6.3. Cold acclimation and nonshivering thermogenesis

The existence of NST in young birds has been studied almost merely in Muscovy ducklings and king penguin chicks. Over ten years ago, Connolly et al. (1989) called for rigorous studies to confirm the existence of avian NST in other bird species. However, before the present work, no new species have been used. The putative development of NST as a result of cold acclimation includes the assumption that NST gradually replaces shivering. In the studies performed with Muscovy ducklings and king penguin chicks, the absence of shivering thermogenesis was reported merely for the gastrocnemius muscle. Nevertheless, as the study by Aulie and Tøien (1988) in domestic chickens revealed, different muscles can have different threshold temperatures for shivering; in the leg muscles (musculus iliotibialis) of the chicken, shivering was observed to appear at 32°C but in breast muscles only at 20°C. This finding was confirmed by Carey et al.’s (1989) observation in winter acclimatized adult house finches (Carpodacus mexicanus), that the thermal thresholds in leg muscles for the onset of shivering were substantially below the thresholds for the onset in the pectoralis; in pectoralis shivering appeared approximately at the ambient temperature of 20°C, while in the gastrocnemius, tibialis and peroneus muscles the corresponding temperatures were -5, -11, and -14°C, respectively. The conclusion one has to draw is that the possibility for different threshold temperatures in different muscles should always be taken into account and all shivering should be excluded before the lack of shivering can reliably be interpreted as evidence of NST. For example, Vittoria and Marsh (1996) showed with more extensive EMG measurements that in cold-acclimated Muscovy ducklings, shivering is present in two thigh muscles (musculus iliofibularis and m. flexor cruris lateralis) even when it is absent in gastrocnemius. This finding suggests that shivering is probably the major source of regulatory heat production in cold-acclimated Muscovy ducklings too.

In the present work, oxygen consumption increased concomitantly with the EMG activity both in the warm and the cold-acclimated birds in at least one of the muscles studied (III). Thus all the heat production can be explained by shivering thermogenesis and no evidence for the existence of NST was found. The intensity of the EMG did not decrease due to cold acclimation but in contrast, it increased. One could claim that the chicks were only partially cold acclimated or that the chicks had grown past or had not yet reached the stage where the capacity of NST is most evident. However, the biological significance of NST occurring in a very short age-period and yet requiring a long exposure to cold is difficult to conceive. Nevertheless, it is possible that with a lower acclimation temperature NST could have developed. However, the intensity of cold-exposure used in cold acclimation should be “ecologically sensible” and similar to that in the wild. For most newly-hatched chicks, continuous three-week cold acclimation at 5°C is far removed from their natural conditions. Moreover, a severe hypothermia caused by a a single period of severe cold exposure may increase uncoupled respiration (Skulachev & Maslov 1960). By exposing sheared domestic pigeons to an ambient temperature of -15°C and by letting birds’ body temperatures fall to 5–10°C, these authors were able to increase mitochondrial uncoupled oxidation artificially. However, it is questionable if NST thus obtained has any biological significance and if increased uncoupled oxidation is just a result of damage in mitochondrial membranes.

In adult winter-acclimatised pheasants and grey partridges, Hohtola et al. (1989) found no clear cold-induced shivering in breast or leg muscles even at -30°C, although oxygen consumption was increased. In Hohtola et al.’s study, because the temperature of the major muscle groups was lower than the colonic temperature and because the thermal gradient between the colon and the muscles even increased in cold, they concluded that the major muscle groups did not participate in cold-induced thermogenesis by shivering or any other heat productive mechanism. This finding suggests that in adult birds, a high degree of localisation of shivering may exist or alternatively a non-muscular regulatory source of heat may exist. In the chicks of the present study, shivering increased as also the oxygen consumption (II–V). Furthermore, the experiments in which the muscle temperatures were measured showed an increase in the electrical activity of the muscles with a simultaneous increase in the muscle-body temperature gradient (Fig. 3). Therefore, it is justified to conclude that shivering was truly the mechanism, which produced the thermoregulatory heat.

The studies by Saarela and Heldmaier (1987) and Saarela et al. (1995) with adult Japanese quails and European finches (Carduelis sp.), respectively, showed that in extreme cold (from -40 to -60°C) the intensity of shivering levelled off or even began to decrease while oxygen consumption was still increasing. The authors raised the possibility that increased O₂-to-EMG ratio indicates the existence of NST acting as a secondary source of heat and supporting shivering thermogenesis in severe cold. A similar change in the O₂-to-EMG ratio was observed in the cold-acclimated Japanese quail chicks of the present study too (III). However, Hohtola (1982) found in pigeons that the correlation between the mean rectified voltage of the EMG and the metabolic rate decreased with decreasing ambient temperature. This decrease may reflect the saturation of the limited field sensed by the electrode. Recruitment of motor units farther from the recording site in the same muscle or different muscles is thus undetectable. Theoretically, when the intensity of shivering increases, negative and positive currents of the myoelectric signal are more likely to contact measurement electrode at the same time and thus cancel each others electrically. Any prediction of total muscular heat production based on recordings of the EMG from a single muscle has to be made with caution. As Hohtola et al. (1998) emphasised, the conclusion on the presence of NST should not be drawn only on the basis of the changes in the O₂-to-EMG ratio before more direct explanations can be ruled out. In any case, it remains clear that shivering was the first line defence mechanism against cold in the species of the present work.