Daily rhythms of nonshivering thermogenesis and responses to photoperiod manipulations in Apodemus mystacinus from two different ecosystems

Comparative physiology is an important tool for understanding adaptation to environment. Regulatory nonshivering thermogenesis (NST) is an essential mechanism in small mammals for coping with low ambient temperatures. Because of its geographical location and its sharp climatic changes across short distances, Israel offers conducting comparative studies between different populations of the same species. The aims of this study were: (1) to compare NST-capacity daily rhythms, between the two populations of the broad-toothed field mouse Apodemus Mystacinus—that of Mount Carmel (Mediterranean) and that of Mount Hermon (Subalpinic), (2) to compare the thermoregulatory daily rhythms response to photoperiod manipulations of mice from the two populations.

Mice were acclimated for at least 3 weeks to long scotophase (16D:8L-LS) and then to long photophase (16L:8D-LP) at a constant ambient temperature (T_a) of 24±1 °C. The following variables were compared at four different times of the day (06, 12, 18, 24 h): minimal body temperature (T_bMin), minimal oxygen consumption (VO₂Min) measured at the lower critical point and their response to noradrenaline (NA), 1.5 mg/1 kg.W_b injected s.c., (VO₂NA and T_bNA). NST-capacity was calculated as the ratio between VO₂NA and VO₂Min. The measurements were carried out at T_a of 28 °C and in light conditions matching those of acclimation. NA was injected after establishing VO₂Min and T_bMin. The values mean±SD are given for each measurement for n=6.

A three-way ANOVA revealed a significant difference between the two populations. Significant differences were revealed at different hours within populations under the different photoperiod regimes for different measured variables.     

Comparative aspects of the thermal biology of the short-tailed gerbil, Desmodillus auricularis, and the bushveld gerbil, Tatera leucogaster

1. 1. The response of oxygen consumption (VO₂), thermal conductance (C_d and C_min, body temperature (T_b), and evaporative water loss (EWL) of Tatera leucogaster and Desmodillus auricularis were measured over the range of ambient temperatures (T_a) from 5–35°C.

2. 2. Basal metabolic rate (BMR) of T. leucogaster was 0.841 ± 0.049 ml O₂ g⁻¹ h⁻¹ and lower than predicted, while that of D. auricularis was similar to the expected value (1.220 ± 0.058 ml O₂ g⁻¹ h⁻¹). D. auricularis had a high, narrow thermoneutral zone (TNZ) typical of nocturnal, xerophilic, burrowing rodents.

3. 3. D. auricularis and T. leucogaster regulated T_b over the range T_a = 5–35°C and kept EWL and dry thermal conductance at a minimum below the TNZ. However, the EWL of T. leucogaster increased rapidly above T_a = 30°C.

4. 4. After comparison with data from other species, it was concluded that there is an optimum size for xeric, nocturnal, burrowing rodents.

Daily rhythms of oxygen consumption, body temperature, activity and melatonin in the Norwegian lemming Lemmus lemmus under northern summer photoperiod

Rodents inhabiting high latitudes, close to the Arctic Circle or above it, are exposed to near 24 h daylight during the summer season. An example to such rodent species is the Norwegian lemming Lemmus lemmus, which is distributed in northern Fennoscandia. We measured daily rhythms of heat production (VO₂), body temperature (T_b), motor activity and melatonin secretion (measured from its metabolite 6-sulfatoximelatonin 6-SMT) in individuals exposed to natural day light, Oulu Finland, in August 1997 and at a controlled ambient temperature of 22 °C. Our results show a daily rhythm of VO₂ with an acrophase at 04:00 h and minimal values measured at 16:00 h, with a significant difference (p<0.001) between mean day and night values. 6-SMT also shows a daily rhythm with maximal secretion during the dark phase 24:00 and 06:00 h in which total 6-SMT values were 2.92±1.1 and 3.87±1.2 ng, respectively. The lowest values were recorded at 12:00 h; 0.86±0.63 ng. These results suggest that lemmings show a VO₂ and melatonin daily rhythms, which seem to correlate with each other and it appears that melatonin secretion increases heat production.     

