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Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation?

The physiological parameters of heterothermy (e.g. minimum body temperature and oxygen consumption, percentage metabolic reduction, and bout length) were measured in two species of Elephantulus elephant shrews (Elephantulus myurus and Elephantulus rozeti; Macroscelidea) as a function of ambient temperature. Both species displayed deep torpor whereby the body temperatures of ca. 5 degrees C and oxygen consumption as low as 2% of basal metabolic rate were attained. Torpor bout length (n = 57 bouts) never exceeded 24 h. These data are characteristic of both hibernation (minimum body temperature and metabolism) and daily torpor (bout length), and argue that these two physiological responses may not necessarily have separate evolutionary origins.

Animals↗

Distribution and partial characterization of the plasma lipoproteins in the hedgehog (Erinaceus europaeus L.), a hibernator with potential use in the study of the hormonal regulation of lipoprotein metabolism.

The hedgehog is a hibernator in which yearly cycles of several endocrine activities and seasonal variations of plasma lipids have already been demonstrated. We have consequently undertaken a study of plasma lipids and lipoproteins in this animal, bled during late April and May. Plasma cholesterol levels (178 +/- 30 mg/100 ml) were comparable with those in normal humans, while triacylglycerol was lower (46 +/- 17 mg/100 ml) and phospholipids higher (252 +/- 35 mg/100 ml). The main characteristics of the plasma lipoprotein spectrum, as determined by sequential and density gradient preparative ultracentrifugation, analytical ultracentrifugation and gel filtration chromatography, were (1) a low concentration of very-low-density components (d less than 1.006 g/ml, about 20 mg/100 ml); (2) a continuity between the low (1.006-1.063 g/ml) and high (1.063-1.21 g/ml) density components, the former (about 150 mg/100 ml) exhibiting a considerable heterogeneity upon polyacrylamide gel electrophoresis while the latter were largely predominating (570 mg/100 ml); (3) the presence, at a density of 1.087 g/ml, of a band migrating electrophoretically like human low-density lipoproteins, a finding consistent with the results of apolipoprotein electrophoresis, which showed the presence of a high-molecular-weight counterpart to apolipoprotein B, in both the low- and high-density ranges defined above; (4) the presence, throughout the entire density spectrum, of an apolipoprotein with molecular weight and mobility in polyacrylamide/urea gels similar to human apolipoprotein A-I, and (5) the presence of very-high-density lipoproteins (d 1.178-1.259 g/ml) responsible for the transport of approximately 15% of plasma cholesterol and 20% of phospholipids.

Animals↗

Fluorescence polarization study of lipids and membranes prepared from brain hemispheres of a hibernating mammal.

The physical behavior of total lipids, microsomes and microsomal lipids prepared from brain hemispheres of European Hamsters (Cricetus cricetus) was approached by the measure of the fluorescence polarization of the probe 1,6-diphenyl 1,3,5-hexatriene. We compare in this study the results obtained for two critical periods for a hibernator: winter (torpid state) and summer (active state). An increase in fluidity was noticed in the winter lipid and membrane preparations. The difference was however of very low magnitude, suggesting that only the microenvironment of some proteins was involved, rather than the bulk membrane fluidity.

Animals↗

Relative 2-deoxyglucose uptake of the paratrigeminal nucleus increases during hibernation.

The paratrigeminal nucleus, a little-studied cell group of the medulla, is the only structure of the brain to significantly increase its relative [14C]2-deoxyglucose accumulation during hibernation in the ground squirrel. The zone of increased activity on the auto-radiographs is continuous between this structure and the marginal zone of the spinal trigeminal nucleus. Because of the known thermoafferent function of the latter structure, a similar function is suggested for the paratrigeminal nucleus.

Animals↗

Vagotomy does not alter circannual body weight cycles in the hibernator Citellus lateralis.

To evaluate a hypothesized role of the vagus in the circannual metabolic cycle of hibernators, measures of annual weight gain, weight loss and cycle period were taken for the ground squirrel, Citellus lateralis, maintained in constant environmental conditions before and after subdiaphragmatic vagotomy. The surgery did not alter the peak weights attained, the lowest weights reached, or the period of the circannual cycle.

