Seasonal changes in thermoregulatory responses to hypoxia in the Eastern chipmunk (Tamias striatus)

Abstract

SUMMARYMammalian heterotherms are known to be more tolerant of low oxygen levels than homeotherms. However, heterotherms demonstrate extreme seasonality in daily heterothermy and torpor expression. Because hypoxia depresses body temperature (T b ) and metabolism in mammals, it was of interest to see if seasonal comparisons of normothermic animals of a species capable of hibernation produce changes in their responses to hypoxia that would reflect a seasonal change in hypoxia tolerance. The species studied, the Eastern chipmunk (Tamias striatus, Linnaeus 1758), is known to enter into torpor exclusively in the winter. To test for seasonal differences in the metabolic and thermoregulatory responses to hypoxia (9.9 kPa), flow-through respirometry was used to compare oxygen consumption, minimum thermal conductance and T b under fixed ambient temperature (T a ) conditions whereas a thermal gradient was used to assess selected T a and T b in response to hypoxia, in both summer-and winteracclimated animals. No differences were observed between seasons in resting metabolism or thermal conductance in normoxic, normothermic animals. Providing the animals with a choice of T a in hypoxia attenuated the hypoxic drop in T b in both seasons, suggesting that the reported fall in T b in hypoxia is not fully manifested in the behavioural pathways responsible for thermoregulation in chipmunks. Instead, T b in hypoxia tends to be more variable and dependent on both T a and season. Although T b dropped in hypoxia in both seasons, the decrease was less in the winter with no corresponding decrease in metabolism, indicating that winter chipmunks are more tolerant to hypoxia than summer animals.

Hypoxia reduces the hypothalamic thermogenic threshold and thermosensitivity

“…One consequence of a suppression of neuronal activity is that the hypoxic decline in T b produces a more variable thermoregulatory pattern due to the reduced gain or sensitivity of the CNS T b regulator. Precedence for this is observed in ectothermic studies showing a decreased precision of regulated T b in hypoxia (Cadena & Tattersall, 2009), as well as studies in mammals that demonstrate that the hypoxic decline in T b is more variable and also strongly dependent on ambient temperature (Barros et al 2001; Bishop et al 2001; Levesque & Tattersall, 2009). Indeed, one interesting result from the present study is the remarkable similarity between the changes in α and T th and those observed during different sleep states in rodents.…”

“…Ground squirrels and other hibernating mammals have served as model animals for elucidating underlying thermoregulatory mechanisms common to mammalian T b control (Hammel et al 1973; Heller et al 1974; Florant & Heller, 1977; Larkin & Heller, 1996). Not only do they exhibit a profound reduction in T b and metabolism in hypoxia (Barros et al 2001) and a high degree of hypoxia tolerance (Drew et al 2007; Levesque & Tattersall, 2009), they also possess a very high α (Heller, 1978, 1979), a profound, cold‐activated thermogenesis from brown adipose tissue (Milner et al 1989), and have been shown to progressively lower T th as they enter into hibernation (Heller et al 1977). Thus, ground squirrels are a powerful model for exploring questions concerning the hypoxic response and thermoregulatory control.…”

Atypical behavioural, metabolic and thermoregulatory responses to hypoxia in the naked mole rat (Heterocephalus glaber)

“…This anapyrexic response widens the thermoneutral zone (TNZ) of an animal and induces a downward shift of its thermogenic threshold (Wood, ). Small rodents such as rats, mice, hamsters and chipmunks exhibit behavioural thermoregulation when exposed to acute hypoxia (Gordon & Fogelson, ; Levesque & Tattersall, ), as do a variety of other species, including goldfish, lizards and toads (Wood & Gonzales, ).…”

Molecular and Physiological Factors of Neuroprotection in Hypoxia-tolerant Models: Pharmacological Clues for the Treatment of Stroke

“… 7 Metabolic suppression is a physiological adaptation that is associated with oxygen consumption being actively reduced without causing any harm to the brain and other vital organs when exposed to hypoxic insults. 8 – 10 Metabolic suppression is the altered state of metabolism adaptation that occurs in hibernators 3 and hypoxia-tolerant species, 11 such as the naked mole-rat. 12 Since the metabolic rate is at a declined level in a hypoxia-tolerant mole-rat, the supply of adenosine triphosphate (ATP) through glycolysis and oxidative phosphorylation pathways must match the cellular demand for ATP.…”