Esa Hohtola

Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold

Adaptive nonshivering thermogenesis may have profound effects on energy balance and is therefore therefore is a potential mechanism for counteracting the development of obesity. The molecular basis for adaptive nonshivering thermogenesis has remained a challenge that sparked acute interest with the identification of proteins (UCP2, UCP3, etc.) with high‐sequence similarity to the original uncoupling protein‐1 (UCP1), which is localized only in brown adipose tissue. Using UCP1‐ablated mice, we examined whether any adaptive nonshivering thermogenesis could be recruited by acclimation to cold. Remarkably, by successive acclimation, the UCP1‐ablated mice could be made to subsist for several weeks at 4°C during which they had to constantly produce heat at four times their resting levels. Despite these extreme requirements for adaptive nonshivering thermogenesis, however, no substitution of shivering by any adaptive nonshivering thermogenic process occurred. Thus, although the existence of, for example, muscular mechanisms for adaptive nonshivering thermogenesis has recurrently been implied, we did not find any indication of such thermogenesis. Not even during prolonged and enhanced demand for extra heat production was any endogenous hormone or neurotransmitter able to recruit any UCP1‐independent adaptive nonshivering thermogenic process in muscle or in any other organ, and no proteins other than UCP1—not even UCP2 or UCP3—therefore have the ability to mediate adaptive nonshivering thermogenesis in the cold.

Thermal and electromyographic correlates of shivering thermogenesis in the pigeon.

1. Electromyographic, thermal and metabolic measurements were made on pigeons subjected to stepwise ambient cooling. Subsequent signal analysis of the EMG-recordings from the pectoral muscle showed that the mean rectified value (Umrv) is the most reliable EMG-based indicator of metabolic heat production (M). 2. The muscle-abdomen temperature difference was linearly related to M, and correlated strongly with Umrv. 3. The long-term and short-term fluctuations of shivering intensity (Umrv) were highly synchronous in the two main muscles, m. pectoralis and m. supracoracoideus. 4. The EMG-signal approached a Gaussian process at high shivering intensities. Evaluation of the changes in EMG median frequency suggested a size-dependent recruitment of motor units for shivering. 5. It is pointed out that Umrv and the integrated value of EMG are interconvertible and that Umrv should be preferred, because it has more physiological relevance.

Nocturnal hypothermia in fasting Japanese quail: The effect of ambient temperature

Japanese quail were equipped with intraperitoneal transmitters for telemetric measurement of body temperature (Tb) and activity. Food deprivation at + 24 degrees C for four days induced a well-defined nocturnal hypothermic response. The normal day-night difference (about 1 degrees C) in Tb increased 1 degrees C per day, reaching 5 degrees C on the fourth night of fast. Nocturnal motor activity decreased during the fast, while daytime activity first increased and then returned to the original level by the end of the fasting period. A strong correlation between Tb and motor activity was found during scotophase (r = .91) but not during photophase (r = .02). At + 4 degrees C, where food was deprived for two days, the level of hypothermia was not different from that at + 24 degrees C, but birds fasting in the cold reached the hypothermic level more rapidly. In control birds, the decrease in Tb at the beginning of scotophase was independent of ambient temperature. In the combined data, the level of hypothermia correlated strongly with body mass loss (r = .90), which shows that quail can directly or indirectly sense the amount of body energy reserves. This is the first report of hypothermia in a fasting gallinaceous bird. The consistent level of hypothermia at varying ambient temperatures suggests that either nonenergetic costs or phylogenetic constraints prevent deeper hypothermia in cold. Accordingly, the regulation of hypothermia cannot be explained by using only energetic arguments.

Specific appetite for carotenoids in a colorful bird.

Background Since carotenoids have physiological functions necessary for maintaining health, individuals should be selected to actively seek and develop a specific appetite for these compounds. Methodology/Principal Findings Great tits Parus major in a diet choice experiment, both in captivity and the field, preferred carotenoid-enriched diets to control diets. The food items did not differ in any other aspects measured besides carotenoid content. Conclusions/Significance Specific appetite for carotenoids is here demonstrated for the first time, placing these compounds on a par with essential nutrients as sodium or calcium.

LOCAL ADAPTATION TO WINTER CONDITIONS IN A PASSERINE SPREADING NORTH: A COMMON-GARDEN APPROACH

Abstract Sedentary passerine birds living in temperate and boreal regions need a high metabolic capacity for thermogenesis to survive winter conditions. As a consequence of the increased thermogenic capacity, basal energetic demands rise at a time when resources and time to acquire them decrease. In a previous study, great tits (Parus major) from two localities in Fennoscandia with contrasting winter conditions differed in their metabolic response to ambient temperature. To investigate the physiological basis underlying interpopulation differences we performed a commongarden experiment to test whether these differences were genetically based. We found basal metabolic rate to be higher in birds originating from transferred eggs from the southern population compared to the ones from the northern population, contrary to the relationship among birds living in their region of origin. Despite previous evidence suggesting that gene flow prevents local adaptation at the northern range limits of a species expanding northward, we found that great tits differ in their reaction norm to winter conditions according to the population of origin.

