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Torpor and Hibernation in Mammals: Metabolic, Physiological, and Biochemical Adaptations

Lawrence C. H. Wang, T. F. Lee

10.1002/cphy.cp040122

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Basic Patterns of Torpor and Hibernation
2 Physiological Manifestations in a Bout of Torpor
2.1 Entry into Torpor
2.2 The Torpor State
2.3 Arousal from Torpor
3 Energetics of Natural Hibernation
3.1 Energetics of Mammals Exhibiting Hibernation and Torpor
3.2 Current Theories on Why Animals Arouse Periodically
4 Physiological and Biochemical Adaptations: Organ Systems, Organs, and Tissues
4.1 Regulation of Heat Production in a Torpor Cycle
4.2 Cardiovascular Functions
4.3 Respiratory Functions
4.4 Reproductive Functions
4.5 Photoperiodism and Rhythmicity
5 Biochemical and Cellular Adaptations
5.1 Substrate Utilization in Hibernation
5.2 Ionic Regulation
5.3 Membrane Aspects
6 The “Hibernation Induction Trigger”: Fact or Fiction?
6.1 Historical Background and Recent Advances
6.2 An Evaluation
6.3 The Opioids
7 Summary and Perspective
Figure 1. Figure 1.

Upper panels: Typical dynamic changes of body temperature (via radiotelemetry) during torpor bout in the Richardson's ground squirrel under field (#33) and laboratory (#205) conditions. Note the relatively long duration of entry into torpor (more than 24 h) and the relatively short duration of arousal from torpor (less than 5 h). Lower panel: A complete hibernation season in a juvenile male Richardson's ground squirrel under field conditions. Note seasonal variations in duration and depth of torpor 140.
Figure 2. Figure 2.

(A) Maximal first postrest contraction (F1max) of electrically stimulated papillary muscle from active (open circle) and hibernating (closed circle) Richardson's ground squirrels in 0.1, 2.8, and 5 mM Ca2+ solutions at 37°, 20°, and 7°C. Note that the amplitude of F1max is always higher in the hibernating group at all tested temperatures 155. (B) Ca2+ dependence of ryanodine binding to Richardson's ground squirrel (closed square) and sheep (open square) cardiac SR. Note the rapid increase in ryanodine binding to ground squirrel cardiac SR after a tenfold increase in Ca2+ concentration from 10−7 to 10−6 M 102.
Figure 3. Figure 3.

(A) Time course of arterial acid‐base variables in two European hamsters (animal A: solid line and closed symbols; animal B: dotted line and open symbols) arousing from hibernation. Samples were taken every 15 min. Dashed line indicates buffer value of extracellular fluid. H: hibernation, N: normothermy. Note marked reduction of PCO2* from 100 to less than 50 torr within the first 15 min by hyperventilation 99. (B) Changes in shoulder muscle pH (solid circles) and imidazole dissociation ratio (αIm, solid triangles) with shoulder temperature (Tsh) of Columbian ground squirrels during arousal from hibernation. E denotes data from euthermic animals. Note the rapid increase in αIm during early arousal (at Tsh below 20°C), whereas the change in pH occurs only at Tsh above 20°C 90.
Figure 4. Figure 4.

Left: Arrhenius plots of H+ efflux, Ca2+ uptake, and O2 consumption in liver mitochondria from summer‐active Richardson's ground squirrels. Apparent energy of activation (Ea; in kcal/mol) was calculated only for upper linear portion of each plot. Right: Same parameters as those from the left panel, but the squirrels were sacrificed during hibernation. The Ea was calculated over entire temperature range examined (4°–37°C). Note the stoichiometric relationship between H/Ca and Ca/O remains constant at all temperatures despite the drastic increase in Ea in the summer‐active ground squirrel 120.
Figure 5. Figure 5.

Left: Representative conventional differential scanning calorimetry thermogram of (a) endothermic (heating) phase transition and (b) exothermic (cooling) phase transition in liver inner mitochondrial membranes from summer and from hibernating Richardson's ground squirrel. Scan rates were 10°C/min at a sensitivity of 0.2 mcal/s full scale. Right: Representative high‐sensitivity differential scanning calorimetry thermograms of freshly isolated inner mitochondrial membranes from summer and from hibernating Richardson's ground squirrels. Membranes were scanned from O° to 70°C at a scan rate of 20°C/h (a), cooled, and scanned again (b). Note, in both panels, no evidence of lipid phase transitions near 20°C even at highest possible instrumental sensitivity 118.
Figure 6. Figure 6.

