6.4. Adjustment of shivering thermogenesis by postprandial heat production and exercise

Thermal by-products of feeding and locomotion may be of benefit in energy saving especially in juvenile birds. The present study clearly showed that the intensity of shivering is dependent on the co-existence of postprandial heat production or exercise thermogenesis (IV, V). Shivering as a form of regulatory heat production is a flexible mode of thermogenesis and its magnitude can be adjusted according to the magnitude of obligatory thermogenesis. This adjustment works towards energy saving and the avoidance of the summation of different modes of heat production. Moreover, in mammals possessing BAT, nonshivering thermogenesis adjusts the use of shivering indirectly via body temperature. It has been found that if NST alone is insufficient to maintain a constant temperature in the upper spinal cord, then shivering is initiated (Heldmaier et al. 1990). This finding suggests that the use of NST in BAT adjusts the use of shivering as well. The indications in favour of the existence of NST in birds also show shivering being flexibly modulated by putative avian NST, use of which precedes the use of shivering. If no adjustment occurs, the nervous system controlling shivering would not respond to the increased heat production and to the changed thermal balance of the body.

The potential for the greatest thermal benefit from postprandial heat production exists in small-sized endothermic animals that consume relatively large high-protein diets and inhabit thermally stressful microhabitats (Campbell et al. 2000). Young precocial chicks fulfil these criteria by feeding mostly on insects and other evertebrates and by being frequently exposed to temperatures below the thermoneutral zone (e.g. Chappell 1980). The present study clearly showed that fasted Japanese quail chicks used shivering to compensate for the decrease in postprandial heat production (IV). In other words, the decreased shivering in the ad libitum fed chicks means that postprandial heat production has the capacity to substitute for shivering thermogenesis. In a review on the energetics of postnatal growth, Weathers (1996) concluded that postprandial heat production has no value for growing chicks because feeding stimulates peripheral circulation and thus facilitates heat loss. However, this worthlessness may be the case in thermoneutrality only where postprandial heat production is equivalent to excess heat which must be dissipated in order to maintain thermal balance and to avoid an increase in body temperature. In contrast to thermoneutrality, in cold, where additional heat production is needed, postprandial heat production may be gradually harnessed to thermoregulation until its whole capacity is used and in addition regulatory thermogenesis is also needed. The results of the present study indicate that also during postprandial heat production, shivering is adjusted indirectly via changed body temperature. The successful use of postprandial heat production in thermoregulation possibly necessitates an ability to adjust thermal conductance. In the Japanese quails in the present study, the dissipation of postprandial heat was seen in the differences in the thermal conductance of the control and fasting groups (IV). Because the magnitude of postprandial thermogenesis cannot be actively regulated, its proportion used for thermoregulatory purposes is regulated by the use of insulation. This hypothesis is supported by the fact that in thermoneutrality, the thermal conductance was higher in fed chicks but in cold there were no differences between the fed and fasted chicks. Thus it is possible that the successful use of postprandial heat production is dependent on the insulative capacity available and in birds with poor insulation, as in newly hatched altricials, postprandial heat is lost to the surroundings.

Although breast muscles do not participate in bipedal exercise in any way, bipedal exercise interferes with the shivering in these muscles (V). In pigeons, the inhibition of shivering is initiated by afferent input from leg muscles and sole skin (Nomoto 1989); from femoral muscles, the inhibitory neural circuit mediating this inhibitory response via afferents includes at least one interneuron in the spinal cord. In the present study, similarly to exercising pigeons in cold (Nomoto & Nomoto-Kozawa 1985), shivering increased during exercise in response to decreased body temperature in the Japanese quail chicks. It seems obvious that during exercise, shivering is adjusted first via inhibitory nervous circuits and later augmented indirectly via the activity of peripheral thermoreceptors in response to a decrease in body temperature. Body temperature may also increase when the exercise is intense and only some of the excess heat is dissipated to the surroundings (e.g. Brackenbury et al. 1981, Nomoto et al. 1983a, Nomoto et al. 1983c). It is obvious that in exercising birds, increased body temperature results in a decrease in shivering, just as in resting birds. However, Nomoto and Nomoto-Kozawa (1985) showed with exercising domestic pigeons that when the spinal cord is cooled with thermodes, intense shivering is initiated in the pectorals, but after termination of the cooling the shivering intensity decreases.

In the present study, due to suppression of shivering and to increased forced convection during exercise, hypothermia developed faster the colder the ambient temperature was (V). Although exercise interacted with regulatory thermogenesis, partially inhibiting it, the benefit of exercise, if any, was restricted to temperatures slightly below thermoneutrality. By optimizing the duration of exercise and the speed of locomotion to the prevailing ambient temperature, a better benefit may be possible. However, this hypothesis has not been studied. Moreover, extremely few experiments concerning the substitution of facultative heat production by exercise in juvenile birds can be found in literature. The data from the studies which do exist, indicate that exercise has only a little benefit for thermoregulation as the present study also indicates. For example, Modrey and Nichelmann (1992) observed that voluntarily exercising turkey chicks aged 1–10 days prefer 1.5–2.5°C lower T_a than resting birds. This preference may indicate a partial substitution in temperatures only slightly below thermoneutrality. In free-living arctic shorebirds chicks, Chappel (1980) found no significant benefit from exercise heat at ambient temperatures 3–7°C.

The benefit of exercise thermogenesis can be divided into energetic and thermal advantages. The energetic advantage results from the substitution of shivering with exercise heat production. The thermal advantage depends on the fate of body temperature as a result of exercise. However, energetic advantage may accompany a thermal disadvantages, as observed in exercising adult rats (Mäkinen et al. 1996). In the Japanese quails chicks of the present study, exercise was not utilized in thermoregulation in cold either in an energetically or a thermally favourable way. In some adult birds (see section 2.2.4), the energetic advantage and the thermal advantage coexists even though the birds are small sized. The co-existence of these advantages may suggest that the potential for substitution is always present and that success in prevention of heat loss during exercise determines whether substitution is complete, partial or non-existent.