Transient peripheral warming accompanies the hypoxic metabolic response in the golden-mantled ground squirrel

Heterothermic mammals tolerate severe hypoxia, as well as a variety of central nervous system insults, better than homeothermic mammals. Tolerance to hypoxia may stem from adaptations associated with the ability to survive hibernation and periodic arousal thermogenesis. Here, we review evidence and mechanisms of hypoxia tolerance during hibernation, euthermy and arousal in heterothermic mammals and consider potential mechanisms for regenerative-like processes, such as synaptogenesis, observed within hours of hypoxic stress associated with arousal thermogenesis. 3156hypothermia and metabolic suppression in ground squirrels as it does in hypoxia-tolerant turtles and fish (Bullard et al., 1960). Additional adaptations in heterothermic mammals may synergize with hypothermia and metabolic suppression to attenuate the cytotoxic cascade. Because many of these protective mechanisms such as hypothermia, metabolic suppression, immunosuppression/leukocytopenia and increased antioxidant defenses differ between hibernating (torpid) and euthermic animals, we will discuss hypoxia tolerance in hibernating animals separately from hypoxia tolerance in euthermic animals (Fig.·1; reviewed in Drew et al., 2001).Hypoxia tolerance in the hibernating state: evidence and mechanisms Reports dating back to the early 1800s describe hypoxia tolerance in the hibernating state in bats, marmots and ground squirrels and show that tolerance displayed during hibernation exceeds tolerance observed during euthermy (Spallanzani et al., 1803; Carlisle, 1805; cited in Biörck et al., 1956; reviewed in Bullard et al., 1960). Biörck et al. (1956) confirmed these initial observations and reported that hibernating hedgehogs (Erinaceus europaeus) survive 50-120·min of 100% N2, in most cases without apparent damage.Interestingly, many hibernating species in steady-state torpor are not hypoxic despite 10-fold or greater decreases in respiratory rates. During torpor, Arctic ground squirrels (Spermophilus parryii), as well as other species of ground squirrel, are well oxygenated with normal to above normal arterial oxygen pressures (Frerichs et al., 1994; Y. L. Ma, X. Zhu, P. M. Rivera, O. Toien, B. M. Barnes, J. C. LaManna, M. A. Smith and K. L. Drew, manuscript submitted for publication). By contrast, other heterothermic species, such as golden-mantled ground squirrels (Spermophilus lateralis) and hedgehogs (E. europaeus), may become hypoxic during torpor owing to long periods of apnea. These species often breathe intermittently during hibernation, waiting up to 30·min or longer between breaths. In hedgehogs, arterial oxygen partial pressure (PaO∑), sampled from chronic aorta cannula, is higher in torpor than in the active state (120 vs 105·mmHg; 160 vs 14.0·kPa) but K. L. Drew and others Release of neurotransmitters, including the excitotoxin glutamate, and activation of NMDA and AMPA receptors contribute to the flood of Ca 2+ from extra-and intracellular stores, which leads to calcium overload (4). Activated microglia release inflammatory cytokines and ni...

Section: Mechanisms Of Metabolic Suppressionmentioning

confidence: 99%

Hypoxia tolerance in mammalian heterotherms

Drew

Harris

LaManna

et al. 2004

“…Despite its known importance for thermoregulation in general, the role and control of peripheral heat loss from thermal windows during hypoxic T b depression has received very little attention (cf. Tattersall and Milsom, 2003).…”

Section: Introductionmentioning

confidence: 99%

Body temperature depression and peripheral heat loss accompany the metabolic and ventilatory responses to hypoxia in low and high altitude birds

Scott

Cadena

Tattersall

et al. 2008

Self Cite

SUMMARYThe objectives of this study were to compare the thermoregulatory, metabolic and ventilatory responses to hypoxia of the high altitude bar-headed goose with low altitude waterfowl. All birds were found to reduce body temperature (T b ) during hypoxia, by up to 1-1.5°C in severe hypoxia. During prolonged hypoxia, T b stabilized at a new lower temperature. A regulated increase in heat loss contributed to T b depression as reflected by increases in bill surface temperatures (up to 5°C) during hypoxia. Bill warming required peripheral chemoreceptor inputs, since vagotomy abolished this response to hypoxia. T b depression could still occur without bill warming, however, because vagotomized birds reduced T b as much as intact birds. Compared to both greylag geese and pekin ducks, bar-headed geese required more severe hypoxia to initiate T b depression and heat loss from the bill. However, when T b depression or bill warming were expressed relative to arterial O 2 concentration (rather than inspired O 2 ) all species were similar; this suggests that enhanced O 2 loading, rather than differences in thermoregulatory control centres, reduces T b depression during hypoxia in bar-headed geese. Correspondingly, bar-headed geese maintained higher rates of metabolism during severe hypoxia (7% inspired O 2 ), but this was only partly due to differences in T b . Time domains of the hypoxic ventilatory response also appeared to differ between bar-headed geese and low altitude species. Overall, our results suggest that birds can adjust peripheral heat dissipation to facilitate T b depression during hypoxia, and that bar-headed geese minimize T b and metabolic depression as a result of evolutionary adaptations that enhance O 2 transport.

“…In numerous taxa, hypoxic exposure augments external heat exchange (Tattersall and Milsom, 2003), lowers thermal preference (Dupré and Wood, 1988;Dupré and Owen, 1992;Tattersall and Boutilier, 1997;Wiggins and Frappell, 2002;Cadena and Tattersall, 2009), reduces metabolic rate (Barros et al, 2001), and inhibits shivering (Barros et al, 2001) and non-shivering heat production (Madden and Morrison, 2005). The prevailing hypothesis is that low environmental oxygen reduces thermoregulatory thresholds for the activation of thermoeffector responses (Steiner and Branco, 2002;Bicego et al, 2007;Tattersall and Milsom, 2009).…”

Section: Introductionmentioning

confidence: 99%

Fluctuations in oxygen influence facultative endothermy in bumblebees

Dzialowski

Tattersall

Nicol

et al. 2014

Self Cite

Bumblebees are facultative endotherms, having the ability to elevate thorax temperature above ambient temperature by elevating metabolism. Here, we investigated the influence of hypoxia on metabolic demands and thermoregulatory capabilities of the bumblebee Bombus terrestris. We measured thorax temperature, rates of oxygen consumption and carbon dioxide production, and abdominal pumping rates of bees randomly exposed to oxygen levels of 20, 15, 10 and 5 kPa at 26°C. Under normoxia, bumblebees maintained an elevated mean thorax temperature of 35.5°C. There was no significant change in thorax temperature at 15 kPa O 2 (33.4°C). Mean thorax temperature decreased significantly at 10 kPa O 2 (31.6°C) and 5 kPa O 2 (27.3°C). Bees were able to maintain an elevated metabolic rate at 15 and 10 kPa O 2 . In normoxia, endothermic bees exhibited periods of rapid abdominal pumping (327 min −1 ) interspaced by periods of no abdominal pumping. At 10 kPa O 2 , abdominal pumping rate decreased (255 min −1 ) but became more continuous. Upon exposure to 5 kPa, metabolic rate and abdominal pumping rate (152 min −1 ) decreased, although the animals continued abdominal pumping at the reduced rate throughout the exposure period. Bumblebees are able to meet the energetic demands of endothermy at 15 kPa O 2 , but become compromised at levels of 10 kPa O 2 and below.