment, transference to captivity). In addition, we used leukocyte profiles to allow discrimination between basal and stress-induced seasonal changes in GC concentrations. Our results showed that cortisol and corticosterone are differently affected by environmental stimuli in C. talarum. Both hormones showed different patterns of variation in the field and responses to captivity. Moreover, only cortisol was responsive to acute stressors. Leukocyte profiles indicated that animals were unstressed in the field and therefore, that we were able to measure basal, stress-independent, fluctuations in GC levels. GC concentrations were low in comparison to values frequently reported for other mammals. Our results suggest differentiated physiological roles for cortisol and corticosterone in our study species and further emphasize the complexity of GC physiology in wild mammals.

Mounting a specific immune response increases energy expenditure of the subterranean rodent Ctenomys talarum (tuco-tuco): implications for intraspecific and interspecific variation in immunological traits.

It was recently hypothesised that specific induced defences, which require substantial time and resources and are mostly beneficial against repeated infections, are more likely to be favoured in 'slow-living-pace' species. Therefore, understanding how different types of immune defences might vary with life history requires knowledge of the costs and benefits of defence components. Studies that have explored the energetic costs of immunity in vertebrates have done so with a focus primarily on birds and less so on mammals, particularly surface-dwelling rodents. In this study, we evaluated whether an experimental induction of the immune system with a non-pathogenic antigen elevates the energetic expenditure of a subterranean rodent: Ctenomys talarum (tuco-tucos). In both seasons studied, a significant increase in oxygen consumption was verified in immune-challenged tuco-tucos injected with sheep red blood cells (SRBC) compared with control animals. The increase in oxygen consumption 10 days after the exposure to SRBC was lower for female tuco-tucos monitored in the breeding season compared with females in the non-breeding season. Interestingly, antibody titres of female tuco-tucos did not decrease during the breeding season. Our results add new insight into the role of other factors such as basal metabolic rate or degree of parasite exposure besides 'pace of life' in modulating the interspecific immunological variation observed in natural populations of mammals.

Effect of diet quality and soil hardness on metabolic rate in the subterranean rodent Ctenomys talarum.

The present work is aimed to establish, in Ctenomys talarum, the physiological and behavioral adjustments undergone by individuals when they are allowed to dig burrows in soils with different hardness and fed with diets of different quality. For each soil-diet combination, we estimated: resting metabolic rate (RMR), body temperature (T(b)), body mass, digestibility, food consumption rate, transit time, reingestion rate, feces production and time devoted to feeding, resting, locomotor activity and coprophagy. Soil type and diet quality affected RMR, but response to soil hardness was verified later. Animals fed with high quality (HQ) diet showed similar body temperature irrespective of soil condition, while animals fed with low quality (LQ) diet showed lower T(b) under soft soil (SS). Individuals fed with LQ diet showed lower RMR and both, lower digestibility and high transit time of food than those fed with HQ diet. Moreover, increments in feeding and defecation rates were observed in the former group. Number of reingested feces did not differ between animals fed with diets of different quality. However, when incidence of reingestion was considered, animals fed with HQ diet showed higher values of feces ingestion. Either feeding, resting and activity patterns were arrhythmic. However, for animals fed with LQ diet a tendency to rhythmic coprophagy was observed and it could be considered as a way to optimize feeding. This study shows that RMR is limited by digestive efficiency which is influenced by diet quality, but also thermal stress may limit the conversion of assimilated energy into work and heat.

Comparative energetics of the subterranean Ctenomys rodents: breaking patterns.

Subterranean mammals show lower mass-independent basal metabolic rates (BMRs). Several competing hypotheses were suggested to explain how microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal stress and the cost-of-burrowing hypotheses. The thermal stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the high energy expenditure of digging. In this article, we assessed the relationship between BMR of Ctenomys and environmental variables through conventional statistics as well as independent contrasts. Moreover, we tested both the thermal stress and the cost-of-burrowing hypotheses at an interspecific level in a very homogeneous genus of subterranean rodents, the South American genus Ctenomys. We compared species from different geographic localities that have contrasting habitat conditions. We measured BMR through open-flow respirometry. After conventional as well as independent contrast analyses, our results support neither the thermal stress nor the cost-of-burrowing hypotheses. We observed that only body mass affects the variability in BMR. Contrasting climatic and soil conditions, habitat productivity, and net primary productivity were not correlated with BMR variability. We suggested that, because BMR and maximum metabolic rates (MMRs) are correlated, low BMRs among Ctenomys species could also be determined by factors that affect MMR rather than BMR.

Decreased glucose tolerance but normal blood glucose levels in the field in the caviomorph rodent Ctenomys talarum: the role of stress and physical activity.

Hystricomorph rodents have a divergent insulin molecule with only 1-10% of the biological activity in comparison to other mammalian species. In this study, we used the subterranean rodent Ctenomys talarum as a model and performed blood glucose tolerance tests (GTTs) with trained and untrained individuals to evaluate blood glucose regulation and the possible role of physical activity as a compensatory mechanism. Additionally, we evaluated the variations in blood glucose during acute and chronic stress and gathered data in the field to evaluate natural-occurring variations in blood glucose levels. The GTTs showed that C. talarum have a diminished capacity of regulating blood glucose levels in comparison to other mammals and suggest that unexplored differences in the compensatory mechanisms, insulin structure and/or glucose transporters exist within species of hystricomorph rodents. However, blood glucose levels in the field stayed within the normal mammalian range. Physical activity did not prove to be a compensatory mechanism for blood glucose regulation. The individuals did not display important increases in blood glucose after acute stressors and managed to adequately regulate blood glucose during chronic stress. We suggest that the species may not face a selective pressure favoring a more tightly, mammalian like, capacity of regulating blood glucose levels.