Shivering Thermogenesis in Leg and Breast Muscles of Galliform Chicks and Nestlings of the Domestic Pigeon

We studied the ontogeny of shivering thermogenesis in breast and leg muscles of precocial galliforms (domestic fowl, grey partridge, and Japanese quail) and the altricial domestic pigeon using electromyography (EMG) and indirect calorimetry. Galliforms were able to increase heat production by shivering in leg muscles at the youngest age studied (1–2 d). Pectorals contributed to heat production from days 7–10 onward, but in the partridge and especially in the fowl, shivering by the pectorals was weaker than in the quail. In the pigeon, shivering began in pectorals and legs at 2 and 4 d of age, respectively, and pectorals had clearly the predominant role in thermogenesis. Despite the early beginning of electrical signs of shivering, significant thermogenesis did not appear in the pigeon before the age of 6 d. All galliforms shivered in bursts, like pigeons aged 2–4 d. From the age of 6 d onward, continuous shivering became predominant in the pigeon. In pectorals of 2–6‐d‐old pigeons, shivering did not increase linearly during decreasing ambient temperature, as in other muscles and species, but started abruptly, at full intensity. Furthermore, in 2–4‐d‐old pigeons, cooling induced movement activity in legs. The median frequency of shivering EMGs varied (1) with maturation of the muscle, (2) with size of the adult bird, and (3) between altricials and precocials.

Energetics and Development of Temperature Regulation in Capercaillie Tetrao urogallus

Thermoregulatory capacities of newly hatched and developing capercaillie chicks (Tetrao urogallus) were studied. Metabolic rate and body temperature measurements were conducted at ambient temperatures (Ta) between −30 and 37 C. The chicks rely primarily on behavioral thermoregulation. A sudden increase of basal heat production at the age of 4–5 days constitutes an important element in the control of stable body temperature (Tb) and coincides with the gradual elevation of the body temperature and capacity to stimulate thermoregulatory heat production. Chicks 1–3 days old can more than double their metabolic rate at 15 C. There is no evidence of regulatory nonshivering thermogenesis. Consequently, the only way to increase heat production is to stimulate muscular activity either by shivering or by voluntary muscular activity. The most rapid development of thermoregulatory capacity occurs at the age of 7–11 days, which may be correlated with the synergistic maturation of neuronal thermoregulatory control elements and a functional hypothalamichypophysis axis. Since the development of insulation is only gradual during the first weeks of hatching, it plays only a secondary role in comparison with the behavioral means of seeking shelter under the female and an increased basal metabolic rate. Our results support the field observations which indicate that newly hatched capercaillie chicks can tolerate 10–15 C only a few minutes.

Shivering and ptiloerection as complementary cold defense responses in the pigeon during sleep and wakefulness

SummaryThe effects of sleep and wakefulness on two autonomic cold defense responses, shivering and ptiloerection, were studied in the pigeon. Shivering (integrated pectoral muscle EMG), axillary and foot temperatures were measured continuously and the magnitude of ptiloerection was estimated by a specially devised feather index (FI) using a TV-monitor. Behavioral signs of sleep and wakefulness were verified by EEG-recordings.In pigeons placed at +4°C, slow-wave sleep was associated with a gradual decline of shivering and a simultaneous increase of FI. Spontaneous bouts of arousal elicited strong bursts of shivering and coincident drops in FI (Fig. 2). Alerting the sleeping pigeons by a standardized stimulus had the same effects as spontaneous arousal, but the changes were more consistent. The stimulus produced behavioral and electrocortical arousal, a 81% increase in shivering intensity, and an almost complete elimination of ptiloerection. A slight vasodilatation of feet and a neglible increase of axillary temperature followed (Fig. 3). The changes in shivering and FI showed a significant negative correlation both during spontaneous and induced bouts of arousal.These results show that ptiloerection is preferentially used for cold defense during sleep, whereas shivering is recruited during periods of arousal. This complementarity of insulative and thermogenic mechanisms may form a physiological basis for explaining some diurnal patterns in avian bioenergetics.

Role of origin and endophyte infection in browning of bud-derived tissue cultures of Scots pine (Pinus sylvestris L.)

Callus tissues originating from buds of mature Scots pine (Pinus sylvestris L.) trees exhibit the typical problem of browning, which leads to degeneration and death of the tissues. The effects of medium, origin (tree and location) and endophyte infection were studied on the browning and growth of bud-derived tissue cultures. The calli growing on medium with higher kinetin content and source of organic nitrogen, and originating from the southern location grew better and exhibited less browning. Endophytic microbial cells were detected in the brown callus tissues by transmission electron microscopy. The natural endophyte infection frequency of Scots pine buds was studied and found dependent on the tree, but not on the location. A well-growing, green callus line was artificially infected by an endophytic strain of Methylobacterium extorquens, and browning was not observed on solid media compared to the uninfected control clones of the same callus. However, suspension cultures started from the infected callus died faster than cultures started from the uninfected callus. The endophyte species composition and plant genotype together with tissue culture conditions are the key factors for gaining plant tissue cultures with high regeneration capacity.

Facultative and obligatory thermogenesis in young birds: a cautionary note

A brief overview on thermogenic mechanisms in young precocial birds is given. While shivering thermogenesis is well documented in these birds, evidence for a facultative non-shivering component of heat production, comparable to that found in the brown adipose tissue of mammals, is ambiguous. One reason for this is the confusion between thermoregulatory and obligatory thermogenesis. In particular, the existence of a thermogenic reaction, even a futile one, does not by itself constitute proof of true thermoregulatory non-shivering thermogenesis. More probably, such a reaction is another obligatory component of heat production. Heat increment of feeding and motor activity are classical examples of such mechanisms. Thermogenesis arising from such mechanisms can often be adaptively used by the thermoregulatory systems in young birds, as well as in adults.