Hostname: page-component-7dd5485656-j7khd Total loading time: 0 Render date: 2025-10-31T03:34:52.942Z Has data issue: false hasContentIssue false
  • English
  • Français

Ontogeny of avian thermoregulation from a neural point of view

Published online by Cambridge University Press:  25 June 2007

P.J.J. BAARENDSE ,
M. DEBONNE ,
E. DECUYPERE ,
B. KEMP  and
H. VAN DEN BRAND
P.J.J. BAARENDSE
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
M. DEBONNE
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Department of Biosystems, Division of Livestock-Nutrition-Quality, Catholic University Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium
E. DECUYPERE
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Department of Biosystems, Division of Livestock-Nutrition-Quality, Catholic University Leuven, Kasteelpark Arenberg 30, B-3001 Leuven, Belgium
B. KEMP
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
H. VAN DEN BRAND*
Affiliation:
Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
*
*Corresponding author: henry.vandenbrand@wur.nl
Get access

Abstract

The ontogeny of thermoregulation differs among (avian) species, but in all species both neural and endocrinological processes are involved. In this review the neural processes in ontogeny of thermoregulation during the prenatal and early postnatal phase are discussed. Only in a few avian species (chicken, ducklings) the ontogeny of some important neural structures are described. In the early post hatching phase, peripheral and deep-body thermoreceptors are present and functional, even in altricial species, in which the thermoregulation is still immature at hatch. It is suggested that the development of peripheral and deep-body thermoreceptors is not responsible for the inability to maintain a stable body temperature at cold ambient temperatures during early postnatal phase, although studies examined the ontogeny of thermoreception only in an indirect manner. Thus, other factors, such as volume to surface ratio and rate of insulation are important. Studies regarding the ontogeny of hypothalamic cold- and warm-sensitivity neurons in precocial species demonstrate that maturation of the hypothalamic temperature sensitivity takes place during the late prenatal and early postnatal period, with a relatively high cold sensitivity of the hypothalamus during the transition from poikilotherm to homeotherm. In addition, incubation temperatures are demonstrated to influence postnatal hypothalamic thermosensitivity. Brain temperature regulation is found to maturate during avian ontogeny as well and is demonstrated to coincide with the ontogenic pattern of general thermoregulation in several avian species. Relevant information of the ontogeny of the spinal cord and effector pathways related to the development of avian thermoregulation is lacking. We concluded that both prenatal and early postnatal temperature affects hypothalamic thermosensitivity and consequently condition thermoregulation in later life.

Keywords

thermoregulationontogenyperinatalneural development

Information

Type
Review Article
Information
World's Poultry Science Journal , Volume 63 , Issue 2 , June 2007 , pp. 267 - 276
Copyright
Copyright © World's Poultry Science Association 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