Animals↗

The area of 2-[125I] iodomelatonin binding in the pars tuberalis of the ground squirrel is decreased during hibernation.

Quantitative receptor autoradiography was used to analyze 2-[125I]iodomelatonin binding sites in the brains of golden-mantled ground squirrels (Citellus lateralis). Specific binding appeared to be discretely localized to the pars tuberalis region of the pituitary that surrounds the medial basal hypothalamus. The total area of binding was significantly decreased in brains of hibernating squirrels as compared to those of awake, euthermic animals. These findings support a role for melatonin receptors of the pars tuberalis in seasonal behavior.

Animals↗

Functional characteristics and responses to adrenergic stimulation of isolated heart preparations from hypothermic and hibernating subjects.

Contemporary studies of isolated hearts from hibernators and nonhibernators are presented. Original experiments with isolated perfused hamster hearts are reported. Such hearts can maintain left ventricular function at temperatures as low as 7 degrees C. Generated left ventricular pressure was 40 +/- 9 mm Hg and heart rate was 7 +/- 1 beats/min. During cooling heart rate dropped dramatically, coronary flow increased, and ventricular pressure decreased initially, plateaued, and then fell as 7 degrees C was approached. Norepinephrine can cause increased heart rate and left ventricular pressure at 22 and 7 degrees C. This positive inotropic and chronotropic response was associated with increased cAMP at 30 sec after stimulation at 22 degrees C but not at 7 degrees C. Furthermore, cAMP was also not changed at peak response at 7 degrees C. Isoproterenol increased cAMP content in 37 degrees C ventricular slices but not at hypothermic temperatures. Possible mechanisms of nonadenylate cyclase mediation of inotropic and chronotropic responses at 7 degrees C are discussed.

Animals↗

Effects of induced hypothermia on organ blood flow in a hibernator and a nonhibernator.

Regional blood flow and hemodynamic variables during induced hypothermia were compared in six guinea pigs and four hedgehogs. Tracer microspheres were used for blood flow measurements, since this technique is more accurate than the earlier method (86Rb+ distribution) used for cardiac output distribution measurements in hibernators. Heart rate and blood pressure decreased with reduced temperature in a comparable fashion in the two species, while cardiac output was less affected in the hedgehogs than in the guinea pigs. Total peripheral resistance increased in both species. At 34 degrees C the hedgehogs had a higher myocardial blood flow per gram tissue than the guinea pigs and it was not reduced in the hedgehogs when the body temperature was lowered to 22 degrees C, whereas in the guinea pigs it was markedly reduced. The brown adipose tissue of the hedgehogs showed a fourfold increase in blood perfusion at 22 degrees C when compared with 34 degrees C. In the hedgehogs the fractional distribution of cardiac output to the myocardium increased with decreasing body temperature, while the renal fraction decreased. In the guinea pigs, on the other hand, the fractional distribution of cardiac output to the myocardium remained unchanged but increased to the kidneys.

Animals↗

Reversible inhibition of electron transfer in the ubiquinol. Cytochrome c reductase segment of the mitochondrial respiratory chain in hibernating ground squirrels.

Electron transfer through the ubiquinol:cytochrome c1-segment of liver mitochondria isolated from hibernating ground squirrels Citellus undulatus is repressed by 70-80% as compared to mitochondria from the active animals. The inhibition site is likely to be localized between ubiquinone and the cytochrome bc1 complex. Partial release of the inhibition can be observed upon swelling of the isolated mitochondria in a hypoosmotic medium, the effect being prevented by phospholipase A2 inhibitors. Possible role of phospholipase A2 in regulation of ubiquinol oxidation by complex bc1 is discussed.

Animals↗

Thyroid hormone resistance in hibernating ground squirrels, Spermophilus richardsoni. I. Increased binding of triiodo-L-thyronine and L-thyroxine by serum proteins.

