Cold-induced Oxygen Consumption Research Articles

Age-Related Changes in the Thermoregulatory Properties in Bank Voles From a Selection Experiment.

As with many physiological performance traits, the capacity of endotherms to thermoregulate declines with age. Aging compromises both the capacity to conserve or dissipate heat and the thermogenesis, which is fueled by aerobic metabolism. The rate of metabolism, however, not only determines thermogenic capacity but can also affect the process of aging. Therefore, we hypothesized that selection for an increased aerobic exercise metabolism, which has presumably been a crucial factor in the evolution of endothermic physiology in the mammalian and avian lineages, affects not only the thermoregulatory traits but also the age-related changes of these traits. Here, we test this hypothesis on bank voles (Myodes glareolus) from an experimental evolution model system: four lines selected for high swim-induced aerobic metabolism (A lines), which have also increased the basal, average daily, and maximum cold-induced metabolic rates, and four unselected control (C) lines. We measured the resting metabolic rate (RMR), evaporative water loss (EWL), and body temperature in 72 young adult (4 months) and 65 old (22 months) voles at seven ambient temperatures (13–32°C). The RMR was 6% higher in the A than in the C lines, but, regardless of the selection group or temperature, it did not change with age. However, EWL was 12% higher in the old voles. An increased EWL/RMR ratio implies either a compromised efficiency of oxygen extraction in the lungs or increased skin permeability. This effect was more profound in the A lines, which may indicate their increased vulnerability to aging. Body temperature did not differ between the selection and age groups below 32°C, but at 32°C it was markedly higher in the old A-line voles than in those from other groups. As expected, the thermogenic capacity, measured as the maximum cold-induced oxygen consumption, was decreased by about 13% in the old voles from both selection groups, but the performance of old A-line voles was the same as that of the young C-line ones. Thus, the selection for high aerobic exercise metabolism attenuated the adverse effects of aging on cold tolerance, but this advantage has been traded off by a compromised coping with hot conditions by aged voles.

Fuel Use in Mammals: Conserved Patterns and Evolved Strategies for Aerobic Locomotion and Thermogenesis.

Effective aerobic locomotion depends on adequate delivery of oxygen and an appropriate allocation of metabolic substrates. The use of metabolic substrates during exercise follows a predictive pattern of lipid and carbohydrate oxidation that is similar in lowland native cursorial mammals. We have found that in two highland lineages of mice (Phyllotis and Peromyscus) the fuel use pattern is shifted to a greater reliance on carbohydrates compared to their lowland conspecifics and congenerics. However, there is variation between lineages in the importance of phenotypic plasticity in the expression of this metabolic phenotype. Moreover, this metabolic phenotype is independent of running aerobic capacity and can also be independent of thermogenic capacity. For example, wild-caught mice from a highland population of deer mice (Peromyscus maniculatus) housed in warm normoxic laboratory conditions maintain higher maximum cold-induced oxygen consumption in acute hypoxia than lowland congenerics, but shivering and non-shivering thermogenesis is supported by high rates of lipid oxidation. This is reflected in the consistently higher activities of oxidative and fatty acid oxidation enzymes in the gastrocnemius of highland deer mice compared to lowlanders, which are resistant to hypoxia acclimation. While a fixed trait in muscle aerobic capacity may reflect the pervasive and unremitting low PO2 at high altitudes, muscle capacities for substrate oxidation may be more flexible to match appropriate substrate use with changing energetic demands. How shivering thermogenesis and locomotion potentially interact in the matching of muscle metabolic capacities to appropriate substrate use is unclear. Perhaps it is possible that shivering serves as "training" to ensure muscles have the capacity to support locomotion or visa-versa.

Effects of parasites and antigenic challenge on metabolic rates and thermoregulation in northern red-backed voles (Myodes rutilus).