ARAD, Z., TOLEDO, C.S. and BERNSTEIN, M.H. (1984) Development of brain temperature regulation in the hatchling Mallard duck (Anas platyrhynchos). Physiological Zoology 57: 493–499.CrossRefGoogle Scholar
ARAD, Z., MIDTGÅRD, U. and BERNSTEIN, M.H. (1987) Post hatching development of the rete ophthalmicum in relation to brain temperature of Mallard ducks (Anas platyrhynchos). American Journal of Anatomy 179: 137–142.CrossRefGoogle Scholar
ARAD, Z. (1989) Ontogeny of brain temperature regulation in pigeon hatchlings (Columba livia). Physiological Zoology 62: 908–918.CrossRefGoogle Scholar
ARAD, Z. (1991) Ontogeny of brain temperature regulation in chicks (Gallus gallus domesticus). British Poultry Science 32: 203–210.CrossRefGoogle ScholarPubMed
BAARENDSE, P.J.J., KEMP, B. and VAN DEN BRAND, H. (2006) Early-age housing temperature affects subsequent broiler chicken performance. British Poultry Science 47: 125–130.CrossRefGoogle ScholarPubMed
BASTA, D., TZSCHENTKE, B. and NICHELMANN, M. (1997) Temperature guardian neurons in the preoptic area of the hypothalamus. Brain Research 767: 361–362.CrossRefGoogle ScholarPubMed
BLIGH, J. (1966) The thermosensitivity of the hypothalamus and thermoregulation in mammals, Biological Reviews 41: 317–367.CrossRefGoogle ScholarPubMed
BERNSTEIN, M.H. (1973) Development of thermoregulation in painted quail, Excalfactoria chenensis. Comparative Biochemistry and Physiology 44: 355–366.CrossRefGoogle Scholar
BOULAND, J.A. (1996) Hypothalamic neurons regulating body temperature. In: Fregly, M.J. and Blatteins, C.M. (ed.) Handbook of Physiology. Oxford Press, New York.Google Scholar
BOULANT, J.A. (2000) Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clinical Infectious Diseases 31: 157–161.CrossRefGoogle ScholarPubMed
DAWSON, W.R. and WHITTOW, G.C. (2000) Thermoregulation. In: Whittow, G.C. (ed), Sturkie's Avian Physiology. Academic Press, London.Google Scholar
DE WITTE, J. and SESSLER, D.I. (2002) Perioperative shivering; review article. Anaesthesiology 96: 467–484.Google Scholar
DIETZ, M.W. (1995) Development of metabolism and thermoregulation in galliforms. Effect of body mass, growth rate and functional maturity. PhD Thesis, Utrecht, The Netherlands.Google Scholar
FREEMAN, B.M. (1964) The emergence of the homeothermic-metabolic response in the fowl (Gallus domesticus). Comparative Biochemistry and Physiology 13: 413–422.CrossRefGoogle ScholarPubMed
FREEMAN, B.M. and VINCE, M.A. (1974) The nervous system. In: Freeman, B.M. and Vince, M.A. (ed.) Development of the avian embryo. A behavioural and physiological study. Academic Press, London, UK.CrossRefGoogle Scholar
HAMMEL, H.T. (1968) Regulation of internal body temperature. Annual Review of Physiology 30: 641–710.Google Scholar
HENSEL, H. (1981) Thermoreception and temperature regulation. Academic Press, Londen, UK.Google ScholarPubMed
LOURENS, A., VAN DEN BRAND, H., HEETKAMP, M.J.W., MEIJERHOF, R. and KEMP, B. (2006) Metabolic responses of chick embryos to short-term temperature fluctuations. Poultry Science 85: 1081–1086.Google Scholar
MARSH, R.L. and WICKLER, S.J. (1982) The role of muscle development in the transition to endothermy in nestling Bank Swallows, Riparia riparia. Journal of Comparative Physiology 149: 99–105.Google Scholar
NAKASHIMA, T., PIERAU, F.K., SIMON, E. and HORI, T. (1987) Comparison between hypothalamic thermoresponsive neurons from duck and rat slices. European Journal of Physiology 409: 236–243.CrossRefGoogle ScholarPubMed
NECKER, R. (1972) Response of trigeminal ganglion neurons of thermal stimulation of the beak in pigeons. Journal of Comparative Physiology 78: 307–314.CrossRefGoogle Scholar
NICHELMANN, M. (2004a) Perinatal epigenetic temperature adaptation in avian species: comparison of turkey and Muscovy duck. Journal of Thermal Biology 29: 613–619.Google Scholar
NICHELMANN, M. (2004b) Importance of prenatal temperature experience on development of the thermoregulatory control system in birds. Thermochimica Acta 422: 25–33.CrossRefGoogle Scholar
NICHELMANN, M. (2004c) Activation of thermoregulatory control elements in precocial birds during the prenatal period. Journal of Thermal Biology 29: 621–627.CrossRefGoogle Scholar
NICHELMANN, M. and TZSCHENTKE, B. (1997) Ontogeny of thermoregulation during the prenatal period in birds. Annals of the New York Academy of Sciences 813: 78–86.Google Scholar
NICHELMANN, M. and TZSCHENTKE, B. (2002) Ontogeny of thermoregulation in precocial birds. Comparative Biochemistry and Physiology 131: 751–763.CrossRefGoogle ScholarPubMed