Development of thermoregulation in Hawaiian brown noddies (Anous stolidus pileatus)

1. 1.|Oxygen consumption ( ) and body temperture (T_b) of Hawaiian brown noddies (Anous stolidus pileatus [Aves: Laridae]) during late incubation and in the first 24 h after hatching were measured at ambient temperatures (T_a) between 28 and 38°C and between 15 and 43°C, respectively. Evaporative cooling by hatchings at T_a of 36–43°C was also measured.

2. 2.|Throughout the late incubation stages studied, and T_b both varied directly with T_a in an ectothermic pattern.

3. 3.|The hatchlings successfully regulated T_b at T_a between ca. 29 and 43°C.

4. 4.|The functional basis of the abrupt increase in thermoregulatory capacity with hatching is discussed.

Geographic variation in field body temperature of sceloporus lizards

1. Using data from the literature, I assessed how broad climatic patterns affected field body temperatures (T_b’s) of lizards in the genus Sceloporus.

2. Sceloporus at temperate latitudes had mean T_b’s of 35°C throughout their elevational range. This pattern is associated with “tropical” temperatures that extend into high north latitudes during the summer and the relatively low elevations occupied by the lizards.

3. At tropical latitudes, mean T_b declined from 35°C at low elevations to 31°C at high elevations. This pattern is associated with low seasonal variation in temperature at tropical latitudes and the relatively high elevations occupied by the lizards.     

Multi-Oscillatory Control of Eclosion and Oviposition Rhythms in Drosophila melanogaster: Evidence from Limits of Entrainment Studies

The eclosion and oviposition rhythms of flies from a population of Drosophila melanogaster maintained under constant conditions of the laboratory were assayed under constant light (LL), constant darkness (DD), and light/dark (LD) cycles of 10:10 h (T20), 12:12 h (T24), and 14:14 h (T28). The mean (±95% confidence interval; CI) free-running period (τ) of the oviposition rhythm was 26.34 ± 1.04 h and 24.50 ± 1.77 h in DD and LL, respectively. The eclosion rhythm showed a τ of 23.33 ± 0.63 h (mean ± 95% CI) in DD, and eclosion was not rhythmic in LL. The τ of the oviposition rhythm in DD was significantly greater than that of the eclosion rhythm. The eclosion rhythm of all 10 replicate vials entrained to the three periodic light regimes, T20, T24, and T28, whereas the oviposition rhythm of only about 24 and 41% of the individuals entrained to T20 and T24 regimes, respectively, while about 74% of the individuals assayed in T28 regimes showed entrainment. Our results thus clearly indicate that the τ and the limits of entrainment of eclosion rhythm are different from those of the oviposition rhythm, and hence this reinforces the view that separate oscillators may regulate these two rhythms in D. melanogaster.     

Development of autonomic and behavioural thermoregulation in turkeys (Meleagris gallopavo)

1. 1.|Heat production (HP) and body temperature (T_b) measurements were conducted at ambient temperatures (T_a) between 10 and 40°C. In addition preference temperatures (PT) were determined in a temperature channel and T_b was measured at preferred T_a

2. 2.|The influence of age on T_b at constant, as well as at PT, was proved. Increasing age was accompanied by an elevation of T_b whereas HP remained constant in the mid-range of T_a

3. 3.|The lower T_b in the first days of life is suggested to result from a lower thermoregulatory set point during the postnatal period.

4. 4.|The PT were different for the observed types of behaviour. The PT at rest was higher than the PT during locomotion, food intake and drinking.