Perturbations in host energetics are considered to be an essential pathway for parasite impact on host fitness. However, direct estimations of parasite-induced variations in basal metabolic rates of vertebrate hosts have so far provided contradictory results. The energy requirements of immunity and other vital functions may be compromised in energy-demanding conditions in comparison to comfortable conditions; therefore, in our study performed on the wild red-backed vole, Myodes rutilus, we compared the values of indices that reflect metabolic and thermoregulatory responses to acute cooling in individuals that had been naturally infected by gut helminths or Ixodes persulcatus taiga ticks to individuals with no signs of infestation. To consider the possible effects of an acquired immune response on host energetics, we also injected some of the tested individuals with sheep red blood cells (SRBC). Red-backed voles infected by the nematode Heligmosomum mixtum injected with SRBC showed significantly lower cold-induced maximum oxygen consumption than the saline control. Additionally, individuals infected with H. mixtum showed significantly lower oxygen consumption during the final minute of the 15-min acute cooling period and a significantly greater decline in body temperature than individuals free from helminths. In individuals concurrently infected by H. mixtum and the cestodes Arostrilepis horrida, these indices did not differ from helminth-free individuals. The number of ticks simultaneously parasitizing the voles at the moment of capture correlated positively with their SMR. Our results suggest that even natural parasites produce deleterious effects on host aerobic capacity and thermoregulatory abilities, although the effects of different parasites might not be additive.

GENETIC CORRELATIONS BETWEEN BASAL AND MAXIMUM METABOLIC RATES IN A WILD RODENT: CONSEQUENCES FOR EVOLUTION OF ENDOTHERMY

According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim- and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (= maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.

GENETIC CORRELATIONS BETWEEN BASAL AND MAXIMUM METABOLIC RATES IN A WILD RODENT: CONSEQUENCES FOR EVOLUTION OF ENDOTHERMY

According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim- and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (= maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.

Effect of tropisetron versus placebo on cold-induced oxygen consumption and shivering in male volunteers

In a prospective, randomized, cross-over, placebo-controlled study in healthy male volunteers, we tested the effect of the 5-HT 3 antagonist tropisetron on cold-induced oxygen consumption and shivering. Cooling was performed by intravenous infusion of isotonic salt solution at 4 °C. Whole-body oxygen consumption (VO 2) was measured with a metabolic monitor. Shivering was qualitatively assessed. When the shivering score evaluated “2” (intense shivering), 5 mg tropisetron or NaCl 0.9% was injected and repeated if necessary, to completely stop shivering. The VO 2 before shivering (178±9 ml/min/m 2) rose significantly during shivering (291±21 ml/min/m 2). 5 mg of tropisetron in 2 volunteers and 10 mg in 3 volunteers stopped shivering but it returned (grade 0–1). The VO 2 decreased significantly (209±17 ml/min/m 2). Placebo had no effect. Tropisetron reduced cold-induced VO 2 and intensity of hypothermic shivering. That an additional dose of tropisetron could not stop the shivering totally may indicate that the effect of tropisetron is not dose dependent.

Seasonal Effects on Metabolism and Thermoregulation in Northern Bobwhite

Seasonal differences in metabolism and cold hardiness are common among small passerine birds. However, seasonal adjustments of metabolism and insulation are less well studied in nonpasserines and in larger birds. We measured basal metabolic rate (BMR), metabolic response to temperature, and maximal capacity for thermogenesis (peak cold-induced oxygen consumption, VO 2sum ) in late spring/summer and winter in outdoor captive Northern Bobwhite (Colinus virginianus) near the northern boundary of their natural range, to determine whether seasonal adjustments in metabolism are a component of acclimatization in this species. Mass, BMR and regression equations describing diurnal and nocturnal metabolic response to temperature were not significantly different between seasons. After metabolic tests below thermoneutrality, cloacal temperature (T b ) was not dependent on ambient temperature (T a ) at either season, and nocturnal T b did not differ significantly between seasons. However, after metabolic tests below thermoneutrality, diurnal T b was significantly greater in summer (38.9 ± 1.1°C) than in winter (37.7 ± 1.1°C). Although body mass of winter birds was significantly greater than their body mass in late spring, maximal thermogenic capacity did not differ significantly on a seasonal basis, and winter bobwhite were only marginally more cold tolerant than late spring birds under severe cold stress. For individual birds tested in both winter and late spring, individual ranking of VO 2sum was not consistent between seasons (i.e., birds with a high VO 2sum in winter did not necessarily have a high VO 2sum in late spring). These data suggest little seasonal adjustment of metabolism or insulation in the Northern Bobwhite, a relatively large nonpasserine species native mainly to regions with relatively mild winter climates.