NICOLARDI, G., AMBROSI, G., RIZZI, A. and CARNOSSO, M.E. (1988) Medullary and mesencephalic neuronal groups reacting to antibodies against VIP, somatostatin and bombesin in adult Gallus gallus domesticus. Basic and Applied Histochemistry 32: 77–88.Google Scholar
ØSTNES, J.E. and BECH, C. (1997) The early emergence of cold sensation in Shag nestlings Phalacrocorax aristotelis. Journal of Avian Biology 28: 24–30.CrossRefGoogle Scholar
PIERAU, F-K., SANN, H., YAKIMOVA, K.S. and HAUG, P. (1998) Plasticity of hypothalamic temperaturesensitive neurons. Progress in Brain Research 115: 63–84.CrossRefGoogle ScholarPubMed
RANDALL, W.C. (1943) Factors influencing the temperature regulation of birds. American Journal of Physiology 139: 56–63.CrossRefGoogle Scholar
ROGERS, L.J. (1995) Development of the brain and behaviour before hatching. In: The development of brain and behaviour in the chicken. CAB International, Wallingford, UK.Google Scholar
ROL'NIK, V.V. (1970) Bird embryology. IPST, Jerusalem, Israel.Google Scholar
SCHMID, H.A., JANSKY, L. and PIERAU, F.K. (1993) Temperature sensitivity of neurons in slices of the rat PO/AH area: effect of bombesin and substance P. American Journal of Physiology 264R: 449–455.Google Scholar
SIMON, E., PIEREAU, F.R. and TAYLOR, D.C.M. (1986) Central and peripheral thermal control of effects in homeothermic temperature regulation. The American Physiological Society 66: 235–300.Google Scholar
SPIERS, D.E., MCNABB, R.A. and MCNABB, F.M.A. (1974) The development of thermoregulatory ability, heat seeking activities, and thyroid function in hatchling Japanese quail (Coturnix coturnix japonica). Journal of Comparative Physiology 89: 159–174.CrossRefGoogle Scholar
STARCK, M. and RICKLEFS, R.E. (1998) Avian growth and development. Evolution within the altricialprecocial spectrum. Oxford University Press, New York, NY.Google Scholar
STITT, J.T. (1983) Hypothalamic generation of effector signals. Journal of Thermal Biology 8: 113–117.Google Scholar
TAZAWA, H., WAKAYAMA, H., TURNER, J.S. and PAGANELL, C.V. (1988) Metabolic compensation for gradual cooling in developing chick embryos. Comparative Biochemistry and Physiology 89A: 125–129.CrossRefGoogle Scholar
TAZAWA, H., MORIYA, K., TAMURA, A., KOMORO, T. and AKIYAMA, R. (2001) Ontogenic study of thermoregulation in birds. Journal of Thermal Biology 26: 281–286.CrossRefGoogle Scholar
TZSCHENTKE, B. and BASTA, D. (2000) Development of hypothalamic neural thermosensitivity in birds during the perinatal period. Journal of Thermal Biology 25: 119–123.Google Scholar
TZSCHENTKE, B. and BASTA, D. (2002) Early development of neural hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation. Comparative Biochemistry and Physiology 131A: 825–832.CrossRefGoogle Scholar
TZSCHENTKE, B. and NICHELMANN, M. (1999) Development of avian thermoregulatory system during the early postnatal period: Development of avian set-point. Ornis Fennica 76: 189–198.Google Scholar
TZSCHENTKE, B., BASTA, D., GOURINE, A.V. and GOURINE, V.N. (2000) Influence of bombesin on neural hypothalamic thermosensitivity during the early postnatal period in the Muscovy duck (Cairina moschata). Regulatory Peptides 88: 33–39.Google Scholar
VISSER, G.H. (1991) Development of metabolism and temperature regulation in precocial birds. Patterns in shorebirds (Charadriiformes) and the domestic fowl (Gallus domesticus). PhD Thesis. Utrecht, The Netherlands.Google Scholar
WHITTOW, G.C. and TAZAWA, H. (1991) The early development of thermoregulation in birds. Physiological Zoology 64: 1371–1390.CrossRefGoogle Scholar
YAHAV, S. and HURWITZ, S. (1996) Induction of thermotolerance in male broiler chickens by temperature conditioning at an early age. Poultry Science 75: 402–406.Google Scholar
YAHAV, S. and PLAVNIK, I. (1999) Effect of early-age thermal conditioning and food restriction on performance and thermotolerance of male broiler chickens. British Poultry Science 40: 120–126.Google Scholar
YAHAV, S., SASSON RATH, R. and SHINDER, D. (2004a) The effect of thermal manipulations during embryogenesis of broiler chicks (Gallus domesticus) on hatchability, body weight and thermoregulation after hatch. Journal of Thermal Biology 29: 245–250.CrossRefGoogle Scholar
YAHAV, S., COLLIN, A., SHINDER, D. and PICARD, M. (2004b) Thermal manipulations during broiler chick embryogenesis: Effects of timing and temperature. Poultry Science 83: 1959–1963.Google Scholar