Thyroid function was examined during the annual cycle of Richardson's ground squirrel, Spermophilus richardsoni. A number of facets were measured to facilitate comparison of thyroid function in active, dormant, and aroused animals. This report discusses changes in the serum thyroid hormone and binding as assessed by radioimmunoassay, equilibrium dialysis, and competitive binding assays. During the hibernation phase (both dormant and aroused), total serum T3 (trioodo-L-thyronine) and T4 (L-thyroxine) are elevated over active levels, two- to fivefold and four- to sixfold, respectively. However, in dormant squirrels, both free T3 and free T4 are reduced compared with both active and aroused phases of the annual cycle, while in aroused squirrels there is an increase in free T3 but no change in free T4 compared with active squirrels. The difference between changes in total and free thyroid hormone levels in the three groups is due to changes in serum binding of thyroid hormone. There is a more than twofold increase in the capacity of a saturable T3-binding site in serum of both dormant and aroused squirrels, and there is an increase in serum binding affinity at the low core temperature of dormant squirrels (6 degrees). Therefore, even though serum total T3 and T4 are elevated during dormancy, free T3 and T4 levels are reduced to half of the levels in active squirrels as a consequence of increased serum binding capacity and affinity. In aroused animals, however, increased serum binding capacity only partially buffers the increase in total T3 and T4, so that free thyroid hormone levels exceed those of active squirrels.

Animals↗

Variability in brain ganglioside content and composition of endothermic mammals, heterothermic hibernators and ectothermic fishes.

Content and composition of brain gangliosides were compared among endothermic mammals, heterothermic hibernators and ectothermic fishes from habitats with extreme ambient temperatures (tropic vs. antarctic waters). In general the content of brain gangliosides in fishes is significantly lower and exhibits a greater variability than in mammals. The composition of brain gangliosides was investigated using both one- and two-dimensional High Performance Thin Layer Chromatography (HPTLC). Both techniques showed a remarkable increase in the number of individual ganglioside fractions and an additional increase of higher polar fractions in fishes as compared with mammals. The 2D-HPTLC revealed a significant decrease in the relative proportion of alkali-labile gangliosides in the course of evolution from fish to mammals. Moreover this decrease in alkali-lability is correlated with the state of thermal adaptation (antarctic fishes, 53-66%; tropical cichlid fish, 35%). These results provide additional evidence for the notion that the extremely high polarity of brain gangliosides, especially of cold-blooded vertebrates, reflects a very efficient mechanism on the molecular level to keep the neuronal membrane functional under low temperature conditions.

Acclimatization↗

O2 and CO2 concentrations in burrows of euthermic and hibernating golden hamsters.

O2 and CO2 concentrations were measured in burrows of golden hamsters (Mesocricetus auratus, W.) simultaneously with body temperature. In sealed burrows of euthermic golden hamsters daily mean concentrations of 15.1 +/- 1.2% O2 and 5.7 +/- 1.2% CO2 were measured, the extreme values amounting to 10.0% O2 and 10.8% CO2. The gas composition showed a daily rhythm. During hibernation, the gas composition of the burrow changed significantly to 20.0 +/- 0.5% O2 and 1.8 +/- 0.8% CO2.

Air↗

Freeze tolerance and intolerance as strategies of winter survival in terrestrially-hibernating amphibians.

The ability to tolerate extracellular freezing as an adaptation for winter survival was tested in seven species of terrestrially-hibernating amphibians found in eastern Canada. All species had only moderate supercooling abilities, with whole animal supercooling points of -1.5 to -3 degrees C. Two salamander species, Plethodon cinereus and Ambystoma laterale, and the toad, Bufo americanus, were freezing intolerant and were killed when frozen for 24 hr at temperatures just below their supercooling points. The major winter strategy of these animals appears to behavioural avoidance of subzero temperatures. Four species of frogs Rana sylvatica, Hyla versicolor, Hyla crucifer and Pseudacris triseriata, survived extracellular freezing at moderate subzero temperatures (-2 to -4 degrees C) for periods of time ranging up to 2 weeks. All four frog species accumulated low molecular weight carbohydrates as cryoprotectants, glycerol being the major cryoprotectant in adult H. versicolor, while immature adults of this species as well as the other three species all produced high levels of glucose as the cryoprotectant.