Sliding vs static cold exposure and the measurement of summit metabolism in birds

1. 1. Maximum cold-induced oxygen consumption (summit metabolism, V̇O 2sum) of endothermic animals is elicited in helium-oxygen atmospheres either by exposing individual animals to a decreasing series of temperatures until oxygen consumption plateaus (Sliding Cold Exposure), or by exposing groups of animals to a single temperature within a range of temperatures (Static Cold Exposure), the lower portion of the range producing hypothermia in most, or all, individuals. It is not known whether these two methods produce similar values for V̇O 2sum. 2. 2. We measured V̇O 2sum by both sliding and static cold exposure methods in summer acclimatized Warbling Vireos ( Vireo gilvus) and Gray Catbirds ( Dumetella carolinensis). 3. 3. Mean (±SD) values for V̇O 2sum generated by the two cold exposure methods were 4.39 ± 0.05 ml O 2·min −1 (n = 15, Static) and 4.37 ± 0.61 ml O 2·min −1 (n = 6, Sliding) for vireos, and 7.57 ± 0.84 ml O 2·min −1 (n = 13, Static) and 7.17 ± 0.85 ml O 2·min −1 (n = 6, Sliding) for catbirds. These values did not differ significantly for either species. 4. 4. We conclude that both methods for measurement of V̇O 2sum produce similar results, and that both are appropriate measures of summit metabolism in birds.

Cold-induced metabolism and brown fat GDP binding in young and old rats

The attenuated thermogenic responses observed in older animals exposed to low environmental temperatures may reflect decreased thermogenic capacity of brown adipose tissue, a major nonshivering thermogenic effector in rats, and/or decreased metabolic capacity of lean body mass. to evaluate these possibilities, the oxygen consumption of female Sprague-Dawley rats aged 5 and 26 months was recorded at rest and during 6 h of exposure to 6°C. The thermogenic capacity of brown fat was estimated from the binding of guanosine-5′-diphosphate (GDP) to isolated brown fat mitochondria. Both resting and cold-induced oxygen consumption expressed on a mass independent basis [ml/(min x kg body mass ·67)] and as a function of lean body mass [ml/(min x g lean body mass)] were significantly lower in the 26-month-old animals. Colonic temperatures of younger and older rats after the 6 h of cold exposure were 37.5 ± 0.1 and 36.1 ± 0.2°C, respectively, and were significantly different. However, no significant differences in the binding of GDP to isolated brown fat mitochondria were observed. These data indicate that the thermogenic capacity of brown fat is not decreased in the aged rat, and that the metabolic capacity as well as the amount of lean body mass is altered with age.

Maximum Cold-Induced Oxygen Consumption in the House Sparrow Passer domesticus L.

The maximum cold-induced oxygen consumption (V̇o2max) was studied in house sparrows in summer. To induce V̇o2max a helium-oxygen atmosphere was used. Measurements were conducted in an atmosphere with normal (21%) or increased (33%) O₂ concentration. The mean ± SD values of V̇o2max in both conditions were almost the same (15.69 ± 1.01 and 15.79 ± 1.03 cm³ O₂ g⁻¹·h⁻¹, respectively). The results indicate that the diffusing capacity of lungs is not the limiting factor for aerobic metabolism of resting birds during cold stress. Females tend to achieve higher values of V̇o2max than do males (16.20 and 15.36 cm³ O₂ g⁻¹h⁻¹, respectively; P < .05).

Development of homeothermy in the diving petrels Pelecanoides urinatrix exsul and P. georgicus, and the Antarctic prion Pachyptila desolata

1. 1. Body temperatures of South Georgia diving petrel ( P. georgiens) chicks increased from about 37.5°C at hatching to between 38.5 and 39°C within two weeks. Temperatures of common diving petrel P. u. exsul chicks averaged 38.8°C after two weeks of age. Burrow temperatures varied between 5 and 10°C. 2. 2. Measurements of oxygen consumption and body temperature indicated that chicks achieve effective endothermy at 5°C after 9 days in P. u. exsul, 5–6 days in P. georgicus, and 0 days in the Antarctic prion ( Pachyptila desolata). 3. 3. The maximum mass-specific, cold-induced oxygen consumption of small chicks that we could measure with our apparatus (ca. 5–6 cc O 2/g per hr) was achieved at 5–6 days in P. u. exsul. 3 days in P. georgicus, and 0 days in P. desolata. 4. 4. Mass-specific thermal conductance decreased with age and body size in all 3 species, but was highest in P. u. exsul and lowest in P. desolata. Conductance was similar at the age of effective endothermy in all 3 species (ca. 3 J/g per hr per °C). 5. 5. The period required for the development of endothermy is related to age-specific changes in both conductance and capacity for heat production and it closely parallels the length of the brooding period. 6. 6. It is suggested that the length of the period of thermal dependence of the chick is related to the distance between feeding areas and the nesting site.

