Skip to main content
Log in

Daily rhythm of oxygen consumption and thermoregulatory responses in some European winter- or summer-acclimatized finches at different ambient temperatures

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The oxygen consumption of European finches, the siskin (Carduelis spinus), the brambling (Fringilla montifringilla), the bullfinch (Pyrhulla pyrhulla), the greenfinch (Carduelis chloris) and the hawfinch (Coccothraustes coccothraustes), was recorded continuously while ambient temperature was decreased stepwise from +30 down to-75°C. The oxygen consumption, body temperature (telemetrically), and shivering (integrated pectoral electromyography) of greenfinches were measured simultaneously at ambient temperatures between +30 and-75°C. Maximum heat production, cold limit, lower critical temperature, basal metabolic rate and thermal conductance (of the greenfinch) were determined. The diurnal variation of oxygen consumption of siskins and greenfinches was recorded at thermoneutrality and below the thermoneutral zone in winter- and summer-acclimatized birds. The diurnal variation of body temperature and thermal conductance of greenfinches were also determined. The diurnal variation of heat production was not seasonal or temperature dependent in the siskin and in the greenfinch. Nocturnal reduction of oxygen consumption saved 15–33% energy in the siskin and greenfinch. Body temperature of the greenfinch was lowered by 2.5–3.4°C. The nocturnal reduction of thermal conductance in the greenfinch was 39–48%. The basal metabolic rate was lowest in the largest bird (hawfinch) and highest in the smallest bird (siskin). The values were in the expected range. The heat production capacity of finches in winter was 4.7 times basal metabolic rate in the siskin, 4.2 times in the brambling, 3.5 times in the greenfinch and 2.9 times in the bullfinch and hawfinch. The heat production capacity of the siskin and greenfinch was not significantly lower in summer. The cold limit temperatures (°C) in winter were-61.2 in the siskin,-41.3 in the greenfinch,-37.0 in the bullfinch,-35.7 in the brambling and-28.9 in the hawfinch. The cold limit was 14.3°C higher in summer than in winter in the siskin and 8.7°C in the greenfinch. Thermal insulation of the greenfinch was significantly better in winter than in summer. The shivering of the greenfinch increased linearly when ambient temperature was decreased down to-40°C. Maintenance of shivering was coincident with season. In severe cold integrated pectoral electromyography did not correlate with oxygen consumption as expected. The possible existence of non-shivering thermogenesis in birds is discussed. It is concluded that the acclimatization of European finches is primarily metabolic and only secondly affected by insulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AAT :

avian adipose tissue

bm :

body mass

BMR :

basal metabolic rate

C t :

thermal conductance

EMG :

electromyogram

HP :

heat production

HP max :

maximum heat production

MR :

metabolic rate

NST :

non-shivering thermogenesis

RMR :

resting metabolic rate

RQ :

respiratory quotient

T a :

ambient temperature

T b :

body temperature

T c :

colonic temperature

T 1c :

lower critical temperature

TNZ :

thermoneutral zone

T st :

shivering threshold temperature

V :

oxygen consumption

References

  • Aschoff J (1981) Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp Biochem Physiol 69:611–619

    Article  Google Scholar 

  • Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism. Fed Proc 29:1541–1552

    PubMed  Google Scholar 

  • Aulie A, Tøien Ø (1988) Threshold for shivering in aerobic and anaerobic muscles in bantam cocks and incubating hens. J Comp Physiol B 158:431–435

    PubMed  Google Scholar 

  • Ballantyne JS, George JC (1978) An ultrastructural and histological analysis of the effects of cold acclimation on vertebrate skeletal muscle. J Therm Biol 3:109–116

    Article  Google Scholar 

  • Barnett LB (1970) Seasonal changes in temperature acclimatization of the house sparrow, Passer domesticus. Comp Biochem Physiol 33:559–578

    Article  Google Scholar 

  • Barré H, Bailly L, Rouanet JL (1987) Increased oxidative capacity in skeletal muscles from cold-acclimated ducklings: a comparison with rats. Comp Biochem Physiol 88B:519–522

    Google Scholar 

  • Barré H, Geloen A, Chatonnet J, Dittmar A, Rouanet J-L (1985) Potentiated muscular thermogenesis in cold-acclimated muscovy duckling. Am J Physiol 249:R533-R538

    PubMed  Google Scholar 

  • Bartholomew GA, Vleck CM, Buche TL (1983) Energy metabolism and nocturnal hypothermia in two tropical passerine frugivores, Manacus vitellinus and Pipra mentalis. Physiol Zool 56:370–379