Heat tolerance of short-beaked echidnas (Tachyglossus aculeatus) in the field

(1) Echidnas occur throughout the hot arid zone of Australia yet laboratory studies have concluded that they are ill equipped physiologically to manage T_a higher than 35°C. (2) Consequently, it is generally assumed that echidnas must rely on behavioural thermoregulation, being nocturnal in hot weather and seeking less extreme microclimates during the day. (3) By monitoring T_b of echidnas in the field and relating these to T_a within their day time shelters in Western Queensland during summer, this study showed that echidnas are able to tolerate T_a of 35–40°C in hollow logs for up to 10 h. (4) Further, as T_b remains < T_a in these situations, echidnas may have physiological mechanisms for dealing with the heat after all.     

Effect of Ramadan on the diurnal variation in short-term high power output

This study examined the effects of Ramadan fasting on anaerobic performances and their diurnal fluctuations. In a balanced and randomized study design, 12 subjects were measured for maximal power (P_max; force-velocity test), peak power (P_peak), and mean power (P_mean) with the Wingate test at 07:00, 17:00, and 21:00 h on four different occasions: one week before Ramadan (BR), the second week of Ramadan (SWR), the fourth week of Ramadan (ER), and two weeks after Ramadan (AR). There was an interval of 28 h between any two successive tests. Oral temperature was measured before each test. Under each condition, the results showed a time-of-day effect on oral temperature. Analysis of variance revealed a significant (Ramadan×time-of-day of test) interaction effect on P_max. This variable improved significantly from morning to evening before Ramadan (1.1±0.2 W · kg^-1), during the second week of Ramadan (0.6±0.2 W · kg^-1), and two weeks after the end of Ramadan (0.9±0.2 W · kg^-1). However, daily fluctuations disappeared during the fourth week of Ramadan. For P_peak and P_mean, there was no significant Ramadan×test-time interaction. These variables improved significantly from morning to evening before Ramadan ([1±0.3 W · kg^-1] for P_peak and [1.7±1.6 W · kg^-1] for P_mean) and in the second week of Ramadan ([0.9±0.6 W · kg^-1] for P_peak and [1.7±1.5 W · kg^-1] for P_mean). However, they were not affected by time-of-day in the fourth week of Ramadan. Considering the effect of Ramadan on anaerobic performances, in comparison with before Ramadan, no significant difference was observed during Ramadan at 07:00 h. The variables were significantly lower in the second week of Ramadan and in the fourth week of Ramadan at 17:00 h and 21:00 h. P_mean was not affected during the second week of Ramadan. In conclusion, the time-of-day effect on anaerobic power variables tends to disappear during Ramadan. In comparison with the period before Ramadan, anaerobic performances were unaffected in the morning but impaired in the evening during Ramadan.     

Effect of pedal rate on diurnal variations in cardiorespiratory variables

Recently, it was observed that the freely chosen pedal rate of elite cyclists was significantly lower at 06:00 than at 18:00 h, and that ankle kinematics during cycling exhibits diurnal variation. The modification of the pedaling technique and pedal rate observed throughout the day could be brought about to limit the effect of diurnal variation on physiological variables. Imposing a pedal rate should limit the subject's possibility of adaptation and clarify the influence of time of day on physiological variables. The purpose of this study was to determine whether diurnal variation in cardiorespiratory variables depends on pedal rate. Ten male cyclists performed a submaximal 15 min exercise on a cycle ergometer (50% W_max). Five test sessions were performed at 06:00, 10:00, 14:00, 18:00, and 22:00 h. The exercise bout was divided into three equivalent 5 min periods during which different pedal rates were imposed (70 rev · min^-1, 90 rev · min^-1 and 120 rev · min^-1). No significant diurnal variation was observed in heart rate and oxygen consumption, whatever the pedal rate. A significant diurnal variation was observed in minute ventilation (p=0.01). In addition, the amplitude of the diurnal variation in minute ventilation depended on pedal rate: the higher the pedal rate, the greater the amplitude of its diurnal variation (p=0.03). The increase of minute ventilation throughout the day is mainly due to variation in breath frequency (p=0.01)—the diurnal variation of tidal volume (all pedal rate conditions taken together) being non-significant—but the effect of pedal rate×time of day interaction on minute ventilation specific to the higher pedal rate conditions (p=0.03) can only be explained by the increase of tidal volume throughout the day. Even though an influence of pedal rate on diurnal rhythms in overall physiological variables was not also evidenced, high pedal rate should have been imposed when diurnal variations of physiological variables in cycling were studied.     