Acclimatization↗

Increased GDP binding and thermogenic activity in brown adipose tissue mitochondria during arousal of the hibernating garden dormouse (Eliomys quercinus L.).

1. The thermogenic activity of brown adipose tissue in hibernating garden dormice during hypothermic torpor and at different states of arousal were studied. High levels of GDP binding were observed on isolated brown fat mitochondria, indicating that the thermogenic proton conductance pathway is very active in brown fat during arousal. 2. In order to investigate this phenomenon, the uncoupling protein was assessed by immunological assay and the mRNA for UCP was analysed. 3. Animals during arousal exhibited neither increase in UCPmRNA nor an increase in UCP. 4. Our results suggest that during the rewarming of garden dormice there is an acute unmasking of GDP binding sites on the protein.

Adipose Tissue, Brown↗

Concentrations of lactate and pyruvate and temperature effects on lactate dehydrogenase activity in the tissues of the big brown bat (Eptesicus fuscus) during arousal from hibernation.

1. The rectal temperatures, steady state concentrations of lactate and pyruvate, and the LDH isoenzyme composition in the heart, liver, and pectoral muscle of hibernating and arousing Eptesicus fuscus were measured. 2. Bat rectal temperature increased from 8.86 to 33.1 degrees C during arousal. 3. During arousal, steady state concentrations of pyruvate and lactate increased significantly in the tissues, however they remained generally below the level necessary to saturate LDH at the respective temperature. 4. The activities of the two LDH isoenzymes, M4, the predominant form in bat liver, and H4, the main form in bat heart and pectoral muscle, show substrate-dependent temperature effects described by the equation, mu = (E beta S + E alpha K t)/(K t + S). 5. Temperature effects (mu) on bat LDH activity increased during arousal but remained significantly lower than mu determined at saturating concentrations of substrate (E beta). 6. The parameters E beta-E alpha, E alpha and K tau are particularly important in describing the temperature dependence of LDH activity in tissues of the arousing bat.

Animals↗

A reinvestigation of hemoglobin alterations in ground squirrels while in various hibernation activity states.

Characterization of the hemoglobins of winter-hibernating, winter-active and summer-active Arctic ground squirrels (Citellus undulatus) by citrate agar electrophoresis and isoelectric focusing (IEF), pH 5.5-8.5, showed no differences in hemoglobin electrophoretic patterns. Previous studies showing alterations in hemoglobins were most likely the result of artifacts due to the use of whole blood. The Arctic ground squirrel's hemoglobin amino terminal sequence was determined for each activity state and was identical in all cases.

Amino Acid Sequence↗

Regulation of the skeletal muscle metabolism during hibernation of Jaculus orientalis.

1. The glycolytic flow in the skeletal muscle was considerably depressed during hibernation of Jaculus orientalis. 2. Although the ATP content was not modified, the ATP/AMP ratio was twice as large than under homeothermic conditions. 3. Furthermore, the hexose phosphates were markedly depressed. 4. The total activities of the key enzymes, hexokinase, phosphofructokinase and pyruvate kinase, which are regulated through the adenylates, decreased. 5. Under in vivo conditions, taking into account the small amount of fructose-6-phosphate and the ATP/AMP ratio, it is likely that phosphofructokinase was totally inhibited, explaining the undetectable amount of fructose 1.6 bisphosphate.

Adenosine Monophosphate↗

Content of DSIP, enkephalins and ACTH in some tissues of active and hibernating ground squirrels (Citellus suslicus).

Seasonal changes in the amount of DSIP-like material have been measured in extracts from the brain of Citellus suslicus. 2. Analysis of extracts from the brain of deeply sleeping ground squirrels shows that the level of enkephalin-like material reliably increases while that of ACTH-like material decreases. 3. It is concluded that the opiate brain activation system is among the factors participating in the induction of hibernation in ground squirrels.

Adrenocorticotropic Hormone↗