    Google Scholar 

  • Bennett PM, Harvey PH (1987) Active and resting metabolism in birds: allometry, phylogeny and ecology. J Zool (London) 213: 327–363

    Google Scholar 

  • Carey C, Johnston RM, Bekoff A (1989) Thermal thresholds for recruitment of muscles during shivering in winter-acclimatized finches. In: Mercer JB (ed) Thermal physiology Elsevier, Amsterdam, pp 685–690

    Google Scholar 

  • Chaplin SB (1976) The physiology of hypothermia in the blackcapped chickadee, Parus domesticus. Comp Biochem Physiol 33: 559–578

    Google Scholar 

  • Connoly E, Nedergaard J, Cannon B (1989) Shivering and nonshivering thermogenesis in birds: a mammalian view. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum, New York, pp 37–48

    Google Scholar 

  • Dawson WR, Carey C (1976) Seasonal acclimatization to temperature in cardueline finches. I. Insulative and metabolic adjustments. J Comp Physiol 112:317–333

    Google Scholar 

  • Dawson WR, Marsh RL (1989) Metabolic acclimatization to cold and season in birds. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum, New York, pp 83–94

    Google Scholar 

  • Dawson WR, Marsh RL, Buttemer WA, Carey C (1983a) Seasonal and geographic variation of cold resistance in house finches Carpodacus mexicanus. Physiol Zool 56:353–369

    Google Scholar 

  • Dawson WR, Marsh RL, Yacoe ME (1983b) Metabolic adjustment of small passerine birds for migration and cold. Am J Physiol 245:R755-R767

    PubMed  Google Scholar 

  • Dement'ev GP, Gladkov NA (1954) Birds of the Soviet Union, vol 5 (translated from Russian, Jerusalem 1970). Nauka, Moskva

    Google Scholar 

  • Duchamp C, Barré H (1993) Skeletal muscle as the major site of non-shivering thermogenesis in cold-acclimated ducklings. Am J Physiol 265:R1076-R1083

    PubMed  Google Scholar 

  • Duchamp C, Chatonnet J, Dittmar A, Barré H (1993a) Increased role of skeletal muscle in the calorigenic response to glucagon of cold-acclimated ducklings. Am J Physiol 265:R1084-R1091

    PubMed  Google Scholar 

  • Duchamp C, Cohen-Adad F, Rouanet J-L, Barré H (1993b) Existence of non-shivering thermogenesis in birds. In: Carey C, et al (eds) Life in the cold III: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 1–3

    Google Scholar 

  • Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236

    Google Scholar 

  • Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 142:429–437

    Google Scholar 

  • Heldmaier G, Klaus S, Wiesinger H, Friedrichs U, Wenzel M (1989) Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds) Living in the cold II. Colloque INSERM. Libbey, London, pp 347–358

    Google Scholar 

  • Hissa R (1988) Controlling mechanisms in avian temperature regulation: a review. Acta Physiol Scand [Suppl 567] 132:1–148

    PubMed  Google Scholar 

  • Hissa R, Saarela S, Rintamäki H, Lindén H, Hohtola E (1983) Energetics and development of temperature regulation in capercaillie Tetrao urogallus. Physiol Zool 56:142–151

    Google Scholar 

  • Hochachka PW (1974) Regulation of heat production at the cellular level. Fed Proc 33:2162–2169

    PubMed  Google Scholar 

  • Hohtola E (1982) Shivering thermogenesis in birds. Acta Univ Oul A 139 Biol 17

    Google Scholar 

  • Hohtola E, Stevens ED (1986) The relationship of muscle electrical activity, tremor and heat production to shivering thermogenesis in Japanese quail. J Exp Biol 125:119–135

    PubMed  Google Scholar 

  • Johnston DW (1971) The absence of brown adipose tissue in birds. Comp Biochem Physiol 40A:1107–1108

    Article  Google Scholar 

  • Lindström Å, Visser GH, Daan S (1993) The energetic cost of feather synthesis is proportional to basal metabolic rate. Physiol Zool 66:490–510

    Google Scholar 

  • Lustick S, Adams J (1977) Seasonal variation in the effect of wetting on the energetics and survival of starlings (Sturnus vulgaris). Comp Biochem Physiol 56A:173–177

    Article  Google Scholar 

  • Marsh RL (1993) Does regulatory non-shivering thermogenesis exist in birds? In: Carey C, et al (eds) Life in the cold III: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 535–538

    Google Scholar 

  • Marsh RL, Dawson WR (1989) Avian adjustments to cold. In: Wang LCH (ed) Advances in comparative and environmental physiology, vol 4. Springer, Berlin Heidelberg, pp 205–253