Early age cold conditioning in broiler chickens (Gallus domesticus): thermotolerance and growth responses

The influence of short repetitive cold exposure at an early age (cold conditioning—exposure to 15°C for 3 h at 3 and 4 days of age) on chickens’ thermotolerance during cold challenge (15°C) at 21 days of age was examined. The first cold exposure elicited a dramatic decline in body temperature (T_b) and a significant elevation in stress response (plasma corticosterone concentration); the second cold exposure resulted in moderate T_b and stress responses. Thereafter, the corticosterone concentration remained at a significantly lower level. Acute cold challenge of conditioned broilers at 21 days of age revealed better T_b and stress recovery during the first 24 h, and a significantly lower mortality rate thereafter. Conditioned chickens exposed to optimal conditions (22°C) achieved significantly higher body weights than others. It may be concluded that early cold conditioning improves thermotolerance in broiler chickens in later life.     

Thermoregulation by the short-horned lizard (Phrynosoma douglassi) at high elevation

The short-horned lizard Phrynosoma douglassi was studied in a montane habitat (elevation of 2290 m) in the Guadalupe Mountains of Texas. The body temperatures (T_b) of active lizards were consistently between 35–36°C (grand mean=35.5°C) in the period from 0900 to 1800 h during the months of May through September. The lizards began their spring activity during April when environmental temperatures were still low. Although T_bs in April were significantly lower than during May through September, on sunny April days the lizards were able to maintain T_bs near 30°C even when air temperatures were as low as 1.5°C. P. douglassi at this site thermoregulated very effectively whenever they were not limited by the physical environment.     

Metabolism and thermoregulation in Maximowiczi's voles (Microtus maximowiczii) and Djungarian hamsters (Phodopus campbelli)

1 Metabolic rates (Vo₂), body temperature (T_b), and thermal conductance (C) were first determined in newly captured Maximowiczi's voles (Microtus maximowiczii) and Djungarian hamsters (Phodopus campbelli) from the Inner Mongolian grasslands at a temperature range from 5 to 35 °C.

2 The thermal neutral zone (TNZ) was between 25 and 32.5 °C for Maximowiczi's voles and between 25 and 30 °C for Djungarian hamsters. Mean T_b was 37.0±0.1 °C for voles and 36.2±0.1 °C for hamsters. Minimum thermal conductance was 0.172±0.004 ml O₂/g h °C for voles and 0.148±0.003 ml O₂/g h °C for hamsters.

3 The mean resting metabolic rate within TNZ was 2.21±0.05 ml O₂/g h in voles and 2.01±0.07 ml O₂/g h in hamsters. Nonshivering thermogenesis was 5.36±0.30 ml O₂/g h for voles and 6.30±0.18 ml O₂/g h for hamsters.

4 All these thermal physiological properties are adaptive for each species and are shaped by both macroenvironmental and microenvironmental conditions, food habits, phylogeny and other factors.

Thermal biology of the fossorial rodent Ctenomys fulvus from the Atacama desert, northern Chile

