Thermogenic mechanisms during the development of endothermy in juvenile birds

Kyösti Marjoniemi

Department of Biology, University of Oulu

Abstract

The use of regulatory and obligatory heat production mechanisms were studied in juvenile birds during the development of endothermy.

The development of shivering thermogenesis was studied in the pectoral and gastrocnemius muscles of the altricial domestic pigeon and in three precocial galliforms (Japanese quail, grey partridge and domestic fowl). The development of shivering was the determinant for the beginning of endothermy. Homeothermy also necessitated avoidance of excess heat loss by insulation and behavioural thermoregulation. In the precocial species, shivering thermogenesis was present in the leg muscles of the youngest age groups (1–2 d) studied. Breast muscles contributed shivering from the second post-hatching week. In the altricial pigeons, significant thermogenesis was apparent later than in the precocials, at the age of 6 d. In contrast to the precocials, the pectoral muscles of the altricials were the most significant heat production tissues. In newly-hatched partridges and pigeons, incipient shivering did not result in significant heat production.

The ability to produce heat in cold by putative nonshivering thermogenesis was studied in Japanese quail chicks and domestic ducklings. In both species, three-week cold acclimation resulted in morphometric and physiological changes, but there was no clear evidence of nonshivering thermogenesis. The lack of NST was evident bacause an increase in shivering amplitude at least in one of the muscles studied paralleled an increase in oxygen consumption. Consequently, shivering thermogenesis was probably the only mode of regulatory heat production.

The amplitudes of shivering EMGs measured during cold exposure were dependent on the coexistence of postprandial thermogenesis or exercise. Japanese quail chicks were able to substitute shivering thermogenesis partially with postprandial heat production when nourished. Bipedal exercise both inhibited shivering in pectorals directly via inhibitory neural circuits and stimulated it indirectly via decreased body temperature. Because of increased heat loss, exercise was not used as a substitute for shivering.

Shivering is a flexible mode of thermogenesis and its magnitude can be adjusted according to the magnitude of obligatory thermogenesis. The adjustment works towards energy saving by avoidance of the summation of different modes of heat production. The prerequisite for successful adjustment of shivering is adequate insulation, whose role in preventing excessive heat loss is pronounced during exercise. It is concluded that the energetics of posthatching thermoregulation includes the potential for optimizations in energy use in order to avoid dissipation of waste energy as heat.

Table of Contents

Acknowledgements

Abbreviations

List of original papers

1. Introduction

2. Endothermy and thermoregulation

2.1. Ontogeny of endothermy

2.1.1. Maturity of hatchlings
2.1.2. Post-hatching development

2.2. Thermogenic mechanisms

2.2.1. Shivering thermogenesis
2.2.2. Nonshivering thermogenesis
2.2.3. Postprandial excess heat production
2.2.4. Exercise thermogenesis

3. Outline of the thesis

4. Material and methods

4.1. Animals
4.2. Temperature measurements
4.3. Measurements of metabolic rate
4.4. Ability to resist cooling
4.5. Behavioural responses in temperature gradient
4.6. Measurements of shivering
4.7. Oxygen consumption of muscles in vitro

5.1. Ontogeny of endothermy

5.2. Development of shivering thermogenesis

5.3. Cold acclimation and nonshivering thermogenesis (III)

5.4. Modulation of shivering by the other forms of thermogenesis

5.4.1. Postprandial thermogenesis (IV)
5.4.2. Exercise thermogenesis (V)

6. Discussion

6.1. Ontogeny of endothermy
6.2. Development of shivering thermogenesis
6.3. Cold acclimation and nonshivering thermogenesis
6.4. Adjustment of shivering thermogenesis by postprandial heat production and exercise

7. Conclusions

List of Figures
1. Development of body temperature recorded using telemetry in a domestic fowl chick (Gallus domesticus) between post-hatching days 0–43 at a room temperature of 22°C. The initial peak is probably due to a febrile response after the implantation of the transmitter (Marjoniemi and Hohtola, unpublished).
2. The intensity of shivering EMGs in surface (solid circles) and intramuscular (open circles) locations of pectoral muscles of 21-d-old Japanese quail chicks at four different ambient temperatures. N = 4–5 at each point. Vertical bars indicate SE. (Marjoniemi, unpublished).
3. A: Oxygen consumption, root mean square EMG of the pectoralis, surface temperature of the pectoral muscle and temperature of the cloaca during steadily decreasing ambient temperature (0.33°C·min^-1) from 32 to -5°C in a 21-day-old Japanese quail chick. B: Temperature difference between the pectoral muscle and the cloaca first versus rms voltage of the EMG and second versus the oxygen consumption (Marjoniemi, unpublished).
4. Development of shivering thermogenesis in chicks of different development modes. Chicks are classified according to Starck and Ricklefs (1998b). Data is based on the direct observations of the age at which shivering is first observed. P = pectoralis; L = leg muscle; x = whole body; italics = visual or acustic observations or palpation; normal font = measurements with vibrometry or electromyography; * = data from the present study. References: 1) Passer montanus (Shichun et al. 1979), 2) Iridiprocne bicolor (Marsh 1980), 3) Sturnus vulgaris (Clark 1982), 4) Troglodytes aedon (Odum 1942), 5) Parus atricapillus (Odum 1942), 6) Zonotrichus leucophrys (Morton & Carey 1971), 7) Delichon urbica (Steen et al. 1989), 8) Agelaius phoeniceus (Olson 1994), 9) Sula bassanus (Montevecchi & Vaughan 1989), 10) Anous stolidus pileatus (Mathiu et al. 1991), 11) Somateria mollisima, (Myhre & Steen 1979), 12) Somateria mollisima (Steen & Gabrielsen 1988), 13) Fulica americana (Sutter & MacArthur 1992), 14) Pelecanus erythrorhynchus (Evans 1994), 15) Gymnorhinus cyanocephalus (Clark & Balda 1981), 16) Larus delawarensis (Dawson et al. 1976), 17) Tetrao urogallus (Hissa et al. 1983), 18) Lagopus lagopus (Aulie 1976), 19) Meleagris gallopavo (Dietz et al. 1997), 20) Numida meleagris (Dietz et al. 1997), 21) Bubulcus ibis (Hudson et al. 1974), 22) Gallus domesticus (Peters et al. 1961), 23) Podiceps cristatus (Keskpaik et al. 1968), 24) Podiceps auritus (Keskpaik et al. 1968), 25) Larus occidentalis (Dawson & Bennet 1981), 26) Larus occidentalis (Eppley 1987), 27) Puffinus pacificus (Mathiu et al. 1992), 28) Columba livia (Marjoniemi & Hohtola 1999), 29) Gallus domesticus (Marjoniemi & Hohtola 1999), 30) Perdix perdix (Marjoniemi & Hohtola 1999), 31) Coturnix c. japonica (Marjoniemi & Hohtola 1999), 32) Tringa totanus (Myhre & Steen 1979), 33) Gallinago gallinago (Myhre & Steen 1979), 34) Gallus domesticus (Randall 1943), 35) Lagopus lagopus (Myhre et al. 1975), 36) Larus ridibundus (Keskpaik & Davydov 1966).
5. Observed and suggested interactions between shivering thermogenesis and other forms of thermogenesis in juvenile birds. + = augmentation, - = inhibition, 1° = direct neuronal action, 2° = indirect action via changed body temperature.

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