Changes in met‐enkephalin immunoreactive elements in the septal area of (a) euthermic (Tb = 37°C), hypothermic (Tb = 7°C), and hibernating (Tb = 7°C) Columbian ground squirrels. NSL: lateral septal nucleus; NSM: medial septal nucleus; dashed line: border between lateral and medial septal nuclei. Note the significantly greater immunoreactivity during hibernation (45% greater than euthermia, p < 0.01 based on computerized image analysis) than in hypothermia and euthermia (no significant difference between the two), indicating the increased met‐enkephalin immunoreactivity during hibernation is state‐dependent rather than Tb‐dependent 113.


Figure 1.

Upper panels: Typical dynamic changes of body temperature (via radiotelemetry) during torpor bout in the Richardson's ground squirrel under field (#33) and laboratory (#205) conditions. Note the relatively long duration of entry into torpor (more than 24 h) and the relatively short duration of arousal from torpor (less than 5 h). Lower panel: A complete hibernation season in a juvenile male Richardson's ground squirrel under field conditions. Note seasonal variations in duration and depth of torpor 140.



Figure 2.

(A) Maximal first postrest contraction (F1max) of electrically stimulated papillary muscle from active (open circle) and hibernating (closed circle) Richardson's ground squirrels in 0.1, 2.8, and 5 mM Ca2+ solutions at 37°, 20°, and 7°C. Note that the amplitude of F1max is always higher in the hibernating group at all tested temperatures 155. (B) Ca2+ dependence of ryanodine binding to Richardson's ground squirrel (closed square) and sheep (open square) cardiac SR. Note the rapid increase in ryanodine binding to ground squirrel cardiac SR after a tenfold increase in Ca2+ concentration from 10−7 to 10−6 M 102.



Figure 3.

(A) Time course of arterial acid‐base variables in two European hamsters (animal A: solid line and closed symbols; animal B: dotted line and open symbols) arousing from hibernation. Samples were taken every 15 min. Dashed line indicates buffer value of extracellular fluid. H: hibernation, N: normothermy. Note marked reduction of PCO2* from 100 to less than 50 torr within the first 15 min by hyperventilation 99. (B) Changes in shoulder muscle pH (solid circles) and imidazole dissociation ratio (αIm, solid triangles) with shoulder temperature (Tsh) of Columbian ground squirrels during arousal from hibernation. E denotes data from euthermic animals. Note the rapid increase in αIm during early arousal (at Tsh below 20°C), whereas the change in pH occurs only at Tsh above 20°C 90.



Figure 4.

Left: Arrhenius plots of H+ efflux, Ca2+ uptake, and O2 consumption in liver mitochondria from summer‐active Richardson's ground squirrels. Apparent energy of activation (Ea; in kcal/mol) was calculated only for upper linear portion of each plot. Right: Same parameters as those from the left panel, but the squirrels were sacrificed during hibernation. The Ea was calculated over entire temperature range examined (4°–37°C). Note the stoichiometric relationship between H/Ca and Ca/O remains constant at all temperatures despite the drastic increase in Ea in the summer‐active ground squirrel 120.



Figure 5.

Left: Representative conventional differential scanning calorimetry thermogram of (a) endothermic (heating) phase transition and (b) exothermic (cooling) phase transition in liver inner mitochondrial membranes from summer and from hibernating Richardson's ground squirrel. Scan rates were 10°C/min at a sensitivity of 0.2 mcal/s full scale. Right: Representative high‐sensitivity differential scanning calorimetry thermograms of freshly isolated inner mitochondrial membranes from summer and from hibernating Richardson's ground squirrels. Membranes were scanned from O° to 70°C at a scan rate of 20°C/h (a), cooled, and scanned again (b). Note, in both panels, no evidence of lipid phase transitions near 20°C even at highest possible instrumental sensitivity 118.



Figure 6.

Changes in met‐enkephalin immunoreactive elements in the septal area of (a) euthermic (Tb = 37°C), hypothermic (Tb = 7°C), and hibernating (Tb = 7°C) Columbian ground squirrels. NSL: lateral septal nucleus; NSM: medial septal nucleus; dashed line: border between lateral and medial septal nuclei. Note the significantly greater immunoreactivity during hibernation (45% greater than euthermia, p < 0.01 based on computerized image analysis) than in hypothermia and euthermia (no significant difference between the two), indicating the increased met‐enkephalin immunoreactivity during hibernation is state‐dependent rather than Tb‐dependent 113.

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Article Title: Torpor and Hibernation in Mammals: Metabolic, Physiological, and Biochemical Adaptations
 

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Lawrence C. H. Wang, T. F. Lee. Torpor and Hibernation in Mammals: Metabolic, Physiological, and Biochemical Adaptations. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 507-532. First published in print 1996. doi: 10.1002/cphy.cp040122