The Andean tuco-tuco, Ctenomys fulvus (Rodentia: Ctenomyidae) inhabits one of the most arid regions of the world, the Salar de Atacama, Northeast of Antofagasta, Chile (23°17′06″S, 68°05′43″W; 2.240 m.a.s.l). We found that a stable microclimate in burrows, a low evaporative water loss (EWL), and a diet of roots (59% water content) are the main factors that permit the survival of this fossorial species in harsh desert conditions. Large circadian variation in T_a was observed above ground. Daily ΔT_a (T_a max − T_a min) = 37.9±0.2°C in summer and in winter. In contrast, circadian variation of T_a inside the burrows was only 5.8±0.5°C in the same seasons. Relative humidity (RH) was 1.9–3.1% during the day, increasing to maximum values of 27% at night and early morning. Inside the burrows RH was higher and quite stable, ranging between 53.1 and 65%, independent of the time of day and season. EWL, measured between 10 and 25°C, was low (1.26 mg/g h), and a moderate increase of 13–20% was observed at higher temperatures. The low EWL may prevent dehydration. However, because of the low heat loss capability, animals became hyperthermic (0.8–1.6°C) in dry air at T_a=30–35°C. As T_a during afternoon normally exceeded 35°C, the microclimate of burrows provided the only way to avoid the lethal effects of hyperthermia.     

Daily Rhythms of Metabolic Rate and Body Temperature of Two Murids from Extremely Different Habitats

Daily circadian rhythms of body temperature (T_b) and oxygen consumption (VO₂) were measured in two murid species, which occupy extremely different habitats in Israel. The golden spiny mouse (Acomys mssalus) is a diurnal murid distributed in arid and hot parts of the great Syrio-African Rift Valley, while the broad-toothed field mouse (Apodeinns mystacinus) is a nocturnal species that inhabits the Mediterranean woodlands. In both species, the daily rhythms of T_b and VO₂ are entrained by the photoperiod. Under laboratory experimental conditions (ambient temperature T_a = 33^oC and photoperiod regime of 12L: 12D), Acomys russatus exhibits a tendency towards a nocturnal activity pattern, compared to the diurnal activity displayed by this species under natural conditions. Under the same photoperiod regime and at T_a = 28^oC, Apodemus mystacinus displays nocturnal activity, as observed under natural conditions. The maximal values of T_b were recorded in Acomys russatus at midnight (23:50 h), while the maximal values of VO₂ were recorded at the beginning of the dark period (18:20 h). In Apodemus mystacinus, the maximal values of T_b and VO₂ were recorded at 23:40 and 20:00 h, respectively. The ecophysiological significance of these results is discussed further.     

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-HT₃ 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 (VO₂) 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 VO₂ before shivering (178±9 ml/min/m²) rose significantly during shivering (291±21 ml/min/m²). 5 mg of tropisetron in 2 volunteers and 10 mg in 3 volunteers stopped shivering but it returned (grade 0–1). The VO₂ decreased significantly (209±17 ml/min/m²). Placebo had no effect.

Tropisetron reduced cold-induced VO₂ 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.     

The effect of acclimation on the acid-base status of pigeons exposed to high ambient temperatures

Arterial pH, PCO₂ (P_aCO₂), plasma bicarbonate [HCO₃⁻ and respiratory frequency were measured in pigeons exposed to ambient temperatures (T_aS) of 30–60°C. Acclimated, nonpanting birds regulated acid-base balance at normal levels, when exposed to T_as) between 30 and 53°C T_a. At higher T_as (55–60°C), both nonpanting and panting acclimated pigeons regulated pH at normal levels, 7.544 ± 0.011 (SD) and 7.531 ± 0.022 (SD), respectively, accompanied by a slight hypocapnia, 24.8 ± 4.0 Torr and 23.8 ± 2.49 Torr (P_aCO₂), respectively. Nonacclimated birds, exposed to 50°C T_a, endured a severe hypocapnia (P_aCO₂ of 9.1 ± 2.52 Torr) and alkalosis (pH of 7.702 ± 0.048). Thirteen exposures to > 50°C T_a, 4–6 h a day, resulted in a significant improvement in the capacity of the panting pigeon to maintain an almost normal acid-base balance, i.e. actual and standard [HCO₃⁻ of 22.6 ± 1.22 and 25.7 ± 1.10 mM/l, respectively, and only a slight hypocapnia (P_aCO₂ of 23.6 ± 3.9 Torr) and alkalosis (pH of 7.589). The suggestion that acclimation to high T_as (50–60°C) is needed for fine adjustment between the competing needs for heat dissipation, pulmonary gas exchange, and acid-base regulation in the heat-exposed pigeon is discussed.     