Thermal and metabolic responses of temperature-acclimated rats during cold and heat exposures.

Some endocrine and metabolic responses to acute cold and heat exposures were observed in rats acclimated to cold, heat, or both cold and heat. Rats exposed to both cold (12 hr, 5 degrees C) and heat (12 hr, 34 degrees C) for 4 to 5 weeks (CHA) showed less fall of colonic temperature (Tc) in the cold (-5 degrees C) than heat-acclimated rats (34 degrees C, 4 to 5 weeks) (HA) and warm controls (WC), but a greater fall than cold-acclimated rats (5 degrees C, 4 to 5 weeks) (CA). CHA possessed a larger quantity of interscapular brown adipose tissue and showed greater cold-induced oxygen consumption (VO2) than WC and HA but less than CA. Blood glycerol levels rose similarly in all groups in the cold, while the increase in blood free fatty acids (FFA) levels was significantly greater in HA and smaller in CA than in WC and CHA. Acute cold exposure caused the elevation of plasma glucagon level in WC and HA, but not in CA and CHA. It lowered plasma insulin levels in HA, and the insulin/glucagon molar ratio (I/G) in WC, HA, and CHA. All groups showed the same increases in Tc during acute heat exposure (34 degrees C). However, the heat-induced increase in VO2 was greater in WC than in HA, CA, and CHA. Blood metabolite levels were not affected by acute heat exposure in all groups. Plasma glucagon levels decreased in CHA, while plasma insulin levels increased in WC and CA. I/G increased in WC and CHA. These results indicate that thermal and metabolic responses would be modified by previous exposures to cold, heat, and cold-heat.

Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-O2.

ROSENMANN, MARIO, AND PETER MORRISON. Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-02 . Am. J. Physiol. 226(3) : 490495. 1974.-The high thermal conductance of an 80% He-20y0 02 atmosphere was used to elicit maximum metabolism (Mmax) in moderate cold in species ranging from 7-g pygmy mice (Baiomys taylori) to 250-g white rats, including redpolls (Acanthis J?ammea), two vesper mice (Calomys d&la, C. callosus), tundra voles (Microtus oeconomus), and four strains of Mus musculus. Values slightly exceeded those in similar animals using other methods to confirm the low metabolic ratio (Mmax/M, in) in rodents (4-8 X). Submaximal values at higher temperatures defined thermal conductance in He-02 and air. In different species the ratios of these conductances ranged from 1.4 to 2.6, differences which relate to the extent and quality of the respective insulation. M,,, was obtained at 13-70°C warmer in He-02 than required in air for the same metabolic effort. Avoidance of low-temperature technology and freezing injury, elimination of treadmills and training in running, prompt attainment of M,,., (3-10 min after He-02 exposure), and obviation of shaving or wetting procedures are advantages of the present technique.

Regulation of shivering and non-shivering heat production during acclimation of rats.

When cold acclimating rats are treated with diathermy, curare and a combination of both, two main fractions of the increase in cold-induced oxygen consumption can be delineated. First, a fraction which diathermy replaces by virtue of the fact that it, in the intensities used, can raise core temperature without altering the temperature of the skin; therefore this fraction appears to be dependent upon changes in central temperature and is found to persist throughout the period of acclimation investigated. Second, a fraction of cold-induced oxygen consumption which is not replaced by diathermy and which is presumed to be dependent upon changes in skin temperature. By the administration of curare, this second fraction can be separated into two further fractions acting reciprocally depending upon the duration of cold exposure. In the early stages of acclimation, the curare-suppressed fraction of oxygen consumption appears to be entirely due to shivering. As shivering disappears with acclimation, it is replaced by a peripherally regulated nonshivering heat source which eventually takes over all the duties of heat production previously performed by shivering.