    Google Scholar 

  • Martin TP (1987) Predictable adaptations by skeletal muscle mitochondria to different exercise training workloads. Comp Biochem Physiol 88B:273–276

    Google Scholar 

  • Oliphant LW (1983) First observations of brown fat in birds. Condor 85:350–354

    Google Scholar 

  • Olson JM, Dawson WR, Camilliere JJ (1988) Fat from black-capped chickadees: avian brown adipose tissue? Condor 90:529–537

    Google Scholar 

  • Prinzinger R, Göppel R, Lorenz A, Kulzer E (1981) Body temperature and metabolism in the red-backed mousebird (Colius castanotus) during fasting and torpor. Comp Biochem Physiol 60:689–692

    Article  Google Scholar 

  • Prinzinger R, Preßmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol 99:499–506

    Article  Google Scholar 

  • Rashotte ME, Henderson D, Phillips D (1989) Thermal and feeding reactions of pigeons during food scarcity and cold. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum, New York, pp 255–264

    Google Scholar 

  • Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637

    Article  PubMed  Google Scholar 

  • Reinertsen RE (1983) Nocturnal hypothermia and its significance for small birds living in the arctic and subarctic regions. A review. Polar Res 1:269–284

    Google Scholar 

  • Reinertsen RE, Haftorn S (1983) Nocturnal hypothermia and metabolism in the willow tit Parus montanus at 63°N. J Comp Physiol 151:109–118

    Google Scholar 

  • Reinertsen RE, Haftorn S (1986) Different metabolic strategies of northern birds for nocturnal survival. J Comp Physiol B 156: 655–663

    Google Scholar 

  • Rintamäki H, Saarela S, Marjakangas A, Hissa R (1983) Summer and winter temperature regulation in the black grouse Lyrurus tetrix. Physiol Zool 56:152–159

    Google Scholar 

  • Saarela S (1980) Sympathetic regulation of body temperature in birds. Acta Univ Oul A 100 Biol 8

    Google Scholar 

  • Saarela S, Heldmaier G (1987) Effect of photoperiod and melatonin on cold resistance, thermoregulation and shivering/nonshivering thermogenesis in the quail. J Comp Physiol B 157:625–633

    PubMed  Google Scholar 

  • Saarela S, Hissa R, Pyörnilä A, Harjula R, Ojanen M (1986) Comparative study of the structure of avian adipose tissue and mammalian brown fat. Proc Scand Soc EM 39th Meeting, 4–6 June 1986. p 41

  • Saarela S, Hissa R, Pyörnilä A, Harjula R, Ojanen M, Orell M (1989) Do birds possess brown adipose tissue? Comp Biochem Physiol 92:219–228

    Article  Google Scholar 

  • Saarela S, Keith JS, Hohtola E, Trayhurn P (1991) Is the “mammalian” brown fat-specific mitochondrial uncoupling protein present in adipose tissues of birds? Comp Biochem Physiol 100:45–49

    Google Scholar 

  • Saarela S, Rintamäki H, Saarela M (1984) Seasonal variation in the dynamics of ptiloerection and shivering correlated changes in the metabolic rate and body temperature of the pigeon. J Comp Physiol B 154:47–53

    Google Scholar 

  • Saarela S, Vakkuri O (1982) Photoperiodic-induced changes in temperature-metabolism curve, shivering threshold and body temperature in the pigeon. Experientia 38:373–374

    PubMed  Google Scholar 

  • Shilov IA (1973) Heat regulation in birds. An ecologicalphysiological outline (translated from Russian by VS Kothekar). Amerind, New Delhi Bombay Calcutta New York

    Google Scholar 

  • Steen J (1958) Climatic adaptation in some small northern birds. Ecology 39:625–629

    Google Scholar 

  • Swanson DL (1991) Seasonal adjustments in metabolism and insulation in the dark-eyed junco. Condor 93:538–545

    Google Scholar 

  • Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89

    Google Scholar 

  • West GC (1965) Shivering and heat production in wild birds. Physiol Zool 38:111–120

    Google Scholar 

  • Voous KH (1960). Atlas of European birds. Nelson

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by H. Langer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saarela, S., Klapper, B. & Heldmaier, G. Daily rhythm of oxygen consumption and thermoregulatory responses in some European winter- or summer-acclimatized finches at different ambient temperatures. J Comp Physiol B 165, 366–376 (1995). https://doi.org/10.1007/BF00387307

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00387307

Key words

Navigation