Determination of the thermodynamics of carbonic anhydrase acid-unfolding by titration calorimetry

The enthalpy of unfolding (Δ_uH) of carbonic anhydrase II was determined by titrating the protein with acid and measuring the heat using isothermal titration calorimetry (ITC) in the temperature range of 5 to 59 °C. By combining the ITC results with our previous findings by differential scanning calorimetry (DSC) in the temperature range of 39 to 72 °C, the Δ_uH dependence over a wide temperature range was obtained. The temperature dependence of the enthalpy displays significant curvature indicating that the heat capacity of unfolding (Δ_uC_p) is dependent on temperature. The T-derivative of Δ_uC_p was equal to 100 ± 30 J/(mol × K²), with the result that the Δ_uC_p is equal to 15.8 kJ/(mol × K) at 5 °C, 19.0 kJ/(mol × K) at 37 °C and 21.8 kJ/(mol × K) at 64 °C. The enthalpy of unfolding is zero at 17 °C. At lower temperatures, the Δ_uH becomes exothermic.

This method of determining protein unfolding thermodynamics using acid-ITC, significantly widens the accessible T-range, provides direct estimate of the thermodynamic parameters at physiological temperature, and gives further insight into the third T-derivative of the Gibbs free energy of unfolding.     

Multiple oscillations in changing cell shape by the plasmodium of Physarum polycephalum: general formula governing oscillatory phenomena by the Physarum plasmodium

The long-term dynamics of an amoeboid cell shape were studied using Physarum polycephalum plasmodia with various sizes. Cell shape varied oscillatorily in a multiple periodic manner. The organism periodically elongated with period of T₇ = 10 h, branched with T₆ = 4 h, became uneven with T₅ = 30 min and T₄ = 10 min, and blew up with T₃ = 1.5 min. Tiny plasmodia changed shape much faster with T₃ = 1.3 min, T₂ = 24 s and T₁ = 3.3 s simultaneously. The plasmodial cytoskeleton also showed periodic pattern formation with T₆, T₅ and T₃. Periods of all known oscillatory phenomena in this organism correspond to some of the periods for the above seven rhythms, and the following geometric progression holds among the periods: T_i + 1/T_i = 7 and T_i + 2/T_i + 1 = 3, where i = 1, 3, 5. Thus, multiple oscillations in the plasmodium are organized globally.     

Ambient temperature limits and stability of temperature regulation in telemetered male and female rats

Knowing the ambient temperature (T_a) limits of normothermia in laboratory rodents is important because their thermoregulatory responses are useful in studies of physiology, pharmacology and toxicology. The present study assessed the T_a limits of normothermia using radiotelemetry to monitor core temperature (T_c), heart rate (HR), and motor activity (MA) in unrestrained, male and female Long-Evans rats over a 24 h period. Rats were housed individually in acrylic cages with wire-screen tops and bottoms and maintained at T'_as ranging from 12 to 33.5°C for 24 h with food and water provided ad libitum on a 12:12 L:D photoperiod. The limits of normothermia (i.e. where there was no significant change in T_c) were <12–29.5°C for females and 14.5–29.5°C for males. T_c of males at T'_as of 12, 32, and 33.5°C increased significantly above the baseline T_c. Female rats had a lower T_c than males at the warmest and coldest T'_as. HR and MA were generally higher in females at all T'_as. Males appeared to be poorly adapted to thermoregulate at T'_as above 30°C as based on their excessively high T'_cs, low MA, and marked weight loss compared to that of the females. Within the limits of normothermia the stability of T_c regulation (i.e. [(ΔT_c/ΔT_a) × 100]/2) was ±1.3 and ± 0.9% for males and females, respectively, over a 24 h period. These data on the stability of T_c in the male and female rat provide a valuable framework to study the acute and chronic effects of drugs, chemicals and other agents that affect temperature regulation.